The uterine secretory cycle: recurring physiology of endometrial outputs that setup the uterine luminal microenvironment
Abstract
Conserved in female reproduction across all mammalian species is the estrous cycle and its regulation by the hypothalamic-pituitary-gonadal (HPG) axis, a collective of intersected hormonal events that are crucial for ensuring uterine fertility. Nonetheless, knowledge of the direct mediators that synchronously shape the uterine microenvironment for successive yet distinct events, such as the transit of sperm and support for progressive stages of preimplantation embryo development, remain principally deficient. Toward understanding the timed endometrial outputs that permit luminal events as directed by the estrous cycle, we used Bovidae as a model system to uniquely surface sample and study temporal shifts to in vivo endometrial transcripts that encode for proteins destined to be secreted. The results revealed the full quantitative profile of endometrial components that shape the uterine luminal microenvironment at distinct phases of the estrous cycle (estrus, metestrus, diestrus, and proestrus). In interpreting this comprehensive log of stage-specific endometrial secretions, we define the “uterine secretory cycle” and extract a predictive understanding of recurring physiological actions regulated within the uterine lumen in anticipation of sperm and preimplantation embryonic stages. This repetitive microenvironmental preparedness to sequentially provide operative support was a stable intrinsic framework, with only limited responses to sperm or embryos if encountered in the lumen within the cyclic time period. In uncovering the secretory cycle and unraveling realistic biological processes, we present novel foundational knowledge of terminal effectors controlled by the HPG axis to direct a recurring sequence of vital functions within the uterine lumen.
NEW & NOTEWORTHY This study unravels the recurring sequence of changes within the uterus that supports vital functions (sperm transit and development of preimplantation embryonic stages) during the reproductive cycle in female Ruminantia. These data present new systems knowledge in uterine reproductive physiology crucial for setting up in vitro biomimicry and artificial environments for assisted reproduction technologies for a range of mammalian species.
Listen to this article’s corresponding podcast at https://apspublicationspodcast.podbean.com/e/what-is-the-uterine-secretory-cycle-and-why-is-it-important/.
REFERENCES
- 1. . Uterine milk. Am J Med Sci 87: 254–255, 1884.
Crossref | Google Scholar - 2. . Sicherer nachweis der sogenannten uterinmilch beim menschen. Zeitschrift fur Geburtshulfe und Gynakologie 7–8: XVI, 258–285, 1882.
Google Scholar - 3. . Uterine glands: development, function and experimental model systems. Mol Hum Reprod 19: 547–558, 2013. doi:10.1093/molehr/gat031.
Crossref | PubMed | Web of Science | Google Scholar - 4. . The functions of uterine secretions. J Reprod Fertil 82: 875–892, 1988. doi:10.1530/jrf.0.0820875.
Crossref | PubMed | Google Scholar - 5. . Biological roles of uterine glands in pregnancy. Semin Reprod Med 32: 346–357, 2014. doi:10.1055/s-0034-1376354.
Crossref | PubMed | Web of Science | Google Scholar - 6. . Maternal influence on the early development of asynchronously transferred bovine embryos. Anim Reprod Sci 24: 25–35, 1991. doi:10.1016/0378-4320(91)90079-F.
Crossref | Web of Science | Google Scholar - 7. . Evidence for maternal control of blastocyst growth after asynchronous transfer of embryos to the uterus of the ewe. J Reprod Fertil 67: 477–483, 1983. doi:10.1530/jrf.0.0670477.
Crossref | PubMed | Google Scholar - 8. . Effect of an asynchronous environment on embryonic development in sheep. J Reprod Fertil 61: 179–184, 1981. doi:10.1530/jrf.0.0610179.
Crossref | PubMed | Google Scholar - 9. Immunohistochemical analysis of human uterine estrogen and progesterone receptors throughout the menstrual cycle. J Clin Endocrinol Metab 67: 334–340, 1988. doi:10.1210/jcem-67-2-334.
Crossref | PubMed | Web of Science | Google Scholar - 10. . The effect of estrogen and progesterone on structural changes in the uterine glandular epithelium of the ovariectomized sheep. Biol Reprod 47: 408–417, 1992. doi:10.1095/biolreprod47.3.408.
Crossref | PubMed | Web of Science | Google Scholar - 11. . Estrogen- and progesterone-dependent secretory changes in the uterus of the sheep. Biol Reprod 47: 917–924, 1992. doi:10.1095/biolreprod47.6.917.
Crossref | PubMed | Web of Science | Google Scholar - 12. . Synthesis and processing of ovine trophoblast protein-1 and bovine trophoblast protein-1, conceptus secretory proteins involved in the maternal recognition of pregnancy. Endocrinology 123: 1274–1280, 1988. doi:10.1210/endo-123-3-1274.
Crossref | PubMed | Web of Science | Google Scholar - 13. . A study of the physiologic action of human chorionic hormone; the production of pseudopregnancy in women by chorionic hormone. Am J Obstet Gynecol 53: 749–757, 1947. doi:10.1016/s0002-9378(15)31597-0.
Crossref | PubMed | Web of Science | Google Scholar - 14. . Purification and properties of a major, low molecular weight protein released by the trophoblast of sheep blastocysts at day 13-21. J Reprod Fertil 65: 141–150, 1982. doi:10.1530/jrf.0.0650141.
Crossref | PubMed | Google Scholar - 15. . Some effects of estrogen injections on the estrual cycle of gilts. J Anim Sci 14: 470–474, 1955. doi:10.2527/jas1955.142470x.
Crossref | Web of Science | Google Scholar - 16. . Trophoblastin, an antiluteolytic protein present in early pregnancy in sheep. J Reprod Fertil 56: 63–73, 1979. doi:10.1530/jrf.0.0560063.
Crossref | PubMed | Google Scholar - 17. . Effects of luteotropic dose of chorionic gonadotropin in women. J Clin Endocrinol Metab 11: 936–944, 1951. doi:10.1210/jcem-11-9-936.
Crossref | PubMed | Web of Science | Google Scholar - 18. . Experimental studies on the elongation of the ewe blastocyst. Reprod Nutr Dev (1980) 26: 1017–1024, 1986. doi:10.1051/rnd:19860609.
Crossref | PubMed | Google Scholar - 19. . Insulin-like growth factor-I expression during early conceptus development in the pig. Biol Reprod 41: 1143–1151, 1989. doi:10.1095/biolreprod41.6.1143.
Crossref | PubMed | Web of Science | Google Scholar - 20. . Role of conceptus secretory products in establishment of pregnancy. J Reprod Fertil 76: 841–850, 1986. doi:10.1530/jrf.0.0760841.
Crossref | PubMed | Google Scholar - 21. . Secretory proteins of the bovine conceptus alter endometrial prostaglandin and protein secretion in vitro. Biol Reprod 39: 977–987, 1988. doi:10.1095/biolreprod39.4.977.
Crossref | PubMed | Web of Science | Google Scholar - 22. . The effect of ovine trophoblast protein-one on endometrial protein secretion and cyclic nucleotides. Biol Reprod 37: 1307–1316, 1987. doi:10.1095/biolreprod37.5.1307.
Crossref | PubMed | Web of Science | Google Scholar - 23. . Normal development following in vitro fertilization in the cow. Biol Reprod 27: 147–158, 1982. doi:10.1095/biolreprod27.1.147.
Crossref | PubMed | Web of Science | Google Scholar - 24. . Birth of normal calves resulting from bovine oocytes matured, fertilized, and cultured with cumulus cells in vitro up to the blastocyst stage. Biol Reprod 42: 114–119, 1990. doi:10.1095/biolreprod42.1.114.
Crossref | PubMed | Web of Science | Google Scholar - 25. . Superovulation and related phenomena in the beef cow. II. Effect of oestrogen administration on production of ova. J Reprod Fertil 5: 381–388, 1963. doi:10.1530/jrf.0.0050381.
Crossref | PubMed | Google Scholar - 26. . Prostaglandin F2α identified as a luteolytic hormone in sheep. Nat New Biol 238: 129–134, 1972. doi:10.1038/newbio238129a0.
Crossref | PubMed | Google Scholar - 27. . A yolk-buffer pabulum for the preservation of bull sperm. J Dairy Sci 23: 399–404, 1940. doi:10.3168/jds.S0022-0302(40)95541-2.
Crossref | Google Scholar - 28. . The production of monozygotic twins of preselected parentage by micromanipulation of non-surgically collected cow embryos. Theriogenology 15: 23–29, 1981. doi:10.1016/s0093-691x(81)80015-5.
Crossref | PubMed | Web of Science | Google Scholar - 29. . Successful transplantation of a fertilized bovine ovum. Science 113:
247 , 1951. doi:10.1126/science.113.2931.247.
Crossref | PubMed | Web of Science | Google Scholar - 30. . Experiments on the low-temperature preservation of cow embryos. Vet Rec 92: 686–690, 1973. doi:10.1136/vr.92.26.686.
Crossref | PubMed | Web of Science | Google Scholar - 31. . Viable offspring derived from fetal and adult mammalian cells. Nature 385: 810–813, 1997 [Erratum in Nature 386: 200, 1997]. doi:10.1038/385810a0.
Crossref | PubMed | Web of Science | Google Scholar - 32. . Studies on the estrous cycle of dairy cattle: cycle length, size of corpus luteum and endometrial changes. Cornell Vet 39: 397–410, 1949.
Google Scholar - 33. . A study of the mucosa of the genital tract of the cow, with special reference to the cyclic changes. Am J Anat 46: 261–301, 1930. doi:10.1002/aja.1000460204.
Crossref | Google Scholar - 34. . Cyclical changes in the fine structure of bovine endometrial gland cells. Z Zellforsch Mikrosk Anat 104: 69–86, 1970. doi:10.1007/bf00340050.
Crossref | PubMed | Google Scholar - 35. . Effects of neonatal progestin exposure on female reproductive tract structure and function in the adult ewe. Biol Reprod 64: 797–804, 2001. doi:10.1095/biolreprod64.3.797.
Crossref | PubMed | Web of Science | Google Scholar - 36. . Endometrial glands are required for preimplantation conceptus elongation and survival. Biol Reprod 64: 1608–1613, 2001. doi:10.1095/biolreprod64.6.1608.
Crossref | PubMed | Web of Science | Google Scholar - 37. . A chemical study of uterine fluid and blood serum of normal cows during the oestrous cycle. J Reprod Fertil 27: 355–367, 1971. doi:10.1530/jrf.0.0270355.
Crossref | PubMed | Google Scholar - 38. . Some chemical constituents of uterine washings: a method of analysis with results from various species. J Endocrinol 24: 367–378, 1962. doi:10.1677/joe.0.0240367.
Crossref | PubMed | Web of Science | Google Scholar - 39. . Les électrolytes du sang et des sécrétions endométriales de la vache à la suite d’une glucocorticothérapie [Electrolytes of the blood and endometrial secretions of the cow following glucocorticoid therapy]. Can J Comp Med 36: 160–166, 1972.
PubMed | Google Scholar - 40. . Relationship of dietary crude protein to composition of uterine secretions and blood in high-producing postpartum dairy cows. J Dairy Sci 66: 1854–1862, 1983. doi:10.3168/jds.S0022-0302(83)82023-2.
Crossref | PubMed | Web of Science | Google Scholar - 41. . Amino acids in oviduct and uterine fluid and blood plasma during the estrous cycle in the bovine. Mol Reprod Dev 74: 445–454, 2007. doi:10.1002/mrd.20607.
Crossref | PubMed | Web of Science | Google Scholar - 42. . Energy substrates in bovine oviduct and uterine fluid and blood plasma during the oestrous cycle. Mol Reprod Dev 75: 496–503, 2008. doi:10.1002/mrd.20760.
Crossref | PubMed | Web of Science | Google Scholar - 43. . Ion concentrations in oviduct and uterine fluid and blood serum during the estrous cycle in the bovine. Theriogenology 68: 538–548, 2007. doi:10.1016/j.theriogenology.2007.04.049.
Crossref | PubMed | Web of Science | Google Scholar - 44. . Effects of changes in the concentration of systemic progesterone on ions, amino acids and energy substrates in cattle oviduct and uterine fluid and blood. Reprod Fertil Dev 22: 684–694, 2010. doi:10.1071/RD09129.
Crossref | PubMed | Web of Science | Google Scholar - 45. . Modulation of periovulatory endocrine profiles in beef cows: consequences for endometrial glucose transporters and uterine fluid glucose levels. Domest Anim Endocrinol 50: 83–90, 2015. doi:10.1016/j.domaniend.2014.09.005.
Crossref | PubMed | Web of Science | Google Scholar - 46. . Select nutrients in the ovine uterine lumen. ii. glucose transporters in the uterus and peri-implantation conceptuses. Biol Reprod 80: 94–104, 2009. doi:10.1095/biolreprod.108.071654.
Crossref | PubMed | Web of Science | Google Scholar - 47. . Select nutrients in the ovine uterine lumen. I. Amino acids, glucose, and ions in uterine lumenal flushings of cyclic and pregnant ewes. Biol Reprod 80: 86–93, 2009. doi:10.1095/biolreprod.108.071597.
Crossref | PubMed | Web of Science | Google Scholar - 48. . Analysis of the uterine lumen in fertility-classified heifers: I. Glucose, prostaglandins, and lipids. Biol Reprod 102: 456–474, 2020. doi:10.1093/biolre/ioz191.
Crossref | PubMed | Web of Science | Google Scholar - 49. . Effects of systemic progesterone during the early luteal phase on the availabilities of amino acids and glucose in the bovine uterine lumen. Reprod Fertil Dev 26: 282–292, 2014. doi:10.1071/RD12319.
Crossref | PubMed | Web of Science | Google Scholar - 50. . Effects of amino acids on development in vitro of cleavage-stage bovine embryos into blastocysts. Reprod Fertil Dev 8: 835–841, 1996. doi:10.1071/RD9960835.
Crossref | PubMed | Web of Science | Google Scholar - 51. . The free amino acid content of uterine fluids and blood serum in the cow. J Reprod Fertil 13: 229–236, 1967. doi:10.1530/jrf.0.0130229.
Crossref | PubMed | Google Scholar - 52. . Analysis of the uterine lumen in fertility-classified heifers: II. Proteins and metabolites. Biol Reprod 102: 571–587, 2020. doi:10.1093/biolre/ioz197.
Crossref | PubMed | Web of Science | Google Scholar - 53. . Biology of preimplantation conceptus at the onset of elongation in dairy cows. Biol Reprod 94:
97 , 2016. doi:10.1095/biolreprod.115.134908.
Crossref | PubMed | Web of Science | Google Scholar - 54. . Progesterone alters the bovine uterine fluid lipidome during the period of elongation. Reproduction 157: 399–411, 2019. doi:10.1530/REP-18-0615.
Crossref | PubMed | Web of Science | Google Scholar - 55. . The influence of progesterone on bovine uterine fluid energy, nucleotide, vitamin, cofactor, peptide, and xenobiotic composition during the conceptus elongation-initiation window. Sci Rep 9:
7716 , 2019. doi:10.1038/s41598-019-44040-6.
Crossref | PubMed | Web of Science | Google Scholar - 56. . Biochemical characterization of progesterone-induced alterations in bovine uterine fluid amino acid and carbohydrate composition during the conceptus elongation window. Biol Reprod 100: 672–685, 2019. doi:10.1093/biolre/ioy234.
Crossref | PubMed | Web of Science | Google Scholar - 57. . Changes in the uterine metabolome of the cow during the first 7 days after estrus. Mol Reprod Dev 86: 75–87, 2019. doi:10.1002/mrd.23082.
Crossref | PubMed | Web of Science | Google Scholar - 58. . The pre-hatching bovine embryo transforms the uterine luminal metabolite composition in vivo. Sci Rep 9:
8354 , 2019. doi:10.1038/s41598-019-44590-9.
Crossref | PubMed | Web of Science | Google Scholar - 59. . Granulocyte-macrophage colony-stimulating factor promotes development of in vitro produced bovine embryos. Biol Reprod 57: 1060–1065, 1997. doi:10.1095/biolreprod57.5.1060.
Crossref | PubMed | Web of Science | Google Scholar - 60. . Effect of fibronectin on early embryo development in cows. J Reprod Fertil 96: 289–297, 1992. doi:10.1530/jrf.0.0960289.
Crossref | PubMed | Google Scholar - 61. . Platelet derived growth factor (PDGF) stimulates development of bovine embryos during the fourth cell cycle. Development 115: 821–826, 1992. doi:10.1242/dev.115.3.821.
Crossref | PubMed | Web of Science | Google Scholar - 62. . Transforming growth factor beta and basic fibroblast growth factor synergistically promote early bovine embryo development during the fourth cell cycle. Mol Reprod Dev 33: 432–435, 1992. doi:10.1002/mrd.1080330409.
Crossref | PubMed | Web of Science | Google Scholar - 63. . Fibroblast growth factor-2 is expressed by the bovine uterus and stimulates interferon-tau production in bovine trophectoderm. Endocrinology 147: 3571–3579, 2006. doi:10.1210/en.2006-0234.
Crossref | PubMed | Web of Science | Google Scholar - 64. . Role of platelet-derived growth factor in development of in vitro matured and in vitro fertilized bovine embryos. J Reprod Fertil 98: 61–66, 1993. doi:10.1530/jrf.0.0980061.
Crossref | PubMed | Google Scholar - 65. . Global proteomic characterization of uterine histotroph recovered from beef heifers yielding good quality and degenerate day 7 embryos. Domest Anim Endocrinol 46: 49–57, 2014. doi:10.1016/j.domaniend.2013.10.003.
Crossref | PubMed | Web of Science | Google Scholar - 66. . A comparison of the bovine uterine and plasma proteome using iTRAQ proteomics. Proteomics 12: 2014–2023, 2012. doi:10.1002/pmic.201100609.
Crossref | PubMed | Web of Science | Google Scholar - 67. . Amino acids in the uterine luminal fluid reflects the temporal changes in transporter expression in the endometrium and conceptus during early pregnancy in cattle. PLoS One 9:
e100010 , 2014. doi:10.1371/journal.pone.0100010.
Crossref | PubMed | Web of Science | Google Scholar - 68. . Proteomic characterization of histotroph during the preimplantation phase of the estrous cycle in cattle. J Proteome Res 11: 3004–3018, 2012. doi:10.1021/pr300144q.
Crossref | PubMed | Web of Science | Google Scholar - 69. . Repeatability and reproducibility in proteomic identifications by liquid chromatography-tandem mass spectrometry. J Proteome Res 9: 761–776, 2010. doi:10.1021/pr9006365.
Crossref | PubMed | Web of Science | Google Scholar - 70. . Sperm survival and transport in the female reproductive tract. J Dairy Sci 66: 2645–2660, 1983. doi:10.3168/jds.S0022-0302(83)82138-9.
Crossref | PubMed | Web of Science | Google Scholar - 71. . Embryo culture and long-term consequences. Reprod Fertil Dev 19: 43–52, 2007. doi:10.1071/rd06129.
Crossref | PubMed | Web of Science | Google Scholar - 72. . Induced pluripotent stem cell generation from bovine somatic cells indicates unmet needs for pluripotency sustenance. Anim Sci J 90: 1149–1160, 2019. doi:10.1111/asj.13272.
Crossref | PubMed | Web of Science | Google Scholar - 73. . Profiling of proteins secreted in the bovine oviduct reveals diverse functions of this luminal microenvironment. PLoS One 12:
e0188105 , 2017. doi:10.1371/journal.pone.0188105.
Crossref | PubMed | Web of Science | Google Scholar - 74. . Physiological profile of undifferentiated bovine blastocyst-derived trophoblasts. Biol Open 8:
bio037937 , 2019. doi:10.1242/bio.037937.
Crossref | PubMed | Web of Science | Google Scholar - 75. . Application of one injection of prostaglandin F2α in the five-day Co-Synch+CIDR protocol for estrous synchronization and resynchronization of dairy heifers. J Dairy Sci 93: 1050–1058, 2010. doi:10.3168/jds.2009-2675.
Crossref | PubMed | Web of Science | Google Scholar - 76. . Hormonal manipulations in the 5-day timed artificial insemination protocol to optimize estrous cycle synchrony and fertility in dairy heifers. J Dairy Sci 96: 7054–7065, 2013. doi:10.3168/jds.2013-7093.
Crossref | PubMed | Web of Science | Google Scholar - 77. . The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update. Nucleic Acids Res 44: W3–W10, 2016. doi:10.1093/nar/gkw343.
Crossref | PubMed | Web of Science | Google Scholar - 78. . De novo assembly of the cattle reference genome with single-molecule sequencing. Gigascience 9:
giaa021 , 2020. doi:10.1093/gigascience/giaa021.
Crossref | PubMed | Web of Science | Google Scholar - 79. . Mapping RNA-seq Reads with STAR. Curr Protoc Bioinforma 51: 11.14.1–11.14.19, 2015. doi:10.1002/0471250953.bi1114s51.
Crossref | PubMed | Google Scholar - 80. . SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785–786, 2011. doi:10.1038/nmeth.1701.
Crossref | PubMed | Web of Science | Google Scholar - 81. . Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005–1016, 2000. doi:10.1006/jmbi.2000.3903.
Crossref | PubMed | Web of Science | Google Scholar - 82. . A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338: 1027–1036, 2004. doi:10.1016/j.jmb.2004.03.016.
Crossref | PubMed | Web of Science | Google Scholar - 83. . Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel 17: 349–356, 2004. doi:10.1093/protein/gzh037.
Crossref | PubMed | Web of Science | Google Scholar - 84. . InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics 16:
169 , 2015. doi:10.1186/s12859-015-0611-3.
Crossref | PubMed | Web of Science | Google Scholar - 85. . ChEA3: transcription factor enrichment analysis by orthogonal omics integration. Nucleic Acids Res 47: W212–W224, 2019. doi:10.1093/nar/gkz446.
Crossref | PubMed | Web of Science | Google Scholar - 86. . The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res 49: D605–D612, 2021 [Erratum in Nucleic Acids Res 49: 10800, 2021]. doi:10.1093/nar/gkaa1074.
Crossref | PubMed | Web of Science | Google Scholar - 87. . ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics 36: 2628–2629, 2020. doi:10.1093/bioinformatics/btz931.
Crossref | PubMed | Web of Science | Google Scholar - 88. . Circos: an information aesthetic for comparative genomics. Genome Res 19: 1639–1645, 2009. doi:10.1101/gr.092759.109.
Crossref | PubMed | Web of Science | Google Scholar - 89. . STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47: D607–D613, 2019. doi:10.1093/nar/gky1131.
Crossref | PubMed | Web of Science | Google Scholar - 90. . Efficient induction and sustenance of pluripotent stem cells from bovine somatic cells. Biol Open 10:
bio058756 , 2021. doi:10.1242/bio.058756.
Crossref | PubMed | Web of Science | Google Scholar - 91. . Massive dysregulation of genes involved in cell signaling and placental development in cloned cattle conceptus and maternal endometrium. Proc Natl Acad Sci USA 113: 14492–14501, 2016. doi:10.1073/pnas.1520945114.
Crossref | PubMed | Web of Science | Google Scholar - 92. . Repeatability of the estrous cycle length in dairy cattle. J Dairy Sci 34: 626–632, 1951. doi:10.3168/jds.S0022-0302(51)91757-2.
Crossref | Web of Science | Google Scholar - 93. . Comprehensive RNA sequencing of healthy human endometrium at two time points of the menstrual cycle. Biol Reprod 96: 24–33, 2017. doi:10.1095/biolreprod.116.142547.
Crossref | PubMed | Web of Science | Google Scholar - 94. . Transcriptomic changes during the pre-receptive to receptive transition in human endometrium detected by RNA-Seq. J Clin Endocrinol Metab 99: E2744–E2753, 2014. doi:10.1210/jc.2014-2155.
Crossref | PubMed | Web of Science | Google Scholar - 95. . The transcriptome signature of the receptive bovine uterus determined at early gestation. PLoS One 10:
e0122874 , 2015. doi:10.1371/journal.pone.0122874.
Crossref | PubMed | Web of Science | Google Scholar - 96. . Uterine influences on conceptus development in fertility-classified animals. Proc Natl Acad Sci USA 115: E1749–E1758, 2018. doi:10.1073/pnas.1721191115.
Crossref | PubMed | Web of Science | Google Scholar - 97. . Alterations in expression of endometrial genes coding for proteins secreted into the uterine lumen during conceptus elongation in cattle. BMC Genomics 14:
321 , 2013. doi:10.1186/1471-2164-14-321.
Crossref | PubMed | Web of Science | Google Scholar - 98. . Single-cell transcriptomic atlas of the human endometrium during the menstrual cycle. Nat Med 26: 1644–1653, 2020. doi:10.1038/s41591-020-1040-z.
Crossref | PubMed | Web of Science | Google Scholar - 99. . The abolition of mating behavior by hypothalamic lesions in guinea pigs. Endocrinology 28: 561–565, 1941. doi:10.1210/endo-28-4-561.
Crossref | Google Scholar - 100. . The ovarian cycle of swine. American Association for the Advancement of Science. Science 53: 420–421, 1921. doi:10.1126/science.53.1374.420.
Crossref | PubMed | Google Scholar - 101. . Progesterone and estrogen in the experimental control of ovulation time and other features of the estrous cycle in the rat. Endocrinology 43: 389–405, 1948. doi:10.1210/endo-43-6-389.
Crossref | PubMed | Web of Science | Google Scholar - 102. . Estrous behavior and hormones in the cow. J Comp Psychol (Baltim) 39: 119–123, 1946. doi:10.1037/h0060346.
Crossref | PubMed | Web of Science | Google Scholar - 103. . Some histological and histochemical observations of the bovine ovary during the estrous cycle. Anat Rec 120: 409–433, 1954. doi:10.1002/ar.1091200205.
Crossref | PubMed | Google Scholar - 104. . The morphology of the oviduct of virgin heifers in relation to the estrous cycle. J Morphol 86: 1–23, 1950. doi:10.1002/jmor.1050860102.
Crossref | PubMed | Web of Science | Google Scholar - 105. . Endometrial biopsy studies in reproductively normal cattle; clinical, histochemical and histological observations during the estrous cycle. Acta Endocrinol Suppl (Copenh) 22: 1–101, 1956.
PubMed | Google Scholar - 106. . Crystallization patterns in vaginal and cervical mucus smears as related to bovine ovarian activity and pregnancy. Am J Vet Res 15: 542–547, 1954.
PubMed | Web of Science | Google Scholar - 107. . Extremely high alkaline phosphatase activity in the vaginal mucus of the cow. Nature 172:
397 , 1953. doi:10.1038/172397a0.
Crossref | PubMed | Web of Science | Google Scholar - 108. . An electron microscopic study of implantation in the cow. Am J Anat 159: 285–306, 1980. doi:10.1002/aja.1001590305.
Crossref | PubMed | Google Scholar - 109. . Implantation and establishment of pregnancy in human and nonhuman primates. Adv Anat Embryol Cell Biol 216: 189–213, 2015. doi:10.1007/978-3-319-15856-3_10.
Crossref | PubMed | Web of Science | Google Scholar - 110.
UniProt Consortium. UniProt: the universal protein knowledgebase in 2021. Nucleic Acids Res 49: D480–D489, 2021. doi:10.1093/nar/gkaa1100.
Crossref | PubMed | Web of Science | Google Scholar - 111. . Detection of matrix metalloproteinase (MMP)-2 and MMP-9 in canine seminal plasma. Anim Reprod Sci 127: 114–119, 2011. doi:10.1016/j.anireprosci.2011.07.004.
Crossref | PubMed | Web of Science | Google Scholar - 112. . Comparison, characterization, and identification of proteases and protease inhibitors in epididymal fluids of domestic mammals. matrix metalloproteinases are major fluid gelatinases. Biol Reprod 66: 1219–1229, 2002. doi:10.1095/biolreprod66.5.1219.
Crossref | PubMed | Web of Science | Google Scholar - 113. . Presence of matrix metalloproteinases and tissue inhibitor of matrix metalloproteinase in human sperm. J Androl 23: 702–708, 2002. doi:10.1002/j.1939-4640.2002.tb02313.x.
Crossref | PubMed | Google Scholar - 114. . Sperm matrix metalloproteinase-2 activity increased in pregnant couples treated with intrauterine insemination: a prospective case control study. J Obstet Gynaecol 39: 675–680, 2019. doi:10.1080/01443615.2018.1558189.
Crossref | PubMed | Google Scholar - 115. . Plasminogen activator activity, plasminogen activator inhibition and plasmin inhibition in spermatozoa and seminal plasma of man and various animal species—effect of plasmin on sperm motility. Fibrinolysis 1: 253–257, 1987. doi:10.1016/0268-9499(87)90045-2.
Crossref | Google Scholar - 116. . Plasminogen activator and mouse spermatozoa: urokinase synthesis in the male genital tract and binding of the enzyme to the sperm cell surface. J Cell Biol 104: 1281–1289, 1987. doi:10.1083/jcb.104.5.1281.
Crossref | PubMed | Web of Science | Google Scholar - 117. . The glutathione and thiol content of mammalian spermatozoa and seminal plasma. Biol Reprod 12: 641–646, 1975. doi:10.1095/biolreprod12.5.641.
Crossref | PubMed | Web of Science | Google Scholar - 118. . Isolation and properties of superoxide dismutase from ram spermatozoa and erythrocytes. Biol Reprod 18: 554–560, 1978. doi:10.1095/biolreprod18.4.554.
Crossref | PubMed | Web of Science | Google Scholar - 119. . Oxygen metabolism of mammalian spermatozoa. Generation of hydrogen peroxide by rabbit epididymal spermatozoa. Biochem J 198: 273–280, 1981. doi:10.1042/bj1980273.
Crossref | PubMed | Web of Science | Google Scholar - 120. . Association of classical semen parameters, sperm DNA fragmentation index, lipid peroxidation and antioxidant enzymatic activity of semen in ram-lambs. Theriogenology 65: 1407–1421, 2006. doi:10.1016/j.theriogenology.2005.05.056.
Crossref | PubMed | Web of Science | Google Scholar - 121. . Glutathione peroxidase (GPX) activity in seminal plasma of healthy and infertile males. J Endocrinol Invest 25: 983–986, 2002. doi:10.1007/BF03344072.
Crossref | PubMed | Web of Science | Google Scholar - 122. . Formation and dissociation of sperm bundles in monotremes. Biol Reprod 95:
91 , 2016. doi:10.1095/biolreprod.116.140491.
Crossref | PubMed | Web of Science | Google Scholar - 123. . Molecular diversification of the seminal fluid proteome in a recently diverged passerine species pair. Mol Biol Evol 37: 488–506, 2020. doi:10.1093/molbev/msz235.
Crossref | PubMed | Web of Science | Google Scholar - 124. . Antibacterial membrane attack by a pore-forming intestinal C-type lectin. Nature 505: 103–107, 2014. doi:10.1038/nature12729.
Crossref | PubMed | Web of Science | Google Scholar - 125. . Adrenomedullin regulates sperm motility and oviductal ciliary beat via cyclic adenosine 5′-monophosphate/protein kinase A and nitric oxide. Endocrinology 151: 3336–3347, 2010. doi:10.1210/en.2010-0077.
Crossref | PubMed | Web of Science | Google Scholar - 126. . Possible functions of adrenomedullin from the seminal fluid in the female reproductive tract of the rat. Syst Biol Reprod Med 58: 306–312, 2012. doi:10.3109/19396368.2012.695855.
Crossref | PubMed | Web of Science | Google Scholar - 127. . Neuropeptide Y in the human male genital tract. Life Sci 35: 2643–2648, 1984. doi:10.1016/0024-3205(84)90033-X.
Crossref | PubMed | Web of Science | Google Scholar - 128. . Peptidergic innervation within the prostate gland and seminal vesicle. Urol Res 18: 337–340, 1990. doi:10.1007/BF00300783.
Crossref | PubMed | Google Scholar - 129. . Prostasomes are neuroendocrine-like vesicles in human semen. Prostate 29: 287–295, 1996. doi:10.1002/(SICI)1097-0045(199611)29:5<287::AID-PROS3>3.0.CO;2-7.
Crossref | PubMed | Web of Science | Google Scholar - 130. . Co-existence of neuropeptides and differential inhibition of vasodilator responses by neuropeptide Y in guinea pig uterine arteries. Neurosci Lett 100: 71–76, 1989. doi:10.1016/0304-3940(89)90662-9.
Crossref | PubMed | Web of Science | Google Scholar - 131. . Seminalplasmin: recent evolution of another member of the neuropeptide Y gene family. Proc Natl Acad Sci USA 92: 594–598, 1995. doi:10.1073/pnas.92.2.594.
Crossref | PubMed | Web of Science | Google Scholar - 132. . Two novel related peptides, neuropeptide Y (NPY) and peptide YY (PYY) inhibit the contraction of the electrically stimulated mouse vas deferens. Neuropeptides 3: 71–77, 1982. doi:10.1016/0143-4179(82)90001-4.
Crossref | PubMed | Web of Science | Google Scholar - 133. . Expression of gastrin-releasing peptide (GRP) in the bovine uterus during the estrous cycle. Arch Histol Cytol 66: 337–346, 2003. doi:10.1679/AOHC.66.337.
Crossref | PubMed | Google Scholar - 134. . Gastrin-releasing peptide receptors in normal and neoplastic human uterus: involvement of multiple tissue compartments. J Clin Endocrinol Metab 90: 4722–4729, 2005. doi:10.1210/JC.2005-0964.
Crossref | PubMed | Web of Science | Google Scholar - 135. . Effect of gastrin-releasing peptide on sperm functions. Mol Hum Reprod 2: 867–872, 1996. doi:10.1093/molehr/2.11.867.
Crossref | PubMed | Web of Science | Google Scholar - 136. . Renin-angiotensin system: biochemistry and mechanisms of action. Physiol Rev 57: 313–370, 1977. doi:10.1152/PHYSREV.1977.57.2.313.
Link | Web of Science | Google Scholar - 137. . Colocalization of angiotensinogen and glial fibrillary acidic protein in astrocytes in rat brain. Brain Res 374: 195–198, 1986. doi:10.1016/0006-8993(86)90411-7.
Crossref | PubMed | Web of Science | Google Scholar - 138. . Brain angiotensinogen: In vitro synthesis and chromatographic characterization. Brain Res 259: 275–283, 1983. doi:10.1016/0006-8993(83)91258-1.
Crossref | PubMed | Web of Science | Google Scholar - 139. . Identity of angiotensinogen precursors of rat brain and liver. Nature 308: 206–208, 1984. doi:10.1038/308206a0.
Crossref | PubMed | Web of Science | Google Scholar - 140. . Components of the renin-angiotensin system in the cerebrospinal fluid of rats and dogs with special consideration of the origin and the fate of angiotensin II. Neuroendocrinology 31: 297–308, 1980. doi:10.1159/000123092.
Crossref | PubMed | Web of Science | Google Scholar - 141. . Location and regulation of rat angiotensinogen messenger RNA. Hypertension 11: 591–596, 1988. doi:10.1161/01.HYP.11.6.591.
Crossref | PubMed | Web of Science | Google Scholar - 142. . Activation of the systemic and adipose renin-angiotensin system in rats with diet-induced obesity and hypertension. Am J Physiol Regul Integr Comp Physiol 287: R943–R949, 2004. doi:10.1152/ajpregu.00265.2004.
Link | Web of Science | Google Scholar - 143. . The human placental renin–angiotensin system. Front Neuroendocrinol 19: 232–252, 1998. doi:10.1006/FRNE.1998.0166.
Crossref | PubMed | Web of Science | Google Scholar - 144. . The expression and localization of the human placental prorenin/renin- angiotensin system throughout pregnancy: roles in trophoblast invasion and angiogenesis? Placenta 32: 956–962, 2011. doi:10.1016/j.placenta.2011.09.020.
Crossref | PubMed | Web of Science | Google Scholar - 145. . Deficiency or blockade of angiotensin II type 2 receptor delays tumorigenesis by inhibiting malignant cell proliferation and angiogenesis. Int J Cancer 127: 2279–2291, 2010. doi:10.1002/ijc.25234.
Crossref | PubMed | Web of Science | Google Scholar - 146. . Dual repressive effect of angiotensin II-type 1 receptor blocker telmisartan on angiotensin II-induced and estradiol-induced uterine leiomyoma cell proliferation. Hum Reprod 23: 440–446, 2008. doi:10.1093/humrep/dem247.
Crossref | PubMed | Web of Science | Google Scholar - 147. . Angiotensin II stimulation of Na+/K+ATPase activity and cell growth by calcium-independent pathway in MCF-7 breast cancer cells. J Endocrinol 173: 315–323, 2002. doi:10.1677/joe.0.1730315.
Crossref | PubMed | Web of Science | Google Scholar - 148. . PKC-ζ is required for angiotensin II-induced activation of ERK and synthesis of C-FOS in MCF-7 cells. J Cell Physiol 197: 61–68, 2003. doi:10.1002/jcp.10336.
Crossref | PubMed | Web of Science | Google Scholar - 149. . Angiotensin II activates extracellular signal regulated kinases via protein kinase C and epidermal growth factor receptor in breast cancer cells. J Cell Physiol 196: 370–377, 2003. doi:10.1002/jcp.10313.
Crossref | PubMed | Web of Science | Google Scholar - 150. . Angiotensin II and epidermal growth factor receptor cross-talk mediated by a disintegrin and metalloprotease accelerates tumor cell proliferation of hepatocellular carcinoma cell lines. Hepatol Res 38: 601–613, 2008. doi:10.1111/j.1872-034X.2007.00304.x.
Crossref | PubMed | Web of Science | Google Scholar - 151. . Angiotensin II is a growth factor in the peri-implantation rat embryo. J Anat 195: 75–86, 1999. doi:10.1046/j.1469-7580.1999.19510075.x.
Crossref | PubMed | Web of Science | Google Scholar - 152. . Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75: 1417–1430, 1993. doi:10.1016/0092-8674(93)90627-3.
Crossref | PubMed | Web of Science | Google Scholar - 153. . Mutations affecting segment number and polarity in drosophila. Nature 287: 795–801, 1980. doi:10.1038/287795a0.
Crossref | PubMed | Web of Science | Google Scholar - 154. . Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo. Development 128: 1717–1730, 2001. doi:10.1242/dev.128.10.1717.
Crossref | PubMed | Web of Science | Google Scholar - 155. . Identification of Indian hedgehog as a progesterone-responsive gene in the murine uterus. Mol Endocrinol 16: 2338–2348, 2002. doi:10.1210/me.2001-0154.
Crossref | PubMed | Google Scholar - 156. . Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nat Genet 38: 1204–1209, 2006. doi:10.1038/ng1874.
Crossref | PubMed | Web of Science | Google Scholar - 157. . Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology 147: 1097–1121, 2006. doi:10.1210/en.2005-1076.
Crossref | PubMed | Web of Science | Google Scholar - 158. . Indian hedgehog and its targets in human endometrium: Menstrual cycle expression and response to CDB-2914. J Clin Endocrinol Metab 95: 5330–5337, 2010. doi:10.1210/jc.2010-0637.
Crossref | PubMed | Web of Science | Google Scholar - 159. . Expression of genes involved in progesterone receptor paracrine signaling and their effect on litter size in pigs. J Anim Sci Biotechnol 7:
31 , 2016. doi:10.1186/s40104-016-0090-z.
Crossref | PubMed | Web of Science | Google Scholar - 160. . Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc Natl Acad Sci USA 101: 8204–8208, 2004. doi:10.1073/PNAS.0402508101.
Crossref | PubMed | Web of Science | Google Scholar - 161. . Role and mechanism of insulin-like growth factor 2 on the proliferation of human trophoblasts in vitro. J Obstet Gynaecol Res 42: 44–51, 2016. doi:10.1111/jog.12853.
Crossref | PubMed | Web of Science | Google Scholar - 162. . Insulin-like growth factor I and II regulate the life cycle of trophoblast in the developing human placenta. Am J Physiol Cell Physiol 294: C1313–C1322, 2008. doi:10.1152/ajpcell.00035.2008.
Link | Web of Science | Google Scholar - 163. . IGF2 actions on trophoblast in human placenta are regulated by the insulin-like growth factor 2 receptor, which can function as both a signaling and clearance receptor. Biol Reprod 84: 440–446, 2011. doi:10.1095/biolreprod.110.088195.
Crossref | PubMed | Web of Science | Google Scholar - 164. . Insulin‐like growth factors i and ii: some biological actions and receptor binding characteristics of two purified constituents of nonsuppressible insulin‐like activity of human serum. Eur J Biochem 87: 285–296, 1978. doi:10.1111/j.1432-1033.1978.tb12377.x.
Crossref | PubMed | Google Scholar - 165. . The effects of infusion of insulinlike growth factor (IGF) I, IGF-II, and insulin on glucose and protein metabolism in fasted lambs. J Clin Invest 88: 614–622, 1991. doi:10.1172/JCI115346.
Crossref | PubMed | Web of Science | Google Scholar - 166. . Pleiotrophin stimulates fibroblasts and endothelial and epithelial cells and is expressed in human cancer. J Biol Chem 267: 25889–25897, 1992. doi:10.1016/S0021-9258(18)35692-8.
Crossref | PubMed | Web of Science | Google Scholar - 167. . Expression of the heparin-binding cytokines, midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesis. Development 121: 37–51, 1995. doi:10.1242/dev.121.1.37.
Crossref | PubMed | Web of Science | Google Scholar - 168. . Pleiotrophin enhances clonal growth and long-term expansion of human embryonic stem cells. Stem Cells 25: 3029–3037, 2007. doi:10.1634/stemcells.2007-0372.
Crossref | PubMed | Web of Science | Google Scholar - 169. . RhoA/ROCK signaling antagonizes bovine trophoblast stem cell self-renewal and regulates preimplantation embryo size and differentiation. Development 149:
dev200115 , 2022. doi:10.1242/DEV.200115.
Crossref | PubMed | Web of Science | Google Scholar - 170. . The proteins in whey. Compte rendu des Travaux du Laboratoire de Carlsberg, Ser Chim 20 (7): 55–99, 1940.
Google Scholar - 171. . Antimicrobial factors in whole saliva of human infants. Infect Immun 51: 49–53, 1986. doi:10.1128/iai.51.1.49-53.1986.
Crossref | PubMed | Web of Science | Google Scholar - 172. . Effect of lactoferrin feeding on the host antifungal response in guinea-pigs infected or immunised with Trichophyton mentagrophytes. J Med Microbiol 51: 844–850, 2002. doi:10.1099/0022-1317-51-10-844.
Crossref | PubMed | Web of Science | Google Scholar - 173. . Lactoferrin feeding augments peritoneal macrophage activities in mice intraperitoneally injected with inactivated Candida albicans. Microbiol Immunol 47: 37–43, 2003. doi:10.1111/j.1348-0421.2003.tb02783.x.
Crossref | PubMed | Web of Science | Google Scholar - 174. . Influence of lactoferrin feeding and injection against systemic staphylococcal infections in mice. J Appl Microbiol 86: 135–144, 1999. doi:10.1046/j.1365-2672.1999.00644.x.
Crossref | PubMed | Web of Science | Google Scholar - 175. . Orally administered bovine lactoferrin inhibits bacterial translocation in mice fed bovine milk. Appl Environ Microbiol 61: 4131–4134, 1995. doi:10.1128/aem.61.11.4131-4134.1995.
Crossref | PubMed | Web of Science | Google Scholar - 176. . Protective influence of lactoferrin on mice infected with the polycythemia-inducing strain of Friend virus complex. Cancer Res 47: 4184–4188, 1987.
PubMed | Web of Science | Google Scholar - 177. . Inhibition with lactoferrin of in vitro infection with human herpes virus. Jpn J Med Sci Biol 47: 73–85, 1994. doi:10.7883/yoken1952.47.73.
Crossref | PubMed | Google Scholar - 178. . Inhibition of bacteria by lactoferrin and other iron-chelating agents. Biochim Biophys Acta 170: 351–365, 1968. doi:10.1016/0304-4165(68)90015-9.
Crossref | PubMed | Web of Science | Google Scholar - 179. . Antibacterial activity of lactoferrin and a pepsin-derived lactoferrin peptide fragment. Infect Immun 61: 719–728, 1993. doi:10.1128/iai.61.2.719-728.1993.
Crossref | PubMed | Web of Science | Google Scholar - 180. . Fluctuations of lactoferrin protein and messenger ribonucleic acid in the reproductive tract of the mouse during the estrous cycle. Biol Reprod 47: 903–915, 1992. doi:10.1095/biolreprod47.5.903.
Crossref | PubMed | Web of Science | Google Scholar - 181. . Lactotransferrin gene expression in the mouse uterus and mammary gland. Endocrinology 124: 992–999, 1989. doi:10.1210/endo-124-2-992.
Crossref | PubMed | Web of Science | Google Scholar - 182. . Characterization of the cervical mucus plug in mares. Reproduction 153: 197–210, 2017. doi:10.1530/REP-16-0396.
Crossref | PubMed | Web of Science | Google Scholar - 183. . Proteins in the uterine secretions of the cow. J Reprod Fertil 56: 119–127, 1979. doi:10.1530/jrf.0.0560119.
Crossref | PubMed | Google Scholar - 184. . Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium. Physiol Genomics 41: 53–62, 2010. doi:10.1152/physiolgenomics.00162.2009.
Link | Web of Science | Google Scholar - 185. . Proteome of the early embryo-maternal dialogue in the cattle uterus. J Proteome Res 11: 751–766, 2012. doi:10.1021/pr200969a.
Crossref | PubMed | Web of Science | Google Scholar - 186. . Serum amyloid A3 binds MD-2 to activate p38 and NF-κB pathways in a MyD88-dependent manner. J Immunol 191: 1856–1864, 2013. doi:10.4049/jimmunol.1201996.
Crossref | PubMed | Web of Science | Google Scholar - 187. . Expression of the third member of the serum amyloid A gene family in mouse adipocytes. J Exp Med 169: 1841–1846, 1989. doi:10.1084/jem.169.5.1841.
Crossref | PubMed | Web of Science | Google Scholar - 188. . Imbalance of Clara cell-mediated homeostatic inflammation is involved in lung metastasis. Oncogene 30: 3429–3439, 2011. doi:10.1038/onc.2011.53.
Crossref | PubMed | Web of Science | Google Scholar - 189. . The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol 10: 1349–1355, 2008. doi:10.1038/ncb1794.
Crossref | PubMed | Web of Science | Google Scholar - 190. . Serum amyloid A3 does not contribute to circulating SAA levels. J Lipid Res 50: 1353–1362, 2009. doi:10.1194/jlr.M900089-JLR200.
Crossref | PubMed | Web of Science | Google Scholar - 191. . Transcriptome profiling of buffalo endometrium reveals molecular signature distinct to early pregnancy. Gene 743:
144614 , 2020. doi:10.1016/j.gene.2020.144614.
Crossref | PubMed | Web of Science | Google Scholar - 192. . The role of bactericidal/permeability-increasing protein as a natural inhibitor of bacterial endotoxin. J Immunol 148: 532–537, 1992.
Crossref | PubMed | Web of Science | Google Scholar - 193. . Bactericidal/permeability-increasing protein and lipopolysaccharide (LPS)-binding protein. LPS binding properties and effects on LPS-mediated cell activation. 269: 17411–17416, 1994. doi:10.1016/S0021-9258(17)32454-7.
Crossref | PubMed | Google Scholar - 194. . Oestrus synchronisation and superovulation alter the cervicovaginal mucus proteome of the ewe. J Proteomics 155: 1–10, 2017. doi:10.1016/j.jprot.2017.01.007.
Crossref | PubMed | Web of Science | Google Scholar - 195. . Proteomic analysis of amniotic and allantoic fluid from buffaloes during foetal development. Reprod Domest Anim 54: 1507–1515, 2019. doi:10.1111/rda.13557.
Crossref | PubMed | Web of Science | Google Scholar - 196. . Early protein profile of human embryonic secretome. Front Biosci (Landmark Ed) 21: 620–634, 2016. doi:10.2741/4410.
Crossref | PubMed | Web of Science | Google Scholar - 197. . Molecular characterization of a gene of the “EGF family” expressed in undifferentiated human NTERA2 teratocarcinoma cells. EMBO J 8: 1987–1991, 1989. doi:10.1002/j.1460-2075.1989.tb03605.x.
Crossref | PubMed | Web of Science | Google Scholar - 198. . Differential expression of epidermal growth factor-related proteins in human colorectal tumors. Proc Natl Acad Sci USA 88: 7792–7796, 1991. doi:10.1073/pnas.88.17.7792.
Crossref | PubMed | Web of Science | Google Scholar - 199. . Differential immunohistochemical detection of amphiregulin and cripto in human normal colon and colorectal tumors. Cancer Res 52: 3467–3473, 1992.
PubMed | Web of Science | Google Scholar - 200. . Epidermal growth factor-related peptides in the pathogenesis of human breast cancer. Breast Cancer Res Treat 29: 11–27, 1994. doi:10.1007/BF00666178.
Crossref | PubMed | Web of Science | Google Scholar - 201. . Abrogation of the Cripto gene in mouse leads to failure of postgastrulation morphogenesis and lack of differentiation of cardiomyocytes. Development 126: 483–494, 1999. doi:10.1242/dev.126.3.483.
Crossref | PubMed | Web of Science | Google Scholar - 202. . Detection of amphiregulin and Cripto-1 in mammary tumors from transgenic mice. Mol Carcinog 15: 44–56, 1996. doi:10.1002/(SICI)1098-2744(199601)15:1<44::AID-MC7>3.0.CO;2-S.
Crossref | PubMed | Web of Science | Google Scholar - 203. . Expression of teratocarcinoma-derived growth factor-1 (TDGF-1) in testis germ cell tumors and its effects on growth and differentiation of embryonal carcinoma cell line NTERA2/D1. Oncogene 15: 927–936, 1997. doi:10.1038/sj.onc.1201260.
Crossref | PubMed | Web of Science | Google Scholar - 204. . Cripto-1 activates nodal- and ALK4-dependent and -independent signaling pathways in mammary epithelial cells. Mol Cell Biol 22: 2586–2597, 2002. doi:10.1128/MCB.22.8.2586-2597.2002.
Crossref | PubMed | Web of Science | Google Scholar - 205. . Cripto-1 ablation disrupts alveolar development in the mouse mammary gland through a progesterone receptor-mediated pathway. Am J Pathol 185: 2907–2922, 2015. doi:10.1016/j.ajpath.2015.07.023.
Crossref | PubMed | Web of Science | Google Scholar - 206. . Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. J Clin Invest 84: 1470–1478, 1989. doi:10.1172/JCI114322.
Crossref | PubMed | Web of Science | Google Scholar - 207. . Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246: 1306–1309, 1989. doi:10.1126/science.2479986.
Crossref | PubMed | Web of Science | Google Scholar - 208. . Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science 246: 1309–1312, 1989. doi:10.1126/science.2479987.
Crossref | PubMed | Web of Science | Google Scholar - 209. . Demonstration of a vascular permeability factor in human placental extract. Lancet 2: 112–114, 1965. doi:10.1016/S0140-6736(65)92226-9.
Crossref | PubMed | Web of Science | Google Scholar - 210. . VEGF-A165B is cytoprotective and antiangiogenic in the retina. Invest Ophthalmol Vis Sci 51: 4273–4281, 2010. doi:10.1167/iovs.09-4296.
Crossref | PubMed | Web of Science | Google Scholar - 211. . The role of VEGF-A165b in trophoblast survival. BMC Pregnancy Childbirth 14:
278 , 2014. doi:10.1186/1471-2393-14-278.
Crossref | PubMed | Web of Science | Google Scholar - 212. . Purification and properties of enkephalin - The possible endogenous ligand for the morphine receptor. Life Sci 16: 1753–1758, 1975. doi:10.1016/0024-3205(75)90268-4.
Crossref | PubMed | Web of Science | Google Scholar - 213. . Posttranslational processing of proenkephalin in AtT-20 cells: evidence for cleavage at a lys-lys site. Endocrinology 131: 2287–2296, 1992. doi:10.1210/endo.131.5.1425427.
Crossref | PubMed | Web of Science | Google Scholar - 214. . Specificity of prohormone convertase 2 on proenkephalin and proenkephalin-related substrates. J Biol Chem 273: 22672–22680, 1998. doi:10.1074/jbc.273.35.22672.
Crossref | PubMed | Web of Science | Google Scholar - 215. . Processing of proenkephalin-A in bovine chromaffin cells: Identification of natural derived fragments by N-terminal sequencing and matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Biol Chem 275: 38355–38362, 2000. doi:10.1074/jbc.M007557200.
Crossref | PubMed | Web of Science | Google Scholar - 216. . Estrous cycle- and pregnancy-related differences in expression of the proenkephalin and proopiomelanocortin genes in the ovary and uterus. Endocrinology 122: 1466–1471, 1988. doi:10.1210/ENDO-122-4-1466.
Crossref | PubMed | Web of Science | Google Scholar - 217. . Local regulation within the female reproductive system and upon embryonic implantation: identification of cells expressing proenkephalin A. Mol Endocrinol 4: 146–154, 1990. doi:10.1210/mend-4-1-146.
Crossref | PubMed | Google Scholar - 218. . A genomic approach to identify novel progesterone receptor regulated pathways in the uterus during implantation. Mol Endocrinol 16: 2853–2871, 2002. doi:10.1210/me.2002-0270.
Crossref | PubMed | Google Scholar - 219. . Expression of opioid receptors and ligands in pregnant mouse uterus and placenta. Biol Reprod 59: 925–932, 1998. doi:10.1095/biolreprod59.4.925.
Crossref | PubMed | Web of Science | Google Scholar - 220. . Gene expression profiling of bovine endometrium during the oestrous cycle: detection of molecular pathways involved in functional changes. J Mol Endocrinol 34: 889–908, 2005. doi:10.1677/jme.1.01799.
Crossref | PubMed | Web of Science | Google Scholar - 221. . The C-terminal bisphosphorylated proenkephalin-A-(209–237)-peptide from adrenal medullary chromaffin granules possesses antibacterial activity. Eur J Biochem 235: 516–525, 1996 [Erratum in Eur J Biochem 237: 883, 1996]. doi:10.1111/J.1432-1033.1996.T01-1-00516.X.
Crossref | PubMed | Google Scholar - 222. . Characterization of antibacterial COOH-terminal proenkephalin-A-derived peptides (PEAP) in infectious fluids: Importance of enkelytin, the antibacterial PEAP209-237 secreted by stimulated chromaffin cells. J Biol Chem 273: 29847–29856, 1998. doi:10.1074/jbc.273.45.29847.
Crossref | PubMed | Web of Science | Google Scholar - 223. . The chromogranin A-derived peptides vasostatin-I and catestatin as regulatory peptides for cardiovascular functions. Cardiovasc Res 85: 9–16, 2010. doi:10.1093/cvr/cvp266.
Crossref | PubMed | Web of Science | Google Scholar - 224. . Antibacterial activity of glycosylated and phosphorylated chromogranin A-derived peptide 173-194 from bovine adrenal medullary chromaffin granules. J Biol Chem 271: 28533–28540, 1996. doi:10.1074/jbc.271.45.28533.
Crossref | PubMed | Web of Science | Google Scholar - 225. . Radioimmunoassay of chromogranin a in plasma as a measure of exocytotic sympathoadrenal activity in normal subjects and patients with pheochromocytoma. N Engl J Med 311: 764–770, 1984. doi:10.1056/NEJM198409203111204.
Crossref | PubMed | Web of Science | Google Scholar - 226. . Processing-independent quantitation of chromogranin A in plasma from patients with neuroendocrine tumors and small-cell lung carcinomas. Clin Chem 53: 438–446, 2007. doi:10.1373/clinchem.2006.076158.
Crossref | PubMed | Web of Science | Google Scholar - 227. . Composition of the bovine uterine proteome is associated with stage of cycle and concentration of systemic progesterone. Proteomics 13: 3333–3353, 2013. doi:10.1002/pmic.201300204.
Crossref | PubMed | Web of Science | Google Scholar - 228. . Granulins: the structure and function of an emerging family of growth factors. J Endocrinol 158: 145–151, 1998. doi:10.1677/joe.0.1580145.
Crossref | PubMed | Web of Science | Google Scholar - 229. . The complementary deoxyribonucleic acid sequence, tissue distribution, and cellular localization of the rat granulin precursor. Endocrinology 133: 2682–2689, 1993. doi:10.1210/endo.133.6.8243292.
Crossref | PubMed | Web of Science | Google Scholar - 230. . Cellular localization of gene expression for progranulin. J Histochem Cytochem 48: 999–1009, 2000. doi:10.1177/002215540004800713.
Crossref | PubMed | Web of Science | Google Scholar - 231. . Modulation of mouse preimplantation embryo development by acrogranin (epithelin/granulin precursor). Dev Biol 217: 406–418, 2000. doi:10.1006/dbio.1999.9564.
Crossref | PubMed | Web of Science | Google Scholar - 232. . Effects of progranulin on blastocyst hatching and subsequent adhesion and outgrowth in the mouse. Biol Reprod 73: 434–442, 2005. doi:10.1095/biolreprod.105.040030.
Crossref | PubMed | Web of Science | Google Scholar - 233. . Spatiotemporal expression pattern of progranulin in embryo implantation and placenta formation suggests a role in cell proliferation, remodeling, and angiogenesis. Reproduction 136: 247–257, 2008. doi:10.1530/REP-08-0044.
Crossref | PubMed | Web of Science | Google Scholar - 234. . Progranulin promotes melanoma progression by inhibiting natural killer cell recruitment to the tumor microenvironment. Cancer Lett 465: 24–35, 2019. doi:10.1016/j.canlet.2019.08.018.
Crossref | PubMed | Web of Science | Google Scholar - 235. . EphA2 is a functional receptor for the growth factor progranulin. J Cell Biol 215: 687–703, 2016. doi:10.1083/jcb.201603079.
Crossref | PubMed | Web of Science | Google Scholar - 236. . Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev 79: 1283–1316, 1999. doi:10.1152/physrev.1999.79.4.1283.
Link | Web of Science | Google Scholar - 237. . Selective expression of PDGF A and its receptor during early mouse embryogenesis. Dev Biol 138: 114–122, 1990. doi:10.1016/0012-1606(90)90181-H.
Crossref | PubMed | Web of Science | Google Scholar - 238. . Temporal expression of platelet-derived growth factor (PDGF)-A and its receptor in human preimplantation embryos. Mol Hum Reprod 2: 507–512, 1996. doi:10.1093/molehr/2.7.507.
Crossref | PubMed | Web of Science | Google Scholar - 239. . The expression of PDGF α- and β-receptors in subpopulations of PDGF-producing cells implicates autocrine stimulatory loops in the control of proliferation in cytotrophoblasts that have invaded the maternal endometrium. Growth Factors 6: 219–231, 1992. doi:10.3109/08977199209026929.
Crossref | PubMed | Google Scholar - 240. . TIMP-2 (tissue inhibitor of metalloproteinase-2) regulates MMP-2 (matrix metalloproteinase-2) activity in the extracellular environment after pro-MMP-2 activation by MT1 (membrane type 1)-MMP. Biochem J 374: 739–745, 2003. doi:10.1042/BJ20030557.
Crossref | PubMed | Web of Science | Google Scholar - 241. . Bovine endometrial metallopeptidases MMP14 and MMP2 and the metallopeptidase inhibitor TIMP2 participate in maternal preparation of pregnancy. Mol Cell Endocrinol 332: 48–57, 2011. doi:10.1016/j.mce.2010.09.009.
Crossref | PubMed | Web of Science | Google Scholar - 242. . TIMP-2 is required for efficient activation of proMMP-2 in vivo. J Biol Chem 275: 26411–26415, 2000. doi:10.1074/jbc.M001270200.
Crossref | PubMed | Web of Science | Google Scholar - 243. . Inactivating mutation of the mouse tissue inhibitor of metalloproteinases-2(Timp-2) gene alters proMMP-2 activation. J Biol Chem 275: 26416–26422, 2000. doi:10.1074/jbc.M001271200.
Crossref | PubMed | Web of Science | Google Scholar - 244. . The expression of tissue inhibitor of metalloproteinase 2 (TIMP-2) is required for normal development of zebrafish embryos. Dev Genes Evol 213: 382–389, 2003. doi:10.1007/s00427-003-0333-9.
Crossref | PubMed | Web of Science | Google Scholar - 245. . Connective tissue growth factor: Structure-function relationships of a mosaic, multifunctional protein. Growth Factors 26: 80–91, 2008. doi:10.1080/08977190802025602.
Crossref | PubMed | Web of Science | Google Scholar - 246. . Immunohistochemical localization of connective tissue growth factor (CTGF) in the mouse embryo between days 7.5 and 14.5 of gestation. Growth Factors 17: 115–124, 1999. doi:10.3109/08977199909103520.
Crossref | PubMed | Web of Science | Google Scholar - 247. . Localization of connective tissue growth factor during the period of embryo implantation in the mouse. Biol Reprod 59: 1207–1213, 1998. doi:10.1095/biolreprod59.5.1207.
Crossref | PubMed | Web of Science | Google Scholar - 248. . Localization of connective tissue growth factor in human uterine tissues. Mol Hum Reprod 6: 1093–1098, 2000. doi:10.1093/molehr/6.12.1093.
Crossref | PubMed | Web of Science | Google Scholar - 249. . Purification and characterization of novel heparin-binding growth factors in uterine secretory fluids. Identification as heparin-regulated M(r) 10,000 forms of connective tissue growth factor. J Biol Chem 272: 20275–20282, 1997. doi:10.1074/jbc.272.32.20275.
Crossref | PubMed | Web of Science | Google Scholar - 250. . Characterization of 16- to 20-kilodalton (kDa) connective tissue growth factors (CTGFs) and demonstration of proteolytic activity for 38-kDa CTGF in pig uterine luminal flushings. Biol Reprod 59: 828–835, 1998 [Erratum in Biol Reprod 59: 1554, 1998]. doi:10.1095/biolreprod59.4.828.
Crossref | PubMed | Web of Science | Google Scholar - 251. . Localisation of stem cell factor, stanniocalcin-1, connective tissue growth factor and heparin-binding epidermal growth factor in the bovine uterus at the time of blastocyst formation. Reprod Fertil Dev 29: 2127–2139, 2017. doi:10.1071/RD16383.
Crossref | PubMed | Web of Science | Google Scholar - 252. . Actions of activin A, connective tissue growth factor, hepatocyte growth factor and teratocarcinoma-derived growth factor 1 on the development of the bovine preimplantation embryo. Reprod Fertil Dev 29: 1329–1339, 2017. doi:10.1071/RD16033.
Crossref | PubMed | Web of Science | Google Scholar - 253. . Supplementation with CTGF, SDF1, NGF, and HGF promotes ovine in vitro oocyte maturation and early embryo development. Domest Anim Endocrinol 65: 38–48, 2018. doi:10.1016/j.domaniend.2018.05.003.
Crossref | PubMed | Web of Science | Google Scholar - 254. . CCN2/CTGF binds to fibroblast growth factor receptor 2 and modulates its signaling. FEBS Lett 586: 4270–4275, 2012. doi:10.1016/j.febslet.2012.10.038.
Crossref | PubMed | Web of Science | Google Scholar - 255. . Connective-tissue growth factor (CTGF) modulates cell signalling by bmp and TGF-β. Nat Cell Biol 4: 599–604, 2002. doi:10.1038/ncb826.
Crossref | PubMed | Web of Science | Google Scholar - 256. . A new function of BMP4: dual role for BMP4 in regulation of Sonic hedgehog expression in the mouse tooth germ. Development 127: 1431–1443, 2000. doi:10.1242/dev.127.7.1431.
Crossref | PubMed | Web of Science | Google Scholar - 257. . Bone morphogenetic proteins in bone stimulate osteoclasts and osteoblasts during bone development. J Bone Miner Res 21: 1022–1033, 2006. doi:10.1359/jbmr.060411.
Crossref | PubMed | Web of Science | Google Scholar - 258. . Novel regulators of bone formation: molecular clones and activities. Science 242: 1528–1534, 1988. doi:10.1126/science.3201241.
Crossref | PubMed | Web of Science | Google Scholar - 259. . Bone: formation by autoinduction. Science 150: 893–899, 1965. doi:10.1126/science.150.3698.893.
Crossref | PubMed | Web of Science | Google Scholar - 260. . Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors . Proc Natl Acad Sci USA 98: 1047–1052, 2001. doi:10.1073/pnas.98.3.1047.
Crossref | PubMed | Web of Science | Google Scholar - 261. . Dynamic expression of bone morphogenetic protein 4 in reproductive organs of female mice. Reproduction 142: 573–579, 2011. doi:10.1530/REP-10-0299.
Crossref | PubMed | Web of Science | Google Scholar - 262. . Expression of bone morphogenetic protein 2, 4, and related components of the BMP signaling pathway in the mouse uterus during the estrous cycle. J Zhejiang Univ Sci B 15: 601–610, 2014. doi:10.1631/jzus.B1300288.
Crossref | PubMed | Web of Science | Google Scholar - 263. . Profiling of circadian genes expressed in the uterus endometrial stromal cells of pregnant rats as revealed by DNA microarray coupled with RNA interference. Front Endocrinol (Lausanne) 4:
82 , 2013. doi:10.3389/fendo.2013.00082.
Crossref | PubMed | Google Scholar - 264. . Inhibitory role of REV-ERBα in the expression of bone morphogenetic protein gene family in rat uterus endometrium stromal cells. Am J Physiol Cell Physiol 308: C528–C538, 2015. doi:10.1152/ajpcell.00220.2014.
Link | Web of Science | Google Scholar - 265. . Paracrine effects of embryo-derived FGF4 and BMP4 during pig trophoblast elongation. Dev Biol 387: 15–27, 2014. doi:10.1016/j.ydbio.2014.01.008.
Crossref | PubMed | Web of Science | Google Scholar - 266. . Short-term BMP-4 treatment initiates mesoderm induction in human embryonic stem cells. Blood 111: 1933–1941, 2008. doi:10.1182/blood-2007-02-074120.
Crossref | PubMed | Web of Science | Google Scholar - 267. . BRACHYURY and CDX2 mediate BMP-induced differentiation of human and mouse pluripotent stem cells into embryonic and extraembryonic lineages. Cell Stem Cell 9: 144–155, 2011. doi:10.1016/j.stem.2011.06.015.
Crossref | PubMed | Web of Science | Google Scholar - 268. . Effects of FGF2 and oxygen in the BMP4-driven differentiation of trophoblast from human embryonic stem cells. Stem Cell Res 1: 61–74, 2007. doi:10.1016/j.scr.2007.09.004.
Crossref | PubMed | Web of Science | Google Scholar - 269. . FGF inhibition directs BMP4-mediated differentiation of human embryonic stem cells to syncytiotrophoblast. Stem Cells Dev 21: 2987–3000, 2012. doi:10.1089/scd.2012.0099.
Crossref | PubMed | Web of Science | Google Scholar - 270. . Midkine and pleiotrophin: two related proteins involved in development, survival, inflammation and tumorigenesis. J Biochem 132: 359–371, 2002. doi:10.1093/oxfordjournals.jbchem.a003231.
Crossref | PubMed | Web of Science | Google Scholar - 271. . cDNA cloning and sequencing of a new gene intensely expressed in early differentiation stages of embryonal carcinoma cells and in mid-gestation period of mouse embryogenesis. Biochem Biophys Res Commun 151: 1312–1318, 1988. doi:10.1016/s0006-291x(88)80505-9.
Crossref | PubMed | Web of Science | Google Scholar - 272. . Midkine inhibits caspase-dependent apoptosis via the activation of mitogen-activated protein kinase and phosphatidylinositol 3-kinase in cultured neurons. J Neurochem 73: 2084–2092, 1999.
Crossref | PubMed | Web of Science | Google Scholar - 273. . Midkine, a heparin-binding growth/differentiation factor, exhibits nerve cell adhesion and guidance activity for neurite outgrowth in vitro. J Biochem 119: 1150–1156, 1996. doi:10.1093/oxfordjournals.jbchem.a021361.
Crossref | PubMed | Web of Science | Google Scholar - 274. . A receptor-like protein-tyrosine phosphatase PTPζ/RPTPβ binds a heparin-binding growth factor midkine: involvement of arginine 78 of midkine in the high affinity binding to PTPζ. J Biol Chem 274: 12474–12479, 1999. doi:10.1074/jbc.274.18.12474.
Crossref | PubMed | Web of Science | Google Scholar - 275. . Midkine, a retinoic acid-inducible growth/differentiation factor: Immunochemical evidence for the function and distribution. Dev Biol 159: 392–402, 1993. doi:10.1006/dbio.1993.1250.
Crossref | PubMed | Web of Science | Google Scholar - 276. . Promotion of self-renewal of embryonic stem cells by midkine. Acta Pharmacol Sin 31: 629–637, 2010. doi:10.1038/aps.2010.39.
Crossref | PubMed | Web of Science | Google Scholar - 277. . Effects of midkine during in vitro maturation of bovine oocytes on subsequent developmental competence. Biol Reprod 63: 1067–1074, 2000. doi:10.1095/biolreprod63.4.1067.
Crossref | PubMed | Web of Science | Google Scholar - 278. . A novel 17 kD heparin-binding growth factor (HBGF-8) in bovine uterus: purification and N-terminal amino acid sequence. Biochem Biophys Res Commun 165: 1096–1103, 1989. doi:10.1016/0006-291X(89)92715-0.
Crossref | PubMed | Web of Science | Google Scholar - 279. . Pleiotrophin: activity and mechanism. Adv Clin Chem 98: 51–89, 2020. doi:10.1016/BS.ACC.2020.02.003.
Crossref | PubMed | Web of Science | Google Scholar - 280. . Wnt signalling in implantation, decidualisation and placental differentiation–review. Placenta 31: 839–847, 2010. doi:10.1016/J.PLACENTA.2010.07.011.
Crossref | PubMed | Web of Science | Google Scholar - 281. . Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet 7: 185–199, 2006. doi:10.1038/nrg1808.
Crossref | PubMed | Web of Science | Google Scholar - 282. . Vascular development in the retina and inner ear: control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair. Cell 116: 883–895, 2004. doi:10.1016/S0092-8674(04)00216-8.
Crossref | PubMed | Web of Science | Google Scholar - 283. . Phenotype discovery by gene expression profiling: mapping of biological processes linked to BMP-2-mediated osteoblast differentiation. J Cell Biochem 89: 401–426, 2003. doi:10.1002/JCB.10515.
Crossref | PubMed | Web of Science | Google Scholar - 284. . Mimecan/osteoglycin-deficient mice have collagen fibril abnormalities. Mol Vis 8: 407–415, 2002.
PubMed | Web of Science | Google Scholar - 285. . Specific requirement of Gli transcription factors in Hedgehog-mediated intestinal development. J Biol Chem 288: 17589–17596, 2013. doi:10.1074/JBC.M113.467498.
Crossref | PubMed | Web of Science | Google Scholar - 286. . Osteoglycin (OGN) reverses epithelial to mesenchymal transition and invasiveness in colorectal cancer via EGFR/Akt pathway. J Exp Clin Cancer Res 37:
41 , 2018. doi:10.1186/S13046-018-0718-2.
Crossref | PubMed | Web of Science | Google Scholar - 287. . Adrenomedullin improves fertility and promotes pinopodes and cell junctionsin the peri-implantation endometrium. Biol Reprod 97: 466–477, 2017. doi:10.1093/BIOLRE/IOX101.
Crossref | PubMed | Web of Science | Google Scholar - 288. . EGFL7: master regulator of cancer pathogenesis, angiogenesis and an emerging mediator of bone homeostasis. J Cell Physiol 233: 8526–8537, 2018. doi:10.1002/JCP.26792.
Crossref | PubMed | Web of Science | Google Scholar - 289. . Epidermal growth factor-like domain 7 (EGFL7) modulates Notch signalling and affects neural stem cell renewal. Nat Cell Biol 11: 873–880, 2009 [Erratum in Nat Cell Biol 11: 1043, 2009]. doi:10.1038/NCB1896.
Crossref | PubMed | Web of Science | Google Scholar - 290. . The integrin αvβ3 is a receptor for the latency-associated peptides of transforming growth factors β1 and β3. Biochem J 369: 311–318, 2003. doi:10.1042/BJ20020809.
Crossref | PubMed | Web of Science | Google Scholar - 291. . The integrin αvβ6 binds and activates latent TGFβ1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96: 319–328, 1999. doi:10.1016/S0092-8674(00)80545-0.
Crossref | PubMed | Web of Science | Google Scholar - 292. . Integrin αvβ6-mediated activation of latent TGF-β requires the latent TGF-β binding protein-1. J Cell Biol 165: 723–734, 2004. doi:10.1083/jcb.200312172.
Crossref | PubMed | Web of Science | Google Scholar - 293. . The effect of activin-A on the development of mouse preimplantation embryos in vitro. J Assist Reprod Genet 13: 669–674, 1996. doi:10.1007/BF02069647.
Crossref | PubMed | Web of Science | Google Scholar - 294. . Activin A and follistatin regulate developmental competence of in vitro-produced bovine embryos. Biol Reprod 59: 1017–1022, 1998. doi:10.1095/BIOLREPROD59.5.1017.
Crossref | PubMed | Web of Science | Google Scholar - 295. . Effect of vascular endothelial growth factor on maturation, fertilization and developmental competence of bovine oocytes. J Vet Med Sci 64: 803–806, 2002. doi:10.1292/JVMS.64.803.
Crossref | PubMed | Web of Science | Google Scholar - 296. . Embryotropic effects of vascular endothelial growth factor on porcine embryos produced by in vitro fertilization. Theriogenology 120: 147–156, 2018. doi:10.1016/J.THERIOGENOLOGY.2018.07.024.
Crossref | PubMed | Web of Science | Google Scholar - 297. . A novel role for vascular endothelial growth factor as an autocrine survival factor for embryonic stem cells during hypoxia. J Biol Chem 280: 3493–3499, 2005. doi:10.1074/JBC.M406613200.
Crossref | PubMed | Web of Science | Google Scholar - 298. . Placental growth factor is secreted by the human endometrium and has potential important functions during embryo development and implantation. PLoS One 11:
e0163096 , 2016. doi:10.1371/JOURNAL.PONE.0163096.
Crossref | PubMed | Web of Science | Google Scholar - 299. . Global transcriptomic response of bovine endometrium to blastocyst-stage embryos. Reproduction 158: 223–235, 2019. doi:10.1530/REP-19-0064.
Crossref | PubMed | Web of Science | Google Scholar - 300. . Sperm enter glands of preovulatory bovine endometrial explants and initiate inflammation. Reproduction 159: 181–192, 2020. doi:10.1530/REP-19-0414.
Crossref | PubMed | Web of Science | Google Scholar - 301. . Neurotensin enhances sperm capacitation and acrosome reaction in mice. Biol Reprod 91:
53 , 2014. doi:10.1095/biolreprod.113.112789.
Crossref | PubMed | Web of Science | Google Scholar - 302. . Effect of neurotensin on cultured mouse preimplantation embryos. J Reprod Dev 66: 421–425, 2020. doi:10.1262/jrd.2020-002.
Crossref | PubMed | Web of Science | Google Scholar - 303. . DMBT1 confers mucosal protection in vivo and a deletion variant is associated with Crohn’s disease. Gastroenterology 133: 1499–1509, 2007. doi:10.1053/j.gastro.2007.08.007.
Crossref | PubMed | Web of Science | Google Scholar - 304. . Sperm binding to porcine oviductal cells is mediated by SRCR domains contained in DMBT1. J Cell Biochem 119: 3755–3762, 2018. doi:10.1002/jcb.26614.
Crossref | PubMed | Web of Science | Google Scholar - 305. . Antioxidant properties of a human neuropeptide and its protective effect on free radical-induced DNA damage. J Pept Sci 20: 429–437, 2014. doi:10.1002/psc.2634.
Crossref | PubMed | Web of Science | Google Scholar - 306. . New antimicrobial activity for the catecholamine release-inhibitory peptide from chromogranin A. Cell Mol Life Sci 62: 377–385, 2005. doi:10.1007/s00018-004-4461-9.
Crossref | PubMed | Web of Science | Google Scholar - 307. . CYR61 stimulates human skin fibroblast migration through integrin αvβ5 and enhances mitogenesis through integrin αvβ3, independent of its carboxyl-terminal domain. J Biol Chem 276: 21943–21950, 2001. doi:10.1074/jbc.M100978200.
Crossref | PubMed | Web of Science | Google Scholar - 308. . CYR61 (CCN1) is essential for placental development and vascular integrity. Mol Cell Biol 22: 8709–8720, 2002. doi:10.1128/mcb.22.24.8709-8720.2002.
Crossref | PubMed | Web of Science | Google Scholar - 309. . Decreased expression of the angiogenic regulators CYR61 (CCN1) and NOV (CCN3) in human placenta is associated with pre-eclampsia. Mol Hum Reprod 12: 389–399, 2006. doi:10.1093/molehr/gal044.
Crossref | PubMed | Web of Science | Google Scholar - 310. . A study of the early stages of implantation in mice. J Reprod Fertil 13: 259–267, 1967. doi:10.1530/jrf.0.0130259.
Crossref | PubMed | Google Scholar - 311. . A morphological analysis of the early implantation stages in the rat. Am J Anat 120: 185–225, 1967. doi:10.1002/aja.1001200202.
Crossref | Google Scholar - 312. . The cell biology of human implantation. Placenta 17: 269–275, 1996. doi:10.1016/s0143-4004(96)90050-8.
Crossref | PubMed | Web of Science | Google Scholar - 313. . The placentome of the cow. Am J Vet Res 9:
125 , 1948.
Web of Science | Google Scholar - 314. . The interval between the time of ovulation and attachment of the bovine embryo. J Anim Sci 10: 993–1005, 1951. doi:10.2527/jas1951.104993x.
Crossref | Web of Science | Google Scholar - 315. . Studies on morphogenesis of uterine horn, especially with uterine caruncle in Japanese native cattle. Jpn J Zootech Sci 35: 92–100, 1964. doi:10.2508/chikusan.35.tokubetu_92.
Crossref | Google Scholar - 316. . Development of the caruncular and intercaruncular regions in the bovine endometrium. Biol Reprod 30: 763–774, 1984. doi:10.1095/biolreprod30.3.763.
Crossref | PubMed | Web of Science | Google Scholar - 317. . Development of bovine blastocyst with a note on implantation. Anat Rec 113: 143–161, 1952. doi:10.1002/ar.1091130203.
Crossref | PubMed | Google Scholar