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Immunoendocrine Functions of Trophoblast Interferons (IFN-τ or TP-1 or Trophoblastins) in the Maternal Recognition of Pregnancy

  • Chapter
Endocrinology of Embryo-Endometrium Interactions

Abstract

It has been recently shown in ruminants that interferons are constitutively produced by the trophoblast during the critical peri-implantation period. Ruminant trophoblast IFN gene sequences provide evidence that these IFNs recently called IFN-τ constitute a distinct family of other interferons of type I (α, β, ω). Embryonic IFNs are not confined in ruminants but have been found in other species though their structural characteristics can be different. In culture of ovine endometrial cells, ovine Trophoblast Protein (oTP) is able to inhibit the biosynthesis of prostaglandin F, even when stimulated by oxytocin. In vivo, recombinant oTP (r.oTP) inhibits the cyclic luteolysis of recipient ewes for 1 month or more as do trophoblast homogenates or trophoblastic vesicles and better than bovine recombinant IFNα. Furthermore, r.oTP is able to block the cyclic PGF pulsatility thus showing the key role played by the ruminant trophoblastins in the mechanisms of maternal recognition of pregnancy. Besides displaying a paracrine antiluteolytic function, r.oTP exhibits immunoregulatory activities similar to the natural oTP isoforms. It blocks phytohemagglutinin A (PHA) driven lymphocyte proliferation on murine, human and ovine lymphocytes. oTP is acting especially on human, murine and ovine CD4 T cells (helper lymphocytes). It does not block in mice interleukin-2 dependent cell proliferation when assayed on CTL-L2 cell line (CD+ 8) but inhibits in sheep PHA driven CD8 T lymphocyte proliferation. oTP and r.oTP were found to be immunosuppressive on a murine and a human Mixed Lymphocyte Reaction which is usually considered as a maternal allo-recognition of paternal antigens of the conceptus. In vivo, r.oTP also exhibits immunosuppressive activity in mice on a Graft Versus Host (Popliteal Lymph Nodes) assay. Finally, r.oTP strongly inhibits immunological embryonic abortion in the usual model of CBA/J × DBA/2 mice if given early in pregnancy, at days 5 and 8 but not later (days 8 and 10). In conclusion, we propose a working hypothesis of the immunoendocrine function of ovine trophoblastin in the mechanisms of embryo immunotolerance.

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References

  • Abdollahi, A., Lord, K.A., Hoffman-Liebermann, B., and Liebermann, D.A., 1991, Interferon regulatory factor-1 is a myeloid differentiation primary response gene induced by interleukin-6 and leukemia inhibitory factor-role in growth inhibition, Cell Growth Diff. 2:401–407

    PubMed  CAS  Google Scholar 

  • Armstrong, D.T., and Chaouat, G., 1989, Effects of lymphokines and immune complexes on murine placental cell growth in vitro, Biol. Reprod. 40:466–474.

    Article  PubMed  CAS  Google Scholar 

  • Assal-Meliani, A., Charpigny, G., Martal, J., and Chaouat, G., 1991, Natural and recombinant oTP1 trophoblastin has immunoregulatory activities. Ann. Meeting of the Intern. Society for Interferon Research, Nice, J. IFN Res. 11, Suppl. 1:S102.

    Google Scholar 

  • Assal-Meliani, A., Charpigny, G., Reinaud, P., Martal, J., and Chaouat, G., 1993, Recombinant ovine trophoblastin inhibits ovine and murine lymphocyte proliferation. J. Reprod. Immunol. (in press).

    Google Scholar 

  • Assal-Meliani, A., Kinsky, R., Charpigny, G., Reinaud, P., Martal, J., Chaouat, G., 1992, Recombinant ovine trophoblastin inhibits ovine and murine lymphocyte proliferation and popliteal lymph node (GVH) assays, 5th International congress of reproductive immunology, Rome (Italie): 73.

    Google Scholar 

  • Athanassakis, I., Bleackley, R.C., Paetkau, V., Guilbert, L., Barr, P.J., Wegmann, T.G., 1987, The immunostimulatory effect of T cells and T cell lymphokines on murine fetally derived-placental cells, J. Immunol. 138:37–44.

    PubMed  CAS  Google Scholar 

  • Baker, D.J., and Nieder, G.L., 1990, Interferon activity is not detected in blastocyst secretions and does not induce decidualization in mice, J. Reprod. Fertil. 88:307–313.

    Article  PubMed  CAS  Google Scholar 

  • Barlow, D.P., Randle, B J., and Burke, D.C., 1984. Interferon synthesis in the early post-implantation mouse embryo, Differentiation 27:229–235.

    Article  PubMed  CAS  Google Scholar 

  • Baumbach, G.A., Duby, R.T., and Godkin, J.D., 1990, N-glycosylated and unglycosylated forms of caprine trophoblast protein-1 are secreted by peri-implantation goat conceptuses, Biochem. Biophys. Res. Comm. 172:16–21.

    Article  PubMed  CAS  Google Scholar 

  • Bazer, F.W., 1989, Establishment of pregnancy in sheep and pigs, Reprod. Fertil. Dev. 1:237–242.

    Article  PubMed  CAS  Google Scholar 

  • Bazer, F.W., and Thatcher, W.W., 1977, Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F-2α by the uterine endometrium, Prostaglandins 14:397–400.

    Article  PubMed  CAS  Google Scholar 

  • Bocci, V., Paulescu, L., and Ricci, M.G., 1985. The physiological interferon response, IV: Production of interferon by the perfused human placenta at term, Proc. Soc. Exp. Biol. Med. 180:137–143.

    PubMed  CAS  Google Scholar 

  • Cerutti, M., Hue, D., Charlier, M., L’Haridon, R., Pernollet, J.C., Devauchelle, G., and Gaye, P., 1991, Expression of a biologically active ovine trophoblastic interferon (oTP) using a Baculovirus expression system, Bioch. Biophys. Res. Commun. 181:443–448.

    Article  CAS  Google Scholar 

  • Chaouat, G., 1978, Aspects immunologiques de l’ovo-implantation, in: “L’implantation de l’oeuf, pp. 231–238, F. du Mesnil du Buisson, A. Psychoyos, and K. Thomas, eds, Masson, Paris.

    Google Scholar 

  • Chaouat, G., Assal-Meliani, A., Martal, J., Raghupathy, R., Hui, L., and Wegmann, T.G., 1993, IL10 corrects resorptions in the CBA/J × DBA/2 murine abortion model and is induceable by tau interferons, (in press).

    Google Scholar 

  • Chaouat, G., Menu, E., Clark, D.A., Dy, M., Minkowski, M., and Wegmann, T.G., 1990a, Control of fetal survival in CBA × DBA/2 mice by lymphokine therapy, J. Reprod. Fert. 89:447–458.

    Article  CAS  Google Scholar 

  • Chaouat, G., Menu, E., and Kinsky, R., 1990b. Animal models of the fetal allograft. Immun. All. Clin. North America, 10, 13–25.

    Google Scholar 

  • Chaouat, G., Menu, E., Lelaidier, C., Delage, G., Moreau, J.F., Assal-Meliani, A., Djian, V., Ropert, S., David, F., Wegmann, T.G., Hui, L., Raghupathy, R., Martal, J., and Frydman, R., 1993, Cytokines and immuno endocrine network as determinants of early pregnancy success or failure and in parturition, VIIIth World congress on in vitro fertilization and alternate assisted reproduction, Kyoto, Japan.

    Google Scholar 

  • Chaouat, G., Menu, E., Szekeres-Bartho, J., Rebut-Bonneton, C., Bustany, P., Kinski, R., Dy, M., Minkowski, M., Clark, D.A., and Wegmann, T.G., 1991, Immunological and endocrinological factors that contribute to successful pregnancy, in: “Molecular and cellular immunobiology of the maternal fetal interface”, T.G. Wegmann, T.J. Gill, and E. Nisbet-Brown, eds, Oxford University Press, New York.

    Google Scholar 

  • Chard, T., 1991, Interferon-α is a reproductive hormone, J. Endocr. 131:337–338.

    Article  PubMed  CAS  Google Scholar 

  • Chard, T., Craig, P.H., Menabaway, M., and Lee, C., 1986, Alpha interferon in human pregnancy, Br. J. Obstet. Gynaecol. 93:1145–1149.

    Article  PubMed  CAS  Google Scholar 

  • Chard, T., and Iles, R., 1992, Interferon as a fetoplacental signal in pregnancy, Troph. Res. 6:55–72, in: “Placental signals autocrine and paracrine control of pregnancy”, L. Cédard and A. Firth, eds, University of Rochester Press.

    Google Scholar 

  • Charlier, M., Hue, D., Boisnard, M., Martal, J., and Gaye, P., 1991, Cloning and structural analysis of two distinct families of ovine interferon-α genes encoding functional class II and trophoblast (oTP) a-interferons, Mol. Cell. Endocrinol. 86:161–171.

    Article  Google Scholar 

  • Charlier, M., Hue, D., Martal, J., and Gaye, P., 1989, Cloning and expression of cDNA encoding ovine trophoblastin: Its identity with a class-II alpha interferon, Gene 77:341–348.

    Article  PubMed  CAS  Google Scholar 

  • Charlier, M., L’Haridon, R., Boisnard, M., Martal, J., and Gaye, P., 1993, Cloning and structural analysis of four genes encoding interferon omega in rabbit, J. IFN Res. (in press).

    Google Scholar 

  • Charpigny, G., Reinaud, P., Huet, J.C., Guillomot, M., Charlier, M., Pernollet, J.C., and Martal, J., 1988a, High homology between a trophoblastic protein (trophoblastin) isolated from ovine embryo and interferons, FEBS Lett. 228:12–16.

    Article  PubMed  CAS  Google Scholar 

  • Charpigny, G., Reinaud, P., La Bonnardiere, C., Guillomot, M., Huet, J.C., Pernolet, J.C., and Martal, J., 1988b, Evidence for antiviral properties of three purified isoforms of oTPB. In Proc. Int. Workshop on maternal recognition of pregnancy and maintenance of the corpus luteum, Jerusalem (Israël) (abstr.):72.

    Google Scholar 

  • Charpigny, G., Reinaud, P., Tamby, J.P., Martal, J., 1991, Ovine embryonic interferon blocks prostaglandin synthesis induced by activators of protein kinase C: evidence for a dual inhibitory mechanisms. Ann. meeting of the intern, J. IFN Res. 11, suppl. 1: Abstr. S166.

    Google Scholar 

  • Chene, N., Hamrouche, N., Puissant, C., Grenouillet, C., and Martal, J., 1991, Distribution of growth factors (IGF-I, IGF-II, TGF beta 1 and TGF beta 2) mRNAs in the ovine conceptus during periimplantation, J. Reprod. Fert. suppl. serie 8:abstr. 107.

    Google Scholar 

  • Clark, D.A., Head, J.R., Drake, B.L., Fulop, G., Brierley, J., Manuel, J., Banwatt, D., and Chaouat, G., 1991, Role of a factor related to transforming growth factor Beta-2 in successful pregnancy, in: “Molecular and cellular immunobiology of the maternal fetal interface”, pp. 294–311, T.G. Wegmann, T.J. Gill and E. Nisbet-Brown, eds, Oxford University Press, New-York.

    Google Scholar 

  • Cross, J.C., Farin, C.E., Sharif, S.F., and Roberts, R.M., 1990, Characterization of the antiviral activity constitutively produced by murine conceptuses: Absence of placental mRNAs for interferon alpha and beta, Mol. Reprod. Dev. 26:122–128.

    Article  PubMed  CAS  Google Scholar 

  • Cross, J.C., and Roberts, R.M., 1989, Porcine conceptuses secrete an interferon during the pre-attachment period of early pregnancy, Biol. Reprod. 40, 1109–1118.

    Article  PubMed  CAS  Google Scholar 

  • Croy, B.A., and Chapeau, C., 1990, Evaluation of the pregnancy immunotrophism hypothesis by assessment of the reproductive performance of young adult mice of genotype scid/scid bg/bg, J. Reprod. Fert. 88:231–239.

    Article  CAS  Google Scholar 

  • Croy, B.A., and Rossant, J., 1987, Mouse embryonic cells become susceptible to CTL mediated lysis after midgestation, Cell Immunol. 104:355–365.

    Article  PubMed  CAS  Google Scholar 

  • Degryse, E., Dietrich, M., Nguyen, M., Achstetter, T., Charlier, M., Charpigny, G., Gaye, P., and Martal, J., 1992, Addition of a dipeptide spacer significantly improves secretion of ovine trophoblast interferon in yeast, Gene 118:47–53.

    Article  PubMed  CAS  Google Scholar 

  • De Mayer, E., and De Mayer-Guignard, J., 1988, Interferon and other regulatory cytokines, Wyleg, New York.

    Google Scholar 

  • Drake, B.L., and Head, J.R., 1988, Murine trophoblast cells are susceptible to Lymphokine Activated Killer (LAK) cell lysis, Am. J. Reprod. Immunol. 16:114.

    Google Scholar 

  • Drake, B.L., and Head, J.R., 1989, Murine trophoblast cells can be killed by allospecific cytotoxic T lymphocytes generated in Gibco OPTI MEM medium, J. Reprod. Immunol. 15:71–77.

    Article  PubMed  CAS  Google Scholar 

  • Duc-Goiran, P., Robert-Galliot, B., Lopez, J., and Chany, C., 1985. Unusual apparently constitutive interferons and antagonists in human placental blood, Proc. Natl. Acad. Sci. USA 82:5010–5014.

    Article  PubMed  CAS  Google Scholar 

  • Farin, C.E., Imakawa, K., and Roberts, R.M., 1989, In situ localization of mRNA for the interferon, ovine trophoblast protein-1, during early embryonic development of the sheep, Mol. Endocr. 3:1099–1107.

    Article  CAS  Google Scholar 

  • Fillion, C., Chaouat, G., Charpigny, G., Reinaud, P., and Martal, J., 1990, Immunoregulatory effects of trophoblastin (oTP): all 5 isoforms are immunosuppressive of PHA driven lymphocyte proliferation, J. Reprod. Immunol. 19:237–249.

    Article  Google Scholar 

  • Fincher, K.B., Bazer, F.W., Hansen, PJ., Thatcher, W.W., and Roberts, R.M., 1986, Ovine conceptus secretory proteins suppress induction of uterine prostaglandin F-2α release by oestradiol and oxytocin, J. Reprod. Fert. 76:425–433.

    Article  CAS  Google Scholar 

  • Flint, A.P.F., Parkinson, T.J., Stewart, H.J., Vallet, J.L., and Lamming, G.E., 1991, Molecular biology of trophoblast interferons and studies of their effects in vivo. J. Reprod. Fert. suppl. 43:13–25.

    CAS  Google Scholar 

  • Flint, A.P.F., and Sheldrick, E.L., 1986, Ovarian oxytocin and the maternal recognition of pregnancy, J. Reprod. Fert. 76:831–839.

    Article  CAS  Google Scholar 

  • Flint, A.P.F., Sheldrick, E.L., McCann, T.J., and Jones, D.S.C., 1990, Luteal oxytocin: characteristics and control of synchronous episodes of oxytocin and PGF secretion at luteolytis in ruminants, Dom. Anim. Endocr. 7:111–124.

    Article  CAS  Google Scholar 

  • Fowler, A.K., Reed, C.D., and Giron, D.J., 1980, Identification of an interferon in murine placentas, Nature 286:266–267.

    Article  PubMed  CAS  Google Scholar 

  • Fry, R.C., Batt, P.A., Fairclough, R.J., and Parr, R.A., 1992, Human leukemia inhibitory factor improves the viability of cultured ovine embryos, Biol. Reprod. 46:470–474.

    Article  PubMed  CAS  Google Scholar 

  • Godkin, J.D., Bazer, F.W., Moffatt, J., Sessions, F., and Roberts, R.M., 1982, Purification and properties of a major, low component weight protein released by the trophoblast of sheep blastocysts at day 13–21, J. Reprod. Fert. 65:141–150.

    Article  CAS  Google Scholar 

  • Godkin, J.D., Bazer, F.W., and Roberts, R.M., 1984a, Ovine trophoblast protein 1, an early secreted blastocyst protein binds specifically to uterine endometrium and affects protein synthesis, Endocrinology 114:120–130.

    Article  PubMed  CAS  Google Scholar 

  • Godkin, J.D., Bazer, F.W., Thatcher, W.W., and Roberts, M., 1984b, Proteins released by cultured day 15–16 conceptuses prolong luteal maintenance when introduced into uterine lumen of cyclic ewes, J. Reprod. Fert. 71:57–64.

    Article  CAS  Google Scholar 

  • Gross, T.S., Thatcher, W.W., Hansen, P.J., Johnson, J.W., and Helmer, S.D., 1988, Presence of an intracellular endometrial inhibitor of prostaglandin synthesis during early pregnancy in the cow, Prostaglandins 35:359–378.

    Article  PubMed  CAS  Google Scholar 

  • Guillomot, M., Michel, C., Gaye, P., Charlier, M., Trojan, J., and Martal, J., 1990, Cellular localization of an embryonic interferon, ovine trophoblastin and its m-RNA in sheep embryos during early pregnancy, Biol. Cell. 68:205–211.

    Article  PubMed  CAS  Google Scholar 

  • Hansen, T.R., Imakawa, K., Polites, H.G., Marotti, K.R., Anthony, R.V., and Roberts, R.M., 1988, Interferon RNA of embryonic origin is expressed transciently during early pregnancy in the ewe, J. Biol. Chem. 263:12801–12804.

    PubMed  CAS  Google Scholar 

  • Hansen, T.R., Kazemi, M., Keisler, D.H., Malathy, P.V., Imakawa, K., Roberts, R.M., 1989, Complex binding of the embryonic interferon, ovine trophoblast protein-1, to endometrial receptors, J. Interferon Res. 9:215–225.

    Article  PubMed  CAS  Google Scholar 

  • Helmer, S.D., Hansen, P.J., Anthony, R.V., Thatcher, W.W., Bazer, F.W., and Roberts, R.M., 1987, Identification of bovine trophoblast protein-1, a secretory protein immunologically related to ovine trophoblast protein-1, J. Reprod. Fert. 79:83–91.

    Article  CAS  Google Scholar 

  • Hernandez-Ledezma, J.J., Sikes, J.D., Murphy, C.N., Watson, A.J., Schultz, G.A., and Roberts, R.M., 1992, Expression of bovine trophoblast interferon in conceptuses derived by in vitro techniques, Biol. Reprod. 47:374–380.

    Article  PubMed  CAS  Google Scholar 

  • Heyman, Y., Camous, S., Fevre, J., Meziou, W., and Martal, J., 1984, Maintenance of corpus luteum after uterine transfer of trophoblastic vesicles in cyclic cows and ewes, J. Reprod. Fert. 70:533–540.

    Article  CAS  Google Scholar 

  • Hooper, S.B., Watkins, W.B., and Thorburn, G.D., 1986, Oxytocin, oxytocin-associated neurophysin, and prostaglandin F-2α concentrations in the utero-ovarian vein of pregnant and nonpregnant sheep, Endocrinology 119:2590–2597.

    Article  PubMed  CAS  Google Scholar 

  • Imakawa, K., Anthony, R.V., Kazemi, M., Marotti, K.R., Polites, H.G., and Roberts, R.M., 1987, Interferon-like sequence of ovine trophoblast protein secreted by embryonic trophectoderm, Nature 330:377–379.

    Article  PubMed  CAS  Google Scholar 

  • Imakawa, K., Hansen, T.R., Malathy, P.C., Anthony, R.V., Polites, H.G., Marotti, K.R., and Roberts, R.M., 1989, Molecular cloning and characterization of complementary deoxyribonucleic acids corresponding to bovine trophoblast protein-1 and bovine interferon-αII, Molec. Endocrinol. 3:127–139.

    Article  CAS  Google Scholar 

  • Isaacs, A., and Lindenmann, J., 1957, Virus interference. I. The interferon. Proc. Royal. Soc. Lond. B 147:258–267.

    Article  CAS  Google Scholar 

  • Khan, N.U.D., Pulford, K.A.F., Farquharson, M.A., Howatson, A., Stewart, C., Jackson, R., McNicol, A.M., and Foulis, A.K., 1989, The distribution of immunoreactive interferon-alpha in normal tissues, Immunology 66:201–206.

    PubMed  CAS  Google Scholar 

  • Klemann, S.W., Imakawa, K., and Roberts, R.M., 1990, Sequence variability among ovine trophoblast interferon cDNA, Nucleic Acids Res. 18:22.

    Article  Google Scholar 

  • Knickerbocker, J.J., Thatcher, W.W., Bazer, F.W., Barron, D.H., and Roberts, R.M., 1986, Inhibition of uterine prostaglandin F2α production by bovine conceptus secretory proteins, Prostaglandins 31:777–793.

    Article  PubMed  CAS  Google Scholar 

  • Ko, Y., Lee, C.Y., Ott, T.L., Davis, M.A., Simmen, R.C.M., Bazer, F.W., Simmen, F.A., 1991, Insulin-like growth factors in sheep uterine fluids: concentrations and relationship to ovine Trophoblast Protein-1 production during early pregnancy, Biol. Reprod. 45:135–142.

    Article  PubMed  CAS  Google Scholar 

  • La Bonnardiere, C., and Martal, J., 1991, Les interférons embryonnaires, Le Point vétérinaire 23: 55–61.

    Google Scholar 

  • La Bonnardiere, C., Martinat-Botte, F., Terqui, M., Lefevre, F., Zouari, K., Martal, J., and Bazer, F.W., 1991, Production of two species of interferon by Large White and Meishan pig conceptuses during the peri-attachment period, J. Reprod. Fert. 91:469–478.

    Article  Google Scholar 

  • Lebon, P., Daffos, F., Checoury, A., Grangeot-Keros, L., Forestier, F., and Toublanc, J.E., 1985, Presence of an acid-labile alpha-interferon in sera from fetuses and children with congenital rubella, J. Clin. Microbiol. 21:775–778.

    PubMed  CAS  Google Scholar 

  • Lebon, P., Girard, S., Thepot, F., and Chany, C., 1982. The presence of α-interferon in human amniotic fluid, J. Gen. Virol. 59:393–396.

    Article  PubMed  CAS  Google Scholar 

  • Lefevre, F., 1989, Le système interféron: structure, biologie, applications, Ann. Rech. Vét. 20:17–38.

    PubMed  CAS  Google Scholar 

  • Lefevre, F., Boulay, V., and La Bonnardiere, C., 1991, A new type one interferon with unusual regulatory elements. J. IFN Res. 11, Suppl. 1:Abstr.14.

    Google Scholar 

  • Lefevre, F., Martinat-Botte, F., Guillomot, M., Zouari, K., Charley, B., and La Bonnardiere, C., 1990, Interferon-gamma gene and protein are spontaneously expressed by the trophectoderm early in gestation. Eur. J. Immunol. 20:2485–2490.

    Article  PubMed  CAS  Google Scholar 

  • Martal, J., Assal, A., Assal, E., Charlier, M., Chene, N., Charpigny, G., Guillomot, M., and Chaouat, G., 1991a, Characterization, antiluteolytic and immunosuppressive effects of ovine trophoblastin (oTP, α-interferon of class “III”), in: “Cellular and Molecular Biology of the materno-fetal relationship”, G. Chaouat, and J. Mowbray, eds, Colloque INSERM/John Libbey Eurotext Ltd, 212:217-324.

    Google Scholar 

  • Martal, J., Assal, N.E., Assal, A., Charpigny, G., Reinaud, P., and Chaouat, G., 1991b, Involvment of trophoblast interferons in the control progesterone-dependant uterine environment and prevention of rejection of the conceptus as an allograft, J. Reprod. Fert. abstr. series No. 8.

    Google Scholar 

  • Martal, J., Charlier, M., Camous, S., Fevre, J., and Heyman, Y., 1984, Origin of embryonic signals allowing the establishment of pregnancy corpus luteum in ruminants, 10th Int. Congress on Animal Reproduction and Artificial Insemination, Urbana-Champaign, USA, 111, 509:3.

    Google Scholar 

  • Martal, J., Charlier, M., Charpigny, G., Camous, S., Chene, N., Reinaud, P., Sade, S., and Guillomot, M., 1987, Interference of trophoblastin in ruminant embryonic mortality. A review, Livest. Prod. Sci. 17:193–210.

    Article  CAS  Google Scholar 

  • Martal, J., Charpigny, G., Reinaud, P., Huet, J.C., Guillomot, M., Zouari, K., Pernollet, J.C., and La Bonnardiere, C., 1988, Embryonic signals and corpus luteum: Why three isoforms of trophoblastin can be considered as interferons α of class II? J. Reprod. Fert. 2: Abstr. 11.

    Google Scholar 

  • Martal, J. and Chene, N., 1992, Functions of embryonic interferons and of the main serum proteins specific for pregnancy, Troph. Res. 6:73–122, in: “Placental signals autocrine and paracrine control of pregnancy”, L. Cédard and A. Firth, eds, University of Rochester Press.

    Google Scholar 

  • Martal, J., Degryse, E., Charpigny, G., Assal, N., Reinaud, P., Charlier, M., Gaye, P., and Lecocq, J.P., 1990, Evidence for extended maintenance of the corpus luteum by uterine infusion of a recombinant trophoblast α-interferon (trophoblastin) in sheep, J. Endocrinol. 127:R5–R8.

    Article  PubMed  CAS  Google Scholar 

  • Martal, J., Lacroix, M.C., Loudes, C., Saunier, M., and Wintenberger-Torres, S., 1979, Trophoblastin, an antiluteolytic protein present in early pregnancy in sheep. J. Reprod. Fert. 56:63–73.

    Article  CAS  Google Scholar 

  • Mathialagan, N., Bixby, J.A., and Roberts, R.M., 1992, Expression of interleukin-6 in porcine, ovine, and bovine preimplantation conceptuses, Mol. Reprod. Dev. 32:324–330.

    Article  PubMed  CAS  Google Scholar 

  • McCracken, J.A., 1980, Hormone receptor control of prostaglandin F-2α secretion by the ovine uterus, Adv. Prostaglandin Thromboxane Res. 8:1329–1344.

    PubMed  CAS  Google Scholar 

  • McCracken, J.A., Carlson, J.C., Glew, M.E., Goding, J.R., Baird, D.T., Green, K., and Samuelsson, B., 1972, Prostaglandin F-2α identified as a luteolytic hormone in sheep. Nature 238:129–134.

    Article  CAS  Google Scholar 

  • Mc Cracken, J.A., Schramm, W., Barcikowski, B., and Wilson, L., 1981, Identification of PGF-2α as a uterine luteolytic hormone and the hormonal control of its synthesis, Acta. Vet. Scand. suppl. 77:71–88.

    PubMed  CAS  Google Scholar 

  • Mirando, M.A., Harney, J.P., Beers, S., Pontzer, C.H., Torres, B.A., Johnson, H.M., and Bazer, F.W., 1990a, Onset of secretion of proteins with antiviral activity by pig conceptuses, J. Reprod. Fert. 88:197–203.

    Article  CAS  Google Scholar 

  • Mirando, M.A., Ott, T.L., Vallet, J.L., Davis, M., and Bazer, F.W., 1990b, Oxytocin-stimulated inositol phosphate turnover in endometrium of ewes is influenced by stage of the estrus cycle, pregnancy and intrauterine infusion of ovine secretory proteins, Biol. Reprod. 42:98–105.

    Article  PubMed  CAS  Google Scholar 

  • Moor, R.M., and Rowson, L.E.A., 1966, The corpus luteum of the sheep: functional relationship between the embryo and the corpus luteum, J. Endocr. 34:233–239.

    Article  PubMed  CAS  Google Scholar 

  • Nephew, K.P., McClure, K.E., Day, M.L., Xie, S., Roberts, R.M., and Pope, W.F., 1990, Effects of intra-muscular administration of recombinant bovine interferon-AlphaI 1 during the period of maternal recognition of pregnancy, J. anim. Sci. 68:2766–2770.

    PubMed  CAS  Google Scholar 

  • Nephew, K.P., Whaley, A.E., Christenson, R.K., and Imakawa, K., 1993, Differential expression of distinct mRNAs for ovine Trophoblast Protein-1 and related sheep type I interferons, Biol. Reprod. 48:768–778.

    Article  PubMed  CAS  Google Scholar 

  • Nett, T.M., Staigmiller, R.B., Akbar, A.M., Diekman, M.A., Ellinwood, W.E., and Niswender, G.D., 1976, Secretion of prostaglandin F-2α in cycling and pregnant ewes, J. Anim. Sci. 42:876–880.

    PubMed  CAS  Google Scholar 

  • Parkinson, T.J., Lamming, G.E., Flint, A.P.F., and Jenner, L.J., 1992, Administration of recombinant bovine interferon-αI at the time of maternal recognition of pregnancy inhibits prostaglandin F secretion and causes luteal maintenance in cyclic ewes, J. Reprod. Fert. 94:489–500.

    Article  CAS  Google Scholar 

  • Perez, A., Riego, E., Martinez, R., Castro, F.O., Lleonart, R., and De La Fuente, J., 1991, Presence of mRNAs homologous to IFN-α, but not to IFN-β in preimplantation mouse embryos, J. IFN Res. 11, suppl. l:Abst. 62.

    Google Scholar 

  • Plante, C., Hansen, P.J., and Thatcher, W.W., 1988. Prolongation of luteal lifespan in cows by intrauterine infusion of recombinant bovine alpha-interferon. Endocrinology 122:2342–2344.

    Article  PubMed  CAS  Google Scholar 

  • Pollard, J.W., Bartocci, A., Arceci, R., Orlofsky, A., Ladner, M.B., and Stanley, E.R., 1987, Nature 330:484–486.

    Article  PubMed  CAS  Google Scholar 

  • Pontzer, C.H., Torres, R.A., Vallet, J.L., Bazer, F.W., and Johnson, H.M., 1988, Antiviral activity of the pregnancy recognition hormone ovine trophoblast protein-1, Bioch. Biophys. Res. Commun. 152:801–807.

    Article  CAS  Google Scholar 

  • Roberts, R.M., Cross, J.C., and Leaman, D.W., 1992b, Interferons as hormones of pregnancy, Endocr. Rev. 13:432–452.

    PubMed  CAS  Google Scholar 

  • Roberts, R.M., Klemann, S.W., Leaman, D.W., Bixby, J.A., Cross, J.C., Farin, C.E.E, Imakawa, K., and Hansen, T.R., 1991, The polypeptides and genes for ovine and bovine trophoblast protein-1, J. Reprod. Fertil. suppl. 43:3–12.

    PubMed  CAS  Google Scholar 

  • Roberts, R.M., Leaman, D.W., and Cross, J.C., 1992a, Role of interferons in maternal recognition of pregnancy in ruminants, Proc. Soc. Exp. Biol. Med. 200:7–18.

    PubMed  CAS  Google Scholar 

  • Rowson, L.E.A., Moor, R.M., 1967, The influence of embryonic tissue homogenate infused into the uterus on life-span of the corpus luteum in the sheep, J. Reprod. Fert. 13:511–516.

    Article  CAS  Google Scholar 

  • Salamonsen, L.A., Cherny, P.A., and Findlay, J.K., 1991, In vitro studies of the effects of interferons on endometrial metabolism in sheep, J. Reprod. Fert. Suppl. 43:27–38.

    CAS  Google Scholar 

  • Salamonsen, L.A., Stuchbery, S.J., O’Grady, C.M., Godkin, J.D., and Findlay, J.K., 1988, Interferon α mimics effects of ovine trophoblast protein-1 on prostaglandin and protein secretion by ovine endometrial cells in vitro, J. Endocr. 117:R1–R4.

    Article  PubMed  CAS  Google Scholar 

  • Schaule-Francis, T.K., Farin, P.W., Cross, J.C., Keisler, D., and Roberts, R.M., 1991, Effect of injected bovine interferon-αI 1 on oestrous cycle length and pregnancy success in sheep, J. Reprod. Fert. 91:347–356.

    Article  Google Scholar 

  • Schramm, W., Boviard, L., Glew, M.E., Schramm, G., and McCracken, J.A., 1983, Corpus luteum regression induced by ultra-low pulses of prostaglandin F-2α. Prostaglandins 26:347–363.

    Article  PubMed  CAS  Google Scholar 

  • Sheldrick, E.L., and Flint, A.P.F., 1985, Endocrine control of uterine oxytocin receptors in the ewe, J. Reprod. Fert. 77:523–529.

    Article  Google Scholar 

  • Shiozawa, S., Chihara, K., Shiozawa, K., Fujita, T., Ikegami, H., Koyama, S., and Kurimoto, M., 1986, A sensitive radioimmunoassay for alpha-interferon circulating alpha-interferon-like substance in the plasma of healthy individuals and rheumatoid arthritis patients, Clin. Exper. Immunol. 66:77–87.

    CAS  Google Scholar 

  • Shiozawa, S., Shiozawa, K., Shimizu, S., Tanaka, Y., Morimoto, M., Yoshihara, R., and Fujita, T., 1989, Age distribution of circulating alpha-interferon, Experientia 45:764–765.

    Article  PubMed  CAS  Google Scholar 

  • Stewart, H.J., Flint, A.P.F., Lamming, G.E., Mccann, S.H.E., and Parkinson, T.J., 1989, Antiluteolytic effects of blastocyst-secreted interferon investigated in vitro and in vivo in the sheep, J. Reprod. Fert. suppl. 37:127–138.

    CAS  Google Scholar 

  • Stewart, C.L., Kaspar, P., Brulet, L.J., Bhatt, H., Gadi, I., Kontgen, F., Abbondanzo, S.J., 1992, Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor, Nature 359:76–79.

    Article  PubMed  CAS  Google Scholar 

  • Stewart, H.J., McCann, S.H.E., Barker, P.J., Lee, K.E., Lamming, G.E., and Flint, A.P.F., 1987, Interferon sequence homology and receptor binding activity of ovine trophoblast antiluteolytic protein, J. Endocr. 115:R13–R15.

    Article  PubMed  CAS  Google Scholar 

  • Stewart, H.J., McCann, S.H.E., and Flint, A.P.F., 1990, Structure of an interferon-αII gene expressed in the bovine conceptus early in gestation, J. Mol. Endocrinol. 2:65–70.

    Article  Google Scholar 

  • Stewart, Hj., Mc Cann, S.H.E., Northrop, A.J., Lamming, G.E., and Flint, A.P.F., 1989b, Sheep antiluteolytic interferon cDNA sequence and analysis of mRNA levels, Mol. Endocrinol. 2:65–70.

    Article  CAS  Google Scholar 

  • Szekeres Bartho, J., Kilar, F., Falkay, G., Csernu, V., Torok, A., and Pacsa, A.S., 1985, Progesterone-treated lymphocytes release a substance inhibiting cytotoxicity and prostaglandin synthesis. Am. J. Reprod. Immunol. 9:15–24.

    Google Scholar 

  • Taguchi, F., Kajioka, J., and Shimada, N., 1985, Presence of interferon and antibodies to BK virus in amniotic fluid of normal pregnant women, Acta Virol. 29:299–304.

    PubMed  CAS  Google Scholar 

  • Tamby, J.P., Charpigny, G., Reinaud, P., and Martal, J., 1991, Evidence for inhibition of phospholipase A2 activity in endometrium by embryonic interferon (ovine Trophoblast Protein, oTP) in sheep, J. IFN Res. 11, Suppl. l:Abstr. S169.

    Google Scholar 

  • Thatcher, W.W., Hansen, P.J., Gross, T.S., Helmer, S.D., Plante, C., and Bazer, F.W., 1989, Antiluteolytic effects of bovine trophoblast protein-1, J. Reprod. Fert. suppl. 37:91–99.

    CAS  Google Scholar 

  • Thorburn, G.D., Cox, R.I., Currie, W.B., Restall, B.J., and Schneider, W., 1973, Prostaglandin F and progesterone concentrations in the utero-ovarian venous plasma of the ewe during the oestrous cycle and early pregnancy, J. Reprod. Fert. suppl. 18:151–158.

    CAS  Google Scholar 

  • Vallet, J.L., and Bazer, F.W., 1989, Effect of ovine trophoblast protein-I, oestrogen and progesterone on oxytocin-induced phosphatidylinositol turnover in endometrium of sheep, J. Reprod. Fert. 87:755–761.

    Article  CAS  Google Scholar 

  • Vallet, J.L., Bazer, F.W., Fliss, M.F.V., and Thatcher, W.W., 1988, Effect of ovine conceptus secretory proteins and purified ovine trophoblast protein-1 on interoestrous interval and plasma concentrations of prostaglandins F2α and E and of 13,14-dihydro-15-prostaglandin F2α in cyclic ewes, J. Reprod. Fert. 84:493–504.

    Article  CAS  Google Scholar 

  • Vallet, J.L., and Lamming, G.E., 1991, Ovine conceptus secretory proteins and bovine recombinant interferon αI 1 decrease endometrial oxytocin receptor concentration in cyclic and progesterone-treated ovariectomized ewes, J. Endocr. 131:475–482.

    Article  PubMed  CAS  Google Scholar 

  • Vallet, J.L., Lamming, G.E, and Batten, M., 1990, Control of endometrial oxytocin receptor and uterine response to oxytocin by progesterone and oestradiol in the ewe, J. Reprod. Fert. 90:625–634.

    Article  CAS  Google Scholar 

  • Warner, S J.C., and Libby, P., 1989, Human vascular smooth muscle. Target for and source of tumor necrosis factor, J. Immunol. 142:100–110.

    PubMed  CAS  Google Scholar 

  • Whaley, A.E., Carroll, R.S., and Imakawa, K., 1991, Cloning and analysis of a gene encoding ovine interferon α-II, Gene 106:281–282.

    Article  PubMed  CAS  Google Scholar 

  • Whaley, A.E., Carroll, R.S., Nephew, K.P., Imakawa, K., 1991, Molecular cloning of unique interferons from human placenta, J. IFN Res. 11, suppl. 1:Abstr. 69.

    Google Scholar 

  • Wegmann, T.G., 1987, Placental immunotrophism: maternal T cells enhance placental growth and function, Am. J. Reprod. Immunol. 15:67–70.

    CAS  Google Scholar 

  • Wegmann, T.G., Athanassakis, I., Guilbert, L., Branch, D., Dy, M., Menu, E., and Chaouat, G., 1989, The role of M-CSF and GM-CSF in fostering placental growth, fetal growth, and fetal survival, Transplantation Proc. 21.1.P1, 89:566–569.

    Google Scholar 

  • Wegmann, T.G., and Gill, T.J. III, 1991, The molecular and cellular nature of maternal-fetal immune signaling: An overview, in: “Molecular and cellular immunobiology of the maternal fetal interface”, T.G. Wegmann, T.J. Gill, and E. Nisbet-Brown, Oxford University Press, New York.

    Google Scholar 

  • Wegmann, T.G., Lin, H., Guilbert, L., and Mosmann, T.R., 1993, Bidirectional cytokine interactions in the maternal-fetal relationship: successful pregnancy is a TH2 phenomenon, Immun. Today (in press).

    Google Scholar 

  • Weislow, O.S., Kiser, R., Allen, P.T., and Fowler, A.K., 1983, Partial purification of a placental interferon with atypical characteristics, J. Interferon Res. 3:291–298.

    Article  CAS  Google Scholar 

  • Yamada, K., Shimizu, Y., Okamura, K., Kumagai, K., and Suzuki, M., 1985, Study of interferon production during pregnancy in mice and antiviral activity in the placenta, Am. J. Obstet. Gynecol. 153:335–341.

    PubMed  CAS  Google Scholar 

  • Zarco, L., Stabenfeldt, G.H., Quirke, J.F., Kindahl, H., Bradford, G.E., 1988, Modification of prostaglandin F-2α synthesis and release in the ewe during the establishment of pregnancy, J. Reprod. Fert. 83:527–536.

    Article  CAS  Google Scholar 

  • Zhang, J., Weston, P.G., Hixon, J.E., 1992, Role of progesterone and oestradiol in the regulation of uterine oxytocin receptors in ewes, J. Reprod. Fert. 94:395–404.

    Article  CAS  Google Scholar 

  • Zouari, K., Bezard, J., Reinaud, P., Guillomot, M., Palmer, E., and Martal, J., 1991a, Evidence for the presence of equine trophoblastic interferons during early pregnancy, J. IFN Res. 11, suppl. 1: Abstr. S134.

    Google Scholar 

  • Zouari, K., Reinaud, P., La Bonnardiere, C., and Martal, J., 1991b, Uterine interferon during early pregnancy and pseudopregnancy in rabbits, J. IFN Res. 11, Suppl. 1: Abstr. S135.

    Google Scholar 

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Martal, J. et al. (1994). Immunoendocrine Functions of Trophoblast Interferons (IFN-τ or TP-1 or Trophoblastins) in the Maternal Recognition of Pregnancy. In: Glasser, S.R., Mulholland, J., Psychoyos, A. (eds) Endocrinology of Embryo-Endometrium Interactions. Reproductive Biology. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1881-5_16

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