Why are Hox genes clustered?

Richard S. Mann,

Richard S. Mann

[email protected]

Department of Biochemistry and Molecular Biophysics, Columbia University College of Physicians and Surgeons, 701 West 168th Street, HHSC 1108, New York, NY 10032

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Richard S. Mann,

Richard S. Mann

[email protected]

Department of Biochemistry and Molecular Biophysics, Columbia University College of Physicians and Surgeons, 701 West 168th Street, HHSC 1108, New York, NY 10032

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First published: 05 February 2005

https://doi.org/10.1002/bies.950190804

Citations: 42

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Abstract

The evolutionarily conserved genomic organization of the Hox genes has been a puzzle ever since it was discovered that their order along the chromosome is similar to the order of their functional domains along the antero-posterior axis. Why has this colinearity been maintained throughout evolution? A close look at regulatory sequences from the mouse Hox clusters^(1,2) suggests that enhancer sharing between adjacent Hox genes may be one reason. Moreover, characterizing the activity of one of these mouse enhancers in Drosophila⁽²⁾ illustrates that despite many similarities, not all Hox clusters are built in the same way.

References

1 Gérard, M., Chen, J. Y., Gronemeyer, H., Chambon, P., Duboule, D. and Zakany, J. (1996). In vivo targeted mutagenesis of a regulatory element required for positioning the Hoxd-11 and Hoxd-10 expression boundaries. Genes Dev. 10, 2326–2334.
10.1101/gad.10.18.2326
CASPubMedWeb of Science®Google Scholar
2 Gould, A., Morrison, A., Sproat, G., White, R. and Krumlauf, R. (1997). Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev. 11, 900–913.
10.1101/gad.11.7.900
CASPubMedWeb of Science®Google Scholar
3 McGinnis, W. and Krumlauf, R. (1992). Homeobox genes and axial patterning. Cell 68, 283–302.
10.1016/0092-8674(92)90471-N
CASPubMedWeb of Science®Google Scholar
4 Krumlauf, R. (1994). Hox genes in Vertebrate Development. Cell 78, 191–201.
10.1016/0092-8674(94)90290-9
CASPubMedWeb of Science®Google Scholar
5 Lewis, E. B. (1978). A gene complex controlling segmentation in Drosophila. Nature 276, 565–570.
10.1038/276565a0
CASPubMedWeb of Science®Google Scholar
6 Bender, W. et al. (1983). Molecular genetics of the Bithorax Complex of Drosophila melanogaster. Science 221, 23–29.
10.1126/science.221.4605.23
CASPubMedWeb of Science®Google Scholar
7 Duboule, D. and Dolle, P. (1989). The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J. 8, 1497–1505.
10.1002/j.1460-2075.1989.tb03534.x
CASPubMedWeb of Science®Google Scholar
8 Graham, A., Papalopulu, N. and Krumlauf, R. (1989). The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell 57, 367–378.
10.1016/0092-8674(89)90912-4
CASPubMedWeb of Science®Google Scholar
9 Duboule, D. and Morata, G. (1994). Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 10, 358–364.
10.1016/0168-9525(94)90132-5
CASPubMedWeb of Science®Google Scholar
10 Struhl, G. (1984). Splitting the bithorax complex of Drosophila. Nature 308, 454–457.
10.1038/308454a0
Web of Science®Google Scholar
11 von Allmen, G. et al. (1996). Splits in fruitfly Hox gene complexes [letter]. Nature 380, 116.
10.1038/380116a0
PubMedWeb of Science®Google Scholar
12 Dolle, P., Izpisua-Belmonte, J. C., Falkenstein, H., Renucci, A. and Duboule, D. (1989). Coordinate expression of the murine Hox-5 complex homoebox-containing genes during limb pattern formation. Nature 342, 767–772.
10.1038/342767a0
CASPubMedWeb of Science®Google Scholar
13 Simeone, A., Acampora, D., Arcioni, L., Andrews, P. W. and Boncinelli, E. (1990). Sequential activation of HOX2 homeobox genes by retinoic acid in human embryonal carcinoma cells. Nature 346, 763–766.
10.1038/346763a0
CASPubMedWeb of Science®Google Scholar
14 Izpisua-Belmonte, J. C., Falkenstein, H., Dolle, P., Renucci, A. and Duboule, D. (1991). Murine genes related to the Drosophila AbdB homeotic genes are sequentially expressed during development of the posterior part of the body. EMBO J. 10, 2279–2289.
10.1002/j.1460-2075.1991.tb07764.x
CASPubMedWeb of Science®Google Scholar
15 Dekker, E.-J., Pannese, M., Houtzager, M., Boncinelli, E. and Durston, A. (1993). Colinearity in the Xenopus laevis Hox-2 complex. Mech. Dev. 40, 3–12.
10.1016/0925-4773(93)90083-A
CASPubMedWeb of Science®Google Scholar
16 van der Hoeven, F., Zakany, J. and Duboule, D. (1996). Gene transpositions in the HoxD complex reveal a hierarchy of regulatory controls. Cell 85, 1025–1035.
10.1016/S0092-8674(00)81303-3
CASPubMedWeb of Science®Google Scholar
17 Simeone, A., Pannese, M., Acampora, D., D'Esposito, M. and Boncinelli, E. (1988). At least three human homeoboxes on chromosome 12 belong to the same transcription unit. Nucleic Acids Res. 16, 5379–5390.
10.1093/nar/16.12.5379
CASPubMedWeb of Science®Google Scholar
18 Gyurkovics, H., Gausz, J., Kummer, J. and Karch, F. (1990). A new homeotic mutation in the Drosophila bithorax complex removes a boundary separating two domains of regulation. EMBO J. 9, 2579–2585.
10.1002/j.1460-2075.1990.tb07439.x
CASPubMedWeb of Science®Google Scholar
19 Galloni, M., Gyurkovics, H., Schedl, P. and Karch, F. (1993). The bluetail transposon: evidence for independent cis-regulatory domains and domain boundaries in the bithorax complex. EMBO J. 12, 1087–1097.
10.1002/j.1460-2075.1993.tb05750.x
CASPubMedWeb of Science®Google Scholar
20 Karch, F., Galloni, M., Sipos, L., Gausz, J., Gyurkovics, H. and Schedl, P. (1994). Mcp and Fab-7: molecular analysis of putative boundaries of cis-regulatory domains in the bithorax complex of Drosophila melanogaster. Nucleic Acid Res. 22, 3138–3146.
10.1093/nar/22.15.3138
CASPubMedWeb of Science®Google Scholar
21 Hagstrom, K., Muller, M. and Schedl, P. (1996). Fab-7 functions as a chromatin domain boundary to ensure proper segment specification by the Drosophila bithorax complex. Genes Dev. 10, 3202–3215.
10.1101/gad.10.24.3202
CASPubMedWeb of Science®Google Scholar
22 Zhou, J., Barolo, S., Szymanski, P. and Levine, M. (1996). The Fab-7 element of the bithorax complex attenuates enhancer promoter interactions in the Drosophila embryo. Genes Dev. 10, 3195–3201.
10.1101/gad.10.24.3195
CASPubMedWeb of Science®Google Scholar
23 Andrew, D. J. and Scott, M. P. (1992). Downstream of the homeotic genes. The New Biologist 4, 5–15.

CASPubMedWeb of Science®Google Scholar
24 Botas, J. (1993). Control of morphogenesis and differentiation by HOM/Hox genes. Curr. Opin. Cell Biol. 5, 1015–1022.
10.1016/0955-0674(93)90086-6
CASPubMedWeb of Science®Google Scholar
25 Gould, A. P., Brookman, J. J., Strutt, D. I. and White, R. A. (1990). Targets of homeotic gene control in Drosophila [published erratum appears in Nature 1990 Dec 6;348(6301):560]. Nature 348, 308–312.
10.1038/348308a0
CASPubMedWeb of Science®Google Scholar
26 Graba, Y. et al. (1992). Homeotic control in Drosophila: the scabrous gene is an in vivo target of Ultrabithorax proteins. EMBO J. 11, 3375–3384.
10.1002/j.1460-2075.1992.tb05416.x
CASPubMedWeb of Science®Google Scholar
27 Vachon, G., Cohen, B., Pfeifle, C., McGuffin, M. E., Botas, J. and Cochen, S. (1992). Homeotic Genes of the Bithorax Complex Repress Limb Development in the Abdomen of the Drosophila Embryo through the Target Gene Distal-less. Cell 71, 437–450.
10.1016/0092-8674(92)90513-C
CASPubMedWeb of Science®Google Scholar
28 Capovilla, M., Brandt, M. and Botas, J. (1994). Direct regulation of decapentaplegic by Ultrabithorax and its role in Drosophila midgut morphogenesis. Cell 76, 461–475.
10.1016/0092-8674(94)90111-2
CASPubMedWeb of Science®Google Scholar
29 Graba, Y., Laurenti, P., Perrin, L., Aragnol, D. and Pradel, J. (1994). The modifier of variegation modulo gene acts downstream of dorsoventral and HOMC genes and is required for morphogenesis in Drosophila. Dev. Biol. 166, 704–715.
10.1006/dbio.1994.1349
CASPubMedWeb of Science®Google Scholar
30 Feinstein, P., Kornfeld, K., Hogness, D. S. and Mann, R. S. (1995). Identification of homeotic target genes in Drosophila including nervy, a protooncogene homolog. Genetics 140, 573–586.

CASPubMedWeb of Science®Google Scholar
31 Duboule, D. (1994). Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Development Supplement, 135–142.

Google Scholar
32 Duboule, D. (1995). Vertebrate Hox genes and proliferation: an alternative pathway to homeosis? Curr. Opin. Genet. Dev. 5, 525–528.
10.1016/0959-437X(95)90058-O
CASPubMedWeb of Science®Google Scholar
33 Hafen, E., Levine, M. and Gehring, W. J. (1984). Regulation of Antennapedia transcript distribution by the bithorax complex in Drosophila. Nature 307, 287–289.
10.1038/307287a0
PubMedWeb of Science®Google Scholar
34 Struhl, G. and White, R. A. (1985). Regulation of the Ultrabithorax gene of Drosophila by other bithorax complex genes. Cell 43, 507–519.
10.1016/0092-8674(85)90180-1
CASPubMedWeb of Science®Google Scholar
35 Garcia-Fernández, J. and Holland, P. W. H. (1994). Archetypal organization of the amphioxus Hox gene cluster. Nature 370, 563–566.
10.1038/370563a0
CASPubMedWeb of Science®Google Scholar
36 Patel, N. H. (1994). The evolution of arthropod segmentation: insights from comparisons of gene expression patterns. Development Supplement, 201–207.

Google Scholar

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Volume19, Issue8

August 1997

Pages 661-664

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