Functional specificity of the nematode Hox gene<i>mab-5</i>

Development (Cambridge) - Tập 130 Số 5 - Trang 983-993 - 2003
Arturo Gutierrez1, Lars Knoch1, Hanh Witte1, Ralf J. Sommer1
1Max-Planck Institut für Entwicklungsbiologie, Abt. Evolutionsbiologie, Spemannstr. 37-39, D-72076 Tübingen, Germany

Tóm tắt

Hox genes encode evolutionarily conserved transcription factors involved in morphological specification along the anteroposterior body axis of animals. The two most striking features of Hox genes are colinearity and the strong sequence conservation. Among all animals studied so far, the nematodeCaenorhabditis elegans contains one of the most divergent Hox clusters. The core cluster contains only four members, which in part deviate from the colinearity rule. In addition, orthologous and paralogous nematode Hox sequences diverged substantially. Given these nematode-specific features,we asked how these Hox proteins evolved and how they provide functional specificity. We investigated the role of MAB-5 during ray formation and established an in vivo assay using Cel-mab-5 regulatory elements to express orthologous, paralogous and chimeric cDNAs in a Cel-mab-5mutant background. We show that the MAB-5 ortholog from Pristionchus pacificus, but not the C. elegans paralogous Hox proteins can rescue Cel-mab-5. Experiments with chimeric, truncated and mutagenized Hox proteins suggest the specificity to be conferred by the N-terminal arm and helix I, but not helix II of the homeodomain.

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Tài liệu tham khảo

Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics77, 71-94.

Chauvet, S., Merabet, S., Bilder, D., Scott, M. P., Pradel, J. and Graba, Y. (2000). Distinct hox protein sequences determine specificity in different tissues. Proc. Natl. Acad. Sci. USA97,4064-4069.

Chisholm, A. (1991). Control of cell fate in the tail region of C. elegans by the gene egl-5.Development111,921-932.

The Caenorhabditis elegans Sequencing Consortium(1998). Genome sequence of the nematode C. elegans: a platform for investigating biology. Science282,2012-2018.

Costa, M., Weir, M., Coulson, A., Sulston, J. and Kenyon, C.(1988). Posterior pattern formation in C. elegans involves position-specific expression of a gene containing a homeobox.Cell55,747-756.

Cowing, D. W. and Kenyon, C. (1992). Expression of the homeotic gene mab-5 during Caenorhabditis elegans embryogenesis.Development116,481-490.

Eizinger, A. and Sommer, R. J. (1997). The homeotic gene lin-39 and the evolution of nematode epidermal cell fates.Science278,452-455.

Eizinger, A., Jungblut, B. and Sommer, R. J.(1999). Evolutionary change in the functional specificity of genes. Trends Genet.15,197-202.

Ferreira, H. B., Zhang, Y., Zhao, C. and Emmons, S. W.(1999). Patterning of Caenorhabditis elegans posterior structures by the Abdominal-B homolog, egl-5. Dev. Biol.207,215-228.

Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y. L. and Postlethwait, J. (1999). Preservation of duplicate genes by complementary, degenerative mutations. Genetics151,1531-1545.

Furukubo-Tokunaga, K., Flister, S. and Gehring, W. J.(1993). Functional specificity of the Antennapedia homeodomain.Proc. Natl. Acad. Sci. USA90,6360-6364.

Galant, R. and Carroll, S. B. (2002). Evolution of a transcriptional repression domain in an insect Hox protein.Nature415,910-913.

Galant, R., Walsh, C. M. and Carroll, S. B.(2002). Hox repression of a target gene:extradenticle-independent, additive action through multiple monomer binding sites. Development129,3115-3126.

Graba, Y., Aragnol, D. and Pradel, J. (1997). Drosophila Hox complex downstream targets and the function of homeotic genes.BioEssays19,379-388.

Grandien, K. and Sommer, R. J. (2001). Functional comparison of the nematode Hox gene lin-39 in C. elegans and P. pacificus reveals evolutionary conservation of protein function despite divergence of primary sequences. Genes Dev.15,2161-2172.

Grenier, J. K. and Carroll, S. B. (2000). Functional evolution of the Ultrabithorax protein. Proc. Natl. Acad. Sci. USA97,704-709.

Gu, T., Orita, S. and Han, M. (1998). Caenorhabditis elegans SUR-5, a novel but conserved protein, negatively regulates LET-60 Ras activity during vulval induction. Mol. Cell. Biol.18,4556-4564.

Hunter, C. P. and Kenyon, C. (1995). Specification of anteroposterior cell fates in Caenorhabditis elegans by Drosophila Hox proteins. Nature377,229-232.

Jungblut, B. and Sommer, R. J. (1998). The Pristionchus pacificus mab-5 gene is involved in the regulation of ventral epidermal cell fates. Curr. Biol.8, 775-778.

Jungblut, B. and Sommer, R. J. (2000). Novel cell-cell interactions during vulva development in Pristionchus pacificus.Development127,3295-3303.

Jungblut, B., Pires-daSilva, A. and Sommer, R. J.(2001). Formation of the egg-laying system in Pristionchus pacificus requires complex interactions between gonadal, mesodermal and epidermal tissues and does not rely on single cell inductions.Development128,3395-3404.

Kenyon, C. (1986). A gene involved in the development of the posterior body region of C. elegans.Cell46,477-487.

Kenyon, C. J., Austin, J., Costa, M., Cowing, D. W., Harris, J. M., Honigberg, L., Hunter, C. P., Maloof, J. N., Muller-Immergluck, M. M.,Salser, S. J. et al. (1997). The dance of the Hox genes:patterning the anteroposterior body axis of Caenorhabditis elegans.Cold Spring Harb. Symp. Quant. Biol.62,293-305.

Liu, J. and Fire, A. (2000). Overlapping roles of two Hox genes and the exd ortholog ceh-20 in diversification of the C. elegans postembryonic mesoderm. Development127,5179-5190.

Ludwig, M. Z., Bergman, C., Patel, N. H. and Kreitman, M.(2000). Evidence for stabilizing selection in a eukaryotic enhancer element. Nature403,564-567.

Maloof, J. N. and Kenyon, C. (1998). The Hox gene lin-39 is required during C. elegans vulval induction to select the outcome of Ras signaling. Development125,181-190.

Mann, R. S. and Affolter, M. (1998). Hox proteins meet more partners. Curr. Opin. Genet. Dev.8, 423-429.

Mann, R. S. and Chan, S. K. (1996). Extra specificity from extradenticle: the partnership between HOX and PBX/EXD homeodomain proteins. Trends Genet.12,258-262.

Mello, C. and Fire, A. (1995). DNA transformation. Methods Cell Biol48,451-482.

Mello, C. C., Kramer, J. M., Stinchcomb, D. and Ambros, V.(1991). Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J.10,3959-3970.

Ronshaugen, M., McGinnis, N. and McGinnis, W.(2002). Hox protein mutation and macroevolution of the insect body plan. Nature415,914-917.

Salser, S. J. and Kenyon, C. (1996). A C. elegans Hox gene switches on, off, on and off again to regulate proliferation,differentiation and morphogenesis. Development122,1651-1661.

Salser, S. J., Loer, C. M. and Kenyon, C.(1993). Multiple HOM-C gene interactions specify cell fates in the nematode central nervous system. Genes Dev.7,1714-1724.

Sambrook, J. and Russell, D. W. (2001).Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press.

Sommer, R., Carta, L. K., Seong-youn, K. and Sternberg, P. W. (1996). Morphological, genetic and molecular description of Pristionchus pacificus sp. n. (Nematoda: Neodiplogastridae.(Fund. Appl. Nematol.19,511-521.

Sommer, R. J., Eizinger, A., Lee, K. Z., Jungblut, B., Bubeck,A. and Schlak, I. (1998). The Pristionchus HOX gene Ppa-lin-39 inhibits programmed cell death to specify the vulva equivalence group and is not required during vulval induction.Development125,3865-3873.

Sulston, J. E. and Horvitz, H. R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans.Dev. Biol.56,110-156.

Tautz, D. (2000). Evolution of transcriptional regulation. Curr. Opin. Genet. Dev.10,575-579.

Van Auken, K., Weaver, D. C., Edgar, L. G. and Wood, W. B.(2000). Caenorhabditis elegans embryonic axial patterning requires two recently discovered posterior-group Hox genes. Proc. Natl. Acad. Sci. USA97,4499-4503.

Van Auken, K., Weaver, D., Robertson, B., Sundaram, M., Saldi,T., Edgar, L., Elling, U., Lee, M., Boese, Q. and Wood, W. B.(2002). Roles of the Homothorax/Meis/Prep homolog UNC-62 and the Exd/Pbx homologs CEH-20 and CEH-40 in C. elegans embryogenesis.Development129,5255-5268.

Zeng, W., Andrew, D. J., Mathies, L. D., Horner, M. A. and Scott, M. P. (1993). Ectopic expression and function of the Antp and Scr homeotic genes: the N terminus of the homeodomain is critical to functional specificity. Development118,339-352.

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Development (Cambridge)

Tập 130 Số 5

983-993

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