Crossref journal-article
The Company of Biologists
Development (237)
Abstract

T-box genes form a large family of conserved transcription factors with diverse roles in animal development, but so far functions for only a few have been studied in detail. Here we show that four Caenorhabditis elegansT-box genes and the even-skipped-like homeobox gene vab-7function within a regulatory network to control embryonic patterning and morphogenesis. tbx-8 and tbx-9 have functionally redundant roles in the intercalation of posterior dorsal hypodermal cells, in muscle cell positioning and in intestinal development. Inhibiting tbx-9alone using RNA interference (RNAi) produces worms that have a thickened,`bobbed tail' phenotype, similar to that seen in mutants of vab-7,which itself has been shown to pattern posterior muscle and hypodermal cells. In support of the view that these genes function in the same pathway, we find that tbx-8 and tbx-9 are both necessary and sufficient for vab-7 expression. In addition, a third T-box gene, tbx-30,acts to repress vab-7 expression in the anterior of embryos. We further show that vab-7 itself represses the T-box gene mab-9 in posterior cells. Thus, during posterior patterning in C. elegans, there are multiple interactions between T-box genes and the vab-7 homeobox gene. Evolutionary parallels in other organisms suggest that regulatory interactions between T-box genes and even-skipped homologues are conserved.

Bibliography

Pocock, R., Ahringer, J., Mitsch, M., Maxwell, S., & Woollard, A. (2004). A regulatory network of T-box genes and theeven-skippedhomologuevab-7controls patterning and morphogenesis inC. elegans. Development, 131(10), 2373–2385.

Authors 5
  1. Roger Pocock (first)
  2. Julie Ahringer (additional)
  3. Michael Mitsch (additional)
  4. Sara Maxwell (additional)
  5. Alison Woollard (additional)
References 45 Referenced 37
  1. Ahringer, J. (1996). Posterior patterning by the Caenorhabditis elegans even-skipped homolog vab-7. Genes Dev.10,1120-1130. (10.1101/gad.10.9.1120)
  2. Ahringer, J. (1997). Maternal control of a zygotic patterning gene in Caenorhabditis elegans. Development124,3865-3869. (10.1242/dev.124.19.3865)
  3. Bamshad, M., Le, T., Watkins, W. S., Dixon, M. E., Kramer, B. E., Roeder, A. D., Carey, J. C., Root, S., Schinzel, A., Van Maldergem, L. et al. (1999). The spectrum of mutations in TBX3:genotype/phenotype relationship in ulnar-mammary syndrome. Am. J. Hum. Genet.64,1550-1562. (10.1086/302417)
  4. Basson, C. T., Huang, T., Lin, R. C., Bachinsky, D. R.,Weremowicz, S., Vaglio, A., Bruzzone, R., Quadrelli, R., Lerone, M., Romeo, G. et al. (1999). Different TBX5 interactions in heart and limb defined by Holt-Oram syndrome mutations. Proc. Natl. Acad. Sci. USA96,2919-2924. (10.1073/pnas.96.6.2919)
  5. Braybrook, C., Doudney, K., Marcano, A. C., Arnason, A.,Bjornsson, A., Patton, M. A., Goodfellow, P. J., Moore, G. E. and Stanier,P. (2001). The T-box transcription factor gene TBX22is mutated in X-linked cleft palate and ankyloglossia. Nat. Genet.29,179-183. (10.1038/ng730)
  6. Brown, S. J., Parrish, J. K., Beeman, R. W. and Denell, R. E. (1997). Molecular characterization and embryonic expression of the even-skipped ortholog of Tribolium castaneum. Mech. Dev.61,165-173. (10.1016/S0925-4773(96)00642-9)
  7. Chapman, D. L. and Papaioannou, V. E. (1998). Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6. Nature391,695-697. (10.1038/35624)
  8. Chin-Sang, I. D. and Chisholm, A. D. (2000). Form of the worm: genetics of epidermal morphogenesis in C. elegans. Trends Genet.16,544-551. (10.1016/S0168-9525(00)02143-0)
  9. Conlon, F. L. and Smith, J. C. (1999). Interference with brachyury function inhibits convergent extension,causes apoptosis, and reveals separate requirements in the FGF and activin signalling pathways. Dev. Biol.213,85-100. (10.1006/dbio.1999.9330)
  10. Conlon, F. L., Sedgwick, S. G., Weston, K. M. and Smith, J. C. (1996). Inhibition of Xbra transcription activation causes defects in mesodermal patterning and reveals autoregulation of Xbra in dorsal mesoderm. Development122,2427-2435. (10.1242/dev.122.8.2427)
  11. Cunliffe, V. and Smith, J. C. (1992). Ectopic mesoderm formation in Xenopus embryos caused by widespread expression of a Brachyury homologue. Nature358,427-430. (10.1038/358427a0)
  12. Esmaeili, B., Ross, J., Neades, C., Miller, D. M. III and Ahringer, J. (2002). The C. elegans even-skippedhomologue, vab-7, specifies DB motoneurone identity and axon trajectory. Development129,853-862.
  13. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E. and Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature391,806-811. (10.1038/35888)
  14. Goh, P.-Y. and Bogaert, T. (1991). Positioning and maintenance of embryonic body wall muscle attachments in C. elegans requires the mup-1 gene. Development111,667-681.
  15. Griffin, K. J., Amacher, S. L., Kimmel, C. B. and Kimelman,D. (1998). Molecular identification of spadetail: regulation of zebrafish trunk and tail mesoderm formation by T-box genes. Development125,3379-3388. (10.1242/dev.125.17.3379)
  16. Han, K. and Manley, J. L. (1993). Transcriptional repression by the Drosophila even-skipped protein:definition of a minimal repression domain. Genes Dev.7, 491-503. (10.1101/gad.7.3.491)
  17. Heid, P. J., Raich, W. B., Smith, R., Mohler, W. A., Simokat,K., Gendreau, S. B., Rothman, J. H. and Hardin, J. (2001). The zinc finger protein DIE-1 is required for late events during epithelial cell rearrangement in C. elegans. Dev. Biol.236,165-180. (10.1006/dbio.2001.0315)
  18. Herrmann, B. G. (1995). The mouse Brachyury(T) gene. Semin. Dev. Biol.6, 385-394. (10.1016/S1044-5781(06)80002-2)
  19. Ho, R. K. and Kane, D. A. (1990). Cell-autonomous action of zebrafish spt-1 mutation in specific mesodermal precursors. Nature348,728-730. (10.1038/348728a0)
  20. Huang, X., Cheng, H. J., Tessier-Lavigne, M. and Jin, Y.(2002). MAX-1, a novel PH/MyTH4/FERM domain cytoplasmic protein implicated in netrin-mediated axon repulsion. Neuron34,563-576. (10.1016/S0896-6273(02)00672-4)
  21. Hunter, C. P. and Kenyon, C. (1996). Spatial and temporal controls target PAL-1 blastomere specification activity to a single blastomere lineage in C. elegans embryos. Cell87,217-226. (10.1016/S0092-8674(00)81340-9)
  22. Joly, J. S., Joly, C., Schulte-Merker, S., Boulekbache, H. and Condamine, H. (1993). The ventral and posterior expression of the zebrafish homeobox gene eve1 is perturbed in dorsalized and mutant embryos. Development119,1261-1275. (10.1242/dev.119.4.1261)
  23. Kispert, A., Herrmann, B. G., Leptin, M. and Reuter, R.(1994). Homologs of the mouse Brachyury gene are involved in the specification of posterior terminal structures in Drosophila,Tribolium, and Locusta. Genes Dev.8,2137-2150. (10.1101/gad.8.18.2137)
  24. Kispert, A., Koschorz, B. and Herrmann, B. G.(1995). The T protein encoded by Brachyury is a tissue-specific transcription factor. EMBO J.14,4763-4772. (10.1002/j.1460-2075.1995.tb00158.x)
  25. Kofron, M., Demel, T., Xanthos, J., Lohr, J., Sun, B., Sive, H.,Osada, S., Wright, C., Wylie, C. and Heasman, J. (1999). Mesoderm induction in Xenopus is a zygotic event regulated by maternal VegT via TGFbeta growth factors. Development126,5759-5770.
  26. Kostas, S. A. and Fire, A. (2002). The T-box factor MLS-1 acts as a molecular switch during specification of nonstriated muscle in C. elegans. Genes Dev.16,257-269. (10.1101/gad.923102)
  27. Kusch, T. and Reuter, R. (1999). Functions for Drosophila brachyenteron and forkhead in mesoderm specification and cell signalling. Development126,3991-4003. (10.1242/dev.126.18.3991)
  28. Kusch, T., Storck, T., Walldorf, U. and Reuter, R.(2002). Brachyury proteins regulate target genes through modular binding sites in a cooperative fashion. Genes Dev.16,518-529. (10.1101/gad.213002)
  29. Li, C. and Manley, J. L. (1998). Even-skipped represses transcription by binding TATA binding protein and blocking the TFIID-TATA box interaction. Mol. Cell Biol.18,3771-3781. (10.1128/MCB.18.7.3771)
  30. Mello, C. and Fire, A. (1995). DNA Transformation. In Caenorhabditis elegans: Modern Biological Analysis of an Organism. Vol. 48 (ed. D. Shakes and H. Epstein), pp. 451-482. San Diego:Academic Press.
  31. Mohler, W. A., Simske, J. S., Williams-Masson, E. M., Hardin, J. D. and White, J. G. (1998). Dynamics and ultrastructure of developmental cell fusions in the Caenorhabditis elegans hypodermis. Curr. Biol.8,1087-1090. (10.1016/S0960-9822(98)70447-6)
  32. Muller, C. W. and Herrmann, B. G. (1997). Crystallographic structure of the T domain-DNA complex of the Brachyury transcription factor. Nature389,884-888. (10.1038/39929)
  33. Papaioannou, V. E. (2001). T-box genes in development: from hydra to humans. Int. Rev. Cytol.207, 1-70. (10.1016/S0074-7696(01)07002-4)
  34. Pflugfelder, G. O. and Heisenberg, M. (1995). Optomotor-blind of Drosophila melanogaster: A neurogenetic approach to optic lobe development and optomotor behaviour. Comp. Biochem. Physiol. A Physiol.110,185-202. (10.1016/0300-9629(94)00159-Q)
  35. Rashbass, P., Wilson, V., Rosen, B. and Beddington, R. S.(1994). Alterations in gene expression during mesoderm formation and axial patterning in Brachyury (T) embryos. Int. J. Dev. Biol.38,35-44.
  36. Simmer, F., Tijsterman, M., Parrish, S., Koushika, S. P., Nonet,M. L., Fire, A., Ahringer, J. and Plasterk, R. H. (2002). Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr. Biol.12,1317-1319.
  37. Simon, H.-G. (1999). T-box genes and the formation of vertebrate forelimb and hindlimb specific pattern. Cell Tissue Res.296,57-66. (10.1007/s004410051266)
  38. Simske, J. S. and Hardin, J. (2001). Getting into shape: epidermal morphogenesis in Caenorhabditis elegansembryos. Bioessays23,12-23. (10.1002/1521-1878(200101)23:1<12::AID-BIES1003>3.0.CO;2-R)
  39. Singer, J. B., Harbecke, R., Kusch, T., Reuter, R. and Lengyel,J. A. (1996). Drosophila brachyenteron regulates gene activity and morphogenesis in the gut. Development122,3707-3718. (10.1242/dev.122.12.3707)
  40. Sinha, S., Abraham, S., Gronostajski, R. M. and Campbell, C. E. (2000). Differential DNA binding and transcription modulation by three T-box proteins, T, TBX1 and TBX2. Gene258,15-29. (10.1016/S0378-1119(00)00417-0)
  41. Smith, J. (1999). T-box genes: what they do and how they do it. Trends Genet.15,154-158. (10.1016/S0168-9525(99)01693-5)
  42. Sulston, J. and Hodgkin, J. (1988). Methods. In The Nematode Caenorhabditis elegans (ed. W. B. Wood),pp. 587-606. New York: Cold Spring Harbor Laboratory Press.
  43. Um, M., Li, C. and Manley, J. L. (1995). The transcriptional repressor even-skipped interacts directly with TATA-binding protein. Mol. Cell Biol.15,5007-5016. (10.1128/MCB.15.9.5007)
  44. Woollard, A. and Hodgkin, J. (2000). The Caenorhabditis elegans fate-determining gene mab-9 encodes a T-box protein required to pattern the posterior hindgut. Genes Dev.14,596-603. (10.1101/gad.14.5.596)
  45. Zhang, J., Houston, D. W., King, M. L., Payne, C., Wylie, C. and Heasman, J. (1998). The role of maternal VegT in establishing the primary germ layers in Xenopus embryos. Cell94,515-524. (10.1016/S0092-8674(00)81592-5)
Dates
Type When
Created 21 years, 4 months ago (April 26, 2004, 8:23 p.m.)
Deposited 2 years, 4 months ago (April 28, 2023, 9:14 a.m.)
Indexed 1 month ago (Aug. 2, 2025, 12:11 a.m.)
Issued 21 years, 3 months ago (May 15, 2004)
Published 21 years, 3 months ago (May 15, 2004)
Published Print 21 years, 3 months ago (May 15, 2004)
Funders 0

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@article{Pocock_2004, title={A regulatory network of T-box genes and theeven-skippedhomologuevab-7controls patterning and morphogenesis inC. elegans}, volume={131}, ISSN={0950-1991}, url={http://dx.doi.org/10.1242/dev.01110}, DOI={10.1242/dev.01110}, number={10}, journal={Development}, publisher={The Company of Biologists}, author={Pocock, Roger and Ahringer, Julie and Mitsch, Michael and Maxwell, Sara and Woollard, Alison}, year={2004}, month=may, pages={2373–2385} }