Oscillations of the snail genes in the presomitic mesoderm coordinate segmental patterning and morphogenesis in vertebrate somitogenesis

Developmental Cell

Volumn 10, Issue 3, 2006, Pages 355-366

  Dale, Jacqueline Kim ^a,b   Malapert, Pascale ^a   Chal, Jérome ^a   Vilhais Neto, Gonçalo ^a   Maroto, Miguel ^a,b   Johnson, Teri ^a   Jayasinghe, Sachintha ^a   Trainor, Paul ^a   Herrmann, Bernhard ^c   Pourquié, Olivier ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

Dev Bio

Indexed keywords

FIBROBLAST GROWTH FACTOR; GLYCOSYLTRANSFERASE; LUNATIC FRINGE PROTEIN; MESO1 PROTEIN; NOTCH RECEPTOR; PARAXIS PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SNAIL1; TRANSCRIPTION FACTOR SNAIL2; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL TISSUE; ARTICLE; CHICK; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYO SEGMENTATION; EPITHELIZATION; GENE EXPRESSION; GENE OVEREXPRESSION; MESENCHYME CELL; MESODERM; MORPHOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SOMITE;

ANIMALS; AVIAN PROTEINS; BODY PATTERNING; CHICK EMBRYO; CYTOSKELETAL PROTEINS; EMBRYO; EMBRYO, NONMAMMALIAN; EPITHELIUM; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOSYLTRANSFERASES; MESODERM; MICE; MORPHOGENESIS; PROTEIN ISOFORMS; RECEPTORS, NOTCH; RNA, MESSENGER; SIGNAL TRANSDUCTION; SOMITES; TRANSCRIPTION FACTORS; WNT PROTEINS;

ANIMALIA; GASTROPODA; VERTEBRATA;

EID: 33644522079     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2006.02.011     Document Type: Article

References (58)

1. A. Aulehla C. Wehrle B. Brand-Saberi R. Kemler A. Gossler B. Kanzler B.G. Herrmann Wnt3a plays a major role in the segmentation clock controlling somitogenesis Dev. Cell 4 2003 395-406
2. R.E. Bachelder S.O. Yoon C. Franci A.G. de Herreros A.M. Mercurio Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: Implications for the epithelial-mesenchymal transition J. Cell Biol. 168 2005 29-33
3. A. Barrallo-Gimeno M.A. Nieto The Snail genes as inducers of cell movement and survival: Implications in development and cancer Development 132 2005 3151-3161
4. E. Batlle E. Sancho C. Franci D. Dominguez M. Monfar J. Baulida A. Garcia De Herreros The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells Nat. Cell Biol. 2 2000 84-89
5. Y. Bessho R. Sakata S. Komatsu K. Shiota S. Yamada R. Kageyama Dynamic expression and essential functions of Hes7 in somite segmentation Genes Dev. 15 2001 2642-2647
6. Y. Bessho H. Hirata Y. Masamizu R. Kageyama Periodic repression by the bHLH factor Hes7 is an essential mechanism for the somite segmentation clock Genes Dev. 17 2003 1451-1456
7. A. Buchberger K. Seidl C. Klein H. Eberhardt H.H. Arnold cMeso-1, a novel bHLH transcription factor, is involved in somite formation in chicken embryos Dev. Biol. 199 1998 201-215
8. R. Burgess P. Cserjesi K.L. Ligon E.N. Olson Paraxis: A basic helix-loop-helix protein expressed in paraxial mesoderm and developing somites Dev. Biol. 168 1995 296-306
9. R. Burgess A. Rawls D. Brown A. Bradley E.N. Olson Requirement of the paraxis gene for somite formation and musculoskeletal patterning Nature 384 1996 570-573
10. A. Cano M.A. Perez-Moreno I. Rodrigo A. Locascio M.J. Blanco M.G. del Barrio F. Portillo M.A. Nieto The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression Nat. Cell Biol. 2 2000 76-83
11. E.A. Carver R. Jiang Y. Lan K.F. Oram T. Gridley The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition Mol. Cell. Biol. 21 2001 8184-8188
12. B. Ciruna J. Rossant FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak Dev. Cell 1 2001 37-49
13. S.E. Cole J.M. Levorse S.M. Tilghman T.F. Vogt Clock regulatory elements control cyclic expression of Lunatic Fringe during somitogenesis Dev. Cell 3 2002 75-84
14. R.A. Conlon A.G. Reaume J. Rossant Notch1 is required for the coordinate segmentation of somites Development 121 1995 1533-1545
15. J. Cowden M. Levine The Snail repressor positions Notch signaling in the Drosophila embryo Development 129 2002 1785-1793
16. J.K. Dale M. Maroto M.L. Dequeant P. Malapert M. McGrew O. Pourquie Periodic Notch inhibition by Lunatic Fringe underlies the chick segmentation clock Nature 421 2003 275-278
17. M.C. Delfini J. Dubrulle P. Malapert J. Chal O. Pourquie Control of the segmentation process by graded MAPK/ERK activation in the chick embryo Proc. Natl. Acad. Sci. USA 102 2005 11343-11348
18. H.F. Dovey V. John J.P. Anderson L.Z. Chen P. de Saint Andrieu L.Y. Fang S.B. Freedman B. Folmer E. Goldbach E.J. Holsztynska et al. Functional γ-secretase inhibitors reduce beta-amyloid peptide levels in brain J. Neurochem. 76 2001 173-181
19. J.L. Duband S. Dufour K. Hatta M. Takeichi G.M. Edelman J.P. Thiery Adhesion molecules during somitogenesis in the avian embryo J. Cell Biol. 104 1987 1361-1374
20. J. Dubrulle O. Pourquie Coupling segmentation to axis formation Development 131 2004 5783-5793
21. J. Dubrulle M.J. McGrew O. Pourquie FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation Cell 106 2001 219-232
22. T.L. Greco S. Takada M.M. Newhouse J.A. McMahon A.P. McMahon S.A. Camper Analysis of the vestigial tail mutation demonstrates that Wnt-3a gene dosage regulates mouse axial development Genes Dev. 10 1996 313-324
23. V. Hamburger H.L. Hamilton A series of normal stages in the development of the chick embryo (1951) Dev. Dyn. 195 1992 231-272
24. D. Henrique J. Adam A. Myat A. Chitnis J. Lewis D. Ish-Horowicz Expression of a Delta homologue in prospective neurons in the chick Nature 375 1995 787-790
25. A. Ishikawa S. Kitajima Y. Takahashi H. Kokubo J. Kanno T. Inoue Y. Saga Mouse Nkd1, a Wnt antagonist, exhibits oscillatory gene expression in the PSM under the control of Notch signaling Mech. Dev. 121 2004 1443-1453
26. W.C. Jen V. Gawantka N. Pollet C. Niehrs C. Kintner Periodic repression of Notch pathway genes governs the segmentation of Xenopus embryos Genes Dev. 13 1999 1486-1499
27. A. Kawamura S. Koshida H. Hijikata T. Sakaguchi H. Kondoh S. Takada Zebrafish hairy/enhancer of split protein links FGF signaling to cyclic gene expression in the periodic segmentation of somites Genes Dev. 19 2005 1156-1161
28. V. Knezevic R. De Santo S. Mackem Two novel chick T-box genes related to mouse Brachyury are expressed in different, non-overlapping mesodermal domains during gastrulation Development 124 1997 411-419
29. N.M. Le Douarin E. Dupin Cell lineage analysis in neural crest ontogeny J. Neurobiol. 24 1993 146-161
30. K.K. Linask C. Ludwig M.D. Han X. Liu G.L. Radice K.A. Knudsen N-cadherin/catenin-mediated morphoregulation of somite formation Dev. Biol. 202 1998 85-102
31. A. Locascio M. Manzanares M.J. Blanco M.A. Nieto Modularity and reshuffling of Snail and Slug expression during vertebrate evolution Proc. Natl. Acad. Sci. USA 99 2002 16841-16846
32. S.G. Megason A.P. McMahon A mitogen gradient of dorsal midline Wnts organizes growth in the CNS Development 129 2002 2087-2098
33. M. Mohammadi G. McMahon L. Sun C. Tang P. Hirth B.K. Yeh S.R. Hubbard J. Schlessinger Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors Science 276 1997 955-960
34. A.V. Morales Y. Yasuda D. Ish-Horowicz Periodic Lunatic Fringe expression is controlled during segmentation by a cyclic transcriptional enhancer responsive to Notch signaling Dev. Cell 3 2002 63-74
35. V. Morel R. Le Borgne F. Schweisguth Snail is required for Delta endocytosis and Notch-dependent activation of single-minded expression Dev. Genes Evol. 213 2003 65-72
36. M. Morimoto Y. Takahashi M. Endo Y. Saga The Mesp2 transcription factor establishes segmental borders by suppressing Notch activity Nature 435 2005 354-359
37. Y. Nakaya S. Kuroda Y.T. Katagiri K. Kaibuchi Y. Takahashi Mesenchymal-epithelial transition during somitic segmentation is regulated by differential roles of Cdc42 and Rac1 Dev. Cell 7 2004 425-438
38. W.J. Nelson R. Nusse Convergence of Wnt, β-catenin, and cadherin pathways Science 303 2004 1483-1487
39. M.A. Nieto The snail superfamily of zinc-finger transcription factors Nat. Rev. Mol. Cell Biol. 3 2002 155-166
40. M.A. Nieto M.F. Bennett M.G. Sargent D.G. Wilkinson Cloning and developmental expression of Sna, a murine homologue of the Drosophila snail gene Development 116 1992 227-237
41. H. Niwa K. Yamamura J. Miyazaki Efficient selection for high-expression transfectants with a novel eukaryotic vector Gene 108 1991 193-199
42. C. Oka T. Nakano A. Wakeham J.L. de la Pompa C. Mori T. Sakai S. Okazaki M. Kawaichi K. Shiota T.W. Mak T. Honjo Disruption of the mouse RBP-J kappa gene results in early embryonic death Development 121 1995 3291-3301
43. I. Palmeirim D. Henrique D. Ish-Horowicz O. Pourquié Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis Cell 91 1997 639-648
44. O. Pourquie The segmentation clock: Converting embryonic time into spatial pattern Science 301 2003 328-330
45. P.C. Rida N. Le Minh Y.J. Jiang A Notch feeling of somite segmentation and beyond Dev. Biol. 265 2004 2-22
46. P. Savagner K.M. Yamada J.P. Thiery The zinc-finger protein slug causes desmosome dissociation, an initial and necessary step for growth factor-induced epithelial-mesenchymal transition J. Cell Biol. 137 1997 1403-1419
47. M. Sefton S. Sanchez M.A. Nieto Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo Development 125 1998 3111-3121
48. K. Serth K. Schuster-Gossler R. Cordes A. Gossler Transcriptional oscillation of Lunatic fringe is essential for somitogenesis Genes Dev. 17 2003 912-925
49. D.E. Smith F. Franco del Amo T. Gridley Isolation of Sna, a mouse gene homologous to the Drosophila genes snail and escargot: Its expression pattern suggests multiple roles during postimplantation development Development 116 1992 1033-1039
50. D. Sosic B. Brand-Saberi C. Schmidt B. Christ E.N. Olson Regulation of paraxis expression and somite formation by ectoderm- and neural tube-derived signals Dev. Biol. 185 1997 229-243
51. E.M. Southard-Smith L. Kos W.J. Pavan Sox10 mutation disrupts neural crest development in Dom Hirschsprung mouse model Nat. Genet. 18 1998 60-64
52. S. Takada K.L. Stark M.J. Shea G. Vassileva J.A. McMahon A.P. McMahon Wnt-3a regulates somite and tailbud formation in the mouse embryo Genes Dev. 8 1994 174-189
53. Y. Takahashi K. Koizumi A. Takagi S. Kitajima T. Inoue H. Koseki Y. Saga Mesp2 initiates somite segmentation through the Notch signalling pathway Nat. Genet. 25 2000 390-396
54. J.P. Thiery A. Delouvee W.J. Gallin B.A. Cunningham G.M. Edelman Ontogenetic expression of cell adhesion molecules: L-CAM is found in epithelia derived from the three primary germ layers Dev. Biol. 102 1984 61-78
55. L.A. Timmerman J. Grego-Bessa A. Raya E. Bertran J.M. Perez-Pomares J. Diez S. Aranda S. Palomo F. McCormick J.C. Izpisua-Belmonte J.L. de la Pompa Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation Genes Dev. 18 2004 99-115
56. T.P. Yamaguchi A. Bradley A.P. McMahon S. Jones A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo Development 126 1999 1211-1223
57. N. Zhang T. Gridley Defects in somite formation in lunatic fringe-deficient mice Nature 394 1998 374-377
58. B.P. Zhou J. Deng W. Xia J. Xu Y.M. Li M. Gunduz M.C. Hung Dual regulation of Snail by GSK-3β-mediated phosphorylation in control of epithelial-mesenchymal transition Nat. Cell Biol. 6 2004 931-940