Timing and kinetics of E- to N-cadherin switch during neurulation in the avian embryo

Developmental Dynamics

Volumn 241, Issue 8, 2012, Pages 1333-1349

  Dady, Alwyn ^a,b   Blavet, Cedrine ^a,b   Duband, Jean Loup ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b Sorbonne Universités   (France)

Author keywords

Chick embryo; E cadherin; Epithelium to mesenchyme transition; N cadherin; Neural crest; Neural induction; Neural tube; Neurulation; Snail 2; Sox 2; Zeb 2

Indexed keywords

NERVE CELL ADHESION MOLECULE; UVOMORULIN;

ANIMAL EXPERIMENT; ARTICLE; BIRD; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; KINETICS; MORPHOLOGY; NERVOUS SYSTEM DEVELOPMENT; NEURULATION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CADHERINS; CHICK EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; NEURULATION;

AVES; GASTROPODA;

EID: 84864006754     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23813     Document Type: Article

References (65)

1. Aaku-Saraste E, Hellwig A, Huttner WB. 1996. Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure-remodeling of the neuroepithelium prior to neurogenesis. Dev Biol 180: 664-679.
2. Acloque H, Ocana OH, Matheu A, Rizzoti K, Wise C, Lovell-Badge R, Nieto MA. 2011. Reciprocal repression between Sox3 and snail transcription factors defines embryonic territories at gastrulation. Dev Cell 21: 546-558.
3. Braga VMM. 2002. Cell-cell adhesion and signaling. Curr. Opin. Cell Biol. 14: 546-556.
4. Bronner-Fraser M, Wolf JJ, Murray BA. 1992. Effects of antibodies against N-cadherin and N-CAM on the cranial neural crest and neural tube. Dev Biol 153: 291-301.
5. Cheung M, Chaboissier M-C, Mynett A, Hirst E, Schedl A, Briscoe J. 2005. The transcriptional control of trunk neural crest induction, survival, and delamination. Dev Cell 8: 179-192.
6. Chu YS, Eder O, Thomas WA, Simcha I, Pincet F, Ben-Ze'ev A, Perez E, Thiery JP, Dufour S. 2006. Prototypical type I E-cadherin and type II cadherin-7 mediate very distinct adhesiveness through their extracellular domains. J Biol Chem 281: 2901-2910.
7. Colas J-F, Schoenwolf GC. 2001. Towards a cellular and molecular understanding of neurulation. Dev Dyn 221: 117-145.
8. del Barrio MG, Nieto MA. 2002. Overexpression of Snail family members highlights their ability to promote chick neural crest formation. Development 129: 1583-1593.
9. Detrick RJ, Dickey D, Kintner CR. 1990. The effects of N-cadherin misexpression on morphogenesis in Xenopus embryos. Neuron 4: 493-506.
10. Duband JL. 2006. Neural crest delamination and migration: integrating regulations of cell interactions, locomotion, survival and fate. Adv Exp Med Biol 589: 45-77.
11. Duband J-L, Volberg T, Sabanay I, Thiery JP, Geiger B. 1988. Spatial and temporal distribution of the adherens-junction-associated adhesion molecule A-CAM during avian embryogenesis. Development 103: 325-344.
12. Duband J-L, Blavet C, Jarov A, Fournier-Thibault C. 2009. Spatio-temporal control of neural epithelial cell migration and epithelium-to-mesenchyme transition during neural tube development. Dev Growth Diff 51: 25-44.
13. Dufour S, Beauvais-Jouneau A, Delouvée A, Thiery JP. 1999. Differential function of N-cadherin and cadherin-7 in the control of embryonic cell motility. J. Cell Biol. 146: 501-516.
14. Duguay D, Foty RA, Steinberg MS. 2003. Cadherin-mediated cell adhesion and tissue segregation: qualitative and quantitative determinants. Dev Biol 253: 309-323.
15. Eisaki A, Kuroda H, Fukui A, Asashima M. 2000. XSIP1, a member of two-handed zinc finger proteins, induced anterior neural markers in Xenopus laevis animal cap. Biochem Biophys Res Commun 271: 151-157.
16. Fernando RI, Litzinger M, Trono P, Hamilton DH, Schlom J, Palena C. 2010. The T-box transcription factor Brachyury promotes epithelial-mesenchymal transition in human tumor cells. J Clin Invest 120: 533-544.
17. Halbleib JM, Nelson WJ. 2006. Cadherins in development: Cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20: 3199-3214.
18. Hamburger V, Hamilton HL. 1951. A series of normal stages in the development of the chick embryo. J Morph 88: 49-92.
19. Hardy KM, Yatskievych TA, Konieczka J, Bobbs AS, Antin PB. 2011. FGF signalling through RAS/MAPK and PI3K pathways regulates cell movement and gene expression in the chicken primitive streak without affecting E-cadherin expression. BMC Dev Biol 11: 20.
20. Hatta K, Takagi S, Fujisawa H, Takeichi M. 1987. Spatial and temporal expression pattern of N-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos. Dev Biol 120: 215-227.
21. Hong E, Brewster R. 2006. N-cadherin is required for the polarized cell behaviors that drive neurulation in the zebrafish. Development 133: 3895-3905.
22. Kan NG, Stemmler MP, Junghans D, Kanzler B, de Vries WN, Dominis M, Kemler R. 2007. Gene replacement reveals a specific role for E-cadherin in the formation of a functional trophectoderm. Development 134: 31-41.
23. Kispert A, Koschorz B, Herrmann BG. 1995. The T protein encoded by Brachyury is a tissue-specific transcription factor. EMBO J 14:4763-4772.
24. Lele Z, Folchert A, Concha M, Rauch GJ, Geisler R, Rosa F, Wilson SW, Hammerschmidt M, Bally-Cuif L. 2002. parachute/n-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube. Development 129: 3281-3294.
25. Libusova L, Stemmler MP, Hierholzer A, Schwarz H, Kemler R. 2010. N-cadherin can structurally substitute for E-cadherin during intestinal development but leads to polyp formation. Development 137: 2297-2305.
26. Linker C, Stern CD. 2004. Neural induction requires BMP inhibition only as a late step, and involves signals other than FGF and Wnt antagonists. Development 131: 5671-5681.
27. Lowery LA, Sive H. 2004. Strategies of vertebrate neurulation and a re-evaluation of teleost neural tube formation. Mech Dev 121: 1189-1197.
28. Luo Y, Ferreira-Cornwell M, Baldwin H, Kostetskii I, Lenox J, Lieberman M, Radice G. 2001. Rescuing the N-cadherin knockout by cardiac-specific expression of N- or E-cadherin. Development 128: 459-469.
29. Matsumata M, Uchikawa M, Kamachi Y, Kondoh H. 2005. Multiple N-cadherin enhancers identified by systematic functional screening indicate its Group B1 SOX-dependent regulation in neural and placodal development. Dev Biol 286: 601-617.
30. Nakaya Y, Sukowati EW, Wu Y, Sheng G. 2008. RhoA and microtubule dynamics control cell-basement membrane interaction in EMT during gastrulation. Nat Cell Biol 10: 765-775.
31. Nandadasa S, Tao Q, Menon NR, Heasman J, Wylie C. 2009. N- and E-cadherins in Xenopus are specifically required in the neural and non-neural ectoderm, respectively, for F-actin assembly and morphogenetic movements. Development 136: 1327-1338.
32. Nelson WJ, Nusse R. 2004. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303: 1483-1487.
33. Nieto M. 2002. The Snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3: 155-166.
34. Ohta S, Suzuki K, Tachibana K, Tanaka H, Yamada G. 2007. Cessation of gastrulation is mediated by suppression of epithelial-mesenchymal transition at the ventral ectodermal ridge. Development 134: 4315-4324.
35. Panorchan P, Thompson MS, Davis KJ, Tseng Y, Konstantopoulos K, Wirtz D. 2006. Single-molecule analysis of cadherin-mediated cell-cell adhesion. J Cell Sci 119: 66-74.
36. Papin C, van Grunsven LA, Verschueren K, Huylebroeck D, Smith JC. 2002. Dynamic regulation of Brachyury expression in the amphibian embryo by XSIP1. Mech Dev 111: 37-46.
37. Patel SD, Chen CP, Bahna F, Honig B, Shapiro L. 2003. Cadherin-mediated cell-cell adhesion: sticking together as a family. Curr Opin Struct Biol 13: 690-698.
38. Peinado H, Olmeda D, Cano A. 2007. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7: 415-428.
39. Perez-Moreno M, Jamora C, Fuchs E. 2003. Sticky business: orchestrating cellular signals at adherens junctions. Cell 112: 535-548.
40. Radice GL, Rayburn H, Matsunami H, Knudsen KA, Takeichi M, Hynes RO. 1997. Developmental defects in mouse embryos lacking N-cadherin. Dev Biol 181: 64-78.
41. Redies C. 1995. Cadherin expression in the developing vertebrate CNS: From neuromeres to brain nuclei and neural circuits. Exp Cell Res 220: 243-256.
42. Rovasio RA, Delouvée A, Yamada KM, Timpl R, Thiery JP. 1983. Neural crest cell migration: Requirements for exogenous fibronectin and high cell density. J Cell Biol 96: 462-473.
43. Sefton M, Sanchez S, Nieto MA. 1998. Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo. Development 125: 3111-3121.
44. Sheng G, dos Reis M, Stern CD. 2003. Churchill, a zinc finger transcriptional activator, regulates the transition between gastrulation and neurulation. Cell 115: 603-613.
45. Simard A, Di Pietro E, Ryan AK. 2005. Gene expression pattern of Claudin-1 during chick embryogenesis. Gene Expr Patterns 5: 553-560.
46. Suzuki SC, Takeichi M. 2008. Cadherins in neuronal morphogenesis and function. Dev Growth Differ 50(Suppl 1): S119-130.
47. Takeichi M. 1988. The cadherins: Cell-cell adhesion molecules controlling animal morphogenesis. Development 102: 639-655.
48. Takemoto T, Uchikawa M, Kamachi Y, Kondoh H. 2006. Convergence of Wnt and FGF signals in the genesis of posterior neural plate through activation of the Sox2 enhancer N-1. Development 133: 297-306.
49. Takemoto T, Uchikawa M, Yoshida M, Bell DM, Lovell-Badge R, Papaioannou VE, Kondoh H. 2011. Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature 470: 394-398.
50. Tavares AT, Izpisuja-Belmonte JC, Rodriguez-Leon J. 2001. Developmental expression of chick twist and its regulation during limb patterning. Int J Dev Biol 45: 707-713.
51. Tepass U, Truong K, Godt D, Ikura M, Peifer M. 2000. Cadherins in embryonic and neural morphogenesis. Nat Rev Mol Cell Biol 1: 91-100.
52. Théveneau E, Duband J-L, Altabef M. 2007. Ets-1 confers cranial features on neural crest delamination. PLoS ONE 2: e1142.
53. Thiery JP, Sleeman JP. 2006. Complex networks orchestrate epithelial-mesenchymal tansitions. Nat Rev Mol Cell Biol 7: 131-142.
54. Thiery JP, Delouvée A, Gallin W, Cunningham BA, Edelman GM. 1984. Ontogenetic expression of cell adhesion molecules: L-CAM is found in epithelia derived from the three primary germ layers. Dev Biol 102: 61-78.
55. Thiery JP, Acloque H, Huang RY, Nieto MA. 2009. Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
56. Uchikawa M, Ishida Y, Takemoto T, Kamachi Y, Kondoh H. 2003. Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammals. Dev Cell 4: 509-519.
57. Uchikawa M, Yoshida M, Iwafuchi-Doi M, Matsuda K, Ishida Y, Takemoto T, Kondoh H. 2011. B1 and B2 Sox gene expression during neural plate development in chicken and mouse embryos: universal versus species-dependent features. Dev Growth Differ 53: 761-771.
58. Van de Putte T, Maruhashi M, Francis A, Nelles L, Kondoh H, Huylebroeck D, Higashi Y. 2003. Mice lacking Zfhx1b, the gene that codes for Smad-interacting protein-1, reveal a role for multiple neural crest cell defects in the ethiology of Hirschsprung disease-mental retardation syndrome. Am J Hum Genet 72: 465-470.
59. Vandewalle C, Comijn J, De Craene B, Vermassen P, Bruyneel E, Andersen H, Tulchinsky E, Van Roy F, Berx G. 2005. SIP1/ZEB2 induces EMT by repressing genes of different epithelial cell-cell junctions. Nucleic Acids Res 33: 6566-6578.
60. Vandewalle C, Van Roy F, Berx G. 2009. The role of the ZEB family of transcription factors in development and disease. Cell Mol Life Sci 66: 773-787.
61. Wakamatsu Y, Endo Y, Osumi N, Weston JA. 2004. Multiple roles of Sox2, an HMG-box transcription factor in avian neural crest development. Dev Dyn 229: 74-86.
62. Wheelock MJ, Shintani Y, Maeda M, Fukumoto Y, Johnson KR. 2008. Cadherin switching. J Cell Sci 121: 727-735.
63. Wilson V, Beddington R. 1997. Expression of T protein in the primitive streak is necessary and sufficient for posterior mesoderm movement and somite differentiation. Dev Biol 192: 45-58.
64. Wilson V, Olivera-Martinez I, Storey KG. 2009. Stem cells, signals and vertebrate body axis extension. Development 136: 1591-1604.
65. Yagi T, Takeichi M. 2000. Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes Dev 14: 1169-1180.