Novel insight into the function and regulation of αN-catenin by Snail2 during chick neural crest cell migration

Developmental Biology

Volumn 344, Issue 2, 2010, Pages 896-910

  Jhingory, S ^a   Wu, C Y ^a   Taneyhill, L A ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

Adherens junctions; Chick embryo; Delamination; EMT; Migration; Neural crest; N catenin

Indexed keywords

ALPHA NEURAL CATENIN; CATENIN; SNAIL2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL JUNCTION; CELL MIGRATION; CELL TYPE; CHICK; CONTROLLED STUDY; CRANIOFACIAL MORPHOLOGY; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; GENE REPRESSION; MELANOCYTE; NEURAL CREST CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

VERTEBRATA;

EID: 77955270907     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.06.006     Document Type: Article

References (59)

1. Acloque H., Adams M.S., Fishwick K., Bronner-Fraser M., Nieto M.A. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J. Clin. Invest. 2009, 119:1438-1449.
2. Ahlstrom J.D., Erickson C.A. The neural crest epithelial-mesenchymal transition in 4D: a 'tail' of multiple non-obligatory cellular mechanisms. Development 2009, 136:1801-1812.
3. Barrallo-Gimeno A., Nieto M.A. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 2005, 132:3151-3161.
4. Bolos V., Peinado H., Perez-Moreno M., Fraga M.F., Esteller M., Cano A. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J. Cell Sci. 2003, 116:499-511.
5. Bogaerts S., Vanlandschoot A., van Hengel J., van Roy F. Nuclear translocation of alphaN-catenin by the novel zinc finger transcriptional repressor ZASC1. Exp. Cell Res. 2005, 311:1-13.
6. Boulay J.L., Dennefeld C., Alberga A. The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. Nature 1987, 330:395-398.
7. Bullions L.C., Notterman D.A., Chung L.S., Levine A.J. Expression of wild-type alpha-catenin protein in cells with a mutant alpha-catenin gene restores both growth regulation and tumor suppressor activities. Mol. Cell. Biol. 1997, 17:4501-4508.
8. Cano A., Perez-Moreno M., Rodrigo I., Locascio A., Blanco M., del Barrio M.G., Portillo F., Nieto M.A. The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2000, 2:76-83.
9. Carver E.A., Jiang R., Lan Y., Oram K.F., Gridley T. The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol. Cell. Biol. 2001, 21:8184-8188.
10. Cavey M., Rauzi M., Lenne P.F., Lecuit T. A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 2008, 453:751-756.
11. Coles E.G., Taneyhill L.A., Bronner-Fraser M. A critical role for Cadherin6B in regulating avian neural crest emigration. Dev. Biol. 2007, 312:533-544.
12. Come C., Arnoux V., Bibeau F., Savagner P. Roles of the transcription factors snail and slug during mammary morphogenesis and breast carcinoma progression. J. Mammary Gland Biol. Neoplasia 2004, 9:183-193.
13. De Craene B., van Roy F., Berx G. Unraveling signalling cascades for the Snail family of transcription factors. Cell. Signal. 2005, 17:535-547.
14. Giroldi L.A., Bringuier P.P., de Weijert M., Jansen C., van Bokhoven A., Schalken J.A. Role of E boxes in the repression of E-cadherin expression. Biochem. Biophys. Res. Commun. 1997, 241:453-458.
15. Grau Y., Carteret C., Simpson P. Mutations and chromosomal rearrangements affecting the expression of Snail, a gene involved in embryonic patterning in Drosophila melanogaster. Genetics 1984, 108:347-360.
16. Gumbiner B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:622-634.
17. Hay E.D. An overview of epithelio-mesenchymal transformation. Acta Anat. (Basel) 1995, 154:8-20.
18. Hemavathy K., Guru S.C., Harris J., Chen J.D., Ip Y.T. Human Slug is a repressor that localizes to sites of active transcription. Mol. Cell. Biol. 2000, 26:5087-5095.
19. Hemavathy K., Hu X., Ashraf S.I., Small S.J., Ip Y.T. The repressor function of snail is required for Drosophila gastrulation and is not replaceable by Escargot or Worniu. Dev. Biol. 2004, 269:411-420.
20. Herrenknecht K., Ozawa M., Eckerskorn C., Lottspeich F., Lenter M., Kemler R. The uvomorulin-anchorage protein alpha catenin is a vinculin homologue. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:9156-9160.
21. Hirano S., Kimoto N., Shimoyama Y., Hirohashi S., Takeichi M. Identification of a neural alpha-catenin as a key regulator of cadherin function and multicellular organization. Cell 1992, 70:293-301.
22. Hirano S., Takeichi M. Differential expression of alpha N-catenin and N-cadherin during early development of chicken embryos. Int. J. Dev. Biol. 1994, 38:379-384.
23. Hyafil F., Babinet C., Jacob F. Cell-cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell 1981, 26:447-454.
24. Itasaki N., Bel-Vialar S., Krumlauf R. 'Shocking' developments in chick embryology: electroporation and in ovo gene expression. Nat. Cell Biol. 1999, 1:E203-E207.
25. Kofron M., Spagnuolo A., Klymkowsky M., Wylie C., Heasman J. The roles of maternal alpha-catenin and plakoglobin in the early Xenopus embryo. Development 1997, 124:1553-1560.
26. Krispin S., Nitzan E., Kassem Y., Kalcheim C. Evidence for a dynamic spatiotemporal fate map and early fate restrictions of premigratory avian neural crest. Development 2010, 137:585-595.
27. Le Douarin N., Kalcheim C. The neural crest 1999, Cambridge University Press, New York.
28. Leptin M., Casal J., Grunewald B., Reuter R. Mechanisms of early Drosophila mesoderm formation. Dev. Suppl. 1992, 23-31.
29. Magie C.R., Pinto-Santini D., Parkhurst S.M. Rho1 interacts with p120ctn and alpha-catenin, and regulates cadherin-based adherens junction components in Drosophila. Development 2002, 129:3771-3782.
30. Nagafuchi A., Takeichi M., Tsukita S. The 102 kd cadherin-associated protein: similarity to vinculin and posttranscriptional regulation of expression. Cell 1991, 65:849-857.
31. Nakagawa S., Takeichi M. Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 1998, 125:2963-2971.
32. Nakaya Y., Sukowati E.W., Wu Y., Sheng G. RhoA and microtubule dynamics control cell-basement membrane interaction in EMT during gastrulation. Nat. Cell Biol. 2008, 10:765-775.
33. Niessen C.M., Gottardi C.J. Molecular components of the adherens junction. Biochim. Biophys. Acta 2008, 1778:562-571.
34. Nieto M.A., Sargent M.G., Wilkinson D.G., Cooke J. Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science 1994, 264:835-839.
35. Nieto M.A. The Snail superfamily of zinc-finger transcription factors. Nat. Rev. Mol. Cell Biol. 2002, 3:155-166.
36. Oda H., Tsukita S., Takeichi M. Dynamic behavior of the cadherin-based cell-cell adhesion system during Drosophila gastrulation. Dev. Biol. 1998, 203:435-450.
37. Park C., Longo C.M., Ackerman S.L. Genetic and physical mapping of the cerebellar deficient folia (cdf) locus on mouse chromosome 6. Genomics 2000, 69:135-138.
38. Park C., Falls W., Finger J.H., Longo-Guess C.M., Ackerman S.L. Deletion in Catna2, encoding alpha N-catenin, causes cerebellar and hippocampal lamination defects and impaired startle modulation. Nat. Genet. 2002, 31:279-284.
39. Park C., Finger J.H., Cooper J.A., Ackerman S.L. The cerebellar deficient folia (cdf) gene acts intrinsically in Purkinje cell migrations. Genesis 2002, 32:32-41.
40. Perez-Mancera P.A., Gonzalez-Herrero I., Perez-Caro M., Gutierrez-Cianca N., Flores T., Gutierrez-Adan A., Pintado B., Snachez-Martin M., Sanchez-Garcia I. SLUG in cancer development. Oncogene 2005, 24:3073-3082.
41. Pokutta S., Drees F., Yamada S., Nelson W.J., Weis W.I. Biochemical and structural analysis of alpha-catenin in cell-cell contacts. Biochem. Soc. Trans. 2008, 36:141-147.
42. Sauka-Spengler T., Bronner-Fraser M. A gene regulatory network orchestrates neural crest formation. Nat. Rev. Mol. Cell Biol. 2008, 9:557-568.
43. Schneider S., Herrenknecht K., Butz S., Kemler R., Hausen P. Catenins in Xenopus embryogenesis and their relation to the cadherin-mediated cell-cell adhesion system. Development 1993, 118:629-640.
44. Shirayoshi Y., Hatta K., Hosoda M., Tsunasawa S., Sakiyama F., Takeichi M. Cadherin cell adhesion molecules with distinct binding specificities share a common structure. EMBO J. 1986, 5:2485-2488.
45. Shoval I., Ludwig A., Kalcheim C. Antagonistic roles of full-length N-cadherin and its soluble BMP cleavage product in neural crest delamination. Development 2007, 134:491-501.
46. Suzuki T., Ueda A., Kobayashi N., Yang J., Tomaru K., Yamamoto M., Takeno M., Ishigatsubo Y. Proteasome-dependent degradation of α-catenin is regulated by interaction with ARMc8α. Biochem. J. 2008, 411:581-591.
47. Taneyhill L.A. To adhere or not to adhere: the role of cadherins in neural crest development. Cell Adh. Migr. 2008, 2:223-230.
48. Taneyhill L.A., Adams M.S. Investigating regulatory factors and their DNA binding affinities through real time quantitative PCR (RT-QPCR) and chromatin immunoprecipitation (ChIP) assays. Meth. Cell Biol. 2008, 87:367-389.
49. Taneyhill L.A., Bronner-Fraser M. Dynamic alterations in gene expression after Wnt-mediated induction of avian neural crest. Mol. Biol. Cell 2005, 16:5283-5293.
50. Taneyhill L.A., Coles E.G., Bronner-Fraser M. Snail2 directly represses cadherin6B during epithelial-to-mesenchymal transitions of the neural crest. Development 2007, 134:1481-1490.
51. Thiery J.P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2002, 2:442-454.
52. Togashi H., Abe K., Mizoguchi A., Takaoka K., Chisaka O., Takeichi M. Cadherin regulates dendritic spine morphogenesis. Neuron 2002, 35:77-89.
53. Torres M., Stoykova A., Huber O., Chowdhury K., Bonaldo P., Mansouri A., Butz S., Kemler R., Gruss P. An alpha-E-catenin gene trap mutation defines its function in preimplantation development. PNAS 1997, 94:901-906.
54. Uchida N., Shimamura K., Miyatani S., Copeland N.G., Gilbert D.J., Jenkins N.A., Takeichi M. Mouse alpha N-catenin: two isoforms, specific expression in the nervous system, and chromosomal localization of the gene. Dev. Biol. 1994, 163:75-85.
55. Uemura M., Takeichi M. Alpha N-catenin deficiency causes defects in axon migration and nuclear organization in restricted regions of the mouse brain. Dev. Dyn. 2006, 235:2559-2566.
56. Volk T., Geiger B. A 135-kd membrane protein of intercellular adherens junctions. EMBO J. 1984, 3:2249-2260.
57. Wilkinson D.G. Whole mount in situ hybridization of vertebrate embryos. In situ hybridization 1992, 75-83. Oxford University Press, Oxford. D.G. Wilkinson (Ed.).
58. Wu S.Y., McClay D.R. The Snail repressor is required for PMC ingression in the sea urchin embryo. Development 2007, 134:1061-1070.
59. Yang J., Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 2008, 14:818-829.