What is bad in cancer is good in the embryo: Importance of EMT in neural crest development

Seminars in Cell and Developmental Biology

Volumn 23, Issue 3, 2012, Pages 320-332

  Kerosuo, Laura ^a   Bronner Fraser, Marianne ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Apicobasal polarity; Dorsal neural tube; EMT; Neural crest; Snail

Indexed keywords

CELL PROTEIN; REGULATOR PROTEIN;

BASEMENT MEMBRANE; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; GENE CONTROL; HUMAN; MULTIPOTENT STEM CELL; NEURAL CREST; NEURAL CREST CELL; NEUROEPITHELIUM; NONHUMAN; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION;

GASTROPODA;

EID: 84860367807     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2012.03.010     Document Type: Review

References (206)

1. Hay E. The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Developmental Dynamics 2005, 233:706-720.
2. Kalluri R., Weinberg R. The basics of epithelial-mesenchymal transition. The Journal of Clinical Investigation 2009, 119:1420-1428.
3. Acloque H., Adams M., Fishwick K., Bronner Fraser M., Nieto M.A. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. The Journal of Clinical Investigation 2009, 119:1438-1449.
4. Thiery J., Acloque H., Huang R.Y.J., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
5. Boutet A., Esteban M., Maxwell P., Nieto M.A. Reactivation of Snail genes in renal fibrosis and carcinomas: a process of reversed embryogenesis. Cell Cycle 2007, 6:638-642.
6. Sauka-Spengler T., Meulemans D., Jones M., Bronner-Fraser M. Ancient evolutionary origin of the neural crest gene regulatory network. Developmental Cell 2007, 13:405-420.
7. Meulemans D., Bronner-Fraser M. Gene-regulatory interactions in neural crest evolution and development. Developmental Cell 2004, 7:291-299.
8. Betancur P., Bronner-Fraser M., Sauka-Spengler T. Assembling neural crest regulatory circuits into a gene regulatory network. Annual Review of Cell and Developmental Biology 2010, 26:581-603.
9. Sauka-Spengler T., Bronner-Fraser M. A gene regulatory network orchestrates neural crest formation. Nature Reviews Molecular Cell Biology 2008, 9:557-568.
10. Nelms B., Labosky P.A. Transcriptional control of neural crest development 2010, Morgan & Claypool Life Sciences, San Rafael, CA.
11. Basch M.L., Bronner-Fraser M., Garcia-Castro M.I. Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 2006, 441:218-222.
12. Ezin A., Fraser S., Bronner-Fraser M. Fate map and morphogenesis of presumptive neural crest and dorsal neural tube. Developmental Biology 2009, 330:221-236.
13. Liem K.F., Tremml G., Roelink H., Jessell T.M. Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 1995, 82:969-979.
14. Liu J.P., Jessell T.M. A role for rhoB in the delamination of neural crest cells from the dorsal neural tube. Development 1998, 125:5055-5067.
15. Garcia-Castro M., Marcelle C., Bronner-Fraser M. Ectodermal Wnt function as a neural crest inducer. Science 2002, 297:848-851.
16. Lewis J., Bonner J., Modrell M., Ragland J., Moon R., Dorsky R., et al. Reiterated Wnt signaling during zebrafish neural crest development. Development 2004, 131:1299-1308.
17. LaBonne C., Bronner-Fraser M. Neural crest induction in Xenopus: evidence for a two-signal model. Development 1998, 125:2403-2414.
18. Monsoro-Burq A.-H., Fletcher R., Harland R. Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. Development 2003, 130:3111-3124.
19. Monsoro-Burq A.-H., Wang E., Harland R. Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction. Developmental Cell 2005, 8:167-178.
20. Sato T., Sasai N., Sasai Y. Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development 2005, 132:2355-2363.
21. Hong C.-S., Saint-Jeannet J.-P. The activity of Pax3 and Zic1 regulates three distinct cell fates at the neural plate border. Molecular Biology of the Cell 2007, 18:2192-2202.
22. Mansouri A., Stoykova A., Torres M., Gruss P. Dysgenesis of cephalic neural crest derivatives in Pax7-/- mutant mice. Development 1996, 122:831-838.
23. Zhou H.-M., Wang J., Rogers R., Conway S. Lineage-specific responses to reduced embryonic Pax3 expression levels. Developmental Biology 2008, 315:369-382.
24. Aybar M., Nieto M.A., Mayor R. Snail precedes slug in the genetic cascade required for the specification and migration of the Xenopus neural crest. Development 2003, 130:483-494.
25. Osrio L., Teillet M.-A., Palmeirim I., Catala M. Neural crest ontogeny during secondary neurulation: a gene expression pattern study in the chick embryo. The International Journal of Developmental Biology 2009, 53:641-648.
26. Kuriyama S., Mayor R. Molecular analysis of neural crest migration. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 2008, 363:1349-1362.
27. Nieto M.A. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annual Review of Cell and Developmental Biology 2011, 27:347-376.
28. Etienne-Manneville S. Control of polarized cell morphology and motility by adherens junctions. Seminars in Cell & Developmental Biology 2011, 22:850-857.
29. Yamada S., Pokutta S., Drees F., Weis W., Nelson W.J. Deconstructing the cadherin-catenin-actin complex. Cell 2005, 123:889-901.
30. Takeichi M. The cadherins-cell-cell adhesion molecules controlling animal morphogenesis. Development 1988, 102:639-655.
31. Hatta K., Takagi S., Fujisawa H., Takeichi M. Spatial and temporal expression pattern of N-cadherin cell-adhesion molecules correlated with morphogenetic processes of chicken embryos. Developmental Biology 1987, 120:215-227.
32. Cano A., Perez-Moreno M.A., Rodrigo I., Locascio A., Blanco M.J., del Barrio M.G., et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nature Cell Biology 2000, 2:76-83.
33. Nakagawa S., Takeichi M. Neural crest cell-cell adhesion controlled by sequential and subpopulation-specific expression of novel cadherins. Development 1995, 121:1321-1332.
34. Akitaya T., Bronner-Fraser M. Expression of cell adhesion molecules during initiation and cessation of neural crest cell migration. Developmental Dynamics 1992, 194:12-20.
35. Park K.S., Gumbiner B.M. Cadherin 6B induces BMP signaling and de-epithelialization during the epithelial mesenchymal transition of the neural crest. Development 2010, 137:2691-2701.
36. Nakagawa S., Takeichi M. Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 1998, 125:2963-2971.
37. Inoue T., Chisaka O., Matsunami H., Takeichi M. Cadherin-6 expression transiently delineates specific rhombomeres, other neural tube subdivisions, and neural crest subpopulations in mouse embryos. Developmental Biology 1997, 183:183-194.
38. 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.
39. Cheung M., Chaboissier M.-C., Mynett A., Hirst E., Schedl A., Briscoe J. The transcriptional control of trunk neural crest induction, survival, and delamination. Developmental Cell 2005, 8:179-192.
40. Theveneau E., Marchant L., Kuriyama S., Gull M., Moepps B., Parsons M., et al. Collective chemotaxis requires contact-dependent cell polarity. Developmental Cell 2010, 19:39-53.
41. Monier Gavelle F., Duband J.L. Cross talk between adhesion molecules: control of N-cadherin activity by intracellular signals elicited by beta1 and beta3 integrins in migrating neural crest cells. The Journal of Cell Biology 1997, 137:1663-1681.
42. 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.
43. Coles E.G., Taneyhill L.A., Bronner-Fraser M. A critical role for Cadherin6B in regulating avian neural crest emigration. Developmental Biology 2007, 312:533-544.
44. Hadeball B., Borchers A., Wedlich D. Xenopus cadherin-11 (Xcadherin-11) expression requires the Wg/Wnt signal. Mechanisms of Development 1998, 72:101-113.
45. Borchers A., David R., Wedlich D. Xenopus cadherin-11 restrains cranial neural crest migration and influences neural crest specification. Development 2001, 128:3049-3060.
46. Vallin J., Girault J.M., Thiery J.P., Broders F. Xenopus cadherin-11 is expressed in different populations of migrating neural crest cells. Mechanisms of Development 1998, 75:171-174.
47. Wheeler A., Ridley A. Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility. Experimental Cell Research 2004, 301:43-49.
48. Liu A.X., Rane N., Liu J.P., Prendergast G.C. RhoB is dispensable for mouse development, but it modifies susceptibility to tumor formation as well as cell adhesion and growth factor signaling in transformed cells. Molecular and Cellular Biology 2001, 21:6906-6912.
49. Groysman M., Shoval I., Kalcheim C. A negative modulatory role for rho and rho-associated kinase signaling in delamination of neural crest cells. Neural Development 2008, 3.
50. Nakaya Y., Sukowati E.W., Wu Y., Sheng G. RhoA and microtubule dynamics control cell-basement membrane interaction in EMT during gastrulation. Nature Cell Biology 2008, 10:765-775.
51. Rupp P., Kulesa P. A role for RhoA in the two-phase migratory pattern of post-otic neural crest cells. Developmental Biology 2007, 311:159-171.
52. Rosso S., Sussman D., Wynshaw Boris A., Salinas P. Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nature Neuroscience 2005, 8:34-42.
53. Broders-Bondon F., Chesneau A., Romero-Oliva F., Mazabraud A., Mayor R., Thiery J.P. Regulation of XSnail2 expression by rho GTPases. Developmental Dynamics 2007, 236:2555-2566.
54. Smolen G., Schott B., Stewart R., Diederichs S., Muir B., Provencher H., et al. A Rap GTPase interactor, RADIL, mediates migration of neural crest precursors. Genes & Development 2007, 21:2131-2136.
55. del Barrio M., Nieto M.A. Overexpression of Snail family members highlights their ability to promote chick neural crest formation. Development 2002, 129:1583-1593.
56. Simard A., Di Pietro E., Ryan A. Gene expression pattern of Claudin-1 during chick embryogenesis. Gene Expression Patterns 2005, 5:553-560.
57. Aaku Saraste E., Hellwig A., Huttner W.B. Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure-remodeling of the neuroepithelium prior to neurogenesis. Developmental Biology 1996, 180:664-679.
58. Steed E., Balda M., Matter K. Dynamics and functions of tight junctions. Trends in Cell Biology 2010, 20:142-149.
59. Harris K., Tepass U. Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis. The Journal of Cell Biology 2008, 183:1129-1143.
60. Corbeil D., Marzesco A.-M., Wilsch-Bruninger M., Huttner W. The intriguing links between prominin-1 (CD133), cholesterol-based membrane microdomains, remodeling of apical plasma membrane protrusions, extracellular membrane particles, and (neuro)epithelial cell differentiation. FEBS Letters 2010, 584:1659-1664.
61. Marzesco A.-M., Janich P., Wilsch-Bräuninger M., Dubreuil V., Langenfeld K., Corbeil D., et al. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. Journal of Cell Science 2005, 118:2849-2858.
62. Röper K., Corbeil D., Huttner W.B. Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nature Cell Biology 2000, 2:582-592.
63. Decker R.S., Friend D.S. Assembly of gap junctions during amphibian neurulation. The Journal of Cell Biology 1974, 62:32-47.
64. Lo C.W., Cohen M.F., Huang G.Y., Lazatin B.O., Patel N., Sullivan R., et al. Cx43 gap junction gene expression and gap junctional communication in mouse neural crest cells. Developmental Genetics 1997, 20:119-132.
65. Cai D.H., Brauer P.R. Synthetic matrix metalloproteinase inhibitor decreases early cardiac neural crest migration in chicken embryos. Developmental Dynamics 2002, 224:441-449.
66. Alfandari D., Cousin H., Gaultier A., Smith K., White J.M., Darribre T., et al. Xenopus ADAM 13 is a metalloprotease required for cranial neural crest-cell migration. Current Biology 2001, 11:918-930.
67. Kee Y., Hwang B., Sternberg P., Bronner-Fraser M. Evolutionary conservation of cell migration genes: from nematode neurons to vertebrate neural crest. Genes & Development 2007, 21:391-396.
68. Lallier T., Bronner-Fraser M. Alpha 1 beta 1 integrin on neural crest cells recognizes some laminin substrata in a Ca(2+)-independent manner. The Journal of Cell Biology 1992, 119:1335-1345.
69. Strachan L., Condic M. Cranial neural crest recycle surface integrins in a substratum-dependent manner to promote rapid motility. The Journal of Cell Biology 2004, 167:545-554.
70. Alfandari D., Cousin H., Gaultier A., Hoffstrom B., DeSimone D. Integrin alpha5beta1 supports the migration of Xenopus cranial neural crest on fibronectin. Developmental Biology 2003, 260:449-464.
71. Breau M., Pietri T., Eder O., Blanche M., Brakebusch C., Fässler R., et al. Lack of beta1 integrins in enteric neural crest cells leads to a Hirschsprung-like phenotype. Development 2006, 133:1725-1734.
72. Perris R., Perissinotto D. Role of the extracellular matrix during neural crest cell migration. Mechanisms of Development 2000, 95:3-21.
73. Barembaum M., Moreno T.A., LaBonne C., Sechrist J., Bronner-Fraser M. Noelin-1 is a secreted glycoprotein involved in generation of the neural crest. Nature Cell Biology 2000, 2:219-225.
74. Endo Y., Osumi N., Wakamatsu Y. Bimodal functions of Notch-mediated signaling are involved in neural crest formation during avian ectoderm development. Development 2002, 129:863-873.
75. Coffman C.R., Skoglund P., Harris W.A., Kintner C.R. Expression of an extracellular deletion of Xotch diverts cell fate in Xenopus embryos. Cell 1993, 73:659-671.
76. Cornell R., Eisen J. Delta/Notch signaling promotes formation of zebrafish neural crest by repressing Neurogenin 1 function. Development 2002, 129:2639-2648.
77. Kanzler B., Foreman R.K., Labosky P.A., Mallo M. BMP signaling is essential for development of skeletogenic and neurogenic cranial neural crest. Development 2000, 127:1095-1104.
78. Burstyn-Cohen T., Stanleigh J., Sela-Donenfeld D., Kalcheim C. Canonical Wnt activity regulates trunk neural crest delamination linking BMP/noggin signaling with G1/S transition. Development 2004, 131:5327-5339.
79. Nguyen V.H., Schmid B., Trout J., Connors S.A., Ekker M., Mullins M.C. Ventral and lateral regions of the zebrafish gastrula, including the neural crest progenitors, are established by a bmp2b/swirl pathway of genes. Developmental Biology 1998, 199:93-110.
80. Sakai D., Tanaka Y., Endo Y., Osumi N., Okamoto H., Wakamatsu Y. Regulation of Slug transcription in embryonic ectoderm by beta-catenin-Lef/Tcf and BMP-Smad signaling. Development, Growth & Differentiation 2005, 47:471-482.
81. Steventon B., Araya C., Linker C., Kuriyama S., Mayor R. Differential requirements of BMP and Wnt signalling during gastrulation and neurulation define two steps in neural crest induction. Development 2009, 136:771-779.
82. Sela-Donenfeld D., Kalcheim C. Inhibition of noggin expression in the dorsal neural tube by somitogenesis: a mechanism for coordinating the timing of neural crest emigration. Development 2000, 127:4845-4854.
83. Sela-Donenfeld D., Kalcheim C. Regulation of the onset of neural crest migration by coordinated activity of BMP4 and Noggin in the dorsal neural tube. Development 1999, 126:4749-4762.
84. Graham A., Francis West P., Brickell P., Lumsden A. The signalling molecule BMP4 mediates apoptosis in the rhombencephalic neural crest. Nature 1994, 372:684-686.
85. Vega S., Morales A., Ocaa O., Valds F., Fabregat I., Nieto M.A. Snail blocks the cell cycle and confers resistance to cell death. Genes & Development 2004, 18:1131-1143.
86. Martinez-Morales P., Diez Del Corral R., Olivera-Martnez I., Quiroga A., Das R., Barbas J., et al. FGF and retinoic acid activity gradients control the timing of neural crest cell emigration in the trunk. The Journal of Cell Biology 2011, 194:489-503.
87. Guemar L., de Santa Barbara P., Vignal E., Maurel B., Fort P., Faure S. The small GTPase RhoV is an essential regulator of neural crest induction in Xenopus. Developmental Biology 2007, 310:113-128.
88. Taneyhill L., Bronner-Fraser M. Dynamic alterations in gene expression after Wnt-mediated induction of avian neural crest. Molecular Biology of the Cell 2005, 16:5283-5293.
89. Coles E., Christiansen J., Economou A., Bronner-Fraser M., Wilkinson D. A vertebrate crossveinless 2 homologue modulates BMP activity and neural crest cell migration. Development 2004, 131:5309-5317.
90. Vallin J., Thuret R., Giacomello E., Faraldo M.M., Thiery J.P., Broders F. Cloning and characterization of three Xenopus slug promoters reveal direct regulation by Lef/beta-catenin signaling. Journal of Biological Chemistry 2001, 276:30350-30358.
91. Safina A., Varga A., Bianchi A., Zheng Q., Kunnev D., Liang P., et al. Ras alters epithelial-mesenchymal transition in response to TGFbeta by reducing actin fibers and cell-matrix adhesion. Cell Cycle 2009, 8:284-298.
92. Oft M., Peli J., Rudaz C., Schwarz H., Beug H., Reichmann E. TGF-beta1 Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes & Development 1996, 10:2462-2477.
93. Sato M., Muragaki Y., Saika S., Roberts A., Ooshima A. Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. The Journal of Clinical Investigation 2003, 112:1486-1494.
94. Scheel C., Eaton E., Li S., Chaffer C., Reinhardt F., Kah K.-J., et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011, 145:926-940.
95. Nieto M.A. The snail superfamily of zinc-finger transcription factors. Nature Reviews Molecular Cell Biology 2002, 3:155-166.
96. Chea H., Wright C., Swalla B. Nodal signaling and the evolution of deuterostome gastrulation. Developmental Dynamics 2005, 234:269-278.
97. Ciruna B., Rossant J. FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Developmental Cell 2001, 1:37-49.
98. Gouti M., Briscoe J., Gavalas A. Anterior Hox genes interact with components of the neural crest specification network to induce neural crest fates. Stem Cells 2011, 29:858-870.
99. Luo T., Lee Y.-H., Saint-Jeannet J.-P., Sargent T. Induction of neural crest in Xenopus by transcription factor AP2alpha. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:532-537.
100. Mani S., Guo W., Liao M.-J., Eaton E., Ayyanan A., Zhou A., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
101. LaBonne C., Bronner-Fraser M. Snail-related transcriptional repressors are required in Xenopus for both the induction of the neural crest and its subsequent migration. Developmental Biology 2000, 221:195-205.
102. Nieto M.A., Bennett M.F., Sargent M.G., Wilkinson D.G. Cloning and developmental expression of Sna, a murine homologue of the Drosophila snail gene. Development 1992, 116:227-237.
103. 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.
104. Sefton M., Sanchez S., Nieto M.A. Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo. Development 1998, 125:3111-3121.
105. Carl T.F., Dufton C., Hanken J., Klymkowsky M.W. Inhibition of neural crest migration in Xenopus using antisense slug RNA. Developmental Biology 1999, 213:101-115.
106. Murray S., Oram K., Gridley T. Multiple functions of Snail family genes during palate development in mice. Development 2007, 134:1789-1797.
107. Blanco M., Barrallo Gimeno A., Acloque H., Reyes A., Tada M., Allende M., et al. Snail1a and Snail1b cooperate in the anterior migration of the axial mesendoderm in the zebrafish embryo. Development 2007, 134:4073-4081.
108. Thisse C., Thisse B., Postlethwait J.H. Expression of snail2, a second member of the zebrafish snail family, in cephalic mesendoderm and presumptive neural crest of wild-type and spadetail mutant embryos. Developmental Biology 1995, 172:86-99.
109. Bolos V., Peinado H., Perez-Moreno M., Fraga M., 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. Journal of Cell Science 2003, 116:499-511.
110. Batlle E., Sancho E., Franc C., Dominguez D., Monfar M., Baulida J., et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nature Cell Biology 2000, 2:84-89.
111. Boutet A., De Frutos C., Maxwell P., Mayol M.J., Romero J., Nieto M.A. Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney. EMBO Journal 2006, 25:5603-5613.
112. Jhingory S., Wu C.Y., Taneyhill L.A. Novel insight into the function and regulation of alphaN-catenin by Snail2 during chick neural crest cell migration. Developmental Biology 2010, 344:896-910.
113. Ikenouchi J., Matsuda M., Furuse M., Tsukita S. Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail. Journal of Cell Science 2003, 116:1959-1967.
114. Whiteman E.L., Liu C.J., Fearon E.R., Margolis B. The transcription factor snail represses Crumbs3 expression and disrupts apico-basal polarity complexes. Oncogene 2008, 27:3875-3879.
115. Langer E., Feng Y., Zhaoyuan H., Rauscher F., Kroll K., Longmore G. Ajuba LIM proteins are snail/slug corepressors required for neural crest development in Xenopus. Developmental Cell 2008, 14:424-436.
116. Casas E., Kim J., Bendesky A., Ohno Machado L., Wolfe C., Yang J. Snail2 is an essential mediator of Twist1-induced epithelial mesenchymal transition and metastasis. Cancer Research 2011, 71:245-254.
117. Dottori M., Gross M.K., Labosky P., Goulding M. The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate. Development 2001, 128:4127-4138.
118. Yamagata M., Noda M. The winged-helix transcription factor CWH-3 is expressed in developing neural crest cells. Neuroscience Letters 1998, 249:33-36.
119. Labosky P.A., Kaestner K.H. The winged helix transcription factor Hfh2 is expressed in neural crest and spinal cord during mouse development. Mechanisms of Development 1998, 76:185-190.
120. Hromas R., Ye H., Spinella M., Dmitrovsky E., Xu D., Costa R.H. Genesis, a Winged Helix transcriptional repressor, has embryonic expression limited to the neural crest, and stimulates proliferation in vitro in a neural development model. Cell and Tissue Research 1999, 297:371-382.
121. Lister J., Cooper C., Nguyen K., Modrell M., Grant K., Raible D. Zebrafish Foxd3 is required for development of a subset of neural crest derivatives. Developmental Biology 2006, 290:92-104.
122. Stewart R., Arduini B., Berghmans S., George R., Kanki J., Henion P., et al. Zebrafish foxd3 is selectively required for neural crest specification, migration and survival. Developmental Biology 2006, 292:174-188.
123. Kos R., Reedy M.V., Johnson R.L., Erickson C.A. The winged-helix transcription factor FoxD3 is important for establishing the neural crest lineage and repressing melanogenesis in avian embryos. Development 2001, 128:1467-1479.
124. Theveneau E., Duband J.-L., Altabef M. Ets-1 confers cranial features on neural crest delamination. PLoS ONE 2007, 2:e1142-e1150.
125. Comijn J., Berx G., Vermassen P., Verschueren K., van Grunsven L., Bruyneel E., et al. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Molecular Cell 2001, 7:1267-1278.
126. Vandewalle C., Comijn J., De Craene B., Vermassen P., Bruyneel E., Andersen H., et al. SIP1/ZEB2 induces EMT by repressing genes of different epithelial cell-cell junctions. Nucleic Acids Research 2005, 33:6566-6578.
127. Bracken C., Gregory P., Kolesnikoff N., Bert A., Wang J., Shannon M.F., et al. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Research 2008, 68:7846-7854.
128. van Grunsven L.A., Papin C., Avalosse B., Opdecamp K., Huylebroeck D., Smith J.C., et al. XSIP1, a Xenopus zinc finger/homeodomain encoding gene highly expressed during early neural development. Mechanisms of Development 2000, 94:189-193.
129. van Grunsven L., Taelman V., Michiels C., Opdecamp K., Huylebroeck D., Bellefroid E. deltaEF1 and SIP1 are differentially expressed and have overlapping activities during Xenopus embryogenesis. Developmental Dynamics 2006, 235:1491-1500.
130. Van de Putte T., Maruhashi M., Francis A., Nelles L., Kondoh H., Huylebroeck D., et al. Mice lacking ZFHX1B, the gene that codes for Smad-interacting protein-1, reveal a role for multiple neural crest cell defects in the etiology of Hirschsprung disease-mental retardation syndrome. American Journal of Human Genetics 2003, 72:465-470.
131. Maka M., Stolt C.C., Wegner M. Identification of Sox8 as a modifier gene in a mouse model of Hirschsprung disease reveals underlying molecular defect. Developmental Biology 2005, 277:155-169.
132. Reiprich S., Stolt C.C., Schreiner S., Parlato R., Wegner M. SoxE proteins are differentially required in mouse adrenal gland development. Molecular Biology of the Cell 2008, 19:1575-1586.
133. Kelsh R.N. Sorting out Sox10 functions in neural crest development. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 2006, 28:788-798.
134. Britsch S., Goerich D.E., Riethmacher D., Peirano R.I., Rossner M., Nave K.A., et al. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes & Development 2001, 15:66-78.
135. Mori-Akiyama Y., Akiyama H., Rowitch D., de Crombrugghe B. Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:9360-9365.
136. Cheung M., Briscoe J. Neural crest development is regulated by the transcription factor Sox9. Development 2003, 130:5681-5693.
137. O'Donnell M., Hong C.-S., Huang X., Delnicki R., Saint-Jeannet J.-P. Functional analysis of Sox8 during neural crest development in Xenopus. Development 2006, 133:3817-3826.
138. Sakai D., Suzuki T., Osumi N., Wakamatsu Y. Cooperative action of Sox9, Snail2 and PKA signaling in early neural crest development. Development 2006, 133:1323-1333.
139. Lee Y.-H., Aoki Y., Hong C.-S., Saint Germain N., Credidio C., Saint Jeannet J.-P. Early requirement of the transcriptional activator Sox9 for neural crest specification in Xenopus. Developmental Biology 2004, 275:93-103.
140. Spokony R., Aoki Y., Saint Germain N., Magner Fink E., Saint-Jeannet J.-P. The transcription factor Sox9 is required for cranial neural crest development in Xenopus. Development 2002, 129:421-432.
141. Betancur P., Bronner-Fraser M., Sauka-Spengler T. Genomic code for Sox10 activation reveals a key regulatory enhancer for cranial neural crest. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:3570-3575.
142. Taylor K.M., LaBonne C. SoxE factors function equivalently during neural crest and inner ear development and their activity is regulated by SUMOylation. Developmental Cell 2005, 9:593-603.
143. Kim J., Lo L., Dormand E., Anderson D. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 2003, 38:17-31.
144. Elworthy S., Lister J.A., Carney T.J., Raible D.W., Kelsh R.N. Transcriptional regulation of mitfa accounts for the sox10 requirement in zebrafish melanophore development. Development 2003, 130:2809-2818.
145. Aoki Y., Saint Germain N., Gyda M., Magner Fink E., Lee Y.H. Sox10 regulates the development of neural crest-derived melanocytes in Xenopus. Developmental Biology 2003, 259:19-33.
146. McKeown S., Lee V., Bronner-Fraser M., Newgreen D., Farlie P. Sox10 overexpression induces neural crest-like cells from all dorsoventral levels of the neural tube but inhibits differentiation. Developmental Dynamics 2005, 233:430-444.
147. Honore S., Aybar M., Mayor R. Sox10 is required for the early development of the prospective neural crest in Xenopus embryos. Developmental Biology 2003, 260:79-96.
148. Perez-Alcala S., Nieto M.A., Barbas J. LSox5 regulates RhoB expression in the neural tube and promotes generation of the neural crest. Development 2004, 131:4455-4465.
149. Stolt C.C., Lommes P., Hillgrtner S., Wegner M. The transcription factor Sox5 modulates Sox10 function during melanocyte development. Nucleic Acids Research 2008, 36:5427-5440.
150. Liu Y., Labosky P. Regulation of embryonic stem cell self-renewal and pluripotency by Foxd3. Stem Cells 2008, 26:2475-2484.
151. Hanna L., Foreman R., Tarasenko I., Kessler D., Labosky P. Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes & Development 2002, 16:2650-2661.
152. Tompers D., Foreman R., Wang Q., Kumanova M., Labosky P. Foxd3 is required in the trophoblast progenitor cell lineage of the mouse embryo. Developmental Biology 2005, 285:126-137.
153. Teng L., Mundell N., Frist A., Wang Q., Labosky P. Requirement for Foxd3 in the maintenance of neural crest progenitors. Development 2008, 135:1615-1624.
154. Montero-Balaguer M., Lang M., Sachdev S., Knappmeyer C., Stewart R., De La Guardia A., et al. The mother superior mutation ablates foxd3 activity in neural crest progenitor cells and depletes neural crest derivatives in zebrafish. Developmental Dynamics 2006, 235:3199-3212.
155. Mundell N., Labosky P. Neural crest stem cell multipotency requires Foxd3 to maintain neural potential and repress mesenchymal fates. Development 2011, 138:641-652.
156. Curran K., Lister J., Kunkel G., Prendergast A., Parichy D., Raible D. Interplay between Foxd3 and Mitf regulates cell fate plasticity in the zebrafish neural crest. Developmental Biology 2010, 344:107-118.
157. Sasai N., Mizuseki K., Sasai Y. Requirement of FoxD3-class signaling for neural crest determination in Xenopus. Development 2001, 128:2525-2536.
158. Zhang C., Carl T.F., Trudeau E.D., Simmet T., Klymkowsky M.W. An NF-kappa B and slug regulatory loop active in early vertebrate mesoderm. PLoS ONE 2006, 1.
159. Linker C., Bronner Fraser M., Mayor R. Relationship between gene expression domains of Xsnail, Xslug, and Xtwist and cell movement in the prospective neural crest of Xenopus. Developmental Biology 2000, 224:215-225.
160. Ansieau S., Morel A.P., Hinkal G., Bastid J., Puisieux A. TWISTing an embryonic transcription factor into an oncoprotein. Oncogene 2010, 29:3173-3184.
161. Tribulo C., Aybar M., Sanchez S., Mayor R. A balance between the anti-apoptotic activity of Slug and the apoptotic activity of msx1 is required for the proper development of the neural crest. Developmental Biology 2004, 275:325-342.
162. Eilers M., Eisenman R. Myc's broad reach. Genes & Development 2008, 22:2755-2766.
163. Bellmeyer A., Krase J., Lindgren J., LaBonne C. The protooncogene c-myc is an essential regulator of neural crest formation in xenopus. Developmental Cell 2003, 4:827-839.
164. Light W., Vernon A., Lasorella A., Iavarone A., LaBonne C. Xenopus Id3 is required downstream of Myc for the formation of multipotent neural crest progenitor cells. Development 2005, 132:1831-1841.
165. Kee Y., Bronner-Fraser M. To proliferate or to die: role of Id3 in cell cycle progression and survival of neural crest progenitors. Genes & Development 2005, 19:744-755.
166. Khudyakov J., Bronner-Fraser M. Comprehensive spatiotemporal analysis of early chick neural crest network genes. Developmental Dynamics 2009, 238:716-723.
167. Malynn B.A., de Alboran I.M., O'Hagan R.C., Bronson R., Davidson L., DePinho R.A., et al. N-myc can functionally replace c-myc in murine development, cellular growth, and differentiation. Genes & Development 2000, 14:1390-1399.
168. Kerosuo L., Piltti K., Fox H., Angers-Loustau A., Häyry V., Eilers M., et al. Myc increases self-renewal in neural progenitor cells through Miz-1. Journal of Cell Science 2008, 121:3941-3950.
169. Nagao M., Campbell K., Burns K., Kuan C.-Y., Trumpp A., Nakafuku M. Coordinated control of self-renewal and differentiation of neural stem cells by Myc and the p19ARF-p53 pathway. The Journal of Cell Biology 2008, 183:1243-1257.
170. Knoepfler P., Cheng P., Eisenman R. N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes & Development 2002, 16:2699-2712.
171. Rinon A., Molchadsky A., Nathan E., Yovel G., Rotter V., Sarig R., et al. p53 coordinates cranial neural crest cell growth and epithelial-mesenchymal transition/delamination processes. Development 2011, 138:1827-1838.
172. Piltti K., Kerosuo L., Hakanen J., Eriksson M., Angers-Loustau A., Lepp S., et al. E6/E7 oncogenes increase and tumor suppressors decrease the proportion of self-renewing neural progenitor cells. Oncogene 2006, 25:4880-4889.
173. Zheng H., Ying H., Yan H., Kimmelman A., Hiller D., Chen A.-J., et al. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008, 455:1129-1133.
174. Chylicki K., Ehinger M., Svedberg H., Gullberg U. Characterization of the molecular mechanisms for p53-mediated differentiation. Cell Growth & Differentiation 2000, 11:561-571.
175. Galderisi U., Jori F., Giordano A. Cell cycle regulation and neural differentiation. Oncogene 2003, 22:5208-5219.
176. Wakamatsu Y., Watanabe Y., Nakamura H., Kondoh H. Regulation of the neural crest cell fate by N-myc: promotion of ventral migration and neuronal differentiation. Development 1997, 124:1953-1962.
177. Strobl-Mazzulla P.H., Sauka-Spengler T., Bronner-Fraser M. Histone demethylase JmjD2A regulates neural crest specification. Developmental Cell 2010, 19:460-468.
178. Corry G., Hendzel M., Underhill D.A. Subnuclear localization and mobility are key indicators of PAX3 dysfunction in Waardenburg syndrome. Human Molecular Genetics 2008, 17:1825-1837.
179. Herranz N., Pasini D., Daz V., Franc C., Gutierrez A., Dave N., et al. Polycomb complex 2 is required for E-cadherin repression by the Snail1 transcription factor. Molecular and Cellular Biology 2008, 28:4772-4781.
180. Peinado H., Ballestar E., Esteller M., Cano A. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Molecular and Cellular Biology 2004, 24:306-319.
181. Yaklichkin S., Steiner A., Lu Q., Kessler D. FoxD3 and Grg4 physically interact to repress transcription and induce mesoderm in Xenopus. Journal of Biological Chemistry 2007, 282:2548-2557.
182. Xu J., Watts J., Pope S., Gadue P., Kamps M., Plath K., et al. Transcriptional competence and the active marking of tissue-specific enhancers by defined transcription factors in embryonic and induced pluripotent stem cells. Genes & Development 2009, 23:2824-2838.
183. Guccione E., Martinato F., Finocchiaro G., Luzi L., Tizzoni L., Dall' Olio V., et al. Myc-binding-site recognition in the human genome is determined by chromatin context. Nature Cell Biology 2006, 8:764-770.
184. Knoepfler P., Zhang X.-y., Cheng P., Gafken P., McMahon S., Eisenman R. Myc influences global chromatin structure. EMBO Journal 2006, 25:2723-2734.
185. Gerlitz G., Bustin M. Efficient cell migration requires global chromatin condensation. Journal of Cell Science 2010, 123:2207-2217.
186. Lander R., Nordin K., Labonne C. The F-box protein Ppa is a common regulator of core EMT factors Twist, Snail, Slug, and Sip1. The Journal of Cell Biology 2011, 194:17-25.
187. Vernon A., LaBonne C. Slug stability is dynamically regulated during neural crest development by the F-box protein Ppa. Development 2006, 133:3359-3370.
188. Vinas-Castells R., Beltran M., Valls G., Gomez I., Garcia J., Montserrat-Sents B., et al. The hypoxia-controlled FBXL14 ubiquitin ligase targets SNAIL1 for proteasome degradation. Journal of Biological Chemistry 2010, 285:3794-3805.
189. Girard M., Goossens M. Sumoylation of the SOX10 transcription factor regulates its transcriptional activity. FEBS Letters 2006, 580:1635-1641.
190. Betancur P., Sauka Spengler T., Bronner M. A Sox10 enhancer element common to the otic placode and neural crest is activated by tissue-specific paralogs. Development 2011, 138:3689-3698.
191. Gupta V., Bei M. Modification of Msx1 by SUMO-1. Biochemical and Biophysical Research Communications 2006, 345:74-77.
192. Polyak K., Weinberg R. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nature Reviews Cancer 2009, 9:265-273.
193. Brabletz S., Brabletz T. The ZEB/miR-200 feedback loop-a motor of cellular plasticity in development and cancer. EMBO Reports 2010, 11:670-677.
194. Wellner U., Schubert J., Burk U., Schmalhofer O., Zhu F., Sonntag A., et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nature Cell Biology 2009, 11:1487-1495.
195. Warzecha C., Jiang P., Amirikian K., Dittmar K., Lu H., Shen S., et al. An ESRP-regulated splicing programme is abrogated during the epithelial-mesenchymal transition. EMBO Journal 2010, 29:3286-3300.
196. Nakaya Y., Sheng G. An amicable separation: Chick's way of doing EMT. Cell Adhesion & Migration 2009, 3:160-163.
197. Erickson C.A., Reedy M.V. Neural crest development: the interplay between morphogenesis and cell differentiation. Current Topics in Developmental Biology 1998, 40:177-209.
198. Bilozur M.E., Hay E.D. Cell migration into neural tube lumen provides evidence for the fixed cortex theory of cell motility. Cell Motility and the Cytoskeleton 1989, 14:469-484.
199. Burstyn-Cohen T., Kalcheim C. Association between the cell cycle and neural crest delamination through specific regulation of G1/S transition. Developmental Cell 2002, 3:383-395.
200. 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.
201. 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.
202. Kasemeier-Kulesa J., Bradley R., Pasquale E., Lefcort F., Kulesa P. Eph/ephrins and N-cadherin coordinate to control the pattern of sympathetic ganglia. Development 2006, 133:4839-4847.
203. Duband J.L., Tucker G.C., Poole T.J., Vincent M., Aoyama H., Thiery J.P. How do the migratory and adhesive properties of the neural crest govern ganglia formation in the avian peripheral nervous system. Journal of Cellular Biochemistry 1985, 27:189-203.
204. Nguyen D., Bos P., Massague J. Metastasis: from dissemination to organ-specific colonization. Nature Reviews Cancer 2009, 9:274-284.
205. Wells A., Yates C., Shepard C. E-cadherin as an indicator of mesenchymal to epithelial reverting transitions during the metastatic seeding of disseminated carcinomas. Clinical & Experimental Metastasis 2008, 25:621-628.
206. Peiró S., Escrivà M., Puig I., Barberà M.J., Dave N., Herranz N., Larriba M.J., Takkunen M., Francí C., Muñoz A., Virtanen I., Baulida J., García de Herreros A. Snail1 transcriptional repressor binds to its own promoter and controls its expression. Nucleic Acids Research 2006, 34(7):2077-2084.