The hypoxia factor Hif-1α controls neural crest chemotaxis and epithelial to mesenchymal transition

Journal of Cell Biology

Volumn 201, Issue 5, 2013, Pages 759-776

  Barriga, Elias H ^a,b   Maxwell, Patrick H ^a   Reyes, Ariel E ^b,c   Mayor, Roberto ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSIDAD ANDRÉS BELLO   (Chile)

^c Interdisciplinary Center for Aquaculture Research   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; HYPOXIA INDUCIBLE FACTOR 1ALPHA; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR TWIST; UVOMORULIN;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL POPULATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; METASTASIS; NEURAL CREST; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; XENOPUS LAEVIS; ZEBRA FISH;

ANIMALS; CELL HYPOXIA; CHEMOTAXIS; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; NEURAL CREST; RECEPTORS, CXCR4; TWIST TRANSCRIPTION FACTOR; XENOPUS LAEVIS; ZEBRAFISH;

DANIO RERIO; XENOPUS LAEVIS;

EID: 84878544545     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201212100     Document Type: Article

References (92)

1. Akimenko, M.A., M. Ekker, J. Wegner, W. Lin, and M. Westerfield. 1994. Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J. Neurosci. 14:3475-3486.
2. Alfandari, D., H. Cousin, A. Gaultier, B.G. Hoffstrom, and D.W. DeSimone. 2003. Integrin alpha5beta1 supports the migration of Xenopus cranial neural crest on fibronectin. Dev. Biol. 260:449-464. http://dx.doi.org/10.1016/S0012-1606(03)00277-X
3. Aybar, M.J., M.A. Nieto, and R. Mayor. 2003. Snail precedes slug in the genetic cascade required for the specification and migration of the Xenopus neural crest. Development. 130:483-494. http://dx.doi.org/10.1242/dev.00238
4. Barrallo-Gimeno, A., and M.A. Nieto. 2005. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development. 132:3151-3161. http://dx.doi.org/10.1242/dev.01907
5. Barrallo-Gimeno, A., J. Holzschuh, W. Driever, and E.W. Knapik. 2004. Neural crest survival and differentiation in zebrafish depends on mont blanc/tfap2a gene function. Development. 131:1463-1477. http://dx.doi.org/10.1242/dev.01033
6. Betancur, P., M. Bronner-Fraser, and T. Sauka-Spengler. 2010. Assembling neural crest regulatory circuits into a gene regulatory network. Annu. Rev. Cell Dev. Biol. 26:581-603. http://dx.doi.org/10.1146/annurev.cellbio.042308.113245
7. Bildsoe, H., D.A. Loebel, V.J. Jones, Y.T. Chen, R.R. Behringer, and P.P. Tam. 2009. Requirement for Twist1 in frontonasal and skull vault development in the mouse embryo. Dev. Biol. 331:176-188. http://dx.doi.org/10.1016/j.ydbio.2009.04.034
8. Breau, M.A., T. Pietri, M.P. Stemmler, J.P. Thiery, and J.A. Weston. 2008. A nonneural epithelial domain of embryonic cranial neural folds gives rise to ectomesenchyme. Proc. Natl. Acad. Sci. USA. 105:7750-7755. http://dx.doi.org/10.1073/pnas.0711344105
9. Cacheux, V., F. Dastot-Le Moal, H. Kääriänen, N. Bondurand, R. Rintala, B. Boissier, M. Wilson, D. Mowat, and M. Goossens. 2001. Loss-offunction mutations in SIP1 Smad interacting protein 1 result in a syndromic Hirschsprung disease. Hum. Mol. Genet. 10:1503-1510. http://dx.doi.org/10.1093/hmg/10.14.1503
10. Cairns, R.A., I.S. Harris, and T.W. Mak. 2011. Regulation of cancer cell metabolism. Nat. Rev. Cancer. 11:85-95. http://dx.doi.org/10.1038/nrc2981
11. Carmona-Fontaine, C., H.K. Matthews, S. Kuriyama, M. Moreno, G.A. Dunn, M. Parsons, C.D. Stern, and R. Mayor. 2008. Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature. 456:957-961. http://dx.doi.org/10.1038/nature07441
12. Carmona-Fontaine, C., E. Theveneau, A. Tzekou, M. Tada, M. Woods, K.M. Page, M. Parsons, J.D. Lambris, and R. Mayor. 2011. Complement fragment C3a controls mutual cell attraction during collective cell migration. Dev. Cell. 21:1026-1037. http://dx.doi.org/10.1016/j.devcel.2011.10.012
13. Chang, Q., I. Jurisica, T. Do, and D.W. Hedley. 2011. Hypoxia predicts aggressive growth and spontaneous metastasis formation from orthotopically grown primary xenografts of human pancreatic cancer. Cancer Res. 71: 3110-3120. http://dx.doi.org/10.1158/0008-5472.CAN-10-4049
14. Chen, Z.F., and R.R. Behringer. 1995. twist is required in head mesenchyme for cranial neural tube morphogenesis. Genes Dev. 9:686-699. http://dx.doi.org/10.1101/gad.9.6.686
15. Chong, S.W., A. Emelyanov, Z. Gong, and V. Korzh. 2001. Expression pattern of two zebrafish genes, cxcr4a and cxcr4b. Mech. Dev. 109:347-354. http://dx.doi.org/10.1016/S0925-4773(01)00520-2
16. Cockman, M.E., N. Masson, D.R. Mole, P. Jaakkola, G.W. Chang, S.C. Clifford, E.R. Maher, C.W. Pugh, P.J. Ratcliffe, and P.H. Maxwell. 2000. Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J. Biol. Chem. 275:25733-25741. http://dx.doi.org/10.1074/jbc.M002740200
17. Compernolle, V., K. Brusselmans, D. Franco, A. Moorman, M. Dewerchin, D. Collen, and P. Carmeliet. 2003. Cardia bifida, defective heart development and abnormal neural crest migration in embryos lacking hypoxiainducible factor-1alpha. Cardiovasc. Res. 60:569-579. http://dx.doi.org/10.1016/j.cardiores.2003.07.003
18. Dady, A., C. Blavet, and J.L. Duband. 2012. Timing and kinetics of E- to N-cadherin switch during neurulation in the avian embryo. Dev. Dyn. 241:1333-1349. http://dx.doi.org/10.1002/dvdy.23813
19. de Beaucourt, A., and P. Coumailleau. 2007. Molecular cloning and characterization of the Xenopus hypoxia-inducible factor 1alpha (xHIF1alpha). J. Cell. Biochem. 102:1542-1552. http://dx.doi.org/10.1002/jcb.21376
20. De Calisto, J., C. Araya, L. Marchant, C.F. Riaz, and R. Mayor. 2005. Essential role of non-canonical Wnt signalling in neural crest migration. Development. 132:2587-2597. http://dx.doi.org/10.1242/dev.01857
21. DeSimone, D.W., L. Davidson, M. Marsden, and D. Alfandari. 2005. The Xenopus embryo as a model system for studies of cell migration. Methods Mol. Biol. 294:235-245.
22. Erler, J.T., C.J. Cawthorne, K.J. Williams, M. Koritzinsky, B.G. Wouters, C. Wilson, C. Miller, C. Demonacos, I.J. Stratford, and C. Dive. 2004. Hypoxia-mediated down-regulation of Bid and Bax in tumors occurs via hypoxia-inducible factor 1-dependent and -independent mechanisms and contributes to drug resistance. Mol. Cell. Biol. 24:2875-2889. http://dx.doi.org/10.1128/MCB.24.7.2875-2889.2004
23. Evans, A.J., R.C. Russell, O. Roche, T.N. Burry, J.E. Fish, V.W. Chow, W.Y. Kim, A. Saravanan, M.A. Maynard, M.L. Gervais, et al. 2007. VHL promotes E2 box-dependent E-cadherin transcription by HIF-mediated regulation of SIP1 and snail. Mol. Cell. Biol. 27:157-169. http://dx.doi.org/10.1128/MCB.00892-06
24. Gómez-Skarmeta, J.L., A. Glavic, E. de la Calle-Mustienes, J. Modolell, and R. Mayor. 1998. Xiro, a Xenopus homolog of the Drosophila Iroquois complex genes, controls development at the neural plate. EMBO J. 17:181- 190. http://dx.doi.org/10.1093/emboj/17.1.181
25. Gort, E.H., G. van Haaften, I. Verlaan, A.J. Groot, R.H. Plasterk, A. Shvarts, K.P. Suijkerbuijk, T. van Laar, E. van der Wall, V. Raman, et al. 2008. The TWIST1 oncogene is a direct target of hypoxia-inducible factor-2alpha. Oncogene. 27:1501-1510. http://dx.doi.org/10.1038/sj.onc.1210795
26. Graeber, T.G., C. Osmanian, T. Jacks, D.E. Housman, C.J. Koch, S.W. Lowe, and A.J. Giaccia. 1996. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature. 379:88-91. http://dx.doi.org/10.1038/379088a0
27. Gray, M.J., J. Zhang, L.M. Ellis, G.L. Semenza, D.B. Evans, S.S. Watowich, and G.E. Gallick. 2005. HIF-1alpha, STAT3, CBP/p300 and Ref-1/APE are components of a transcriptional complex that regulates Src-dependent hypoxia-induced expression of VEGF in pancreatic and prostate carcinomas. Oncogene. 24:3110-3120. http://dx.doi.org/10.1038/sj.onc.1208513
28. Gupta, G.P., and J. Massagué 2006. Cancer metastasis: building a framework. Cell. 127:679-695. http://dx.doi.org/10.1016/j.cell.2006.11.001
29. Harland, R.M. 1991. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36:685-695. http://dx.doi.org/10.1016/S0091-679X(08)60307-6
30. Harland, R., and H. Weintraub. 1985. Translation of mRNA injected into Xenopus oocytes is specifically inhibited by antisense RNA. J. Cell Biol. 101:1094-1099. http://dx.doi.org/10.1083/jcb.101.3.1094
31. Harris, A.L. 2002. Hypoxia-a key regulatory factor in tumour growth. Nat. Rev. Cancer. 2:38-47. http://dx.doi.org/10.1038/nrc704
32. Hendrix, M.J., E.A. Seftor, R.E. Seftor, J. Kasemeier-Kulesa, P.M. Kulesa, and L.M. Postovit. 2007. Reprogramming metastatic tumour cells with embryonic microenvironments. Nat. Rev. Cancer. 7:246-255. http://dx.doi.org/10.1038/nrc2108
33. Hill, R.P., D.T. Marie-Egyptienne, and D.W. Hedley. 2009. Cancer stem cells, hypoxia and metastasis. Semin. Radiat. Oncol. 19:106-111. http://dx.doi.org/10.1016/j.semradonc.2008.12.002
34. Hong, C.S., and J.P. Saint-Jeannet. 2007. The activity of Pax3 and Zic1 regulates three distinct cell fates at the neural plate border. Mol. Biol. Cell. 18:2192-2202. http://dx.doi.org/10.1091/mbc.E06-11-1047
35. Hopwood, N.D., A. Pluck, and J.B. Gurdon. 1989. A Xenopus mRNA related to Drosophila twist is expressed in response to induction in the mesoderm and the neural crest. Cell. 59:893-903. http://dx.doi.org/10.1016/0092-8674(89)90612-0
36. Ishii, M., A.E. Merrill, Y.S. Chan, I. Gitelman, D.P. Rice, H.M. Sucov, and R.E. Maxson Jr. 2003. Msx2 and Twist cooperatively control the development of the neural crest-derived skeletogenic mesenchyme of the murine skull vault. Development. 130:6131-6142. http://dx.doi.org/10.1242/dev.00793
37. Kamura, T., S. Sato, K. Iwai, M. Czyzyk-Krzeska, R.C. Conaway, and J.W. Conaway. 2000. Activation of HIF1alpha ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc. Natl. Acad. Sci. USA. 97:10430-10435. http://dx.doi.org/10.1073/pnas.190332597
38. Kelsh, R.N., K. Dutton, J. Medlin, and J.S. Eisen. 2000. Expression of zebrafish fkd6 in neural crest-derived glia. Mech. Dev. 93:161-164. http://dx.doi.org/10.1016/S0925-4773(00)00250-1
39. Kimmel, C.B., W.W. Ballard, S.R. Kimmel, B. Ullmann, and T.F. Schilling. 1995. Stages of embryonic development of the zebrafish. Dev. Dyn. 203:253-310. http://dx.doi.org/10.1002/aja.1002030302
40. Kioi, M., H. Vogel, G. Schultz, R.M. Hoffman, G.R. Harsh, and J.M. Brown. 2010. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J. Clin. Invest. 120:694-705. http://dx.doi.org/10.1172/JCI40283
41. Kirby, B.B., N. Takada, A.J. Latimer, J. Shin, T.J. Carney, R.N. Kelsh, and B. Appel. 2006. In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development. Nat. Neurosci. 9:1506-1511. http://dx.doi.org/10.1038/nn1803
42. Knight, R.D., S. Nair, S.S. Nelson, A. Afshar, Y. Javidan, R. Geisler, G.J. Rauch, and T.F. Schilling. 2003. lockjaw encodes a zebrafish tfap2a required for early neural crest development. Development. 130:5755-5768. http://dx.doi.org/10.1242/dev.00575
43. Koh, M.Y., and G. Powis. 2009. HAF: the new player in oxygen-independent HIF-1alpha degradation. Cell Cycle. 8:1359-1366. http://dx.doi.org/10.4161/cc.8.9.8303
44. Kucia, M., R. Reca, K. Miekus, J. Wanzeck, W. Wojakowski, A. Janowska-Wieczorek, J. Ratajczak, and M.Z. Ratajczak. 2005. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1-CXCR4 axis. Stem Cells. 23:879-894. http://dx.doi.org/10.1634/stemcells.2004-0342
45. Kulesa, P.M., J.C. Kasemeier-Kulesa, J.M. Teddy, N.V. Margaryan, E.A. Seftor, R.E. Seftor, and M.J. Hendrix. 2006. Reprogramming metastatic melanoma cells to assume a neural crest cell-like phenotype in an embryonic microenvironment. Proc. Natl. Acad. Sci. USA. 103:3752-3757. http://dx.doi.org/10.1073/pnas.0506977103
46. Kuriyama, S., and R. Mayor. 2008. Molecular analysis of neural crest migration. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363:1349-1362. http://dx.doi.org/10.1098/rstb.2007.2252
47. Linker, C., M. Bronner-Fraser, and R. Mayor. 2000. Relationship between gene expression domains of Xsnail, Xslug, and Xtwist and cell movement in the prospective neural crest of Xenopus. Dev. Biol. 224:215-225. http://dx.doi.org/10.1006/dbio.2000.9723
48. Locascio, A., M. Manzanares, M.J. Blanco, and M.A. Nieto. 2002. Modularity and reshuffling of Snail and Slug expression during vertebrate evolution. Proc. Natl. Acad. Sci. USA. 99:16841-16846. http://dx.doi.org/10.1073/pnas.262525399
49. Luo, R., M. An, B.L. Arduini, and P.D. Henion. 2001. Specific pan-neural crest expression of zebrafish Crestin throughout embryonic development. Dev. Dyn. 220:169-174. http://dx.doi.org/10.1002/1097-0177(2000)9999:9999::AID-DVDY10973.0.CO;2-1
50. Mancilla, A., and R. Mayor. 1996. Neural crest formation in Xenopus laevis: mechanisms of Xslug induction. Dev. Biol. 177:580-589. http://dx.doi.org/10.1006/dbio.1996.0187
51. Matthews, H.K., L. Marchant, C. Carmona-Fontaine, S. Kuriyama, J. Larraín, M.R. Holt, M. Parsons, and R. Mayor. 2008. Directional migration of neural crest cells in vivo is regulated by Syndecan-4/Rac1 and noncanonical Wnt signaling/RhoA. Development. 135:1771-1780. http://dx.doi.org/10.1242/dev.017350
52. Mayor, R., R. Morgan, and M.G. Sargent. 1995. Induction of the prospective neural crest of Xenopus. Development. 121:767-777.
53. Moepps, B., M. Braun, K. Knöpfle, K. Dillinger, W. Knöpfle, and P. Gierschik. 2000. Characterization of a Xenopus laevis CXC chemokine receptor 4: implications for hematopoietic cell development in the vertebrate embryo. Eur. J. Immunol. 30:2924-2934. http://dx.doi.org/10.1002/1521-4141(200010)30:102924::AID-IMMU29243.0.CO;2-Y
54. Morrison, S.J., M. Csete, A.K. Groves, W. Melega, B. Wold, and D.J. Anderson. 2000. Culture in reduced levels of oxygen promotes clonogenic sympathoadrenal differentiation by isolated neural crest stem cells. J. Neurosci. 20:7370-7376.
55. Nagao, K., Y. Taniyama, T. Kietzmann, T. Doi, I. Komuro, and R. Morishita. 2008. HIF-1alpha signaling upstream of NKX2.5 is required for cardiac development in Xenopus. J. Biol. Chem. 283:11841-11849. http://dx.doi.org/10.1074/jbc.M702563200
56. Nandadasa, S., Q. Tao, N.R. Menon, J. Heasman, and C. Wylie. 2009. N- and E-cadherins in Xenopus are specifically required in the neural and nonneural ectoderm, respectively, for F-actin assembly and morphogenetic movements. Development. 136:1327-1338. http://dx.doi.org/10.1242/dev.031203
57. Nieuwkoop, P.D., and J. Faber. 1967. Normal Table of Xenopus laevis (Daudin): A systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis. Second edition. North-Holland Pub. Co., Amsterdam. 260 pp.
58. Ocaña, O.H., R. Córcoles, A. Fabra, G. Moreno-Bueno, H. Acloque, S. Vega, A. Barrallo-Gimeno, A. Cano, and M.A. Nieto. 2012. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell. 22:709-724. http://dx.doi.org/10.1016/j.ccr.2012.10.012
59. Ohh, M., C.W. Park, M. Ivan, M.A. Hoffman, T.Y. Kim, L.E. Huang, N. Pavletich, V. Chau, and W.G. Kaelin. 2000. Ubiquitination of hypoxiainducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nat. Cell Biol. 2:423-427. http://dx.doi.org/10.1038/35017054
60. Olesnicky Killian, E.C., D.A. Birkholz, and K.B. Artinger. 2009. A role for chemokine signaling in neural crest cell migration and craniofacial development. Dev. Biol. 333:161-172. http://dx.doi.org/10.1016/j.ydbio.2009.06.031
61. Ota, M.S., D.A. Loebel, M.P. O'Rourke, N. Wong, B. Tsoi, and P.P. Tam. 2004. Twist is required for patterning the cranial nerves and maintaining the viability of mesodermal cells. Dev. Dyn. 230:216-228. http://dx.doi.org/10.1002/dvdy.20047
62. Peinado, H., D. Olmeda, and A. Cano. 2007. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat. Rev. Cancer. 7:415-428. http://dx.doi.org/10.1038/nrc2131
63. Pennacchietti, S., P. Michieli, M. Galluzzo, M. Mazzone, S. Giordano, and P.M. Comoglio. 2003. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell. 3:347-361. http://dx.doi.org/10.1016/S1535-6108(03)00085-0
64. Rojas, D.A., D.A. Perez-Munizaga, L. Centanin, M. Antonelli, P. Wappner, M.L. Allende, and A.E. Reyes. 2007. Cloning of hif-1alpha and hif-2alpha and mRNA expression pattern during development in zebrafish. Gene Expr. Patterns. 7:339-345. http://dx.doi.org/10.1016/j.modgep.2006.08.002
65. Rouschop, K.M., T. van den Beucken, L. Dubois, H. Niessen, J. Bussink, K. Savelkouls, T. Keulers, H. Mujcic, W. Landuyt, J.W. Voncken, et al. 2010. The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. J. Clin. Invest. 120:127-141. http://dx.doi.org/10.1172/JCI40027
66. Schulte-Merker, S., R.K. Ho, B.G. Herrmann, and C. Nüsslein-Volhard. 1992. The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. Development. 116:1021-1032.
67. Sefton, M., S. Sánchez, and M.A. Nieto. 1998. Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo. Development. 125:3111-3121.
68. Semenza, G.L. 2000. HIF-1: using two hands to flip the angiogenic switch. Cancer Metastasis Rev. 19:59-65. http://dx.doi.org/10.1023/A:1026544214667
69. Semenza, G.L. 2002. HIF-1 and tumor progression: pathophysiology and therapeutics. Trends Mol. Med. 8(Suppl.):S62-S67. http://dx.doi.org/10.1016/S1471-4914(02)02317-1
70. Semenza, G.L. 2007. Hypoxia and cancer. Cancer Metastasis Rev. 26:223-224. http://dx.doi.org/10.1007/s10555-007-9058-y
71. Semenza, G.L. 2010. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene. 29:625-634. http://dx.doi.org/10.1038/onc.2009.441
72. Semenza, G.L., M.K. Nejfelt, S.M. Chi, and S.E. Antonarakis. 1991. Hypoxiainducible nuclear factors bind to an enhancer element located 3' to the human erythropoietin gene. Proc. Natl. Acad. Sci. USA. 88:5680-5684. http://dx.doi.org/10.1073/pnas.88.13.5680
73. Soo, K., M.P. O'Rourke, P.L. Khoo, K.A. Steiner, N. Wong, R.R. Behringer, and P.P. Tam. 2002. Twist function is required for the morphogenesis of the cephalic neural tube and the differentiation of the cranial neural crest cells in the mouse embryo. Dev. Biol. 247:251-270. http://dx.doi.org/10.1006/dbio.2002.0699
74. Stachel, S.E., D.J. Grunwald, and P.Z. Myers. 1993. Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish. Development. 117:1261-1274.
75. Staller, P., J. Sulitkova, J. Lisztwan, H. Moch, E.J. Oakeley, and W. Krek. 2003. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL. Nature. 425:307-311. http://dx.doi.org/10.1038/nature01874
76. Steventon, B., C. Carmona-Fontaine, and R. Mayor. 2005. Genetic network during neural crest induction: from cell specification to cell survival. Semin. Cell Dev. Biol. 16:647-654. http://dx.doi.org/10.1016/j.semcdb.2005.06.001
77. Stoetzel, C., B. Weber, P. Bourgeois, A.L. Bolcato-Bellemin, and F. Perrin-Schmitt. 1995. Dorso-ventral and rostro-caudal sequential expression of M-twist in the postimplantation murine embryo. Mech. Dev. 51:251-263. http://dx.doi.org/10.1016/0925-4773(95)00369-X
78. Studer, L., M. Csete, S.H. Lee, N. Kabbani, J. Walikonis, B. Wold, and R. McKay. 2000. Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J. Neurosci. 20:7377-7383.
79. Tanimoto, K., Y. Makino, T. Pereira, and L. Poellinger. 2000. Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein. EMBO J. 19:4298-4309. http://dx.doi.org/10.1093/emboj/19.16.4298
80. Theveneau, E., and R. Mayor. 2010. Integrating chemotaxis and contact-inhibition during collective cell migration: Small GTPases at work. Small GTPases. 1:113-117. http://dx.doi.org/10.4161/sgtp.1.2.13673
81. Theveneau, E., and R. Mayor. 2011. Collective cell migration of the cephalic neural crest: the art of integrating information. Genesis. 49:164-176. http://dx.doi.org/10.1002/dvg.20700
82. Theveneau, E., L. Marchant, S. Kuriyama, M. Gull, B. Moepps, M. Parsons, and R. Mayor. 2010. Collective chemotaxis requires contact-dependent cell polarity. Dev. Cell. 19:39-53. http://dx.doi.org/10.1016/j.devcel.2010.06.012
83. Thiery, J.P., H. Acloque, R.Y. Huang, and M.A. Nieto. 2009. Epithelialmesenchymal transitions in development and disease. Cell. 139:871-890. http://dx.doi.org/10.1016/j.cell.2009.11.007
84. Tsai, J.H., J.L. Donaher, D.A. Murphy, S. Chau, and J. Yang. 2012. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell. 22:725-736. http://dx.doi.org/10.1016/j.ccr.2012.09.022
85. Wang, Y., and M. Ohh. 2010. Oxygen-mediated endocytosis in cancer. J. Cell. Mol. Med. 14:496-503.
86. Weinberg, E.S., M.L. Allende, C.S. Kelly, A. Abdelhamid, T. Murakami, P. Andermann, O.G. Doerre, D.J. Grunwald, and B. Riggleman. 1996. Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development. 122:271-280.
87. Westerfield, M. 2000. The Zebrafish Book: a guide for the laboratory use of zebrafish (Brachydanio rerio). Fourth edition. University of Oregon Press, Eugene, OR.
88. Yang, J., S.A. Mani, J.L. Donaher, S. Ramaswamy, R.A. Itzykson, C. Come, P. Savagner, I. Gitelman, A. Richardson, and R.A. Weinberg. 2004. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 117:927-939. http://dx.doi.org/10.1016/j.cell.2004.06.006
89. Yang, M.H., M.Z. Wu, S.H. Chiou, P.M. Chen, S.Y. Chang, C.J. Liu, S.C. Teng, and K.J. Wu. 2008. Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat. Cell Biol. 10:295-305. http://dx.doi.org/10.1038/ncb1691
90. Zhang, C., and M.W. Klymkowsky. 2009. Unexpected functional redundancy between Twist and Slug (Snail2) and their feedback regulation of NF-kappaB via Nodal and Cerberus. Dev. Biol. 331:340-349. http://dx.doi.org/10.1016/j.ydbio.2009.04.016
91. Zhong, H., K. Chiles, D. Feldser, E. Laughner, C. Hanrahan, M.M. Georgescu, J.W. Simons, and G.L. Semenza. 2000. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res. 60: 1541-1545.
92. Zhou, J., and B. Brüne. 2006. Cytokines and hormones in the regulation of hypoxia inducible factor-1alpha (HIF-1alpha). Cardiovasc. Hematol. Agents Med. Chem. 4:189-197. http://dx.doi.org/10.2174/187152506777698344