Riding the crest of the wave: Parallels between the neural crest and cancer in epithelial-to-mesenchymal transition and migration

Wiley Interdisciplinary Reviews: Systems Biology and Medicine

Volumn 5, Issue 4, 2013, Pages 511-522

  Powell, Davalyn R ^a,b   Blasky, Alex J ^a,c   Britt, Steven G ^a   Artinger, Kristin B ^b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c University of Colorado Denver and Children s Hospital Colorado   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM PROTEIN; BETA CATENIN; BONE MORPHOGENETIC PROTEIN; CADHERIN; CADHERIN 6B; CHEMOKINE RECEPTOR CXCR4; CLAUDIN; GELATINASE A; HELIX LOOP HELIX PROTEIN; MATRIX METALLOPROTEINASE 14; NERVE CELL ADHESION MOLECULE; NEUTROPHIL COLLAGENASE; OCCLUDIN; PROTEIN ADAM13; PROTEIN ADAM9; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SNAIL1; TRANSCRIPTION FACTOR SNAIL2; TRANSCRIPTION FACTOR SOX10; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; UVOMORULIN; WNT PROTEIN;

ARTICLE; CANCER CELL; CANCER PROGNOSIS; CANCER SURVIVAL; CARCINOGENESIS; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; EPITHELIAL MESENCHYMAL TRANSITION; GENE REGULATORY NETWORK; GENETIC REGULATION; HUMAN; METASTASIS; NEOPLASM; NERVE CELL DIFFERENTIATION; NEURAL CREST; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR INVASION;

CELL ADHESION; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; NEOPLASM METASTASIS; NEOPLASMS; NEURAL CREST; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84879305891     PISSN: 19395094     EISSN: 1939005X     Source Type: Journal    
DOI: 10.1002/wsbm.1224     Document Type: Article

References (103)

1. Bronner ME, LeDouarin NM. Development and evolution of the neural crest: an overview. Dev Biol 2012, 366:2-9.
2. Sauka-Spengler T, Bronner-Fraser M. A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cell Biol 2008, 9:557-568.
3. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 2007, 7:415-428.
4. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 2006, 7:131-142.
5. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 2008, 14:818-829.
6. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
7. Strobl-Mazzulla PH, Bronner ME. Epithelial to mesenchymal transition: new and old insights from the classical neural crest model. Semin Cancer Biol 2012, 22:411-416.
8. Theveneau E, Mayor R. Neural crest delamination and migration: from epithelium-to-mesenchyme transition to collective cell migration. Dev Biol 2012, 366:34-54.
9. Kulesa PM, Gammill LS. Neural crest migration: patterns, phases and signals. Dev Biol 2010, 344:566-568.
10. Cheung M, Chaboissier MC, Mynett A, Hirst E, Schedl A, Briscoe J. The transcriptional control of trunk neural crest induction, survival, and delamination. Dev Cell 2005, 8:179-192.
11. 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. Dev Biol 2000, 221:195-205.
12. Nieto MA, Sargent MG, Wilkinson DG, Cooke J. Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science 1994, 264:835-839.
13. Blanco MJ, Barrallo-Gimeno A, Acloque H, Reyes AE, Tada M, Allende ML, Mayor R, Nieto MA. Snail1a and Snail1b cooperate in the anterior migration of the axial mesendoderm in the zebrafish embryo. Development 2007, 134:4073-4081.
14. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2000, 2:84-89.
15. Cano A, Pérez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000, 2:76-83.
16. Olmeda D, Jorda M, Peinado H, Fabra A, Cano A. Snail silencing effectively suppresses tumour growth and invasiveness. Oncogene 2007, 26:1862-1874.
17. Tang P, Yu Z, Zhang K, Wang Y, Ma Z, Zhang S, Chen D, Zhou Y. Slug down-regulation by RNA interference inhibits invasion growth in human esophageal squamous cell carcinoma. BMC Gastroenterol 2011, 11:60.
18. Wang X, Zhang K, Sun L, Liu J, Lu H. Short interfering RNA directed against Slug blocks tumor growth, metastasis formation, and vascular leakage in bladder cancer. Med Oncol 2011, 28 (suppl 1):S413-S422.
19. Gupta PB, Kuperwasser C, Brunet JP, Ramaswamy S, Kuo WL, Gray JW, Naber SP, Weinberg RA. The melanocyte differentiation program predisposes to metastasis after neoplastic transformation. Nat Genet 2005, 37:1047-1054.
20. Van de Putte T, Francis A, Nelles L, van Grunsven LA, Huylebroeck D. Neural crest-specific removal of Zfhx1b in mouse leads to a wide range of neurocristopathies reminiscent of Mowat-Wilson syndrome. Hum Mol Genet 2007, 16:1423-1436.
21. Van de Putte T, Maruhashi M, Francis A, Nelles L, Kondoh H, Huylebroeck D, Higashi Y. 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. Am J Hum Genet 2003, 72:465-470.
22. Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L, Bruyneel E, Mareel M, Huylebroeck D, van Roy F. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell 2001, 7:1267-1278.
23. Cacheux V, Dastot-Le Moal F, Kaariainen H, Bondurand N, Rintala R, Boissier B, Wilson M, Mowat D, Goossens M. Loss-of-function mutations in SIP1 Smad interacting protein 1 result in a syndromic Hirschsprung disease. Hum Mol Genet 2001, 10:1503-1510.
24. Wakamatsu N, Yamada Y, Yamada K, Ono T, Nomura N, Taniguchi H, Kitoh H, Mutoh N, Yamanaka T, Mushiake K, et al. Mutations in SIP1, encoding Smad interacting protein-1, cause a form of Hirschsprung disease. Nat Genet 2001, 27:369-370.
25. Schmalhofer O, Brabletz S, Brabletz T. E-cadherin, β-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev 2009, 28:151-166.
26. Hong CS, Saint-Jeannet JP. Sox proteins and neural crest development. Semin Cell Dev Biol 2005, 16:694-703.
27. Kim J, Lo L, Dormand E, Anderson DJ. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 2003, 38:17-31.
28. Harris ML, Baxter LL, Loftus SK, Pavan WJ. Sox proteins in melanocyte development and melanoma. Pigment Cell Melanoma Res 2010, 23:496-513.
29. Herbarth B, Pingault V, Bondurand N, Kuhlbrodt K, Hermans-Borgmeyer I, Puliti A, Lemort N, Goossens M, Wegner M. Mutation of the Sry-related Sox10 gene in Dominant megacolon, a mouse model for human Hirschsprung disease. Proc Natl Acad Sci U S A 1998, 95:5161-5165.
30. Kelsh RN, Eisen JS. The zebrafish colourless gene regulates development of non-ectomesenchymal neural crest derivatives. Development 2000, 127:515-525.
31. Shakhova O, Zingg D, Schaefer SM, Hari L, Civenni G, Blunschi J, Claudinot S, Okoniewski M, Beermann F, Mihic-Probst D, et al. Sox10 promotes the formation and maintenance of giant congenital naevi and melanoma. Nat Cell Biol 2012, 14:882-890.
32. Soo K, O'Rourke MP, Khoo PL, Steiner KA, Wong N, Behringer RR, Tam PP. 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 2002, 247:251-270.
33. Vincentz JW, Barnes RM, Rodgers R, Firulli BA, Conway SJ, Firulli AB. An absence of Twist1 results in aberrant cardiac neural crest morphogenesis. Dev Biol 2008, 320:131-139.
34. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117:927-939.
35. Casas E, Kim J, Bendesky A, Ohno-Machado L, Wolfe CJ, Yang J. Snail2 is an essential mediator of Twist1-induced epithelial mesenchymal transition and metastasis. Cancer Res 2011, 71:245-254.
36. Sanchez-Tillo E, Liu Y, de Barrios O, Siles L, Fanlo L, Cuatrecasas M, Darling DS, Dean DC, Castells A, Postigo A. EMT-activating transcription factors in cancer: beyond EMT and tumor invasiveness. Cell Mol Life Sci 2012, 69:3429-3456.
37. Aaku-Saraste E, Hellwig A, Huttner WB. Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure-remodeling of the neuroepithelium prior to neurogenesis. Dev Biol 1996, 180:664-679.
38. 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. J Cell Sci 2003, 116 (Pt 10):1959-1967.
39. Martinez-Estrada OM, Culleres A, Soriano FX, Peinado H, Bolos V, Martinez FO, Reina M, Cano A, Fabre M, Vilaro S. The transcription factors Slug and Snail act as repressors of Claudin-1 expression in epithelial cells. Biochem J 2006, 394 (Pt 2):449-457.
40. Fishwick KJ, Neiderer TE, Jhingory S, Bronner ME, Taneyhill LA. The tight junction protein claudin-1 influences cranial neural crest cell emigration. Mech Dev 2012, 129:275-283.
41. Martin TA, Jiang WG. Loss of tight junction barrier function and its role in cancer metastasis. Biochim Biophys Acta 2009, 1788:872-891.
42. Nakagawa S, Takeichi M. Neural crest cell-cell adhesion controlled by sequential and subpopulation-specific expression of novel cadherins. Development 1995, 121:1321-1332.
43. 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. Dev Biol 1997, 183:183-194.
44. Liu Q, Liu B, Wilson AL, Rostedt J. cadherin-6 message expression in the nervous system of developing zebrafish. Dev Dyn 2006, 235:272-278.
45. Berx G, van Roy F. Involvement of members of the cadherin superfamily in cancer. Cold Spring Harb Perspect Biol 2009, 1:a003129.
46. Nakagawa S, Takeichi M. Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 1998, 125:2963-2971.
47. Vallin J, Girault JM, Thiery JP, Broders F. Xenopus cadherin-11 is expressed in different populations of migrating neural crest cells. Mech Dev 1998, 75:171-174.
48. 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.
49. Nieman MT, Prudoff RS, Johnson KR, Wheelock MJ. N-cadherin promotes motility in human breast cancer cells regardless of their E-cadherin expression. J Cell Biol 1999, 147:631-644.
50. Hazan RB, Phillips GR, Qiao RF, Norton L, Aaronson SA. Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis. J Cell Biol 2000, 148:779-790.
51. Mellman I, Nelson WJ. Coordinated protein sorting, targeting and distribution in polarized cells. Nat Rev Mol Cell Biol 2008, 9:833-845.
52. Karp CM, Tan TT, Mathew R, Nelson D, Mukherjee C, Degenhardt K, Karantza-Wadsworth V, White E. Role of the polarity determinant crumbs in suppressing mammalian epithelial tumor progression. Cancer Res 2008, 68:4105-4115.
53. Aigner K, Dampier B, Descovich L, Mikula M, Sultan A, Schreiber M, Mikulits W, Brabletz T, Strand D, Obrist P, et al. The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 2007, 26:6979-6988.
54. Spaderna S, Schmalhofer O, Wahlbuhl M, Dimmler A, Bauer K, Sultan A, Hlubek F, Jung A, Strand D, Eger A, et al. The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res 2008, 68:537-544.
55. Whiteman EL, Liu CJ, Fearon ER, Margolis B. The transcription factor snail represses Crumbs3 expression and disrupts apico-basal polarity complexes. Oncogene 2008, 27:3875-3879.
56. Wang X, Nie J, Zhou Q, Liu W, Zhu F, Chen W, Mao H, Luo N, Dong X, Yu X. Downregulation of Par-3 expression and disruption of Par complex integrity by TGF-β during the process of epithelial to mesenchymal transition in rat proximal epithelial cells. Biochim Biophys Acta 2008, 1782:51-59.
57. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 2010, 29:4741-4751.
58. Ozdamar B, Bose R, Barrios-Rodiles M, Wang HR, Zhang Y, Wrana JL. Regulation of the polarity protein Par6 by TGFβ receptors controls epithelial cell plasticity. Science 2005, 307:1603-1609.
59. Huang L, Muthuswamy SK. Polarity protein alterations in carcinoma: a focus on emerging roles for polarity regulators. Curr Opin Genet Dev 2010, 20:41-50.
60. Cai DH, Vollberg TM Sr, Hahn-Dantona E, Quigley JP, Brauer PR. MMP-2 expression during early avian cardiac and neural crest morphogenesis. Anat Rec 2000, 259:168-179.
61. Giambernardi TA, Sakaguchi AY, Gluhak J, Pavlin D, Troyer DA, Das G, Rodeck U, Klebe RJ. Neutrophil collagenase (MMP-8) is expressed during early development in neural crest cells as well as in adult melanoma cells. Matrix Biol 2001, 20:577-587.
62. Anderson RB. Matrix metalloproteinase-2 is involved in the migration and network formation of enteric neural crest-derived cells. Int J Dev Biol 2010, 54:63-69.
63. Duong TD, Erickson CA. MMP-2 plays an essential role in producing epithelial-mesenchymal transformations in the avian embryo. Dev Dyn 2004, 229:42-53.
64. Alfandari D, Cousin H, Gaultier A, Smith K, White JM, Darribere T, DeSimone DW. Xenopus ADAM 13 is a metalloprotease required for cranial neural crest-cell migration. Curr Biol 2001, 11:918-930.
65. McCusker C, Cousin H, Neuner R, Alfandari D. Extracellular cleavage of cadherin-11 by ADAM metalloproteases is essential for Xenopus cranial neural crest cell migration. Mol Biol Cell 2009, 20:78-89.
66. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 2006, 25:9-34.
67. Xu X, Wang Y, Chen Z, Sternlicht MD, Hidalgo M, Steffensen B. Matrix metalloproteinase-2 contributes to cancer cell migration on collagen. Cancer Res 2005, 65:130-136.
68. Mendes O, Kim HT, Lungu G, Stoica G. MMP2 role in breast cancer brain metastasis development and its regulation by TIMP2 and ERK1/2. Clin Exp Metastasis 2007, 24:341-351.
69. Trudel D, Fradet Y, Meyer F, Harel F, Tetu B. Significance of MMP-2 expression in prostate cancer: an immunohistochemical study. Cancer Res 2003, 63:8511-8515.
70. Leinonen T, Pirinen R, Bohm J, Johansson R, Kosma VM. Increased expression of matrix metalloproteinase-2 (MMP-2) predicts tumour recurrence and unfavourable outcome in non-small cell lung cancer. Histol Histopathol 2008, 23:693-700.
71. Masson V, de la Ballina LR, Munaut C, Wielockx B, Jost M, Maillard C, Blacher S, Bajou K, Itoh T, Itohara S, et al. Contribution of host MMP-2 and MMP-9 to promote tumor vascularization and invasion of malignant keratinocytes. FASEB J 2005, 19:234-236.
72. Rocks N, Paulissen G, El Hour M, Quesada F, Crahay C, Gueders M, Foidart JM, Noel A, Cataldo D. Emerging roles of ADAM and ADAMTS metalloproteinases in cancer. Biochimie 2008, 90:369-379.
73. Jiang C, Zhang Y, Yu HF, Yu XT, Zhou SJ, Tan YF. Expression of ADAM8 and its clinical values in diagnosis and prognosis of hepatocellular carcinoma. Tumour Biol 2012, 33:2167-2172.
74. Roy R, Wewer UM, Zurakowski D, Pories SE, Moses MA. ADAM 12 cleaves extracellular matrix proteins and correlates with cancer status and stage. J Biol Chem 2004, 279:51323-51330.
75. Xiao LJ, Lin P, Lin F, Liu X, Qin W, Zou HF, Guo L, Liu W, Wang SJ, Yu XG. ADAM17 targets MMP-2 and MMP-9 via EGFR-MEK-ERK pathway activation to promote prostate cancer cell invasion. Int J Oncol 2012, 40:1714-1724.
76. Zhang Y, Tan YF, Jiang C, Zhang K, Zha TZ, Zhang M. High ADAM8 expression is associated with poor prognosis in patients with hepatocellular carcinoma. Pathol Oncol Res 2013, 19:79-88.
77. Olesnicky Killian EC, Birkholz DA, Artinger KB. A role for chemokine signaling in neural crest cell migration and craniofacial development. Dev Biol 2009, 333:161-172.
78. Theveneau E, Marchant L, Kuriyama S, Gull M, Moepps B, Parsons M, Mayor R. Collective chemotaxis requires contact-dependent cell polarity. Dev Cell 2010, 19:39-53.
79. Belmadani A, Tran PB, Ren D, Assimacopoulos S, Grove EA, Miller RJ. The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J Neurosci 2005, 25:3995-4003.
80. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56.
81. Zlotnik A, Burkhardt AM, Homey B. Homeostatic chemokine receptors and organ-specific metastasis. Nat Rev Immunol 2011, 11:597-606.
82. Krull CE, Lansford R, Gale NW, Collazo A, Marcelle C, Yancopoulos GD, Fraser SE, Bronner-Fraser M. Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. Curr Biol 1997, 7:571-580.
83. Gammill LS, Gonzalez C, Gu C, Bronner-Fraser M. Guidance of trunk neural crest migration requires neuropilin 2/semaphorin 3F signaling. Development 2006, 133:99-106.
84. Schwarz Q, Maden CH, Davidson K, Ruhrberg C. Neuropilin-mediated neural crest cell guidance is essential to organise sensory neurons into segmented dorsal root ganglia. Development 2009, 136: 1785-1789.
85. Smith A, Robinson V, Patel K, Wilkinson DG. The EphA4 and EphB1 receptor tyrosine kinases and ephrin-B2 ligand regulate targeted migration of branchial neural crest cells. Curr Biol 1997, 7:561-570.
86. Harburg GC, Hinck L. Navigating breast cancer: axon guidance molecules as breast cancer tumor suppressors and oncogenes. J Mammary Gland Biol Neoplasia 2011, 16:257-270.
87. Nasarre P, Potiron V, Drabkin H, Roche J. Guidance molecules in lung cancer. Cell Adh Migr 2010, 4:130-145.
88. 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.
89. Thisse C, Thisse B, Postlethwait JH. 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. Dev Biol 1995, 172:86-99.
90. Montero-Balaguer M, Lang MR, Sachdev SW, Knappmeyer C, Stewart RA, De La Guardia A, Hatzopoulos AK, Knapik EW. The mother superior mutation ablates foxd3 activity in neural crest progenitor cells and depletes neural crest derivatives in zebrafish. Dev Dyn 2006, 235:3199-3212.
91. Murray SA, Gridley T. Snail family genes are required for left-right asymmetry determination, but not neural crest formation, in mice. Proc Natl Acad Sci U S A 2006, 103:10300-10304.
92. Vandewalle C, Van Roy F, Berx G. The role of the ZEB family of transcription factors in development and disease. Cell Mol Life Sci 2009, 66:773-787.
93. Perk J, Iavarone A, Benezra R. Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer 2005, 5:603-614.
94. Norton JD. ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J Cell Sci 2000, 113 (Pt 22):3897-3905.
95. Dow LE, Humbert PO. Polarity regulators and the control of epithelial architecture, cell migration, and tumorigenesis. Int Rev Cytol 2007, 262:253-302.
96. Martin-Belmonte F, Perez-Moreno M. Epithelial cell polarity, stem cells and cancer. Nat Rev Cancer 2012, 12:23-38.
97. Moreno-Bueno G, Portillo F, Cano A. Transcriptional regulation of cell polarity in EMT and cancer. Oncogene 2008, 27:6958-6969.
98. Wu CY, Jhingory S, Taneyhill LA. The tight junction scaffolding protein cingulin regulates neural crest cell migration. Dev Dyn 2011, 240:2309-2323.
99. Etienne-Manneville S. Control of polarized cell morphology and motility by adherens junctions. Semin Cell Dev Biol 2011, 22:850-857.
100. Wheelock MJ, Shintani Y, Maeda M, Fukumoto Y, Johnson KR. Cadherin switching. J Cell Sci 2008, 121 (Pt 6):727-735.
101. Anderson RB, Newgreen DF, Young HM. Neural crest and the development of the enteric nervous system. Adv Exp Med Biol 2006, 589:181-196.
102. Zhang Y, Kim TH, Niswander L. Phactr4 regulates directional migration of enteric neural crest through PP1, integrin signaling, and cofilin activity. Genes Dev 2012, 26:69-81.
103. Friedl P, Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 2003, 3:362-374.