WAVE2 Regulates Epithelial Morphology and Cadherin Isoform Switching through Regulation of Twist and Abl

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Bryce, Nicole S ^a   Reynolds, Albert B ^a   Koleske, Anthony J ^b   Weaver, Alissa M ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; CADHERIN; CRK LIKE PROTEIN; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; PROTEIN WAVE2; REGULATOR PROTEIN; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; UVOMORULIN;

ACINAR CELL; ARTICLE; BREAST EPITHELIUM; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; MORPHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

CADHERINS; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; NUCLEAR PROTEINS; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS C-ABL; REAL-TIME POLYMERASE CHAIN REACTION; TWIST TRANSCRIPTION FACTOR; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY;

EID: 84877764094     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064533     Document Type: Article

References (79)

1. Bell PB Jr, (1978) Contact inhibition of movements in transformed and nontransformed cells. Birth Defects Orig Artic Ser 14: 177-194.
2. Fisher HW, Yeh J, (1967) Contact inhibition in colony formation. Science 155: 581-582.
3. Nishimura T, Takeichi M, (2009) Remodeling of the adherens junctions during morphogenesis. Curr Top Dev Biol 89: 33-54.
4. Takeichi M, (1995) Morphogenetic roles of classic cadherins. Curr Opin Cell Biol 7: 619-627.
5. Feigin ME, Muthuswamy SK, (2009) Polarity proteins regulate mammalian cell-cell junctions and cancer pathogenesis. Curr Opin Cell Biol 21: 694-700.
6. Thiery JP, Acloque H, Huang RY, Nieto MA, (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
7. Savagner P, (2001) Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays 23: 912-923.
8. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715.
9. Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, et al. (2008) Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 3: e2888.
10. Helwani FM, Kovacs EM, Paterson AD, Verma S, Ali RG, et al. (2004) Cortactin is necessary for E-cadherin-mediated contact formation and actin reorganization. J Cell Biol 164: 899-910.
11. Ivanov AI, Hunt D, Utech M, Nusrat A, Parkos CA, (2005) Differential roles for actin polymerization and a myosin II motor in assembly of the epithelial apical junctional complex. Mol Biol Cell 16: 2636-2650.
12. Kobielak A, Pasolli HA, Fuchs E, (2004) Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat Cell Biol 6: 21-30.
13. Perez-Moreno M, Jamora C, Fuchs E, (2003) Sticky business: orchestrating cellular signals at adherens junctions. Cell 112: 535-548.
14. Vasioukhin V, Bauer C, Yin M, Fuchs E, (2000) Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100: 209-219.
15. Verma S, Shewan AM, Scott JA, Helwani FM, den Elzen NR, et al. (2004) Arp2/3 activity is necessary for efficient formation of E-cadherin adhesive contacts. J Biol Chem 279: 34062-34070.
16. Yamada S, Nelson WJ, (2007) Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J Cell Biol 178: 517-527.
17. Yamada S, Pokutta S, Drees F, Weis WI, Nelson WJ, (2005) Deconstructing the cadherin-catenin-actin complex. Cell 123: 889-901.
18. Yamazaki D, Oikawa T, Takenawa T, (2007) Rac-WAVE-mediated actin reorganization is required for organization and maintenance of cell-cell adhesion. J Cell Sci 120: 86-100.
19. Baum B, Georgiou M, (2011) Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J Cell Biol 192: 907-917.
20. Georgiou M, Marinari E, Burden J, Baum B, (2008) Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr Biol 18: 1631-1638.
21. Yap AS, Crampton MS, Hardin J, (2007) Making and breaking contacts: the cellular biology of cadherin regulation. Curr Opin Cell Biol 19: 508-514.
22. Verma S, Han SP, Michael M, Gomez GA, Yang Z, et al. (2012) A WAVE2-Arp2/3 actin nucleator apparatus supports junctional tension at the epithelial zonula adherens. Mol Biol Cell 23: 4601-4610.
23. Dahl JP, Wang-Dunlop J, Gonzales C, Goad ME, Mark RJ, et al. (2003) Characterization of the WAVE1 knock-out mouse: implications for CNS development. J Neurosci 23: 3343-3352.
24. Escobar B, de Carcer G, Fernandez-Miranda G, Cascon A, Bravo-Cordero JJ, et al. (2010) Brick1 is an essential regulator of actin cytoskeleton required for embryonic development and cell transformation. Cancer Res 70: 9349-9359.
25. Liu R, Abreu-Blanco MT, Barry KC, Linardopoulou EV, Osborn GE, et al. (2009) Wash functions downstream of Rho and links linear and branched actin nucleation factors. Development 136: 2849-2860.
26. Snapper SB, Takeshima F, Anton I, Liu C-H, Thomas SM, et al. (2001) N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat Cell Biol 3: 897-904.
27. Yae K, Keng VW, Koike M, Yusa K, Kouno M, et al. (2006) Sleeping beauty transposon-based phenotypic analysis of mice: lack of Arpc3 results in defective trophoblast outgrowth. Mol Cell Biol 26: 6185-6196.
28. Yamazaki D, Suetsugu S, Miki H, Kataoka Y, Nishikawa S, et al. (2003) WAVE2 is required for directed cell migration and cardiovascular development. Nature 424: 452-456.
29. Yan C, Martinez-Quiles N, Eden S, Shibata T, Takeshima F, et al. (2003) WAVE2 deficiency reveals distinct roles in embryogenesis and Rac-mediated actin-based motility. Embo J 22: 3602-3612.
30. Yu D, Zhang H, Blanpied TA, Smith E, Zhan X, (2010) Cortactin is implicated in murine zygotic development. Exp Cell Res 316: 848-858.
31. Shankar J, Messenberg A, Chan J, Underhill TM, Foster LJ, et al. (2010) Pseudopodial Actin Dynamics Control Epithelial-Mesenchymal Transition in Metastatic Cancer Cells. Cancer Res 70: 3780-3790.
32. Suetsugu S, Yamazaki D, Kurisu S, Takenawa T, (2003) Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev Cell 5: 595-609.
33. Bryce NS, Clark ES, Leysath JL, Currie JD, Webb DJ, et al. (2005) Cortactin promotes cell motility by enhancing lamellipodial persistence. Curr Biol 15: 1276-1285.
34. Sarmiento C, Wang W, Dovas A, Yamaguchi H, Sidani M, et al. (2008) WASP family members and formin proteins coordinate regulation of cell protrusions in carcinoma cells. J Cell Biol 180: 1245-1260.
35. Debnath J, Brugge JS, (2005) Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer 5: 675-688.
36. Thoreson MA, Anastasiadis PZ, Daniel JM, Ireton RC, Wheelock MJ, et al. (2000) Selective uncoupling of p120(ctn) from E-cadherin disrupts strong adhesion. J Cell Biol 148: 189-202.
37. Baranwal S, Alahari SK, (2009) Molecular mechanisms controlling E-cadherin expression in breast cancer. Biochem Biophys Res Commun 384: 6-11.
38. Yori JL, Johnson E, Zhou G, Jain MK, Keri RA, (2010) Kruppel-like factor 4 inhibits epithelial-to-mesenchymal transition through regulation of E-cadherin gene expression. J Biol Chem 285: 16854-16863.
39. Werth M, Walentin K, Aue A, Schonheit J, Wuebken A, et al. (2010) The transcription factor grainyhead-like 2 regulates the molecular composition of the epithelial apical junctional complex. Development 137: 3835-3845.
40. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, et al. (2004) Twist, a Master Regulator of Morphogenesis, Plays an Essential Role in Tumor Metastasis. Cell 117: 927-939.
41. Hajra KM, Chen DYS, Fearon ER, (2002) The SLUG Zinc-Finger Protein Represses E-Cadherin in Breast Cancer. Cancer Res 62: 1613-1618.
42. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, et al. (2000) The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2: 76-83.
43. Leng Y, Zhang J, Badour K, Arpaia E, Freeman S, et al. (2005) Abelson-interactor-1 promotes WAVE2 membrane translocation and Abelson-mediated tyrosine phosphorylation required for WAVE2 activation. Proc Natl Acad Sci U S A 102: 1098-1103.
44. Stuart JR, Gonzalez FH, Kawai H, Yuan ZM, (2006) c-Abl interacts with the WAVE2 signaling complex to induce membrane ruffling and cell spreading. J Biol Chem 281: 31290-31297.
45. Yang L, Lin C, Liu ZR, (2006) P68 RNA helicase mediates PDGF-induced epithelial mesenchymal transition by displacing Axin from beta-catenin. Cell 127: 139-155.
46. Allington TM, Galliher-Beckley AJ, Schiemann WP, (2009) Activated Abl kinase inhibits oncogenic transforming growth factor-beta signaling and tumorigenesis in mammary tumors. FASEB J 23: 4231-4243.
47. Lin TY, Huang CH, Kao HH, Liou GG, Yeh SR, et al. (2009) Abi plays an opposing role to Abl in Drosophila axonogenesis and synaptogenesis. Development 136: 3099-3107.
48. Zandy NL, Pendergast AM, (2008) Abl tyrosine kinases modulate cadherin-dependent adhesion upstream and downstream of Rho family GTPases. Cell Cycle 7: 444-448.
49. Zandy NL, Playford M, Pendergast AM, (2007) Abl tyrosine kinases regulate cell-cell adhesion through Rho GTPases. Proc Natl Acad Sci U S A 104: 17686-17691.
50. de Jong R, Haataja L, Voncken JW, Heisterkamp N, Groffen J, (1995) Tyrosine phosphorylation of murine Crkl. Oncogene 11: 1469-1474.
51. Krystal GW, Honsawek S, Litz J, Buchdunger E, (2000) The selective tyrosine kinase inhibitor STI571 inhibits small cell lung cancer growth. Clin Cancer Res 6: 3319-3326.
52. McGary EC, Weber K, Mills L, Doucet M, Lewis V, et al. (2002) Inhibition of platelet-derived growth factor-mediated proliferation of osteosarcoma cells by the novel tyrosine kinase inhibitor STI571. Clin Cancer Res 8: 3584-3591.
53. Sini P, Cannas A, Koleske AJ, Di Fiore PP, Scita G, (2004) Abl-dependent tyrosine phosphorylation of Sos-1 mediates growth-factor-induced Rac activation. Nat Cell Biol 6: 268-274.
54. Ly KT, Casanova JE, (2009) Abelson tyrosine kinase facilitates Salmonella enterica serovar Typhimurium entry into epithelial cells. Infect Immun 77: 60-69.
55. Harmon B, Campbell N, Ratner L, (2010) Role of Abl Kinase and the Wave2 Signaling Complex in HIV-1 Entry at a Post-Hemifusion Step. PLoS Pathog 6: e1000956.
56. Nolz JC, Nacusi LP, Segovis CM, Medeiros RB, Mitchell JS, et al. (2008) The WAVE2 complex regulates T cell receptor signaling to integrins via Abl- and CrkL-C3G-mediated activation of Rap1. J Cell Biol 182: 1231-1244.
57. Stuart JR, Gonzalez FH, Kawai H, Yuan Z-M, (2006) c-Abl Interacts with the WAVE2 Signaling Complex to Induce Membrane Ruffling and Cell Spreading. J Biol Chem 281: 31290-31297.
58. Suetsugu S, Kurisu S, Oikawa T, Yamazaki D, Oda A, et al. (2006) Optimization of WAVE2 complex-induced actin polymerization by membrane-bound IRSp53, PIP(3), and Rac. J Cell Biol 173: 571-585.
59. Dubielecka PM, Ladwein KI, Xiong X, Migeotte I, Chorzalska A, et al. (2011) Essential role for Abi1 in embryonic survival and WAVE2 complex integrity. Proc Natl Acad Sci U S A 108: 7022-7027.
60. Baum B, Perrimon N, (2001) Spatial control of the actin cytoskeleton in Drosophila epithelial cells. Nat Cell Biol 3: 883-890.
61. Bradley WD, Koleske AJ, (2009) Regulation of cell migration and morphogenesis by Abl-family kinases: emerging mechanisms and physiological contexts. J Cell Sci 122: 3441-3454.
62. Grevengoed EE, Loureiro JJ, Jesse TL, Peifer M, (2001) Abelson kinase regulates epithelial morphogenesis in Drosophila. J Cell Biol 155: 1185-1198.
63. Loureiro J, Peifer M, (1998) Roles of Armadillo, a Drosophila catenin, during central nervous system development. Curr Biol 8: 622-632.
64. Eckert MA, Lwin TM, Chang AT, Kim J, Danis E, et al. (2011) Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell 19: 372-386.
65. Micalizzi DS, Farabaugh SM, Ford HL, (2010) Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J Mammary Gland Biol Neoplasia 15: 117-134.
66. Qin Q, Xu Y, He T, Qin C, Xu J, (2012) Normal and disease-related biological functions of Twist1 and underlying molecular mechanisms. Cell Res 22: 90-106.
67. Otani T, Ichii T, Aono S, Takeichi M, (2006) Cdc42 GEF Tuba regulates the junctional configuration of simple epithelial cells. J Cell Biol 175: 135-146.
68. Ryu JR, Echarri A, Li R, Pendergast AM, (2009) Regulation of cell-cell adhesion by Abi/Diaphanous complexes. Mol Cell Biol 29: 1735-1748.
69. Silva JM, Ezhkova E, Silva J, Heart S, Castillo M, et al. (2009) Cyfip1 is a putative invasion suppressor in epithelial cancers. Cell 137: 1047-1061.
70. Debnath J, Muthuswamy SK, Brugge JS, (2003) Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30: 256-268.
71. Shi J, Scita G, Casanova JE, (2005) WAVE2 signaling mediates invasion of polarized epithelial cells by Salmonella typhimurium. J Biol Chem 280: 29849-29855.
72. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, et al. (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117: 927-939.
73. Ireton RC, Davis MA, van Hengel J, Mariner DJ, Barnes K, et al. (2002) A novel role for p120 catenin in E-cadherin function. J Cell Biol 159: 465-476.
74. Jackson P, Baltimore D, (1989) N-terminal mutations activate the leukemogenic potential of the myristoylated form of c-abl. Embo J 8: 449-456.
75. Sossey-Alaoui K, Head K, Nowak N, Cowell JK, (2003) Genomic organization and expression profile of the human and mouse WAVE gene family. Mamm Genome 14: 314-322.
76. Alexander NR, Tran NL, Rekapally H, Summers CE, Glackin C, et al. (2006) N-cadherin gene expression in prostate carcinoma is modulated by integrin-dependent nuclear translocation of Twist1. Cancer Res 66: 3365-3369.
77. Sossey-Alaoui K, Ranalli TA, Li X, Bakin AV, Cowell JK, (2005) WAVE3 promotes cell motility and invasion through the regulation of MMP-1, MMP-3, and MMP-9 expression. Exp Cell Res 308: 135-145.
78. Takahashi Y, Hamada J, Murakawa K, Takada M, Tada M, et al. (2004) Expression profiles of 39 HOX genes in normal human adult organs and anaplastic thyroid cancer cell lines by quantitative real-time RT-PCR system. Exp Cell Res 293: 144-153.
79. Wang BJ, Zhang ZQ, Ke Y, (2006) Conversion of cadherin isoforms in cultured human gastric carcinoma cells. World J Gastroenterol 12: 966-970.