Drosophila actin-Capping Protein limits JNK activation by the src proto-oncogene

Oncogene

Volumn 33, Issue 16, 2014, Pages 2027-2039

  Fernandez B G ^a   Jezowska, B ^a   Janody, F ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

capping protein; Drosophila wing discs epithelium; F actin; JNK signaling; Src family kinases

Indexed keywords

ACTIN CAPPING PROTEINS; ACTINS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; BLOTTING, WESTERN; CATENINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPITHELIUM; GREEN FLUORESCENT PROTEINS; IMAGINAL DISCS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICROSCOPY, CONFOCAL; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; RHO GTP-BINDING PROTEINS; WING;

EID: 84899417132     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.155     Document Type: Article

References (96)

1. Nowell PC. The clonal evolution of tumor cell populations. Science 1976; 194: 23-28
2. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990; 61: 759-767
3. Hariharan IK, Bilder D. Regulation of imaginal disc growth by tumor-suppressor genes in Drosophila. Annu Rev Genet 2006; 40: 335-361
4. Brumby AM, Richardson HE. Using Drosophila melanogaster to map human cancer pathways. Nat Rev Cancer 2005; 5: 626-639
5. Khoo P, Allan K, Willoughby L, Brumby AM, Richardson HE. RhoGEF2 cooperates with activated Ras in tumourigenesis through a pathway involving Rho1-Rok-Myosin II and JNK Signalling. Dis Model Mech (e-pub ahead of print 21 February 2013
6. Brumby AM, Goulding KR, Schlosser T, Loi S, Galea R, Khoo P, et al. Identification of novel Ras-cooperating oncogenes in Drosophila melanogaster: A RhoGEF/Rho-family/ JNK pathway is a central driver of tumorigenesis. Genetics 2011; 188: 105-125
7. Pagliarini RA, Xu T. A genetic screen in Drosophila for metastatic behavior. Science 2003; 302: 1227-1231
8. Brumby AM, Richardson HE. Scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila. Embo J 2003; 22: 5769-5779
9. Vidal M, Warner S, Read R, Cagan RL. Differing Src signaling levels have distinct outcomes in Drosophila. Cancer Res 2007; 67: 10278-10285
10. Leong GR, Goulding KR, Amin N, Richardson HE, Brumby AM. Scribble mutants promote aPKC and JNK-dependent epithelial neoplasia independently of Crumbs. BMC Biol 2009; 7: 62
11. Uhlirova M, Bohmann D. JNK-And Fos-regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila. EMBO J 2006; 25: 5294-5304
12. Igaki T, Pagliarini RA, Xu T. Loss of cell polarity drives tumor growth and invasion through JNK activation in Drosophila. Curr Biol 2006; 16: 1139-1146
13. Doggett K, Grusche FA, Richardson HE, Brumby AM. Loss of the Drosophila cell polarity regulator Scribbled promotes epithelial tissue overgrowth and cooperation with oncogenic Ras-Raf through impaired Hippo pathway signaling. BMC Dev Biol 11: 57
14. Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 2009; 9: 537-549
15. Vidal M, Larson DE, Cagan RL. Csk-deficient boundary cells are eliminated from normal Drosophila epithelia by exclusion, migration, and apoptosis. Dev Cell 2006; 10: 33-44
16. Read RD, Bach EA, Cagan RL. Drosophila C-Terminal Src kinase negatively regulates organ growth and cell proliferation through inhibition of the Src, Jun N-Terminal kinase, and STAT pathways. Mol Cell Biol 2004; 24: 6676-6689
17. Yeatman TJ. A renaissance for SRC. Nat Rev Cancer 2004; 4: 470-480
18. Nagao M, Kaziro Y, Itoh H. The Src family tyrosine kinase is involved in Rhodependent activation of c-Jun N-Terminal kinase by Galpha12. Oncogene 1999; 18: 4425-4434
19. Brunton VG, MacPherson IR, Frame MC. Cell adhesion receptors, tyrosine kinases and actin modulators: A complex three-way circuitry. Biochim Biophys Acta 2004; 1692: 121-144
20. Takahashi F, Endo S, Kojima T, Saigo K. Regulation of cell-cell contacts in developing Drosophila eyes by Dsrc41, a new, close relative of vertebrate c-src. Genes Dev 1996; 10: 1645-1656
21. Dodson GS, Guarnieri DJ, Simon MA. Src64 is required for ovarian ring canal morphogenesis during Drosophila oogenesis. Development 1998; 125: 2883-2892
22. Simon MA, Drees B, Kornberg T, Bishop JM. The nucleotide sequence and the tissue-specific expression of Drosophila c-src. Cell 1985; 42: 831-840
23. Tateno M, Nishida Y, Adachi-Yamada T. Regulation of JNK by Src during Drosophila development. Science 2000; 287: 324-327
24. Stewart RA, Li DM, Huang H, Xu T. A genetic screen for modifiers of the lats tumor suppressor gene identifies C-Terminal Src kinase as a regulator of cell proliferation in Drosophila. Oncogene 2003; 22: 6436-6444
25. Pedraza LG, Stewart RA, Li DM, Xu T. Drosophila Src-family kinases function with Csk to regulate cell proliferation and apoptosis. Oncogene 2004; 23: 4754-4762
26. Thomas JH, Wieschaus E. src64 and tec29 are required for microfilament contraction during Drosophila cellularization. Development 2004; 131: 863-871
27. Lu N, Guarnieri DJ, Simon MA. Localization of Tec29 to ring canals is mediated by Src64 and PtdIns(3,4,5)P3-dependent mechanisms. EMBO J 2004; 23: 1089-1100
28. Shindo M, Wada H, Kaido M, Tateno M, Aigaki T, Tsuda L, et al. Dual function of Src in the maintenance of adherens junctions during tracheal epithelial morphogenesis. Development 2008; 135: 1355-1364
29. Enomoto M, Igaki T. Src controls tumorigenesis via JNK-dependent regulation of the Hippo pathway in Drosophila. EMBO Rep 2012; 14: 65-72
30. Cooper JA, Sept D. New insights into mechanism and regulation of actin capping protein. Int Rev Cell Mol Biol 2008; 267: 183-206
31. Spiering D, Hodgson L. Dynamics of the Rho-family small GTPases in actin regulation and motility. Cell Adh Migr 2011; 5: 170-180
32. Somogyi K, Rorth P. Cortactin modulates cell migration and ring canal morphogenesis during Drosophila oogenesis. Mech Dev 2004; 121: 57-64
33. Bresnick AR. Molecular mechanisms of nonmuscle myosin-II regulation. Curr Opin Cell Biol 1999; 11: 26-33
34. Jezowska B, Fernandez BG, Amandio AR, Duarte P, Mendes C, Bras-Pereira C, et al. A dual function of Drosophila capping protein on DE-cadherin maintains epithelial integrity and prevents JNK-mediated apoptosis. Dev Biol 2011; 360: 143-159
35. Fernandez BG, Gaspar P, Bras-Pereira C, Jezowska B, Rebelo SR, Janody F. Actin-Capping Protein and the Hippo pathway regulate F-Actin and tissue growth in Drosophila. Development 2011; 138: 2337-2346
36. Sansores-Garcia L, Bossuyt W, Wada KI, Yonemura S, Tao C, Sasaki H, et al. Modulating F-Actin organization induces organ growth by affecting the Hippo pathway. EMBO J 2011; 30: 2325-2335
37. Huang J, Wu S, Barrera J, Matthews K, Pan D. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 2005; 122: 421-434
38. Oh H, Irvine KD. In vivo regulation of Yorkie phosphorylation and localization. Development 2008; 135: 1081-1088
39. Wear MA, Cooper JA. Capping protein binding to S100B: Implications for the tentacle model for capping the actin filament barbed end. J Biol Chem 2004; 279: 14382-14390
40. Kim K, Yamashita A, Wear MA, Maeda Y, Cooper JA. Capping protein binding to actin in yeast: Biochemical mechanism and physiological relevance. J Cell Biol 2004; 164: 567-580
41. Wear MA, Yamashita A, Kim K, Maeda Y, Cooper JA. How capping protein binds the barbed end of the actin filament. Curr Biol 2003; 13: 1531-1537
42. Janody F, Treisman JE. Actin capping protein {alpha} maintains vestigial-expressing cells within the Drosophila wing disc epithelium. Development 2006; 133: 3349-3357
43. Gates J, Nowotarski SH, Yin H, Mahaffey JP, Bridges T, Herrera C, et al. Enabled and Capping protein play important roles in shaping cell behavior during Drosophila oogenesis. Dev Biol 2009; 333: 90-107
44. Delalle I, Pfleger CM, Buff E, Lueras P, Hariharan IK. Mutations in the Drosophila orthologs of the F-Actin capping protein alpha-And beta-subunits cause actin accumulation and subsequent retinal degeneration. Genetics 2005; 171: 1757-1765
45. Fan Y, Bergmann A. The cleaved-Caspase-3 antibody is a marker of Caspase-9-like DRONC activity in Drosophila. Cell Death Differ 2010; 17: 534-539
46. Duffy JB. GAL4 system in Drosophila: A fly geneticist's Swiss army knife. Genesis 2002; 34: 1-15
47. Amatruda JF, Gattermeir DJ, Karpova TS, Cooper JA. Effects of null mutations and overexpression of capping protein on morphogenesis, actin distribution and polarized secretion in yeast. J Cell Biol 1992; 119: 1151-1162
48. Schafer DA, Mooseker MS, Cooper JA. Localization of capping protein in chicken epithelial cells by immunofluorescence and biochemical fractionation. J Cell Biol 1992; 118: 335-346
49. Wear MA, Cooper JA. Capping protein: New insights into mechanism and regulation. Trends Biochem Sci 2004; 29: 418-428
50. Kim JY, Lee YG, Kim MY, Byeon SE, Rhee MH, Park J, et al. Src-mediated regulation of inflammatory responses by actin polymerization. Biochem Pharmacol 2009; 79: 431-443
51. Desprat N, Supatto W, Pouille PA, Beaurepaire E, Farge E. Tissue deformation modulates twist expression to determine anterior midgut differentiation in Drosophila embryos. Dev Cell 2008; 15: 470-477
52. Giannone G, Sheetz MP. Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol 2006; 16: 213-223
53. Forster D, Luschnig S. Src42A-dependent polarized cell shape changes mediate epithelial tube elongation in Drosophila. Nat Cell Biol 2012; 14: 526-534
54. Nelson KS, Khan Z, Molnar I, Mihaly J, Kaschube M, Beitel GJ. Drosophila Src regulates anisotropic apical surface growth to control epithelial tube size. Nat Cell Biol 2012; 14: 518-525
55. Oktay M, Wary KK, Dans M, Birge RB, Giancotti FG. Integrin-mediated activation of focal adhesion kinase is required for signaling to Jun NH2-Terminal kinase and progression through the G1 phase of the cell cycle. J Cell Biol 1999; 145: 1461-1469
56. Saito K, Scharenberg AM, Kinet JP. Interaction between the Btk PH domain and phosphatidylinositol-3,4,5-Trisphosphate directly regulates Btk. J Biol Chem 2001; 276: 16201-16206
57. Reynolds AB, Roesel DJ, Kanner SB, Parsons JT. Transformation-specific tyrosine phosphorylation of a novel cellular protein in chicken cells expressing oncogenic variants of the avian cellular src gene. Mol Cell Biol 1989; 9: 629-638
58. Tsai YT, Su YH, Fang SS, Huang TN, Qiu Y, Jou YS, et al. Etk, a Btk family tyrosine kinase, mediates cellular transformation by linking Src to STAT3 activation. Mol Cell Biol 2000; 20: 2043-2054
59. Rawlings DJ, Scharenberg AM, Park H, Wahl MI, Lin S, Kato RM, et al. Activation of BTK by a phosphorylation mechanism initiated by SRC family kinases. Science 1996; 271: 822-825
60. Castano J, Solanas G, Casagolda D, Raurell I, Villagrasa P, Bustelo XR, et al. Specific phosphorylation of p120-catenin regulatory domain differently modulates its binding to RhoA. Mol Cell Biol 2007; 27: 1745-1757
61. Cozzolino M, Stagni V, Spinardi L, Campioni N, Fiorentini C, Salvati E, et al. p120 Catenin is required for growth factor-dependent cell motility and scattering in epithelial cells. Mol Biol Cell 2003; 14: 1964-1977
62. Chang YW, Bean RR, Jakobi R. Targeting RhoA/Rho kinase and p21-Activated kinase signaling to prevent cancer development and progression. Recent Pat Anticancer Drug Discov 2009; 4: 110-124
63. Neisch AL, Speck O, Stronach B, Fehon RG. Rho1 regulates apoptosis via activation of the JNK signaling pathway at the plasma membrane. J Cell Biol 2010; 189: 311-323
64. Warner SJ, Yashiro H, Longmore GD. The Cdc42/Par6/aPKC polarity complex regulates apoptosis-induced compensatory proliferation in epithelia. Curr Biol 2010; 20: 677-686
65. Magie CR, Pinto-Santini D, Parkhurst SM. Rho1 interacts with p120ctn and alphacatenin, and regulates cadherin-based adherens junction components in Drosophila. Development 2002; 129: 3771-3782
66. Fanning PJ, Emkey G, Smith RJ, Grodzinsky AJ, Szasz N, Trippel SB. Mechanical regulation of mitogen-Activated protein kinase signaling in articular cartilage. J Biol Chem 2003; 278: 50940-50948
67. Huang C, Rajfur Z, Borchers C, Schaller MD, Jacobson K. JNK phosphorylates paxillin and regulates cell migration. Nature 2003; 424: 219-223
68. Chan HL, Chou HC, Duran M, Gruenewald J, Waterfield MD, Ridley A, et al. Major role of epidermal growth factor receptor and Src kinases in promoting oxidative stress-dependent loss of adhesion and apoptosis in epithelial cells. J Biol Chem 2010; 285: 4307-4318
69. Kulshammer E, Uhlirova M. The actin cross-linker Filamin/Cheerio mediates tumor malignancy downstream of JNK signaling. J Cell Sci 2012; 126: 927-938
70. Smadja-Lamere N, Boulanger MC, Champagne C, Branton PE, Lavoie JN. JNKmediated phosphorylation of paxillin in adhesion assembly and tension-induced cell death by the adenovirus death factor E4orf4. J Biol Chem 2008; 283: 34352-34364
71. Rudrapatna VA, Cagan RL, Das TK. Drosophila cancer models. Dev Dyn 241: 107-118
72. Chen F. JNK-induced apoptosis, compensatory growth, and cancer stem cells. Cancer Res 2012; 72: 379-386
73. Ridley AJ. Rho proteins and cancer. Breast Cancer Res Treat 2004; 84: 13-19
74. Gomez del Pulgar T, Benitah SA, Valeron PF, Espina C, Lacal JC. Rho GTPase expression in tumourigenesis: Evidence for a significant link. Bioessays 2005; 27: 602-613
75. Shah V, Braverman R, Prasad GL. Suppression of neoplastic transformation and regulation of cytoskeleton by tropomyosins. Somat Cell Mol Genet 1998; 24: 273-280
76. Mahadev K, Raval G, Bharadwaj S, Willingham MC, Lange EM, Vonderhaar B, et al. Suppression of the transformed phenotype of breast cancer by tropomyosin-1. Exp Cell Res 2002; 279: 40-51
77. Mammoto A, Ingber DE. Cytoskeletal control of growth and cell fate switching. Curr Opin Cell Biol 2009; 21: 864-870
78. Yamamoto N, Okano T, Ma X, Adelstein RS, Kelley MW. Myosin II regulates extension, growth and patterning in the mammalian cochlear duct. Development 2009; 136: 1977-1986
79. Bischof J, Maeda RK, Hediger M, Karch F, Basler K. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci USA 2007; 104: 3312-3317
80. Whited JL, Cassell A, Brouillette M, Garrity PA. Dynactin is required to maintain nuclear position within postmitotic Drosophila photoreceptor neurons. Development 2004; 131: 4677-4686
81. Hay BA, Wolff T, Rubin GM. Expression of baculovirus P35 prevents cell death in Drosophila. Development 1994; 120: 2121-2129
82. Adachi-Yamada T, Fujimura-Kamada K, Nishida Y, Matsumoto K. Distortion of proximodistal information causes JNK-dependent apoptosis in Drosophila wing. Nature 1999; 400: 166-169
83. Harden N, Ricos M, Ong YM, Chia W, Lim L. Participation of small GTPases in dorsal closure of the Drosophila embryo: Distinct roles for Rho subfamily proteins in epithelial morphogenesis. J Cell Sci 1999; 112(Pt 3): 273-284
84. Luo L, Liao YJ, Jan LY, Jan YN. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev 1994; 8: 1787-1802
85. Spradling AC, Stern D, Beaton A, Rhem EJ, Laverty T, Mozden N, et al. The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes. Genetics 1999; 153: 135-177
86. Uemura T, Oda H, Kraut R, Hayashi S, Kotaoka Y, Takeichi M. Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev 1996; 10: 659-671
87. Hay BA, Wassarman DA, Rubin GM. Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 1995; 83: 1253-1262
88. Hamaratoglu F, Willecke M, Kango-Singh M, Nolo R, Hyun E, Tao C, et al. The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat Cell Biol 2006; 8: 27-36
89. Roulier EM, Panzer S, Beckendorf SK. The Tec29 tyrosine kinase is required during Drosophila embryogenesis and interacts with Src64 in ring canal development. Mol Cell 1998; 1: 819-829
90. Myster SH, Cavallo R, Anderson CT, Fox DT, Peifer M. Drosophila p120catenin plays a supporting role in cell adhesion but is not an essential adherens junction component. J Cell Biol 2003; 160: 433-449
91. Glise B, Bourbon H, Noselli S. hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 1995; 83: 451-461
92. Klein T, Arias AM. Different spatial and temporal interactions between Notch, wingless, and vestigial specify proximal and distal pattern elements of the wing in Drosophila. Dev Biol 1998; 194: 196-212
93. Calleja M, Moreno E, Pelaz S, Morata G. Visualization of gene expression in living adult Drosophila. Science 1996; 274: 253-255
94. Lee JD, Treisman JE. Sightless has homology to transmembrane acyltransferases and is required to generate active Hedgehog protein. Curr Biol 2001; 11: 1147-1152
95. Kurant E, Pai CY, Sharf R, Halachmi N, Sun YH, Salzberg A. Dorsotonals/homothorax, the Drosophila homologue of meis1, interacts with extradenticle in patterning of the embryonic PNS. Development 1998; 125: 1037-1048
96. Casares F, Mann RS. Control of antennal versus leg development in Drosophila. Nature 1998; 392: 723-726