Src, p130Cas, and Mechanotransduction in Cancer Cells

Genes and Cancer

Volumn 3, Issue 5-6, 2012, Pages 394-401

  Matsui, Hiroyuki ^a   Harada, Ichiro ^a   Sawada, Yasuhiro ^a,b,c  

^a Nadogaya Hosp   (Japan)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

anchorage independent cell growth; cancer; mechanotransduction; p130Cas; Src

Indexed keywords

CRK ASSOCIATED SUBSTRATE PROTEIN; FOCAL ADHESION KINASE; INTEGRIN; ION CHANNEL; PROTEIN TYROSINE KINASE;

ACTIN FILAMENT; AMINO TERMINAL SEQUENCE; ARTICLE; CANCER CELL; CANCER CONTROL; CANCER GROWTH; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL ADHESION; CELL DIFFERENTIATION; CELL INTERACTION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; CELL VIABILITY; CYTOSKELETON; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MECHANOTRANSDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

EID: 84875547010     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: 10.1177/1947601912461443     Document Type: Article

References (106)

1. Hoffman BD,Grashoff C,Schwartz MA.Dynamic molecular processes mediate cellular mechanotransduction.Nature. 2011;475:316-23.
2. Desgrosellier JS,Barnes LA,Shields DJ, et al.An integrin alpha(v)beta(3)-c-Src oncogenic unit promotes anchorage-independence and tumor progression.Nat Med. 2009;15:1163-9.
3. Cabodi S,Tinnirello A,Bisaro B, et al.p130Cas is an essential transducer element in ErbB2 transformation.FASEB J. 2010;24:3796-808.
4. Hanahan D,Weinberg RA.Hallmarks of cancer: the next generation.Cell. 2011;144:646-74.
5. Eisenmann KM,McCarthy JB,Simpson MA, et al.Melanoma chondroitin sulphate proteoglycan regulates cell spreading through Cdc42, Ack-1 and p130cas.Nat Cell Biol. 1999;1:507-13.
6. Avizienyte E,Wyke AW,Jones RJ, et al.Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signalling.Nat Cell Biol. 2002;4:632-8.
7. Li W,Lee J,Vikis HG, et al.Activation of FAK and Src are receptor-proximal events required for netrin signaling.Nat Neurosci. 2004;7:1213-21.
8. Sandilands E,Serrels B,McEwan DG, et al.Autophagic targeting of Src promotes cancer cell survival following reduced FAK signalling.Nat Cell Biol. 2012;14:51-60.
9. Vogel V,Sheetz M.Local force and geometry sensing regulate cell functions.Nat Rev Mol Cell Biol. 2006;7:265-75.
10. Desai RA,Gao L,Raghavan S,Liu WF,Chen CS.Cell polarity triggered by cell-cell adhesion via E-cadherin.J Cell Sci. 2009;122:905-11.
11. Dupont S,Morsut L,Aragona M, et al.Role of YAP/TAZ in mechanotransduction.Nature. 2011;474:179-83.
12. Fink J,Carpi N,Betz T, et al.External forces control mitotic spindle positioning.Nat Cell Biol. 2011;13:771-8.
13. Prager-Khoutorsky M,Lichtenstein A,Krishnan R, et al.Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing.Nat Cell Biol. 2011;13:1457-65.
14. Weber GF,Bjerke MA,DeSimone DW.A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration.Dev Cell. 2012;22:104-15.
15. Tzima E,Irani-Tehrani M,Kiosses WB, et al.A mechanosensory complex that mediates the endothelial cell response to fluid shear stress.Nature. 2005;437:426-31.
16. Maruthamuthu V,Sabass B,Schwarz US,Gardel ML.Cell-ECM traction force modulates endogenous tension at cell-cell contacts.Proc Natl Acad Sci U S A. 2011;108:4708-13.
17. Zhang H,Landmann F,Zahreddine H,Rodriguez D,Koch M,Labouesse M.A tension-induced mechanotransduction pathway promotes epithelial morphogenesis.Nature. 2011;471:99-103.
18. Nelson CM,Jean RP,Tan JL, et al.Emergent patterns of growth controlled by multicellular form and mechanics.Proc Natl Acad Sci U S A. 2005;102:11594-9.
19. Liu WF,Nelson CM,Tan JL,Chen CS.Cadherins, RhoA, and Rac1 are differentially required for stretch-mediated proliferation in endothelial versus smooth muscle cells.Circ Res. 2007;101:e44-52.
20. Vogel V,Sheetz MP.Cell fate regulation by coupling mechanical cycles to biochemical signaling pathways.Curr Opin Cell Biol. 2009;21:38-46.
21. Behrens J,Mareel MM,Van Roy FM,Birchmeier W.Dissecting tumor cell invasion: epithelial cells acquire invasive properties after the loss of uvomorulin-mediated cell-cell adhesion.J Cell Biol. 1989;108:2435-47.
22. Valastyan S,Weinberg RA.Tumor metastasis: molecular insights and evolving paradigms.Cell. 2011;147:275-92.
23. Ohsawa S,Sugimura K,Takino K,Xu T,Miyawaki A,Igaki T.Elimination of oncogenic neighbors by JNK-mediated engulfment in Drosophila.Dev Cell. 2011;20:315-28.
24. Cabodi S,Tinnirello A,Di Stefano P, et al.p130Cas as a new regulator of mammary epithelial cell proliferation, survival, and HER2-neu oncogene-dependent breast tumorigenesis.Cancer Res. 2006;66:4672-80.
25. Yeatman TJ.A renaissance for SRC.Nat Rev Cancer. 2004;4:470-80.
26. Cartwright CA,Eckhart W,Simon S,Kaplan PL.Cell transformation by pp60c-src mutated in the carboxy-terminal regulatory domain.Cell. 1987;49:83-91.
27. Xu W,Harrison SC,Eck MJ.Three-dimensional structure of the tyrosine kinase c-Src.Nature. 1997;385:595-602.
28. Young MA,Gonfloni S,Superti-Furga G,Roux B,Kuriyan J.Dynamic coupling between the SH2 and SH3 domains of c-Src and Hck underlies their inactivation by C-terminal tyrosine phosphorylation.Cell. 2001;105:115-26.
29. Cowan-Jacob SW,Fendrich G,Manley PW, et al.The crystal structure of a c-Src complex in an active conformation suggests possible steps in c-Src activation.Structure. 2005;13:861-71.
30. Irby RB,Mao W,Coppola D, et al.Activating SRC mutation in a subset of advanced human colon cancers.Nat Genet. 1999;21:187-90.
31. Cabodi S,del Pilar Camacho-Leal M,Di Stefano P,Defilippi P.Integrin signalling adaptors: not only figurants in the cancer story.Nat Rev Cancer. 2010;10:858-70.
32. Ruest PJ,Shin NY,Polte TR,Zhang X,Hanks SK.Mechanisms of CAS substrate domain tyrosine phosphorylation by FAK and Src.Mol Cell Biol. 2001;21:7641-52.
33. Abram CL,Courtneidge SA.Src family tyrosine kinases and growth factor signaling.Exp Cell Res. 2000;254:1-13.
34. Playford MP,Schaller MD.The interplay between Src and integrins in normal and tumor biology.Oncogene. 2004;23:7928-46.
35. Hsia DA,Mitra SK,Hauck CR, et al.Differential regulation of cell motility and invasion by FAK.J Cell Biol. 2003;160:753-67.
36. Webb DJ,Donais K,Whitmore LA, et al.FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly.Nat Cell Biol. 2004;6:154-61.
37. Kypta RM,Goldberg Y,Ulug ET,Courtneidge SA.Association between the PDGF receptor and members of the src family of tyrosine kinases.Cell. 1990;62:481-92.
38. Mori S,Ronnstrand L,Yokote K, et al.Identification of two juxtamembrane autophosphorylation sites in the PDGF beta-receptor: involvement in the interaction with Src family tyrosine kinases.EMBO J. 1993;12:2257-64.
39. Hansen K,Johnell M,Siegbahn A, et al.Mutation of a Src phosphorylation site in the PDGF beta-receptor leads to increased PDGF-stimulated chemotaxis but decreased mitogenesis.EMBO J. 1996;15:5299-313.
40. Tice DA,Biscardi JS,Nickles AL,Parsons SJ.Mechanism of biological synergy between cellular Src and epidermal growth factor receptor.Proc Natl Acad Sci U S A. 1999;96:1415-20.
41. 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;9:629-38.
42. Corey SJ,Anderson SM.Src-related protein tyrosine kinases in hematopoiesis.Blood. 1999;93:1-14.
43. Irby RB,Yeatman TJ.Role of Src expression and activation in human cancer.Oncogene. 2000;19:5636-42.
44. Finn RS.Targeting Src in breast cancer.Ann Oncol. 2008;19:1379-86.
45. Giaccone G,Zucali PA.Src as a potential therapeutic target in non-small-cell lung cancer.Ann Oncol. 2008;19:1219-23.
46. Boukerche H,Su ZZ,Prevot C,Sarkar D,Fisher PB.mda-9/Syntenin promotes metastasis in human melanoma cells by activating c-Src.Proc Natl Acad Sci U S A. 2008;105:15914-9.
47. Siu MK,Chan HY,Kong DS, et al.p21-activated kinase 4 regulates ovarian cancer cell proliferation, migration, and invasion and contributes to poor prognosis in patients.Proc Natl Acad Sci U S A. 2010;107:18622-7.
48. Cai H,Smith DA,Memarzadeh S,Lowell CA,Cooper JA,Witte ON.Differential transformation capacity of Src family kinases during the initiation of prostate cancer.Proc Natl Acad Sci U S A. 2011;108:6579-84.
49. Oneyama C,Hikita T,Nada S,Okada M.Functional dissection of transformation by c-Src and v-Src.Genes Cells. 2008;13:1-12.
50. Zhu S,Bjorge JD,Fujita DJ.PTP1B contributes to the oncogenic properties of colon cancer cells through Src activation.Cancer Res. 2007;67:10129-37.
51. Arias-Romero LE,Saha S,Villamar-Cruz O, et al.Activation of Src by protein tyrosine phosphatase 1B is required for ErbB2 transformation of human breast epithelial cells. Cancer Res. 2009;69:4582-8.
52. Yamamoto T,Ikawa S,Akiyama T, et al.Similarity of protein encoded by the human c-erb-B-2 gene to epidermal growth factor receptor.Nature. 1986;319:230-4.
53. Meyer C,Sevko A,Ramacher M, et al.Chronic inflammation promotes myeloid-derived suppressor cell activation blocking antitumor immunity in transgenic mouse melanoma model.Proc Natl Acad Sci U S A. 2011;108:17111-6.
54. Qian BZ,Li J,Zhang H, et al.CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011;475:222-5.
55. Zitvogel L,Kepp O,Galluzzi L,Kroemer G.Inflammasomes in carcinogenesis and anticancer immune responses.Nat Immunol. 2012;13:343-51.
56. Toutant M,Costa A,Studler JM,Kadare G,Carnaud M,Girault JA.Alternative splicing controls the mechanisms of FAK autophosphorylation.Mol Cell Biol. 2002;22:7731-43.
57. Felsenfeld DP,Schwartzberg PL,Venegas A,Tse R,Sheetz MP.Selective regulation of integrin-cytoskeleton interactions by the tyrosine kinase Src.Nat Cell Biol. 1999;1:200-6.
58. Wang Y,Botvinick EL,Zhao Y, et al.Visualizing the mechanical activation of Src.Nature. 2005;434:1040-5.
59. Boutahar N,Guignandon A,Vico L,Lafage-Proust MH.Mechanical strain on osteoblasts activates autophosphorylation of focal adhesion kinase and proline-rich tyrosine kinase 2 tyrosine sites involved in ERK activation.J Biol Chem. 2004;279:30588-99.
60. Shimizu T,Ueda J,Ho JC, et al.Dual inhibition of Src and GSK3 maintains mouse embryonic stem cells, whose differentiation is mechanically regulated by Src signaling.Stem Cells. 2012;30:1394-404.
61. Na S,Collin O,Chowdhury F, et al.Rapid signal transduction in living cells is a unique feature of mechanotransduction.Proc Natl Acad Sci U S A. 2008;105:6626-31.
62. Sawada Y,Tamada M,Dubin-Thaler BJ, et al.Force sensing by mechanical extension of the Src family kinase substrate p130Cas.Cell. 2006;127:1015-26.
63. Burnham MR,Bruce-Staskal PJ,Harte MT, et al.Regulation of c-SRC activity and function by the adapter protein CAS.Mol Cell Biol. 2000;20:5865-78.
64. Pellicena P,Miller WT.Processive phosphorylation of p130Cas by Src depends on SH3-polyproline interactions.J Biol Chem. 2001;276:28190-6.
65. Sakai R,Iwamatsu A,Hirano N, et al.A novel signaling molecule, p130, forms stable complexes in vivo with v-Crk and v-Src in a tyrosine phosphorylation-dependent manner.EMBO J. 1994;13:3748-56.
66. Honda H,Oda H,Nakamoto T, et al.Cardiovascular anomaly, impaired actin bundling and resistance to Src-induced transformation in mice lacking p130Cas.Nat Genet. 1998;19:361-5.
67. Goldberg GS,Alexander DB,Pellicena P,Zhang ZY,Tsuda H,Miller WT.Src phosphorylates Cas on tyrosine 253 to promote migration of transformed cells.J Biol Chem. 2003;278:46533-40.
68. Shin NY,Dise RS,Schneider-Mergener J,Ritchie MD,Kilkenny DM,Hanks SK.Subsets of the major tyrosine phosphorylation sites in Crk-associated substrate (CAS) are sufficient to promote cell migration.J Biol Chem. 2004;279:38331-7.
69. Zhang Y,Wolf-Yadlin A,Ross PL, et al.Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules.Mol Cell Proteomics. 2005;4:1240-50.
70. Nakamoto T,Sakai R,Honda H, et al.Requirements for localization of p130cas to focal adhesions.Mol Cell Biol. 1997;17:3884-97.
71. Nasertorabi F,Tars K,Becherer K, et al.Molecular basis for regulation of Src by the docking protein p130Cas.J Mol Recognit. 2006;19:30-8.
72. Polte TR,Hanks SK.Interaction between focal adhesion kinase and Crk-associated tyrosine kinase substrate p130Cas.Proc Natl Acad Sci U S A. 1995;92:10678-82.
73. Sawasdikosol S,Ravichandran KS,Lee KK,Chang JH,Burakoff SJ.Crk interacts with tyrosine-phosphorylated p116 upon T cell activation.J Biol Chem. 1995;270:2893-6.
74. Duong LT,Rodan GA.Integrin-mediated signaling in the regulation of osteoclast adhesion and activation.Front Biosci. 1998;3:d757-68.
75. Liu F,Sells MA,Chernoff J.Transformation suppression by protein tyrosine phosphatase 1B requires a functional SH3 ligand.Mol Cell Biol. 1998;18:250-9.
76. Cheresh DA,Leng J,Klemke RL.Regulation of cell contraction and membrane ruffling by distinct signals in migratory cells.J Cell Biol. 1999;146:1107-16.
77. Yi J,Kloeker S,Jensen CC, et al.Members of the Zyxin family of LIM proteins interact with members of the p130Cas family of signal transducers.J Biol Chem. 2002;277:9580-9.
78. Lai YJ,Chen CS,Lin WC,Lin FT.c-Src-mediated phosphorylation of TRIP6 regulates its function in lysophosphatidic acid-induced cell migration.Mol Cell Biol. 2005;25:5859-68.
79. Pratt SJ,Epple H,Ward M,Feng Y,Braga VM,Longmore GD.The LIM protein Ajuba influences p130Cas localization and Rac1 activity during cell migration.J Cell Biol. 2005;168:813-24.
80. Honda H,Nakamoto T,Sakai R,Hirai H.p130(Cas), an assembling molecule of actin filaments, promotes cell movement, cell migration, and cell spreading in fibroblasts.Biochem Biophys Res Commun. 1999;262:25-30.
81. Kawauchi K,Tan WW,Araki K, et al.p130Cas-dependent actin remodeling regulates myogenic differentiation.Biochem J. 2012;445:323-32.
82. Baldassarre M,Razinia Z,Brahme N,Buccione R,Calderwood DA.Filamin A controls matrix metalloprotease activity and regulates cell invasion in human fibrosarcoma cells.J Cell Sci. 2012;:17.
83. Rossier OM,Gauthier N,Biais N, et al.Force generated by actomyosin contraction builds bridges between adhesive contacts.EMBO J. 2010;29:1055-68.
84. Lo CM,Wang HB,Dembo M,Wang YL.Cell movement is guided by the rigidity of the substrate.Biophys J. 2000;79:144-52.
85. Sukharev SI,Martinac B,Arshavsky VY,Kung C.Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution.Biophys J. 1993;65:177-83.
86. Sukharev SI,Blount P,Martinac B,Blattner FR,Kung C.A large-conductance mechanosensitive channel in E. coli encoded by mscL alone.Nature. 1994;368:265-8.
87. Kung C,Martinac B,Sukharev S.Mechanosensitive channels in microbes.Annu Rev Microbiol. 2010;64:313-29.
88. Sawada Y,Sheetz MP.Force transduction by Triton cytoskeletons.J Cell Biol. 2002;156:609-15.
89. Tamada M,Sheetz MP,Sawada Y.Activation of a signaling cascade by cytoskeleton stretch.Dev Cell. 2004;7:709-18.
90. Sawada Y,Nakamura K,Doi K, et al.Rap1 is involved in cell stretching modulation of p38 but not ERK or JNK MAP kinase.J Cell Sci. 2001;114:1221-7.
91. Salgia R,Pisick E,Sattler M, et al.p130CAS forms a signaling complex with the adapter protein CRKL in hematopoietic cells transformed by the BCR/ABL oncogene.J Biol Chem. 1996;271:25198-203.
92. van der Flier S,Chan CM,Brinkman A, et al.BCAR1/p130Cas expression in untreated and acquired tamoxifen-resistant human breast carcinomas. Int J Cancer. 2000;89:465-8.
93. Pylayeva Y,Gillen KM,Gerald W,Beggs HE,Reichardt LF,Giancotti FG.Ras- and PI3K-dependent breast tumorigenesis in mice and humans requires focal adhesion kinase signaling.J Clin Invest. 2009;119:252-66.
94. Brabek J,Constancio SS,Siesser PF,Shin NY,Pozzi A,Hanks SK.Crk-associated substrate tyrosine phosphorylation sites are critical for invasion and metastasis of SRC-transformed cells.Mol Cancer Res. 2005;3:307-15.
95. Holcomb M,Rufini A,Barila D,Klemke RL.Deregulation of proteasome function induces Abl-mediated cell death by uncoupling p130CAS and c-CrkII.J Biol Chem. 2006;281:2430-40.
96. Kobashigawa Y,Sakai M,Naito M, et al.Structural basis for the transforming activity of human cancer-related signaling adaptor protein CRK.Nat Struct Mol Biol. 2007;14:503-10.
97. Paszek MJ,Zahir N,Johnson KR, et al.Tensional homeostasis and the malignant phenotype.Cancer Cell. 2005;8:241-54.
98. Levental KR,Yu H,Kass L, et al.Matrix crosslinking forces tumor progression by enhancing integrin signaling.Cell. 2009;139:891-906.
99. Lu H,Shah P,Ennis D, et al.The differentiation of skeletal muscle cells involves a protein-tyrosine phosphatase-alpha-mediated C-Src signaling pathway.J Biol Chem. 2002;277:46687-95.
100. Soriano P,Montgomery C,Geske R,Bradley A.Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice.Cell. 1991;64:693-702.
101. Nakamura I,Rodan GA,Duong le T.Distinct roles of p130Cas and c-Cbl in adhesion-induced or macrophage colony-stimulating factor-mediated signaling pathways in prefusion osteoclasts.Endocrinology. 2003;144:4739-41.
102. Wang E,Goldberg AR.Changes in microfilament organization and surface topogrophy upon transformation of chick embryo fibroblasts with Rous sarcoma virus.Proc Natl Acad Sci U S A. 1976;73:4065-9.
103. Fearon ER,Vogelstein B.A genetic model for colorectal tumorigenesis.Cell. 1990;61:759-67.
104. Munevar S,Wang Y,Dembo M.Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts.Biophys J. 2001;80:1744-57.
105. Chen CS.Mechanotransduction: a field pulling together?.J Cell Sci. 2008;121:3285-92.
106. Kraning-Rush CM,Califano JP,Reinhart-King CA.Cellular traction stresses increase with increasing metastatic potential.PLoS One. 2012;7:e32572.