Cyclic stretch induces reorientation of cells in a Src family kinase- and p130Cas-dependent manner

European Journal of Cell Biology

Volumn 91, Issue 2, 2012, Pages 118-128

  Niediek, Verena ^a   Born, Simone ^a   Hampe, Nico ^a   Kirchgeßner, Norbert ^a,b   Merkel, Rudolf ^a   Hoffmann, Bernd ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b ETH ZURICH   (Switzerland)

Author keywords

C Src; Cell reorientation; Cyclic stretch; Fyn; Mechanotransduction; P130Cas; Tyrosine phosphorylation; Yes

Indexed keywords

CRK ASSOCIATED SUBSTRATE PROTEIN; PROTEIN KINASE FYN; PROTEIN KINASE YES; PROTEIN TYROSINE KINASE;

ADHESION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DATA ANALYSIS; EMBRYO CELL; ENZYME ACTIVITY; ENZYME REGULATION; FIBROBLAST; MECHANOTRANSDUCTION; MEDICAL RECORD; MOUSE; MYOTATIC REFLEX; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSOR;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CRK-ASSOCIATED SUBSTRATE PROTEIN; FIBROBLASTS; FOCAL ADHESIONS; GENE KNOCKOUT TECHNIQUES; MECHANOTRANSDUCTION, CELLULAR; MICE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-FYN; PROTO-ONCOGENE PROTEINS C-YES; PYRAZOLES; PYRIMIDINES; RNA, SMALL INTERFERING; SRC-FAMILY KINASES; STRESS, MECHANICAL; TRANSFECTION;

EID: 84855538157     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2011.10.003     Document Type: Article

References (69)

1. Appleby M.W., Gross J.A., Cooke M.P., Levin S.D., Qian X., Perlmutter R.M. Defective T cell receptor signaling in mice lacking the thymic isoform of p59fyn. Cell 1992, 70:751-763.
2. Bain J., McLauchlan H., Elliott M., Cohen P. The specificities of protein kinase inhibitors: an update. Biochem. J. 2003, 371:199-204.
3. Balaban N.Q., Schwarz U.S., Riveline D., Goichberg P., Tzur G., Sabanay I., Mahalu D., Safran S., Bershadsky A., Addadi L., Geiger B. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nature Cell Biol. 2001, 3:466-472.
4. Bellis S.L., Miller J.T., Turner C.E. Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J. Biol. Chem. 1995, 270:17437-17441.
5. Birge R.B., Kalodimos C., Inagaki F., Tanaka S. Crk and CrkL adaptor proteins: networks for physiological and pathological signaling. Cell Commun. Signaling 2009, 7:13.
6. Boggon T.J., Eck M.J. Structure and regulation of Src family kinases. Oncogene 2004, 23:7918-7927.
7. Bouton A.H., Riggins R.B., Bruce-Staskal P.J. Functions of the adapter protein Cas: signal convergence and the determination of cellular responses. Oncogene 2001, 20:6448-6458.
8. Brown M.T., Cooper J.A. Regulation, substrates and functions of src. Biochim. Biophys. Acta 1996, 1287:121-149.
9. Butler J.P., Tolić-Nørrelykke I.M., Fabry B., Fredberg J.J. Traction fields, moments, and strain energy that cells exert on their surroundings. Am. J. Physiol. Cell. Physiol. 2002, 282:C595-C605.
10. Cary L.A., Klinghoffer R.A., Sachsenmaier C., Cooper J.A. SRC catalytic but not scaffolding function is needed for integrin-regulated tyrosine phosphorylation, cell migration, and cell spreading. Mol. Cell. Biol. 2002, 22:2427-2440.
11. Cesa C.M., Kirchgessner N., Mayer D., Schwarz U.S., Hoffmann B., Merkel R. Micropatterned silicone elastomer substrates for high resolution analysis of cellular force patterns. Rev. Sci. Instrum. 2007, 78:034301.
12. Collinsworth A.M., Torgan C.E., Nagda S.N., Rajalingam R.J., Kraus W.E., Truskey G.A. Orientation and length of mammalian skeletal myocytes in response to a unidirectional stretch. Cell Tissue Res. 2000, 302:243-251.
13. Curtis A., Wilkinson C. Topographical control of cells. Biomaterials 1997, 18:1573-1583.
14. Dadke D., Jarnik M., Pugacheva E.N., Singh M.K., Golemis E.A. Deregulation of HEF1 impairs M-phase progression by disrupting the RhoA activation cycle. Mol. Biol. Cell 2006, 17:1204-1217.
15. Defilippi P., Di Stefano P., Cabodi S. p130Cas: a versatile scaffold in signaling networks. Trends Cell Biol. 2006, 16:257-263.
16. Dembo M., Wang Y.L. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 1999, 76:2307-2316.
17. Discher D.E., Janmey P., Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
18. Eastwood M., Mudera V.C., McGrouther D.A., Brown R.A. Effect of precise mechanical loading on fibroblast populated collagen lattices: morphological changes. Cell Motil. Cytoskeleton 1998, 40:13-21.
19. Faust, U., Hampe, N., Rubner, W., Kirchgeßner, N., Safran, S., Hoffmann, B., Merkel, R. Cyclic stress at mHz frequencies aligns fibroblasts in direction of zero strain. PLoS ONE, in press.
20. Fonseca P.M., Shin N.Y., Brábek J., Ryzhova L., Wu J., Hanks S.K. Regulation and localization of CAS substrate domain tyrosine phosphorylation. Cell. Signalling 2004, 16:621-629.
21. Geiger B., Bershadsky A., Pankov R., Yamada K.M. Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2001, 2:793-805.
22. Geiger B., Spatz J.P., Bershadsky A.D. Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 2009, 10:21-33.
23. Giannone G., Sheetz M.P. Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol. 2006, 16:213-223.
24. Goldberg G.S., Alexander D.B., Pellicena P., Zhang Z.-Y., Tsuda H., Miller W.T. Src phosphorylates Cas on tyrosine 253 to promote migration of transformed cells. J. Biol. Chem. 2003, 278:46533-46540.
25. Gustavsson A., Yuan M., Fällman M. Temporal dissection of beta1-integrin signaling indicates a role for p130Cas-Crk in filopodia formation. J. Biol. Chem. 2004, 279:22893-22901.
26. Hanke J.H., Gardner J.P., Dow R.L., Changelian P.S., Brissette W.H., Weringer E.J., Pollok B.A., Connelly P.A. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 1996, 271:695-701.
27. Hayakawa K., Sato N., Obinata T. Dynamic reorientation of cultured cells and stress fibers under mechanical stress from periodic stretching. Exp. Cell Res. 2001, 268:104-114.
28. Herreman A., Serneels L., Annaert W., Collen D., Schoonjans L., De Strooper B. Total inactivation of gamma-secretase activity in presenilin-deficient embryonic stem cells. Nat. Cell Biol. 2000, 2:461-462.
29. Honda H., Nakamoto T., Sakai R., Hirai H. Cardiovascular anomaly, impaired actin bundling and resistance to Src-induced transformation in mice lacking p130Cas. Nat. Genet. 1998, 19:361-365.
30. Klemke R.L. CAS/Crk coupling serves as a molecular switch for induction of cell migration. J. Cell Biol. 1998, 140:961-972.
31. Klinghoffer R., Sachsenmaier C., Cooper J., Soriano P. Src family kinases are required for integrin but not PDGFR signal transduction. EMBO J. 1999, 18:2459-2471.
32. Küpper K., Lang N., Möhl C., Kirchgeßner N., Born S., Goldmann W.H., Hoffmann B., Merkel R. Tyrosine phosphorylation of vinculin at position 1065 modifies focal adhesion dynamics and cell tractions. Biochem. Biophys. Res. Commun. 2010, 399:560-564.
33. Langille B.L., Adamson S.L. Relationship between blood flow direction and endothelial cell orientation at arterial branch sites in rabbits and mice. Circ. Res. 1981, 48:481-488.
34. Li L., Okura M., Imamoto A. Focal adhesions require catalytic activity of Src family kinases to mediate integrin-matrix adhesion. Mol. Cell. Biol. 2002, 22:1203-1217.
35. Lord E. The use of range in place of standard deviation in the tau-test. Biometrika 1947, 34(1-2):41-67.
36. Ma A., Richardson A., Schaefer E.M., Parsons J.T. Serine phosphorylation of focal adhesion kinase in interphase and mitosis: a possible role in modulating binding to p130(Cas). Mol. Biol. Cell 2001, 12:1-12.
37. Martinac B., Adler J., Kung C. Mechanosensitive ion channels of E. coli activated by amphipaths. Nature 1990, 348:261-263.
38. Mayer B.J., Hirai H., Sakai R. Evidence that SH2 domains promote processive phosphorylation by protein-tyrosine kinases. Curr. Biol. 1995, 5:296-305.
39. Merkel R., Kirchgessner N., Cesa C.M., Hoffmann B. Cell force microscopy on elastic layers of finite thickness. Biophys. J. 2007, 93:3314-3323.
40. 2+ entry. J. Cell Sci. 2004, 117:85-92.
41. Möhl C., Kirchgessner N., Schäfer C., Küpper K., Born S., Diez G., Goldmann W.H., Merkel R., Hoffmann B. Becoming stable and strong: the interplay between vinculin exchange dynamics and adhesion strength during adhesion site maturation. Cell Motil. Cytoskeleton 2009, 66:350-364.
42. Moore P. The two-sample t-test based on range. Biometrika 1957, 44(3/4):482-489.
43. Naruse K., Yamada T., Sai X.R., Hamaguchi M., Sokabe M. Pp125FAK is required for stretch dependent morphological response of endothelial cells. Oncogene 1998, 17:455-463.
44. Ohba Y., Ikuta K., Ogura A., Matsuda J., Mochizuki N., Nagashima K., Kurokawa K., Mayer B.J., Maki K., Miyazaki J., Matsuda M. Requirement for C3G-dependent Rap1 activation for cell adhesion and embryogenesis. EMBO J. 2001, 20:3333-3341.
45. Rinne, H., 2003. Taschenbuch der Statistik, 4. vollständig überarbeitete und erweiterte Aufl. Verlag Harri Deutsch, Frankfurt/Main, Germany.
46. Ruest P.J., Shin N.Y., Polte T.R., Zhang X., Hanks S.K. Mechanisms of CAS substrate domain tyrosine phosphorylation by FAK and Src. Mol. Cell. Biol. 2001, 21:7641-7652.
47. Sai X., Naruse K., Sokabe M. Activation of pp60(src) is critical for stretch-induced orienting response in fibroblasts. J. Cell Sci. 1999, 112:1365-1373.
48. Sakai R., Iwamatsu A., Hirano N., Ogawa S., Tanaka T., Mano H., Yazaki Y., Hirai H. 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, 13:3748-3756.
49. Sawada Y., Tamada M., Dubin-Thaler B.J., Cherniavskaya O., Sakai R., Tanaka S., Sheetz M.P. Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 2006, 127:1015-1026.
50. Shin N.-Y., Dise R.S., Schneider-Mergener J., Ritchie M.D., Kilkenny D.M., Hanks S.K. Subsets of the major tyrosine phosphorylation sites in Crk-associated substrate (CAS) are sufficient to promote cell migration. J. Biol. Chem. 2004, 279:38331-38337.
51. 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.
52. Stein P.L., Lee H.M., Rich S., Soriano P. pp59fyn mutant mice display differential signaling in thymocytes and peripheral T cells. Cell 1992, 70:741-750.
53. Tachibana K., Urano T., Fujita H., Ohashi Y., Kamiguchi K., Iwata S., Hirai H., Morimoto C. Tyrosine phosphorylation of Crk-associated substrates by focal adhesion kinase. A putative mechanism for the integrin-mediated tyrosine phosphorylation of Crk-associated substrates. J. Biol. Chem. 1997, 272:29083-29090.
54. Tamada M., Sheetz M.P., Sawada Y. Activation of a signaling cascade by cytoskeleton stretch. Dev. Cell 2004, 7:709-718.
55. Thomas S.M., Brugge J.S. Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 1997, 13:513-609.
56. Thomas W.E., Trintchina E., Forero M., Vogel V., Sokurenko E.V. Bacterial adhesion to target cells enhanced by shear force. Cell 2002, 109:913-923.
57. Volberg T., Romer L., Zamir E., Geiger B. pp60(c-src) and related tyrosine kinases: a role in the assembly and reorganization of matrix adhesions. J. Cell Sci. 2001, 114:2279-2289.
58. Waschbüsch D., Born S., Niediek V., Kirchgessner N., Tamboli I.Y., Walter J., Merkel R., Hoffmann B. Presenilin 1 affects focal adhesion site formation and cell force generation via c-Src transcriptional and posttranslational regulation. J. Biol. Chem. 2009, 284:10138-10149.
59. Webb D.J., Donais K., Whitmore L.A., Thomas S.M., Turner C.E., Parsons J.T., Horwitz A.F. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell Biol. 2004, 6:154-161.
60. Webb D.J., Parsons J.T., Horwitz A.F. Adhesion assembly, disassembly and turnover in migrating cells - over and over and over again. Nat. Cell Biol. 2002, 4:E97-E100.
61. Wong A.J., Pollard T.D., Herman I.M. Actin filament stress fibers in vascular endothelial cells in vivo. Science 1983, 219:867-869.
62. Yoshigi M., Hoffman L.M., Jensen C.C., Yost H.J., Beckerle M.C. Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J. Cell Biol. 2005, 171:209-215.
63. Zaidel-Bar R., Cohen M., Addadi L., Geiger B. Hierarchical assembly of cell-matrix adhesion complexes. Biochem. Soc. Trans. 2004, 32:416-420.
64. Zaidel-Bar R., Itzkovitz S., Ma'ayan A., Iyengar R., Geiger B. Functional atlas of the integrin adhesome. Nat. Cell Biol. 2007, 9:858-867.
65. Zamir E., Katz B.Z., Aota S., Yamada K.M., Geiger B., Kam Z. Molecular diversity of cell-matrix adhesions. J. Cell Sci. 1999, 112:1655-1669.
66. Zhang X.A., He B., Zhou B., Liu L. Requirement of the p130CAS-Crk coupling for metastasis suppressor KAI1/CD82-mediated inhibition of cell migration. J. Biol. Chem. 2003, 278:27319-27328.
67. Zhang Z., Izaguirre G., Lin S.-Y., Lee H.Y., Schaefer E., Haimovich B. The phosphorylation of vinculin on tyrosine residues 100 and 1065, mediated by SRC kinases, affects cell spreading. Mol. Biol. Cell 2004, 15:4234-4247.
68. Zhong C., Chrzanowska-Wodnicka M., Brown J., Shaub A., Belkin A.M., Burridge K. Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J. Cell Biol. 1998, 141:539-551.
69. Zhu X., Kim J.L., Newcomb J.R., Rose P.E., Stover D.R., Toledo L.M., Zhao H., Morgenstern K.A. Structural analysis of the lymphocyte-specific kinase Lck in complex with non-selective and Src family selective kinase inhibitors. Structure 1999, 7:651-661.