Muscle costameric protein, Chisel/Smpx, associates with focal adhesion complexes and modulates cell spreading in vitro via a Rac1/p38 pathway

Experimental Cell Research

Volumn 307, Issue 2, 2005, Pages 367-380

  Schindeler, Aaron ^a   Lavulo, Lopeti ^a,c   Harvey, Richard P ^a,b  

^a VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Chisel; Costamere; Focal adhesion; Nkx2 5; p38; Rac1; Smpx

Indexed keywords

ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; BETA1 INTEGRIN; CELL EXTRACT; FIBRONECTIN; GUANOSINE TRIPHOSPHATASE; HEAT SHOCK PROTEIN 27; MITOGEN ACTIVATED PROTEIN KINASE P38; MUSCLE PROTEIN; MYC PROTEIN; PAXILLIN; PROTEIN CHISEL; PROTEIN SMPX; PROTEIN SUBUNIT; RAC1 PROTEIN; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; VINCULIN;

ANIMAL CELL; ARTICLE; CELL SPREADING; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; FILOPODIUM; IMMUNOPRECIPITATION; LAMELLIPODIUM; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

MURINAE;

EID: 20444397832     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2005.04.006     Document Type: Article

References (81)

1. I.N. Rybakova, J.R. Patel, and J.M. Ervasti The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin J. Cell Biol. 150 2000 1209 1214
2. J.M. Ervasti Costameres: the Achilles' heel of Herculean muscle J. Biol. Chem. 278 2003 13591 13594
3. C. Berthier, and S. Blaineau Supramolecular organization of the subsarcolemmal cytoskeleton of adult skeletal muscle fibers. A review Biol. Cell 89 1997 413 434
4. B.A. Danowski, K. Imanaka-Yoshida, J.M. Sanger, and J.W. Sanger Costameres are sites of force transmission to the substratum in adult rat cardiomyocytes J. Cell Biol. 118 1992 1411 1420
5. J. Stamler, and G. Meissner Physiology of nitric oxide in skeletal muscles Physiol. Rev. 81 2001 209 233
6. D.J. Blake, A. Weir, S.E. Newey, and K.E. Davies Function and genetics of dystrophin and dystrophin-related proteins in muscle Physiol. Rev. 82 2002 291 329
7. J.S. Davis, S. Hassanzadeh, S. Winitsky, H. Lin, C. Satorius, R. Vemuri, A.H. Aletras, H. Wen, and N.D. Epstein The overall patern of cardiac contraction depends on a spatial gradient of myosin regulatory light chain phosphorylation Cell 107 2001 631 641
8. J. Sadoshima, and S. Izumo The cellular and molecular response of cardiac myocytes to mechanical stress Annu. Rev. Physiol. 59 1997 551 571
9. G. Goldspink Changes in muscle mass and phenotype and the expression of autocrine and systemic growth factors by muscle in response to stretch and overload J. Anat. 194 1999 323 334
10. H. Hirota, J. Chen, U.A.K. Betz, K. Rajewsky, Y. Gu, J.J. Ross, W. Muller, and K.R. Chien Loss of a gp130 cardiac muscle cell survival pathway is a critical event in the onset of heart failure during biomechanical stress Cell 97 1999 189 198
11. R. Knoll, M. Hoshijima, H.M. Hoffman, V. Person, I. Lorenzen-Schmidt, M.L. Bang, T. Hayashi, N. Shiga, H. Yasukawa, W. Schaper, W. McKenna, M. Yokoyama, N.J. Schork, J.H. Omens, A.D. McCulloch, A. Kimura, C.C. Gregorio, W. Poller, J. Schaper, H.P. Schultheiss, and K.R. Chien The cardiac mechanical stretch sensor machinery involves a Z disc complex that is defective in a subset of human dilated cardiomyopathy Cell 111 2002 943 955
12. N.D. Epstein, and J.S. Davis Sensing stretch is fundamental Cell 112 2003 147 150
13. Y. Sawada, and M.P. Sheetz Force transduction by Triton cytoskeletons J. Cell Biol. 156 2002 609 615
14. O.C. Rodriguez, A.W. Schaefer, C.A. Mandato, P. Forscher, W.M. Bement, and C.M. Waterman-Storer Conserved mictrotubule-actin interactions in cell movement and morphogenesis Nat. Cell Biol. 5 2003 599
15. F. Duclos, V. Straub, S.A. Moore, D.P. Venzke, R.F. Hrstka, R.H. Crosbie, M. Durbeej, C.S. Lebakken, A.J. Ettinger, J. van der Meulen, K.H. Holt, L.E. Lim, J.R. Sanes, B.L. Davidson, J.A. Faulkner, R. Williamson, and K.P. Campbell Progressive muscular dystrophy in alpha-sarcoglycan-deficient mice J. Cell Biol. 142 1998 1461 1471
16. Y. Hosaka, T. Yokota, Y. Miyagoe-Suzuki, K. Yuasa, M. Imamura, R. Matsuda, T. Ikemoto, S. Kameya, and S. Takeda Alpha1-syntrophin-deficient skeletal muscle exhibits hypertrophy and aberrant formation of neuromuscular junctions during regeneration J. Cell Biol. 158 2002 1097 1107
17. A. Ishii, and S.H. Lo A role of tensin in skeletal-muscle regeneration Biochem. J. 356 2001 737 745
18. C.A. Collins, and J.E. Morgan Duchenne's muscular dystrophy: animal models used to investigate pathogenesis and develop therapeutic strategies Int. J. Exp. Pathol. 84 2003 165 172
19. M. Brancaccio, L. Fratta, A. Notte, E. Hirsch, R. Poulet, S. Guazzone, M. De Acetis, C. Vecchione, G. Marino, F. Altruda, L. Silengo, G. Tarone, and G. Lembo Melusin, a muscle-specific integrin beta(1)-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload Nat. Med. 9 2003 68 75
20. D. Patzak, O. Zhuchenko, C.C. Lee, and M. Wehnert Identification, mapping, and genomic structure of a novel X-chromosomal human gene (SMPX) encoding a small muscular protein Hum. Genet. 105 1999 506 512
21. S. Palmer, N. Groves, A. Schindeler, T. Yeoh, C. Biben, C.C. Wang, D.B. Sparrow, L. Barnett, N.A. Jenkins, N.G. Copeland, F. Koentgen, T. Mohun, and R.P. Harvey The small muscle-specific protein Csl modifies cell shape and promotes myocyte fusion in an insulin-like growth factor 1-dependent manner J. Cell Biol. 153 2001 985 998
22. T.J. Kemp, T.J. Sadusky, M. Simon, R. Brown, M. Eastwood, D.A. Sassoon, and G.R. Coulton Identification of a novel stretch-responsive skeletal muscle gene (Smpx) Genomics 72 2001 260 271
23. V.M. Christoffels, P.E. Habets, D. Franco, M. Campione, F. de Jong, W.H. Lamers, Z.Z. Bao, S. Palmer, C. Biben, R.P. Harvey, and A.F. Moorman Chamber formation and morphogenesis in the developing mammalian heart Dev. Biol. 223 2000 266 278
24. K. Burridge, and K. Wennerberg Rho and rac take centre stage Cell 116 2004 167 179
25. C.D. Nobes, and A. Hall Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia Cell 81 1995 53 62
26. C.D. Nobes, and A. Hall Rho GTPases control polarity, protrusion, and adhesion during cell movement J. Cell Biol. 144 1999 1235 1244
27. Y.-L. Hu, S. Li, T.-C. Tsou, M.A. del Pozo, and S. Chien Roles of microtubule dynamics and small GTPase Rac in endothelial cell migration and lamellipodium formation under flow J. Vasc. Res. 39 2002 465 476
28. M.A. del Pozo, W.B. Kiosses, N.B. Alderson, N. Meller, K.M. Hahn, and M.A. Schwartz Integrins regulate GTP-Rac localized effector interactions through dissociation of Rho-GDI Nat. Cell Biol. 4 2002 232 239
29. A.J. Putnam, J.J. Cunningham, B.B. Pillemer, and D.J. Mooney External mechanical strain regulates membrane targeting of Rho GTPases by controlling microtubule assembly Am. J. Physiol.: Cell Physiol. 284 2003 C627 C639
30. E.A. Clark, W.G. King, J.S. Brugge, M. Symons, and R.O. Hynes Integrin-mediated signals regulated by members of the rho family of GTPases J. Cell Biol. 142 1998 573 586
31. L.S. Price, J. Leng, M.A. Schwartz, and G.M. Bokoch Activation of Rac and Cdc42 by integrins mediates cell spreading Mol. Biol. Cell 9 1998 1863 1871
32. S. Eden, R. Rohatgi, A.V. Podtelejnikov, M. Mann, and M.W. Kirschner Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck Nature 418 2002 790 793
33. T. Takenawa, and H. Miki WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement J. Cell Sci. 114 2001 1801 1809
34. K.A. DeMali, C.A. Barlow, and K. Burridge Recruitment of the Arp2/3 complex to vinculin: coupling membrane protrusion to matrix adhesion J. Cell Biol. 159 2002 881 891
35. C. Brakebusch, and R. Fassler The integrin-actin connection, an external love affair EMBO J. 22 2003 2324 2333
36. W. Xu, H. Baribault, and E.D. Adamson Vinculin knockout results in heart and brain defects during embryonic development Development 125 1998 327 337
37. R.I. Ludowyke, J. Holst, L.M. Mudge, and A.T. Sim Transient translocation and activation of protein phosphatase 2A during mast cell secretion J. Biol. Chem. 275 2000 6144 6152
38. A. Lyubimova, A.D. Bershadsky, and A. Ben-Ze'ev Autoregulation of actin synthesis requires the 3′-UTR of actin mRNA and protects cells from actin overproduction J. Cell. Biochem. 76 1999 1 12
39. X.-D. Ren, W.B. Kiosses, and M.A. Schwartz Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton EMBO J. 18 1999 578 585
40. M.A. del Pozo, L.S. Price, N.B. Alderson, X.D. Ren, and M.A. Schwartz Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK EMBO J. 19 2000 2008 2014
41. S.K. Salstry, and K. Burridge Focal adhesions: a nexus for intracellular signalling and cytoskeletal dynamics Exp. Cell Res. 261 2000 25 36
42. J.C. Norman, D. Jones, S.T. Barry, M.R. Holt, S. Cockcroft, and D.R. Critchley ARF1 mediates paxillin recruitment to focal adhesions and potentiates Rho-stimulated stress fiber formation in intact and permeabilized Swiss 3T3 fibroblasts J. Cell Biol. 143 1998 1981 1995
43. B. Herman, and W.J. Pledger Platelet-derived growth factor-induced alterations in vinculin and actin distribution in Balb/c-3T3 cells J. Cell Biol. 100 1985 1031 1040
44. J.A. DePasquale, and C.S. Izzard Accumulation of talin in nodes at the edge of the lamellipodium and separate incorporation into adhesion plaques at focal contacts in fibroblasts J. Cell Biol. 113 1991 1351 1359
45. F.D. Brown, A.L. Rozelle, H.L. Yin, T. Balla, and J.G. Donaldson Phosphatidylinositol 4, 5-bisphosphate and Arf6-regulated membrane traffic J. Cell Biol. 154 2001 1007 1017
46. J.G. Donaldson Mulitple roles for Arf6: sorting, structuring, and signalling at the plasma membrane JBC 278 2003 41573 41576
47. E. Sandilands, C. Cans, V.J. Fincham, V.G. Brunton, H. Mellor, G.C. Prendergast, J.C. Norman, G. Superti-Furga, and M.C. Frame RhoB and actin polymerisation coordinate Src activation with endosome-mediated delivery to the membrane Dev. Cell 7 2004 855 869
48. A. Huttenlocher, R. Sandborg, and A.F. Horwitz Adhesion in cell migration Curr. Opin. Cell Biol. 7 1995 697 706
49. J.L. Coll, A. Ben-Zev'ev, R.M. Ezzell, J.L. Rodriguez Fernandez, H. Baribault, R.G. Oshima, and E.D. Adamson Targeted disruption of the vinculin gene in F9 and ES cells changes cell morphology, adhesion and locomotion Proc. Natl. Acad. Sci. 92 1995 9161 9165
50. D. Ilic, Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, and T. Yamamoto Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice Nature 377 1995 539 544
51. A. Nayal, D.J. Webb, and A.F. Horwitz Talin: an emerging focal point of adhesion dynamics Curr. Opin. Cell Biol. 16 2004 94 98
52. J. Suzuki, Y. Yamazaki, G. Li, Y. Kaziro, and H. Koide Involvement of Ras and Ral in chemotactic migration of skeletal myoblasts Mol. Cell. Biol. 20 2000 4658 4665
53. T.D. Pollard, and G. Borisy Cellular motility driven by assembly and disassembly of actin filaments Cell 112 2003 453 465
54. N. Lamarche, N. Tapon, L. Stowers, P.D. Burbelo, P. Aspenstrom, T. Bridges, J. Chant, and A. Hall Rac and Cdc42 induce actin polymerization and G1 cell cycle progression independently of p65PAK and the JNK/SAPK MAP kinase cascade Cell 87 1996 519 529
55. S. Wagner, T.A. Flood, P. O'Reilly, K. Hume, and L.A. Sabourin Association of the Ste20-like kinase (SLK) with the microtubule. Role in Rac1-mediated regulation of actin dynamics during cell adhesion and spreading J. Biol. Chem. 277 2002 37685 37692
56. H. Radhakrishna, O. Al-Awar, Z. Khachikian, and J.G. Donaldson ARF6 requirement for Rac ruffling suggests a role for membrane trafficking in cortical actin rearrangements J. Cell Sci. 112 1999 855 866
57. M. Uehata, T. Ishizaki, H. Satoh, T. Ono, T. Kawahara, T. Morishita, H. Tamakawa, K. Yamagami, J. Inui, M. Maekawa, and S. Narumiya Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension Nature 389 1997 990 994
58. C. Ballestrem, B. Hinz, B.A. Imhof, and B. Wehrle-Haller Marching at the front and dragging behind: differential αVβ3-integrin turnover regulates focal adhesion behaviour J. Cell Biol. 155 2001 1319 1332
59. C. Ballestrem, B. Wehrle-Haller, B. Hinz, and B.A. Imhof Actin-dependent lamellipodia formation and microtubule-dependent tail retraction control-directed cell migration Mol. Biol. Cell 11 2000 2999 3012
60. R. Conejo, and M. Lorenzo Insulin signaling leading to proliferation, survival, and membrane ruffling in C2C12 myoblasts J. Cell. Physiol. 187 2001 96 108
61. J.C. Hedges, M.A. Dechert, I.A. Yamboliev, J.L. Martin, E. Hickey, L.A. Weber, and W.T. Gerthoffer A role for p38(MAPK)/HSP27 pathway in smooth muscle cell migration J. Biol. Chem. 274 1999 24211 24219
62. S. Zhang, J. Han, M.A. Sells, J. Chernoff, U.G. Knaus, R.J. Ulevitch, and G.M. Bokoch Rho family GTPases regulate p38 mitogen-activated protein kinase through the downstream mediator Pak1 J. Biol. Chem. 270 1995 23934 23936
63. Y. Hou, R.E. Ye, and D.D. Browning Activation of the small GTPase Rac1 by cGMP-dependent protein kinase Cellular Signalling 16 2004 1061 1069
64. A.N. Abell, A.M. DeCathelineau, S.A. Weed, D.R. Ambruso, D.W. Riches, and G.L. Johnson Rac2D57N, a dominant inhibitory Rac2 mutant that inhibits p38 kinase signaling and prevents surface ruffling in bone-marrow-derived macrophages J. Cell Sci. 117 2003 243 255
65. L. New, Y. Jiang, M. Zhao, K. Liu, W. Zhu, L.J. Flood, Y. Kato, G.C. Parry, and J. Han PRAK, a novel protein kinase regulated by the p38 MAP kinase EMBO J. 17 1998 3372 3384
66. J. Landry, and J. Huot Modulation of actin dynamics during stress and physiological stimulation by a signaling pathway involving p38 MAP kinase and heat-shock protein 27 Biochem. Cell. Biol. 73 1995 703 707
67. S. Pichon, M. Bryckaert, and E. Berrou Control of actin dynamics by p38 MAP kinase-Hsp27 distribution in the lamellipodium of smooth muscle cells J. Cell Sci. 117 2004 2569 2577
68. H.L. Goel, and C.S. Dey Insulin stimulates spreading of skeletal muscle cells involving the activation of focal adhesion kinase, phosphatidylinositol 3-kinase and extracellular signal regulated kinases J. Cell. Physiol. 193 2002 187 198
69. E.H.J. Danen, and A. Sonnenberg Integrins in regulation of tissue development and function J. Pathol. 200 2003 471 480
70. R.L. Juliano, P. Reddig, S. Alahari, M. Edin, A. Howe, and A. Aplin Integrin regulation of cell signalling and motility Biochem. Soc. Trans. 32 2004 443 446
71. A. Cuenda, and D.R. Alessi Use of kinase inhibitors to dissect signalling pathways Methods Mol. Biol. 99 2000 161 175
72. J.A. Swanson, and C. Watts Macropinocytosis Trends Cell Biol. 5 1995 424 428
73. L. Lanzetti, A. Palamidessi, L. Areces, G. Scita, and P.P. Di Fiore Rab5 is a signalling GTPase involved in actin remodelling by receptor tyrosine kinases Nature 429 2004 309 314
74. V.S. Kraynov, C. Chamberlain, G.M. Bokoch, M.A. Schwartz, S. Slabaugh, and K.M. Hahn Localized Rac activation dynamics visualized in living cells Science 290 2000 333 337
75. M.A. del Pozo, N.B. Alderson, W.B. Kiosses, H.-H. Chiang, R.G.W. Anderson, and M.A. Schwartz Integrins regulate Rac targeting by internalisation of membrane domains Science 303 2004 839 842
76. A. Hall Rho GTPases and the actin cytoskeleton Science 279 1998 509 514
77. R. Kozma, S. Sarner, S. Ahmed, and L. Lim Rho family GTPases are neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid Mol. Cell. Biol. 17 1997 1201 1211
78. J. Guay, H. Lambert, G. Gingras-Breton, J.N. Lavoie, J. Huot, and J. Landry Regulationof actin filament dynamics by p38 map kinase-mediated phosphorylation of heatshock protein 27 J. Cell Sci. 110 1997 357 368
79. A. Cuenda, J. Rouse, Y.N. Doza, R. Meier, P. Cohen, T.F. Gallagher, P.R. Young, and J.C. Lee SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stress and interleukin-1 FEBS Lett. 364 1995 229 233
80. R.S. Piotrowicz, E. Hickey, and E.G. Levin Heat shock protein 27 kDa expression and phosphorylation regulates endothelial cell migration FASEB J. 12 1998 1481 1490
81. E. Furnish, W. Zhou, C. Cunningham, J. Kas, and C. Schmidt Gelsolin overexpression enhances neurite outgrowth in PC12 cells FEBS Lett. 508 2001 282 286