Integrin mechanotransduction stimulates caveolin-1 phosphorylation and recruitment of Csk to mediate actin reorganization

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 288, Issue 2 57-2, 2005, Pages

  Radel, C ^a   Rizzo, V ^a,b  

^a ALBANY MEDICAL COLLEGE   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Caveolae; Myosin light chain; Shear stress

Indexed keywords

ACTIN; ANTIBODY; CAVEOLIN 1; INTEGRIN; MYOSIN LIGHT CHAIN; PEPTIDE; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN TYROSINE KINASE;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; AORTA; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM CELL; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MECHANOTRANSDUCTION; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; SHEAR STRESS; SWINE; WESTERN BLOTTING;

ACTINS; ANIMALS; ANTIGENS, CD29; AORTA, THORACIC; CATTLE; CAVEOLIN 1; CAVEOLINS; CELLS, CULTURED; CYTOSKELETAL PROTEINS; ENDOTHELIUM, VASCULAR; FOCAL ADHESIONS; MECHANOTRANSDUCTION, CELLULAR; MYOSIN LIGHT CHAINS; PAXILLIN; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; STRESS, MECHANICAL;

EID: 12344250442     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.00519.2004     Document Type: Article

References (52)

1. Aoki T, Nomura R, and Fujimoto T. Tyrosine phosphorylation of caveolin-1 in the endothelium. Exp Cell Res 253: 629-636, 1999.
2. Arthur WT, Fetch LA, and Burridge K. Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr Biol 10: 719-722, 2000.
3. 5 integrin, and interferes with HeLa cell spreading. Mol Cell Biol 15: 711-722, 1995.
4. Birukov KG, Birukova AA, Dudek SM, Verin AD, Crow MT, Zhan X, DePaola N, and Garcia JG. Shear stress-mediated cytoskeletal remodeling and cortactin translocation in pulmonary endothelial cells. Am J Respir Cell Mol Biol 26: 453-464, 2002.
5. Cao H, Courchesne WE, and Mastick CC. A phosphotyrosine-dependent protein interaction screen reveals a role for phosphorylation of caveolin-1 on tyrosine 14: recruitment of C-terminal Src kinase. J Biol Chem 277: 8771-8774, 2002.
6. Chapman HA, Wei Y, Simon DI, and Waltz DA. Role of urokinase receptor and caveolin in regulation of integrin signaling. Thromb Haemost 82: 291-297, 1999.
7. Chen KD, Li YS, Kim M, Li S, Yuan S, Chien S, and Shyy JY. Mechanotransduction in response to shear stress. Roles of receptor tyrosine kinases, integrins, and Shc. J Biol Chem 274: 18393-18400, 1999.
8. Cheresh DA, Leng J, and Klemke RL. Regulation of cell contraction and membrane ruffling by distinct signals in migratory cells. J Cell Biol 146: 1107-1116, 1999.
9. Couet J, Li S, Okamoto T, Ikezu T, and Lisanti MP. Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J Biol Chem 272: 6525-6533, 1997.
10. Davies PF. Mechanical sensing mechanisms: shear stress and endothelial cells. J Vasc Surg 13: 729-731, 1991.
11. Davies PF. Flow-mediated endothelial mechanotransduction. Physiol Rev 75: 519-560, 1995.
12. Davies PF, Robotewskyj A, and Griem ML. Quantitative studies of endothelial cell adhesion. Directional remodeling of focal adhesion sites in response to flow forces. J Clin Invest 93: 2031-2038, 1994.
13. DePaola N, Davies PF, Pritchard WF Jr, Florez L, Harbeck N, and Polacek DC. Spatial and temporal regulation of gap junction connexin43 in vascular endothelial cells exposed to controlled disturbed flows in vitro. Proc Natl Acad Sci USA 96: 3154-3159, 1999.
14. DePaola N, Gimbrone MA Jr, Davies PF, and Dewey CF Jr. Vascular endothelium responds to fluid shear stress gradients. Arterioscler Thromb 12: 1254-1257, 1992.
15. Dudek SM, Birukov KG, Zhan S, and Garcia JG. Novel interaction of cortactin with endothelial cell myosin light chain kinase. Biochem Biophys Res Commun 298: 511-519, 2002.
16. Dudek SM, Jacobson JR, Chiang ET, Birukov KG, Wang P, Zhan X, and Garcia JG. Pulmonary endothelial cell barrier enhancement by sphingosine 1-phosphate: roles for cortactin and myosin light chain kinase. J Biol Chem 279: 24692-24700, 2004.
17. Engelman JA, Wykoff CC, Yasuhara S, Song KS, Okamoto T, and Lisanti MP. Recombinant expression of caveolin-1 in oncogenically transformed cells abrogates anchorage-independent growth. J Biol Chem 272: 16374-16381, 1997.
18. Garcia JG, Davis HW, and Patterson CE. Regulation of endothelial cell gap formation and barrier dysfunction: role of myosin light chain phosphorylation. J Cell Physiol 163: 510-522, 1995.
19. src. Am J Physiol Lung Cell Mol Physiol 276: L989-L998, 1999.
20. Girard PR and Nerem RM. Shear stress modulates endothelial cell morphology and F-actin organization through the regulation of focal adhesion-associated proteins. J Cell Physiol 163: 179-193, 1995.
21. Glenney JR Jr and Soppet D. Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts. Proc Natl Acad Sci USA 89: 10517-10521, 1992.
22. Han DC, Shen TL, and Guan JL. Role of Grb7 targeting to focal contacts and its phosphorylation by focal adhesion kinase in regulation of cell migration. J Biol Chem 275: 28911-28917, 2000.
23. Harada N, Masuda M, and Fujiwara K. Fluid flow and osmotic stress induce tyrosine phosphorylation of an endothelial cell 128 kDa surface glycoprotein. Biochem Biophys Res Commun 214: 69-74, 1995.
24. 1 integrins and tyrosine kinases. Circ Res 79: 310-316, 1996.
25. Jalali S, del Pozo MA, Chen K, Miao H, Li Y, Schwartz MA, Shyy JY, and Chien S. Integrin-mediated mechanotransduction requires its dynamic interaction with specific extracellular matrix (ECM) ligands. Proc Natl Acad Sci USA 98: 1042-1046, 2001.
26. Jalali S, Li YS, Sotoudeh M, Yuan S, Li S, Chien S, and Shyy JY. Shear stress activates p60src-Ras-MAPK signaling pathways in vascular endothelial cells. Arterioscler Thromb Vasc Biol 18: 227-234, 1998.
27. Klemke RL, Leng J, Molander R, Brooks PC, Vuori K, and Cheresh DA. CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J Cell Biol 140: 961-972, 1998.
28. Kuchan MJ, Jo H, and Frangos JA. Role of G proteins in shear stress-mediated nitric oxide production by endothelial cells. Am J Physiol Cell Physiol 267: C753-C758, 1994.
29. Lee H, Volonte D, Galbiati F, Iyengar P, Lublin DM, Bregman DB, Wilson MT, Campos-Gonzalez R, Bouzahzah B, Pestell RG, Scherer PE, and Lisanti MP. Constitutive and growth factor-regulated phosphorylation of caveolin-1 occurs at the same site (Tyr-14) in vivo: identification of a c-Src/Cav-1/Grb7 signaling cassette. Mol Endocrinol 14: 1750-1775, 2000.
30. Lowry WE, Huang J, Ma YC, Ali S, Wang D, Williams DM, Okada M, Cole PA, and Huang XY. Csk, a critical link of g protein signals to actin cytoskeletal reorganization. Dev Cell 2: 733-744, 2002.
31. Maekawa M, Ishizaki T, Boku S, Watanabe N, Fujita A, Iwamatsu A, Obinata T, Ohashi K, Mizuno K, and Narumiya S. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285: 895-898, 1999.
32. Mayer BJ and Baltimore D. Signalling through SH2 and SH3 domains. Trends Cell Biol 3: 8-13, 1993.
33. Nomura R and Fujimoto T. Tyrosine-phosphorylated caveolin-1: immunolocalization and molecular characterization. Mol Biol Cell 10: 975-986, 1999.
34. Ohno M, Gibbons GH, Dzau VJ, and Cooke JP. Shear stress elevates endothelial cGMP. Role of a potassium channel and G protein coupling. Circulation 88: 193-197, 1993.
35. cas tyrosine phosphorylation requires calcium-dependent. c-Src activation. J Biol Chem 274: 26803-26809, 1999.
36. Osawa M, Masuda M, Harada N, Lopes RB, and Fujiwara K. Tyrosine phosphorylation of platelet endothelial cell adhesion molecule-1 (PECAM-1, CD31) in mechanically stimulated vascular endothelial cells. Eur J Cell Biol 72: 229-237, 1997.
37. Park H, Go YM, Darji R, Choi JW, Lisanti MP, Maland MC, and Jo H. Caveolin-1 regulates shear stress-dependent activation of extracellular signal-regulated kinase. Am J Physiol Heart Circ Physiol 278: H1285-H1293, 2000.
38. Rizzo V, McIntosh DP, Oh P, and Schnitzer JE. In situ flow activates endothelial nitric oxide synthase in luminal caveolae of endothelium with rapid caveolin dissociation and calmodulin association. J Biol Chem 273: 34724-34729, 1998.
39. Rizzo V, Morton C, DePaola N, Schnitzer JE, and Davies PF. Recruitment of endothelial caveolae into mechanotransduction pathways by flow conditioning in vitro. Am J Physiol Heart Circ Physiol 285: H1720-H1729, 2003.
40. Rizzo V, Sung A, Oh P, and Schnitzer JE. Rapid mechanotransduction in situ at the luminal cell-surface of vascular endothelium and its caveolae. J Biol Chem 273: 26323-26329, 1998.
41. Rubanyi GM. Ionic mechanisms involved in the flow- and pressure-sensor function of the endothelium. Z Kardiol 80, Suppl 7: 91-94, 1991.
42. Sanguinetti AR, Cao H, and Corley Mastick C. Fyn is required for oxidative- and hyperosmotic-stress-induced tyrosine phosphorylation of caveolin-1. Biochem J 376: 159-168, 2003.
43. Shyy JY and Chien S. Role of integrins in endothelial mechanosensing of shear stress. Circ Res 91: 769-775, 2002.
44. 2+-binding protein p22 associates with microtubules in an N-myristoylation-dependent manner. Mol Biol Cell 10: 3473-3488, 1999.
45. Totsukawa G, Yamakita Y, Yamashiro S, Hartshorne DJ, Sasaki Y, and Matsumura F. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J Cell Biol 150: 797-806, 2000.
46. Tzima E, del Pozo MA, Shattil SJ, Chien S, and Schwartz MA. Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. EMBO J 20: 4639-4647, 2001.
47. 14) via activation of p38 mitogen-activated protein kinase and c-Src kinase. Evidence for caveolae, the actin cytoskeleton, and focal adhesions as mechanical sensors of osmotic stress. J Biol Chem 276: 8094-8103, 2001.
48. Wang Y, Miao H, Li S, Chen KD, Li YS, Yuan S, Shyy JY, and Chien S. Interplay between integrins and FLK-1 in shear stress-induced signaling. Am J Physiol Cell Physiol 283: C1540-C1547, 2002.
49. Wary KK, Mariotti A, Zurzolo C, and Giancotti FG. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94: 625-634, 1998.
50. 1 positive T lymphocytes. J Cell Biol 121: 1141-1152, 1993.
51. Wechezak AR, Viggers RF, and Sauvage LR. Fibronectin and F-actin redistribution in cultured endothelial cells exposed to shear stress. Lab Invest 53: 639-647, 1985.
52. Wei Y, Yang X, Liu Q, Wilkins JA, and Chapman HA. A role for caveolin and the urokinase receptor in integrin-mediated adhesion and signaling. J Cell Biol 144: 1285-1294, 1999.