Lipid incorporation inhibits src-dependent assembly of fibronectin and type i collagen by vascular smooth muscle cells

Circulation Research

Volumn 104, Issue 7, 2009, Pages 832-841

  Frontini, Matthew J ^a,b   O'neil, Caroline ^a   Sawyez, Cynthia ^a   Chan, Bosco M C ^b   Huff, Murray W ^a,b   Pickering, J Geoffrey ^a,b  

^a LONDON HEALTH SCIENCES CENTRE   (Canada)

^b WESTERN UNIVERSITY   (Canada)

Author keywords

Collagen; Fibronectin; Integrin; Lipids; Smooth muscle cell; Src

Indexed keywords

ACTIN; BIOCHEMICAL MARKER; COLLAGEN FIBRIL; COLLAGEN TYPE 1; FIBRONECTIN; FOCAL ADHESION KINASE; LIPID; LOW DENSITY LIPOPROTEIN; PROTEIN; SRC PROTEIN; TENSIN; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5; VERY LOW DENSITY LIPOPROTEIN; VINCULIN; ACTIN BINDING PROTEIN; FOCAL ADHESION KINASE 1; INTEGRIN ALPHAVBETA1; PROTEIN TYROSINE KINASE; PTK2 PROTEIN, HUMAN; TENSINS; VCL PROTEIN, HUMAN; VITRONECTIN RECEPTOR;

ARTICLE; ATHEROSCLEROTIC PLAQUE; CONTROLLED STUDY; CYTOSKELETON; FOAM CELL; FOCAL ADHESION; HUMAN; HUMAN CELL; LIPID STORAGE; MICROSCOPY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PHOSPHORYLATION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; ATHEROSCLEROSIS; CELL LINE; ENZYMOLOGY; GENETIC TRANSDUCTION; GENETICS; METABOLISM; PARTICLE SIZE; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TIME;

ATHEROSCLEROSIS; CELL LINE; COLLAGEN TYPE I; FIBRONECTINS; FOAM CELLS; FOCAL ADHESION KINASE 1; FOCAL ADHESIONS; HUMANS; LIPOPROTEINS, LDL; LIPOPROTEINS, VLDL; MICROFILAMENT PROTEINS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PARTICLE SIZE; PHENOTYPE; PHOSPHORYLATION; RECEPTORS, VITRONECTIN; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TIME FACTORS; TRANSDUCTION, GENETIC; VINCULIN;

EID: 65249121502     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.108.187302     Document Type: Article

References (34)

1. Ross R. The pathogenesis of atherosclerosis: A perspective for the 1990s. Nature. 1993;362:801-809.
2. Faggiotto A, Ross R, Harker L. Studies of hypercholesterolemia in the nonhuman primate. I. Changes that lead to fatty streak formation. Arteriosclerosis. 1984;4:323-340. (Pubitemid 14092676)
3. Glukhova MA, Ornatsky OI, Frid MG, Kabakov AE, Adany RR, Muszbek L, Smirnov VN. Identification of smooth muscle-derived foam cells in the atherosclerotic plaque of human aorta with monoclonal antibody IIG10. Tissue Cell. 1987;19:657-663.
4. Vollmer E, Roessner A, Bosse A, Bocker W, Kaesberg B, Robenek H, Sorg C, Winde G. Immunohistochemical double labeling of macrophages, smooth muscle cells, and apolipoprotein E in the atherosclerotic plaque. Pathol Res Pract. 1991;187:184-188.
5. Campbell JH, Popadynec L, Nestel PJ, Campbell GR. Lipid accumulation in arterial smooth muscle cells. Influence of phenotype. Atherosclerosis. 1983;47:279-295.
6. Argmann CA, Sawyez CG, Li S, Nong Z, Hegele RA, Pickering JG, Huff MW. Human smooth muscle cell subpopulations differentially accumulate cholesteryl ester when exposed to native and oxidized lipoproteins. Arterioscler Thromb Vasc Biol. 2004;24:1290-1296.
7. Feng B, Yao PM, Li Y, Devlin CM, Zhang D, Harding HP, Sweeney M, Rong JX, Kuriakose G, Fisher EA, Marks AR, Ron D, Tabas I. The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nat Cell Biol. 2003;5:781-792.
8. Rong JX, Kusunoki J, Oelkers P, Sturley SL, Fisher EA. Acyl-coenzymeA (CoA):cholesterol acyltransferase inhibition in rat and human aortic smooth muscle cells is nontoxic and retards foam cell formation. Arterioscler Thromb Vasc Biol. 2005;25:122-127.
9. Lee RT, Libby P. The unstable atheroma. Arterioscler Thromb Vasc Biol. 1997;17:1859-1867.
10. Williams BR, Gelman RA, Poppke DC, Piez KA. Collagen fibril formation. Optimal in vitro conditions and preliminary kinetic results. J Biol Chem. 1978;253:6578-6585.
11. Velling T, Risteli J, Wennerberg K, Mosher DF, Johansson S. Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins alpha 11beta 1 and alpha 2beta 1. J Biol Chem. 2002;277:37377-37381.
12. Li S, Van Den Diepstraten C, D'Souza SJ, Chan BM, Pickering JG. Vascular smooth muscle cells orchestrate the assembly of type I collagen viaα2β1 integrin, RhoA, and fibronectin polymerization. Am J Pathol. 2003;163:1045-1056.
13. Sottile J, Hocking DC. Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions. Mol Biol Cell. 2002;13:3546-3559.
14. Li S, Fan YS, Chow LH, Van Den Diepstraten C, van Der Veer E, Sims SM, Pickering JG. Innate diversity of adult human arterial smooth muscle cells: cloning of distinct subtypes from the internal thoracic artery. Circ Res. 2001;89:517-525.
15. Li S, Sims S, Jiao Y, Chow LH, Pickering JG. Evidence from a novel human cell clone that adult vascular smooth muscle cells can convert reversibly between noncontractile and contractile phenotypes. Circ Res. 1999;85:338-348.
16. Pickering JG, Chow LH, Li S, Rogers KA, Rocnik EF, Zhong R, Chan BM. alpha5beta1 integrin expression and luminal edge fibronectin matrix assembly by smooth muscle cells after arterial injury. Am J Pathol. 2000;156:453-465.
17. Rocnik EF, Van Der Veer E, Cao H, Hegele RA, Pickering JG. Functional linkage between the endoplasmic reticulum protein Hsp47 and pro-collagen expression in human vascular smooth muscle cells. J Biol Chem. 2002;277:38571-128578
18. Small TW, Bolender Z, Bueno C, O'Neil C, Nong Z, Rushlow W, Rajakumar N, Kandel C, Strong J, Madrenas J, Pickering JG. Wilms' tumor 1-associating protein regulates the proliferation of vascular smooth muscle cells. Circ Res. 2006;99:1338-1346.
19. Pickering JG, Uniyal S, Ford CM, Chau T, Laurin MA, Chow LH, Ellis CG, Fish J, Chan BM. Fibroblast growth factor-2 potentiates vascular smooth muscle cell migration to platelet-derived growth factor: Upregu-lation of alpha2beta1 integrin and disassembly of actin filaments. Circ Res. 1997;80:627-637.
20. Rong JX, Shapiro M, Trogan E, Fisher EA. Transdifferentiation of mouse aortic smooth muscle cells to a macrophage-like state after cholesterol loading. Proc Natl Acad Sci U S A. 2003;100:13531-13536.
21. Pankov R, Cukierman E, Katz BZ, Matsumoto K, Lin DC, Lin S, Hahn C, Yamada KM. Integrin dynamics and matrix assembly: Tensin-dependent translocation of alpha(5)beta(1) integrins promotes early fibronectin fibrillogenesis. J Cell Biol. 2000;148:1075-1090.
22. Zamir E, Katz M, Posen Y, Erez N, Yamada KM, Katz BZ, Lin S, Lin DC, Bershadsky A, Kam Z, Geiger B. Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts. Nat Cell Biol. 2000;2: 191-196.
23. 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.
24. Ren XD, Kiosses WB, Sieg DJ, Otey CA, Schlaepfer DD, Schwartz MA. Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J Cell Sci. 2000;113:3673-3678.
25. Ilic D, Kovacic B, Johkura K, Schlaepfer DD, Tomasevic N, Han Q, Kim JB, Howerton K, Baumbusch C, Ogiwara N, Streblow DN, Nelson JA, Dazin P, Shino Y, Sasaki K, Damsky CH. FAK promotes organization of fibronectin matrix and fibrillar adhesions. J Cell Sci. 2004;117:177-187.
26. Wierzbicka-Patynowski I, Schwarzbauer JE. Regulatory role for Src and phosphatidylinositol 3-kinase in initiation of fibronectin matrix assembly. J Biol Chem. 2002;277:19703-19708.
27. Cooper JA, Gould KL, Cartwright CA, Hunter T. Tyr527 is phosphory-lated in pp60c-src: Implications for regulation. Science. 1986;231: 1431-1434.
28. Gonfloni S, Weijland A, Kretzschmar J, Superti-Furga G. Crosstalk between the catalytic and regulatory domains allows bidirectional regulation of Src. Nat Struct Biol. 2000;7:281-286.
29. Canty EG, Starborg T, Lu Y, Humphries SM, Holmes DF, Meadows RS, Huffman A, O'Toole ET, Kadler KE. Actin filaments are required for fibripositor-mediated collagen fibril alignment in tendon. J Biol Chem. 2006;281:38592-38598.
30. Baneyx G, Baugh L, Vogel V. Fibronectin extension and unfolding within cell matrix fibrils controlled by cytoskeletal tension. Proc Natl Acad Sci U S A. 2002;99:5139-5143.
31. Brasaemle DL, Dolios G, Shapiro L, Wang R. Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J Biol Chem. 2004;279:46835-46842.
32. Pol A, Martin S, Fernandez MA, Ingelmo-Torres M, Ferguson C, Enrich C, Parton RG. Cholesterol and fatty acids regulate dynamic caveolin trafficking through the Golgi complex and between the cell surface and lipid bodies. Mol Biol Cell. 2005;16:2091-2105.
33. Deguchi JO, Aikawa E, Libby P, Vachon JR, Inada M, Krane SM, Whittaker P, Aikawa M. Matrix metalloproteinase-13/collagenase-3 deletion promotes collagen accumulation and organization in mouse atherosclerotic plaques. Circulation. 2005;112:2708-2715.
34. Dollery CM, Libby P. Atherosclerosis and proteinase activation. Cardiovasc Res. 2006;69:625-635.