Migration and growth are attenuated in vascular smooth muscle cells with type VIII collagen-null alleles

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 26, Issue 1, 2006, Pages 56-61

  Adiguzel, Eser ^a   Hou, Guangpei ^a   Mulholland, Diane ^a   Hopfer, Ulrike ^b   Fukai, Naomi ^c   Olsen, Bjorn ^c   Bendeck, Michelle ^a,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF HAMBURG   (Germany)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Atherosclerosis; Collagen; MMP; Restenosis; Smooth muscle cell migration

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 8; THYMIDINE; COL8A2 PROTEIN, MOUSE; GELATINASE A; GELATINASE B;

ANIMAL CELL; AORTA; ARTICLE; ATHEROSCLEROSIS; BLOOD VESSEL INJURY; CELL ADHESION; CELL GROWTH; CELL MIGRATION; CONTROLLED STUDY; MOUSE; MOUSE STRAIN; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; WOUND; ZYMOGRAPHY; ALLELE; ANIMAL; CELL CULTURE; CELL DIVISION; CELL MOTION; CYTOLOGY; EXTRACELLULAR MATRIX; GENETICS; METABOLISM; MICROSCOPY; MOUSE MUTANT; PHYSIOLOGY; UPREGULATION;

ALLELES; ANIMALS; AORTA; CELL DIVISION; CELL MOVEMENT; CELLS, CULTURED; COLLAGEN TYPE I; COLLAGEN TYPE VIII; EXTRACELLULAR MATRIX; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; MICROSCOPY, VIDEO; MUSCLE, SMOOTH, VASCULAR; UP-REGULATION;

EID: 33644828771     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000194155.96456.b7     Document Type: Article

References (33)

1. Raines EW. The extracellular matrix can regulate vascular cell migration, proliferation, and survival: relationships to vascular disease. Int J Exp Pathol. 2000;81:173-182.
2. Koyama H, Raines EW, Bornfeldt KE, Roberts JM, Ross R. Fibrillar collagen inhibits arterial smooth muscle cell proliferation through regulation of Cdk2 inhibitors. Cell. 1996;87:1069-1078.
3. Carragher NO, Levkau B, Ross R, Raines EW. Degraded collagen fragments promote rapid disassembly of smooth muscle focal adhesions that correlates with cleavage of pp125(FAK), paxillin, and talin. J Cell Biol. 1999;147:619-630.
4. Ichii T, Koyama H, Tanaka S, Kim S, Shioi A, Okuno Y, Raines EW, Iwao H, Otani S, Nishizawa Y. Fibrillar collagen specifically regulates human vascular smooth muscle cell genes involved in cellular responses and the pericellular matrix environment. Circ Res. 2001;88:460-467.
5. Iraela-Arispe ML, Diglio CA, Sage EH. Modulation of extracellular matrix proteins by endothelial cells undergoing angiogenesis in vitro. Arterioscler Thromb. 1991;11:805-815.
6. Sage H, Pritzl P, Bornstein P. A unique, pepsin-sensitive collagen synthesized by aortic endothelial cells in culture. Biochemistry. 1980;19:5747-5755.
7. Rosenblum ND, Briscoe DM, Karnovsky MJ, Olsen BR. α1-VIII collagen is expressed in the rat glomerulus and in resident glomerular cells. Am J Physiol. 1993;264:F1003-F1010.
8. Rosenblum ND, Karnovsky MJ, Olsen BR. Non-fibrillar collagenous proteins synthesized by rat mesangial cells. J Am Soc Nephrol. 1990;1:785-791.
9. Plenz G, Deng MC, Robenek H, Volker W. Vascular collagens: spotlight on the role of type VIII collagen in atherogenesis. Atherosclerosis. 2003;166:1-11.
10. Bendeck MP, Regenass S, Tom WD, Giachelli CM, Schwartz SM, Hart C, Reidy MA. Differential expression of α1 type VIII collagen in injured, platelet-derived growth factor-BB stimulated rat carotid arteries. Circ Res. 1996;79:524-531.
11. Sibinga NES, Foster LC, Hsieh C-M, Perrella MA, Lee W-S, Endege WO, Sage EH, Lee M-E, Haber E. Collagen VIII is expressed by vascular smooth muscle cells in response to vascular injury. Circ Res. 1997;80:532-541.
12. Sinha S, Kielty CM, Heagerty AM, Canfield AE, Shuttleworth CA. Upregulation of collagen VIII following porcine coronary artery angioplasty is related to smooth muscle cell migration not angiogenesis. Int J Exp Pathol. 2001;82:295-302.
13. Yasuda O, Zhang SH, Miyamoto Y, Maeda N. Differential expression of the alpha1 type VIII collagen gene by smooth muscle cells from atherosclerotic plaques of apolipoprotein-E-deficient mice. J Vasc Res. 2000;37:158-169.
14. Plenz G, Dorszewski A, Breithardt G, Robenek H. Expression of type VIII collagen after cholesterol diet and injury in the rabbit model of atherosclerosis. Arterioscler Thromb Vasc Biol. 1999;19:1201-1209.
15. Weitkamp B, Cullen P, Plenz G, Robenek H, Rauterberg J. Human macrophages synthesize type VIII collagen in vitro and in the atherosclerotic plaque. FASEB J. 1999;13:1445-1457.
16. MacBeath JRE, Kielty CM, Shuttleworth CA. Type VIII collagen is a product of vascular smooth-muscle cells in development and disease. Biochem J. 1996;319:993-998.
17. Plenz G, Reichenberg S, Koenig C, Rauterberg J, Deng MC, Baba HA, Robenek H. Granulocyte-macrophage colony-stimulating factor (GM-CSF) modulates the expression of type VIII collagen mRNA in vascular smooth muscle cells and both are codistributed during atherogenesis. Arterioscler Thromb Vasc Biol. 1999;19:1658-1668.
18. Hou G, Mulholland D, Gronska MA, Bendeck MP. Type VIII collagen stimulates smooth muscle cell migration and matrix metalloproteinase synthesis after arterial injury. Am J Pathol. 2000;156:467-476.
19. Hopfer U, Fukai N, Hopfer H, Wolf G, Joyce N, Li E, Olsen BR. Targeted disruption of Col8a1 and Col8a2 genes in mice leads to anterior segment abnormalities in the eye. FASEB J. 2005;19:1232-1244.
20. Hou G, Vogel W, Bendeck MP. The discoidin domain-receptor tyrosine kinase DDR1 in arterial wound repair. J Clin Invest. 2001;107:727-735.
21. Kapoor R, Bornstein P, Sage EH. Type VIII collagen from bovine Descement's membrane: structural characterization of a triple helical domain. Biochemistry. 1986;25:3930-3937.
22. Lauffenburger DA, Horwitz AF. Cell migration: a physically integrated molecular process. Cell. 1996;84:359-369.
23. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. Cell migration: integrating signals from front to back. Science. 2003;302:1704-1709.
24. Palecek SP, Loftus JC, Ginsberg MH, Lauffenburger DA, Horwitz AF. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature. 1997;385:537-540.
25. Rocnik EF, Chan BMC, Pickering JG. Evidence for a role of collagen synthesis in arterial smooth muscle cell migration. J Clin Invest. 1998;101:1889-1898.
26. Biswas S, Munier FL, Yardley J, Hart-Holden N, Perveen R, Cousin P, Sutphin JE, Noble B, Batterbury M, Kielty C, Hackett A, Bonshek R, Ridgway A, McLeod D, Sheffield VC, Stone EM, Schorderet DF, Black GC. Missense mutations in COL8A2, the gene encoding the alpha2 chain of type VIII collagen, cause two forms of comeal endothelial dystrophy. Hum Mol Genet. 2001;10:2415-2423.
27. Pozzi A, Wary KK, Giancotti FG, Gardner HA. Integrin α1β1 mediates a unique collagen-dependent proliferation pathway in vivo. J Cell Biol. 1998;142:587-594.
28. Vogel W, Gish GD, Alves F, Pawson T. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell. 1997;1:13-23.
29. Hou G, Vogel WF, Bendeck MP. Tyrosine kinase activity of discoidin domain receptor 1 is necessary for smooth muscle cell migration and matrix metalloproteinase expression. Circ Res. 2002;90:1147-1149.
30. Wang DR, Sato M, Li LN, Miura M, Kojima N, Senoo H. Stimulation of pro-MMP-2 production and activation by native form of extracellular type I collagen in cultured hepatic stellate Cells. Cell Struct Funct. 2003;28:505-513.
31. Takahara T, Zhang LP, Yata Y, Xue F, Minemura M, Sato H, Watanabe A. Modulation of matrix metalloproteinase-9 in hepatic stellate cells by three-dimensional type I collagen: its activation and signaling pathway. Hepatol Res. 2003;26:318-326.
32. Ravanti L, Heino J, Lopez-Otin C, Kahari VM. Induction of collagenase-3 (MMP-13) expression in human skin fibroblasts by three-dimensional collagen is mediated by p38 mitogen-activated protein kinase. J Biol Chem. 1999;274:2446-2455.
33. Gotwals PJ, Chi-Rosso G, Lindner V, Yang J, Ling L, Fawell SE, Koteliansky VE. The α1β1 integrin is expressed during neointima formation in rat arteries and mediates collagen matrix reorganization. J Clin Invest. 1996;97:2469-2477.