Smooth muscle cell phenotypes in atherosclerotic lesions

Current Opinion in Lipidology

Volumn 10, Issue 6, 1999, Pages 507-513

  Shanahan, Catherine M ^a,b   Weissberg, Peter L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID;

APOPTOSIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CALCIFICATION; CELL DEATH; HUMAN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; REVIEW; VASCULAR SMOOTH MUSCLE;

APOPTOSIS; ARTERIOSCLEROSIS; CALCINOSIS; CELL AGING; HUMANS; MUSCLE, SMOOTH, VASCULAR;

EID: 0033379343     PISSN: 09579672     EISSN: None     Source Type: Journal    
DOI: 10.1097/00041433-199912000-00005     Document Type: Review

References (63)

1. Ross R, Glomset JA. Atherosclerosis and the arterial smooth muscle. Proliferation of smooth muscle is a key event in the genesis of the lesions of atherosclerosis. Science 1973; 180:1332-1339.
2. Schwartz S, Campbell G, Campbell J. Replication of smooth muscle cells in vascular disease. Circ Res 1986; 58:427-444.
3. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 1993; 362:801-809.
4. Newby AC, Libby P, van der Wal AC. Plaque instability-the real challenge for atherosclerosis research in the next decade? Cardiovasc Res 1999; 41:321-322. • A thorough summary of current thinking on plaque instability and its implications.
5. Shanahan CM, Weissberg PL. Smooth muscle cell heterogeneity-patterns of gene expression in vascular smooth muscle cells in vitro and in vivo. Arterioscler Thromb Vasc Biol 1998; 18:333-338. •• In this review both the in-vitro and in-vivo evidence for VSMC heterogeneity and the current arguments concerning its generation/origin are discussed. The importance of defining VSMC function in terms of the gene expression profile of phenotypic subsets is highlighted, and potential experimental approaches for dissecting the genetic regulation of VSMC phenotype are presented.
6. Schwartz SM, deBlois D, O'Brien ERM. The intima. Soil for atherosclerosis and restenosis. Circ Res 1995; 77:445-465.
7. Mosse PRL, Campbell GR, Wang ZL, Campbell JH. Smooth muscle phenotypic expression in human carotid arteries. I. Comparison of cells from diffuse intimal thickenings adjacent to atheromatous plaques with those of the media. Lab Invest 1985; 53:556-562.
8. Campbell GR, Campbell JH. Smooth muscle phenotypic changes in arterial wall homeostasis: implications for the pathogenesis of atherosclerosis. Exp Mol Pathol 1985; 42:139-162.
9. Chamley-Campbell JH, Campbell GR, Ross R. Smooth muscle cell in culture. Physiol Rev 1979; 59:1-61.
10. Song J, Rolfe BE, Campbell JH, Campbell GR. Changes in three dimensional architecture of microfilaments in cultured vascular smooth muscle cells during phenotypic modulation. Tissue Cell 1998; 30:324-333.
11. Gittenberger-de Groot AC, DeRuiter MC, Bergwerff M, Poelmann RE. Smooth muscle cell origin and its relation to heterogeneity in development and disease. Arterioscler Thromb Vasc Biol 1999; 19:1589-1594. The authors thoroughly review the different developmental origins of VSMC and the evidence and criteria for establishing VSMC heterogeneity, citing both in-vitro and animal studies. However, they conclude that as yet there is no evidence for the origin for heterogeneity observed in disease to be based on developmental origin.
12. Arar C, Gaudin J-C, Capron L, Legrand A. Galectin-3 gene (LGALS3) expression in experimental atherosclerosis and cultured smooth muscle cells. FEBS Lett 1998; 430:307-311.
13. Kowal RC, Richardson JA, Miano JM, Olsen EN. EVEC, a novel epidermal growth factor-like repeat-containing protein upregulated in embryonic and diseased adult vasculature. Circ Res 1999; 84:1166-1176.
14. Schwartz SM. The definition of cell type. Circ Res 1999; 84:1234-1235. • Arguments for defining VSMC phenotypes in terms of their function and an outline of the potential benefits of modern screening technologies.
15. Proudfoot D, Skepper JN, Shanahan CM, Weissberg PL. Calcification of human vascular cells in vitro is correlated with high levels of matrix Gla protein and low levels of osteopontin expression. Arterioscler Thromb Vasc Biol 1998; 18:379-388. •• This report provides the first detailed description of the 'osteoblastic' properties of human aortic VSMC in vitro.
16. Bonin LR, Madden K, Shera K, Ihle J, Matthews C, Aziz S, et al. Generation and characterization of human smooth muscle cell lines derived from atherosclerotic plaque. Arterioscler Thromb Vasc Biol 1999; 19:575-587.
17. Christen T, Bochaton-Piallat ML, Neuville P, Rensen S, Redard M, van Eys G, Gabbiani G. Cultured porcine coronary artery smooth muscle cells. A new model with advanced differentiation. Circ Res 1999; 85:99-107. • This study describes the careful characterization of a novel porcine VSMC culture system in which the cells maintain a high degree of differentiation in vitro. The potential uses of such a 'differentiated' culture system are discussed.
18. Simone NL, Bonner RF, Gillespie JW, Emmert-Buck MR, Liotta LA. Laser-capture microdissection: opening the microscopic frontier to molecular analysis. Trends Genet 1998; 14:272-276.
19. Tjurmin AV, Ananyeva NM, Smith EP, Gao Y, Hong MK, Leon MB, Haudenschild CC. Studies on the histogenesis of myxomatous tissue of human coronary lesions. Arterioscler Thromb Vasc Biol 1999; 19: 93-97.
20. Masur SK, Dewal HS, Dinh TT, Erenburg I, Petridou S. Myofibroblasts differentiate from fibroblasts when plated a low density. Proc Natl Acad Sci U S A 1996; 93:4219-4223.
21. Galmiche MC, Koteliansky VE, Briere J, Herve P, Charbord P. Stromal cells from human long-term marrow cultures are mesenchymal cells that differentiate following a vascular smooth muscle differentiation pathway. Blood 1993; 82:66-76.
22. Shi Y, Pieniek M, Fard A, O'Brien J, Mannion JD, Zalewski A. Adventitial remodelling after coronary arterial injury. Circulation. 1996; 93:340-348.
23. Newby AC, Zaltsman AB. Fibrous cap formation or destruction-the critical importance of vascular smooth muscle cell proliferation, migration and matrix formation. Cardiovasc Res 1999; 41:345-360. •• A comprehensive review of the origin, heterogeneity and function of VSMC in the fibrous cap of human atherosclerotic plaques. Detailed arguments for the importance of VSMC migration and proliferation in cap synthesis and maintenance are presented, and the potential role of senescent and apoptotic VSMC in cap degeneration is discussed.
24. Aikawa M, Rabkin E, Voglic SJ, Sshing H, Nagai R, Schoen FJ, Libby P. Lipid lowering promotes accumulation of mature smooth muscle cells expressing smooth muscle myosin heavy chain isoforms in rabbit atheroma. Circ Res 1998; 83:1015-1026. •• In this study the effects of cholesterol lowering on a number of aspects of VSMC phenotype are examined in an attempt to correlate phenotypic changes with changes in the distribution of cytokines within the plaque and in plaque stability. This is an example of the type of integrated in-vivo study which is now required to define functional VSMC phenotypes in vivo.
25. Shanahan CM, Weissberg PL, Metcalfe JC. Isolation of gene markers of differentiated and proliferating vascular smooth muscle cells. Circ Res 1993; 73:193-204.
26. Majesky MW, Giachelli CM, Reidy MA, Schwartz SM. Rat carotid neointimal cells re-express a developmentally regulated mRNA phenotype during repair of arterial injury. Circ Res 1992; 71:759-768.
27. George SJ. Tissue inhibitors of metalloproteinases and metalloproteinases in atherosclerosis. Curr Opin Lipidol 1998; 9:413-423. • A 'state of the art' review of the expression and functions of tissue inhibitors of metalloproteinases and MMP in atherosclerosis.
28. Bennett MR, Boyle JJ. Apoptosis of vascular smooth muscle cells in atherosclerosis. Atherosclerosis 1998; 138:3-9.
29. Kockx MM. Apoptosis in the atherosclerotic plaque. Quantitative and qualitative aspects. Arterioscler Thromb Vasc Biol 1998; 18:1519-1522. • A review examining the evidence for apoptosis in atherosclerotic plaques and documenting recent evidence for the presence of VSMC primed for apoptosis in fatty streak lesions. However, this only indicates that the cells are susceptible to apoptosis, and additional factors present in advanced lesions are required to complete the death pathway in these cells.
30. Bennett MR, Evan GI, Schwartz SM. Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J Clin Invest 1995; 95:2266-2274.
31. Bennett MR, MacDonald K, Chan SW, Boyle JJ, Weissberg PL. Cooperative interactions between RB and p53 regulate cell proliferation, cell senescence, and apoptosis in human vascular smooth muscle cells from atherosclerotic plaques. Circ Res 1998; 82:704-712. • A detailed examination of the growth properties and signalling pathways in normal versus plaque-derived VSMC.
32. Kockx MM, De Meyer GRY, Buyssens N, Knaaper MWM, Bult H, Herman AG. Cell composition, replication, and apoptosis in atherosclerotic plaques after 6 months of cholesterol withdrawal. Circ Res 1998; 83:378-387. •• An in-vivo study in a rabbit model of atherosclerosis demonstrating that cholesterol withdrawal changes the cell composition of atherosclerotic plaques as a result of reductions in cell replication and apoptotic cell death. These changes are accompanied by reduced expression of the proapoptotic factor, BAX in VSMC, and suggest a mechanism for plaque stabilization.
33. Kockx MM, De Meyer GRY, Muhring J, Jacob W, Bult H, Herman AG. Apoptosis and related proteins in different stages of human atherosclerotic plaques. Circulation 1998; 97:2307-2315.
34. Steinberg D. Low density lipoprotein oxidation and its pathobiological significance. J Biol Chem 1997; 272:20963-20966.
35. Kataoka H, Kume N, Miyamoto S, Minami M, Moriwaki H, Murase T, et al. Expression of a lectin-like oxidized low-density lipoprotein receptor-1 in human atherosclerotic lesions. Circulation 1999; 99:3110-3117.
36. Thyberg J, Calara F, Dimayuga P, Nilsson J, Regnstrom J. Role of caveolae in cholesterol transport in arterial smooth muscle cells exposed to lipoproteins in vitro and in vivo. Lab Invest 1998; 78:825-837.
37. Greaves DR, Gough PJ, Gordon S. Recent progress in defining the role of scavenger receptors in lipid transport, atherosclerosis and host defense. Curr Opin Lipidol 1998; 9:425-432.
38. Staels B, Koenig W, Habib A, Merval R, Lebret M, Torra IP, et al. Activation of human aortic smooth-muscle cells is inhibited by PPARχ but not by PPARγactivators. Nature 1998; 393:790-793. • An important study predicting a role for VSMC in the inflammatory processes associated with atherosclerosis.
39. Aikawa M, Rabkin E, Okada Y, Voglic SJ, Clinton SK, Brinckerhoff CE, et al. Lipid lowering reduces matrix metalloproteinase activity and increases collagen content of rabbit atheroma: a potential mechanism of lesion stabilization. Circulation 1998; 97:2433-2444.
40. Siow RCM, Sato H, Mann GE. Heme oxygenase-carbon monoxide signalling pathway in atherosclerosis: anti-atherogenic actions of bilirubin and carbon monoxide? Cardiovasc Res 1999; 41:385-394.
41. Damiani E, Sugiyama T, Shimamura K, Greci L, Matsuda Y. Altered expression of χ-actin, smooth muscle myosin heavy chain-1 and calponin in cultured smooth muscle cells by oxidized low density lipoproteins. FEBS Lett 1998; 425:123-125.
42. Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M, Detrano R. Quantification of coronary artery calcification using ultrafast computed tomography. J Am Coll Cardiol 1990; 15:827-832.
43. Richardson PD, Davies MJ, Born GVR. Influence of plaque configuration and stress distribution on fissuring of coronary athersclerotic plaques. Lancet 1989; ii:141-144.
44. Doherty TM, Deltrano RC. Coronary arterial calcification as an active process: a new perspective on an old problem. Calcif Tissue Int 1994; 54:224-230.
45. Demer LL, Tintut Y. Osteopontin. Between a rock and a hard plaque. Circ Res 1999; 84:250-252. •• A succinct review of the evidence for the active regulation of vascular calcification, focusing on the potential role for mineralization-regulating proteins in the process.
46. Jeziorska M, McCollum C, Woolley DE. Observations on bone formation and remodelling in advanced atherosclerotic lesions of human carotid arteries. Virch Arch 1998; 433:559-565.
47. Bostrom K, Watson KE, Horn S, Wortham C, Herman IM, Demer LL. Bone morphogenetic protein expression in human atherosclerotic lesions. J Clin Invest 1993; 91:1800-1809.
48. Shanahan CM, Cary NRB, Metcalfe JC, Weissberg PL. High expression of genes for calcification-regulating proteins in human atherosclerotic plaques. J Clin Invest 1994; 93:2393-2402.
49. Giachelli CM, Bae N, Alemida M, Denhardt DT, Alpers CE, Schwartz SM. Osteopontin is elevated during neointima formation in rat arteries and is a novel component of human atherosclerotic plaques. J Clin Invest 1993; 92:1686-1696.
50. Watson KE, Parhami F, Shin V, Demer LL. Fibronectin and collagen I matrixes promote calcification of vascular cells in vitro, whereas collagen IV matrix is inhibitory. Arterioscler Thromb Vasc Biol 1998; 18:1964-1971. • Evidence that the extracellular matrix may influence the osteoblastic phenotype of VSMC.
51. Wada T, McKee MD, Steitz S, Giachelli CM. Calcification of vascular smooth muscle cell cultures-inhibition by osteopontin. Circ Res 1999; 84:166-178. • The first experimental evidence that the role of osteopontin, a mineralization-regulating matrix protein, in the vessel wall is likely to be the inhibition of hydroxyapatite crystal growth.
52. Newman CM, Bruun BC, Porter KE, Mistry PK, Shanahan CM, Weissberg PL. Osteopontin is not a marker for proliferating human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 1995; 15:2010-2018.
53. Bini A, Mann KG, Kudryk BJ, Schoen FJ. Noncollagenous bone matrix proteins, calcification, and thrombosis in carotid artery atherosclerosis. Arterioscler Thromb Vasc Biol 1999; 19:1852-1861. • A descriptive study showing detailed co-localizations of bone-associated proteins, MMP, lipids, calcium phosphate and thrombosis in atherosclerotic plaques.
54. Kockyx MM, Herman AG. Apoptosis in atherogenesis: implications for plaque destabilization. Eur Heart J 1998; 19:G23-G28.
55. Parhami F, Morrow AD, Balucan J, Leitinger N, Watson AD, Tintut Y, et al. Lipid oxidation products have opposite effects on calcifying vascular cell and bone differentiation. A possible explanation for the paradox of arterial calcification in osteoporotic patients. Arterioscler Thromb Vasc Biol 1997; 17:680-687.
56. Watson KE, Bostrom K, Tavindranath R, Lam T, Norton B, Demer LL. TGF-β1 and 25-hydroxycholesterol stimulate osteoblast-like vascular cells to calcify. J Clin Invest 1994; 93:2106-2113.
57. Song J, Wan Y, Rolfe BE, Campbell JH, Campbell GR. Effect of estrogen on vascular smooth muscle cells is dependent upon cellular phenotype. Artherosclerosis 1998; 140:97-104.
58. Campbell JH, Campbell GR. The cell biology of atherosclerosis-new developments. Aust NZ J Med 1997; 27:497-500.
59. Jono S, Nishizawa Y, Shioi A, Morii H. 1,25-Dihydroxyvitamin D3 increases in vitro vascular calcification by modulating secretion of endogenous parathyroid hormone-related peptide. Circulation 1998; 98:1302-1306. • A study of the effects of vitamin D3 on vascular calcification in vitro, highlighting the potential effects of this hormone on vascular calcification in vivo.
60. Price PA, Faus SA, Williamson MK. Warfarin causes rapid calcification of the elastic lamellae in rat arteries and heart valves. Arterioscler Thromb Vasc Biol 1998; 18:1400-1407.
61. Mano T, Luo Z, Malendowicz SL, Evans T, Walsh K. Reversal of GATA-6 downregulation promotes smooth muscle differentiation and inhibits intimal hyperplasia in balloon-injured rat carotid artery. Circ Res 1999; 84:647-654. •• A demonstration of the use of gene transfer to influence transcription factor availability in the vessel wall. GATA6 plays a role in VSMC differentiation and this study shows that by influencing differentiation other aspects of VSMC phenotypic behaviour can also be regulated.
62. Schulick AH, Taylor AJ, Zuo W, Qiu CB, Dong G, Woodward RN, et al. Overexpression of transforming growth factor β1 in arterial endothelium causes hyperplasia, apoptosis, and cartilaginous metaplasia. Proc Natl Acad Sci USA 1998; 95:6983-6988. • A report describing gene transfer into the endothelium and its effects on the phenotype of underlying VSMC.
63. Rekhter MD, Simari RD, Work CW, Nabel GJ, Nabel EG, Gordon D. Gene transfer into normal and atherosclerotic human blood vessels. Circ Res 1998; 82:1243-1252. • A study outlining the potential, and the problems, associated with gene transfer into complex atherosclerotic plaques.