Arterial smooth muscle cell heterogeneity: Implications for atherosclerosis and restenosis development

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 23, Issue 9, 2003, Pages 1510-1520

  Hao, Hiroyuki ^b   Gabbiani, Giulio ^b   Bochaton Piallat, Marie Luce ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b NONE

Author keywords

Heterogeneity; Smooth muscle cell

Indexed keywords

CELL MARKER;

ANIMAL CELL; ARTERY INTIMA PROLIFERATION; ARTERY MUSCLE; ATHEROMA; ATHEROSCLEROSIS; CELL HETEROGENEITY; CELL SHAPE; CELL SUBPOPULATION; EPITHELIOID CELL; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RESTENOSIS; SHORT SURVEY;

ANIMALS; ARTERIOSCLEROSIS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MUSCLE, SMOOTH, VASCULAR; PHENOTYPE; RECURRENCE;

EID: 0042190658     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000090130.85752.ED     Document Type: Short Survey

References (128)

1. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med. 1999;340:115-126.
2. Campbell G, Campbell J. The phenotypes of smooth muscle expressed in human atheroma. Ann N Y Acad Sci. 1990;598:143-158.
3. Thyberg J, Blomgren K, Hedin U, Dryjski M. Phenotypic modulation of smooth muscle cells during the formation of neointimal thickenings in the rat carotid artery after balloon injury: an electron-microscopic and stereological study. Cell Tissue Res. 1995;281:421-433.
4. Benditt EP, Benditt JM. Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Natl Acad Sci U S A. 1973;70:1753-1756.
5. Pearson TA, Dillman JM, Solez K, Heptinstall RH. Clonal characteristics in layers of human atherosclerotic plaques: a study of the selection hypothesis of monoclonality. Am J Pathol. 1978;93:93-116.
6. Pearson TA, Dillman JM, Solez K, Heptinstall RH. Clonal markers in the study of the origin and growth of human atherosclerotic lesions. Circ Res. 1978;43:10-18.
7. Thomas WA, Kim DN. Biology of disease: atherosclerosis as a hyperplastic and/or neoplastic process. Lab Invest. 1983;48:245-255.
8. Schwartz SM, Murry CE. Proliferation and the monoclonal origins of atherosclerotic lesions. Annu Rev Med. 1998;49:437-460.
9. Zalewski A, Shi Y, Johnson AG. Diverse origin of intimal cells: smooth muscle cells, myofibroblasts, fibroblasts, and beyond? Circ Res. 2002;91:652-655.
10. 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.
11. Hillebrands JL, Klatter FA, Rozing J. Origin of vascular smooth muscle cells and the role of circulating stem cells in transplant arteriosclerosis. Arterioscler Thromb Vasc Biol. 2003;23:380-387.
12. Walker LN, Bowen-Pope DF, Ross R, Reidy MA. Production of platelet-derived growth factor-like molecules by cultured arterial smooth muscle cells accompanies proliferation after arterial injury. Proc Natl Acad Sci U S A. 1986;83:7311-7315.
13. Orlandi A, Ehrlich HP, Ropraz P, Spagnoli LG, Gabbiani G. Rat aortic smooth muscle cells isolated from different layers and at different times after endothelial denudation show distinct biological features in vitro. Arterioscler Thromb Vasc Biol. 1994;14:982-989.
14. Bochaton-Piallat ML, Ropraz P, Gabbiani F, Gabbiani G. Phenotypic heterogeneity of rat arterial smooth muscle cell clones: implications for the development of experimental intimal thickening. Arterioscler Thromb Vasc Biol. 1996;16:815-820.
15. Yan ZQ, Hansson GK. Overexpression of inducible nitric oxide synthase by neointimal smooth muscle cells. Circ Res. 1998;82:21-29.
16. Seifert RA, Schwartz SM, Bowen-Pope DF. Developmentally regulated production of platelet-derived growth factor-like molecules. Nature. 1984;311:669-671.
17. Gordon D, Mohai LG, Schwartz SM. Induction of polyploidy in cultures of neonatal rat aortic smooth muscle cells. Circ Res. 1986;59:633-644.
18. McCaffrey TA, Nicholson AC, Szabo PE, Weksler ME, Weksler BB. Aging and arteriosclerosis: the increased proliferation of arterial smooth muscle cells isolated from old rats is associated with increased platelet-derived growth factor-like activity. J Exp Med. 1988;167:163-174.
19. Hültgardh-Nilsson A, Krondahl U, Querol-Ferrer V, Ringertz NR. Differences in growth factor response in smooth muscle cells isolated from adult and neonatal rat arteries. Differentiation. 1991;47:99-105.
20. Majesky MW, Giachelli CM, Reidy MA, Schwartz SM. Rat carotid neointimal smooth muscle cells reexpress a developmentally regulated mRNA phenotype during repair of arterial injury. Circ Res. 1992;71:759-768.
21. Bochaton-Piallat ML, Gabbiani F, Ropraz P, Gabbiani G. Age influences the replicative activity and the differentiation features of cultured rat aortic smooth muscle cell populations and clones. Arterioscler Thromb Vasc Biol. 1993;13:1449-1455.
22. Cook CL, Weiser MC, Schwartz PE, Jones CL, Majack RA. Developmentally timed expression of an embryonic growth phenotype in vascular smooth muscle cells. Circ Res. 1994;74:189-196.
23. Lemire JM, Covin CW, White S, Giachelli CM, Schwartz SM. Characterization of cloned aortic smooth muscle cells from young rats. Am J Pathol. 1994;144:1068-1081.
24. Villaschi S, Nicosia RF, Smith MR. Isolation of a morphologically and functionally distinct smooth muscle cell type from the intimal aspect of the normal rat aorta; evidence for smooth muscle cell heterogeneity. In Vitro Cell Dev Biol Anim. 1994;30A:589-595.
25. Lau HK. Regulation of proteolytic enzymes and inhibitors in two smooth muscle cell phenotypes. Cardiovasc Res. 1999;43:1049-1059.
26. 2-induced cytotoxicity in 'epithelioid' smooth muscle cells: implications for neointimal regression. Arterioscler Thromb Vasc Biol. 2000;20:1473-1479.
27. Holifield B, Helgason T, Jemelka S, Taylor A, Navran S, Allen J, Seidel C. Differentiated vascular myocytes: are they involved in neointimal formation? J Clin Invest. 1996;97:814-825.
28. Frid MG, Aldashev AA, Dempsey EC, Stenmark KR. Smooth muscle cells isolated from discrete compartments of the mature vascular media exhibit unique phenotypes and distinct growth capabilities. Circ Res. 1997;81:940-952.
29. Hao H, Ropraz P, Verin V, Camenzind E, Geinoz A, Pepper MS, Gabbiani G, Bochaton-Piallat ML. Heterogeneity of smooth muscle cell populations cultured from pig coronary artery. Arterioscler Thromb Vasc Biol. 2002;22:1093-1099.
30. Benzakour O, Kanthou C, Kanse SM, Scully MF, Kakkar VV, Cooper DN. Evidence for cultured human vascular smooth muscle cell heterogeneity: isolation of clonal cells and study of their growth characteristics. Thromb Haemost. 1996;75:854-858.
31. 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.
32. 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.
33. Bochaton-Piallat ML, Gabbiani F, Ropraz P, Gabbiani G. Cultured aortic smooth muscle cells from newborn and adult rats show distinct cytoskeletal features. Differentiation. 1992;49:175-185.
34. Haudenschild CC, Grünwald J. Proliferative heterogeneity of vascular smooth muscle cells and its alteration by injury. Exp Cell Res. 1985;157:364-370.
35. Skalli O, Bloom WS, Ropraz P, Azzarone B, Gabbiani G. Cytoskeletal remodeling of rat aortic smooth muscle cells in vitro: relationships to culture conditions and analogies to in vivo situations. J Submicrosc Cytol Pathol. 1986;18:481-493.
36. Hariri RJ, Alonso DR, Hajjar DP, Coletti D, Weksler ME. Aging and arteriosclerosis. I: development of myointimal hyperplasia after endothelial injury. J Exp Med. 1986;164:1171-1178.
37. Stemerman MB, Weinstein R, Rowe JW, Maciag T, Fuhro R, Gardner R. Vascular smooth muscle cell growth kinetics in vivo in aged rats. Proc Natl Acad Sci U S A. 1982;79:3863-3866.
38. Chen L, Daum G, Fischer JW, Hawkins S, Bochaton-Piallat ML, Gabbiani G, Clowes AW. Loss of expression of the β-subunit of soluble guanylyl cyclase prevents nitric oxide-mediated inhibition of DNA synthesis in smooth muscle cells of old rats. Circ Res. 2000;86:520-525.
39. Ehler E, Jat PS, Noble MD, Citi S, Draeger A. Vascular smooth muscle cells of H-2Kb-tsA58 transgenic mice: characterization of cell lines with distinct properties. Circulation. 1995;92:3289-3296.
40. Hall KL, Harding JW, Hosick HL. Isolation and characterization of clonal vascular smooth muscle cell lines from spontaneously hypertensive and normotensive rat aortas. In Vitro Cell Dev Biol. 1991;27:791-798.
41. Frid MG, Moiseeva EP, Stenmark KR. Multiple phenotypically distinct smooth muscle cell populations exist in the adult and developing bovine pulmonary arterial media in vivo. Circ Res. 1994;75:669-681.
42. 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.
43. Chamley-Campbell JH, Campbell GR, Ross R. Phenotype-dependent response of cultured aortic smooth muscle to serum mitogens. J Cell Biol. 1981;89:379-383.
44. Patel S, Shi Y, Niculescu R, Chung EH, Martin JL, Zalewski A. Characteristics of coronary smooth muscle cells and adventitial fibroblasts. Circulation. 2000;101:524-532.
45. Orekhov AN, Karpova II, Tertov VV, Rudchenko SA, Andreeva ER, Krushinsky AV, Smimov VN. Cellular composition of atherosclerotic and uninvolved human aortic subendothelial intima: light-microscopic study of dissociated aortic cells. Am J Pathol. 1984;115:17-24.
46. Orekhov AN, Andreeva ER, Krushinsky AV, Novikov ID, Tertov VV, Nestaiko GV, Khashimov KhA, Repin VS, Smirnov VN. Intimal cells and atherosclerosis: relationship between the number of intimal cells and major manifestations of atherosclerosis in the human aorta. Am J Pathol. 1986;125:402-415.
47. Orekhov AN, Krushinsky AV, Andreeva ER, Repin VS, Smirnov VN. Adult human aortic cells in primary culture: heterogeneity in shape. Heart Vessels. 1986;2:193-201.
48. Björkerud S. Cultivated human arterial smooth muscle displays heterogeneous pattern of growth and phenotypic variation. Lab Invest. 1985;53:303-310.
49. Bonin LR, Madden K, Shera K, Ihle J, Matthews C, Aziz S, Perez-Reyes N, McDougall JK, Conroy SC. Generation and characterization of human smooth muscle cell lines derived from atherosclerotic plaque. Arterioscler Thromb Vasc Biol. 1999;19:575-587.
50. Llorente-Cortes V, Martinez-Gonzalez J, Badimon L. Differential cholesteryl ester accumulation in two human vascular smooth muscle cell subpopulations exposed to aggregated LDL: effect of PDGF-stimulation and HMG-CoA reductase inhibition. Atherosclerosis. 1999;144:335-342.
51. Martinez-Gonzalez J, Berrozpe M, Varela O, Badimon L. Heterogeneity of smooth muscle cells in advanced human atherosclerotic plaques: intimal smooth muscle cells expressing a fibroblast surface protein are highly activated by platelet-released products. Eur J Clin Invest. 2001;31:939-949.
52. Bochaton-Piallat ML, Clowes AW, Clowes MM, Fischer JW, Redard M, Gabbiani F, Gabbiani G. Cultured arterial smooth muscle cells maintain distinct phenotypes when implanted into carotid artery. Arterioscler Thromb Vasc Biol. 2001;21:949-954.
53. Grünwald J, Haudenschild CC. Intimal injury in vivo activates vascular smooth muscle cell migration and explant outgrowth in vitro. Arteriosclerosis. 1984;4:183-188.
54. Schwartz SM, Foy L, Bowen-Pope DF, Ross R. Derivation and properties of platelet-derived growth factor-independent rat smooth muscle cells. Am J Pathol. 1990;136:1417-1428.
55. McCaffrey TA, Falcone DJ. Evidence for an age-related dysfunction in the antiproliferative response to transforming growth factor-β in vascular smooth muscle cells. Mol Biol Cell. 1993;4:315-322.
56. Topouzis S, Majesky MW. Smooth muscle lineage diversity in the chick embryo: two types of aortic smooth muscle cell differ in growth and receptor-mediated transcriptional responses to transforming growth factor-β. Dev Biol. 1996;178:430-445.
57. Li Z, Cheng H, Lederer WJ, Froehlich J, Lakatta EG. Enhanced proliferation and migration and altered cytoskeletal proteins in early passage smooth muscle cells from young and old rat aortic explants. Exp Mol Pathol. 1997;64:1-11.
58. Bochaton-Piallat M-L, Gabbiani G, Pepper MS. Plasminogen activator expression in rat arterial smooth muscle cells depends on their phenotype and is modulated by cytokines. Circ Res. 1998;82:1086-1093.
59. Clowes AW, Clowes MM, Au YP, Reidy MA, Belin D. Smooth muscle cells express urokinase during mitogenesis and tissue-type plasminogen activator during migration in injured rat carotid artery. Circ Res. 1990;67:61-67.
60. Reidy MA, Irvin C, Lindner V. Migration of arterial wall cells: expression of plasminogen activators and inhibitors in injured rat arteries. Circ Res. 1996;78:405-414.
61. Carmeliet P, Moons L, Herbert JM, Crawley J, Lupu F, Lijnen R, Collen D. Urokinase but not tissue plasminogen activator mediates arterial neointima formation in mice. Circ Res. 1997;81:829-839.
62. Lupu F, Heim DA, Bachmann F, Hurni M, Kakkar VV, Kruithof EK. Plasminogen activator expression in human atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 1995;15:1444-1455.
63. Noda-Heiny H, Daugherty A, Sobel BE. Augmented urokinase receptor expression in atheroma. Arterioscler Thromb Vasc Biol. 1995;15:37-43.
64. Raghunath PN, Tomaszewski JE, Brady ST, Caron RJ, Okada SS, Barnathan ES. Plasminogen activator system in human coronary atherosclerosis. Arterioscler Thromb Vasc Biol. 1995;15:1432-1443.
65. Steins MB, Padro T, Li CX, Mesters RM, Ostermann H, Hammel D, Scheld HH, Berdel WE, Kienast J. Overexpression of tissue-type plasminogen activator in atherosclerotic human coronary arteries. Atherosclerosis. 1999;145:173-180.
66. Kocher O, Gabbiani G. Cytoskeletal features of normal and atheromatous human arterial smooth muscle cells. Hum Pathol. 1986;17:875-880.
67. Schwartz SM, deBlois D, O'Brien ER. The intima: soil for atherosclerosis and restenosis. Circ Res. 1995;77:445-465.
68. 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.
69. Owens GK. Molecular control of vascular smooth muscle cell differentiation. Acta Physiol Scand. 1998;164:623-635.
70. Sartore S, Franch R, Roelofs M, Chiavegato A. Molecular and cellular phenotypes and their regulation in smooth muscle. Rev Physiol Biochem Pharmacol. 1999;134:235-320.
71. Skalli O, Ropraz P, Trzeciak A, Benzonana G, Gillessen D, Gabbiani G. A monoclonal antibody against α-smooth muscle actin: a new probe for smooth muscle differentiation. J Cell Biol. 1986;103:2787-2796.
72. Owens GK. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev. 1995;75:487-517.
73. Campbell JH, Reardon MF, Campbell GR, Nestel PJ. Metabolism of atherogenic lipoproteins by smooth muscle cells of different phenotype in culture. Arteriosclerosis. 1985;5:318-328.
74. Parlavecchia M, Skalli O, Gabbiani G. LDL accumulation in cultured rat aortic smooth muscle cells with different cytoskeletal phenotypes. J Vasc Med Biol. 1989;1:308-313.
75. Thyberg J. Caveolae and cholesterol distribution in vascular smooth muscle cells of different phenotypes. J Histochem Cytochem. 2002;50:185-195.
76. Dusserre E, Bourdillon MC, Pulcini T, Berthezene F. Decrease in high density lipoprotein binding sites is associated with decrease in intracellular cholesterol efflux in dedifferentiated aortic smooth muscle cells. Biochim Biophys Acta. 1994;1212:235-244.
77. Orlandi A, Francesconi A, Cocchia D, Corsini A, Spagnoli LG. Phenotypic heterogeneity influences apoptotic susceptibility to retinoic acid and cis-platinum of rat arterial smooth muscle cells in vitro: implications for the evolution of experimental intimal thickening. Arterioscler Thromb Vasc Biol. 2001;21:1118-1123.
78. Chan SW, Hegyi L, Scott S, Cary NR, Weissberg PL, Bennett MR. Sensitivity to Fas-mediated apoptosis is determined below receptor level in human vascular smooth muscle cells. Circ Res. 2000;86:1038-1046.
79. Kockx MM, Herman AG. Apoptosis in atherosclerosis: beneficial or detrimental? Cardiovasc Res. 2000;45:736-746.
80. McCarthy NJ, Bennett MR. The regulation of vascular smooth muscle cell apoptosis. Cardiovasc Res. 2000;45:747-755.
81. Geng YJ, Libby P. Progression of atheroma: a struggle between death and procreation. Arterioscler Thromb Vasc Biol. 2002;22:1370-1380.
82. Cremona O, Muda M, Appel RD, Frutiger S, Hughes GJ, Hochstrasser DF, Geinoz A, Gabbiani G. Differential protein expression in aortic smooth muscle cells cultured from newborn and aged rats. Exp Cell Res. 1995;217:280-287.
83. Neuville P, Geinoz A, Benzonana G, Redard M, Gabbiani F, Ropraz P, Gabbiani G. Cellular retinol-binding protein-I is expressed by distinct subsets of rat arterial smooth muscle cell in vitro and in vivo. Am J Pathol. 1997;150:509-521.
84. Bochaton-Piallat ML, Gabbiani F, Redard M, Desmouliere A, Gabbiani G. Apoptosis participates in cellularity regulation during rat aortic intimal thickening. Am J Pathol. 1995;146:1059-1064.
85. Han DK, Haudenschild CC, Hong MK, Tinkle BT, Leon MB, Liau G. Evidence for apoptosis in human atherogenesis and in a rat vascular injury model. Am J Pathol. 1995;147:267-277.
86. Perlman H, Maillard L, Krasinski K, Walsh K. Evidence for the rapid onset of apoptosis in medial smooth muscle cells after balloon injury. Circulation. 1997;95:981-987.
87. Adams LD, Lemire JM, Schwartz SM. A systematic analysis of 40 random genes in cultured vascular smooth muscle subtypes reveals a heterogeneity of gene expression and identifies the tight junction gene zonula occludens 2 as a marker of epithelioid 'pup' smooth muscle cells and a participant in carotid neointimal formation. Arterioscler Thromb Vasc Biol. 1999;19:2600-2608.
88. Jahn L, Kreuzer J, von Hodenberg E, Kubler W, Franke WW, Allenberg J, Izumo S. Cytokeratins 8 and 18 in smooth muscle cells: detection in human coronary artery, peripheral vascular, and vein graft disease and in transplantation-associated arteriosclerosis. Arterioscler Thromb. 1993;13:1631-1639.
89. Giachelli C, Bae N, Lombardi D, Majesky M, Schwartz S. Molecular cloning and characterization of 2B7, a rat mRNA which distinguishes smooth muscle cell phenotypes in vitro and is identical to osteopontin (secreted phosphoprotein I, 2aR). Biochem Biophys Res Commun. 1991;177:867-873.
90. Gadeau AP, Campan M, Millet D, Candresse T, Desgranges C. Osteopontin overexpression is associated with arterial smooth muscle cell proliferation in vitro. Arterioscler Thromb. 1993;13:120-125.
91. Giachelli CM, Bae N, Almeida 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.
92. Shanahan CM, Weissberg PL, Metcalfe JC. Isolation of gene markers of differentiated and proliferating vascular smooth muscle cells. Circ Res. 1993;73:193-204.
93. Giachelli CM, Majesky MW, Schwartz SM. Developmentally regulated cytochrome P-450IA1 expression in cultured rat vascular smooth muscle cells. J Biol Chem. 1991;266:3981-3986.
94. Liaw L, Almeida M, Hart CE, Schwartz SM, Giachelli CM. Osteopontin promotes vascular cell adhesion and spreading and is chemotactic for smooth muscle cells in vitro. Circ Res. 1994;74:214-224.
95. Chaulet H, Desgranges C, Renault MA, Dupuch F, Ezan G, Peiretti F, Loirand G, Pacaud P, Gadeau AP. Extracellular nucleotides induce arterial smooth muscle cell migration via osteopontin. Circ Res. 2001;89:772-778.
96. Gadeau AP, Chaulet H, Daret D, Kockx M, Daniel-Lamaziere JM, Desgranges C. Time course of osteopontin, osteocalcin, and osteonectin accumulation and calcification after acute vessel wall injury. J Histochem Cytochem. 2001;49:79-86.
97. Hirota S, Imakita M, Kohri K, Ito A, Morii E, Adachi S, Kim HM, Kitamura Y, Yutani C, Nomura S. Expression of osteopontin messenger RNA by macrophages in atherosclerostic plaques: a possible association with calcification. Am J Pathol. 1993;143:1003-1008.
98. Fitzpatrick LA, Severson A, Edwards WD, Ingram RT. Diffuse calcification in human coronary arteries: association of osteopontin with atherosclerosis. J Clin Invest. 1994;94:1597-1604.
99. O'Brien ER, Garvin MR, Stewart DK, Hinohara T, Simpson JB, Schwartz SM, Giachelli CM. Osteopontin is synthesized by macrophage, smooth muscle, and endothelial cells in primary and restenotic human coronary atherosclerotic plaques. Arterioscler Thromb. 1994;14:1648-1656.
100. Steitz SA, Speer MY, Curinga G, Yang HY, Haynes P, Aebersold R, Schinke T, Karsenty G, Giachelli CM. Smooth muscle cell phenotypic transition associated with calcification: upregulation of Cbfa1 and downregulation of smooth muscle lineage markers. Circ Res. 2001;89:1147-1154.
101. Weiser-Evans MC, Schwartz PE, Grieshaber NA, Quinn BE, Grieshaber SS, Belknap JK, Mourani PM, Majack RA, Stenmark KR. Novel embryonic genes are preferentially expressed by autonomously replicating rat embryonic and neointimal smooth muscle cells. Circ Res. 2000;87:608-615.
102. Frid MG, Aldashev AA, Nemenoff RA, Higashito R, Westcott JY, Stenmark KR. Subendothelial cells from normal bovine arteries exhibit autonomous growth and constitutively activated intracellular signaling. Arterioscler Thromb Vasc Biol. 1999;19:2884-2893.
103. de Vries CJ, van Achterberg TA, Horrevoets AJ, ten Cate JW, Pannekoek H. Differential display identification of 40 genes with altered expression in activated human smooth muscle cells: local expression in atherosclerotic lesions of smags, smooth muscle activation-specific genes. J Biol Chem. 2000;275:23939-23947.
104. Blindt R, Vogt F, Lamby D, Zeiffer U, Krott N, Hilger-Eversheim K, Hanrath P, vom Dahl J, Bosserhoff AK. Characterization of differential gene expression in quiescent and invasive human arterial smooth muscle cells. J Vasc Res. 2002;39:340-352.
105. Geary RL, Wong JM, Rossini A, Schwartz SM, Adams LD. Expression profiling identifies 147 genes contributing to a unique primate neointimal smooth muscle cell phenotype. Arterioscler Thromb Vasc Biol. 2002;22:2010-2016.
106. Qin M, Zeng Z, Zheng J, Shah PK, Schwartz SM, Adams LD, Sharifi BG. Suppression subtractive hybridization identifies distinctive expression markers for coronary and internal mammary arteries. Arterioscler Thromb Vasc Biol. 2003;23:425-433.
107. Kohler A, Jostarndt-Fogen K, Rottner K, Alliegro MC, Draeger A. Intima-like smooth muscle cells: developmental link between endothelium and media? Anat Embryol (Berl). 1999;200:313-323.
108. Nicosia RF, Villaschi S. Rat aortic smooth muscle cells become pericytes during angiogenesis in vitro. Lab Invest. 1995;73:658-666.
109. van Royen N, Piek JJ, Buschmann I, Hoefer I, Voskuil M, Schaper W. Stimulation of arteriogenesis: a new concept for the treatment of arterial occlusive disease. Cardiovasc Res. 2001;49:543-553.
110. Verfaillie CM. Adult stem cells: assessing the case for pluripotency. Trends Cell Biol. 2002;12:502-508.
111. Frid MG, Kale VA, Stenmark KR. Mature vascular endothelium can give rise to smooth muscle cells via endothelial-mesenchymal transdifferentiation: in vitro analysis. Circ Res. 2002;90:1189-1196.
112. Shimizu K, Sugiyama S, Aikawa M, Fukumoto Y, Rabkin E, Libby P, Mitchell RN. Host bone-marrow cells are a source of donor intimal smooth-muscle-like cells in murine aortic transplant arteriopathy. Nat Med. 2001;7:738-741.
113. Religa P, Bojakowski K, Maksymowicz M, Bojakowska M, Sirsjo A, Gaciong Z, Olszewski W, Hedin U, Thyberg J. Smooth-muscle progenitor cells of bone marrow origin contribute to the development of neointimal thickenings in rat aortic allografts and injured rat carotid arteries. Transplantation. 2002;74:1310-1315.
114. Campbell JH, Han CL, Campbell GR. Neointimal formation by circulating bone marrow cells. Ann N Y Acad Sci. 2001;947:18-24.
115. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med. 2002;8:403-409.
116. Karnovsky MJ, Wright TC Jr, Castellot JJ Jr, Choay J, Lormeau JC, Petitou M. Heparin, heparan sulfate, smooth muscle cells, and atherosclerosis. Ann N Y Acad Sci. 1989;556:268-281.
117. Au YP, Kenagy RD, Clowes MM, Clowes AW. Mechanisms of inhibition by heparin of vascular smooth muscle cell proliferation and migration. Haemostasis. 1993;23(suppl 1):177-182.
118. Orlandi A, Ropraz P, Gabbiani G. Proliferative activity and α-smooth muscle actin expression in cultured rat aortic smooth muscle cells are differently modulated by transforming growth factor-β1 and heparin. Exp Cell Res. 1994;214:528-536.
119. Neuville P, Yan Z, Gidlof A, Pepper MS, Hansson GK, Gabbiani G, Sirsjo A. Retinoic acid regulates arterial smooth muscle cell proliferation and phenotypic features in vivo and in vitro through an RARα-dependent signaling pathway. Arterioscler Thromb Vasc Biol. 1999;19:1430-1436.
120. Miano JM, Kelly LA, Artacho CA, Nuckolls TA, Piantedosi R, Blaner WS. All-trans-retinoic acid reduces neointimal formation and promotes favorable geometric remodeling of the rat carotid artery after balloon withdrawal injury. Circulation. 1998;98:1219-1227.
121. DeRose JJ Jr, Madigan J, Umana JP, Prystowsky JH, Nowygrod R, Oz MC, Todd GJ. Retinoic acid suppresses intimal hyperplasia and prevents vessel remodeling following arterial injury. Cardiovasc Surg. 1999;7:633-639.
122. Yan ZQ, Sirsjo A, Bochaton-Piallat ML, Gabbiani G, Hansson GK. Augmented expression of inducible NO synthase in vascular smooth muscle cells during aging is associated with enhanced NF-κB activation. Arterioscler Thromb Vasc Biol. 1999;19:2854-2862.
123. Peiro C, Redondo J, Rodriguez-Martinez MA, Angulo J, Marin J, Sanchez-Ferrer CF. Influence of endothelium on cultured vascular smooth muscle cell proliferation. Hypertension. 1995;25:748-751.
124. Nackman GB, Bech FR, Fillinger MF, Wagner RJ, Cronenwett JL. Endothelial cells modulate smooth muscle cell morphology by inhibition of transforming growth factor-β1 activation. Surgery. 1996;120:418-425.
125. Fillinger MF, Sampson LN, Cronenwett JL, Powell RJ, Wagner RJ. Coculture of endothelial cells and smooth muscle cells in bilayer and conditioned media models. J Surg Res. 1997;67:169-178.
126. Vernon SM, Campos MJ, Haystead T, Thompson MM, DiCorleto PE, Owens GK. Endothelial cell-conditioned medium downregulates smooth muscle contractile protein expression. Am J Physiol. 1997;272: C582-C591.
127. Petzelbauer E, Springhorn JP, Tucker AM, Madri JA. Role of plasminogen activator inhibitor in the reciprocal regulation of bovine aortic endothelial and smooth muscle cell migration by TGF-β1. Am J Pathol. 1996;149:923-931.
128. Powell RJ, Bhargava J, Basson MD, Sumpio BE. Coculture conditions alter endothelial modulation of TGF-β1 activation and smooth muscle growth morphology. Am J Physiol. 1998;274:H642-H649.