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Modulation of Smooth Muscle Cell Proliferation and Migration: Role of Smooth Muscle Cell Heterogeneity

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Atherosclerosis: Diet and Drugs

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 170))

Abstract

Proliferation and migration of smooth muscle cells (SMCs) from the media towards the intima are key events in atherosclerosis and restenosis. During these processes, SMC undergo phenotypic modulations leading to SMC dedifferentiation. The identification and characterization of factors controlling these phenotypic changes are crucial in order to prevent the formation of intimal thickening. One of the questions which presently remains open, is to know whether any SMCs of the media are capable of accumulating into the intima or whether only a predisposed medial SMC subpopulation is involved in this process. The latter hypothesis implies that arterial SMCs are phenotypically heterogenous. In this chapter, we will describe the distinct SMC phenotypes identified in arteries of various species, including humans. Their role in the formation of intimal thickening will be discussed.

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References

  • Adams LD, Lemire JM, Schwartz SM (1999) 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 19:2600–2608

    PubMed  Google Scholar 

  • Au YP, Kenagy RD, Clowes MM, Clowes AW (1993) Mechanisms of inhibition by heparin of vascular smooth muscle cell proliferation and migration. Haemostasis 23Suppl 1:177–182

    PubMed  Google Scholar 

  • Benditt EP, Benditt JM (1973) Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Natl Acad Sci USA 70:1753–1756

    PubMed  Google Scholar 

  • Benzakour O, Kanthou C, Kanse SM, Scully MF, Kakkar VV, Cooper DN (1996) Evidence for cultured human vascular smooth muscle cell heterogeneity: isolation of clonal cells and study of their growth characteristics. Thromb Haemost 75:854–858

    PubMed  Google Scholar 

  • Blank RS, Swartz EA, Thompson MM, Olson EN, Owens GK (1995) A retinoic acid-induced clonal cell line derived from multipotential P19 embryonal carcinoma cells expresses smooth muscle characteristics. Circ Res 76:742–749

    PubMed  Google Scholar 

  • Bochaton-Piallat ML, Gabbiani F, Ropraz P, Gabbiani G (1992) Cultured aortic smooth muscle cells from newborn and adult rats show distinct cytoskeletal features. Differentiation 49:175–185

    PubMed  Google Scholar 

  • Bochaton-Piallat ML, Gabbiani F, Ropraz P, Gabbiani G (1993) Age influences the replicative activity and the differentiation features of cultured rat aortic smooth muscle cell populations and clones. Arterioscler Thromb Vasc Biol 13:1449–1455

    Google Scholar 

  • Bochaton-Piallat ML, Gabbiani F, Redard M, Desmouliere A, Gabbiani G (1995) Apoptosis participates in cellularity regulation during rat aortic intimal thickening. Am J Pathol 146:1059–1064

    PubMed  Google Scholar 

  • Bochaton-Piallat ML, Ropraz P, Gabbiani F, Gabbiani G (1996) Phenotypic heterogeneity of rat arterial smooth muscle cell clones. Implications for the development of experimental intimal thickening. Arterioscler Thromb Vasc Biol 16:815–820.

    PubMed  Google Scholar 

  • Bochaton-Piallat M-L, Gabbiani G, Pepper MS (1998) Plasminogen activator expression in rat arterial smooth muscle cells depends on their phenotype and is modulated by cytokines. Circ Res 82:1086–1093

    PubMed  Google Scholar 

  • Bochaton-Piallat ML, Clowes AW, Clowes MM, Fischer JW, Redard M, Gabbiani F, Gabbiani G (2001) Cultured arterial smooth muscle cells maintain distinct phenotypes when implanted into carotid artery. Arterioscler Thromb Vasc Biol 21:949–954

    PubMed  Google Scholar 

  • Bonin LR, Madden K, Shera K, Ihle J, Matthews C, Aziz S, Perez-Reyes N, McDougall JK, Conroy SC (1999) Generation and characterization of human smooth muscle cell lines derived from atherosclerotic plaque. Arterioscler Thromb Vasc Biol 19:575–587

    PubMed  Google Scholar 

  • Campbell G, Campbell J (1990) The phenotypes of smooth muscle expressed in human atheromaa. Ann NY Acad Sci 598:143–158

    PubMed  Google Scholar 

  • Campbell JH, Reardon MF, Campbell GR, Nestel PJ (1985) Metabolism of atherogenic lipoproteins by smooth muscle cells of different phenotype in culture. Arteriosclerosis 5:318–328

    PubMed  Google Scholar 

  • Carmeliet P, Moons L, Herbert JM, Crawley J, Lupu F, Lijnen R, Collen D (1997) Urokinase but not tissue plasminogen activator mediates arterial neointima formation in mice. Circ Res 81:829–839

    PubMed  Google Scholar 

  • Chan SW, Hegyi L, Scott S, Cary NR, Weissberg PL, Bennett MR (2000) Sensitivity to Fas-mediated apoptosis is determined below receptor level in human vascular smooth muscle cells. Circ Res 86:1038–1046

    PubMed  Google Scholar 

  • Chen L, Daum G, Fischer JW, Hawkins S, Bochaton-Piallat ML, Gabbiani G, Clowes AW (2000) 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 86:520–525

    PubMed  Google Scholar 

  • Christen T, Bochaton-Piallat ML, Neuville P, Rensen S, Redard M, van Eys G, Gabbiani G (1999) Cultured porcine coronary artery smooth muscle cells. A new model with advanced differentiation. Circ Res 85:99–107

    PubMed  Google Scholar 

  • Clowes AW, Reidy MA, Clowes MM (1983) Kinetics of cellular proliferation after arterial injury. I. Smooth muscle growth in the absence of endothelium. Lab Invest 49:327–333

    PubMed  Google Scholar 

  • Clowes AW, Clowes MM, Au YP, Reidy MA, Belin D (1990) Smooth muscle cells express urokinase during mitogenesis and tissue-type plasminogen activator during migration in injured rat carotid artery. Circ Res 67:61–67

    PubMed  Google Scholar 

  • Colbert MC, Kirby ML, Robbins J (1996) Endogenous retinoic acid signaling colocalizes with advanced expression of the adult smooth muscle myosin heavy chain isoform during development of the ductus arteriosus. Circ Res 78:790–798

    PubMed  Google Scholar 

  • Cook CL, Weiser MC, Schwartz PE, Jones CL, Majack RA (1994) Developmentally timed expression of an embryonic growth phenotype in vascular smooth muscle cells. Circ Res 74:189–196

    PubMed  Google Scholar 

  • Cremona O, Muda M, Appel RD, Frutiger S, Hughes GJ, Hochstrasser DF, Geinoz A, Gabbiani G (1995) Differential protein expression in aortic smooth muscle cells cultured from newborn and aged rats. Exp Cell Res 217:280–287

    PubMed  Google Scholar 

  • DeRose JJ, Jr., Madigan J, Umana JP, Prystowsky JH, Nowygrod R, Oz MC, Todd GJ (1999) Retinoic acid suppresses intimal hyperplasia and prevents vessel remodeling following arterial injury. Cardiovasc Surg 7:633–639

    Article  PubMed  Google Scholar 

  • Dusserre E, Bourdillon MC, Pulcini T, Berthezene F (1994) Decrease in high density lipoprotein binding sites is associated with decrease in intracellular cholesterol efflux in dedifferentiated aortic smooth muscle cells. Biochim Biophys Acta 1212:235–244

    PubMed  Google Scholar 

  • Ehler E, Jat PS, Noble MD, Citi S, Draeger A (1995) Vascular smooth muscle cells of H-2KbtsA58 transgenic mice. Characterization of cell lines with distinct properties. Circulation 92:3289–3296

    PubMed  Google Scholar 

  • Fillinger MF, Sampson LN, Cronenwett JL, Powell RJ, Wagner RJ (1997) Coculture of endothelial cells and smooth muscle cells in bilayer and conditioned media models. J Surg Res 67:169–178

    Article  PubMed  Google Scholar 

  • Frid MG, Aldashev AA, Dempsey EC, Stenmark KR (1997) Smooth muscle cells isolated from discrete compartments of the mature vascular media exhibit unique phenotypes and distinct growth capabilities. Circ Res 81:940–952

    PubMed  Google Scholar 

  • Frid MG, Aldashev AA, Nemenoff RA, Higashito R, Westcott JY, Stenmark KR (1999) Subendothelial cells from normal bovine arteries exhibit autonomous growth and constitutively activated intracellular signaling. Arterioscler Thromb Vasc Biol 19:2884–2893

    PubMed  Google Scholar 

  • Gadeau AP, Campan M, Millet D, Candresse T, Desgranges C (1993) Osteopontin overexpression is associated with arterial smooth muscle cell proliferation in vitro. Arterioscler Thromb 13:120–125

    PubMed  Google Scholar 

  • Geng YJ, Libby P (2002) Progression of atheroma: a struggle between death and procreation. Arterioscler Thromb Vasc Biol 22:1370–1380

    PubMed  Google Scholar 

  • Giachelli C, Bae N, Lombardi D, Majesky M, Schwartz S (1991a) 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 177:867–873

    PubMed  Google Scholar 

  • Giachelli CM, Majesky MW, Schwartz SM (1991b) Developmentally regulated cytochrome P-450IA1 expression in cultured rat vascular smooth muscle cells. J Biol Chem 266:3981–3986

    PubMed  Google Scholar 

  • Giachelli CM, Bae N, Almeida M, Denhardt DT, Alpers CE, Schwartz SM (1993) Osteopontin is elevated during neointima formation in rat arteries and is a novel component of human atherosclerotic plaques. J Clin Invest 92:1686–1696

    PubMed  Google Scholar 

  • Gollasch M, Haase H, Ried C, Lindschau C, Morano I, Luft FC, Haller H (1998) L-type calcium channel expression depends on the differentiated state of vascular smooth muscle cells. Faseb J 12:593–601

    PubMed  Google Scholar 

  • Gordon D, Mohai LG, Schwartz SM (1986) Induction of polyploidy in cultures of neonatal rat aortic smooth muscle cells. Circ Res 59:633–644

    PubMed  Google Scholar 

  • Grünwald J, Haudenschild CC (1984) Intimal injury in vivo activates vascular smooth muscle cell migration and explant outgrowth in vitro. Arteriosclerosis 4:183–188

    PubMed  Google Scholar 

  • Han DK, Haudenschild CC, Hong MK, Tinkle BT, Leon MB, Liau G (1995) Evidence for apoptosis in human atherogenesis and in a rat vascular injury model. Am J Pathol 147:267–277

    PubMed  Google Scholar 

  • Hao H, Ropraz P, Verin V, Camenzind E, Geinoz A, Pepper MS, Gabbiani G, Bochaton-Piallat ML (2002) Heterogeneity of smooth muscle cell populations cultured from pig coronary artery. Arterioscler Thromb Vasc Biol 22:1093–1099

    Article  PubMed  Google Scholar 

  • Hao H, Gabbiani G, Bochaton-Piallat ML (2003) Arterial smooth muscle cell heterogeneity. Implications for atherosclerosis and restenosis development. Arterioscler Thromb Vasc Biol (in press)

    Google Scholar 

  • Hariri RJ, Alonso DR, Hajjar DP, Coletti D, Weksler ME (1986) Aging and arteriosclerosis. I. Development of myointimal hyperplasia after endothelial injury. J ExpMed 164:1171–1178

    Google Scholar 

  • Holifield B, Helgason T, Jemelka S, Taylor A, Navran S, Allen J, Seidel C (1996) Differentiated vascular myocytes: are they involved in neointimal formation? J Clin Invest 97:814–825

    PubMed  Google Scholar 

  • Hültgardh-Nilsson A, Krondahl U, Querol-Ferrer V, Ringertz NR (1991) Differences in growth factor response in smooth muscle cells isolated from adult and neonatal rat arteries. Differentiation 47:99–105

    PubMed  Google Scholar 

  • Jahn L, Kreuzer J, von Hodenberg E, Kubler W, Franke WW, Allenberg J, Izumo S (1993) 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 13:1631–1639

    PubMed  Google Scholar 

  • Karnovsky MJ, Wright TC, Jr., Castellot JJ, Jr., Choay J, Lormeau JC, Petitou M (1989) Heparin, heparan sulfate, smooth muscle cells, and atherosclerosis. Ann NY Acad Sci 556:268–281

    PubMed  Google Scholar 

  • Kockx MM, Herman AG (2000) Apoptosis in atherosclerosis: beneficial or detrimental? Cardiovasc Res 45:736–746

    PubMed  Google Scholar 

  • Lau HK (1999) Regulation of proteolytic enzymes and inhibitors in two smooth muscle cell phenotypes. Cardiovasc Res 43:1049–1059

    Article  PubMed  Google Scholar 

  • Lemire JM, Covin CW, White S, Giachelli CM, Schwartz SM (1994) Characterization of cloned aortic smooth muscle cells from young rats. Am J Pathol 144:1068–1081

    PubMed  Google Scholar 

  • Li S, Fan YS, Chow LH, Van Den Diepstraten C, van Der Veer E, Sims SM, Pickering JG (2001) Innate diversity of adult human arterial smooth muscle cells: cloning of distinct subtypes from the internal thoracic artery. Circ Res 89:517–525

    PubMed  Google Scholar 

  • Li WG, Miller FJ, Jr., Brown MR, Chatterjee P, Aylsworth GR, Shao J, Spector AA, Oberley LW, Weintraub NL (2000) Enhanced H2O2-induced cytotoxicity in “epithelioid” smooth muscle cells: implications for neointimal regression. Arterioscler Thromb Vasc Biol 20:1473–1479

    PubMed  Google Scholar 

  • Li Z, Cheng H, Lederer WJ, Froehlich J, Lakatta EG (1997) Enhanced proliferation and migration and altered cytoskeletal proteins in early passage smooth muscle cells from young and old rat aortic explants. Exp Mol Pathol 64:1–11

    Article  PubMed  Google Scholar 

  • Llorente-Cortes V, Martinez-Gonzalez J, Badimon L (1999) 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 144:335–342

    Article  PubMed  Google Scholar 

  • Lupu F, Heim DA, Bachmann F, Hurni M, Kakkar VV, Kruithof EK (1995) Plasminogen activator expression in human atherosclerotic lesions. Arterioscler Thromb Vasc Biol 15:1444–1455

    PubMed  Google Scholar 

  • Majesky MW, Giachelli CM, Reidy MA, Schwartz SM (1992) Rat carotid neointimal smooth muscle cells reexpress a developmentally regulated mRNA phenotype during repair of arterial injury. Circ Res 71:759–768

    PubMed  Google Scholar 

  • Martinez-Gonzalez J, Berrozpe M, Varela O, Badimon L (2001) 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 31:939–949

    Article  PubMed  Google Scholar 

  • McCaffrey TA, Nicholson AC, Szabo PE, Weksler ME, Weksler BB (1988) 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 167:163–174

    Article  PubMed  Google Scholar 

  • McCaffrey TA, Falcone DJ (1993) Evidence for an age-related dysfunction in the antiproliferative response to transforming growth factor-β in vascular smooth muscle cells. Mol Biol Cell 4:315–322

    PubMed  Google Scholar 

  • McCarthy NJ, Bennett MR (2000) The regulation of vascular smooth muscle cell apoptosis. Cardiovasc Res 45:747–755

    Article  PubMed  Google Scholar 

  • Miano JM, Kelly LA, Artacho CA, Nuckolls TA, Piantedosi R, Blaner WS (1998) all-transretinoic acid reduces neointimal formation and promotes favorable geometric remodeling of the rat carotid artery after balloon withdrawal injury. Circulation 98:1219–1227

    PubMed  Google Scholar 

  • Murry CE, Gipaya CT, Bartosek T, Benditt EP, Schwartz SM (1997) Monoclonality of smooth muscle cells in human atherosclerosis. Am J Pathol 151:697–705

    PubMed  Google Scholar 

  • Nackman GB, Bech FR, Fillinger MF, Wagner RJ, Cronenwett JL (1996) Endothelial cells modulate smooth muscle cell morphology by inhibition of transforming growth factor-β1 activation. Surgery 120:418–425

    PubMed  Google Scholar 

  • Neuville P, Geinoz A, Benzonana G, Redard M, Gabbiani F, Ropraz P, Gabbiani G (1997) Cellular retinol-binding protein-1 is expressed by distinct subsets of rat arterial smooth muscle cell in vitro and in vivo. Am J Pathol 150:509–521

    PubMed  Google Scholar 

  • Neuville P, Yan Z, Gidlof A, Pepper MS, Hansson GK, Gabbiani G, Sirsjo A (1999) 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 19:1430–1436

    PubMed  Google Scholar 

  • Noda-Heiny H, Daugherty A, Sobel BE (1995) Augmented urokinase receptor expression in atheroma. Arterioscler Thromb Vasc Biol 15:37–43

    PubMed  Google Scholar 

  • Orlandi A, Ehrlich HP, Ropraz P, Spagnoli LG, Gabbiani G (1994a) Rat aortic smooth muscle cells isolated from different layers and at different times after endothelial denudation show distinct biological features in vitro. Arterioscler Thromb 14:982–989

    PubMed  Google Scholar 

  • Orlandi A, Ropraz P, Gabbiani G (1994b) 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 214:528–536

    Article  PubMed  Google Scholar 

  • Orlandi A, Francesconi A, Cocchia D, Corsini A, Spagnoli LG (2001) 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 21:1118–1123

    PubMed  Google Scholar 

  • Owens GK (1995) Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75:487–517

    PubMed  Google Scholar 

  • Owens GK (1998) Molecular control of vascular smooth muscle cell differentiation. Acta Physiol Scand 164:623–635

    PubMed  Google Scholar 

  • Parlavecchia M, Skalli O, Gabbiani G (1989) LDL accumulation in cultured rat aortic smooth muscle cells with different cytoskeletal phenotypes. J Vasc Med Biol 1:308–313

    Google Scholar 

  • Peiro C, Redondo J, Rodriguez-Martinez MA, Angulo J, Marin J, Sanchez-Ferrer CF (1995) Influence of endotheliumon cultured vascular smooth muscle cell proliferation. Hypertension 25:748–751

    PubMed  Google Scholar 

  • Perlman H, Maillard L, Krasinski K, Walsh K (1997) Evidence for the rapid onset of apoptosis in medial smooth muscle cells after balloon injury. Circulation 95:981–987

    PubMed  Google Scholar 

  • Petzelbauer E, Springhorn JP, Tucker AM, Madri JA (1996) Role of plasminogen activator inhibitor in the reciprocal regulation of bovine aortic endothelial and smooth muscle cell migration by TGF-β1. Am J Pathol 149:923–931

    PubMed  Google Scholar 

  • Powell RJ, Bhargava J, Basson MD, Sumpio BE (1998) Coculture conditions alter endothelial modulation of TGF-β1 activation and smooth muscle grow thmorphology. AmJ Physiol 274: H642–H649

    Google Scholar 

  • Raghunath PN, Tomaszewski JE, Brady ST, Caron RJ, Okada SS, Barnathan ES (1995) Plasminogen activator system in human coronary atherosclerosis. Arterioscler Thromb Vasc Biol 15:1432–1443

    PubMed  Google Scholar 

  • Reidy MA, Irvin C, Lindner V (1996) Migration of arterial wall cells. Expression of plasminogen activators and inhibitors in injured rat arteries. Circ Res 78:405–414

    PubMed  Google Scholar 

  • Ross R (1999) Atherosclerosis: an inflammatory disease. N Engl J Med 340:115–126

    Article  PubMed  Google Scholar 

  • Sartore S, Franch R, Roelofs M, Chiavegato A (1999) Molecular and cellular phenotypes and their regulation in smooth muscle. Rev Physiol Biochem Pharmacol 134:235–320

    PubMed  Google Scholar 

  • Schwartz SM, Foy L, Bowen-Pope DF, Ross R (1990) Derivation and properties of platelet-derived growth factor-independent rat smooth muscle cells. Am J Pathol 136:1417–1428

    PubMed  Google Scholar 

  • Schwartz SM, deBlois D, O'Brien ER (1995) The intima. Soil for atherosclerosis and restenosis. Circ Res 77:445–465

    PubMed  Google Scholar 

  • Seifert RA, Schwartz SM, Bowen-Pope DF (1984) Developmentally regulated production of platelet-derived growth factor-like molecules. Nature 311:669–671

    Article  PubMed  Google Scholar 

  • Shanahan CM, Weissberg PL, Metcalfe JC (1993) Isolation of gene markers of differentiated and proliferating vascular smooth muscle cells. Circ Res 73:193–204

    PubMed  Google Scholar 

  • Shanahan CM, Weissberg PL (1998) Smooth muscle cell heterogeneity: patterns of gene expression in vascular smooth muscle cells in vitro and in vivo. Arterioscler Thromb Vasc Biol 18:333–338

    PubMed  Google Scholar 

  • Steins MB, Padro T, Li CX, Mesters RM, Ostermann H, Hammel D, Scheld HH, Berdel WE, Kienast J (1999) Overexpression of tissue-type plasminogen activator in atherosclerotic human coronary arteries. Atherosclerosis 145:173–180

    Article  PubMed  Google Scholar 

  • Stemerman MB, Weinstein R, Rowe JW, Maciag T, Fuhro R, Gardner R (1982) Vascular smooth muscle cell growth kinetics in vivo in aged rats. Proc Natl Acad Sci USA 79:3863–3866

    PubMed  Google Scholar 

  • Thyberg J, Blomgren K, Hedin U, Dryjski M (1995) 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 281:421–433

    PubMed  Google Scholar 

  • Thyberg J (2002) Caveolae and cholesterol distribution in vascular smooth muscle cells of different phenotypes. J Histochem Cytochem 50:185–195

    PubMed  Google Scholar 

  • Topouzis S, Majesky MW (1996) Smooth muscle lineage diversity in the chick embryo. Two types of aortic smooth muscle cell differing row than dreceptor-mediated transcriptional responses to transforming growth factor-β. Dev Biol 178:430–445

    Google Scholar 

  • Vernon SM, Campos MJ, Haystead T, Thompson MM, DiCorleto PE, Owens GK (1997) Endothelial cell-conditioned medium downregulates smooth muscle contractile protein expression. Am J Physiol 272: C582–C591

    PubMed  Google Scholar 

  • Villaschi S, Nicosia RF, Smith MR (1994) 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 30A:589–595

    PubMed  Google Scholar 

  • Walker LN, Bowen-Pope DF, Ross R, Reidy MA (1986) Production of platelet-derived growth factor-like molecules by cultured arterial smooth muscle cells accompanies proliferation after arterial injury. Proc Natl Acad Sci USA 83:7311–7315

    PubMed  Google Scholar 

  • Yan ZQ, Hansson GK (1998) Overexpression of inducible nitric oxide synthase by neointimal smooth muscle cells. Circ Res 82:21–29

    PubMed  Google Scholar 

  • Yan ZQ, Sirsjo A, Bochaton-Piallat ML, Gabbiani G, Hansson GK (1999) Augmented expression of inducible NO synthase in vascular smooth muscle cells during aging is associated with enhanced NF-κB activation. Arterioscler Thromb Vasc Biol 19:2854–2862

    PubMed  Google Scholar 

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Bochaton-Piallat, ML., Gabbiani, G. (2005). Modulation of Smooth Muscle Cell Proliferation and Migration: Role of Smooth Muscle Cell Heterogeneity. In: von Eckardstein, A. (eds) Atherosclerosis: Diet and Drugs. Handbook of Experimental Pharmacology, vol 170. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-27661-0_24

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