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A PIVOTAL ROLE FOR TGF-β* IN ATHEROGENESIS?
DAVID J. GRAINGER,
JAMES C. METCALFE,
Corresponding Author
DAVID J. GRAINGER
Department of Biochemistry, University of Cambridge, Tennis Court Road, Cambridge CB2 1QW, U.K.
†To whom correspondence should be addressed.Search for more papers by this authorJAMES C. METCALFE
Department of Biochemistry, University of Cambridge, Tennis Court Road, Cambridge CB2 1QW, U.K.
Search for more papers by this authorDAVID J. GRAINGER,
JAMES C. METCALFE,
Corresponding Author
DAVID J. GRAINGER
Department of Biochemistry, University of Cambridge, Tennis Court Road, Cambridge CB2 1QW, U.K.
†To whom correspondence should be addressed.Search for more papers by this authorJAMES C. METCALFE
Department of Biochemistry, University of Cambridge, Tennis Court Road, Cambridge CB2 1QW, U.K.
Search for more papers by this authorAbbreviations:
-
- apo(a)
-
- apolipoprotein(a);
-
- ECM
-
- extracellular matrix;
-
- LAP
-
- latency-associated peptide;
-
- LDL
-
- low-density lipoprotein;
-
- Lp(a)
-
- lipoprotein(a);
-
- OP
-
- osteopontin;
-
- PDGF
-
- platelet-derived growth factor;
-
- TGF-β
-
- transforming growth factor type β
-
- VSMC
-
- vascular smooth muscle cell.
REFERENCES
- Assoian, R. K. & Sporn, M. B. (1986). Type beta transforming growth factor in human platelets: release during degranulation and action on vascular smooth muscle cells. Journal of Cell Biology 102, 1712–1733.
- Battegay, E. J., Raines, E. W., Seifert, R. A., Bowen-Pope, D. F. & Ross, R. (1990). TGF-/? induces bimodal proliferation of connective tissue cells via complex control of an autocrine PDGF loop. Cell 63, 515–524.
- Bilder, G. E., Krawiec, J. A., McVety, K., Gazit, A., Gilon, C., Lyall, R., Zilberstein, A., Levistzki, A., Perrone, M. H. & Schreiber, A. B. (1991). Tyrphostins inhibit PDGF-induced DNA synthesis and associated early events in smooth muscle cells. American Journal of Physiology 260, C721–730.
- Bjorkerud, S. (1991). Effects of transforming growth factor-/? i on human arterial smooth muscle cells in vitro. Arteriosclerosis and Thrombosis 11, 892–902.
- Border, W. A. & Rouslahti, E. (1991). Transforming growth factor beta: the dark side of tissue repair. Journal of Clinical Investigation 90, 1–7.
- Breslow, J. L. (1993). Transgenic mouse models of lipoprotein metabolism of atherosclerosis. Proceedings of the National Academy of Sciences, U.S.A. 90, 8314–8318.
- Butta, A., MacLennan, K., Flanders, K. C., Sacks, N. P. M., Smith, I., Mackinna, A., Dowsett, M., Wakefield, L. M., Sporn, M. B., Baum, M. & Colletta, A. A. (1992). Induction of transforming growth factor /? i in human breast cancer in vivo following tamoxifen treatment. Cancer Research 52, 4261–4264.
- Campbell, J. H., Reardon, M. F., Campbell, G. R. & Nestel, P.J. (1985). Metabolism of atherogenic lipoproteins by smooth muscle cells of different phenotype in culture. Arteriosclerosis 5, 318–324.
- Campbell, G. R. & Campbell, J. H. (1987). Phenotypic modulation of smooth muscle cells in primary culture. In Vascular Smooth Muscle in Culture (ed. J. H. Campbell and G. R. Campbell), volume 1, pp. 39–55. CRC Press, London .
- Castellot, J. J., Favreau, L. V., Karnovsky, M. J. & Rosenberg, R. D. (1982). Inhibition of vascular smooth muscle cell growth by endothelial cell-derived heparin. Possible role for platelet endoglycosidase. Journal of Biological Chemistry 257, 11256–11261.
- Chamley-Campbell, J. H., Campbell, G. R. & Ross, R. (1979). The smooth muscle cell in culture. Physiological Reviews 59, 1–59.
- Chamley-Campbell, J. H. & Campbell, G. R. (1981). What controls smooth muscle phenotype? Atherosclerosis 40, 347–340.
- Chamley-Campbell, J. H., Campbell, G. R. & Ross, R. (1981). Phenotype-dependant response of cultured aortic smooth muscle to serum mitogens. Journal of Cell Biology 89, 379–383.
- Cheifetz, S., Weatherbee, J. A., Tsang, M. L. S., Anderson, J. K. & Mole, J. E. (1987). The transforming growth factor-/? system, a complex pattern of cross-reactive ligands and receptors. Cell 48, 409–415.
- Childs, C. B., Proper, J. A., Tucker, R. F. & Moses, H. L. (1982). Serum contains a platelet-derived transforming growth factor. Proceedings of the National Academy of Sciences, U.S.A. 79, 5312–5316.
- Clowes, A. & Karnovsky, M. (1977). Supression by heparin of smooth muscle cell proliferation in injured arteries. Nature 265, 625–626.
- Colletta, A. A., Wakefield, L. M., Howell, F. V., Danielpour, D., Baum, M. & Sporn, M. B. (1991). The growth inhibition of human breast cancer cells by a novel synthetic progestin involves the induction of transforming growth factor beta. Journal of Clinical Investigation 87, 277–283.
- Connor, T. B., Roberts, A. B., Sporn, M. B., Danielpour, D. & Dart, L. L. (1989). Correlation of fibrosis and transforming growth factor-/? type 2 in the eye. Journal of Clinical Investigation 83, 1661–1666.
-
Currier, J. W.,
Pow, T. K.,
Haudenschild, C. C.,
Minihan, A. C. &
Faxon, D. P. (1991). Low molecular weight heparin (enoxaparin) reduces restenosis after iliac angioplasty in the hypercholesterolemic rabbit.
Journal of the American College of Cardiology
17, 188B–125B.
10.1016/0735-1097(91)90947-8 Google Scholar
- Danielpour, D., Dart, L. L., Flanders, K. C., Roberts, A. B. & Sporn, M. B. (1989). Immunodetection and quantification of two forms of transforming growth factor beta (TGF-/?i and TGF'-/?2) secreted by cells in culture. Journal of Cellular Physiology 138, 79–86.
- Davies, M. J., Woolf, N., Rowies, P.M. & Pepper, J. (1988). Morphology of the endothelium over atherosclerotic plaques in human coronary arteries. British Heart Journal 60, 459–464.
- Ebner, R., Chen, R.-H., Shiim, L., Lawler, S., Zioncheck, T. F., Lee, A., Lopez, A. R. & Derynck, R. (1993). Cloning of a type 1 TGF-/J receptor and its effect on TGF-/? binding to the type II receptor. Science 260, 1344–1347.
- Ellis, S. G., Roubin, G. S., Wilentz, J., Douglas, J. S. & King, S. B. (1989). Effect of 19- to 24-hour heparin administration for prevention of restenosis after uncomplicated coronary angioplasty. American Heart Journal 7. 777–782.
- Gahdiani, G., Kocher, O., Bloom, W. S., Vandekerchove, J. & Weber, K. (1984). Actin expression in smooth muscle cells in rat aortic intimal thickening, human atherosclerotic plaque and cultured rat aortic media. Journal of Clinical Investigation 73, 148–154.
- Geisterfer, A. A. T., Peach, M. J. & Owens, G. K. (1988). Angiotensin II induces hypertrophy, not hyperplasia of cultured rat aortic smooth muscle cells. Circulation Research 62, 749–756.
- Giachelli, C., Bae, N., Lombardi, D., Majesky, M. & Schwartz, S. (1991). Molecular cloning and characterisation of 2B7, a rat mRNA which distinguishes smooth muscle cell phenotypes in vitro and is identical to osteopontin (secreted phosphoprotein I; 2aR). Biochemical and Biophysical Research Communications 177, 867–873.
- Giachelli, CM., Bae, N., Almeida, M., Denhardt, D. T., Alpers, C. E. & Schwartz, S. M. (1993). Osteopontin is elevated during neointima formation in rat arteries and is a novel component of human atherosclerotic plaques. Journal of Clinical Investigation 92, 1686–1696.
- Gordon, D. & Schwartz, S. M. (1987). Arterial smooth muscle differentiation. In Vascular Smooth Muscle in Culture (ed. J. H. Campbell and G. R. Campbell), volume 1. pp. 1–10.CRC Press, London .
- Grainger, D. J., Hesketh, T. R., Metcalfe, J. C. & Weissberg, P. L. (1991). A large accumulation of non-muscle myosin heavy chain occurs at first entry into M phase in rat vascular smooth muscle cells. Biochemical Journal 277, 145–151.
- Grainger, D. J., Hesketh, T. R., Weissberg, P. L. & Metcalfe, J. C. (1992). Hexamethylene bisacetamide selectively inhibits the proliferation of human and rat vascular smooth muscle cells. Biochemical Journal 283, 403–408.
- Grainger, D. J. (1992). Control of the proliferation and differentiation of vascular smooth muscle cells. Ph.D. Thesis, University of Cambridge.
- Grainger, D. J., Witchell, CM., Watson, J. V., Metcalfe, J. C. & Weissberg, P. L. (1993a). Heparin decreases the rate of proliferation of rat vascular smooth muscle cells by releasing transforming growth factor-/?-like activity from serum. Cardiovascular Research 27, 2238–2247.
- Grainger, D. J., Weissberg, P. L. & Metcalfe, J. C. (1993b). Tamoxifen decreases the rate of proliferation of rat vascular smooth muscle cells in culture by inducing production of transforming growth factor?. Biochemical Journal 294, 109–112.
- Grainger, D. J., Kirschenlohr, H. L., Metcalfe, J. C., Weissberg, P. L., Wade, D. P. & Lawn, R. M. (1993b). Proliferation of human smooth muscle cells promoted by lipoprotein(a). Science 260, 1655–1658.
- Grainger, D. J., Witchell, C. M., Weissberg, P. L. & Metcalfe, J. C. (1994a). Mitogens for adult rat aortic vascular smooth muscle cells in serum-free primary culture. Cardiovascular Research 28, 1238–1244.
-
Grainger, D. J.,
Kemp, P. R.,
Witchell, C. M.,
Weissberg, P. L. &
Metcalfe, J. C. (1994b). TGF- decreases the rate of proliferation of rat vascular smooth muscle cells by extending the G2 phase of the cell cycle and delays the rise in cAMP before entry into M phase.
Biochemical Journal
299, 107–112.
10.1042/bj2990227 Google Scholar
- Grainger, D. J., Kemp, P. R., Liu, A. C., Lawn, R. M. & Metcalfe, J. C. (1994c). Activation of transforming growth factor /? is inhibited in apolipoprotein(a) transgenic mice. Nature 370, 460–462.
- Grainger, D. J., Kemp, P. R., Metcalfe, J. C., Liu, A. C., Lawn, R. M., Grace, A. A., Schofield, P. & Chauhan, A. C. (1994). Active TGF-is depressed five-fold in triple vessel disease patients compared with syndrome X patients. Journal of Cellular Biochemistry 18A, 267.
- Grainger, D. J., Mosedale, D. E., Metcalfe, J. C., Weissberg, P. L. & Kemp, P. R. (1995). Active and acid activatable T9F-/? in human sera, platelets and plasma. Clin. Chim. Acta. 253, 11–31.
- Groschei-Stewart, U., Chamley, J. H., Campbell, G. R. & Burnstock, G. (1975). Changes in myosin distribution in dedifferentiating and redifferentiating smooth muscle cells in tissue culture. Cell and Tissue Research 165, 13–22.
- Hajjar, Gavish, Breslow & Nachman (1989). Lipoprotein (a) modulation of endothelial cell surface fibrinolysis and its potential role in atherosclerosis. Nature 339, 303–305.
- Hanke, H., Oberhoff, M., Hanke, S., Hassenstein, S., Kamenz, J., Schmid, K. M., Betz, E. & Karsh, K. R. (1992). Inhibition of cellular proliferation after experimental ballon angioplasty by low molecular weight heparin. Circulation 85, 1548–1556.
- Henriksson, P., Angelin, B. & Berglund, L. (1992). Hormonal regulation of serum Lp(a) levels. Journal of Clinical Investigation 89, 1166–1171.
- Hermsmeyer, K., De Cino, P. & White, R. (1975). Spontaneous contractions of dispersed vascular muscle in cell culture. In Vitro 12, 628–633.
- Ho, L. (1994). Regulation of differentiation and proliferation of vascular smooth muscle cells. Ph.D. Thesis, University of Cambridge.
- Holderbaum, D. & Ehrhart, L. A. (1984). Modulation of types I and III procollagen biosynthesis at various stages of arterial smooth muscle cell growth in vitro. Experimental Cell Research 153, 16–24.
- Howe, P. H. & Leof, E. B. (1988). Transforming growth factor /?i treatment of AKR-2B cells is coupled through a pertussis toxin-sensitive G-protein(s). Biochemical Journal 261, 875–886.
- Ignotz, R. A. & Massague, J. (1986). Transforming growth factor /? stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. Journal of Biological Chemistry 261, 4337–4345.
- Janat, M. F. & Liau, G. (1992). Transforming growth factor/Si is a powerful regulator of platelet-derived growth factor action in vascular smooth muscle cells. Journal of Cellular Physiology 150, 232–242.
- Kemp, P. R., Grainger, D. J., Shanahan, C. M., Weissberg, P. L. & Metcalfe, J. C. (1991). The Id-gene is activated by serum but is not required for dedifferentiation in rat vascular smooth muscle cells. Biochemical Journal 277, 285–288.
- Kirschenlohr, H. L., Metcalfe, J. C., Weissberg, P. L. & Grainger, D. J. (1993). Adult human aortic smooth muscle cells in culture produce active TGF. Americal Journal of Physiology 265, C571–C575.
- Kocher, O., Skulli, O., Cerutti, D., Gabbiani, F. & Gabbiani, G. (1985). Cytoskeletal features of rat aortic cells during development: an electron microscopic, immunohistochemical and biochemical study. Circulation Research 56, 829–838.
- Koff, A., Ohtsuki, M., Polyak, K., Roberts, J. M. & Massague, J. (1993). Negative regulation of Gi in mammalian cells: Inhibition of cyclin-E dependant kinase by TGF-/?. Science 260, 536–538.
- Kreuzer, J., Lloyd, M. B., Bok, D., Fless, G. M., Scanu, A. M., Lusis, A. J. & Haberland, M. E. (1994). Lipoprotein(a) displays increased accumulation compared to low density lipoprotein in the murine arterial wall. Chemistry and Physics of Lipids 67, 175–190.
- Laiho, M., Decapricio, J. A., Ludlow, J. W., Livingston, D. M. & Massague, J. (1990). Growth inhibition by TGF-/? linked to suppression of retinoblastoma protein phosphorylation. Cell 62, 175–185.
- Lamarre, J., Hayes, A., Wollenberg, G. K., Hussaini, I., Hall, S. W. & Gonias, S. L. (1991). An az- macroglobulin receptor-dependant mechanism for the plasma clearance of transforming growth factor /?i in mice. Journal of Clinical Investigation 87, 49–54.
- Lawn, R. M., Wade, D. P., Hammer, R. E., Chiesa, G., Verstuyft, J. G. & Rubin, E. M. (1992). Atherogenesis in transgenic mice expressing human apolipoprotein(a). Nature 360, 670–672.
- Lawrence, D. A., Pircher, R. & Jullien, P. (1985). Conversion of a high molecular weight latent TGF-/? from chicken embryo fibroblasts into a low molecular weight active TGF-/J under acidic conditions. Biochemical and Biophysical Acta 133, 1026–1029.
- Lefer, A. M., Tsao, P., Aoki, N. & Palladino, M. A. Jr. (1990). Mediation of cardioprotection by transforming growth factor?. Science 249, 61–64.
- Lefer, A. M., Tsao, P. S., Lefer, D. J. & Ma, X-I (1991). Role of endothelial dysfunction in the pathogenesis of reperfusion injury after myocardial ischaemia, FASEB J. 5, 2039–2034.
- Liaw, L., Almeida, M., Hart, C. E., Schwartz, S. M. & Giachelli, C. M. (1994a). Osteopontin promotes vascular cell-adhesion and spreading and is chemotactic for smooth muscle cells in vitro. Circulation Research 74, 214–224.
- Liaw, L., Almeida, M., Skinner, M. P., Schwartz, S. M. & Giachelli, C. M. (1994b). Interaction of integrins with osteopontin mediates adhesion and chemotaxis of vascular cells in vitro. Journal of Cellular Biochemistry 18A, 291.
- Lin, H. Y., Wang, X.-F., Ng-Eaton, E., Weinberg, R. A. & Lodish, H. F. (1992). Expression cloning of the TGF-/? type II receptor, a functional transmembrane serine/threonine kinase. Cell 68, 775–785.
- Lopez-Casillas, F., Wrana, J. L. & Massague, J. (1993). Betaglycan presents ligand to the TGF-/? signalling receptor. Cell 73, 1435–1444.
- Lyons, R. M., Keski-Oja, J. & Moses, H. L. (1988). Proteolytic activation of latent transforming growth factor-P from fibroblast conditioned medium. Journal of Cell Biology 106, 1659–1665.
- MacDonald, C. C. & Stewart, H. J. (1991). Fatal myocardial infarction in the Scottish adjuvant tamoxifen trial. British Medical Journal 303, 435–437.
- McLean, J. W., Tomlinson, J. E., Kuang, W.-J., Eaton, D. L., Chen, E. Y., Fiess, G. M., Scanu, A. M. & Lawn, R. M. (1987). cDNA sequence of human apolipoprotein (a) is homologous to plasminogen. Nature 330, 132–137.
- Maori, J. A., Bell, L. & Merwin, J. R. (1992). Modulation of vascular cell behaviour by transforming growth factor beta. Molecular Reproduction and Development 3a, 121–126.
- Majack, R. A. & Bornstein, P. (1987). Biosynthesis and modulation of extracellular matrix components by cultured vascular smooth muscle cells. In Vascular Smooth Muscle in Culture (ed. J. H. Campbell and G. R. Campbell), volume 1. pp. 117–T30. CRC Press, London .
- Majesky, M. W., Lindner, V., Twardzik, D. R. & Schwartz, S. M. (1991). Production of transforming growth factor beta-i during repair of arterial injury. Journal of Clinical Investigation 88, 904–910.
- Masuda, J. & Ross, R. (1990a). Atherogenesis during low level hypercholesterolaemia in the non-human primate. Arteriosclerosis 10, 164–177.
- Masuda, J. & Ross, R. (1990b). Atherogenesis during low level hypercholesterolaemia in the non-human primate: II. Fatty streak conversion to fibrous plaque. Arteriosclerosis 10, 178–187.
- McCaffrey, T. A., Falcone, D. J., Agawal, L. A., Brayton, C. F., Welt, F. G. & Weksler, B. B. (1989). Transforming growth factor-beta activity is potentiated by heparin via dissociation of the transforming growth factor-beta/alpha-2-macroglobulin inactive complex. Journal of Cell Biology 109, 441–448.
- Mecham, R. P., Stenmark, K. R. & Parks, W. C. (1991). Connective tissue production by vascular smooth muscle in development and disease. Chest 99, 43S–47S.
- Metcalfe, J. C., Kemp, P. R., Liu, A. C., Lawn, R. M. & Grainger, D. J. (1994). Protein markers of lesion development in the vessels of transgenic apo(a) mice. Journal of Cellular Biochemistry 18A, 280.
- Miiani, S., Herbst, H., Schuppan, D., Stein, H. & Surrenti, C. (1991). Transforming growth factors beta 1 and 2 are differentially expressed in fibrotic liver disease. Americal Journal of Pathology 139, 1221–1229.
- Mora, R., Lupu, F. & Simionescu, N. (1987). Prelesional events in atherogenesis: colocalisation of apoB, unesterified cholesterol and extracellular phospholipid liposomes in the aorta of hyperlipidaemic rabbit. Atherosclerosis 67, 143–154.
- Morisaki, N., Kawano, M., Koyama, N., Koshikawa, T., Umemiya, K., Saito, Y. & Yoshida, S. (1991). Effects of transforming growth factor-/? on growth of aortic smooth muscle cells. Atherosclerosis 88, 227–234.
- Moses, H. L., Tucker, R. F., Leof, E. B., Coffey, R. J., Halper, J. & Shipley, G. D. (1985). Type transforming growth factor is a growth stimulator and growth inhibitor. In Cancer Cells (ed. J. Feramisco, B. Ozanne and C. Stiles), Vol. 3, 65–75. Cold Spring Harbor Press, New York .
- Murthy, U. S., Anzano, M. A., Stadel, J. M. & Greig, R. (1988). Coupling of TGF-/? induced mitogenesis to G-protein activation in AKR-zB cells. Biochemical and Biophysical Research Communications 15a, 1228–1235.
- Mustoe, T. A., Pierce, G. F., Thomason, A., Gramates, P., Sporn, M. B. & Deuel, T. F. (1987). Transforming growth factor-/? induces accelerated healing of incisional wounds in rats. Science 237, I333–I336.
- Nabel, E. G., Shum, L., Pompili, V. J., Yang, Z. Y., San, H., Shu, H. B., Liptay, S., Gold, L., Gordon, D., Derynck, R. & Nabel, G. J. (1993). Direct transfer of transforming growth factor gene into arteries stimulates fibrocellular hyperplasia. Proceedings of the National Academy of Sciences, U.S.A. 90, 10759–10763.
- Naftilan, A. J., Pratt, R. E. & Dzau, V. J. (1989). Induction of platelet-derived growth factor A chain and c-myc gene expression by angiotensin II in cultured rat vascular smooth muscle cells. Journal of Clinical Investigation 83, 1419–1424.
- Nikol, S., Isner, J. M., Pickering, G., Kearney, M., Leclerc, G. & Weir, L. (1992). Expression of transforming growth factor is increased in human vascular restenosis lesions. Journal of Clinical Investigation 90, 1582–1592.
- Obrien, E. R., Garvin, M. R., Stewart, D. K., Hinohara, T., Simpson, J. B., Schwartz, S. M. & Giachelli, C. M. (1993). Osteopontin messenger-RNA and protein are overexpressed in human coronary atherectomy specimens - clues to lesion calcification. Circulation 88, 619.
- Ouchi, Y., Hirosumi, I., Watanabe, M., Hattori, A., Nakamura, T. & Orimo, H. (1988). Inhibitory effects of transforming growth factor /? on epidermal growth factor-induced proliferation of cultured rat aortic smooth muscle cells. Biochemical and Biophysical Research Communications 157, 301–303.
- Owens, G. K., Loeb, A., Gordon, D. & Thompson, M. M. (1986). Expression of smooth muscle-specific a-lsoactin in cultured vascular smooth muscle cells: relationship between growth and cytodifferentiation. Journal of Cell Biology 102, 343–352.
- Owens, G. K., Geisterfer, A. A., Yang, Y. W. & Komoriya, A. (1988). Transforming growth factor-/? induced growth inhibition and cellular hypertrophy in cultured vascular smooth muscle cells. Journal of Biological Chemistry 107, 771–780.
- Pelton, R. W., Johnson, M. D., Perkett, E. A., Gold, L. I. & Moses, H. L. (1991). Expression of transforming growth factor-beta 1, -beta 2 and -beta 3 raRNA protein in the murine lung. American Journal of Respiratory Cell and Molecular Biology 5, 522–530.
- Pfeilschifter, J., D'Sousa, S. M. & Mundy, G. R. (1987). Effects of transforming growth factor-? on osteoblastic osteosarcoma cells. Endocrinology 121, 212–218.
- Rauterberg, J., Jaeger, E. & Althaus, M. (1993). Collagens in atherosclerotic lesions. Current Topics in Pathology 87, 163–192.
- Reid, V. C., Hardwick, S.J. & Mitchinson, M.J. (1993). Fragmentation of DNA in P388D1 macrophages exposed to oxidised low-density lipoprotein. FEBS Letters 332, 218–220.
- Ross, R., Wight, T. N., Strandness, E. & Thiele, B. (1984). Human atherosclerosis 1. Cell constitution and characteristics of advanced lesions of the superficial femoral artery. American Journal of Pathology 114, 79–93.
- Ross, R. (1986). The pathogenesis of atherosclerosis: an update. New England Journal of Medicine 314, 488–500.
- Ross, R. (1993). The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362, 801–809.
- Rovner, A. S., Murphy, R. A. & Owens, G. K. (1986). Expression of smooth-muscle and non-muscle myosin heavy chain in cultured vascular smooth muscle cells. Journal of Biological Chemistry 261, 14740–14745.
- Sato, Y. & Rifkin, D. B. (1989). Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of latent transforming growth factor-/?i -like molecules during co-culture. Journal of Cell Biology 109, 309–315.
- Schneiderman, J., Sawdey, M. S., Keeton, M. R., Bordin, G. M., Bernstein, E. F., Dilley, R. B. & Loskutoff, D. J. (1992). Increased type 1 plasminogen activator inhibitor gene expression in atherosclerotic human arteries. Proceedings of the National Academy of Sciences, U.S.A. 89, 6998–7002.
- Shanahan, C. M., Weissberg, P. L. & Metcalfe, J. C. (1993). Isolation of gene markers of differentiated and proliferating vascular smooth muscle cells. Circulation Research 73, 193–204.
- Shanahan, C. M., Cary, N. R. B., Metcalfe, J. C. & Weissberg, P. L. (1994). High expression of genes for calcification-regulating proteins in human atherosclerotic plaques. Journal of Clinical Investigation, (In the press).
- Shewmon, D. A., Stock, J. L., Heiniluoma, K. M., Arpano, M., Ukena, T. R. & Weale, V. W. (1992). Tamoxifen lowers Lp(a) in males with heart disease. Circulation 86, I–338.
- Simons, M. & Rosenberg, R. D. (1992). Antisense non-muscle myosin heavy chain and c-myb oligonucleotides supress smooth muscle proliferation in vitro. Circulation Research 70, 835–843.
- Spinler, S. A. & Cziraky, M. J. (1994). Lipoprotein(a): Physilogic function, association with atherosclerosis and effects of lipid-lowering drugs. Annals of Pharmacology 28, 343–351.
- Sporn, M. B. & Roberts, A. B. (1992). Transforming growth factor-/?: Recent progress and new challenges. Journal of Cell Biology 119, 1017–1021.
- Stary, H. C. (1987). Macrophages, macrophage foam cells, and eccentric intimal thickening in the coronary arteries of young children. Atherosclerosis 64, 91–108.
- Stary, H. C., Blankenhorn, D. H., Chandler, A. B., Glagov, S., Insull, W., Richardson, M., Rosenfield, M. E., Schaffer, A., Schwartz, C. J., Wagner, W. D. & Wissler, R. W. (1992). A definition of the intima of human arteries and of its atherosclerosis-prone regions. Circulation 85, 391–405.
- Streuli, C. H., Schmidhause, C., Kobrin, M., Bissel, M.J. & Derynck, R. (1993). Extracellular matrix regulates expression of the TGF-/?i gene. Journal of Cell Biology 120, 253–260.
- Thyberg, J., Palmberg, L., Nilsson, J., Ksaizek, T. & Sjolund, M. (1983). Phenotype modulation in primary cultures of arterial smooth muscle cells. On the role of platelet-derived growth factor. Differentiation 25, 156–167.
- Thyberg, J., Nilsson, J., Palmberg, L. & Sjolund, M. (1985). Adult human arterial smooth muscle cells in primary culture. Modulation from contractile to synthetic phenotypes. Cell and Tissue Research 239, 69–76.
- Van Obberghen-Schilling, E., Roche, N. S., Flanders, K. C., Sporn, M. B. & Roberts, A. B. (1988). Transforming growth factor positively regulates its own expression in normal and transformed cells. Journal of Biological Chemistry 263, 7741–7746.
- Wahl, S. M., Hunt, D. A., Wong, H. L., Dougherty, S., McCartney-Francis, N., Wahl, L. M., Ellingsworth, L., Schmidt, J. A., Hall, G., Roberts, A. B. & Sporn, M. B. (1988). Transforming growth factor fi is a potent immunosuppressive agent that inhibits IL-i-dependant lymphocyte proliferation. Journal of Immunology 140, 3026–3032.
- Wakefield, L. M., Smith, D. M., Flanders, K. C. & Sporn, M. B. (1988). Latent transforming growth factor-/? from human platelets. Journal of Biological Chemistry 263, 7646–7654.
- Wang, X.-F., Lin, H. Y., Ng-Eaton, E., Downward, J., Lodish, H. F. & Weinberg, R. A. (1991). Expression cloning and characterisation of the TGF-/? type III receptor. Cell 67, 797–805.
-
Weissberg, P. L.,
Grainger, D. J. &
Metcalfe, J. C. (1993). Effects of TGF-/? on vascular smooth muscle cell growth. In Growth Factors and the Cardiovascular System (ed.
P. Cummins). Kluwer Academic Publishers pp. 189–205.
10.1007/978-1-4615-3098-5_11 Google Scholar
- Wrana, J. L., Attisano, L., Wieser, R., Ventura, F. & Massague, J. (1994). Mechanism of activation of the TGF receptor. Nature 370, 341–347.
- Yamamoto, I. (1961). Journal of Electron Microscopy 10, 145–153.
- Yamauchi, A. & Burnstock, G. (1969). Post-natal development of the innervation of the mouse vas deferens. A fine structural study. Journal of Anatomy 104, 1–9.
- Zuckerman, S. H., Evans, G. F. & O'Neal, L. (1993). Exogenous glucocorticoids increase macrophage secretion of apoE by cholesterol-independent pathways. Atherosclerosis 103, 43–54.