Collagen synthesis in atherosclerosis: too much and not enough.

Fibrillar collagen is a critical component of atherosclerotic lesions. Uncontrolled collagen accumulation leads to arterial stenosis, while excessive collagen breakdown combined with inadequate synthesis weakens plaques thereby making them prone to rupture. This review discusses cellular sources of collagen synthesis in atherosclerosis, local and systemic factors modulating collagen gene expression, as well as temporal and spatial patterns of collagen production in human and experimental atherosclerotic lesions.

[1]  J. Risteli,et al.  Thrombolytic Therapy With Streptokinase Stimulates Collagen Breakdown , 1991, Circulation.

[2]  J. Pickering,et al.  Evidence for rapid accumulation and persistently disordered architecture of fibrillar collagen in human coronary restenosis lesions. , 1996, The American journal of cardiology.

[3]  M. Rekhter,et al.  Cell proliferation and collagen synthesis are two independent events in human atherosclerotic plaques. , 1994, Journal of vascular research.

[4]  D. Grainger,et al.  Tamoxifen elevates transforming growth factor–β and suppresses diet–induced formation of lipid lesions in mouse aorta , 1995, Nature Medicine.

[5]  S. Moore,et al.  Pathogenesis of atherosclerosis. , 1985, Metabolism: clinical and experimental.

[6]  D. Clemmons,et al.  The Effect of Extracellular Matrix Proteins on Porcine Smooth Muscle Cell Insulin-like Growth Factor (IGF) Binding Protein-5 Synthesis and Responsiveness to IGF-I* , 1998, The Journal of Biological Chemistry.

[7]  M. Rekhter,et al.  Animal model that mimics atherosclerotic plaque rupture. , 1998, Circulation research.

[8]  E. Braunwald Heart Disease: A Textbook of Cardiovascular Medicine , 1992, Annals of Internal Medicine.

[9]  S. Kato,et al.  Basic fibroblast growth factor regulates extracellular matrix and contractile protein expression independent of proliferation in vascular smooth muscle cells , 1998, In Vitro Cellular & Developmental Biology - Animal.

[10]  T. McCaffrey,et al.  Antiproliferative and Fibrosuppressive Effects on Smooth Muscle Cells from Human Coronary Arteries , 1995 .

[11]  W Schlumberger,et al.  Aortic smooth muscle cells in collagen lattice culture: effects on ultrastructure, proliferation and collagen synthesis. , 1991, European journal of cell biology.

[12]  T. Rönnemaa,et al.  Serum from type IIA hyperlipoproteinemic patients does not stimulate proliferation of and collagen synthesis in human fetal aortic smooth muscle cells in culture. , 1985, Atherosclerosis.

[13]  P. Richardson,et al.  Collagen types I and III, collagen content, GAGs and mechanical strength of human atherosclerotic plaque caps: span-wise variations. , 1992, Atherosclerosis.

[14]  A. Banes,et al.  Enhanced collagen production by smooth muscle cells during repetitive mechanical stretching. , 1988, Archives of surgery.

[15]  J. Thyberg Differentiated properties and proliferation of arterial smooth muscle cells in culture. , 1996, International review of cytology.

[16]  M. Adams,et al.  Wound healing: a paradigm for lumen narrowing after arterial reconstruction. , 1998, Journal of vascular surgery.

[17]  B. Buchholz,et al.  Joint occurrence of collagen mRNA containing cells and macrophages in human atherosclerotic vessels. , 1991, Atherosclerosis.

[18]  D J Prockop,et al.  Collagens: molecular biology, diseases, and potentials for therapy. , 1995, Annual review of biochemistry.

[19]  G. Hansson,et al.  Interferon-gamma inhibits arterial stenosis after injury. , 1991, Circulation.

[20]  M A Schork,et al.  Type I collagen gene expression in human atherosclerosis. Localization to specific plaque regions. , 1993, The American journal of pathology.

[21]  J. Pickering,et al.  Coordinated effects of fibroblast growth factor-2 on expression of fibrillar collagens, matrix metalloproteinases, and tissue inhibitors of matrix metalloproteinases by human vascular smooth muscle cells. Evidence for repressed collagen production and activated degradative capacity. , 1997, Arteriosclerosis, thrombosis, and vascular biology.

[22]  H. Vlassara Advanced glycation end-products and atherosclerosis. , 1996, Annals of medicine.

[23]  S. Jimi,et al.  Oxidized LDL induces an increase in the relative collagen synthesis of rabbit aortic smooth muscle cells. , 1994, Journal of atherosclerosis and thrombosis.

[24]  W. Hume Proline and Thymidine Uptake in Rabbit Ear Artery Segments In Vitro Increased by Chronic Tangential Load , 1980, Hypertension.

[25]  M. Reidy,et al.  Expression of extracellular matrix proteins accompanies lesion growth in a model of intimal reinjury. , 1998, Circulation research.

[26]  T. Kulik,et al.  Effect of stretch on growth and collagen synthesis in cultured rat and lamb pulmonary arterial smooth muscle cells , 1993, Journal of cellular physiology.

[27]  Artur,et al.  Specific inhibition of eIF-5A and collagen hydroxylation by a single agent. Antiproliferative and fibrosuppressive effects on smooth muscle cells from human coronary arteries. , 1995, The Journal of clinical investigation.

[28]  K. Murata,et al.  Collagen types in various layers of the human aorta and their changes with the atherosclerotic process. , 1986, Atherosclerosis.

[29]  A. Ooshima,et al.  Collagen Metabolism in Atherogenesis , 1990, Annals of the New York Academy of Sciences.

[30]  G. Sonenshein,et al.  B-Myb Expression in Vascular Smooth Muscle Cells Occurs in a Cell Cycle-dependent Fashion and Down-regulates Promoter Activity of Type I Collagen Genes (*) , 1996, The Journal of Biological Chemistry.

[31]  B. Buchholz,et al.  Localization of cytoplasmic collagen mRNA in human aortic coarctation: mRNA enhancement in high blood pressure-induced intimal and medial thickening. , 1990, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[32]  L. Ehrhart,et al.  Inhibition of collagen and non-collagen protein synthesis in cultured aortic smooth muscle cells by hyperlipoproteinemic serum. , 1980, Artery.

[33]  R. Mecham,et al.  Extracellular matrix protein gene expression in atherosclerotic hypertensive pulmonary arteries. , 1992, The American journal of pathology.

[34]  M. Rekhter,et al.  Gene transfer into normal and atherosclerotic human blood vessels. , 1998, Circulation research.

[35]  A. Tall,et al.  IFN-gamma potentiates atherosclerosis in ApoE knock-out mice. , 1997, The Journal of clinical investigation.

[36]  A. Majors,et al.  Cell density and proliferation modulate collagen synthesis and procollagen mRNA levels in arterial smooth muscle cells. , 1992, Experimental cell research.

[37]  A. Tedgui,et al.  Smooth muscle cells : another source of tissue factor-containing microparticles in atherothrombosis? , 2000, Circulation research.

[38]  A. Majors,et al.  Basic fibroblast growth factor in the extracellular matrix suppresses collagen synthesis and type III procollagen mRNA levels in arterial smooth muscle cell cultures. , 1993, Arteriosclerosis and thrombosis : a journal of vascular biology.

[39]  C. Jackson,et al.  Type I collagen fibrils promote rapid vascular tube formation upon contact with the apical side of cultured endothelium. , 1991, Experimental cell research.

[40]  P. R. Myers,et al.  Vascular endothelial cell regulation of extracellular matrix collagen: role of nitric oxide. , 1998, Arteriosclerosis, thrombosis, and vascular biology.

[41]  James M. Roberts,et al.  Fibrillar Collagen Inhibits Arterial Smooth Muscle Proliferation through Regulation of Cdk2 Inhibitors , 1996, Cell.

[42]  Yasuteru Muragaki,et al.  Stretch-Induced Collagen Synthesis in Cultured Smooth Muscle Cells from Rabbit Aortic Media and a Possible Involvement of Angiotensin II and Transforming Growth Factor-β , 1998, Journal of Vascular Research.

[43]  M. Ferguson,et al.  Smooth muscle cell expression of extracellular matrix genes after arterial injury. , 1994, The American journal of pathology.

[44]  V. Fuster Elucidation off the role of plaque instability and rupture in acute coronary events , 1995 .

[45]  E. B. Smith THE INFLUENCE OF AGE AND ATHEROSCLEROSIS ON THE CHEMISTRY OF AORTIC INTIMA.2. COLLAGEN AND MUCOPOLYSACCHARIDES. , 1965, Journal of atherosclerosis research.

[46]  J. Risteli,et al.  Changes in interstitial collagen metabolism during acute myocardial infarction treated with streptokinase or tissue plasminogen activator. , 1996, American heart journal.

[47]  P. Libby,et al.  Lipid lowering by diet reduces matrix metalloproteinase activity and increases collagen content of rabbit atheroma: a potential mechanism of lesion stabilization. , 1998, Circulation.

[48]  S. Katsuda,et al.  Collagen Synthesis by Cultured Arterial Smooth Muscle Cells during Spontaneous Phenotypic Modulation , 1990, Acta pathologica japonica.

[49]  V. Fuster Mechanisms of arterial thrombosis: foundation for therapy. , 1998, American heart journal.

[50]  M. Alavi,et al.  Collagen biosynthesis by neointimal smooth muscle cells cultured from rabbit aortic explants 15 weeks after de‐endothelialization , 1998, International journal of experimental pathology.

[51]  R. Ross,et al.  Human atherosclerosis. I. Cell constitution and characteristics of advanced lesions of the superficial femoral artery. , 1984, The American journal of pathology.

[52]  S. Schwartz,et al.  Production of transforming growth factor beta 1 during repair of arterial injury. , 1991, The Journal of clinical investigation.

[53]  A. Majors,et al.  Homocysteine as a risk factor for vascular disease. Enhanced collagen production and accumulation by smooth muscle cells. , 1997, Arteriosclerosis, thrombosis, and vascular biology.

[54]  H. Robenek,et al.  Aortic smooth muscle cells in a three-dimensional collagen lattice culture. Evidence for posttranslational regulation of collagen synthesis. , 1993, Arteriosclerosis and thrombosis : a journal of vascular biology.

[55]  P. Bornstein,et al.  Regulation of expression of the type I collagen genes. , 1993, American journal of medical genetics.

[56]  K. Kivirikko,et al.  Collagen biosynthesis: a mini-review cluster. , 1998, Matrix biology : journal of the International Society for Matrix Biology.

[57]  G. Sonenshein,et al.  Basic fibroblast growth factor decreases type V/XI collagen expression in cultured bovine aortic smooth muscle cells , 1998, Journal of cellular biochemistry.

[58]  V. Koteliansky,et al.  Relative distribution of fibronectin and type I, III, IV, V collagens in normal and atherosclerotic intima of human arteries. , 1987, Atherosclerosis.

[59]  G. M. Fischer,et al.  Effects of estradiol and progesterone on the increased synthesis of collagen in atherosclerotic rabbit aortas. , 1985, Atherosclerosis.

[60]  P. Libby,et al.  The unstable atheroma. , 1997, Arteriosclerosis, thrombosis, and vascular biology.

[61]  Jussi Taipale,et al.  Growth factors in the extracellular matrix , 1997, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[62]  P. Libby,et al.  Cytokines and growth factors positively and negatively regulate interstitial collagen gene expression in human vascular smooth muscle cells. , 1991, Arteriosclerosis and thrombosis : a journal of vascular biology.

[63]  Z. Galis,et al.  Extracellular matrix modulates macrophage functions characteristic to atheroma: collagen type I enhances acquisition of resident macrophage traits by human peripheral blood monocytes in vitro. , 1998, Arteriosclerosis, thrombosis, and vascular biology.

[64]  S. Glagov,et al.  Cyclic AMP inhibits increased collagen production by cyclically stretched smooth muscle cells. , 1987, Laboratory investigation; a journal of technical methods and pathology.

[65]  S. Katsuda,et al.  Collagen synthesis of human arterial smooth muscle cells: Effects of platelet‐derived growth factor, transforming growth factor‐β1 and interleukin‐1 , 1993, Acta pathologica japonica.

[66]  P. Libby,et al.  Current concepts in cardiovascular pathology: the role of LDL cholesterol in plaque rupture and stabilization. , 1998, The American journal of medicine.

[67]  Elspeth B. Smith,et al.  The influence of age and atherosclerosis on the chemistry of aortic intima , 1965 .

[68]  V. Tertov,et al.  Triggerlike stimulation of cholesterol accumulation and DNA and extracellular matrix synthesis induced by atherogenic serum or low density lipoprotein in cultured cells. , 1990, Circulation research.

[69]  G. Sonenshein,et al.  Serum deprivation of vascular smooth muscle cells enhances collagen gene expression. , 1988, The Journal of biological chemistry.

[70]  P. Erne,et al.  Ca2+ channel blockers modulate metabolism of collagens within the extracellular matrix. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[71]  E. Nabel,et al.  Expression and function of a recombinant PDGF B gene in porcine arteries. , 1995, Arteriosclerosis, thrombosis, and vascular biology.

[72]  F. Parhami,et al.  cAMP Stimulates Osteoblast-like Differentiation of Calcifying Vascular Cells , 1998, The Journal of Biological Chemistry.

[73]  G. Karsenty,et al.  Regulation of type I collagen genes expression. , 1995, International reviews of immunology.

[74]  R. Mecham,et al.  Neointimal macrophages colocalize with extracellular matrix gene expression in human atherosclerotic pulmonary arteries. , 1993, The Journal of clinical investigation.

[75]  M. Rekhter,et al.  The importance of thrombus organization and stellate cell phenotype in collagen I gene expression in human, coronary atherosclerotic and restenotic lesions. , 1996, Cardiovascular research.

[76]  H. Robenek,et al.  Collagen synthesis in cultured aortic smooth muscle cells. Modulation by collagen lattice culture, transforming growth factor-beta 1, and epidermal growth factor. , 1991, Arteriosclerosis and thrombosis : a journal of vascular biology.

[77]  M. Pines,et al.  Inhibition of collagen synthesis, smooth muscle cell proliferation, and injury-induced intimal hyperplasia by halofuginone. , 1997, Arteriosclerosis, thrombosis, and vascular biology.

[78]  G. Liau,et al.  Regulation of extracellular matrix RNA levels in cultured smooth muscle cells. Relationship to cellular quiescence. , 1989, The Journal of biological chemistry.

[79]  T. Lüscher,et al.  Connective tissue growth factor. Friend or foe? , 1997, Arteriosclerosis, thrombosis, and vascular biology.

[80]  R. Clair,et al.  Failure of Hypercholesterolemic Serum to Stimulate Collagen Synthesis in Aortic Smooth Muscle Cells from Two Species of Nonhuman Primates Having Different Rates of Collagen Synthesis 1 , 1983, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[81]  S. Jimi,et al.  Oxidized low density lipoprotein stimulates collagen production in cultured arterial smooth muscle cells. , 1995, Atherosclerosis.

[82]  T. Krieg,et al.  Pathogenesis of fibrosis: type 1 collagen and the skin , 1998, Journal of Molecular Medicine.

[83]  Julie H. Campbell,et al.  Collagen synthesis by cultured rabbit aortic smooth-muscle cells. Alteration with phenotype. , 1990, The Biochemical journal.

[84]  D. Garcia-Dorado,et al.  Cardiovascular Research , 1966 .

[85]  K. Miyazawa,et al.  Inhibitory effects of tranilast on proliferation, migration, and collagen synthesis of human vascular smooth muscle cells. , 1996, Canadian journal of physiology and pharmacology.

[86]  R. Ross,et al.  The pathogenesis of atherosclerosis (first of two parts). , 1976, The New England journal of medicine.

[87]  E. Falk,et al.  Homocysteine and atherothrombosis , 2001, Lipids.

[88]  J. Pickering,et al.  Evidence for a role of collagen synthesis in arterial smooth muscle cell migration. , 1998, The Journal of clinical investigation.

[89]  Y Okada,et al.  Collagens in human atherosclerosis. Immunohistochemical analysis using collagen type-specific antibodies. , 1992, Arteriosclerosis and thrombosis : a journal of vascular biology.

[90]  S. Schwartz,et al.  Death by any other name. , 1995, The American journal of pathology.

[91]  E. Andreeva,et al.  Collagen-synthesizing cells in initial and advanced atherosclerotic lesions of human aorta. , 1997, Atherosclerosis.

[92]  T. Lyberg,et al.  Collagen-induced thrombus formation in flowing nonanticoagulated human blood from habitual smokers and nonsmoking patients with severe peripheral atherosclerotic disease. , 1995, Arteriosclerosis, thrombosis, and vascular biology.

[93]  M. Reidy,et al.  Mechanisms of stenosis after arterial injury. , 1983, Laboratory investigation; a journal of technical methods and pathology.

[94]  J. Davidson,et al.  Modulation of transforming growth factor‐beta 1 stimulated elastin and collagen production and proliferation in porcine vascular smooth muscle cells and skin fibroblasts by basic fibroblast growth factor, transforming growth factor‐α, and insulin‐like growth factor‐I , 1993 .

[95]  M. Rekhter,et al.  Effect of mechanical forces on growth and matrix protein synthesis in the in vitro pulmonary artery. Analysis of the role of individual cell types. , 1995, Circulation research.

[96]  S. Holm,et al.  T lymphocytes inhibit the vascular response to injury. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[97]  A. Canfield,et al.  Aortic endothelial cell heterogeneity in vitro. Lack of association between morphological phenotype and collagen biosynthesis. , 1992, Journal of cell science.

[98]  G. M. Fischer,et al.  Increased vascular collagen and elastin synthesis in experimental atherosclerosis in the rabbit. Variation in synthesis among major vessels. , 1980, Atherosclerosis.

[99]  L. Katwa,et al.  The effects of endothelin-1 on collagen type I and type III synthesis in cultured porcine coronary artery vascular smooth muscle cells. , 1996, Journal of molecular and cellular cardiology.

[100]  T. McCaffrey,et al.  Genomic instability in the type II TGF-beta1 receptor gene in atherosclerotic and restenotic vascular cells. , 1997, The Journal of clinical investigation.

[101]  G. M. Fischer,et al.  Increased synthesis of aortic collagen and elastin in experimental atherosclerosis. Inhibition by contraceptive steroids. , 1981, Atherosclerosis.

[102]  D. Brenner,et al.  Fibrogenesis and type I collagen gene regulation. , 1994, The Journal of laboratory and clinical medicine.

[103]  D. Faxon,et al.  Collagen content is significantly lower in restenotic versus nonrestenotic vessels after balloon angioplasty in the atherosclerotic rabbit model. , 1997, Circulation.

[104]  T. McCaffrey,et al.  Decreased type II/type I TGF-beta receptor ratio in cells derived from human atherosclerotic lesions. Conversion from an antiproliferative to profibrotic response to TGF-beta1. , 1995, The Journal of clinical investigation.

[105]  R. Diegelmann,et al.  Protamine selectively inhibits collagen synthesis by human intestinal smooth muscle cells and other mesenchymal cells , 1989, Journal of cellular physiology.

[106]  R. Burgeson,et al.  Collagen types. Molecular structure and tissue distribution. , 1992, Clinical orthopaedics and related research.

[107]  J. Greilberger,et al.  In vitro interactions of oxidatively modified LDL with type I, II, III, IV, and V collagen, laminin, fibronectin, and poly-D-lysine. , 1997, Arteriosclerosis, thrombosis, and vascular biology.

[108]  L. Robert,et al.  Derivatized dextrans modulate collagen synthesis in aortic smooth muscle cells. , 1995, Biochemical pharmacology.

[109]  L. Ehrhart,et al.  Modulation of types I and III procollagen synthesis at various stages of arterial smooth muscle cell growth in vitro. , 1984, Experimental cell research.

[110]  M. Ferguson,et al.  Expression of collagen, interstitial collagenase, and tissue inhibitor of metalloproteinases-1 in restenosis after carotid endarterectomy. , 1996, The American journal of pathology.

[111]  G. Hansson,et al.  Immune mechanisms in atherosclerosis. , 1994, Coronary artery disease.

[112]  P. Armstrong,et al.  Extracellular matrix remodeling after balloon angioplasty injury in a rabbit model of restenosis. , 1994, Circulation research.

[113]  D. Gordon,et al.  Nitric oxide-generating compounds inhibit total protein and collagen synthesis in cultured vascular smooth muscle cells. , 1995, Circulation research.

[114]  T. Saruta,et al.  Angiotensin II stimulates collagen synthesis in cultured vascular smooth muscle cells , 1991, Journal of hypertension.

[115]  L. Ehrhart,et al.  Substratum influence on collagen and fibronectin biosynthesis by arterial smooth muscle cells in vitro , 1986, Journal of cellular physiology.

[116]  L. Ehrhart,et al.  Stimulation of aortic protein synthesis in experimental rabbit atherosclerosis. , 1977, Atherosclerosis.

[117]  R. Derynck,et al.  Direct transfer of transforming growth factor beta 1 gene into arteries stimulates fibrocellular hyperplasia. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[118]  J. Thyberg,et al.  Phenotype modulation in primary cultures of smooth-muscle cells from rat aorta. Synthesis of collagen and elastin. , 1986, Differentiation; research in biological diversity.

[119]  Accelerated Rates of Collagen Synthesis in Atherosclerotic Arteries Quantified In Vivo , 1987, Arteriosclerosis.

[120]  B. Strauss,et al.  In vivo collagen turnover following experimental balloon angioplasty injury and the role of matrix metalloproteinases. , 1996, Circulation research.