The extracellular matrix can regulate vascular cell migration, proliferation, and survival: relationships to vascular disease

The extra cellular matrix (ECM) of the normal artery wall is a collection of fibrous proteins and associated glycoproteins embedded in a hydrated ground substance of glycosaminoglycans and proteoglycans. These distinct molecules are organized into a highly ordered network that are closely associated with the vascular cells that produce them. In addition to providing the architectural framework for the artery wall that imparts mechanical support and viscoelasticity, the ECM can regulate the behaviour of vascular cells, including their ability to migrate, proliferate and survive injury. The composition of the ECM is different within intimal lesions of atherosclerosis, which are composed of monocytes and lymphocytes from the circulation and smooth muscle cells (SMC) that migrate from the media to the intima ( Ross 1993, 1999), and these differences may contribute to the altered phenotype of vascular cells within lesions. This review will briefly outline the ECM changes observed in atherosclerosis and restenosis and the potential relationship of these changes to altered vascular cell functions.

[1]  Z. Werb,et al.  Degradation of connective tissue matrices by macrophages. II. Influence of matrix composition on proteolysis of glycoproteins, elastin, and collagen by macrophages in culture , 1980, The Journal of experimental medicine.

[2]  R. Mecham,et al.  Chemotactic activity of elastin-derived peptides. , 1980, The Journal of clinical investigation.

[3]  R. Rosenberg,et al.  An antiproliferative heparan sulfate species produced by postconfluent smooth muscle cells , 1985, The Journal of cell biology.

[4]  V. Muzykantov,et al.  Distribution of type I, III, IV and V collagen in normal and atherosclerotic human arterial wall: immunomorphological characteristics. , 1985, Collagen and related research.

[5]  P. Bornstein,et al.  Light microscopic immunolocation of thrombospondin in human tissues. , 1985, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[6]  M. Reidy,et al.  Kinetics of cellular proliferation after arterial injury. III. Endothelial and smooth muscle growth in chronically denuded vessels. , 1986, Laboratory investigation; a journal of technical methods and pathology.

[7]  B. Voss,et al.  Localization of collagen types I, III, IV and V, fibronectin and laminin in human arteries by the indirect immunofluorescence method. , 1986, Pathology, research and practice.

[8]  M. Jacob,et al.  Effect of elastin peptides on human monocytes: Ca2+ mobilization, stimulation of respiratory burst and enzyme secretion. , 1986, Biochemical and biophysical research communications.

[9]  J. Thyberg,et al.  Diverse effects of fibronectin and laminin on phenotypic properties of cultured arterial smooth muscle cells , 1988, The Journal of cell biology.

[10]  V. Velebný,et al.  Biological effects of elastin peptides. , 1988, Sbornik vedeckych praci Lekarske fakulty Karlovy university v Hradci Kralove.

[11]  E. Ruoslahti Fibronectin and its receptors. , 1988, Annual review of biochemistry.

[12]  R. Clark,et al.  Cryptic chemotactic activity of fibronectin for human monocytes resides in the 120-kDa fibroblastic cell-binding fragment. , 1988, The Journal of biological chemistry.

[13]  J. Thyberg,et al.  Regulation of differentiated properties and proliferation of arterial smooth muscle cells. , 1990, Arteriosclerosis.

[14]  J. Schittny,et al.  Molecular architecture of basement membranes , 1990, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[15]  I. Stamenkovic,et al.  CD44 is the principal cell surface receptor for hyaluronate , 1990, Cell.

[16]  J. Schwarzbauer Fibronectin: from gene to protein. , 1991, Current opinion in cell biology.

[17]  P. Bornstein,et al.  Extracellular proteins that modulate cell-matrix interactions. SPARC, tenascin, and thrombospondin. , 1991, The Journal of biological chemistry.

[18]  U. Hedin,et al.  Induction of tenascin in rat arterial injury. Relationship to altered smooth muscle cell phenotype. , 1991, The American journal of pathology.

[19]  S. Haskill,et al.  Integrins as a primary signal transduction molecule regulating monocyte immediate-early gene induction. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

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

[21]  T. Wight,et al.  The role of proteoglycans in cell adhesion, migration and proliferation , 1992, Current Biology.

[22]  R. Ross,et al.  The extracellular glycoprotein SPARC interacts with platelet-derived growth factor (PDGF)-AB and -BB and inhibits the binding of PDGF to its receptors. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[23]  D. Beezhold,et al.  Fibronectin fragments stimulate tumor necrosis factor secretion by human monocytes , 1992, Journal of leukocyte biology.

[24]  E. Dejana,et al.  Human endothelial cells express integrin receptors on the luminal aspect of their membrane. , 1992, Blood.

[25]  A. Colombatti,et al.  Emilin, a component of elastic fibers preferentially located at the elastin-microfibrils interface , 1993, The Journal of cell biology.

[26]  J. Rosenbloom,et al.  Extracellular matrix 4: The elastic fiber , 1993, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[27]  R. Ross The pathogenesis of atherosclerosis: a perspective for the 1990s , 1993, Nature.

[28]  M. Schwartz,et al.  The extracellular matrix as a cell survival factor. , 1993, Molecular biology of the cell.

[29]  C. Alpers,et al.  Osteopontin is elevated during neointima formation in rat arteries and is a novel component of human atherosclerotic plaques. , 1993, The Journal of clinical investigation.

[30]  L. Water,et al.  Adhesive properties of osteopontin: regulation by a naturally occurring thrombin-cleavage in close proximity to the GRGDS cell-binding domain. , 1994, Molecular biology of the cell.

[31]  R. Ross,et al.  Dynamic expression of alpha 1 beta 1 and alpha 2 beta 1 integrin receptors by human vascular smooth muscle cells. Alpha 2 beta 1 integrin is required for chemotaxis across type I collagen-coated membranes. , 1994, The American journal of pathology.

[32]  M. Jaye,et al.  Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation , 1994, Cell.

[33]  R. Timpl,et al.  The laminins. , 1994, Matrix biology : journal of the International Society for Matrix Biology.

[34]  P. Libby,et al.  Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. , 1994, The Journal of clinical investigation.

[35]  J. Isner,et al.  Regional differences in the distribution of the proteoglycans biglycan and decorin in the extracellular matrix of atherosclerotic and restenotic human coronary arteries. , 1994, The American journal of pathology.

[36]  M. Reed,et al.  Expression of thrombospondins by endothelial cells. Injury is correlated with TSP-1. , 1995, The American journal of pathology.

[37]  P. Bornstein,et al.  Diversity of Function Is Inherent in Matricellular Proteins: an Appraisal of Thrombospondin I , 1995 .

[38]  R. Savani,et al.  The role of hyaluronan and its receptors in restenosis after balloon angioplasty: development of a potential therapy. , 1995, International journal of tissue reactions.

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

[40]  M. Tzardi,et al.  Immunohistochemical detection of fibronectin in early and advanced atherosclerosis. , 1995, In vivo.

[41]  R. Ross,et al.  The adhesive and migratory effects of osteopontin are mediated via distinct cell surface integrins. Role of alpha v beta 3 in smooth muscle cell migration to osteopontin in vitro. , 1995, The Journal of clinical investigation.

[42]  E. Anggard,et al.  Hyaluronan (HYAL-BV 5200) inhibits neo-intimal macrophage influx after balloon-catheter induced injury in the cholesterol-fed rabbit. , 1995, Atherosclerosis.

[43]  R. Jaenisch,et al.  Type I collagen‐deficient Mov‐13 mice do not retain SPARC in the extracellular matrix: Implications for fibroblast function , 1996, Developmental dynamics : an official publication of the American Association of Anatomists.

[44]  D. Sheppard,et al.  Osteopontin N-terminal Domain Contains a Cryptic Adhesive Sequence Recognized by α9β1 Integrin* , 1996, The Journal of Biological Chemistry.

[45]  S. Shapiro,et al.  Matrilysin is expressed by lipid-laden macrophages at sites of potential rupture in atherosclerotic lesions and localizes to areas of versican deposition, a proteoglycan substrate for the enzyme. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[46]  R. Iozzo,et al.  Proteoglycans of the extracellular environment: clues from the gene and protein side offer novel perspectives in molecular diversity and function , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[47]  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.

[48]  M. Reidy,et al.  Inhibition of matrix metalloproteinase activity inhibits smooth muscle cell migration but not neointimal thickening after arterial injury. , 1996, Circulation research.

[49]  A. Clowes,et al.  Overexpression of tissue inhibitor of matrix metalloproteinase-1 inhibits vascular smooth muscle cell functions in vitro and in vivo. , 1996, Circulation research.

[50]  M. Burdick,et al.  Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44. , 1996, The Journal of clinical investigation.

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

[52]  E. Haber,et al.  Collagen VIII is expressed by vascular smooth muscle cells in response to vascular injury. , 1997, Circulation research.

[53]  J. Schlessinger Direct Binding and Activation of Receptor Tyrosine Kinases by Collagen , 1997, Cell.

[54]  M. Horton,et al.  Hyaluronan Fragments Induce Nitric-oxide Synthase in Murine Macrophages through a Nuclear Factor κB-dependent Mechanism* , 1997, The Journal of Biological Chemistry.

[55]  D. Carey,et al.  Syndecan-4 is a primary-response gene induced by basic fibroblast growth factor and arterial injury in vascular smooth muscle cells. , 1997, Arteriosclerosis, thrombosis, and vascular biology.

[56]  J. Fraser,et al.  Hyaluronan: its nature, distribution, functions and turnover , 1997, Journal of internal medicine.

[57]  J. Thyberg,et al.  Phenotypic Modulation of Smooth Muscle Cells after Arterial Injury Is Associated with Changes in the Distribution of Laminin and Fibronectin , 1997, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[58]  C. Shuttleworth Type VIII collagen. , 1997, The international journal of biochemistry & cell biology.

[59]  Pieces of eight: bioactive fragments of extracellular proteins as regulators of angiogenesis. , 1997, Trends in cell biology.

[60]  M. Ginsberg,et al.  Perspectives series: cell adhesion in vascular biology. Integrin signaling in vascular biology. , 1997, The Journal of clinical investigation.

[61]  T. Wight,et al.  Selective Expression and Processing of Biglycan during Migration of Bovine Aortic Endothelial Cells , 1997, The Journal of Biological Chemistry.

[62]  Z. Werb ECM and Cell Surface Proteolysis: Regulating Cellular Ecology , 1997, Cell.

[63]  William Arbuthnot Sir Lane,et al.  Endostatin: An Endogenous Inhibitor of Angiogenesis and Tumor Growth , 1997, Cell.

[64]  J. Thyberg,et al.  Expression of phenotype- and proliferation-related genes in rat aortic smooth muscle cells in primary culture. , 1997, Cardiovascular research.

[65]  C. S. Chen,et al.  Geometric control of cell life and death. , 1997, Science.

[66]  S. Schwartz,et al.  Neutralizing antibodies directed against osteopontin inhibit rat carotid neointimal thickening after endothelial denudation. , 1997, Arteriosclerosis, thrombosis, and vascular biology.

[67]  J. Isner,et al.  Selective deposits of versican in the extracellular matrix of restenotic lesions from human peripheral arteries. , 1997, The American journal of pathology.

[68]  J. J. Schwartz,et al.  Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated? , 1997, The Journal of clinical investigation.

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

[70]  P. Libby,et al.  Expression of the elastolytic cathepsins S and K in human atheroma and regulation of their production in smooth muscle cells. , 1998, The Journal of clinical investigation.

[71]  R. Ross,et al.  Proteoglycan distribution in lesions of atherosclerosis depends on lesion severity, structural characteristics, and the proximity of platelet-derived growth factor and transforming growth factor-beta. , 1998, The American journal of pathology.

[72]  J. Isner,et al.  Immunolocalization of thrombospondin-1 in human atherosclerotic and restenotic arteries. , 1998, American heart journal.

[73]  M. Slepian,et al.  β3-Integrins Rather Than β1-Integrins Dominate Integrin-Matrix Interactions Involved in Postinjury Smooth Muscle Cell Migration , 1998 .

[74]  N. Fausto,et al.  NF-κB Mediates αvβ3 Integrin-induced Endothelial Cell Survival , 1998, The Journal of cell biology.

[75]  Dean Y. Li,et al.  Elastin is an essential determinant of arterial morphogenesis , 1998, Nature.

[76]  K. O. Mercurius,et al.  Inhibition of vascular smooth muscle cell growth by inhibition of fibronectin matrix assembly. , 1998, Circulation research.

[77]  Masato Kato,et al.  Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2 , 1998, Nature Medicine.

[78]  R. Mecham,et al.  Novel arterial pathology in mice and humans hemizygous for elastin. , 1998, The Journal of clinical investigation.

[79]  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.

[80]  M. Crow,et al.  Adenovirus-mediated gene transfer of the human tissue inhibitor of metalloproteinase-2 blocks vascular smooth muscle cell invasiveness in vitro and modulates neointimal development in vivo. , 1998, Circulation.

[81]  K. Watson,et al.  Fibronectin and collagen I matrixes promote calcification of vascular cells in vitro, whereas collagen IV matrix is inhibitory. , 1998, Arteriosclerosis, thrombosis, and vascular biology.

[82]  R. Mecham,et al.  Action of tropoelastin and synthetic elastin sequences on vascular tone and on free Ca2+ level in human vascular endothelial cells. , 1998, Circulation research.

[83]  S. Kaul,et al.  Tenascin-C is expressed in macrophage-rich human coronary atherosclerotic plaque. , 1999, Circulation.

[84]  Induction and regulation of macrophage metalloelastase by hyaluronan fragments in mouse macrophages. , 1999, Journal of immunology.

[85]  S. Tyagi,et al.  Responses of vascular smooth muscle cell to extracellular matrix degradation , 1999, Journal of cellular biochemistry.

[86]  G. Neufeld,et al.  Glypican-1 Is a VEGF165 Binding Proteoglycan That Acts as an Extracellular Chaperone for VEGF165 * , 1999, The Journal of Biological Chemistry.

[87]  J. Isner,et al.  Antibody blockade of thrombospondin accelerates reendothelialization and reduces neointima formation in balloon-injured rat carotid artery. , 1999, Circulation.

[88]  C. Owen,et al.  The cell biology of leukocyte‐mediated proteolysis , 1999, Journal of leukocyte biology.

[89]  N. Carragher,et al.  Degraded Collagen Fragments Promote Rapid Disassembly of Smooth Muscle Focal Adhesions That Correlates with Cleavage of Pp125FAK, Paxillin, and Talin , 1999, The Journal of cell biology.

[90]  P. Cullen,et al.  Human macrophages synthesize type VIII collagen in vitro and in the atherosclerotic plaque , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[91]  R. Ross,et al.  Atherosclerosis is an inflammatory disease. , 1998, American heart journal.

[92]  A. Clowes,et al.  Matrix metalloproteinase-9 overexpression enhances vascular smooth muscle cell migration and alters remodeling in the injured rat carotid artery. , 1999, Circulation research.

[93]  P. Libby,et al.  Evidence for increased collagenolysis by interstitial collagenases-1 and -3 in vulnerable human atheromatous plaques. , 1999, Circulation.

[94]  M. Hirose,et al.  Restoration to a quiescent and contractile phenotype from a proliferative phenotype of myofibroblast-like human aortic smooth muscle cells by culture on type IV collagen gels. , 1999, Journal of biochemistry.

[95]  R. Timpl,et al.  Angiogenesis inhibitor endostatin is a distinct component of elastic fibers in vessel walls , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[96]  T. Cruz,et al.  Receptor for hyaluronan-mediated motility (RHAMM), a hyaladherin that regulates cell responses to growth factors. , 1999, Biochemical Society transactions.

[97]  M A Konerding,et al.  Angiogenesis inhibitors endostatin or TNP-470 reduce intimal neovascularization and plaque growth in apolipoprotein E-deficient mice. , 1999, Circulation.

[98]  G. Breithardt,et al.  Cholesterol-induced changes of type VIII collagen expression and distribution in carotid arteries of rabbit. , 1999, Arteriosclerosis, thrombosis, and vascular biology.

[99]  T. Wight,et al.  Formation of hyaluronan- and versican-rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells. , 1999, Arteriosclerosis, thrombosis, and vascular biology.

[100]  M. Entman,et al.  Fibronectin fragments modulate monocyte VLA-5 expression and monocyte migration. , 1999, The Journal of clinical investigation.

[101]  H. Baba,et al.  Granulocyte-macrophage colony-stimulating factor (GM-CSF) modulates the expression of type VIII collagen mRNA in vascular smooth muscle cells and both are codistributed during atherogenesis. , 1999, Arteriosclerosis, thrombosis, and vascular biology.

[102]  M D McKee,et al.  Calcification of vascular smooth muscle cell cultures: inhibition by osteopontin. , 1999, Circulation research.

[103]  H. Lijnen,et al.  Tissue inhibitor of matrix metalloproteinases-1 impairs arterial neointima formation after vascular injury in mice. , 1999, Circulation research.

[104]  N. Carragher,et al.  The Extracellular Matrix Dynamically Regulates Smooth Muscle Cell Responsiveness to PDGF a , 2000, Annals of the New York Academy of Sciences.

[105]  J. Pickering,et al.  α5β1 Integrin Expression and Luminal Edge Fibronectin Matrix Assembly by Smooth Muscle Cells after Arterial Injury , 2000 .

[106]  Peter C. Brooks,et al.  New Functions for Non-collagenous Domains of Human Collagen Type IV , 2000, The Journal of Biological Chemistry.

[107]  G. Hou,et al.  Type VIII collagen stimulates smooth muscle cell migration and matrix metalloproteinase synthesis after arterial injury. , 2000, The American journal of pathology.

[108]  C. Shanahan,et al.  Vascular Extracellular Matrix , 2002 .