Chemokines in the pathogenesis of vascular disease.

Our increasing appreciation of the importance of inflammation in vascular disease has focused attention on the molecules that direct the migration of leukocytes from the blood stream to the vessel wall. In this review, we summarize roles of the chemokines, a family of small secreted proteins that selectively recruit monocytes, neutrophils, and lymphocytes to sites of vascular injury, inflammation, and developing atherosclerosis. Chemokines induce chemotaxis through the activation of G-protein-coupled receptors, and the receptors that a given leukocyte expresses determines the chemokines to which it will respond. Monocyte chemoattractant protein 1 (MCP-1), acting through its receptor CCR2, appears to play an early and important role in the recruitment of monocytes to atherosclerotic lesions and in the formation of intimal hyperplasia after arterial injury. Acute thrombosis is an often fatal complication of atherosclerotic plaque rupture, and recent evidence suggests that MCP-1 contributes to thrombin generation and thrombus formation by generating tissue factor. Because of their critical roles in monocyte recruitment in vascular and nonvascular diseases, MCP-1 and CCR2 have become important therapeutic targets, and efforts are underway to develop potent and specific antagonists of these and related chemokines.

[1]  Steffen Jung,et al.  The chemokine KC, but not monocyte chemoattractant protein-1, triggers monocyte arrest on early atherosclerotic endothelium. , 2001, The Journal of clinical investigation.

[2]  F. Luscinskas,et al.  Fractalkine Preferentially Mediates Arrest and Migration of CD16+ Monocytes , 2003, The Journal of experimental medicine.

[3]  Melinda Fitzgerald,et al.  Immunol. Cell Biol. , 1995 .

[4]  T. Kita,et al.  Molecular Cloning of a Novel Scavenger Receptor for Oxidized Low Density Lipoprotein, SR-PSOX, on Macrophages* , 2000, The Journal of Biological Chemistry.

[5]  N. Maeda,et al.  CCR5 deficiency is not protective in the early stages of atherogenesis in apoE knockout mice. , 2003, Atherosclerosis.

[6]  R. Doms,et al.  Influence of the CCR2-V64I Polymorphism on Human Immunodeficiency Virus Type 1 Coreceptor Activity and on Chemokine Receptor Function of CCR2b, CCR3, CCR5, and CXCR4 , 1998, Journal of Virology.

[7]  B. Rollins,et al.  MCP‐1‐dependent signaling in CCR2−/− aortic smooth muscle cells , 2004, Journal of leukocyte biology.

[8]  I. Charo,et al.  Decreased atherosclerosis in CX3CR1-/- mice reveals a role for fractalkine in atherogenesis. , 2003, The Journal of clinical investigation.

[9]  S. Gordon,et al.  Linked Chromosome 16q13 Chemokines, Macrophage-Derived Chemokine, Fractalkine, and Thymus- and Activation-Regulated Chemokine, Are Expressed in Human Atherosclerotic Lesions , 2001, Arteriosclerosis, thrombosis, and vascular biology.

[10]  Y. Kawakami,et al.  The role of the C-C chemokine receptor 2 gene polymorphism V64I (CCR2-64I) in sarcoidosis in a Japanese population. , 1999, American journal of respiratory and critical care medicine.

[11]  E. Prossnitz,et al.  The role of the third intracellular loop of the neutrophil N-formyl peptide receptor in G protein coupling. , 1993, The Biochemical journal.

[12]  S M Schwartz,et al.  Developmental mechanisms underlying pathology of arteries. , 1990, Physiological reviews.

[13]  M. Reidy,et al.  Factors controlling the development of arterial lesions after injury. , 1992, Circulation.

[14]  B. Rollins,et al.  Tissue Factor Is Induced by Monocyte Chemoattractant Protein-1 in Human Aortic Smooth Muscle and THP-1 Cells* , 1997, The Journal of Biological Chemistry.

[15]  B. Rollins,et al.  Monocyte chemoattractant protein-1 accelerates atherosclerosis in apolipoprotein E-deficient mice. , 1999, Arteriosclerosis, thrombosis, and vascular biology.

[16]  B. Rollins,et al.  Abnormalities in Monocyte Recruitment and Cytokine Expression in Monocyte Chemoattractant Protein 1–deficient Mice , 1998, The Journal of experimental medicine.

[17]  O. Quehenberger,et al.  Expression of the monocyte chemoattractant protein-1 receptor CCR2 is increased in hypercholesterolemia. Differential effects of plasma lipoproteins on monocyte function. , 1999, Journal of lipid research.

[18]  P. Kubes,et al.  Human fractalkine mediates leukocyte adhesion but not capture under physiological shear conditions; a mechanism for selective monocyte recruitment , 2003, European journal of immunology.

[19]  N. Maeda,et al.  Absence of CC chemokine receptor-2 reduces atherosclerosis in apolipoprotein E-deficient mice. , 1999, Atherosclerosis.

[20]  B. Rollins,et al.  JE mRNA accumulates rapidly in aortic injury and in platelet-derived growth factor-stimulated vascular smooth muscle cells. , 1992, Circulation research.

[21]  U. Ikeda,et al.  Monocyte chemoattractant protein 1 inhibits growth of rat vascular smooth muscle cells. , 1995, The American journal of physiology.

[22]  J. Bernhagen,et al.  Stabilization of Atherosclerotic Plaques by Blockade of Macrophage Migration Inhibitory Factor After Vascular Injury in Apolipoprotein E–Deficient Mice , 2004, Circulation.

[23]  W. Kuo,et al.  A physical map of chromosome 20 established using fluorescence in situ hybridization and digital image analysis. , 1995, Genomics.

[24]  Gerrity Rg,et al.  Ultrastructural identification of monocyte-derived foam cells in fatty streak lesions. , 1980 .

[25]  Ose,et al.  Comparison of C-reactive protein and low-density lipoprotein cholesterol levels in the prediction of first cardiovascular events* , 2002 .

[26]  I. Charo,et al.  Molecular Uncoupling of Fractalkine-mediated Cell Adhesion and Signal Transduction , 1999, The Journal of Biological Chemistry.

[27]  P. Dempsey,et al.  A Disintegrin and Metalloproteinase 10-Mediated Cleavage and Shedding Regulates the Cell Surface Expression of CXC Chemokine Ligand 16 , 2004, The Journal of Immunology.

[28]  U. Ikeda,et al.  Expression of intercellular adhesion molecule-1 on rat vascular smooth muscle cells by pro-inflammatory cytokines. , 1993, Atherosclerosis.

[29]  T. Katagiri,et al.  Monocyte chemotactic protein 1 amplifies serotonin-induced vascular smooth muscle cell proliferation. , 2002, Journal of vascular research.

[30]  P. Libby,et al.  Inflammation and atherosclerosis: role of C-reactive protein in risk assessment. , 2004, The American journal of medicine.

[31]  C. Weber,et al.  Chemokine receptor (CCR2) genotype is associated with myocardial infarction and heart failure in patients under 65 years of age , 2003, Journal of Molecular Medicine.

[32]  R. D'Agostino,et al.  Chemokine receptor mutant CX3CR1-M280 has impaired adhesive function and correlates with protection from cardiovascular disease in humans. , 2003, The Journal of clinical investigation.

[33]  A. J. Valente,et al.  Minimally modified low density lipoprotein induces monocyte chemotactic protein 1 in human endothelial cells and smooth muscle cells. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[34]  G. McFadden,et al.  The viral anti-inflammatory chemokine-binding protein M-T7 reduces intimal hyperplasia after vascular injury. , 2000, The Journal of clinical investigation.

[35]  P. Libby Inflammation in atherosclerosis , 2002, Nature.

[36]  Steffen Jung,et al.  Blood monocytes consist of two principal subsets with distinct migratory properties. , 2003, Immunity.

[37]  U. V. von Andrian,et al.  Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. , 2004, Annual review of immunology.

[38]  D. Dichek,et al.  Adhesion of monocytes to vascular cell adhesion molecule-1-transduced human endothelial cells: implications for atherogenesis. , 1998, Circulation research.

[39]  A. Quyyumi,et al.  Association Between Polymorphism in the Chemokine Receptor CX3CR1 and Coronary Vascular Endothelial Dysfunction and Atherosclerosis , 2001, Circulation research.

[40]  Wei Wang,et al.  A new class of membrane-bound chemokine with a CX3C motif , 1997, Nature.

[41]  J J Goedert,et al.  Contrasting genetic influence of CCR2 and CCR5 variants on HIV-1 infection and disease progression. Hemophilia Growth and Development Study (HGDS), Multicenter AIDS Cohort Study (MACS), Multicenter Hemophilia Cohort Study (MHCS), San Francisco City Cohort (SFCC), ALIVE Study. , 1997, Science.

[42]  F. Welt,et al.  Targeting CCR2 or CD18 Inhibits Experimental In-Stent Restenosis in Primates: Inhibitory Potential Depends on Type of Injury and Leukocytes Targeted , 2002, Circulation research.

[43]  S. Coughlin,et al.  Monocyte chemoattractant protein-1 in human atheromatous plaques. , 1991, The Journal of clinical investigation.

[44]  D. Steinberg Oxidative Modification of LDL and Atherogenesis , 1998 .

[45]  Sharon Engel,et al.  A transmembrane CXC chemokine is a ligand for HIV-coreceptor Bonzo , 2000, Nature Immunology.

[46]  I. Charo,et al.  Decreased lesion formation in CCR2−/− mice reveals a role for chemokines in the initiation of atherosclerosis , 1998, Nature.

[47]  Osamu Yoshie,et al.  Cutting Edge: Profile of Chemokine Receptor Expression on Human Plasma Cells Accounts for Their Efficient Recruitment to Target Tissues 1 , 2003, The Journal of Immunology.

[48]  F. Mach,et al.  Antagonism of RANTES Receptors Reduces Atherosclerotic Plaque Formation in Mice , 2004, Circulation research.

[49]  J. Badimón,et al.  CCR2 Deficiency Decreases Intimal Hyperplasia After Arterial Injury , 2002, Arteriosclerosis, thrombosis, and vascular biology.

[50]  R. Gerrity,et al.  Ultrastructural identification of monocyte-derived foam cells in fatty streak lesions. , 1980, Artery.

[51]  E. Boerwinkle,et al.  From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part I. , 2003, Circulation.

[52]  I. Charo,et al.  Tumor Necrosis Factor- (cid:1) -converting Enzyme Mediates the Inducible Cleavage of Fractalkine* , 2022 .

[53]  M. Voskuil,et al.  Effects of local MCP-1 protein therapy on the development of the collateral circulation and atherosclerosis in Watanabe hyperlipidemic rabbits. , 2003, Cardiovascular research.

[54]  W. Schaper,et al.  Collateral Artery Growth (Arteriogenesis) After Experimental Arterial Occlusion Is Impaired in Mice Lacking CC-Chemokine Receptor-2 , 2004, Circulation research.

[55]  Robert V Farese,et al.  Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. , 1997, The Journal of clinical investigation.

[56]  D. Soler,et al.  Expression Cloning of the STRL33/BONZO/TYMSTR Ligand Reveals Elements of CC, CXC, and CX3C Chemokines , 2001, The Journal of Immunology.

[57]  W. Kübler,et al.  Monocyte chemoattractant protein-1 induces proliferation and interleukin-6 production in human smooth muscle cells by differential activation of nuclear factor-kappaB and activator protein-1. , 2002, Arteriosclerosis, thrombosis, and vascular biology.

[58]  T. Kurihara,et al.  Cloning and Functional Expression of mCCR2, a Murine Receptor for the C-C Chemokines JE and FIC (*) , 1996, The Journal of Biological Chemistry.

[59]  E. Antman,et al.  Association Between Plasma Levels of Monocyte Chemoattractant Protein-1 and Long-Term Clinical Outcomes in Patients With Acute Coronary Syndromes , 2003, Circulation.

[60]  B. Rollins,et al.  Transgenic monocyte chemoattractant protein-1 (MCP-1) in pancreatic islets produces monocyte-rich insulitis without diabetes: abrogation by a second transgene expressing systemic MCP-1. , 1997, Journal of immunology.

[61]  J. Gutiérrez-Ramos,et al.  Neurotactin, a membrane-anchored chemokine upregulated in brain inflammation , 1997, Nature.

[62]  Marc W. Kirschner,et al.  A PtdInsP3- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity , 2002, Nature Cell Biology.

[63]  A. Takeshita,et al.  Importance of Monocyte Chemoattractant Protein-1 Pathway in Neointimal Hyperplasia After Periarterial Injury in Mice and Monkeys , 2002, Circulation research.

[64]  A. J. Valente,et al.  Elevated expression of monocyte chemoattractant protein 1 by vascular smooth muscle cells in hypercholesterolemic primates. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[65]  K. Ley,et al.  Deposition of Platelet RANTES Triggering Monocyte Recruitment Requires P-Selectin and Is Involved in Neointima Formation After Arterial Injury , 2002, Circulation.

[66]  T. Kita,et al.  Cell surface‐anchored SR‐PSOX/CXC chemokine ligand 16 mediates firm adhesion of CXC chemokine receptor 6‐expressing cells , 2004, Journal of leukocyte biology.

[67]  R. Ross,et al.  Growth Regulatory Mechanisms and Formation of the Lesions of Atherosclerosis a , 1994, Annals of the New York Academy of Sciences.

[68]  Armin Helisch,et al.  Arteriogenesis The Development and Growth of Collateral Arteries , 2003, Microcirculation.

[69]  Jingsong Xu,et al.  Divergent Signals and Cytoskeletal Assemblies Regulate Self-Organizing Polarity in Neutrophils , 2003, Cell.

[70]  A. Alcamí,et al.  Inhibition of intimal hyperplasia in transgenic mice conditionally expressing the chemokine-binding protein M3. , 2004, The American journal of pathology.

[71]  M. Voskuil,et al.  Local Monocyte Chemoattractant Protein-1 Therapy Increases Collateral Artery Formation in Apolipoprotein E–Deficient Mice but Induces Systemic Monocytic CD11b Expression, Neointimal Formation, and Plaque Progression , 2003, Circulation research.

[72]  A. Matsumori,et al.  Anti-monocyte chemoattractant protein-1/monocyte chemotactic and activating factor antibody inhibits neointimal hyperplasia in injured rat carotid arteries. , 1999, Circulation research.

[73]  B. Brenner,et al.  Chemokine receptor polymorphism and risk of acute rejection in human renal transplantation. , 2002, Journal of the American Society of Nephrology : JASN.

[74]  Weixin Zhao,et al.  Human Vascular Smooth Muscle Cells Possess Functional CCR5* , 2000, The Journal of Biological Chemistry.

[75]  D. Salant,et al.  Targeted deletion of CX3CR1 reveals a role for fractalkine in cardiac allograft rejection , 2001 .

[76]  R. Ross,et al.  Studies of Hypercholesterolemia in the Nonhuman Primate: I. Changes that Lead to Fatty Streak Formation , 1984, Arteriosclerosis.

[77]  B. Rollins,et al.  MCP-1 deficiency is associated with reduced intimal hyperplasia after arterial injury. , 2003, Biochemical and biophysical research communications.

[78]  A. Luster,et al.  Murine Monocyte Chemoattractant Protein (MCP)-5: A Novel CC Chemokine That Is a Structural and Functional Homologue of Human MCP-1 , 1997, The Journal of experimental medicine.

[79]  Christine M. Miller,et al.  CCL11 (Eotaxin) Induces CCR3-Dependent Smooth Muscle Cell Migration , 2004, Arteriosclerosis, thrombosis, and vascular biology.

[80]  Y. Minami,et al.  Fractalkine, a CX3C‐chemokine, functions predominantly as an adhesion molecule in monocytic cell line THP‐1 , 2001, Immunology and cell biology.

[81]  P. Debré,et al.  Decreased Atherosclerotic Lesion Formation in CX3CR1/Apolipoprotein E Double Knockout Mice , 2003, Circulation.

[82]  D. Salant,et al.  Targeted deletion of CX(3)CR1 reveals a role for fractalkine in cardiac allograft rejection. , 2001, The Journal of clinical investigation.

[83]  J. Fallon,et al.  Chemokine receptor-8 (CCR8) mediates human vascular smooth muscle cell chemotaxis and metalloproteinase-2 secretion. , 2004, Blood.

[84]  M. Loda,et al.  Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1 , 2000, Nature.

[85]  B. Rollins,et al.  Chemokines and disease , 2001, Nature Immunology.

[86]  J. Badimón,et al.  Mouse model of femoral artery denudation injury associated with the rapid accumulation of adhesion molecules on the luminal surface and recruitment of neutrophils. , 2000, Arteriosclerosis, thrombosis, and vascular biology.

[87]  R. Terkeltaub,et al.  A leukocyte homologue of the IL-8 receptor CXCR-2 mediates the accumulation of macrophages in atherosclerotic lesions of LDL receptor-deficient mice. , 1998, The Journal of clinical investigation.

[88]  G. Mancia,et al.  Treatment of Hypertension and Ischemic Heart Disease , 1989, Journal of cardiovascular pharmacology.

[89]  P. Norman,et al.  Monocyte chemoattractant protein‐1 gene expression in injured pig artery coincides with early appearance of infiltrating monocyte/macrophages , 1996, Journal of cellular biochemistry.

[90]  Andrew C. Li,et al.  Oxidized LDL reduces monocyte CCR2 expression through pathways involving peroxisome proliferator-activated receptor gamma. , 2000, The Journal of clinical investigation.

[91]  Antonio Colombo,et al.  From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part II. , 2003, Circulation.

[92]  U. Hedin,et al.  CXCL16/SR-PSOX Is an Interferon-&ggr;–Regulated Chemokine and Scavenger Receptor Expressed in Atherosclerotic Lesions , 2004, Arteriosclerosis, thrombosis, and vascular biology.

[93]  P. Libby,et al.  Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. , 1998, Molecular cell.

[94]  F. Luscinskas,et al.  MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions , 1999, Nature.

[95]  D. Steinberg,et al.  Lewis A. Conner Memorial Lecture. Oxidative modification of LDL and atherogenesis. , 1997, Circulation.

[96]  D. Rader,et al.  Val64Ile Polymorphism in the C-C Chemokine Receptor 2 Is Associated With Reduced Coronary Artery Calcification , 2002, Arteriosclerosis, thrombosis, and vascular biology.

[97]  D. Patel,et al.  Fractalkine and CX3CR1 Mediate a Novel Mechanism of Leukocyte Capture, Firm Adhesion, and Activation under Physiologic Flow , 1998, The Journal of experimental medicine.

[98]  A. Schober,et al.  Crucial Role of Stromal Cell–Derived Factor-1&agr; in Neointima Formation After Vascular Injury in Apolipoprotein E–Deficient Mice , 2003, Circulation.

[99]  B. Rollins,et al.  MCP-1 deficiency reduces susceptibility to atherosclerosis in mice that overexpress human apolipoprotein B. , 1999, The Journal of clinical investigation.

[100]  M. Reidy,et al.  Regulation of Smooth Muscle Cell Growth in Injured Artery , 1989, Journal of cardiovascular pharmacology.