Extracellular matrix alterations in hypertensive vascular remodeling.

Vascular cells are very sensitive to their hemodynamic environment. Any change in blood pressure or blood flow can be sensed by endothelial and vascular smooth muscle cells and ultimately results in structural modifications within the vascular wall that accommodate the new conditions. In the case of hypertension, the increase in arterial stretch stimulates vessel thickening to normalize the tensile forces. This process requires modification of the extracellular matrix and of cell-matrix interactions, which mainly involves extracellular proteases. In hypertension, chronic exposure of the arterial wall to stretch leads to vascular remodeling, arterial stiffness and calcification, which finally affect target organ function. This review surveys how mechanical stretch regulates extracellular proteases, considering the signaling pathways involved and the consequences on the cardiovascular system.

[1]  Z. Galis,et al.  This Review Is Part of a Thematic Series on Matrix Metalloproteinases, Which Includes the following Articles: Matrix Metalloproteinase Inhibition after Myocardial Infarction: a New Approach to Prevent Heart Failure? Matrix Metalloproteinases in Vascular Remodeling and Atherogenesis: the Good, the Ba , 2022 .

[2]  P. Libby,et al.  Arterial and Aortic Valve Calcification Abolished by Elastolytic Cathepsin S Deficiency in Chronic Renal Disease , 2009, Circulation.

[3]  H. Jo,et al.  Expression of cathepsin K is regulated by shear stress in cultured endothelial cells and is increased in endothelium in human atherosclerosis. , 2007, American journal of physiology. Heart and circulatory physiology.

[4]  P. Carmeliet,et al.  Temporal and Topographic Matrix Metalloproteinase Expression after Vascular Injury in Mice , 1999, Thrombosis and Haemostasis.

[5]  Albert Hofman,et al.  Arterial Stiffness and Risk of Coronary Heart Disease and Stroke: The Rotterdam Study , 2006, Circulation.

[6]  J. Avruch,et al.  Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. , 2001, Physiological reviews.

[7]  Stefan Störk,et al.  Carotid Artery Plaque Burden, Stiffness, and Mortality Risk in Elderly Men: A Prospective, Population-Based Cohort Study , 2004, Circulation.

[8]  AlainTedgui,et al.  Pulsatile Stretch–Induced Extracellular Signal–Regulated Kinase 1/2 Activation in Organ Culture of Rabbit Aorta Involves Reactive Oxygen Species , 2000 .

[9]  A. Tedgui,et al.  Signal transduction of mechanical stresses in the vascular wall. , 1998, Hypertension.

[10]  Ali A Haydar,et al.  Coronary artery calcification and aortic pulse wave velocity in chronic kidney disease patients. , 2004, Kidney international.

[11]  J. Díez,et al.  Abnormalities of the extracellular degradation of collagen type I in essential hypertension. , 1998, Circulation.

[12]  D. Kass,et al.  Mechanisms, pathophysiology, and therapy of arterial stiffness. , 2005, Arteriosclerosis, thrombosis, and vascular biology.

[13]  H. van Essen,et al.  Determination of Aortic Elastic Modulus by Pulse Wave Velocity and Wall Tracking in a Rat Model of Aortic Stiffness , 2001, Journal of Vascular Research.

[14]  D. Seals,et al.  The ADAMs family of metalloproteases: multidomain proteins with multiple functions. , 2003, Genes & development.

[15]  A. Pries,et al.  Microcirculation in Hypertension: A New Target for Treatment? , 2001, Circulation.

[16]  K. Brew,et al.  Tissue inhibitors of metalloproteinases: evolution, structure and function. , 2000, Biochimica et biophysica acta.

[17]  R. Guldberg,et al.  Inactivation of the Osteopontin Gene Enhances Vascular Calcification of Matrix Gla Protein–deficient Mice , 2002, The Journal of experimental medicine.

[18]  K. Hruska,et al.  Bone Morphogenetic Proteins in Vascular Calcification , 2005, Circulation research.

[19]  V. Tkachuk,et al.  Increased pressure induces sustained protein kinase C-independent herbimycin A-sensitive activation of extracellular signal-related kinase 1/2 in the rabbit aorta in organ culture. , 1997, Circulation research.

[20]  N. Fukuda,et al.  Contribution of synthetic phenotype on the enhanced angiotensin II-generating system in vascular smooth muscle cells from spontaneously hypertensive rats. , 1999, Journal of hypertension.

[21]  A. Tedgui,et al.  Role of Matrix Metalloproteinases in Early Hypertensive Vascular Remodeling , 2007, Hypertension.

[22]  M. Gorospe,et al.  Acute hypertension activates mitogen-activated protein kinases in arterial wall. , 1996, The Journal of clinical investigation.

[23]  B. Sobel,et al.  Maladaptive arterial remodeling with systemic hypertension associated with increased concentrations in blood of plasminogen activator inhibitor type-1 (PAI-1). , 2004, The American journal of cardiology.

[24]  A. Tedgui,et al.  Pressure-Induced Matrix Metalloproteinase-9 Contributes to Early Hypertensive Remodeling , 2004, Circulation.

[25]  T. Haas,et al.  Static strain stimulates expression of matrix metalloproteinase‐2 and VEGF in microvascular endothelium via JNK‐ and ERK‐dependent pathways , 2007, Journal of cellular biochemistry.

[26]  B. Pannier,et al.  Creatinine clearance, pulse wave velocity, carotid compliance and essential hypertension. , 2001, Kidney international.

[27]  P. Ducimetiere,et al.  Aortic Stiffness Is an Independent Predictor of All-Cause and Cardiovascular Mortality in Hypertensive Patients , 2001, Hypertension.

[28]  L. Demer A skeleton in the atherosclerosis closet. , 1995, Circulation.

[29]  Edward G Lakatta,et al.  Arterial and Cardiac Aging: Major Shareholders in Cardiovascular Disease Enterprises: Part III: Cellular and Molecular Clues to Heart and Arterial Aging , 2003, Circulation.

[30]  M. Matsumoto,et al.  Associations of Brachial-Ankle Pulse Wave Velocity and Carotid Atherosclerotic Lesions with Silent Cerebral Lesions , 2007, Hypertension Research.

[31]  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.

[32]  I. Wilkinson,et al.  ARTERIAL STIFFNESS, ENDOTHELIAL FUNCTION AND NOVEL PHARMACOLOGICAL APPROACHES , 2004, Clinical and experimental pharmacology & physiology.

[33]  Huan Wang,et al.  The upregulation of ICAM-1 and P-selectin requires high blood pressure but not circulating renin–angiotensin system in vivo , 2004, Journal of hypertension.

[34]  M. Daemen,et al.  Cathepsin cysteine proteases in cardiovascular disease , 2007, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[35]  S. Morony,et al.  osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. , 1998, Genes & development.

[36]  G. London Large arteries haemodynamics: conduit versus cushioning function. , 1997, Blood pressure. Supplement.

[37]  J. McEwan,et al.  Matrix metalloproteinases and cardiovascular disease. , 1995, Circulation research.

[38]  E. Mannarino,et al.  Relation Between Renal Function Within the Normal Range and Central and Peripheral Arterial Stiffness in Hypertension , 2006, Hypertension.

[39]  Y. Castier,et al.  Role of NF-kappaB in flow-induced vascular remodeling. , 2009, Antioxidants & redox signaling.

[40]  E. Lakatta,et al.  Elevated Aortic Pulse Wave Velocity, a Marker of Arterial Stiffness, Predicts Cardiovascular Events in Well-Functioning Older Adults , 2005, Circulation.

[41]  C. Rondelli,et al.  Morphological and biochemical characterization of remodeling in aorta and vena cava of DOCA-salt hypertensive rats. , 2007, American journal of physiology. Heart and circulatory physiology.

[42]  Anne-Sophie Rigaud,et al.  Relationship Between Arterial Stiffness and Cognitive Function in Elderly Subjects With Complaints of Memory Loss , 2005, Stroke.

[43]  Robert M. Graham,et al.  Transglutaminases: crosslinking enzymes with pleiotropic functions , 2003, Nature Reviews Molecular Cell Biology.

[44]  L. Romanowicz,et al.  Preeclampsia-associated reduction of cathepsin D activity in the umbilical cord. , 2005, Clinica chimica acta; international journal of clinical chemistry.

[45]  D. Vaughan,et al.  Potential roles of plasminogen activator system in coronary vascular remodeling induced by long-term nitric oxide synthase inhibition. , 2002, Journal of molecular and cellular cardiology.

[46]  M. Laule,et al.  Downregulation of Matrix Metalloproteinases and Collagens and Suppression of Cardiac Fibrosis by Inhibition of the Proteasome , 2004, Hypertension.

[47]  Jay D. Humphrey,et al.  Time Courses of Growth and Remodeling of Porcine Aortic Media During Hypertension: A Quantitative Immunohistochemical Examination , 2008, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[48]  Robert T Tranquillo,et al.  Elastic fiber production in cardiovascular tissue-equivalents. , 2003, Matrix biology : journal of the International Society for Matrix Biology.

[49]  A. Tedgui,et al.  Pressure-Induced Vascular Activation of Nuclear Factor-&kgr;B: Role in Cell Survival , 2003, Circulation research.

[50]  Avrum I. Gotlieb,et al.  Wall Tissue Remodeling Regulates Longitudinal Tension in Arteries , 2002, Circulation research.

[51]  K. Fujiwara,et al.  ECM remodeling in hypertensive heart disease. , 2007, The Journal of clinical investigation.

[52]  P. Toutouzas,et al.  Plasma levels of active extracellular matrix metalloproteinases 2 and 9 in patients with essential hypertension before and after antihypertensive treatment , 2003, Journal of Human Hypertension.

[53]  London Gm Large arteries haemodynamics: conduit versus cushioning function. , 1997 .

[54]  R. Terkeltaub,et al.  Transglutaminase 2 Is Central to Induction of the Arterial Calcification Program by Smooth Muscle Cells , 2008, Circulation research.

[55]  T. Hunter,et al.  Focal Adhesion Kinase Overexpression Enhances Ras-dependent Integrin Signaling to ERK2/Mitogen-activated Protein Kinase through Interactions with and Activation of c-Src* , 1997, The Journal of Biological Chemistry.

[56]  Roger D. Kamm,et al.  Mechanotransduction through growth-factor shedding into the extracellular space , 2004, Nature.

[57]  Z. Ungvari,et al.  Regulation of Bone Morphogenetic Protein-2 Expression in Endothelial Cells , 2005 .

[58]  Z. Ungvari,et al.  Chronic high pressure-induced arterial oxidative stress: involvement of protein kinase C-dependent NAD(P)H oxidase and local renin-angiotensin system. , 2004, The American journal of pathology.

[59]  Shunqiang Li,et al.  Angiotensin II and EGF receptor cross-talk in chronic kidney diseases: a new therapeutic approach , 2005, Nature Medicine.

[60]  N. Winer,et al.  Vascular compliance in hypertension: Therapeutic implications , 2008, Current diabetes reports.

[61]  J. Blacher,et al.  Conventional Antihypertensive Drug Therapy Does Not Prevent the Increase of Pulse Pressure With Age , 2001, Hypertension.

[62]  Attila Kovacs,et al.  Developmental adaptation of the mouse cardiovascular system to elastin haploinsufficiency. , 2003, The Journal of clinical investigation.

[63]  A. Clowes,et al.  Regulation of vascular smooth muscle cell migration and proliferation in vitro and in injured rat arteries by a synthetic matrix metalloproteinase inhibitor. , 1996, Arteriosclerosis, thrombosis, and vascular biology.

[64]  A. Tedgui,et al.  Transforming Growth Factor- Mediates Nuclear Factor B Activation in Strained Arteries , 2006 .

[65]  A. Cho,et al.  Matrix Metalloproteinase-9 Is Necessary for the Regulation of Smooth Muscle Cell Replication and Migration After Arterial Injury , 2002, Circulation research.

[66]  Michael F O'Rourke,et al.  Arterial aging: pathophysiological principles , 2007, Vascular medicine.

[67]  A. Tedgui,et al.  Differential Regulation of Vascular Focal Adhesion Kinase by Steady Stretch and Pulsatility , 2005, Circulation.

[68]  M. Aoki,et al.  Hypertension Accelerated Experimental Abdominal Aortic Aneurysm Through Upregulation of Nuclear Factor &kgr;B and Ets , 2006, Hypertension.

[69]  A. D'Angelo,et al.  Matrix metalloproteinase-2, -9, and tissue inhibitor of metalloproteinase-1 in patients with hypertension. , 2006, Endothelium : journal of endothelial cell research.

[70]  R. Nemenoff,et al.  Activation of JNK/SAPK and ERK by mechanical strain in vascular smooth muscle cells depends on extracellular matrix composition. , 1997, Biochemical and biophysical research communications.

[71]  A. Newby,et al.  Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. , 2005, Physiological reviews.

[72]  N Westerhof,et al.  Haemodynamic basis for the development of left ventricular failure in systolic hypertension and for its logical therapy. , 1995, Journal of hypertension.

[73]  Gillian Murphy,et al.  Metalloproteinase inhibitors: biological actions and therapeutic opportunities , 2002, Journal of Cell Science.