Mass transport in arteries and the localization of atherosclerosis.

Atherosclerosis is a disease of the large arteries that involves a characteristic accumulation of high-molecular-weight lipoprotein in the arterial wall. This review focuses on the mass transport processes that mediate the focal accumulation of lipid in arteries and places particular emphasis on the role of fluid mechanical forces in modulating mass transport phenomena. In the final analysis, four mass transport mechanisms emerge that may be important in the localization of atherosclerosis: blood phase controlled hypoxia, leaky endothelial junctions, transient intercellular junction remodeling, and convective clearance of the subendothelial intima and media. Further study of these mechanisms may contribute to the development of therapeutic strategies for atherosclerotic diseases.

[1]  J. Tarbell,et al.  In vitro Study of Starling’s Hypothesis in a Cultured Monolayer of Bovine Aortic Endothelial Cells , 2003, Journal of Vascular Research.

[2]  J. Tarbell,et al.  Solute Transport to the Endothelial Intercellular Cleft: The Effect of Wall Shear Stress , 2002, Annals of Biomedical Engineering.

[3]  S. Wada,et al.  Theoretical Prediction of Low-Density Lipoproteins Concentration at the Luminal Surface of an Artery with a Multiple Bend , 2002, Annals of Biomedical Engineering.

[4]  J. Tarbell,et al.  Oscillatory shear alters endothelial hydraulic conductivity and nitric oxide levels. , 2002, Biochemical and biophysical research communications.

[5]  C. R. Ethier,et al.  Computational Modeling of Mass Transfer and Links to Atherosclerosis , 2002, Annals of Biomedical Engineering.

[6]  G. Truskey,et al.  Effect of Fluid Shear Stress on the Permeability of the Arterial Endothelium , 2002, Annals of Biomedical Engineering.

[7]  H. Okumura,et al.  Molecular basis for the inhibition of hypoxia-induced apoptosis by 2-deoxy-D-ribose. , 2002, Biochemical and biophysical research communications.

[8]  Gregory Y H Lip,et al.  Vascular endothelial growth factor and its receptor, Flt-1, in the plasma of patients with coronary or peripheral atherosclerosis, or Type II diabetes. , 2002, Clinical science.

[9]  A. Zeiher,et al.  Aging Enhances the Sensitivity of Endothelial Cells Toward Apoptotic Stimuli: Important Role of Nitric Oxide , 2001, Circulation research.

[10]  J A Frangos,et al.  Analysis of temporal shear stress gradients during the onset phase of flow over a backward-facing step. , 2001, Journal of biomechanical engineering.

[11]  P. Friedl,et al.  Proatherogenic flow conditions initiate endothelial apoptosis via thrombospondin-1 and the integrin-associated protein. , 2001, Biochemical and biophysical research communications.

[12]  M. Bernfield,et al.  Structural Characterization of Heparan Sulfate and Chondroitin Sulfate of Syndecan-1 Purified from Normal Murine Mammary Gland Epithelial Cells , 2001, The Journal of Biological Chemistry.

[13]  M. Aoki,et al.  Endothelial Apoptosis Induced by Oxidative Stress Through Activation of NF-&kgr;B: Antiapoptotic Effect of Antioxidant Agents on Endothelial Cells , 2001, Hypertension.

[14]  J. Tarbell,et al.  Shear stress regulates occludin content and phosphorylation. , 2001, American journal of physiology. Heart and circulatory physiology.

[15]  M. Lever,et al.  Effect of altered flow on the pattern of permeability around rabbit aortic branches. , 2001, American journal of physiology. Heart and circulatory physiology.

[16]  P. Cowin,et al.  General Themes in Cell–Cell Junctions and Cell Adhesion , 2001 .

[17]  C. Smith,et al.  Relationship between Tight Junctions and Leukocyte Transmigration , 2001 .

[18]  J. Tarbell,et al.  Fenestral Pore Size in the Internal Elastic Lamina Affects Transmural Flow Distribution in the Artery Wall , 2001, Annals of Biomedical Engineering.

[19]  John A. Frangos,et al.  Temporal Gradients in Shear, but Not Spatial Gradients, Stimulate Endothelial Cell Proliferation , 2001, Circulation.

[20]  J. Tarbell,et al.  Kinetics of placenta growth factor/vascular endothelial growth factor synergy in endothelial hydraulic conductivity and proliferation. , 2001, Microvascular research.

[21]  C. R. Ethier,et al.  Mass Transport in an Anatomically Realistic Human Right Coronary Artery , 2001, Annals of Biomedical Engineering.

[22]  J. Tarbell,et al.  A biphasic, anisotropic model of the aortic wall. , 2001, Journal of biomechanical engineering.

[23]  J. Tarbell,et al.  Effect of VEGF on retinal microvascular endothelial hydraulic conductivity: the role of NO. , 2000, Investigative ophthalmology & visual science.

[24]  J. Coles,et al.  Plant lectin binding specificity to carbohydrates on porcine endothelial cells. , 2000, Transplantation proceedings.

[25]  S. Weinbaum,et al.  Starling forces that oppose filtration after tissue oncotic pressure is increased. , 2000, American journal of physiology. Heart and circulatory physiology.

[26]  Eugene S. Lee,et al.  Transarterial wall oxygen gradients at a prosthetic vascular graft to artery anastomosis in the rabbit. , 2000, Journal of vascular surgery.

[27]  O. Tricot,et al.  Relation between endothelial cell apoptosis and blood flow direction in human atherosclerotic plaques. , 2000, Circulation.

[28]  ZiadMallat,et al.  Relation Between Endothelial Cell Apoptosis and Blood Flow Direction in Human Atherosclerotic Plaques , 2000 .

[29]  Y. Taniyama,et al.  Hypoxia-Induced Endothelial Apoptosis Through Nuclear Factor-κB (NF-κB)–Mediated bcl-2 Suppression In Vivo Evidence of the Importance of NF-κB in Endothelial Cell Regulation , 2000 .

[30]  T. W. Secomb,et al.  The endothelial surface layer , 2000, Pflügers Archiv.

[31]  T W Gardner,et al.  Effect of vascular endothelial growth factor on cultured endothelial cell monolayer transport properties. , 2000, Microvascular research.

[32]  Juin-jen Chang,et al.  Casual police corruption and the economics of crime:: Further results , 2000 .

[33]  J. Tarbell,et al.  Numerical simulation of pulsatile flow in a compliant curved tube model of a coronary artery. , 2000, Journal of biomechanical engineering.

[34]  J. Tarbell,et al.  Effect of shear stress on the hydraulic conductivity of cultured bovine retinal microvascular endothelial cell monolayers , 2000, Current eye research.

[35]  J. Tarbell,et al.  Arterial Wall Mass Transport: The Possible Role of Blood Phase Resistance in the Localization of Arterial Disease , 1999 .

[36]  M. Kajimura,et al.  Flow modulates the transport of K+ through the walls of single perfused mesenteric venules in anaesthetised rats , 1999, The Journal of physiology.

[37]  S. Weinbaum,et al.  A new view of Starling's hypothesis at the microstructural level. , 1999, Microvascular research.

[38]  B L Langille,et al.  Transient and steady-state effects of shear stress on endothelial cell adherens junctions. , 1999, Circulation research.

[39]  D. Goodenough,et al.  Paracellular Channels! , 1999, Science.

[40]  J. Tarbell,et al.  Effect of pressure on hydraulic conductivity of endothelial monolayers: role of endothelial cleft shear stress. , 1999, Journal of applied physiology.

[41]  D. Williams,et al.  Network assessment of capillary hydraulic conductivity after abrupt changes in fluid shear stress. , 1999, Microvascular research.

[42]  C Kleinstreuer,et al.  Relation between non-uniform hemodynamics and sites of altered permeability and lesion growth at the rabbit aorto-celiac junction. , 1999, Atherosclerosis.

[43]  R. Bizios,et al.  Exposure of human vascular endothelial cells to sustained hydrostatic pressure stimulates proliferation. Involvement of the alphaV integrins. , 1999, Circulation research.

[44]  H. Dvorak,et al.  Caveolae and Vesiculo-Vacuolar Organelles in Bovine Capillary Endothelial Cells Cultured with VPF/VEGF on Floating Matrigel-collagen Gels , 1999, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[45]  S. Weinbaum,et al.  Structural changes in rat aortic intima due to transmural pressure. , 1998, Journal of biomechanical engineering.

[46]  Sheldon Weinbaum,et al.  1997 Whitaker Distinguished Lecture: Models to Solve Mysteries in Biomechanics at the Cellular Level; A New View of Fiber Matrix Layers , 1998, Annals of Biomedical Engineering.

[47]  M. Kuzuya,et al.  Induction of macrophage VEGF in response to oxidized LDL and VEGF accumulation in human atherosclerotic lesions. , 1998, Arteriosclerosis, thrombosis, and vascular biology.

[48]  Kazushi Fujimoto,et al.  Claudin-1 and -2: Novel Integral Membrane Proteins Localizing at Tight Junctions with No Sequence Similarity to Occludin , 1998, The Journal of cell biology.

[49]  G. Thurston,et al.  Inhibition of nitric oxide synthesis increases venular permeability and alters endothelial actin cytoskeleton. , 1998, American journal of physiology. Heart and circulatory physiology.

[50]  K. Oka,et al.  Albumin concentration profile inside cultured endothelial cells exposed to shear stress , 1997 .

[51]  H. Schnittler,et al.  Role of cadherins and plakoglobin in interendothelial adhesion under resting conditions and shear stress. , 1997, American journal of physiology. Heart and circulatory physiology.

[52]  A. Cho,et al.  Effects of changes in blood flow rate on cell death and cell proliferation in carotid arteries of immature rabbits. , 1997, Circulation research.

[53]  J. Tarbell,et al.  Wall shear rate distribution in an abdominal aortic bifurcation model: effects of vessel compliance and phase angle between pressure and flow waveforms. , 1997, Journal of biomechanical engineering.

[54]  P. Weinberg,et al.  Changes with age in the influence of endogenous nitric oxide on transport properties of the rabbit aortic wall near branches. , 1997, Arteriosclerosis, thrombosis, and vascular biology.

[55]  K J Gooch,et al.  Exogenous, basal, and flow‐induced nitric oxide production and endothelial cell proliferation , 1997, Journal of cellular physiology.

[56]  J. Isner,et al.  Vascular endothelial growth factor/vascular permeability factor (VEGF/VPF) in normal and atherosclerotic human arteries. , 1997, The American journal of pathology.

[57]  S. Weinbaum,et al.  A fiber matrix model for the filtration through fenestral pores in a compressible arterial intima. , 1997, The American journal of physiology.

[58]  N. Ferrara,et al.  The biology of vascular endothelial growth factor. , 1997, Endocrine reviews.

[59]  M. Nehls,et al.  Shear stress inhibits apoptosis of human endothelial cells , 1996, FEBS letters.

[60]  M. Lever,et al.  Plasma protein entry and retention in the vascular wall: possible factors in atherogenesis. , 1996, Canadian journal of physiology and pharmacology.

[61]  B. Ward,et al.  Microvascular permeability of the isolated rat heart to various solutes in well-oxygenated and hypoxic conditions. , 1996, International journal of microcirculation, clinical and experimental.

[62]  L. Nielsen,et al.  Transfer of low density lipoprotein into the arterial wall and risk of atherosclerosis. , 1996, Atherosclerosis.

[63]  T. Yoshimoto,et al.  Astroglial cells inhibit the increasing permeability of brain endothelial cell monolayer following hypoxia/reoxygenation , 1996, Neuroscience Letters.

[64]  W. Schaper,et al.  Effects of barbiturates on hypoxic cultures of brain derived microvascular endothelial cells , 1996, Brain Research.

[65]  K. Jan,et al.  Ultrastructural studies on macromolecular permeability in relation to endothelial cell turnover. , 1995, Atherosclerosis.

[66]  C. V. Van Itallie,et al.  Tight junctions and the molecular basis for regulation of paracellular permeability. , 1995, The American journal of physiology.

[67]  M. Corada,et al.  Endothelial cell‐to‐cell junctions , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[68]  G. Truskey,et al.  The distribution of intimal white blood cells in the normal rabbit aorta. , 1995, Atherosclerosis.

[69]  J A Frangos,et al.  Shear stress increases hydraulic conductivity of cultured endothelial monolayers. , 1995, The American journal of physiology.

[70]  P. Oh,et al.  Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules , 1994, The Journal of cell biology.

[71]  Choll W. Kim,et al.  Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and development-specific patterns. , 1994, Molecular biology of the cell.

[72]  W D Wagner,et al.  A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. , 1994, Arteriosclerosis and thrombosis : a journal of vascular biology.

[73]  D. Predescu,et al.  Transcytosis in the continuous endothelium of the myocardial microvasculature is inhibited by N-ethylmaleimide. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[74]  G. Truskey,et al.  Characterization of sites with elevated LDL permeability at intercostal, celiac, and iliac branches of the normal rabbit aorta. , 1994, Arteriosclerosis and thrombosis : a journal of vascular biology.

[75]  M. Itoh,et al.  Occludin: a novel integral membrane protein localizing at tight junctions , 1993, The Journal of cell biology.

[76]  D. L. Fry,et al.  Arterial permeability dynamics and vascular disease. , 1993, Atherosclerosis.

[77]  R. Ross,et al.  Rous-Whipple Award Lecture. Atherosclerosis: a defense mechanism gone awry. , 1993, The American journal of pathology.

[78]  P. Kubes,et al.  Inhibition of nitric oxide production. Mechanisms of vascular albumin leakage. , 1993, Circulation research.

[79]  R. Adamson,et al.  Microvascular endothelial cell shape and size in situ. , 1993, Microvascular research.

[80]  P. Davies,et al.  Mechanical stress mechanisms and the cell. An endothelial paradigm. , 1993, Circulation research.

[81]  Q. Yu,et al.  Transient disruptions of aortic endothelial cell plasma membranes. , 1992, The American journal of pathology.

[82]  M. Thubrikar,et al.  Distribution of low density lipoprotein in the branch and non-branch regions of the aorta. , 1992, Atherosclerosis.

[83]  M. Gimbrone,et al.  Vascular endothelium responds to fluid shear stress gradients. , 1992, Arteriosclerosis and thrombosis : a journal of vascular biology.

[84]  H. Granger,et al.  Flow modulates coronary venular permeability by a nitric oxide-related mechanism. , 1992, The American journal of physiology.

[85]  J. Tarbell,et al.  The effect of luminal flow in rabbit carotid artery on transmural fluid transport , 1992, Experimental physiology.

[86]  D. Blankenhorn,et al.  Arterial wall oxygenation, oxyradicals, and atherosclerosis. , 1991, Atherosclerosis.

[87]  J. Tarbell,et al.  The effect of varying albumin concentration and hydrostatic pressure on hydraulic conductivity and albumin permeability of cultured endothelial monolayers. , 1991, Microvascular research.

[88]  R M Nerem,et al.  The pathogenesis of atherosclerosis: An overview , 1991, Clinical cardiology.

[89]  P. Marynen,et al.  Molecular cloning of a phosphatidylinositol-anchored membrane heparan sulfate proteoglycan from human lung fibroblasts , 1990, The Journal of cell biology.

[90]  R M Nerem,et al.  Vascular endothelial cell proliferation in culture and the influence of flow. , 1990, Biomaterials.

[91]  G. Getz The Involvement of Lipoproteins in Atherogenesis Evolving Concepts a , 1990 .

[92]  M. Lever,et al.  Albumin and Cr-EDTA uptake by systemic arteries, veins, and pulmonary artery of rabbit. , 1990, Arteriosclerosis.

[93]  T. Carew,et al.  Initiation of atherosclerotic lesions in cholesterol-fed rabbits. II. Selective retention of LDL vs. selective increases in LDL permeability in susceptible sites of arteries. , 1989, Arteriosclerosis.

[94]  C G Caro,et al.  The effect of varying albumin concentration of the hydraulic conductivity of the rabbit common carotid artery. , 1988, Microvascular research.

[95]  R M Nerem,et al.  Influence of a laminar steady-state fluid-imposed wall shear stress on the binding, internalization, and degradation of low-density lipoproteins by cultured arterial endothelium. , 1987, Circulation.

[96]  C. Michel,et al.  Steady‐state fluid filtration at different capillary pressures in perfused frog mesenteric capillaries. , 1987, The Journal of physiology.

[97]  M. Lyon,et al.  Structure and function of heparan sulphate proteoglycans. , 1986, The Biochemical journal.

[98]  G W Moore,et al.  Distribution of the Geometric Parameters of Human Aortic Bifurcations , 1986, Arteriosclerosis.

[99]  E. Morrel,et al.  Local Variation in Arterial Wall Permeability to Low Density Lipoprotein in Normal Rabbit Aorta , 1986, Arteriosclerosis.

[100]  A. Svindland,et al.  Distribution pattern of sudanophilic plaques in the descending thoracic and proximal abdominal human aorta. , 1985, Atherosclerosis.

[101]  S. Weinbaum,et al.  Effect of cell turnover and leaky junctions on arterial macromolecular transport. , 1985, The American journal of physiology.

[102]  D. Ku,et al.  Pulsatile Flow and Atherosclerosis in the Human Carotid Bifurcation: Positive Correlation between Plaque Location and Low and Oscillating Shear Stress , 1985, Arteriosclerosis.

[103]  M. Lever,et al.  Filtration through damaged and undamaged rabbit thoracic aorta. , 1984, The American journal of physiology.

[104]  M. Gimbrone,et al.  Influence of hemodynamic forces on vascular endothelial function. In vitro studies of shear stress and pinocytosis in bovine aortic cells. , 1984, The Journal of clinical investigation.

[105]  A. Svindland,et al.  Localization of atherosclerotic lesions in the bifurcation of the main left coronary artery. , 1983, Atherosclerosis.

[106]  G. Hutchins,et al.  Arterial geometry affects hemodynamics. A potential risk factor for athersoclerosis. , 1983, Atherosclerosis.

[107]  D. Buerk,et al.  Arterial wall oxygen consumption rate varies spatially. , 1982, The American journal of physiology.

[108]  B. Fox,et al.  Location of early atheroma in the human coronary arteries. , 1981, Journal of biomechanical engineering.

[109]  C F Dewey,et al.  The dynamic response of vascular endothelial cells to fluid shear stress. , 1981, Journal of biomechanical engineering.

[110]  B L Langille,et al.  Relationship between Blood Flow Direction and Endothelial Cell Orientation at Arterial Branch Sites in Rabbits and Mice , 1981, Circulation research.

[111]  S. K. Gupta,et al.  The heat/mass transfer to a finite strip at small Péclet numbers , 1978, Journal of Fluid Mechanics.

[112]  R. Gerrity,et al.  Endothelial cell morphology in areas of in vivo Evans blue uptake in the aorta of young pigs. II. Ultrastructure of the intima in areas of differing permeability to proteins. , 1977, The American journal of pathology.

[113]  Robert M. Nerem,et al.  Transport of 14C‐4‐Cholesterol between Serum and Wall in the Perfused Dog Common Carotid Artery , 1973 .

[114]  R. Lees,et al.  Ultrafiltration of lipoproteins through a synthetic membrane. Implications for the filtration theory of atherogenesis. , 1972, The Journal of clinical investigation.

[115]  R. Schroter,et al.  Atheroma and arterial wall shear - Observation, correlation and proposal of a shear dependent mass transfer mechanism for atherogenesis , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[116]  D. L. Fry Acute Vascular Endothelial Changes Associated with Increased Blood Velocity Gradients , 1968, Circulation research.

[117]  D A Goldstein,et al.  The flow of solute and solvent across a two-membrane system. , 1963, Journal of theoretical biology.

[118]  J. Pappenheimer,et al.  Filtration, diffusion and molecular sieving through peripheral capillary membranes; a contribution to the pore theory of capillary permeability. , 1951, The American journal of physiology.

[119]  E. Starling On the Absorption of Fluids from the Connective Tissue Spaces , 1896, The Journal of physiology.

[120]  J. Tarbell,et al.  Numerical Simulation of Oxygen Mass Transfer in a Compliant Curved Tube Model of a Coronary Artery , 2004, Annals of Biomedical Engineering.

[121]  G. Thurston,et al.  Mechanics of endothelial cell architecture and vascular permeability. , 2001, Critical reviews in biomedical engineering.

[122]  J. Tarbell,et al.  Shear-induced increase in hydraulic conductivity in endothelial cells is mediated by a nitric oxide-dependent mechanism. , 2000, Arteriosclerosis, thrombosis, and vascular biology.

[123]  J. Henderson,et al.  Effect of periodic alterations in shear on vascular macromolecular uptake. , 2000, Biorheology.

[124]  Y. Taniyama,et al.  Hypoxia-induced endothelial apoptosis through nuclear factor-kappaB (NF-kappaB)-mediated bcl-2 suppression: in vivo evidence of the importance of NF-kappaB in endothelial cell regulation. , 2000, Circulation research.

[125]  M. Götte,et al.  Functions of cell surface heparan sulfate proteoglycans. , 1999, Annual review of biochemistry.

[126]  S. Chien,et al.  Effects of mechanical forces on signal transduction and gene expression in endothelial cells. , 1998, Hypertension.

[127]  H. Dvorak,et al.  Vascular permeability factor/vascular endothelial growth factor: a multifunctional angiogenic cytokine. , 1997, EXS.

[128]  Robert M. Nerem,et al.  Atherosclerosis and the Role of Wall Shear Stress , 1995 .

[129]  W D Payne,et al.  Transarterial wall oxygen gradients at the dog carotid bifurcation. , 1995, The American journal of physiology.

[130]  C. P. Winlove,et al.  Focal and regional variations in the composition of the glycocalyx of large vessel endothelium. , 1994, Journal of vascular research.

[131]  A. Baldwin,et al.  Endothelium increases medial hydraulic conductance of aorta, possibly by release of EDRF. , 1993, The American journal of physiology.

[132]  M. Shibata,et al.  Blood flow dependence of local capillary permeability of Cr-EDTA in the rabbit skeletal muscle. , 1992, The Japanese journal of physiology.

[133]  D H Blankenhorn,et al.  A definition of the intima of human arteries and of its atherosclerosis-prone regions. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. , 1992, Circulation.

[134]  H. Sinzinger,et al.  Quantitative investigation of sudanophilic lesions around the aortic ostia of human fetuses, newborn and children. , 1980, Blood vessels.

[135]  B. Zweifach,et al.  Microcirculatory basis of fluid exchange. , 1974, Advances in biological and medical physics.

[136]  Yukio Saito,et al.  A Theoretical Study on the Diffusion Current at the Stationary Electrodes of Circular and Narrow Band Types , 1968 .

[137]  A. Katchalsky,et al.  Thermodynamic analysis of the permeability of biological membranes to non-electrolytes. , 1958, Biochimica et biophysica acta.

[138]  G. Grotte Passage of dextran molecules across the blood-lymph barrier. , 1956, Acta chirurgica Scandinavica. Supplementum.