Advertisement
Research Article| Volume 32, ISSUE 2, P185-191, March 2012

Flow-Dependent Endothelial Function and Kidney Dysfunction

  • Marc-Olivier Timsit
    Affiliations
    Laboratory for Systems Biology, Center for Excellence in Vascular Biology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA
    Search for articles by this author
  • Guillermo García-Cardeña
    Correspondence
    Address reprint requests to Guillermo García-Cardeña, PhD, Department of Pathology, Harvard Medical School, 77 Ave Louis Pasteur, NRB-730C, Boston, MA 02115
    Affiliations
    Laboratory for Systems Biology, Center for Excellence in Vascular Biology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA
    Search for articles by this author

      Summary

      The vascular endothelium constantly integrates biomechanical and humoral signals and responds by secreting or metabolizing multiple factors that act in an autocrine or paracrine manner on the vasculature and adjacent tissues. Several studies have documented the effects of blood flow on renal endothelial cells and its effects on the pathophysiology of the kidney. In contrast, less is known about the effects of acute flow cessation on renal endothelium and kidney function. Here we review our current knowledge on flow cessation, endothelial function, and kidney dysfunction in the context of two clinically relevant settings, namely, the no-reflow phenomenon, observed during periods of renal warm ischemia, and the cold storage of kidney transplants.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Seminars in Nephrology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Galbraith C.G.
        • Skalak R.
        • Chien S.
        Shear stress induces spatial reorganization of the endothelial cell cytoskeleton.
        Cell Motil Cytoskeleton. 1998; 40: 317-330
        • Garcia-Cardeña G.
        • Comander J.
        • Anderson K.R.
        • Blackman B.R.
        • Gimbrone Jr, M.A.
        Biomechanical activation of vascular endothelium as a determinant of its functional phenotype.
        Proc Natl Acad Sci U S A. 2001; 98: 4478-4485
        • Davies P.F.
        Flow-mediated endothelial mechanotransduction.
        Physiol Rev. 1995; 75: 519-560
        • Davies P.F.
        Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology.
        Nat Clin Pract Cardiovasc Med. 2009; 6: 16-26
        • Lansman J.B.
        • Hallam T.J.
        • Rink T.J.
        Single stretch-activated ion channels in vascular endothelial cells as mechanotransducers?.
        Nature. 1987; 325: 811-813
        • Tzima E.
        • Irani-Tehrani M.
        • Kiosses W.B.
        • Dejana E.
        • Schultz D.A.
        • Engelhardt B.
        • et al.
        A mechanosensory complex that mediates the endothelial cell response to fluid shear stress.
        Nature. 2005; 437: 426-431
        • Khachigian L.M.
        • Resnick N.
        • Gimbrone Jr, M.A.
        • Collins T.
        Nuclear factor-kappa B interacts functionally with the platelet-derived growth factor B-chain shear-stress response element in vascular endothelial cells exposed to fluid shear stress.
        J Clin Invest. 1995; 96: 1169-1175
        • Chu T.J.
        • Peters D.G.
        Serial analysis of the vascular endothelial transcriptome under static and shear stress conditions.
        Physiol Genomics. 2008; 34: 185-192
        • Yamawaki H.
        • Pan S.
        • Lee R.T.
        • Berk B.C.
        Fluid shear stress inhibits vascular inflammation by decreasing thioredoxin-interacting protein in endothelial cells.
        J Clin Invest. 2005; 115: 733-738
        • Dayton C.
        • Yamaguchi T.
        • Warren A.
        • Korthuis R.J.
        Ischemic preconditioning prevents postischemic arteriolar, capillary, and postcapillary venular dysfunction: signaling pathways mediating the adaptive metamorphosis to a protected phenotype in preconditioned endothelium.
        Microcirculation. 2002; 9: 73-89
        • Gimbrone Jr, M.A.
        • Topper J.N.
        • Nagel T.
        • Anderson K.R.
        • Garcia-Cardeña G.
        Endothelial dysfunction, hemodynamic forces, and atherogenesis.
        Ann N Y Acad Sci. 2000; 902: 230-239
        • Chen B.P.
        • Li Y.S.
        • Zhao Y.
        • Chen K.D.
        • Li S.
        • Lao J.
        • et al.
        DNA microarray analysis of gene expression in endothelial cells in response to 24-h shear stress.
        Physiol Genomics. 2001; 7: 55-63
        • Chiu J.J.
        • Lee P.L.
        • Chang S.F.
        • Chen L.J.
        • Lee C.I.
        • Lin K.M.
        • et al.
        Shear stress regulates gene expression in vascular endothelial cells in response to tumor necrosis factor-alpha: a study of the transcription profile with complementary DNA microarray.
        J Biomed Sci. 2005; 12: 481-502
        • Dekker R.J.
        • van Soest S.
        • Fontijn R.D.
        • Salamanca S.
        • de Groot P.G.
        • VanBavel E.
        • et al.
        Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Krüppel-like factor (KLF2).
        Blood. 2002; 100: 1689-1698
        • Grabowski E.F.
        • Reininger A.J.
        • Petteruti P.G.
        • Tsukurov O.
        • Orkin R.W.
        Shear stress decreases endothelial cell tissue factor activity by augmenting secretion of tissue factor pathway inhibitor.
        Arterioscler Thromb Vasc Biol. 2001; 21: 157-162
        • McCormick S.M.
        • Eskin S.G.
        • McIntire L.V.
        • Teng C.L.
        • Lu C.M.
        • Russell C.G.
        • et al.
        DNA microarray reveals changes in gene expression of shear stressed human umbilical vein endothelial cells.
        Proc Natl Acad Sci U S A. 2001; 98: 8955-8960
        • Peters D.G.
        • Zhang X.C.
        • Benos P.V.
        • Heidrich-O'Hare E.
        • Ferrell R.E.
        Genomic analysis of immediate/early response to shear stress in human coronary artery endothelial cells.
        Physiol Genomics. 2002; 12: 25-33
        • Yamawaki H.
        • Lehoux S.
        • Berk B.C.
        Chronic physiological shear stress inhibits tumor necrosis factor-induced proinflammatory responses in rabbit aorta perfused ex vivo.
        Circulation. 2003; 108: 1619-1625
        • Parmar K.M.
        • Larman H.B.
        • Dai G.
        • Zhang Y.
        • Wang E.T.
        • Moorthy S.N.
        • et al.
        Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2.
        J Clin Invest. 2006; 116: 49-58
        • Dekker R.J.
        • Boon R.A.
        • Rondaij M.G.
        • Kragt A.
        • Volger O.L.
        • Elderkamp Y.W.
        • et al.
        KLF2 provokes a gene expression pattern that establishes functional quiescent differentiation of the endothelium.
        Blood. 2006; 107: 4354-4363
        • Berk B.C.
        Atheroprotective signaling mechanisms activated by steady laminar flow in endothelial cells.
        Circulation. 2008; 117: 1082-1089
        • Dai G.
        • Kaazempur-Mofrad M.R.
        • Natarajan S.
        • Zhang Y.
        • Vaughn S.
        • Blackman B.R.
        • et al.
        Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature.
        Proc Natl Acad Sci U S A. 2004; 101: 14871-14876
        • Anggrahini D.W.
        • Emoto N.
        • Nakayama K.
        • Widyantoro B.
        • Adiarto S.
        • Iwasa N.
        • et al.
        Vascular endothelial cell-derived endothelin-1 mediates vascular inflammation and neointima formation following blood flow cessation.
        Cardiovasc Res. 2009; 82: 143-151
        • Matharu N.M.
        • McGettrick H.M.
        • Salmon M.
        • Kissane S.
        • Vohra R.K.
        • Rainger G.E.
        • et al.
        Inflammatory responses of endothelial cells experiencing reduction in flow after conditioning by shear stress.
        J Cell Physiol. 2008; 216: 732-741
        • Milovanova T.
        • Chatterjee S.
        • Hawkins B.J.
        • Hong N.
        • Sorokina E.M.
        • Debolt K.
        • et al.
        Caveolae are an essential component of the pathway for endothelial cell signaling associated with abrupt reduction of shear stress.
        Biochim Biophys Acta. 2008; 1783: 1866-1875
        • Weight S.C.
        • Bell P.R.
        • Nicholson M.L.
        Renal ischaemia-reperfusion injury.
        Br J Surg. 1996; 83: 162-170
        • Basile D.P.
        The endothelial cell in ischemic acute kidney injury: implications for acute and chronic function.
        Kidney Int. 2007; 72: 151-156
        • Sutton T.A.
        • Fisher C.J.
        • Molitoris B.A.
        Microvascular endothelial injury and dysfunction during ischemic acute renal failure.
        Kidney Int. 2002; 62: 1539-1549
        • Yamamoto T.
        • Tada T.
        • Brodsky S.V.
        • Tanaka H.
        • Noiri E.
        • Kajiya F.
        • et al.
        Intravital videomicroscopy of peritubular capillaries in renal ischemia.
        Am J Physiol Renal Physiol. 2002; 282: 1150-1155
        • Sutton T.A.
        • Mang H.E.
        • Campos S.B.
        • Sandoval R.M.
        • Yoder M.C.
        • Molitoris B.A.
        Injury of the renal microvascular endothelium alters barrier function after ischemia.
        Am J Physiol Renal Physiol. 2003; 285: 191-198
        • Norman J.T.
        • Fine L.G.
        Intrarenal oxygenation in chronic renal failure.
        Clin Exp Pharmacol Physiol. 2006; 33: 989-996
        • Basile D.P.
        • Donohoe D.L.
        • Roethe K.
        • Mattson D.L.
        Chronic renal hypoxia after acute ischemic injury: effects of L-arginine on hypoxia and secondary damage.
        Am J Physiol Renal Physiol. 2003; 284: 338-348
        • Becherucci F.
        • Mazzinghi B.
        • Ronconi E.
        • Peired A.
        • Lazzeri E.
        • Sagrinati C.
        • et al.
        The role of endothelial progenitor cells in acute kidney injury.
        Blood Purif. 2009; 27: 261-270
        • Brodsky S.V.
        • Yamamoto T.
        • Tada T.
        • Kim B.
        • Chen J.
        • Kajiya F.
        • et al.
        Endothelial dysfunction in ischemic acute renal failure: rescue by transplanted endothelial cells.
        Am J Physiol Renal Physiol. 2002; 282: 1140-1149
        • Majno G.
        • Ames A.
        • Chaing J.
        • Wright R.L.
        No reflow after cerebral ischemia.
        Lancet. 1967; 2: 569-570
        • Kloner R.A.
        • Ganote C.E.
        • Jennings R.B.
        The “no reflow” phenomenon after temporary occlusion in the dog.
        J Clin Invest. 1974; 54: 1496-1508
        • Summers W.K.
        • Jamison R.L.
        The no reflow phenomenon in renal ischemia.
        Lab Invest. 1971; 25: 635-643
        • Flores J.
        • DiBona D.R.
        • Beck C.H.
        • Leaf A.
        The role of cell swelling in ischemic renal damage and the protective effect of hypertonic solute.
        J Clin Invest. 1972; 51: 118-126
        • Eeckhout E.
        • Kern M.J.
        The coronary no-reflow phenomenon: a review of mechanisms and therapies.
        Eur Heart J. 2001; 22: 729-739
        • Schofer J.
        • Montz R.
        • Mathey D.
        Scintigraphic evidence of the “no-reflow” phenomenon in human beings after coronary thrombolysis.
        J Am Coll Cardiol. 1985; 5: 593-598
        • Bates E.R.
        • Krell M.J.
        • Dean E.N.
        • N'Neill W.W.
        • Vogel R.A.
        Demonstration of “no reflow” phenomenon by digital coronary arteriography.
        Am J Cardiol. 1986; 57: 177-178
        • Wilson R.F.
        • Laxson D.D.
        • Lesser J.R.
        • White C.W.
        Intense microvascular constriction after angioplasty of acute thrombotic coronary arterial lesions.
        Lancet. 1989; 1: 807-811
        • Ito H.
        • Tomooka T.
        • Sakai N.
        • Yu H.
        • Higashino Y.
        • Fujii K.
        • et al.
        Lack of myocardial perfusion immediately after successful thrombolysis: a predictor of poor recovery of left ventricular function in anterior myocardial infarction.
        Circulation. 1992; 85: 1699-1705
        • Ito H.
        No-reflow phenomenon in patients with acute myocardial infarction: its pathophysiology and clinical implications.
        Acta Med Okayama. 2009; 63: 161-168
        • Fuster V.
        • Moreno P.R.
        • Fayad Z.A.
        • Corti R.
        • Badimon J.J.
        Atherothrombosis and high-risk plaque: part I: evolving concepts.
        J Am Coll Cardiol. 2005; 46: 937-954
        • Patel B.
        • Fisher M.
        Therapeutic advances in myocardial microvascular resistance: unraveling the enigma.
        Pharmacol Ther. 2010; 127: 131-147
        • Tomai F.
        • Ribichini F.
        • Ghini A.S.
        • Ferrero V.
        • Andò G.
        • Vassanelli C.
        • et al.
        Elevated C-reactive protein levels and coronary microvascular dysfunction in patients with coronary artery disease.
        Eur Heart J. 2005; 26: 2099-2105
        • Hansen P.R.
        Inflammatory alterations in the myocardial microcirculation.
        J Mol Cell Cardiol. 1998; 30: 2555-2559
        • Jerome S.N.
        • Doré M.
        • Paulson J.C.
        • Smith C.W.
        • Korthuis R.J.
        P-selectin and ICAM-1-dependant adherence reactions: role in the genesis of postischemic no-reflow.
        Am J Physiol. 1994; 266: 1316-1321
        • Bonderman D.
        • Teml A.
        • Jakowitsch J.
        • Adlbrecht C.
        • Gyongyosi M.
        • Sperker W.
        • et al.
        Coronary no-reflow is caused by shedding of active tissue factor from dissected atherosclerotic plaque.
        Blood. 2002; 99: 2794-2800
        • Eitel I.
        • Nowak M.
        • Stehl C.
        • Adams V.
        • Fuernau G.
        • Hildebrand L.
        • et al.
        Endothelin-1 release in acute myocardial infarction as a predictor of long-term prognosis and no-reflow assessed by contrast-enhanced magnetic resonance imaging.
        Am Heart J. 2010; 159: 882-890
        • Niccoli G.
        • Burzotta F.
        • Galiuto L.
        • Crea F.
        Myocardial no-reflow in humans.
        J Am Coll Cardiol. 2009; 54: 281-292
        • Schmitz V.
        • Schaser K.D.
        • Olschewski P.
        • Neuhaus P.
        • Puhl G.
        In vivo visualization of early microcirculatory changes following ischemia/reperfusion injury in human kidney transplantation.
        Eur Surg Res. 2008; 40: 19-25
        • Angelescu M.
        • Kraus T.
        • Wiesel M.
        • Hergesell O.
        • Haberkorn U.
        • Klar E.
        Assessment of renal graft function by perioperative monitoring of cortical microcirculation in kidney transplantation.
        Transplantation. 2003; 75: 1190-1196
        • Pomfret E.A.
        • Sung R.S.
        • Allan J.
        • Kinkhabwala M.
        • Melancon J.K.
        • Roberts J.P.
        Solving the organ shortage crisis: the 7th annual American Society of Transplant Surgeons' State-of-the-Art Winter Symposium.
        Am J Transplant. 2008; 8: 745-752
        • Alexander J.W.
        • Zola J.C.
        Expanding the donor pool: use of marginal donors for solid organ transplantation.
        Clin Transplant. 1996; 10: 1-19
        • Hoogland E.R.
        • Snoeijs M.G.
        • van Heurn L.W.
        DCD kidney transplantation: results and measures to improve outcome.
        Curr Opin Organ Transplant. 2010; 15: 177-182
        • Pascual J.
        • Zamora J.
        • Pirsch J.D.
        A systematic review of kidney transplantation from expanded criteria donors.
        Am J Kidney Dis. 2008; 52: 553-586
        • Schold J.D.
        • Sehgal A.R.
        • Srinivas T.R.
        • Poggio E.D.
        • Navaneethan S.D.
        • Kaplan B.
        Marked variation of the association of ESRD duration before and after wait listing on kidney transplant outcomes.
        Am J Transplant. 2010; 10: 2008-2016
        • Yuan X.
        • Theruvath A.J.
        • Ge X.
        • Floerchinger B.
        • Jurisch A.
        • Garcia-Cardeña G.
        • et al.
        Machine perfusion or cold storage in organ transplantation: indication, mechanisms, and future perspectives.
        Transpl Int. 2010; 23: 561-570
        • Massie A.B.
        • Desai N.M.
        • Montgomery R.A.
        • Singer A.L.
        • Segev D.L.
        Improving distribution efficiency of hard-to-place deceased donor kidneys: predicting probability of discard or delay.
        Am J Transplant. 2010; 10: 1613-1620
        • Maathuis M.H.
        • Leuvenink H.G.
        • Ploeg R.J.
        Perspectives in organ preservation.
        Transplantation. 2007; 83: 1289-1298
        • Opelz G.
        • Döhler B.
        Multicenter analysis of kidney preservation.
        Transplantation. 2007; 83: 247-253
        • Moers C.
        • Smits J.M.
        • Maathuis M.H.
        • Treckmann J.
        • van Gelder F.
        • Napieralski B.
        • et al.
        Machine perfusion or cold storage in deceased-donor kidney transplantation.
        N Engl J Med. 2009; 360: 7-19
        • Belzer F.O.
        • Park H.Y.
        • Vetto R.M.
        Factors influencing renal blood flow during isolated perfusion.
        Surg Forum. 1964; 15: 222-224
        • Hoffmann R.M.
        • Southard J.H.
        • Lutz M.
        • Mackety A.
        • Belzer F.O.
        Synthetic perfusate for kidney preservation.
        Arch Surg. 1983; 118: 919-921
        • Ploeg R.J.
        • Goossens D.
        • Vreugdenhil P.
        • McAnulty J.F.
        • Southard J.H.
        • Belzer F.O.
        Successful 72-hour cold storage kidney preservation with UW solution.
        Transplant Proc. 1988; 20: 935-938
        • Lee C.Y.
        • Mangino M.J.
        Preservation methods for kidney and liver.
        Organogenesis. 2009; 5: 105-112
        • Hosgood S.A.
        • Yang B.
        • Bagul A.
        • Mohamed I.H.
        • Nicholson M.L.
        A comparison of hypothermic machine perfusion versus static cold storage in an experimental model of renal ischemia reperfusion injury.
        Transplantation. 2010; 89: 830-837
        • Tullius S.
        • Garcia-Cardeña G.
        Organ procurement and perfusion before transplantation.
        N Eng J Med. 2009; 360: 78-80
        • Gracia-Sancho J.
        • Villarreal Jr, G.
        • Zhang Y.
        • Yu J.X.
        • Liu Y.
        • Tullius S.G.
        • et al.
        Flow cessation triggers endothelial dysfunction during organ cold storage conditions: strategies for pharmacologic intervention.
        Transplantation. 2010; 90: 142-149
        • Snoeijs M.G.
        • van Heurn L.W.
        • Buurman W.A.
        Biological modulation of renal ischemia-reperfusion injury.
        Curr Opin Organ Transplant. 2010; 15: 190-199
        • Matzinger P.
        The danger model: a renewed sense of self.
        Science. 2002; 296: 301-305
        • Paterson H.M.
        • Murphy T.J.
        • Purcell E.J.
        • Shelley O.
        • Kriynovich S.J.
        • Lien E.
        • et al.
        Injury primes the innate immune system for enhanced Toll-like receptor reactivity.
        J Immunol. 2003; 171: 1473-1483
        • Zhao J.L.
        • Yang Y.J.
        • Pei W.D.
        • Sun Y.H.
        • Chen J.L.
        The effect of statins on the no-reflow phenomenon: an observational study in patients with hyperglycemia before primary angioplasty.
        Am J Cardiovasc Drugs. 2009; 9: 81-89