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Mechanism of Shear Stress-Induced Coronary Microvascular Dilation

  • Lih Kuo
  • Travis W. Hein

Abstract

In the coronary circulation, fluid shear stress acts as an important, moment-to-moment regulator of vascular resistance. Coronary microvessels display profound vasodilation to increased shear stress, a response shown to be mediated by endothelium-dependent release of nitric oxide. However, the sensory transduction mechanism and the intracellular signaling pathway by which shear stress stimulates release of nitric oxide in endothelial cells is not completely understood. In this chapter, the involvement of cytoskeleton, integrin/focal adhesion proteins, protein kinases, membrane potassium channels and calcium mobilization in endothelial activation and vasodilation to elevated shear stress is discussed. The vasomotor regulation by shear stress in the coronary microcirculation is specially emphasized.

Keywords

Nitric Oxide Fluid Shear Stress Bovine Aortic Endothelial Cell Coronary Microcirculation Myogenic Response 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Amezcua JL, Palmer RM, de Souza BM, Moncada S (1989) Nitric oxide synthesized from L-arginine regulates vascular tone in the coronary circulation of the rabbit. Br J Pharmacol 97: 1119–1124PubMedCrossRefGoogle Scholar
  2. Ando J, Ohtsuka A, Korenaga R, Kawamura T, Kamiya A (1993) Wall shear stress rather than shear rate regulates cytoplasmic Ca+ + responses to flow in vascular endothelial cells. Biochem Biophys Res Commun 190: 716–723PubMedCrossRefGoogle Scholar
  3. Ayajiki K, Kindermann M, Hecker M, Fleming I, Busse R (1996) Intracellular pH and tyrosine phosphorylation but not calcium determine shear stress-induced nitric oxide production in native endothelial cells. Circ Res 78: 750–758PubMedCrossRefGoogle Scholar
  4. Burridge K, Fath K, Kelly T, Nuckolls G, Turner C (1988) Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu Rev Cell Biol 4: 487–525PubMedCrossRefGoogle Scholar
  5. Chilian WM, Layne SM (1990) Coronary micro-vascular responses to reductions in perfusion pressure. Evidence for persistent arteriolar vasomotor tone during coronary hypoperfusion. Circ Res 66: 1227–1238PubMedCrossRefGoogle Scholar
  6. Chu A, Chambers DE, Lin C-C, Kuehl WD, Palmer RMJ, Moncada S, Cobb FR (1991) Effects of inhibition of nitric oxide formation on basal vasomotion and endothelium-dependent responses of the coronary arteries in awake dogs. J Clin Invest 87: 1964–1968PubMedCrossRefGoogle Scholar
  7. Cooke JP, Rossitch E Jr, Andon NA, Loscalzo J, Dzau VJ (1991) Flow activates an endothelial potassium channel to release an endogenous nitrovasodilator. J Clin Invest 88: 1663–1671PubMedCrossRefGoogle Scholar
  8. Corson MA, James NL, Latta SE, Nerem RM, Berk BC, Harrison DG (1996) Phosphorylation of endothelial nitric oxide synthase in response to fluid shear stress. Circ Res 79: 984–991PubMedCrossRefGoogle Scholar
  9. Davies PF, Robotewskyj A, Griem ML (1994) Quantitative studies of endothelial cell adhesion. Directional remodeling of focal adhesion sites in response to flow forces. J Clin Invest 93: 2031–2038PubMedCrossRefGoogle Scholar
  10. Davis MJ, Hill MA (1999) Signaling mechanisms underlying the vascular myogenic response. Physiol Rev 79: 387–423PubMedGoogle Scholar
  11. DeFily DV (1998) Control of microvascular resistance in physiological conditions and reperfusion. J Mol Cell Cardiol 30: 2547–2554PubMedCrossRefGoogle Scholar
  12. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601–605PubMedCrossRefGoogle Scholar
  13. Dora KA, Doyle MP, Duling BR (1997) Elevation of intracellular calcium in smooth muscle causes endothelial cell generation of NO in arterioles. Proc Natl Acad Sci USA 94: 6529–6534PubMedCrossRefGoogle Scholar
  14. Drexler H (1999) Nitric oxide and coronary endothelial dysfunction in humans. Cardiovasc Res 43: 572–579PubMedCrossRefGoogle Scholar
  15. Drexler H, Zeiher AM, Wollschläger H, Meinertz T, Just H, Bonzel T (1989) Flow-dependent coronary artery dilatation in humans. Circulation 80: 466–474.PubMedCrossRefGoogle Scholar
  16. Feigl EO (1983) Coronary Physiology. Physiol Rev 63: 1–205PubMedGoogle Scholar
  17. Fisslthaler B, Dimmeler S, Hermann C, Busse R, Fleming I (2000) Phosphorylation and activation of the endothelial nitric oxide synthase by fluid shear stress. Acta Physiol Scand 168: 81–88PubMedCrossRefGoogle Scholar
  18. Fleming I, Bauersachs J, Fisslthaler B, Busse R (1998) Ca2+-independent activation of the endothelial nitric oxide synthase in response to tyrosine phosphatase inhibitors and fluid shear stress. Circ Res 82: 686–695PubMedCrossRefGoogle Scholar
  19. Fleming I, Busse R (1999) Signal transduction of eNOS activation. Cardiovasc Res 43: 532–541PubMedCrossRefGoogle Scholar
  20. Förstermann U, Pollock JS, Schmidt HHHW, Heller M, Murad F (1991) Calmodulin-dependent endothelium-derived relaxing factor/nitric oxide synthase activity is present in the particulate and cytosolic fractions of bovine aortic endothelial cells. Proc Natl Acad Sci USA 88: 1788–1792PubMedCrossRefGoogle Scholar
  21. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC (1999) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399: 597–601PubMedCrossRefGoogle Scholar
  22. Gallis B, Corthals GL, Goodlett DR, Ueba H, Kim F, Presnell SR, Figeys D, Harrison DG, Berk BC, Aebersold R, Corson MA (1999) Identification of flow-dependent endothelial nitric-oxide synthase phosphorylation sites by mass spectrometry and regulation of phosphorylation and nitric oxide production by the phosphatidylinositol 3-kinase inhibitor LY294002. J Biol Chem 274: 30101–30108PubMedCrossRefGoogle Scholar
  23. Garcia-Cardena G, Fan R, Stern DF, Liu J, Sessa WC (1996) Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts with caveolin-1. J Biol Chem 271: 27237–27240PubMedCrossRefGoogle Scholar
  24. Geiger RV, Berk BC, Alexander RW, Nerem RM (1992) Flow-induced calcium transients in single endothelial cells: spatial and temporal analysis. Am J Physiol 262: C1411–C1417PubMedGoogle Scholar
  25. Gerova M, Gero J, Barta E, Dolezel S, Smiesko V, Levicky V (1981) Neurogenic and myogenic control of conduit coronary a.: a possible interference. Basic Res Cardiol 76: 503–507PubMedCrossRefGoogle Scholar
  26. Graier WF, Paltauf-Doburzynska J, Hill BJ, Fleischhacker E, Hoebel BG, Kostner GM, Sturek M (1998) Submaximal stimulation of porcine endothelial cells causes focal Ca2+ elevation beneath the cell membrane. J Physiol 506: 109–125PubMedCrossRefGoogle Scholar
  27. Hecker M, Mülsch A, Bassenge E, Busse R (1993) Vasoconstriction and increased flow: two principal mechanisms of shear stress-dependent endothelial autacoid release. Am J Physiol 265: H828–H833PubMedGoogle Scholar
  28. Hein TW, Belardinelli L, Kuo L (1999) Adenosine A2A receptors mediate coronary microvascular dilation to adenosine: role of nitric oxide and ATP-sensitive potassium channels. J Pharmacol Exp Ther 291: 655–664PubMedGoogle Scholar
  29. Hein TW, Kuo L (1999) cAMP-independent dilation of coronary arterioles to adenosine: role of nitric oxide, G proteins, and KATP channels. Circ Res 85: 634–642PubMedCrossRefGoogle Scholar
  30. Hein TW, Liao JC, Kuo L (2000) oxLDL specifically impairs endothelium-dependent, NO-mediated dilation of coronary arterioles. Am J Physiol 278: H175–H183Google Scholar
  31. Hintze TH, Vatner SF (1984) Reactive dilation of large coronary arteries in conscious dogs. Circ Res 54: 50–57PubMedCrossRefGoogle Scholar
  32. Holtz J, Forstermann U, Pohl U, Giesler M, Bassenge E (1984) Flow-dependent, endothelium-mediated dilation of epicardial coronary arteries in conscious dogs: effects of cyclooxygenase inhibition. J Cardiovasc Pharmacol 6: 1161–1169PubMedGoogle Scholar
  33. Hoyer J, Kohler R, Distler A (1998) Mechanosensitive Ca2+ oscillations and STOC activation in endothelial cells. FASEB J 12: 359–366PubMedGoogle Scholar
  34. Hull SS Jr, Kaiser L, Jaffe MD, Sparks HV Jr. (1986) Endothelium-dependent flow-induced dilation of canine femoral and saphenous arteries. Blood Vessels 23: 183–198PubMedGoogle Scholar
  35. Hutcheson IR, Griffith TM (1994) Heterogeneous populations of K+ channels mediate EDRF release to flow but not agonists in rabbit aorta. Am J Physiol 266: H590–H596PubMedGoogle Scholar
  36. Hutcheson IR, Griffith TM (1996) Mechanotransduction through the endothelial cytoskeleton: mediation of flow-but not agonist-induced EDRF release. Br J Pharmacol 118: 720–726PubMedCrossRefGoogle Scholar
  37. Hutcheson IR, Griffith TM (1997) Central role of intracellular calcium stores in acute flow-and agonist-evoked endothelial nitric oxide release. Br J Pharmacol 122: 117–125PubMedCrossRefGoogle Scholar
  38. Ikeda M, Kito H, Sumpio BE (1999) Phosphatidylinositol-3 kinase dependent MAP kinase activation via p2lras in endothelial cells exposed to cyclic strain. Biochem Biophys Res Commun 257: 668–671PubMedCrossRefGoogle Scholar
  39. Ishida T, Peterson TE, Kovach NL, Berk BC (1996) MAP kinase activation by flow in endothelial cells. Role of beta 1 integrins and tyrosine kinases. Circ Res 79: 310–316PubMedCrossRefGoogle Scholar
  40. Ishizaka H, Kuo L (1996) Acidosis-induced coronary arteriolar dilation is mediated by the ATP-sensitive potassium channels in vascular smooth muscle. Circ Res 78: 50–57PubMedCrossRefGoogle Scholar
  41. Ishizaka H, Kuo L (1997) Endothelial ATP-sensitive potassium channels mediate coronary microvascular dilation to hyperosmolarity. Am J Physiol 273: H104–H112PubMedGoogle Scholar
  42. Jacobs ER, Cheliakine C, Gebremedhin D, Birks EK, Davies PF, Harder DR (1995) Shear activated channels in cell-attached patches of cultured bovine aortic endothelial cells. Pflügers Arch 431: 129–131PubMedCrossRefGoogle Scholar
  43. James NL, Harrison DG, Nerem RM (1995) Effects of shear on endothelial cell calcium in the presence and absence of ATP. FASEB J 9: 968–973PubMedGoogle Scholar
  44. Jones CJ, Kuo L, Davis MJ, Chilian WM (1996) In vivo and in vitro vasoactive reactions of coronary arteriolar microvessels to nitroglycerin. Am J Physiol 271: H461–H468PubMedGoogle Scholar
  45. Jones CJH, Kuo L, Davis MJ, DeFily DV, Chilian WM (1995) Role of nitric oxide in the coronary microvascular responses to adenosine and increased metabolic demand. Circulation 91: 1807–1813PubMedCrossRefGoogle Scholar
  46. Kanatsuka H, Lamping KG, Eastham CL, Dellsperger KC, Marcus ML (1989) Comparison of the effects of increased myocardial oxygen consumption and adenosine on the coronary microvascular resistance. Circ Res 65: 1296–1305PubMedCrossRefGoogle Scholar
  47. Khwaja A, Rodriguez-Viciana P, Wennstrom S, Warne PH, Downward J (1997) Matrix adhesion and Ras transformation both activate a phosphoinositide 3-OH kinase and protein Mechanism of Flow-Induced Microvascular Dilation 211 kinase B/Akt cellular survival pathway. EMBO J 16: 2783–2793PubMedCrossRefGoogle Scholar
  48. Koller A, Kaley G (1990) Prostaglandins mediate arteriolar dilation to increased blood flow velocity in skeletal muscle microcirculation. Circ Res 67: 529–534PubMedCrossRefGoogle Scholar
  49. Korenaga R, Ando J, Tsuboi H, Yang W, Sakuma I, Toyo-oka T, Kamiya A (1994) Laminar flow stimulates ATP- and shear stress-dependent nitric oxide production in cultured bovine endothelial cells. Biochem Biophys Res Commun 198: 213–219PubMedCrossRefGoogle Scholar
  50. Kornberg L, Earp HS, Parsons JT, Schaller M, Juliano RL (1992) Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase. J Biol Chem 267: 23439–23442PubMedGoogle Scholar
  51. Kuchan MJ, Frangos JA (1994) Role of calcium and calmodulin in flow-induced nitric oxide production in endothelial cells. Am J Physiol 266: C628–C636PubMedGoogle Scholar
  52. Kuo L, Arko F, Chilian WM, Davis MJ (1993) Coronary venular responses to flow and pressure. Circ Res 72: 607–615PubMedCrossRefGoogle Scholar
  53. Kuo L, Chancellor JD (1995) Adenosine potentiates flow-induced dilation of coronary arterioles by activating KATP channels in endothelium. Am J Physiol 269: H541–H549PubMedGoogle Scholar
  54. Kuo L, Chilian WM, Davis MJ (1990a) Coronary arteriolar myogenic response is independent of endothelium. Circ Res 66: 860–866PubMedCrossRefGoogle Scholar
  55. Kuo L, Chilian WM, Davis MJ (1991) Interaction of pressure-and flow-induced responses in porcine coronary resistance vessels. Am J Physiol 261: H1706–H1715PubMedGoogle Scholar
  56. Kuo L, Davis MJ, Cannon MS, Chilian WM (1992) Pathophysiological consequences of atherosclerosis extend into the coronary microcirculation. Restoration of endothelium-dependent responses by L-arginine. Circ Res 70: 465–476PubMedCrossRefGoogle Scholar
  57. Kuo L, Davis MJ, Chilian WM (1990b) Endothelium-dependent, flow-induced dilation of isolated coronary arterioles. Am J Physiol 259: H1063–H1070PubMedGoogle Scholar
  58. Kuo L, Davis MJ, Chilian WM (1995) Longitudinal gradient for endothelium-dependent and -independent vascular responses in the coronary microcirculation. Circulation 92: 518–525PubMedCrossRefGoogle Scholar
  59. Lamping KG, Dole WP (1988) Flow-mediated dilation attenuates constriction of large coronary arteries to serotonin. Am J Physiol 255: H1317–H1324PubMedGoogle Scholar
  60. Leavesley DI, Schwartz MA, Rosenfeld M, Cheresh DA (1993) Integrin beta 1- and beta 3-mediated endothelial cell migration is trig-gered through distinct signaling mechanisms. J Cell Biol 121: 163–170PubMedCrossRefGoogle Scholar
  61. Liao JC, Kuo L (1997) Interaction between adenosine and flow-induced dilation in coronary microvascular network. Am J Physiol 272: H1571–H1581PubMedGoogle Scholar
  62. Lie M, Sejersted OM, Kiil F (1970) Local regulation of vascular cross section during changes in femoral arterial blood flow in dogs. Circ Res 27: 727–737PubMedCrossRefGoogle Scholar
  63. Ling S, Woronuk G, Sy L, Lev S, Braun AP (2000) Enhanced activity of a large conductance, calcium-sensitive K+ channel in the presence of Src tyrosine kinase. J Biol Chem 275: 30683–30689PubMedCrossRefGoogle Scholar
  64. Lückhoff A, Busse R (1990a) Activators of potassium channels enhance calcium influx into endothelial cells as a consequence of potassium currents. Naunyn-Schmiedeberg’s Arch Pharmacol 342: 94–99CrossRefGoogle Scholar
  65. Lückhoff A, Busse R (1990b) Calcium influx into endothelial cells and formation of endothelium-derived relaxing factor is controlled by the membrane potential. Pflügers Arch 416: 305–311PubMedCrossRefGoogle Scholar
  66. Maniotis AJ, Chen CS, Ingber DE (1997) Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci USA 94: 849–854PubMedCrossRefGoogle Scholar
  67. McCabe TJ, Fulton D, Roman LJ, Sessa WC (2000) Enhanced electron flux and reduced calmodulin dissociation may explain “calcium-independent” eNOS activation by phosphorylation. J Biol Chem 275: 6123–6128PubMedCrossRefGoogle Scholar
  68. Miura H, Wachtel RE, Liu Y, Loberiza FR Jr., Saito T, Miura M, Gutterman DD (2001) Flow-induced dilation of human coronary arterioles: important role of Cat+-activated K+ channels. Circulation 103: 1992–1998PubMedCrossRefGoogle Scholar
  69. Muller JM, Chilian WM, Davis MJ (1997) Integrin signaling transduces shear stress-dependent vasodilation of coronary arterioles. Circ Res 80: 320–326PubMedCrossRefGoogle Scholar
  70. Muller JM, Davis MJ, Chilian WM (1996) Coronary arteriolar flow-induced vasodilation signals through tyrosine kinase. Am J Physiol 270: H1878–H1884PubMedGoogle Scholar
  71. Muller JM, Davis MJ, Kuo L, Chilian WM (1999) Changes in coronary endothelial cell Ca2+ concentration during shear stress-and agonist-induced vasodilation. Am J Physiol 276: H1706–H1714PubMedGoogle Scholar
  72. Nakache M, Gaub HE (1988) Hydrodynamic hyperpolarization of endothelial cells. Proc Natl Acad Sci USA 85: 1841–1843PubMedCrossRefGoogle Scholar
  73. Naruse K, Sokabe M (1993) Involvement of stretch-activated ion channels in Ca2+ mobilization to mechanical stretch in endothelial cells. Am J Physiol 264: C1037–C1044PubMedGoogle Scholar
  74. Ohno M, Gibbons GH, Dzau VJ, Cooke JP (1993) Shear stress elevates endothelial cGMP. Role of a potassium channel and G protein coupling. Circulation 88: 193–197PubMedCrossRefGoogle Scholar
  75. Olesen S-P, Clapham DE, Davies PF (1988) Haemodynamic shear stress activates a K+ current in vascular endothelial cells. Nature 331: 168–170PubMedCrossRefGoogle Scholar
  76. Paltauf-Doburzynska J, Posch K, Paltauf G, Graier WF (1998) Stealth ryanodine-sensitive Ca2 + release contributes to activity of capacitative Ca2+ entry and nitric oxide synthase in bovine endothelial cells. J Physiol 513: 369–379PubMedCrossRefGoogle Scholar
  77. Pohl U, Holtz J, Busse R, Bassenge E (1986) Crucial role of endothelium in the vasodilator response to increased flow in vivo. Hypertension 8: 37–44PubMedCrossRefGoogle Scholar
  78. Pohl U, Lamontagne D, Bassenge E, Busse R (1994) Attenuation of coronary autoregulation in the isolated rabbit heart by endothelium derived nitric oxide. Cardiovasc Res 28: 414–419PubMedCrossRefGoogle Scholar
  79. Prevarskaya NB, Skryma RN, Vacher P, Daniel N, Djiane J, Dufy B (1995) Role of tyrosine phosphorylation in potassium channel activation. Functional association with prolactin receptor and JAK2 tyrosine kinase. J Biol Chem 270: 24292–24299PubMedCrossRefGoogle Scholar
  80. Schretzenmayr A (1933) Über Kreislaufregulatorische Vorgänge an den groben Arterien bei der Muskelarbeit. Pflügers Arch 232: 743–748CrossRefGoogle Scholar
  81. Schwartz MA (1993) Spreading of human endothelial cells on fibronectin or vitronectin triggers elevation of intracellular free calcium. J Cell Biol 120: 1003–1010PubMedCrossRefGoogle Scholar
  82. Schwarz G, Droogmans G, Nilius B (1992) Shear stress induced membrane currents and calcium transients in human vascular endothelial cells. Pflügers Arch 421: 394–396PubMedCrossRefGoogle Scholar
  83. Shaul PW, Anderson RG (1998) Role of plasmalemmal caveolae in signal transduction. Am J Physiol 275: L843–L851PubMedGoogle Scholar
  84. Shen J, Luscinskas FW, Connolly A, Dewey CF Jr., Gimbrone MA Jr. (1992) Fluid shear stress modulates cytosolic free calcium in vascular endothelial cells. Am J Physiol 262: C384–C390Google Scholar
  85. Takahashi M, Berk BC (1996) Mitogen-activated protein kinase (ERK1/2) activation by shear stress and adhesion in endothelial cells. Essential role for a herbimycin-sensitive kinase J Clin Invest 98: 2623–2631Google Scholar
  86. Vinten-Johansen J, Zhao ZQ, Nakamura M, Jordan JE, Ronson RS, Thourani VH, Guyton RA (1999) Nitric oxide and the vascular endothelium in myocardial ischemia-reperfusion injury. Ann N Y Acad Sci 874: 354–370PubMedCrossRefGoogle Scholar
  87. Wellman GC, Bevan JA (1995) Barium inhibits the endothelium-dependent component of flow but not acetylcholine-induced relaxation in isolated rabbit cerebral arteries. J Pharmacol Exp Ther 274: 47–53PubMedGoogle Scholar
  88. Xie H, Bevan JA (1998) Barium and 4-aminopyridine inhibit flow-initiated endothelium-independent relaxation. J Vasc Res 35: 428–436PubMedCrossRefGoogle Scholar

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© Springer-Verlag Wien 2003

Authors and Affiliations

  • Lih Kuo
  • Travis W. Hein

There are no affiliations available

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