What is the mechanism of flow-mediated arterial dilatation

Clinical and Experimental Pharmacology and Physiology

Volumn 40, Issue 8, 2013, Pages 489-494

  Markos, Farouk ^a   Ruane O'Hora, Therese ^a   Noble, Mark I M ^b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Endothelial nitric oxide; Glycocalyx; Shear stress

Indexed keywords

NITRIC OXIDE SYNTHASE;

ARTERY BLOOD FLOW; ARTERY DILATATION; ARTERY DISEASE; ARTERY WALL; CYTOSKELETON; ENDOTHELIUM CELL; FLOW KINETICS; FLOW MEDIATED ARTERIAL DILATATION; GLYCOCALYX; HYPERPOLARIZATION; MECHANOTRANSDUCTION; PERIPHERAL VASCULAR SYSTEM; REVIEW; SHEAR STRESS; SMOOTH MUSCLE; VASCULAR SMOOTH MUSCLE;

EID: 84880988856     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/1440-1681.12120     Document Type: Review

References (91)

1. Snow HM, Markos F, O'Regan D, Pollock K. Characteristics of arterial wall shear stress which cause endothelium-dependent vasodilatation in the anaesthetised dog. J. Physiol. 2011; 531: 480-6.
2. Schretzenmayer A. Über Kreislaufregulatorische Vorgänge an den grossen Arterien bei der Muskelarbeit. Pflügers Arch. 1933; 232: 743-8.
3. Inoue T, Tomoike H, Hisano K, Nakamura M. Endothelium determines flow-dependent dilation of the epicardial coronary artery in dogs. J. Am. Coll. Cardiol. 1988; 11: 187-91.
4. Pohl U, Holtz J, Busse R, Bassenge E. Crucial role of endothelium in the vasodilator response to increased flow in vivo. Hypertension 1986; 8: 37-44.
5. Hull SS, Kaiser L, Jaffe MD, Sparks HV Jr. Endothelium-dependent flow-induced dilation of canine femoral and saphenous arteries. Blood Vessels 1986; 23: 183-98.
6. Muramatsu K, Numaguchi K, Egashira K, Takahashi T, Kasuya H, Takeshita A. Effects of N-nitro-l-arginine on coronary artery tone and reactive hyperemia after brief coronary occlusion in conscious dogs. Coron. Artery Dis. 1994; 5: 815-20.
7. Chu A, Chambers DE, Lin CC et al. Effects of inhibition of nitric oxide formation on basal vasomotion and endothelium-dependent responses of the coronary arteries in awake dogs. J. Clin. Invest. 1991; 87: 1964-8.
8. Kelly R, Ruane-O'Hora T, Noble MIM, Drake-Holland AJ, Snow HM. Differential inhibition by hyperglycaemia of shear stress- but not acetylcholine-mediated dilatation in the iliac artery of the anaesthetized pig. J. Physiol. 2006; 573: 133-45.
9. Kelly R, Snow HM. Characteristics of the response of the iliac artery to wall shear stress in the anaesthetised pig. J. Physiol. 2007; 562: 731-43.
10. Wang J, Wolin MS, Hintze TH. Chronic exercise enhances endothelium-mediated dilation of epicardial coronary artery in conscious dogs. Circ. Res. 1993; 73: 829-38.
11. Kelm M, Feelisch M, Deussen A, Strauer BE, Schrader J. Release of endothelium derived nitric oxide in relation to pressure and flow. Cardiovasc. Res. 1991; 25: 831-6.
12. Berdeaux A, Ghaleh B, Dubois-Rande JL et al. Role of vascular endothelium in exercise-induced dilation of large epicardial coronary arteries in conscious dogs. Circulation 1994; 89: 2799-808.
13. Hilton SM. A peripheral arterial conducting mechanism underlying dilatation of the femoral artery and concerned in functional vasodilatation in skeletal muscle. J. Physiol. 1959; 149: 93-111.
14. White CR, Frangos JA. The shear stress of it all. Cell membrane and mechanotransduction. Philos. Trans. R. Soc. London B Biol. Sci. 2007; 362: 1459-67.
15. Weinbaum S, Zhang X, Han Y, Vink H, Cowin SC. Mechanotransduction and flow across the endothelial glycocalyx. Proc. Natl Acad. Sci. USA 2003; 100: 7988-95.
16. Baersachs J, Popp R, Hecker M, Sauer E, Fleming I, Busse R. Nitric oxide attenuates the release of endothelium derived hyperpolarising factor. Circulation 1996; 94: 3341-7.
17. Sandow SL, Tare M, Coleman H, Hill C, Parkington H. Involvement of myoendothelial gap junctions in the actions of endothelium derived hyperpolarizing factor. Circ. Res. 2002; 90: 1108-13.
18. Busse R, Fleming I. Vascular endothelium and blood flow. Handb. Exp. Pharmacol. 2006; 176: 43-78.
19. De Wit C, Hoepf B, Wolfle S. Endothelial mediators and communication through vascular gap junctions. Biol. Chem. 2006; 387: 3-9.
20. Sandow S, Tare M. C-Type natriuretic peptide: A new endothelium-derived hyperpolarizing factor. Trends Pharmacol. Sci. 2007; 28: 61-7.
21. Rivers RJ. Cumulative conducted vasodilatation within a single arteriole and maximum conducted response. Am. J. Physiol. 1997; 273: H310-6.
22. Emerson G, Segal SS. Electrical coupling between endothelial cells and smooth muscle cells in hamster feed arteries; role in vasomotor control. Circ. Res. 2000; 87: 474-9.
23. Griffith TM. Endothelial control of vascular tone by nitric oxide and gap junctions: A haemodynamic perspective. Biorheology 2002; 39: 307-18.
24. Markos F, Ruane-O'Hora T, Snow HM et al. Dilatation of the femoral vascular bed does not cause retrograde relaxation of the iliac artery in the anaesthetised pig. Acta Physiol. 2008; 194: 207-13.
25. Bellien J, Iacob M, Gutierrez L et al. Crucial role of NO and endothelium-derived hyperpolarizing factor in human sustained artery flow-mediated dilation. Hypertension 2006; 48: 1088-94.
26. Behringer EJ, Segal SS. Spreading the signal for vasodilatation. Implications for skeletal muscle blood flow control and the effects of ageing. J. Physiol. 2012; 590: 6277-84.
27. Mullen MJ, Kharbanda RK, Cross J et al. Heterogenous nature of flow-mediated dilatation in human conduit arteries in vivo. Circ. Res. 2001; 88: 145-51.
28. Gunduz F, Kocer G, Ulker S, Meiselman HJ, Baskurt OK, Senturk UK. Exercise training enhances flow-mediated dilation in spontaneously hypertensive rats. Physiol. Res. 2011; 60: 589-97.
29. Rubanyi GM, Romero JC, Vanhoutte PM. Flow-induced release of endothelium-derived relaxing factor. Am. J. Physiol. Heart Circ. Physiol. 1986; 250: H1145-9.
30. Duffy SJ, Castle SF, Harper RW, Meredith IT. Contribution of vasodilator prostanoids and nitric oxide to resting flow, metabolic vasodilation, and flow-mediated dilation in human coronary circulation. Circulation 1999; 100: 1951-7.
31. Holtz J, Fostermann U, Pohl U, Gieler M, Bassenge E. Flow-dependent, endothelium-mediated dilation of epicardial coronary arteries in conscious dogs: Effects of cyclooxygenase inhibition. J. Cardiovasc. Pharmacol. 1984; 6: 1161-9.
32. Callies C, Fels J, Liashkovich I et al. Membrane potential depolarization decreases the stiffness of vascular endothelial cells. J. Cell Sci. 2012; 124: 1936-42.
33. Clough G. Relationship between microvascular permeability and ultrastructure. Prog. Biophys. Mol. Biol. 1991; 55: 47-69.
34. Vink H, Duling BR. Capillary endothelial surface layer selectively reduces plasma solute distribution volume. Am. J. Physiol. Heart Circ. Physiol. 2000; 278: H285-9.
35. Squire JM, Chew M, Nneji GN, Barry J, Michel CC. Quasi-periodic substructure in the microvessel endothelial glycocalyx: A possible explanation for molecular filtering? J. Struct. Biol. 2001; 136: 239-55.
36. Pries AR, Keubler WM. Normal endothelium. Handb. Exp. Pharmacol. 2006; 176: 1-40.
37. Van den Berg BM, Nieuwdorp M, Stroes ES, Vink H. Glycocalyx and endothelial (dys) function: From mice to men. Pharmacol. Rep. 2006; 58(Suppl.): 75-80.
38. Reitsma S, Slaaf DW, Vink H, van Zandvoort MA, oude Egbrink MG. The endothelial glycocalyx: Composition, functions and visualization. Pflügers Arch. 2007; 454: 345-59.
39. Weinbaum S, Tarbell JM, Damiano ER. The structure and function of the endothelial glycocalyx. Annu. Rev. Biomed. Eng. 2007; 9: 121-67.
40. Van Teeffelen JW, Brands J, Stroes ES, Vink H. Endothelial glycocalyx: Sweet shield of blood vessels. Trends Cardiovasc. Med. 2007; 17: 101-5.
41. Mochizuko S, Vink H, Hiramatsu O et al. Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. Am. J. Physiol. Heart Circ. Physiol. 2003; 285: H722-6.
42. Pahakis M, Kosky JR, Dull RO, Tarbell JM. The role of endothelial glycocalyx components in mechanotransduction of fluid shear stress. Biochem. Biophys. Res. Commun. 2007; 355: 228-33.
43. Ingber DE. Cellular mechanotransduction: Putting all the pieces together again. FASEB J. 2006; 20: 811-27.
44. Martinac B. Mechanosensitive ion channels: Molecules of mechanotransduction. J. Cell Sci. 2004; 117: 2449-60.
45. Aplin AE, Howe A, Alahari SK, Juliano RL. Signal transduction and signal modulation by cell adhesion receptors. The role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins. Pharmacol. Rev. 1988; 50: 197-264.
46. Yao Y, Rabodzey A, Dewey CF. Glycocalyx modulates the motility and proliferative response of vascular endothelium to fluid shear stress. Am. J. Physiol. Heart Circ. Physiol. 2007; 293: H1023-30.
47. Wang W. Change in properties of the glycocalyx affects the shear rate and stress distribution on endothelial cells. J. Biomech. Eng. 2007; 129: 324-9.
48. Liu X, Fan Y, Deng X. Mechanotransduction of flow-induced shear stress by endothelial glycocalyx fibers is torque determined. ASAIO J. 2011; 57: 487-94.
49. Feletou M. Endothelium-Dependent Hyperpolarizations The Classical 'EDHF' Pathway. The Endothelium, Part 2. Morgan, Claypool Life Sciences Publisher, Bethesda, MD. 2011.
50. Opie LH. Heart Physiology: From Cell to Circulation, 4th edn. Lippincott Williams & Williams, Philadelphia. 2004.
51. + channels. Circulation 2001; 103: 1992-8.
52. Williams SB, Goldfine AB, Timimi FK et al. Acute hyperglycemia attenuates endothelium-dependent vasodilation in humans in vivo. Circulation 1998; 97: 1695-701.
53. Kawano H, Motoyama T, Hirashima O et al. Hyperglycemia rapidly suppresses flow-mediated endothelium-dependent vasodilation of brachial artery. J. Am. Coll. Cardiol. 1999; 34: 146-54.
54. Martin H, Hu J, Gennser G, Norman M. Impaired endothelial function and increased carotid stiffness in 9-year-old children with low birthweight. Circulation 2000; 102: 2739-44.
55. Caro C, Fitz-Gerald J, Schroter R. Arterial wall shear and distribution of early atheroma in man. Nature 1969; 223: 1159-60.
56. Napoli C, Ignarro SW, de Nigris F et al. Long-term combined beneficial effects of physical training and metabolic treatment on atherosclerosis in hypercholesterolemic mice. Proc. Natl Acad. Sci. USA 2004; 101: 8797-802.
57. Ignarro LJ, Byrns RE, Buga GM, Wood KS. Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacological and chemical properties that are identical to those for nitric oxide radical. Circ. Res. 1987; 61: 866-79.
58. Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl Acad. Sci. USA 1987; 84: 9265-9.
59. Noble MIM, Drake-Holland AJ, Vink H. Hypothesis: Arterial glycocalyx dysfunction is the first step in the atherothrombotic process. Q. J. Med. 2008; 101: 513-8.
60. Shechter M, Sharir M, Labrador MJP, Forrester J, Silver B, Merz NB. Oral magnesium therapy improves endothelial function in patients with coronary artery disease. Circulation 2000; 102: 2353-8.
61. Schröder S, Enderle MD, Meisner C et al. Ultraschallmessung der Endothelfunktion der Arteria brachialis bei Verdacht auf eine koronare Herzkrankheit. Dtsch. Med. Wochenschr. 1999; 124: 886-90.
62. Schnell GB, Robertson A, Houston D, Malley L, Anderson TJ. Impaired brachial artery endothelial function is not predicted by elevated triglycerides. J. Am. Coll. Cardiol. 1999; 33: 2038-43.
63. Nagy L, Toth K, Roth E, Tarian J. Effect of transfusion on the endothelium dependent dilatation of brachial artery in patients with chronic anemia. Clin. Hemorheol. Microcirc. 1999; 20: 145-50.
64. Miyazaki H, Matsuoka H, Itabe H et al. Hemodialysis impairs endothelial function via oxidative stress. Effects of vitamin E-coated dialyzer. Circulation 2000; 101: 1002-6.
65. Lieberman EH, Gerhard MD, Uehata A et al. Flow-induced vasodilation of the human brachial artery is impaired in patients <40 years of age with coronary artery disease. Am. J. Cardiol. 1996; 78: 1210-4.
66. Levine GN, Frei B, Koulouris NA, Gerhard MD, Keaney JF Jr, Vita JA. Ascorbic acid reverses endothelial vasomotor dysfunction (brachial FMD) in patients with coronary artery disease. Circulation 1996; 93: 1107-13.
67. Leeson CPM, Whincup PH, Cook DG et al. Flow-mediated dilation in 9- to 11-year-old children. The influence of intrauterine and childhood factors. Circulation 1997; 96: 2233-8.
68. Ghiadoni L, Donald A, Cropley M et al. Mental stress induces transient endothelial dysfunction in humans. Circulation 2000; 102: 2473-8.
69. Esper RJ, Vilarino J, Cacharron JL et al. Impaired endothelial function in patients with rapidly stabilized unstable angina: Assessment by noninvasive brachial artery ultrasonography. Clin. Cardiol. 1999; 22: 699-703.
70. Celermajer DS, Adams MR, Clarkson P et al. Passive smoking and impaired endothelium-dependent arterial dilatation in healthy young adults. N. Engl. J. Med. 1996; 334: 150-4.
71. Clarkson P, Celermajer DS, Powe AJ, Donald A, Henry RMA, Deanfield J. Endothelium-dependent dilatation is impaired in young healthy subjects with a family history of premature coronary disease. Circulation 1997; 96: 3378-83.
72. Clarkson P, Montgomery HE, Mullen MJ et al. Exercise training enhances endothelial function in young men. J. Am. Coll. Cardiol. 1999; 33: 1379-85.
73. Celermajer DS, Sorensen KE, Gooch VM et al. Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 1992; 340: 1111-5.
74. Wilson RF, White CW. Intracoronary papaverine: An ideal coronary vasodilator for studies of the coronary circulation in conscious humans. Circulation 1986; 73: 444-51.
75. Treasure CB, Klein JL, Weintraub WS et al. Beneficial effects of cholesterol-lowering therapy on the coronary endothelium in patients with coronary artery disease. N. Engl. J. Med. 1995; 332: 481-7.
76. Solzbach U, Hornig B, Jeserich M, Just H. Vitamin C improves endothelial dysfunction of epicardial coronary arteries in hypertensive patients. Circulation 1997; 96: 1513-9.
77. Quyyami AA, Dakak N, Andrews NP, Gilligan DM, Panza JA, Cannon RO. Contribution of nitric oxide to metabolic coronary vasodilation in the human heart. Circulation 1995; 92: 320-6.
78. Shiode N, Morishima N, Nakayana K, Yamagata T, Matsuura H, Kajiyama G. Flow-mediated vasodilation of human epicardial coronary arteries: Effect of inhibition of nitric oxide synthesis. J. Am. Coll. Cardiol. 1996; 27: 304-10.
79. Seiler C, Hess OM, Buechi M, Sutter TM, Krayenbuehl HP. Influence of serum cholesterol and other coronary risk factors on vasomotion of angiographically normal coronary arteries. Circulation 1993; 88: 2139-48.
80. Schächinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction including depressed FMD on adverse long-term outcome of coronary heart disease. Circulation 2000; 101: 1899-906.
81. Preik M, Lauer T, Heiss C, Tabery S, Strauer BE, Kelm M. Automated ultrasonic measurement of human arteries for the determination of endothelial function. Ultraschall Med. 2000; 21: 1-5.
82. Cox DA, Vita JA, Treasure CB et al. Atherosclerosis impairs flow-mediated dilation of coronary arteries in humans. Circulation 1989; 80: 458-65.
83. Antony I, Lerebours G, Nitenberg A. Loss of flow-dependent coronary artery dilatation in patients with hypertension. Circulation 1995; 91: 1624-8.
84. Kelm M, Feelisch M, Krebber T, Deussen A, Motz W, Strauer BE. Role of nitric oxide in the regulation of coronary vascular tone in hearts from hypertensive rats: Maintenance of nitric oxide-forming capacity and increased basal production of nitric oxide. Hypertension 1995; 25: 186-93.
85. Meuwese MC, Mooij HL, Nieudorp M et al. Partial recovery of the endothelial glycocalyx upon rosuvastatin therapy in patients with heterozygous familial hypercholesterolemia. J. Lipid Res. 2009; 50: 148-53.
86. Evans M, Anderson RA, Graham J et al. Ciprofibrate therapy improves endothelial function and reduces postprandial lipemia and oxidative stress in type 2 diabetes mellitus. Circulation 2000; 101: 1773-9.
87. Gilbert SE, Tew GA, Bourke L, Winter EM, Rosario DJ. Assessment of endothelial dysfunction by flow-mediated dilatation in men on long- term androgen deprivation therapy (ADT) for prostate cancer. Exp. Physiol. 2013; Epub 10 May 2013; doi:10.1113/expphysiol. 2013.073353
88. Zeiher AM, Drexler H, Saurbier B, Just H. Endothelium-mediated coronary blood flow modulation in humans. J. Clin. Invest. 1993; 92: 652-62.
89. Anderson TJ, Elstein E, Haber H, Charbonneau F. Comparative study of ACE-inhibition, angiotensin II antagonism, and calcium channel blockade on flow-mediated vasodilation in patients with coronary disease (BANFF study). J. Am. Coll. Cardiol. 2000; 35: 60-6.
90. Gokce N, Keaney JF Jr, Frei B et al. Long-term ascorbic acid administration reverses endothelial vasomotor dysfunction in patients with coronary artery disease. Circulation 1999; 99: 3234-40.
91. Duffy S, Gokce N, Holbrook M et al. Effect of ascorbic acid treatment on conduit vessel endothelial dysfunction in patients with hypertension. Am. J. Physiol. Heart Circ. Physiol. 2001; 280: H528-34.