Vitamin C prevents the acute decline of flow-mediated dilation after altered shear rate patterns

Applied Physiology, Nutrition and Metabolism

Volumn 38, Issue 3, 2013, Pages 268-274

  Johnson, Blair D ^a   Mather, Kieren J ^b   Newcomer, Sean C ^c   Mickleborough, Timothy D ^a   Wallace, Janet P ^a  

^a INDIANA UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

Antegrade shear; Endothelium; Oscillatory; Oxidative stress; Retrograde shear

Indexed keywords

ASCORBIC ACID;

BRACHIAL ARTERY; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; HUMAN; RANDOMIZED CONTROLLED TRIAL; VASCULAR ENDOTHELIUM; VASODILATATION;

ASCORBIC ACID; BRACHIAL ARTERY; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; ENDOTHELIUM, VASCULAR; HUMANS; VASODILATION;

EID: 84875587486     PISSN: 17155312     EISSN: 17155320     Source Type: Journal    
DOI: 10.1139/apnm-2012-0169     Document Type: Article

References (43)

1. American College of Sports Medicine. 2006. ACSM's guidelines for exercise testing and prescription. Lippencott, Williams & Wilkins, Philadelphia, Penn., USA.
2. Anderson, R.A., Evans, L.M., Ellis, G.R., Kahn, N., Morris, K., Jackson, S.K., et al. 2006. Prolonged deterioration of endothelial dysfunction in response to postprandial lipaemia is attenuated by vitamin C in type 2 diabetes. Diabet. Med. 23: 258-264. doi:10.1111/j.1464-5491.2005.01767.x. PMID:16492208.
3. Black, M.A., Cable, N.T., Thijssen, D.H.J., and Green, D.J. 2008. Importance of measuring the time course of flow-mediated dilation in humans. Hypertension, 51: 203-210. doi:10.1161/HYPERTENSIONAHA.107.101014. PMID:18086954.
4. Chappell, D.C., Varner, S.E., Nerem, R.M., Medford, R.M., and Alexander, R.W. 1998. Oscillatory shear stress stimulates adhesion molecule expression in cultured human endothelium. Circ. Res. 82(5): 532-539. doi:10.1161/01.RES. 82.5.532. PMID:9529157.
5. DeKeulenaer, G.W., Chappell, D.C., Ishizaka, N., Nerem, R.M., Alexander, R.W., and Griendling, K.K. 1998. Oscillatory and steady laminar shear stress differentially affect human endothelial redox state: Role of a superoxide-producing NADH oxidase. Circ. Res. 82(10): 1094-1101. doi:10.1161/01.RES. 82.10.1094. PMID:9622162.
6. Fisslthaler, B., Michaelis, U.R., Randriamboavonjy, V., Busse, R., and Fleming, I. 2003. Cytochrome p450 epoxygenases and vascular tone: Novel role for HMGCoA reductase inhibitors in the regulation of CYP 2C expression. Biochim. Biophys. Acta, 1619(3): 332-339. doi:10.1016/S0304-4165(02)00492-0. PMID: 12573493.
7. Förstermann, U. 2010. Nitric oxide and oxidative stress in vascular disease. Pflügers Arch. 459(6): 923-939. doi:10.1007/s00424-010-0808-2. PMID: 20306272.
8. Harris, R.A., Padilla, J., Hanlon, K.P., Rink, L.D., and Wallace, J.P. 2008. The flow-mediated dilation response to acute exercise in overweight active and inactive men. Obes. Res. 16: 578-584. doi:10.1038/oby.2007.87.
9. Harris, R., Nishiyama, S., Wray, D., Tedjasaputra, V., Bailey, D., and Richardson, R. 2009. The effect of oral antioxidants on brachial artery flowmediated dilation following 5 and 10 min of ischemia. Eur. J. Appl. Physiol. 107(4): 445-453. doi:10.1007/s00421-009-1147-x. PMID:19669786.
10. Hsiai, T.K., Cho, S.K., Wong, P.A.K.K., Ing, M., Salazar, A., Sevanian, A., et al. 2003. Monocyte recruitment to endothelial cells in response to oscillatory shear stress. FASEB J. 17(12): 1648. doi:10.1096/fj.02-1064com. PMID:12958171.
11. Huang, A., Vita, J.A., Venema, R.C., and Keaney, J.F. 2000. Ascorbic acid enhances endothelialnitric-oxidesynthaseactivitybyincreasingintracellulartetrahydrobiopterin. J. Biol. Chem. 275(23): 17399-17406. doi:10.1074/jbc. M002248200. PMID:10749876.
12. Hwang, J., Ing, M.H., Salazar, A., Lassegue, B., Griendling, K., Navab, M., et al. 2003. Pulsatile versus oscillatory shear stress regulates NADPH oxidase subunit expression: Implication for native LDL oxidation. Circ. Res. 93(12): 1225-1232. doi:10.1161/01.RES.0000104087.29395.66. PMID:14593003.
13. Johnson, B.D., Padilla, J., Harris, R.A., and Wallace, J.P. 2011. Vascular consequences of a high-fat meal in physically active and inactive adults. Appl. Physiol. Nutr. Metab. 36(3): 368-375. doi:10.1139/h11-028. PMID:21574775.
14. Johnson, B.D., Padilla, J., and Wallace, J.P. 2012. The exercise dose affects oxidative stress and brachial artery flow-mediated dilation in trained men. Eur. J. Appl. Physiol. 112(1): 33-42. doi:10.1007/s00421-011-1946-8. PMID:21472439.
15. Kizhakekuttu, T.J., Gutterman, D.D., Phillips, S.A., Jurva, J.W., Arthur, E.I.L., Das, E., et al. 2010. Measuring FMD in the brachial artery: How important is QRS gating? J. Appl. Physiol. 109(4): 959-965. doi:10.1152/japplphysiol.00532. 2010. PMID:20671033.
16. Krasnoff, J.B., Vintro, A.Q., Ascher, N.L., Bass, N.M., Dodd, M.J., and Painter, P.L. 2005. Objective measures of health-related quality of life over 24 months post-liver transplantation. Clin. Transplant. 19(1): 1-9. doi:10.1111/j.1399-0012. 2004.00306.x. PMID:15659126.
17. Kuzkaya, N., Weissmann, N., Harrison, D.G., and Dikalov, S. 2003. Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols. J. Biol. Chem. 278(25): 22546. doi:10.1074/jbc.M302227200. PMID:12692136.
18. Landmesser, U., Dikalov, S., Price, S.R., McCann, L., Fukai, T., Holland, S.M., et al. 2003. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J. Clin. Invest. 111(8): 1201-1209. doi:10.1172/JCI200314172, 10.1172/JCI14172. PMID:12697739.
19. Laursen, J.B., Somers, M., Kurz, S., McCann, L., Warnholtz, A., Freeman, B.A., et al. 2001. Endothelial regulation of vasomotion in apoE-deficient mice: implications for interactions between peroxynitrite and tetrahydrobiopterin. Circulation, 103(9): 1282. doi:10.1161/01.CIR.103.9.1282. PMID: 11238274.
20. Levine, M., Conry-Cantilena, C., Wang, Y., Welch, R., Washko, P., Dhariwal, K., et al. 1996. Vitamin C pharmacokinetics in healthy volunteers: evidence for a recommended dietary allowance. Proc. Natl. Acad. Sci. U.S.A. 93(8): 3704. doi:10.1073/pnas.93.8.3704. PMID:8623000.
21. Li, Y.-S.J., Haga, J.H., and Chien, S. 2005. Molecular basis of the effects of shear stress on vascular endothelial cells. J. Biomech. 38(10): 1949-1971. doi:10.1016/ j.jbiomech.2004.09.030. PMID:16084198.
22. May, J.M., Qu, Z.-C., and Li, X. 2003. Ascorbic acid blunts oxidant stress due to menadione in endothelial cells. Arch. Biochem. Biophys. 411(1): 136-144. doi: 10.1016/S0003-9861(02)00715-4. PMID:12590932.
23. McNally, J.S., Davis, M.E., Giddens, D.P., Saha, A., Hwang, J., Dikalov, S., et al. 2003. Role of xanthine oxidoreductase and NAD(P)H oxidase in endothelial superoxide production in response to oscillatory shear stress. Am. J. Physiol. Heart Circ. Physiol. 285(6): H2290-H2297. PMID:12958034.
24. Newcomer, S.C., Sauder, C.L., Kuipers, N.T., Laughlin, M.H., and Ray, C.A. 2008. Effects of posture on shear rates in human brachial and superficial femoral arteries. Am. J. Physiol. Heart Circ. Physiol. 294(4): H1833-H1839. doi:10.1152/ ajpheart.01108.2007. PMID:18245564.
25. Nishikimi, M. 1975. Oxidation of ascorbic acid with superoxide anion generated by the xanthine-xanthine oxidase system. Biochem. Biophys. Res. Commun. 63(2): 463-468. doi:10.1016/0006-291X(75)90710-X. PMID:235924.
26. Padayatty, S.J., Sun, H., Wang, Y., Riordan, H.D., Hewitt, S.M., Katz, A., et al. 2004. Vitamin C pharmacokinetics: Implications for oral and intravenous use. Ann. Intern. Med. 140(7): 533-537. PMID:15068981.
27. Padilla, J., Johnson, B.D., Newcomer, S.C., Wilhite, D.P., Mickleborough, T.D., Fly, A.D., et al. 2008. Normalization of flow-mediated dilation to shear stress area under the curve eliminates the impact of variable hyperemic stimulus. Cardiovasc. Ultrasound, 6: 44-54. doi:10.1186/1476-7120-6-44. PMID:18771594.
28. Padilla, J., Johnson, B.D., Newcomer, S.C., Wilhite, D.P., Mickleborough, T.D., Fly, A.D., et al. 2009a. Adjusting flow-mediated dilation for shear stress stimulus allows demonstration of endothelial dysfunction in a population with moderate cardiovascular risk. J. Vasc. Res. 46: 592-600. doi:10.1159/ 000226227. PMID:19571579.
29. Padilla, J., Sheldon, R.D., Sitar, D.M., and Newcomer, S.C. 2009b. Impact of acute exposure to increased hydrostatic pressure and reduced shear rate on conduit artery endothelial function: A limb-specific response. Am. J. Physiol. Heart Circ. Physiol. 297(3): H1103-H1108. doi:10.1152/ajpheart.00167.2009. PMID:19633210.
30. Padilla, J., Young, C.N., Simmons, G.H., Deo, S.H., Newcomer, S.C., Sullivan, J.P., et al. 2010. Increased muscle sympathetic nerve activity acutely alters conduit artery shear rate patterns. Am. J. Physiol. Heart Circ. Physiol. 298(4): H1128-H1135. doi:10.1152/ajpheart.01133.2009. PMID:20154260.
31. Potter, K., Reed, C., Green, D., Hankey, G., and Arnolda, L. 2008. Ultrasound settings significantly alter arterial lumen and wall thickness measurements. Cardiovasc. Ultrasound, 6(1): 6. doi:10.1186/1476-7120-6-6. PMID:18208623.
32. Pyke, K.E., and Tschakovsky, M.E. 2007. Peak vs. Total reactive hyperemia: which determines the magnitude of flow-mediated dilation? J. Appl. Physiol. 102: 1510-1519. doi:10.1152/japplphysiol.01024.2006. PMID:17170205.
33. Ross, R. 1999. Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 340: 115-128. doi:10.1056/NEJM199901143400207. PMID:9887164.
34. Silvestro, A., Scopacasa, F., Oliva, G., de, Cristofaro, T., Iuliano, L., and Brevetti, G. 2002. Vitamin C prevents endothelial dysfunction induced by acute exercise in patients with intermittent claudication. Atherosclerosis, 165(2): 277-283. doi:10.1016/S0021-9150(02)00235-6. PMID:12417278.
35. Smith, A.R., Visioli, F., and Hagen, T.M. 2002. Vitamin C matters: Increased oxidative stress in cultured human aortic endothelial cells without supplemental ascorbic acid. FASEB J. 10.1096/fj.01-0825fje. 12039848.
36. Takabe, W., Jen, N., Ai, L., Hamilton, R., Wang, S., Holmes, K., et al. 2011. Oscillatory shear stress induces mitochondrial superoxide production: Implication of NADPH oxidase and c-Jun NH2-terminal kinase signaling. Antioxid. Redox Signal. 15(5): 1379-1388. doi:10.1089/ars.2010.3645. PMID:20919940.
37. Thijssen, D.H.J., Dawson, E.A., Tinken, T.M., Cable, N.T., and Green, D.J. 2009. Retrograde flow and shear rate acutely impair endothelial function in humans. Hypertension, 53(6): 986-992. doi:10.1161/HYPERTENSIONAHA.109. 131508. PMID:19380611.
38. Thijssen, D.H.J., Black, M.A., Pyke, K.E., Padilla, J., Atkinson, G., Harris, R.A., et al. 2011. Assessment of flow mediated dilation in humans: a methodological and physiological guideline. Am. J. Physiol. Heart Circ. Physiol. 300(1): H2-H12. doi:10.1152/ajpheart.00471.2010. PMID:20952670.
39. Tinken, T.M., Thijssen, D.H.J., Hopkins, N., Black, M.A., Dawson, E.A., Minson, C.T., et al. 2009. Impact of shear rate modulation on vascular function in humans. Hypertension, 54(2): 278-285. doi:10.1161/HYPERTENSIONAHA. 109.134361. PMID:19546374.
40. Tinken, T.M., Thijssen, D.H.J., Hopkins, N., Dawson, E.A., Cable, N.T., and Green, D.J. 2010. Shear stress mediates endothelial adaptations to exercise training in humans. Hypertension, 55(2): 312-318. doi:10.1161/HYPERTENSIONAHA. 109.146282. PMID:20048193.
41. Valkonen, M., and Kuusi, T. 2000. Vitamin C prevents the acute atherogenic effects of passive smoking. Free Radic. Biol. Med. 28(3): 428-436. doi:10.1016/ S0891-5849(99)00260-9. PMID:10699755.
42. Wu, S.P., Ringgaard, S., Oyre, S., Hansen, M.S., Rasmus, S., and Pedersen, E.M. 2004. Wall shear rates differ between the normal carotid, femoral, and brachial arteries: an in vivo MRI study. J. Magn. Reson. Imaging, 19(2): 188-193. doi:10.1002/jmri.10441. PMID:14745752.
43. Ziegler, T., Bouzourene, K., Harrison, V.J., Brunner, H.R., and Hayoz, D. 1998. Influence of oscillatory and unidirectional flow environments on the expression of endothelin and nitric oxide synthase in cultured endothelial cells. Arterioscler. Thromb. Vasc. Biol. 18(5): 686-692. doi:10.1161/01.ATV.18.5.686. PMID:9598825.