Does vitamin C enhance nitric oxide bioavailability in a tetrahydrobiopterin-dependent manner? in vitro, in vivo and clinical studies

Nitric Oxide - Biology and Chemistry

Volumn 36, Issue , 2014, Pages 51-57

  Mortensen, Alan ^a   Lykkesfeldt, Jens ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Ascorbate; Dihydrobiopterin; Nitric oxide bioavailability; Tetrahydrobiopterin

Indexed keywords

ASCORBIC ACID; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; TETRAHYDROBIOPTERIN;

AORTA; BIOAVAILABILITY; CELL FUNCTION; CLINICAL STUDY; ENDOTHELIUM CELL; GUINEA PIG MODEL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOUSE MODEL; MUSCLE; NITROSYLATION; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RAT MODEL; REVIEW;

ASCORBATE; DIHYDROBIOPTERIN; NITRIC OXIDE BIOAVAILABILITY; TETRAHYDROBIOPTERIN;

ANIMALS; ASCORBIC ACID; BIOLOGICAL MARKERS; BIOPTERIN; CARDIOVASCULAR DISEASES; GUINEA PIGS; HUMANS; MICE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; NITROGEN; OXYGEN; PHOSPHORYLATION; RATS; REACTIVE OXYGEN SPECIES; RISK; VASODILATION;

EID: 84891789062     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2013.12.001     Document Type: Review

References (61)

1. E.R. Werner, N. Blau, and B. Thöny Tetrahydrobiopterin: biochemistry and pathophysiology Biochem. J. 438 2011 397 414
2. J. Vasquez-Vivar Tetrahydrobiopterin, superoxide, and vascular dysfunction Free Radic. Biol. Med. 47 2009 1108 1119
3. A. Mortensen, and J. Lykkesfeldt Kinetics of acid-induced degradation of tetra- and dihydrobiopterin in relation to their relevance as biomarkers of endothelial function Biomarkers 18 2013 55 62
4. M.J. Crabtree, C.L. Smith, G. Lam, M.S. Goligorsky, and S.S. Gross Ratio of 5,6,7,8-tetrahydrobiopterin to 7,8-dihydrobiopterin in endothelial cells determines glucose-elicited changes in NO vs. superoxide production by eNOS Am. J. Physiol. Heart Circ. Physiol. 294 2008 H1530 H1540
5. A. Presta, U. Siddhanta, C. Wu, N. Sennequier, L. Huang, H.M. Abu-Soud, S. Erzurum, and D.J. Stuehr Comparative functioning of dihydro- and tetrahydropterins in supporting electron transfer, catalysis, and subunit dimerization in inducible nitric oxide synthase Biochemistry 37 1998 298 310
6. J. Vásquez-Vivar, P. Martásek, J. Whitsett, J. Joseph, and B. Kalyanaraman The ratio between tetrahydrobiopterin and oxidized tetrahydrobiopterin analogues controls superoxide release from endothelial nitric oxide synthase: an EPR spin trapping study Biochem. J. 362 2002 733 739
7. N. Kuzkaya, N. Weissmann, D.G. Harrison, and S. Dikalov Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols J. Biol. Chem. 278 2003 22546 22554
8. K.B. Patel, M.R.L. Stratford, P. Wardman, and S.A. Everett Oxidation of tetrahydrobiopterin by biological radicals and scavenging of the trihydrobiopterin radical by ascorbate Free Radic. Biol. Med. 32 2002 203 211
9. J. Lykkesfeldt, M. Viscovich, and H.E. Poulsen Ascorbic acid recycling in human erythrocytes is induced by smoking in vivo Free Radic. Biol. Med. 35 2003 1439 1447
10. B. Frei, I. Birlouez-Aragon, and J. Lykkesfeldt What is the optimum intake of vitamin C in humans? Crit. Rev. Food Sci. Nutr. 52 2012 815 829
11. M. Takeda, T. Yamashita, M. Shinohara, N. Sasaki, T. Takaya, K. Nakajima, N. Inoue, T. Masano, H. Tawa, S. Satomi-Kobayashi, R. Toh, D. Sugiyama, K. Nishimura, M. Yokoyama, K.i. Hirata, and S. Kawashima Plasma tetrahydrobiopterin/dihydrobiopterin ratio: a possible marker of endothelial dysfunction Circ. J. 73 2009 955 962
12. K. Noguchi, N. Hamadate, T. Matsuzaki, M. Sakanashi, J. Nakasone, T. Uchida, K. Arakaki, H. Kubota, S. Ishiuchi, H. Masuzaki, K. Sugahara, Y. Ohya, M. Sakanashi, and M. Tsutsui Increasing dihydrobiopterin causes dysfunction of endothelial nitric oxide synthase in rats in vivo Am. J. Physiol. Heart Circ. Physiol. 301 2011 H721 H729
13. M.V. Tsapenko, L.V. d'Uscio, J.P. Grande, A.J. Croatt, M.C. Hernandez, A.W. Ackerman, Z.S. Katusic, and K.A. Nath Increased production of superoxide anion contributes to dysfunction of the arteriovenous fistula Am. J. Physiol. Renal Physiol. 303 2012 F1601 F1607
14. L.V. d'Uscio, S. Milstien, D. Richardson, L. Smith, and Z.S. Katusic Long-term vitamin C treatment increases vascular tetrahydrobiopterin levels and nitric oxide synthase activity Circ. Res. 92 2003 88 95
15. S. Kar, and M. Kavdia Modeling of biopterin-dependent pathways of eNOS for nitric oxide and superoxide production Free Radic. Biol. Med. 51 2011 1411 1427
16. D.W. Howells, and K. Hyland Direct analysis of tetrahydrobiopterin in cerebrospinal fluid by high-performance liquid chromatography with redox electrochemistry: prevention of autoxidation during storage and analysis Clin. Chim. Acta 167 1987 23 30
17. J. Vásquez-Vivar, J. Whitsett, P. Martásek, N. Hogg, and B. Kalyanaraman Reaction of tetrahydrobiopterin with superoxide: EPR-kinetic analysis and characterization of the pteridine radical Free Radic. Biol. Med. 31 2001 975 985
18. M. Tóth, Z. Kukor, and S. Valent Chemical stabilization of tetrahydrobiopterin by l-ascorbic acid: contribution to placental endothelial nitric oxide synthase activity Mol. Hum. Reprod. 8 2002 271 280
19. S. Valent, and M. Toth Spectrophotometric analysis of the protective effect of ascorbate against spontaneous oxidation of tetrahydrobiopterin in aqueous solution: kinetic characteristics and potentiation by catalase of ascorbate action Int. J. Biochem. Cell Biol. 36 2004 1266 1280
20. R. Heller, A. Unbehaun, B. Schellenberg, B. Mayer, G. Werner-Felmayer, and E.R. Werner l-Ascorbic acid potentiates endothelial nitric oxide synthesis via a chemical stabilization of tetrahydrobiopterin J. Biol. Chem. 276 2001 40 47
21. S. Valent, and M. Tóth Activation energy determinations suggest that thiols reverse autooxidation of tetrahydrobiopterin by a different mechanism than ascorbate Int. J. Biochem. Cell Biol. 38 2006 1786 1793
22. C.C. Wei, Z.Q. Wang, J. Tejero, Y.P. Yang, C. Hemann, R. Hille, and D.J. Stuehr Catalytic reduction of a tetrahydrobiopterin radical within nitric-oxide synthase J. Biol. Chem. 283 2008 11734 11742
23. N. Gotoh, and E. Niki Rates of interactions of superoxide with vitamin E, vitamin C and related compounds as measured by chemiluminescence Biochim. Biophys. Acta 1115 1992 201 207
24. R.E. Huie, and S. Padmaja The reaction of NO with superoxide Free Radic. Res. Commun. 18 1993 195 199
25. 2 - a pulse-radiolysis study Free Radic. Biol. Med. 19 1995 505 510
26. K. Kobayashi, M. Miki, and S. Tagawa Pulse-radiolysis study of the reaction of nitric oxide with superoxide J. Chem. Soc., Dalton Trans. 1995 2885 2889
27. J. Whitsett, M.J. Picklo Sr., and J. Vasquez-Vivar 4-Hydroxy-2-nonenal increases superoxide anion radical in endothelial cells via stimulated gtp cyclohydrolase proteasomal degradation Arterioscler. Thromb. Vasc. Biol. 27 2007 2340 2347
28. A. Huang, J.A. Vita, R.C. Venema, and J.F. Keaney Ascorbic acid enhances endothelial nitric-oxide synthase activity by increasing intracellular tetrahydrobiopterin J. Biol. Chem. 275 2000 17399 17406
29. E. Alexandra, K. Ström, and I.A. Cotgreave The uptake of ascorbic acid into human umbilical vein endothelial cells and its effect on oxidant insult Biochem. Pharmacol. 50 1995 1339 1346
30. A. Martin, and B. Frei Both intracellular and extracellular vitamin C inhibit atherogenic modification of ldl by human vascular endothelial cells Arterioscler. Thromb. Vasc. Biol. 17 1997 1583 1590
31. K.A. Best, M.E. Holmes, S.E. Samson, J. Mwanjewe, J.X. Wilson, S.J. Dixon, and A.K. Grover Ascorbate uptake in pig coronary artery endothelial cells Mol. Cell. Biochem. 271 2005 43 49
32. H. Hofmann, and H.H.H.W. Schmidt Thiol dependence of nitric oxide synthase Biochemistry 34 1995 13443 13452
33. R. Heller, F. Münscher-Paulig, R. Gräbner, and U. Till l-Ascorbic acid potentiates nitric oxide synthesis in endothelial cells J. Biol. Chem. 274 1999 8254 8260
34. P. Sharma, S.A.V. Raghavan, and M. Dikshit Role of ascorbate in the regulation of nitric oxide generation by polymorphonuclear leukocytes Biochem. Biophys. Res. Commun. 309 2003 12 17
35. T.A. Baker, S. Milstien, and Z.S. Katusic Effect of vitamin C on the availability of tetrahydrobiopterin in human endothelial cells J. Cardiovasc. Pharmacol. 37 2001 333 338
36. A. Ladurner, C.A. Schmitt, D. Schachner, A.G. Atanasov, E.R. Werner, V.M. Dirsch, and E.H. Heiss Ascorbate stimulates endothelial nitric oxide synthase enzyme activity by rapid modulation of its phosphorylation status Free Radic. Biol. Med. 52 2012 2082 2090
37. M. Chatterjee, R. Saluja, V. Kumar, A. Jyoti, G. Kumar, M. Jain, M. Kumar Barthwal, and Dikshit Ascorbate sustains neutrophil NOS expression, catalysis, and oxidative burst Free Radic. Biol. Med. 45 2008 1084 1093
38. K. Nakai, M. Urushihara, Y. Kubota, and H. Kosaka Ascorbate enhances iNOS activity by increasing tetrahydrobiopterin in RAW 264.7 cells Free Radic. Biol. Med. 35 2003 929 937
39. H.J. Kim, S.I. Lee, D.H. Lee, D. Smith, H. Jo, H.E. Schellhorn, and Y.C. Boo Ascorbic acid synthesis due to l-gulono-1,4-lactone oxidase expression enhances NO production in endothelial cells Biochem. Biophys. Res. Commun. 345 2006 1657 1662
40. P.A. Erwin, A.J. Lin, D.E. Golan, and T. Michel Receptor-regulated dynamic S-nitrosylation of endothelial nitric-oxide synthase in vascular endothelial cells J. Biol. Chem. 280 2005 19888 19894
41. A. Mizutani, H. Maki, Y. Torii, K. Hitomi, and N. Tsukagoshi Ascorbate-dependent enhancement of nitric oxide formation in activated macrophages Nitric Oxide 2 1998 235 241
42. K.C. McKenna, K.M. Beatty, R.C. Scherder, F. Li, H. Liu, A.F. Chen, A. Ghosh, and D.J. Stuehr Ascorbate in aqueous humor augments nitric oxide production by macrophages J. Immunol. 190 2013 556 564
43. B.M. Mitchell, A.M. Dorrance, A. Ergul, and R.C. Webb Sepiapterin decreases vasorelaxation in nitric oxide synthase inhibition-induced hypertension J. Cardiovasc. Pharmacol. 43 2004 93 98
44. J. Yan, G. Tie, and L.M. Messina Tetrahydrobiopterin, l-arginine and vitamin C act synergistically to decrease oxidative stress, increase nitric oxide and improve blood flow after induction of hind limb ischemia in the rat (vol 18, pg 1221, 2012) Mol. Med. 18 2012 1221 1230
45. T. Okazaki, H. Otani, T. Shimazu, K. Yoshioka, M. Fujita, and T. Iwasaka Ascorbic acid and N-acetyl cysteine prevent uncoupling of nitric oxide synthase and increase tolerance to ischemia/reperfusion injury in diabetic rat heart Free Radic. Res. 45 2011 1173 1183
46. K. Izumi, R.G. Cassens, and M.L. Greaser Reaction of nitrite with ascorbic acid and its significant role in nitrite-cured food Meat Sci. 26 1989 141 153
47. J.O. Lundberg, and E. Weitzberg Nitrite reduction to nitric oxide in the vasculature Am. J. Physiol. Heart Circ. Physiol. 295 2008 H477 H478
48. H. Frikke-Schmidt, and J. Lykkesfeldt Role of marginal vitamin C deficiency in atherogenesis. In vivo models and clinical studies Basic Clin. Pharmacol. Toxicol. 104 2009 419 433
49. P. Tveden-Nyborg, S. Hasselholt, N. Miyashita, T. Moos, H.E. Poulsen, and J. Lykkesfeldt Chronic vitamin C deficiency does not accelerate oxidative stress in ageing brains of guinea pigs Basic Clin. Pharmacol. Toxicol. 110 2012 524 529
50. A. Mortensen, S. Hasselholt, P. Tveden-Nyborg, and J. Lykkesfeldt Ascorbate status predicts tetrahydrobiopterin plasma concentration and oxidation ratio in vivo Nutr. Res. 33 2013 859 867
51. T. Takaya, K.i. Hirata, T. Yamashita, M. Shinohara, N. Sasaki, N. Inoue, T. Yada, M. Goto, A. Fukatsu, T. Hayashi, N.J. Alp, K.M. Channon, M. Yokoyama, and S. Kawashima A specific role for eNOS-derived reactive oxygen species in atherosclerosis progression Arterioscler. Thromb. Vasc. Biol. 27 2007 1632 1637
52. P. Tveden-Nyborg, J. Lykkesfeldt, Does vitamin C deficiency Increase lifestyle-associated vascular disease progression? Evidence based on experimental and clinical studies, Antioxid. Redox Sign.
53. M. Porkert, S. Sher, U. Reddy, F. Cheema, C. Niessner, P. Kolm, D.P. Jones, C. Hooper, W.R. Taylor, D. Harrison, and A.A. Quyyumi Tetrahydrobiopterin: a novel antihypertensive therapy J. Hum. Hypertens. 22 2008 401 407
54. F. Mittermayer, J. Pleiner, G. Schaller, S. Zorn, K. Namiranian, S. Kapiotis, G. Bartel, M. Wolfrum, M. Brügel, J. Thiery, R.J. MacAllister, and M. Wolzt Tetrahydrobiopterin corrects Escherichia coli endotoxin-induced endothelial dysfunction Am. J. Physiol. Heart Circ. Physiol. 289 2005 H1752 H1757
55. T. Heitzer, C. Brockhoff, B. Mayer, A. Warnholtz, H. Mollnau, S. Henne, T. Meinertz, and T. Münzel Tetrahydrobiopterin improves endothelium-dependent vasodilation in chronic smokers: evidence for a dysfunctional nitric oxide synthase Circ. Res. 86 2000 e36 e41
56. J. Lykkesfeldt, and H.E. Poulsen Is vitamin C supplementation beneficial? lessons learned from randomised controlled trials Br. J. Nutr. 103 2010 1251 1259
57. W.J. Blot, J.Y. Li, P.R. Taylor, W. Guo, S. Dawsey, G.Q. Wang, C.S. Yang, S.F. Zheng, M. Gail, G.Y. Li, Y. Yu, B.q. Liu, J. Tangrea, Y.h. Sun, F. Liu, J.F. Fraumeni, Y.H. Zhang, and B. Li Nutrition intervention trials in Linxian, China: supplementation with specific vitamin/mineral combinations, cancer incidence, and disease-specific mortality in the general population J. Natl. Cancer I 85 1993 1483 1491
58. N.R. Cook, C.M. Albert, J.M. Gaziano, E. Zaharris, J. MacFadyen, E. Danielson, J.E. Buring, and J.E. Manson A randomized factorial trial of vitamins C and E and beta carotene in the secondary prevention of cardiovascular events in women: results from the women's antioxidant cardiovascular study Arch. Intern. Med. 167 2007 1610 1618
59. Heart Protection Study Collaborative Group MRC/BHF heart protection study of antioxidant vitamin supplementation in 20536 high-risk individuals: a randomised placebo-controlled trial Lancet 360 2002 23 33
60. S. Hercberg, P. Galan, P. Preziosi, S. Bertrais, L. Mennen, D. Malvy, A.-M. Roussel, A. Favier, and S. Briançon The SU.VI.MAX study: A randomized, placebo-controlled trial of the health effects of antioxidant vitamins and minerals Arch. Intern. Med. 164 2004 2335 2342
61. H.D. Sesso, J.E. Buring, W.G. Christen, T. Kurth, C. Belanger, J. MacFadyen, V. Bubes, J.E. Manson, R.J. Glynn, and J.M. Gaziano Vitamins E and C in the prevention of cardiovascular disease in men: the physicians' health study II randomized controlled trial JAMA 300 2008 2123 2133