Dietary nitrite prevents hypercholesterolemic microvascular inflammation and reverses endothelial dysfunction

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 296, Issue 5, 2009, Pages

  Stokes, Karen Y ^a   Dugas, Tammy R ^a   Tang, Yaoping ^b   Garg, Harsha ^b   Guidry, Eric ^a   Bryan, Nathan S ^b  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

C reactive protein; Leukocyte adhesion; Nitrosothiols; Tetrahydrobiopterin

Indexed keywords

C REACTIVE PROTEIN; CHOLESTEROL; DRINKING WATER; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRITE; TETRAHYDROBIOPTERIN; TRIACYLGLYCEROL;

ACUTE DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD CELL COUNT; CARDIOVASCULAR RISK; CARDITIS; CELL PROTECTION; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; CONTROLLED STUDY; DIET; ENDOTHELIAL DYSFUNCTION; HOMEOSTASIS; HYPERCHOLESTEROLEMIA; INFLAMMATION; LEUKOCYTE ADHERENCE; LEUKOCYTE MIGRATION; MALE; MEAN ARTERIAL PRESSURE; MICROANGIOPATHY; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SUPPLEMENTATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BIOPTERIN; BLOOD PRESSURE; C-REACTIVE PROTEIN; CHOLESTEROL, DIETARY; DIET; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HYPERCHOLESTEROLEMIA; INFLAMMATION; LEUKOCYTE ROLLING; LIVER; MALE; MICE; MICE, INBRED C57BL; MICROVESSELS; MYOCARDIUM; NITRIC OXIDE; SODIUM NITRITE; TRIGLYCERIDES; VASODILATION; VASODILATOR AGENTS;

EID: 66149131355     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01291.2008     Document Type: Article

References (69)

1. Anderson TJ. Nitric oxide, atherosclerosis and the clinical relevance of endothelial dysfunction. Heart Fail Rev 8: 71-86, 2003.
2. Angelo M, Singel DJ, Stamler JS. An S-nitrosothiol (SNO) synthase function of hemoglobin that utilizes nitrite as a substrate. Proc Natl Acad Sci USA 103: 8366-8371, 2006. (Pubitemid 43838461)
3. Argenbright LW, Letts LG, Rothlein R. Monoclonal antibodies to the leukocyte membrane CD18 glycoprotein complex and to intercellular adhesion molecule-1 inhibit leukocyte-endothelial adhesion in rabbits. J Leukoc Biol 49: 253-257, 1991.
4. Balkwill F, Coussens LM. Cancer: an inflammatory link. Nature 431: 405-406, 2004. (Pubitemid 39329565)
5. Binkerd EF, Kolari OE. The history and use of nitrate and nitrite in the curing of meat. Food Cosmet Toxicol 13: 665-1661, 1975.
6. Black S, Kushner I, Samols D. C-reactive protein. J Biol Chem 279: 48487-48490, 2004. (Pubitemid 39625721)
7. Bonini MG, Stadler K, Silva SO, Corbett J, Dore M, Petranka J, Fernandes DC, Tanaka LY, Duma D, Laurindo FR, Mason RP. Constitutive nitric oxide synthase activation is a significant route for nitroglycerin-mediated vasodilation. Proc Natl Acad Sci USA 105: 8569-8574, 2008.
8. Bryan NS. Nitrite in nitric oxide biology: cause or consequence? A systems-based review. Free Radic Biol Med 41: 691-701, 2006.
9. Bryan NS, Calvert JW, Elrod JW, Gundewar S, Ji SY, Lefer DJ. Dietary nitrite supplementation protects against myocardial ischemia-reperfusion injury. Proc Natl Acad Sci USA 104: 19144-19149, 2007.
10. Bryan NS, Calvert JW, Gundewar S, Lefer DJ. Dietary nitrite restores NO homeostasis and is cardioprotective in endothelial nitric oxide synthase- deficient mice. Free Radic Biol Med 45: 468-474, 2008.
11. Bryan NS, Fernandez BO, Bauer SM, Garcia-Saura MF, Milsom AB, Rassaf T, Maloney RE, Bharti A, Rodriguez J, Feelisch M. Nitrite is a signaling molecule and regulator of gene expression in mammalian tissues. Nat Chem Biol 1: 290-297, 2005.
12. Bryan NS, Rassaf T, Maloney RE, Rodriguez CM, Saijo F, Rodriguez JR, Feelisch M. Cellular targets and mechanisms of nitros(yl)ation: an insight into their nature and kinetics in vivo. Proc Natl Acad Sci USA 101: 4308-4313, 2004. (Pubitemid 38405925)
13. Bryan NS, Rassaf T, Rodriguez J, Feelisch M. Bound NO in human red blood cells: fact or artifact? Nitric Oxide 10: 221-228, 2004. (Pubitemid 38953393)
14. --mediated modification of low density lipoprotein. J Biol Chem 276: 1822-1828, 2001.
15. Cosby K, Partovi KS, Crawford JH, Patel RK, Reiter CD, Martyr S, Yang BK, Waclawiw MA, Zalos G, Xu X, Huang KT, Shields H, Kim-Shapiro DB, Schechter AN, Cannon RO 3rd, Gladwin MT. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 9: 1498-1505, 2003. (Pubitemid 38004777)
16. Craddock VM. Nitrosamines and human cancer: proof of an association? Nature 306: 638, 1983.
17. Creager MA, Gallagher SJ, Girerd XJ, Coleman SM, Dzau VJ, Cooke JP. L-Arginine improves endothelium-dependent vasodilation in hypercholesterolemic humans. J Clin Invest 90: 1248-1253, 1992.
18. Davignon J, Ganz P. Role of endothelial dysfunction in atherosclerosis. Circulation 109: III27-III32, 2004. (Pubitemid 38786440)
19. Duranski MR, Greer JJ, Dejam A, Jaganmohan S, Hogg N, Langston W, Patel RP, Yet SF, Wang X, Kevil CG, Gladwin MT, Lefer DJ. Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver. J Clin Invest 115: 1232-1240, 2005. (Pubitemid 40629041)
20. Elrod JW, Calvert JW, Gundewar S, Bryan NS, Lefer DJ. Cardiac derived nitric oxide promotes distant organ protection: evidence for an endocrine role of nitrite. In press.
21. Engler MM, Engler MB, Malloy MJ, Chiu EY, Schloetter MC, Paul SM, Stuehlinger M, Lin KY, Cooke JP, Morrow JD, Ridker PM, Rifai N, Miller E, Witztum JL, Mietus-Snyder M. Antioxidant vitamins C and E improve endothelial function in children with hyperlipidemia: Endothelial Assessment of Risk from Lipids in Youth (EARLY) Trial. Circulation 108: 1059-1063, 2003. (Pubitemid 37071514)
22. Eriksson EE. Leukocyte recruitment to atherosclerotic lesions, a complex web of dynamic cellular and molecular interactions. Curr Drug Targets 3: 309-325, 2003.
23. Eriksson EE, Xie X, Werr J, Thoren P, Lindbom L. Importance of primary capture and L-selectin-dependent secondary capture in leukocyte accumulation in inflammation and atherosclerosis in vivo. J Exp Med 194: 205-218, 2001. (Pubitemid 32673353)
24. Feelisch M, Noack E, Schroder H. Explanation of the discrepancy between the degree of organic nitrate decomposition, nitrite formation and guanylate cyclase stimulation. Eur Heart J 9, Suppl A: 57-62, 1988. (Pubitemid 18156411)
25. Fenton JI, Hursting SD, Perkins SN, Hord NG. Leptin induces an Apc genotype-associated colon epithelial cell chemokine production pattern associated with macrophage chemotaxis and activation. Carcinogenesis 28: 455-464, 2007.
26. Foster MW, McMahon TJ, Stamler JS. S-nitrosylation in health and disease. Trends Mol Med 9: 160-168, 2003.
27. Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 340: 448-454, 1999. (Pubitemid 29084777)
28. Granger DN, Kubes P. The microcirculation and inflammation: modulation of leukocyte-endothelial cell adhesion. J Leukoc Biol 55: 662-675, 1994. (Pubitemid 24171735)
29. Halcox JP, Schenke WH, Zalos G, Mincemoyer R, Prasad A, Waclawiw MA, Nour KR, Quyyumi AA. Prognostic value of coronary vascular endothelial dysfunction. Circulation 106: 653-658, 2002.
30. Hansson GK, Robertson AK, Soderberg-Naucler C. Inflammation and atherosclerosis. Annu Rev Pathol 1: 297-329, 2006.
31. Hattori Y, Hattori S, Wang X, Satoh H, Nakanishi N, Kasai K. Oral administration of tetrahydrobiopterin slows the progression of atherosclerosis in apolipoprotein E-knockout mice. Arterioscler Thromb Vasc Biol 27: 865-870, 2007. (Pubitemid 46606718)
32. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein S-nitrosylation: purview and parameters. Nat Rev 6: 150-166, 2005.
33. Houghton AN, Uchi H, Wolchok JD. The role of the immune system in early epithelial carcinogenesis: B-ware the double-edged sword. Cancer Cell 7: 403-405, 2005. (Pubitemid 40719122)
34. Jansson EA, Huang L, Malkey R, Govoni M, Nihlen C, Olsson A, Stensdotter M, Petersson J, Holm L, Weitzberg E, Lundberg JO. A mammalian functional nitrate reductase that regulates nitrite and nitric oxide homeostasis. Nat Chem Biol 4: 411-417, 2008.
35. Kaesemeyer WH, Caldwell RB, Huang J, Caldwell RW. Pravastatin sodium activates endothelial nitric oxide synthase independent of its cholesterol-lowering actions. J Am Coll Cardiol 33: 234-241, 1999. (Pubitemid 29064099)
36. Kelm M. Nitric oxide metabolism and breakdown. Biochim Biophys Acta 1411: 273-289, 1999. (Pubitemid 29221955)
37. Klatt P, Schmid M, Leopold E, Schmidt K, Werner ER, Mayer B. The pteridine binding site of brain nitric oxide synthase. Tetrahydrobiopterin binding kinetics, specificity, and allosteric interaction with the substrate domain. J Biol Chem 269: 13861-13866, 1994. (Pubitemid 24191131)
38. Lamping K, Faraci F. Enhanced vasoconstrictor responses in eNOS deficient mice. Nitric Oxide 8: 207-213, 2003. (Pubitemid 36937106)
39. Larsen FJ, Ekblom B, Sahlin K, Lundberg JO, Weitzberg E. Effects of dietary nitrate on blood pressure in healthy volunteers. N Engl J Med 355: 2792-2793, 2006. (Pubitemid 46021534)
40. Libby P, Ridker PM. Inflammation and atherosclerosis: role of C-reactive protein in risk assessment. Am J Med 116, Suppl 6A: 9S-16S, 2004. (Pubitemid 38402010)
41. Lundberg JO, Feelisch M, Bjorne H, Jansson EA, Weitzberg E. Cardioprotective effects of vegetables: is nitrate the answer? Nitric Oxide 15: 359-362, 2006. (Pubitemid 44647889)
42. Lundberg JO, Govoni M. Inorganic nitrate is a possible source for systemic generation of nitric oxide. Free Radic Biol Med 37: 395-400, 2004. (Pubitemid 38834005)
43. Lundberg JO, Weitzberg E, Cole JA, Benjamin N. Nitrate, bacteria and human health. Nat Rev Microbiol 2: 593-602, 2004. (Pubitemid 39200033)
44. Lundberg JO, Weitzberg E, Gladwin MT. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 7: 156-167, 2008.
45. Marletta MA. Nitric oxide synthase structure and mechanism. J Biol Chem 268: 12231-12234, 1993.
46. McBride P. Triglycerides and risk for coronary artery disease. Curr Atheroscler Rep 10: 386-390, 2008.
47. McKnight GM, Smith LM, Drummond RS, Duncan CW, Golden M, Benjamin N. Chemical synthesis of nitric oxide in the stomach from dietary nitrate in humans. Gut 40: 211-214, 1997. (Pubitemid 27093095)
48. Moens AL, Kass DA. Tetrahydrobiopterin and cardiovascular disease. Arterioscler Thromb Vasc Biol 26: 2439-2444, 2006.
49. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 329: 2002-2012, 1993. (Pubitemid 24015045)
50. Moncada S, Palmer RMJ, Higgs A. Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev 43: 109-142, 1991.
51. 1 Mice. Research Triangle Park, NC: National Toxicology Program (National Institutes of Health), 2001, p. 1-276.
52. Prasad R, Giri S, Nath N, Singh I, Singh AK. GSNO attenuates EAE disease by S-nitrosylation-mediated modulation of endothelial-monocyte interactions. Glia 55: 65-77, 2007.
53. Rhodes P, Leone AM, Francis PL, Struthers AD, Moncada S. The L-arginine:nitric oxide pathway is the major source of plasma nitrite in fasted humans. Biochem Biophys Res Commun 209: 590-596, 1995.
54. Ridker PM, Hennekens CH, Buring JE, Rifai N. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med 342: 836-843, 2000. (Pubitemid 30646496)
55. Ridker PM, Rifai N, Rose L, Buring JE, Cook NR. Comparison of C-reactive protein and low-density lipoprotein cholesterol levels in the prediction of first cardiovascular events. N Engl J Med 347: 1557-1565, 2002. (Pubitemid 35315836)
56. Russell J, Cooper D, Tailor A, Stokes KY, Granger DN. Low venular shear rates promote leukocyte-dependent recruitment of adherent platelets. Am J Physiol Gastrointest Liver Physiol 284: G123-G129, 2003. (Pubitemid 36076257)
57. Shahidi F, Hong C. Evaluation of malonaldehyde as a marker of oxidative rancidity in meat products. J Food Biochem 15: 97-105, 1991.
58. Shiva S, Wang X, Ringwood LA, Xu X, Yuditskaya S, Annavajjhala V, Miyajima H, Hogg N, Harris ZL, Gladwin MT. Ceruloplasmin is a NO oxidase and nitrite synthase that determines endocrine NO homeostasis. Nat Chem Biol 2: 486-493, 2006. (Pubitemid 44266311)
59. Sickert D, Aust DE, Langer S, Haupt I, Baretton GB, Dieter P. Characterization of macrophage subpopulations in colon cancer using tissue microarrays. Histopathology 46: 515-521, 2005. (Pubitemid 40632308)
60. Stokes KY, Clanton EC, Russell JM, Ross CR, Granger DN. NAD(P)H oxidase-derived superoxide mediates hypercholesterolemia-induced leukocyte- endothelial cell adhesion. Circ Res 88: 499-505, 2001.
61. Stokes KY, Cooper D, Tailor A, Granger DN. Hypercholesterolemia promotes inflammation and microvascular dysfunction: role of nitric oxide and superoxide. Free Radic Biol Med 33: 1026-1036, 2002.
62. Takahashi K, Ohyanagi M, Ikeoka K, Iwasaki T. Acetylcholine-induced response of coronary resistance arterioles in cholesterol-fed rabbits. Jpn J Pharmacol 81: 156-162, 1999. (Pubitemid 29532973)
63. Thom SR, Bhopale VM, Mancini DJ, Milovanova TN. Actin S-nitrosylation inhibits neutrophil beta2 integrin function. J Biol Chem 283: 10822-10834, 2008.
64. Tsuchiya K, Kanematsu Y, Yoshizumi M, Ohnishi H, Kirima K, Izawa Y, Shikishima M, Ishida T, Kondo S, Kagami S, Takiguchi Y, Tamaki T. Nitrite is an alternative source of NO in vivo. Am J Physiol Heart Circ Physiol 288: H2163-H2170, 2005. (Pubitemid 40604101)
65. Ward MH, deKok TM, Levallois P, Brender J, Gulis G, Nolan BT, VanDerslice J. Workgroup report: drinking-water nitrate and health-recent findings and research needs. Environ Health Perspect 113: 1607-1614, 2005.
66. Webb A, Bond R, McLean P, Uppal R, Benjamin N, Ahluwalia A. Reduction of nitrite to nitric oxide during ischemia protects against myocardial ischemia-reperfusion damage. Proc Natl Acad Sci USA 101: 13683-13688, 2004. (Pubitemid 39238463)
67. Webb AJ, Patel N, Loukogeorgakis S, Okorie M, Aboud Z, Misra S, Rashid R, Miall P, Deanfield J, Benjamin N, MacAllister R, Hobbs AJ, Ahluwalia A. Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite. Hypertension 51: 784-790, 2008.
68. Whitsett J, Picklo MJ Sr, Vasquez-Vivar J. 4-Hydroxy-2-nonenal increases superoxide anion radical in endothelial cells via stimulated GTP cyclohydrolase proteasomal degradation. Arterioscler Thromb Vasc Biol 27: 2340-2347, 2007. (Pubitemid 350203948)
69. World Cancer Research Fund/American Institute for Cancer Research. Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective. Washington, DC: American Institute for Cancer Research, 2007.