Insights into the effect of nitric oxide and its metabolites nitrite and nitrate at inhibiting neointimal hyperplasia

Nitric Oxide - Biology and Chemistry

Volumn 25, Issue 1, 2011, Pages 22-30

  Vavra, Ashley K ^a   Havelka, George E ^a   Martinez, Janet ^a   Lee, Vanessa R ^a   Fu, Bo ^a   Jiang, Qun ^a   Keefer, Larry K ^b   Kibbe, Melina R ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Neointimal hyperplasia; Nitric oxide; Nitrite nitrate; Peripheral vascular disease

Indexed keywords

CD45 ANTIGEN; DIAZENIUMDIOLATE DISODIUM 1 [2 (CARBOXYLATO)PYRROLIDIN 1 YL]DIAZEN 1 IUM1,2 DIOLATE; NITRATE; NITRIC OXIDE; NITRIC OXIDE DONOR; NITRITE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTERY INJURY; ARTICLE; BLOOD PRESSURE; BLOOD VESSEL WALL; CAROTID ARTERY; CELL DEATH; CELL INFILTRATION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFICACY; HALF LIFE TIME; HEART RATE; HYPOTENSION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MALE; NEOINTIMA; NEOINTIMAL HYPERPLASIA; NONHUMAN; PRIORITY JOURNAL; RAT; VASCULAR SMOOTH MUSCLE;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CORONARY ARTERY DISEASE; DISEASE MODELS, ANIMAL; HYPERPLASIA; MALE; NEOINTIMA; NITRATES; NITRIC OXIDE; NITRITES; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 79958193814     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2011.04.013     Document Type: Article

References (39)

1. A.T. Hirsch, Z.J. Haskal, N.R. Hertzer, C.W. Bakal, M.A. Creager, J.L. Halperin, L.F. Hiratzka, W.R. Murphy, J.W. Olin, J.B. Puschett, K.A. Rosenfield, D. Sacks, J.C. Stanley, L.M. Taylor Jr., C.J. White, J. White, R.A. White, E.M. Antman, S.C. Smith Jr., C.D. Adams, J.L. Anderson, D.P. Faxon, V. Fuster, R.J. Gibbons, J.L. Halperin, L.F. Hiratzka, S.A. Hunt, A.K. Jacobs, R. Nishimura, J.P. Ornato, R.L. Page, B. Riegel, ACC/AHA 2005 guidelines for the management of patients with peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic): executive summary a collaborative report from the American Association for Vascular Surgery/Society for Vascular Surgery, Society for Cardiovascular Angiography and Interventions, Society for Vascular Medicine and Biology, Society of Interventional Radiology, and the ACC/AHA Task Force on Practice Guidelines (Writing Committee to Develop Guidelines for the Management of Patients With Peripheral Arterial Disease) endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation; National Heart, Lung, and Blood Institute; Society for Vascular Nursing; TransAtlantic Inter-Society Consensus; and Vascular Disease Foundation, J. Am. Coll. Cardiol. 47 (2006) 1239-1312.
2. C.G. Pearce, S.F. Najjar, M.R. Kapadia, J. Murar, J. Eng, B. Lyle, O.O. Aalami, Q. Jiang, J.A. Hrabie, J.E. Saavedra, L.K. Keefer, M.R. Kibbe, Beneficial effect of a short-acting NO donor for the prevention of neointimal hyperplasia, Free Radic. Biol. Med. 44 (2008) 73-81. (Pubitemid 350138632)
3. K.S. Masters, E.A. Lipke, E.E. Rice, M.S. Liel, H.A. Myler, C. Zygourakis, D.A. Tulis, J.L. West, Nitric oxide-generating hydrogels inhibit neointima formation, J. Biomater. Sci. Polym. Ed. 16 (2005) 659-672. (Pubitemid 41348797)
4. M.R. Kapadia, L.W. Chow, N.D. Tsihlis, S.S. Ahanchi, J.W. Eng, J. Murar, J. Martinez, D.A. Popowich, Q. Jiang, J.A. Hrabie, J.E. Saavedra, L.K. Keefer, J.F. Hulvat, S.I. Stupp, M.R. Kibbe, Nitric oxide and nanotechnology: a novel approach to inhibit neointimal hyperplasia, J. Vasc. Surg. 47 (2008) 173-182.
5. G.J. Fulton, M.G. Davies, L. Barber, J.L. Gray, E. Svendsen, P.O. Hagen, Local effects of nitric oxide supplementation and suppression in the development of intimal hyperplasia in experimental vein grafts, Eur. J. Vasc. Endovasc. Surg. 15 (1998) 279-289. (Pubitemid 28205985)
6. S. Kaul, B. Cercek, J. Rengstrom, X.P. Xu, M.D. Molloy, P. Dimayuga, A.K. Parikh, M.C. Fishbein, J. Nilsson, T.B. Rajavashisth, P.K. Shah, Polymeric-based perivascular delivery of a nitric oxide donor inhibits intimal thickening after balloon denudation arterial injury: role of nuclear factor-kappaB, J. Am. Coll. Cardiol. 35 (2000) 493-501. (Pubitemid 30125544)
7. A. Chaux, X.M. Ruan, M.C. Fishbein, Y. Ouyang, S. Kaul, J.A. Pass, J.M. Matloff, Perivascular delivery of a nitric oxide donor inhibits neointimal hyperplasia in vein grafts implanted in the arterial circulation, J. Thorac. Cardiovasc. Surg. 115 (1998) 604-612.
8. J.A. Hrabie, L.K. Keefer, Chemistry of the nitric oxide-releasing diazeniumdiolate (''nitrosohydroxylamine'') functional group and its oxygen-substituted derivatives, Chem. Rev. 102 (2002) 1135-1154.
9. A. Dejam, C.J. Hunter, C. Tremonti, R.M. Pluta, Y.Y. Hon, G. Grimes, K. Partovi, M.M. Pelletier, E.H. Oldfield, R.O. Cannon III, A.N. Schechter, M.T. Gladwin, Nitrite infusion in humans and nonhuman primates: endocrine effects, pharmacokinetics, and tolerance formation, Circulation 116 (2007) 1821-1831.
10. B.S. Zuckerbraun, S. Shiva, E. Ifedigbo, M.A. Mathier, K.P. Mollen, J. Rao, P.M. Bauer, J.J. Choi, E. Curtis, A.M. Choi, M.T. Gladwin, Nitrite potently inhibits hypoxic and inflammatory pulmonary arterial hypertension and smooth muscle proliferation via xanthine oxidoreductase-dependent nitric oxide generation, Circulation 121 (2010) 98-109.
11. J.O. Lundberg, E. Weitzberg, M.T. Gladwin, The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics, Nat. Rev. Drug Discov. 7 (2008) 156-167. (Pubitemid 351194063)
12. L.K. Keefer, Progress toward clinical application of the nitric oxide-releasing diazeniumdiolates, Annu. Rev. Pharmacol. Toxicol. 43 (2003) 585-607. (Pubitemid 37372654)
13. Y.S. Nan, G.G. Feng, Y. Hotta, K. Nishiwaki, Y. Shimada, A. Ishikawa, N. Kurimoto, T. Shigei, N. Ishikawa, Neuropeptide Y enhances permeability across a rat aortic endothelial cell monolayer, Am. J. Physiol. Heart Circ. Physiol. 286 (2004) H1027-H1033. (Pubitemid 38248618)
14. 2+ signalling, Pflugers Arch. 438 (1999) 612-620.
15. Y. Ding, N.D. Vaziri, Calcium channel blockade enhances nitric oxide synthase expression by cultured endothelial cells, Hypertension 32 (1998) 718-723. (Pubitemid 28480550)
16. H. Li, A. Samouilov, X. Liu, J.L. Zweier, Characterization of the magnitude and kinetics of xanthine oxidase-catalyzed nitrite reduction. Evaluation of its role in nitric oxide generation in anoxic tissues, J. Biol. Chem. 276 (2001) 24482-24489.
17. E.A. Jansson, L. Huang, R. Malkey, M. Govoni, C. Nihlen, A. Olsson, M. Stensdotter, J. Petersson, L. Holm, E. Weitzberg, J.O. Lundberg, A mammalian functional nitrate reductase that regulates nitrite and nitric oxide homeostasis, Nat. Chem. Biol. 4 (2008) 411-417. (Pubitemid 351860549)
18. C. Duncan, H. Dougall, P. Johnston, S. Green, R. Brogan, C. Leifert, L. Smith, M. Golden, N. Benjamin, Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate, Nat. Med. 1 (1995) 546-551.
19. J.L. Zweier, P. Wang, A. Samouilov, P. Kuppusamy, Enzyme-independent formation of nitric oxide in biological tissues, Nat. Med. 1 (1995) 804-809.
20. Z. Huang, S. Shiva, D.B. Kim-Shapiro, R.P. Patel, L.A. Ringwood, C.E. Irby, K.T. Huang, C. Ho, N. Hogg, A.N. Schechter, M.T. Gladwin, Enzymatic function of hemoglobin as a nitrite reductase that produces NO under allosteric control, J. Clin. Invest. 115 (2005) 2099-2107.
21. T.M. Millar, C.R. Stevens, D.R. Blake, Xanthine oxidase can generate nitric oxide from nitrate in ischaemia, Biochem. Soc. Trans. 25 (1997) 528S.
22. B.L. Godber, J.J. Doel, G.P. Sapkota, D.R. Blake, C.R. Stevens, R. Eisenthal, R. Harrison, Reduction of nitrite to nitric oxide catalyzed by xanthine oxidoreductase, J. Biol. Chem. 275 (2000) 7757-7763.
23. Z. Chen, J. Zhang, J.S. Stamler, Identification of the enzymatic mechanism of nitroglycerin bioactivation, Proc. Natl. Acad. Sci. USA 99 (2002) 8306-8311. (Pubitemid 34651048)
24. K. Cosby, K.S. Partovi, J.H. Crawford, R.P. Patel, C.D. Reiter, S. Martyr, B.K. Yang, M.A. Waclawiw, G. Zalos, X. Xu, K.T. Huang, H. Shields, D.B. Kim-Shapiro, A.N. Schechter, R.O. Cannon III, M.T. Gladwin, Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation, Nat. Med. 9 (2003) 1498-1505.
25. F.J. Larsen, B. Ekblom, K. Sahlin, J.O. Lundberg, E. Weitzberg, Effects of dietary nitrate on blood pressure in healthy volunteers, N. Engl. J. Med. 355 (2006) 2792-2793. (Pubitemid 46021534)
26. A. Modin, H. Bjorne, M. Herulf, K. Alving, E. Weitzberg, J.O. Lundberg, Nitrite-derived nitric oxide: a possible mediator of 'acidic-metabolic' vasodilation, Acta Physiol. Scand. 171 (2001) 9-16.
27. K.H. Jung, K. Chu, S.Y. Ko, S.T. Lee, D.I. Sinn, D.K. Park, J.M. Kim, E.C. Song, M. Kim, J.K. Roh, Early intravenous infusion of sodium nitrite protects brain against in vivo ischemia-reperfusion injury, Stroke 37 (2006) 2744-2750. (Pubitemid 44922536)
28. A. Webb, R. Bond, P. McLean, R. Uppal, N. Benjamin, A. Ahluwalia, Reduction of nitrite to nitric oxide during ischemia protects against myocardial ischemia-reperfusion damage, Proc. Natl. Acad. Sci. USA 101 (2004) 13683-13688. (Pubitemid 39238463)
29. N.S. Bryan, B.O. Fernandez, S.M. Bauer, M.F. Garcia-Saura, A.B. Milsom, T. Rassaf, R.E. Maloney, A. Bharti, J. Rodriguez, M. Feelisch, Nitrite is a signaling molecule and regulator of gene expression in mammalian tissues, Nat. Chem. Biol. 1 (2005) 290-297.
30. M.R. Kibbe, J. Li, S. Nie, S.C. Watkins, A. Lizonova, I. Kovesdi, R.L. Simmons, T.R. Billiar, E. Tzeng, Inducible nitric oxide synthase (iNOS) expression upregulates p21 and inhibits vascular smooth muscle cell proliferation through p42/44 mitogen-activated protein kinase activation and independent of p53 and cyclic guanosine monophosphate, J. Vasc. Surg. 31 (2000) 1214-1228.
31. M.R. Kibbe, S. Nie, D.W. Seol, I. Kovesdi, A. Lizonova, M. Makaroun, T.R. Billiar, E. Tzeng, Nitric oxide prevents p21 degradation with the ubiquitin-proteasome pathway in vascular smooth muscle cells, J. Vasc. Surg. 31 (2000) 364-374.
32. M. Feelisch, B.O. Fernandez, N.S. Bryan, M.F. Garcia-Saura, S. Bauer, D.R. Whitlock, P.C. Ford, D.R. Janero, J. Rodriguez, H. Ashrafian, Tissue processing of nitrite in hypoxia: an intricate interplay of nitric oxide-generating and -scavenging systems, J. Biol. Chem. 283 (2008) 33927-33934.
33. M.G. Davies, P.O. Hagen, Pathobiology of intimal hyperplasia, Br. J. Surg. 81 (1994) 1254-1269.
34. P. Libby, D. Schwartz, E. Brogi, H. Tanaka, S.K. Clinton, A cascade model for restenosis. A special case of atherosclerosis progression, Circulation 86 (1992) III47-III52.
35. M.R. Kibbe, E. Tzeng, S.L. Gleixner, S.C. Watkins, I. Kovesdi, A. Lizonova, M.S. Makaroun, T.R. Billiar, R.Y. Rhee, Adenovirus-mediated gene transfer of human inducible nitric oxide synthase in porcine vein grafts inhibits intimal hyperplasia, J. Vasc. Surg. 34 (2001) 156-165.
36. K.Y. Stokes, T.R. Dugas, Y. Tang, H. Garg, E. Guidry, N.S. Bryan, Dietary nitrite prevents hypercholesterolemic microvascular inflammation and reverses endothelial dysfunction, Am. J. Physiol. Heart Circ. Physiol. 296 (2009) H1281-H1288.
37. S.S. Ahanchi, V.N. Varu, N.D. Tsihlis, J. Martinez, C.G. Pearce, M.R. Kapadia, Q. Jiang, J.E. Saavedra, L.K. Keefer, J.A. Hrabie, M.R. Kibbe, Heightened efficacy of nitric oxide-based therapies in type II diabetes mellitus and metabolic syndrome, Am. J. Physiol. Heart Circ. Physiol. 295 (2008) H2388-H2398.
38. V.N. Varu, S.S. Ahanchi, M.E. Hogg, H.A. Bhikhapurwala, A. Chen, D.A. Popowich, A.K. Vavra, J. Martinez, Q. Jiang, J.E. Saavedra, J.A. Hrabie, L.K. Keefer, M.R. Kibbe, Insulin enhances the effect of nitric oxide at inhibiting neointimal hyperplasia in a rat model of type 1 diabetes, Am. J. Physiol. Heart Circ. Physiol. 299 (2010) H772-H779.
39. M.E. Hogg, V.N. Varu, A.K. Vavra, D.A. Popowich, M.N. Banerjee, J. Martinez, Q. Jiang, J.E. Saavedra, L.K. Keefer, M.R. Kibbe, Effect of nitric oxide on neointimal hyperplasia based on sex and hormone status, Free Radic. Biol. Med. 50 (2011) 1065-1074.