Nitrite-generated NO circumvents dysregulated arginine/NOS signaling to protect against intimal hyperplasia in Sprague-Dawley rats

Journal of Clinical Investigation

Volumn 121, Issue 4, 2011, Pages 1646-1656

  Alef, Matthew J ^a   Vallabhaneni, Raghuveer ^a   Carchman, Evie ^a   Morris Jr , Sidney M ^a   Shiva, Sruti ^a   Wang, Yinna ^a   Kelley, Eric E ^a   Tarpey, Margaret M ^a,b   Gladwin, Mark T ^a   Tzeng, Edith ^a,b   Zuckerbraun, Brian S ^a,b,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c NW653 MUH ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; ARGININE; CYCLIN DEPENDENT KINASE INHIBITOR 1; NITRATE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITE; NITRITE REDUCTASE; P21 ACTIVATED KINASE; SODIUM NITRATE; XANTHINE OXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOAVAILABILITY; BLOOD VESSEL INJURY; BLOOD VESSEL WALL; CELL PROLIFERATION; CONTROLLED STUDY; DIET; DIET SUPPLEMENTATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SYNTHESIS; FEMALE; HYPERPLASIA; INTIMAL HYPERPLASIA; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SMOOTH MUSCLE FIBER;

ANIMALS; ARGINASE; ARGININE; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; HYPERPLASIA; MALE; MYOCYTES, SMOOTH MUSCLE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SODIUM NITRITE; TUNICA INTIMA; XANTHINE DEHYDROGENASE;

EID: 79953328509     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI44079     Document Type: Article

References (63)

1. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362(6423):801-809. (Pubitemid 23132154)
2. Barbato JE, Tzeng E. Nitric oxide and arterial disease. J Vasc Surg. 2004;40(1):187-193. (Pubitemid 38813085)
3. Ahanchi SS, Tsihlis ND, Kibbe MR. The role of nitric oxide in the pathophysiology of intimal hyperplasia. J Vasc Surg. 2007;45(6 suppl A):A64-A73.
4. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med. 1993;329(27):2002-2012. (Pubitemid 24015045)
5. Wei LH, Wu G, Morris SM Jr, Ignarro LJ. Elevated arginase I expression in rat aortic smooth muscle cells increases cell proliferation. Proc Natl Acad Sci U S A. 2001;98(16):9260-9264. (Pubitemid 32743904)
6. Romero MJ, et al. Diabetes-induced coronary vascular dysfunction involves increased arginase activity. Circ Res. 2008;102(1):95-102.
7. Closs EI. Expression, regulation and function of carrier proteins for cationic amino acids. Curr Opin Nephrol Hypertens. 2002;11(1):99-107. (Pubitemid 34053345)
8. Peyton KJ, et al. Arginase promotes neointima formation in rat injured carotid arteries. Arterioscler Thromb Vasc Biol. 2009;29(4):488-494.
9. Blum A, et al. Oral L-arginine in patients with coronary artery disease on medical management. Circulation. 2000;101(18):2160-2164. (Pubitemid 30253044)
10. Dudek D, et al. L-arginine supplementation does not inhibit neointimal formation after coronary stenting in human beings: an intravascular ultrasound study. Am Heart J. 2004;147(1):E12.
11. Walker HA, et al. Endothelium-dependent vasodilation is independent of the plasma L-arginine/ADMA ratio in men with stable angina: lack of effect of oral L-arginine on endothelial function, oxidative stress and exercise performance. J Am Coll Cardiol. 2001;38(2):499-505. (Pubitemid 32721780)
12. Wilson AM, Harada R, Nair N, Balasubramanian N, Cooke JP. L-arginine supplementation in peripheral arterial disease: no benefit and possible harm. Circulation. 2007;116(2):188-195. (Pubitemid 47057525)
13. Boger RH. L-Arginine therapy in cardiovascular pathologies: beneficial or dangerous? Curr Opin Clin Nutr Metab Care. 2008;11(1):55-61.
14. Ansel GM, Lumsden AB. Evolving modalities for femoropopliteal interventions. J Endovasc Ther. 2009;16(1):II82-II97.
15. Griffiths MJ, Evans TW. Inhaled nitric oxide therapy in adults. N Engl J Med. 2005;353(25):2683-2695. (Pubitemid 41817717)
16. Ichinose F, Roberts JD Jr, Zapol WM. Inhaled nitric oxide: a selective pulmonary vasodilator: current uses and therapeutic potential. Circulation. 2004;109(25):3106-3111.
17. Barbato JE, Kibbe MR, Tzeng E. The emerging role of gene therapy in the treatment of cardiovascular diseases. Crit Rev Clin Lab Sci. 2003;40(5):499-545. (Pubitemid 37449502)
18. Kibbe MR, Tzeng E. Nitric oxide synthase gene therapy in vascular pathology. Semin Perinatol. 2000;24(1):51-54. (Pubitemid 30115272)
19. Matsumoto A, Momomura S, Hirata Y, Aoyagi T, Sugiura S, Omata M. Inhaled nitric oxide and exercise capacity in congestive heart failure. Lancet. 1997;349(9057):999-1000. (Pubitemid 27149811)
20. Roger N, Barbera JA, Roca J, Rovira I, Gomez FP, Rodriguez-Roisin R. Nitric oxide inhalation during exercise in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1997;156(3 pt 1):800-806. (Pubitemid 27396418)
21. Gladwin MT, et al. The emerging biology of the nitrite anion. Nat Chem Biol. 2005;1(6):308-314.
22. Lundberg JO, Weitzberg E, Gladwin MT. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov. 2008;7(2):156-167. (Pubitemid 351194063)
23. Zweier JL, Wang P, Samouilov A, Kuppusamy P. Enzyme-independent formation of nitric oxide in biological tissues. Nat Med. 1995;1(8):804-809.
24. Duncan C, et al. Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate. Nat Med. 1995;1(6):546-551.
25. Gladwin MT, et al. Nitrite as a vascular endocrine nitric oxide reservoir that contributes to hypoxic signaling, cytoprotection, and vasodilation. Am J Physiol Heart Circ Physiol. 2006;291(5):H2026-H2035.
26. Cosby K, et al. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med. 2003;9(12):1498-1505. (Pubitemid 38004777)
27. Huang Z, et al. Enzymatic function of hemoglobin as a nitrite reductase that produces NO under allosteric control. J Clin Invest. 2005;115(8):2099-2107. (Pubitemid 41134151)
28. Millar TM, Stevens CR, Benjamin N, Eisenthal R, Harrison R, Blake DR. Xanthine oxidoreductase catalyses the reduction of nitrates and nitrite to nitric oxide under hypoxic conditions. FEBS Lett. 1998;427(2):225-228. (Pubitemid 28225062)
29. Shiva S, et al. Deoxymyoglobin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration. Circ Res. 2007;100(5):654-661. (Pubitemid 46594879)
30. Shiva S, et al. Nitrite augments tolerance to ischemia/reperfusion injury via the modulation of mitochondrial electron transfer. J Exp Med. 2007;204(9):2089-2102. (Pubitemid 47360871)
31. Tripatara P, et al. Nitrite-derived nitric oxide protects the rat kidney against ischemia/reperfusion injury in vivo: role for xanthine oxidoreductase. J Am Soc Nephrol. 2007;18(2):570-580. (Pubitemid 46193322)
32. Dezfulian C, Raat N, Shiva S, Gladwin MT. Role of the anion nitrite in ischemia-reperfusion cytoprotection and therapeutics. Cardiovasc Res. 2007;75(2):327-338. (Pubitemid 46961934)
33. Duranski MR, et al. Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver. J Clin Invest. 2005;115(5):1232- 1240. (Pubitemid 40629041)
34. Hunter CJ, et al. Inhaled nebulized nitrite is a hypoxia-sensitive NO-dependent selective pulmonary vasodilator. Nat Med. 2004;10(10):1122-1127. (Pubitemid 39424875)
35. Lundberg JO, Feelisch M, Bjorne H, Jansson EA, Weitzberg E. Cardioprotective effects of vegetables: is nitrate the answer? Nitric Oxide. 2006;15(4):359-362.
36. Maeda S, et al. Moderate regular exercise increases basal production of nitric oxide in elderly women. Hypertens Res. 2004;27(12):947-953. (Pubitemid 40425397)
37. Shiva S, et al. Ceruloplasmin is a NO oxidase and nitrite synthase that determines endocrine NO homeostasis. Nat Chem Biol. 2006;2(9):486-493. (Pubitemid 44266311)
38. Larsen FJ, Ekblom B, Sahlin K, Lundberg JO, Weitzberg E. Effects of dietary nitrate on blood pressure in healthy volunteers. N Engl J Med. 2006;355(26):2792-2793. (Pubitemid 46021534)
39. Sarkar R, Gordon D, Stanley JC, Webb RC. Cell cycle effects of nitric oxide on vascular smooth muscle cells. Am J Physiol. 1997;272(4 pt 2):H1810-H1818.
40. Bauer PM, Buga GM, Ignarro LJ. Role of p42/p44 mitogen-activated-protein kinase and p21waf1/cip1 in the regulation of vascular smooth muscle cell proliferation by nitric oxide. Proc Natl Acad Sci U S A. 2001;98(22):12802- 12807. (Pubitemid 33020025)
41. Kibbe MR, et al. 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. 2000;31(6):1214-1228. (Pubitemid 30418493)
42. Zuckerbraun BS, et al. Nitric oxide-induced inhibition of smooth muscle cell proliferation involves Snitrosation and inactivation of RhoA. Am J Physiol Cell Physiol. 2007;292(2):C824-C831.
43. Zuckerbraun BS, et al. Nitrite potently inhibits hypoxic and inflammatory pulmonary arterial hypertension and smooth muscle proliferation via xanthine oxidoreductase-dependent nitric oxide generation. Circulation. 2010;121(1):98-109.
44. Shears LL, et al. Efficient inhibition of intimal hyperplasia by adenovirus-mediated inducible nitric oxide synthase gene transfer to rats and pigs in vivo. J Am Coll Surg. 1998;187(3):295-306.
45. von der Leyen HE, et al. Gene therapy inhibiting neointimal vascular lesion: in vivo transfer of endothelial cell nitric oxide synthase gene. Proc Natl Acad Sci U S A. 1995;92(4):1137-1141.
46. Webb AJ, et al. Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite. Hypertension. 2008;51(3):784-790. (Pubitemid 351301536)
47. de LM, Salen P. The Mediterranean diet: rationale and evidence for its benefit. Curr Atheroscler Rep. 2008;10(6):518-522.
48. Fung TT, Rexrode KM, Mantzoros CS, Manson JE, Willett WC, Hu FB. Mediterranean diet and incidence of and mortality from coronary heart disease and stroke in women. Circulation. 2009;119(8):1093-1100.
49. Berry CE, Hare JM. Xanthine oxidoreductase and cardiovascular disease: molecular mechanisms and pathophysiological implications. J Physiol. 2004;555(pt 3):589-606. (Pubitemid 38404582)
50. Zharikov S, et al. Uric acid decreases NO production and increases arginase activity in cultured pulmonary artery endothelial cells. Am J Physiol Cell Physiol. 2008;295(5):C1183-C1190. (Pubitemid 352790338)
51. Shears LL. Inducible nitric oxide synthase suppresses the development of allograft arteriosclerosis. J Clin Invest. 1997;100(8):2035-2042.
52. Mensinga TT, Speijers GJ, Meulenbelt J. Health implications of exposure to environmental nitrogenous compounds. Toxicol Rev. 2003;22(1):41-51. (Pubitemid 37270711)
53. Pluta RM, Dejam A, Grimes G, Gladwin MT, Oldfield EH. Nitrite infusions to prevent delayed cerebral vasospasm in a primate model of subarachnoid hemorrhage. JAMA. 2005;293(12):1477-1484. (Pubitemid 40393292)
54. National Toxicology Program. NTP technical report on the toxicology and carcinogenesis studies of sodium nitrite (cas no. 7632-00-0) in F344/N rats and B6C3F1 mice (drinking water studies). NIH publication no. 01-3954. http://www.ntp.niehs.nih.gov/ntp/htdocs/LT-rpts/tr495.pdf. Published May 2001. Accessed March 4, 2011.
55. Yu SM, Tsai SY, Guh JH, Ko FN, Teng CM, Ou JT. Mechanism of catecholamine-induced proliferation of vascular smooth muscle cells. Circulation. 1996;94(3):547-554. (Pubitemid 26266144)
56. Granada JF, et al. Single perivascular delivery of mitomycin C stimulates p21 expression and inhibits neointima formation in rat arteries. Arterioscler Thromb Vasc Biol. 2005;25(11):2343-2348. (Pubitemid 41552652)
57. Tulis DA, Durante W, Liu X, Evans AJ, Peyton KJ, Schafer AI. Adenovirus-mediated heme oxygenase-1 gene delivery inhibits injury-induced vascular neointima formation. Circulation. 2001;104(22):2710-2715. (Pubitemid 33108139)
58. Raat NJ, et al. Dietary nitrate and nitrite modulate blood and organ nitrite and the cellular ischemic stress response. Free Radic Biol Med. 2009;47(5):510-517.
59. Tzeng E, et al. Vascular gene transfer of the human inducible nitric oxide synthase: characterization of activity and effects on myointimal hyperplasia. Mol Med. 1996;2(2):211-225. (Pubitemid 26421991)
60. Zuckerbraun BS, Shapiro RA, Billiar TR, Tzeng E. RhoA influences the nuclear localization of extracellular signal-regulated kinases to modulate p21Waf/Cip1 expression. Circulation. 2003;108(7):876-881. (Pubitemid 37022132)
61. Morris SM Jr, Kepka-Lenhart D, Chen LC. Differential regulation of arginases and inducible nitric oxide synthase in murine macrophage cells. Am J Physiol. 1998;275(5 pt 1):E740-E747.
62. MacArthur PH, Shiva S, Gladwin MT. Measurement of circulating nitrite and S-nitrosothiols by reductive chemiluminescence. J Chromatogr B Analyt Technol Biomed Life Sci. 2007;851(1-2):93-105. (Pubitemid 46720142)
63. Yang BK, Vivas EX, Reiter CD, Gladwin MT. Methodologies for the sensitive and specific measurement of S-nitrosothiols, iron-nitrosyls, and nitrite in biological samples. Free Radic Res. 2003;37(1):1-10. (Pubitemid 36124324)