Oral nitrite circumvents antiseptic mouthwash-induced disruption of enterosalivary circuit of nitrate and promotes nitrosation and blood pressure lowering effect

Free Radical Biology and Medicine

Volumn 101, Issue , 2016, Pages 226-235

  Pinheiro, Lucas C ^a   Ferreira, Graziele C ^a   Amaral, Jefferson H ^a   Portella, Rafael L ^a   Tella, Sandra de O C ^a   Passos, Madla A ^a   Tanus Santos, Jose E ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Hypertension; Mouthwash; Nitrates; Nitrites; Nitrosation

Indexed keywords

CHLORHEXIDINE GLUCONATE; NITRATE; NITRIC ACID DERIVATIVE; S NITROSOTHIOL; SODIUM NITRATE; SODIUM NITRITE; ANTIHYPERTENSIVE AGENT; MOUTHWASH; NITRITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIHYPERTENSIVE ACTIVITY; ARTICLE; BLOOD LEVEL; COLONY FORMING UNIT; CONTROLLED STUDY; HYPERTENSION; MALE; MEAN ARTERIAL PRESSURE; NITROSATION; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; RAT; SALIVA; STOMACH; SYSTOLIC BLOOD PRESSURE; ANIMAL; BLOOD PRESSURE; DISEASE MODEL; DRUG EFFECTS; KIDNEY ARTERY; KIDNEY ARTERY STENOSIS; METABOLISM; PATHOPHYSIOLOGY; WISTAR RAT;

ANIMALS; ANTIHYPERTENSIVE AGENTS; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; HYPERTENSION; MALE; MOUTHWASHES; NITRATES; NITRITES; NITROSATION; RATS; RATS, WISTAR; RENAL ARTERY; RENAL ARTERY OBSTRUCTION; S-NITROSOTHIOLS;

EID: 84993965180     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.10.013     Document Type: Article

References (53)

1. [1] van Faassen, E.E., Bahrami, S., Feelisch, M., Hogg, N., Kelm, M., Kim-Shapiro, D.B., Kozlov, A.V., Li, H., Lundberg, J.O., Mason, R., Nohl, H., Rassaf, T., Samouilov, A., Slama-Schwok, A., Shiva, S., Vanin, A.F., Weitzberg, E., Zweier, J., Gladwin, M.T., Nitrite as regulator of hypoxic signaling in mammalian physiology. Med. Res. Rev. 29 (2009), 683–741.
2. [2] Lundberg, J.O., Gladwin, M.T., Ahluwalia, A., Benjamin, N., Bryan, N.S., Butler, A., Cabrales, P., Fago, A., Feelisch, M., Ford, P.C., Freeman, B.A., Frenneaux, M., Friedman, J., Kelm, M., Kevil, C.G., Kim-Shapiro, D.B., Kozlov, A.V., Lancaster, J.R. Jr, Lefer, D.J., McColl, K., McCurry, K., Patel, R.P., Petersson, J., Rassaf, T., Reutov, V.P., Richter-Addo, G.B., Schechter, A., Shiva, S., Tsuchiya, K., van Faassen, E.E., Webb, A.J., Zuckerbraun, B.S., Zweier, J.L., Weitzberg, E., Nitrate and nitrite in biology, nutrition and therapeutics. Nat. Chem. Biol. 5 (2009), 865–869.
3. [3] Gladwin, M.T., Schechter, A.N., Kim-Shapiro, D.B., Patel, R.P., Hogg, N., Shiva, S., Cannon, R.O., Kelm, M., Wink, D. a., Espey, M.G., Oldfield, E.H., Pluta, R.M., Freeman, B. a., Lancaster, J.R., Feelisch, M., Lundberg, J.O., The emerging biology of the nitrite anion. Nat. Chem. Biol., 1, 2005, 308–314.
4. [4] Cosby, K., Partovi, K.S., Crawford, J.H., Patel, R.P., Reiter, C.D., Martyr, S., Yang, B.K., Waclawiw, M.A., Zalos, G., Xu, X., Huang, K.T., Shields, H., Kim-Shapiro, D.B., Schechter, A.N., Cannon, R.O. 3rd, Gladwin, M.T., Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat. Med. 9 (2003), 1498–1505.
5. [5] Montenegro, M.F., Amaral, J.H., Pinheiro, L.C., Sakamoto, E.K., Ferreira, G.C., Reis, R.I., Marçal, D.M.O., Pereira, R.P., Tanus-Santos, J.E., Sodium nitrite downregulates vascular NADPH oxidase and exerts antihypertensive effects in hypertension. Free Radic. Biol. Med. 51 (2011), 144–152.
6. [6] Webb, A.J., Patel, N., Loukogeorgakis, S., Okorie, M., Aboud, Z., Misra, S., Rashid, R., Miall, P., Deanfield, J., Benjamin, N., MacAllister, R., Hobbs, A.J., Ahluwalia, A., Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite. Hypertension 51 (2008), 784–790.
7. [7] 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 (2005), H2163–H2170.
8. [8] Larsen, F.J., Ekblom, B., Sahlin, K., Lundberg, J.O., Weitzberg, E., Effects of dietary nitrate on blood pressure in healthy volunteers. N. Engl. J. Med. 355 (2006), 2792–2793.
9. [9] Kapil, V., Milsom, A.B., Okorie, M., Maleki-Toyserkani, S., Akram, F., Rehman, F., Arghandawi, S., Pearl, V., Benjamin, N., Loukogeorgakis, S., Macallister, R., Hobbs, A.J., Webb, A.J., Ahluwalia, A., Inorganic nitrate supplementation lowers blood pressure in humans: role for nitrite-derived NO. Hypertension 56 (2010), 274–281.
10. [10] Lundberg, J.O., Weitzberg, E., Gladwin, M.T., The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat. Rev. Drug Discov. 7 (2008), 156–167.
11. [11] Benjamin, N., O'Driscoll, F., Dougall, H., Duncan, C., Smith, L., Golden, M., McKenzie, H., Stomach NO synthesis. Nature, 368, 1994, 502.
12. [12] Lundberg, J.O., Weitzberg, E., Lundberg, J.M., Alving, K., Intragastric nitric oxide production in humans: measurements in expelled air. Gut 35 (1994), 1543–1546.
13. [13] Lundberg, J.O., Weitzberg, E., Biology of nitrogen oxides in the gastrointestinal tract. Gut, 2012.
14. [14] Jansson, E.A., Huang, L., Malkey, R., Govoni, M., Nihlen, C., Olsson, A., Stensdotter, M., Petersson, J., Holm, L., Weitzberg, E., Lundberg, J.O., A mammalian functional nitrate reductase that regulates nitrite and nitric oxide homeostasis. Nat. Chem. Biol. 4 (2008), 411–417.
15. [15] Huang, L., Borniquel, S., Lundberg, J.O., Enhanced xanthine oxidoreductase expression and tissue nitrate reduction in germ free mice. Nitric Oxide 22 (2010), 191–195.
16. [16] Kapil, V., Haydar, S.M. a., Pearl, V., Lundberg, J.O., Weitzberg, E., Ahluwalia, A., Physiological role for nitrate-reducing oral bacteria in blood pressure control. Free Radic. Biol. Med 55 (2013), 93–100.
17. [17] Petersson, J., Carlström, M., Schreiber, O., Phillipson, M., Christoffersson, G., Jägare, A., Roos, S., Jansson, E. a., Persson, a.E.G., Lundberg, J.O., Holm, L., Gastroprotective and blood pressure lowering effects of dietary nitrate are abolished by an antiseptic mouthwash. Free Radic. Biol. Med 46 (2009), 1068–1075.
18. [18] Hyde, E.R., Luk, B., Cron, S., Kusic, L., McCue, T., Bauch, T., Kaplan, H., Tribble, G., Petrosino, J.F., Bryan, N.S., Characterization of the rat oral microbiome and the effects of dietary nitrate. Free Radic. Biol. Med 77 (2014), 249–257.
19. [19] Govoni, M., Jansson, E.A., Weitzberg, E., Lundberg, J.O., The increase in plasma nitrite after a dietary nitrate load is markedly attenuated by an antibacterial mouthwash. Nitric Oxide 19 (2008), 333–337.
20. [20] Shiva, S., Huang, Z., Grubina, R., Sun, J., Ringwood, L.A., MacArthur, P.H., Xu, X., Murphy, E., Darley-Usmar, V.M., Gladwin, M.T., Deoxymyoglobin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration. Circ. Res. 100 (2007), 654–661.
21. [21] Dejam, A., Hunter, C.J., Tremonti, C., Pluta, R.M., Hon, Y.Y., Grimes, G., Partovi, K., Pelletier, M.M., Oldfield, E.H., Cannon, R.O., Schechter, A.N., Gladwin, M.T., Nitrite infusion in humans and nonhuman primates: endocrine effects, pharmacokinetics, and tolerance formation. Circulation 116 (2007), 1821–1831.
22. [22] Gao, X., Yang, T., Liu, M., Peleli, M., Zollbrecht, C., Weitzberg, E., Lundberg, J.O., Persson, A.E., Carlstrom, M., NADPH oxidase in the renal microvasculature is a primary target for blood pressure-lowering effects by inorganic nitrate and nitrite. Hypertension 65 (2015), 161–170.
23. [23] Pinheiro, L.C., Amaral, J.H., Ferreira, G.C., Portella, R.L., Ceron, C.S., Montenegro, M.F., Toledo, J.C. Jr, Tanus-Santos, J.E., Gastric S-nitrosothiol formation drives the antihypertensive effects of oral sodium nitrite and nitrate in a rat model of renovascular hypertension. Free Radic. Biol. Med. 87 (2015), 252–262.
24. [24] Montenegro, M.F., Pinheiro, L.C., Amaral, J.H., Marçal, D.M.O., Palei, A.C.T., Costa-Filho, A.J., Tanus-Santos, J.E., Antihypertensive and antioxidant effects of a single daily dose of sodium nitrite in a model of renovascular hypertension. Naunyn Schmiede. Arch. Pharm. 385 (2012), 509–517.
25. [25] Pinheiro, L.C., Amaral, J.H., Ferreira, G.C., Montenegro, M.F., Oliveira-Paula, G.H., Tanus-Santos, J.E., The antihypertensive effects of sodium nitrite are not associated with circulating angiotensin converting enzyme inhibition. Nitric Oxide 40C (2014), 52–59.
26. [26] Ceron, C.S., Rizzi, E., Guimaraes, D.A., Martins-Oliveira, A., Gerlach, R.F., Tanus-Santos, J.E., Nebivolol attenuates prooxidant and profibrotic mechanisms involving TGF-beta and MMPs, and decreases vascular remodeling in renovascular hypertension. Free Radic. Biol. Med. 65C (2013), 47–56.
27. [27] Martins-Oliveira, A., Castro, M.M., Oliveira, D.M., Rizzi, E., Ceron, C.S., Guimaraes, D., Reis, R.I., Costa-Neto, C.M., Casarini, D.E., Ribeiro, A.A., Gerlach, R.F., Tanus-Santos, J.E., Contrasting effects of aliskiren versus losartan on hypertensive vascular remodeling. Int. J. Cardiol. 167 (2013), 1199–1205.
28. [28] Pinheiro, L.C., Montenegro, M.F., Amaral, J.H., Ferreira, G.C., Oliveira, A.M., Tanus-Santos, J.E., Increase in gastric pH reduces hypotensive effect of oral sodium nitrite in rats. Free Radic. Biol. Med. 53 (2012), 701–709.
29. [29] Amaral, J.H., Montenegro, M.F., Pinheiro, L.C., Ferreira, G.C., Barroso, R.P., Costa-Filho, A.J., Tanus-Santos, J.E., TEMPOL enhances the antihypertensive effects of sodium nitrite by mechanisms facilitating nitrite-derived gastric nitric oxide formation. Free Radic. Biol. Med. 65C (2013), 446–455.
30. [30] Montenegro, M.F., Pinheiro, L.C., Amaral, J.H., Ferreira, G.C., Portella, R.L., Tanus-Santos, J.E., Vascular xanthine oxidoreductase contributes to the antihypertensive effects of sodium nitrite in L-NAME hypertension. Naunyn Schmiede. Arch. Pharm. 387 (2014), 591–598.
31. [31] Amaral, J.H., Ferreira, G.C., Pinheiro, L.C., Montenegro, M.F., Tanus-Santos, J.E., Consistent antioxidant and antihypertensive effects of oral sodium nitrite in DOCA-salt hypertension. Redox Biol. 5 (2015), 340–346.
32. [32] Feelisch, M., Rassaf, T., Mnaimneh, S., Singh, N., Bryan, N.S., Jourd'heuil, D., Kelm, M., Concomitant S-, N-, and heme-nitros (yl) ation in biological tissues and fluids: implications for the fate of NO in vivo. FASEB J., 2002, 1775–1785.
33. [33] Figueiredo-Freitas, C., Dulce, R.A., Foster, M.W., Liang, J., Yamashita, A.M., Lima-Rosa, F.L., Thompson, J.W., Moseley, M.A., Hare, J.M., Nogueira, L., Sorenson, M.M., Pinto, J.R., S-nitrosylation of sarcomeric proteins depresses myofilament Ca2+)sensitivity in intact cardiomyocytes. Antioxid. Redox Signal. 23 (2015), 1017–1034.
34. [34] Ghosh, S.M., Kapil, V., Fuentes-Calvo, I., Bubb, K.J., Pearl, V., Milsom, A.B., Khambata, R., Maleki-Toyserkani, S., Yousuf, M., Benjamin, N., Webb, A.J., Caulfield, M.J., Hobbs, A.J., Ahluwalia, A., Enhanced vasodilator activity of nitrite in hypertension: critical role for erythrocytic xanthine oxidoreductase and translational potential. Hypertension 61 (2013), 1091–1102.
35. [35] Li, H., Samouilov, A., Liu, X., Zweier, J.L., Characterization of the magnitude and kinetics of xanthine oxidase-catalyzed nitrate reduction: evaluation of its role in nitrite and nitric oxide generation in anoxic tissues. Biochemistry 42 (2003), 1150–1159.
36. [36] Li, H., Samouilov, A., Liu, X., Zweier, J.L., Characterization of the effects of oxygen on xanthine oxidase-mediated nitric oxide formation. J. Biol. Chem. 279 (2004), 16939–16946.
37. [37] Zweier, J.L., Li, H., Samouilov, A., Liu, X., Mechanisms of nitrite reduction to nitric oxide in the heart and vessel wall. Nitric Oxide 22 (2010), 83–90.
38. [38] Dejam, A., Hunter, C.J., Pelletier, M.M., Hsu, L.L., Machado, R.F., Shiva, S., Power, G.G., Kelm, M., Gladwin, M.T., Schechter, A.N., Erythrocytes are the major intravascular storage sites of nitrite in human blood. Blood 106 (2005), 734–739.
39. [39] Alzawahra, W.F., Talukder, M.A., Liu, X., Samouilov, A., Zweier, J.L., Heme proteins mediate the conversion of nitrite to nitric oxide in the vascular wall. Am. J. Physiol. Heart Circ. Physiol. 295 (2008), H499–H508.
40. [40] Liu, T., Schroeder, H.J., Wilson, S.M., Terry, M.H., Romero, M., Longo, L.D., Power, G.G., Blood, A.B., Local and systemic vasodilatory effects of low molecular weight S-nitrosothiols. Free Radic. Biol. Med. 91 (2016), 215–223.
41. [41] McKnight, G.M., Smith, L.M., Drummond, R.S., Duncan, C.W., Golden, M., Benjamin, N., Chemical synthesis of nitric oxide in the stomach from dietary nitrate in humans. Gut 40 (1997), 211–214.
42. [42] Broniowska, K. a., Hogg, N., The chemical biology of S-nitrosothiols. Antioxid. Redox Signal. 17 (2012), 969–980.
43. [43] Foster, M.W., McMahon, T.J., Stamler, J.S., S-nitrosylation in health and disease. Trends Mol. Med. 9 (2003), 160–168.
44. [44] Richardson, G., Hicks, S.L., O'Byrne, S., Frost, M.T., Moore, K., Benjamin, N., McKnight, G.M., The ingestion of inorganic nitrate increases gastric S-nitrosothiol levels and inhibits platelet function in humans. Nitric Oxide 7 (2002), 24–29.
45. [45] Zhang, Y., Hogg, N., The mechanism of transmembrane S-nitrosothiol transport. Proc. Natl. Acad. Sci. USA 101 (2004), 7891–7896.
46. [46] Leclerc, P.C., Lanctot, P.M., Auger-Messier, M., Escher, E., Leduc, R., Guillemette, G., S-nitrosylation of cysteine 289 of the AT1 receptor decreases its binding affinity for angiotensin II. Br. J. Pharm. 148 (2006), 306–313.
47. [47] Ceron, C.S., Rizzi, E., Guimaraes, D.A., Martins-Oliveira, A., Cau, S.B., Ramos, J., Gerlach, R.F., Tanus-Santos, J.E., Time course involvement of matrix metalloproteinases in the vascular alterations of renovascular hypertension. Matrix Biol. 31 (2012), 261–270.
48. [48] Pinheiro, L.C., Oliveira-Paula, G.H., Portella, R.L., Guimaraes, D.A., de Angelis, C.D., Tanus-Santos, J.E., Omeprazole impairs vascular redox biology and causes xanthine oxidoreductase-mediated endothelial dysfunction. Redox Biol. 9 (2016), 134–143.
49. [49] Maron, B.A., Tang, S.S., Loscalzo, J., S-nitrosothiols and the S-nitrosoproteome of the cardiovascular system. Antioxid. Redox Signal. 18 (2013), 270–287.
50. [50] Castro, M.M., Rizzi, E., Rodrigues, G.J., Ceron, C.S., Bendhack, L.M., Gerlach, R.F., Tanus-Santos, J.E., Antioxidant treatment reduces matrix metalloproteinase-2-induced vascular changes in renovascular hypertension. Free Radic. Biol. Med. 46 (2009), 1298–1307.
51. [51] Carlstrom, M., Persson, A.E., Larsson, E., Hezel, M., Scheffer, P.G., Teerlink, T., Weitzberg, E., Lundberg, J.O., Dietary nitrate attenuates oxidative stress, prevents cardiac and renal injuries, and reduces blood pressure in salt-induced hypertension. Cardiovasc. Res. 89 (2011), 574–585.
52. [52] Hezel, M., Peleli, M., Liu, M., Zollbrecht, C., Jensen, B.L., Checa, A., Giulietti, A., Wheelock, C.E., Lundberg, J.O., Weitzberg, E., Carlstrom, M., Dietary nitrate improves age-related hypertension and metabolic abnormalities in rats via modulation of angiotensin II receptor signaling and inhibition of superoxide generation. Free Radic. Biol. Med. 99 (2016), 87–98.
53. [53] Lundberg, J.O., Gladwin, M.T., Weitzberg, E., Strategies to increase nitric oxide signalling in cardiovascular disease. Nat. Rev. Drug Discov. 14 (2015), 623–641.