Dietary inorganic nitrate improves mitochondrial efficiency in humans

Cell Metabolism

Volumn 13, Issue 2, 2011, Pages 149-159

  Larsen, Filip J ^a   Schiffer, Tomas A ^a   Borniquel, Sara ^a   Sahlin, Kent ^a   Ekblom, Björn ^a   Lundberg, Jon O ^a   Weitzberg, Eddie ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ATRACTYLOSIDE; CYCLIC GMP; NITRATE; NITRITE; PLACEBO; SODIUM NITRITE; UNCOUPLING PROTEIN 3;

ADULT; ARTICLE; BLOOD LEVEL; CROSSOVER PROCEDURE; DIETARY INTAKE; DOUBLE BLIND PROCEDURE; HUMAN; HUMAN TISSUE; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MUSCLE BIOPSY; MUSCLE EXERCISE; MUSCLE MITOCHONDRION; NORMAL HUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; THERMODYNAMICS;

ADULT; CYCLIC GMP; DIETARY SUPPLEMENTS; DOUBLE-BLIND METHOD; EXERCISE; HUMANS; ION CHANNELS; MALE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NITRATES; NITRITES; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION;

EID: 79551510834     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2011.01.004     Document Type: Article

References (63)

1. C. Affourtit, P.G. Crichton, N. Parker, and M.D. Brand Novel uncoupling proteins Novartis Found. Symp. 287 2007 70 80 discussion 80-91
2. E. Aguirre, F. Rodriguez-Juarez, A. Bellelli, E. Gnaiger, and S. Cadenas Kinetic model of the inhibition of respiration by endogenous nitric oxide in intact cells Biochim. Biophys. Acta 1797 2010 557 565
3. P.O. strand, K. Rodahl, H.A. Dahl, and S.B. Strömme Textbook of Work Physiology: Physiological Bases of Exercise 4th ed. 2003 Human Kinetics Stockholm
4. S.J. Bailey, P. Winyard, A. Vanhatalo, J.R. Blackwell, F.J. Dimenna, D.P. Wilkerson, J. Tarr, N. Benjamin, and A.M. Jones Dietary nitrate supplementation reduces the O2 cost of low-intensity exercise and enhances tolerance to high-intensity exercise in humans J. Appl. Physiol. 107 2009 1144 1155
5. S.J. Bailey, J. Fulford, A. Vanhatalo, P.G. Winyard, J.R. Blackwell, F.J. Dimenna, D.P. Wilkerson, N. Benjamin, and A.M. Jones Dietary nitrate supplementation enhances muscle contractile efficiency during knee-extensor exercise in humans J. Appl. Physiol. 109 2010 135 148
6. D.E. Befroy, K.F. Petersen, S. Dufour, G.F. Mason, D.L. Rothman, and G.I. Shulman Increased substrate oxidation and mitochondrial uncoupling in skeletal muscle of endurance-trained individuals Proc. Natl. Acad. Sci. USA 105 2008 16701 16706
7. L. Bevilacqua, E.L. Seifert, C. Estey, M.F. Gerrits, and M.E. Harper Absence of uncoupling protein-3 leads to greater activation of an adenine nucleotide translocase-mediated proton conductance in skeletal muscle mitochondria from calorie restricted mice Biochim. Biophys. Acta. 1797 2010 1389 1397
8. S. Borniquel, E.A. Jansson, M.P. Cole, B.A. Freeman, and J.O. Lundberg Nitrated oleic acid up-regulates PPARgamma and attenuates experimental inflammatory bowel disease Free Radic. Biol. Med. 48 2010 499 505
9. M.D. Brand, J.L. Pakay, A. Ocloo, J. Kokoszka, D.C. Wallace, P.S. Brookes, and E.J. Cornwall The basal proton conductance of mitochondria depends on adenine nucleotide translocase content Biochem. J. 392 2005 353 362
10. E. Brouwer On simple formulae for calculating the heat expenditure and the quantities of carbohydrate and fat oxidized in metabolism of men and animals, from gaseous exchange (oxygen intake and carbonic acid output) and urine-N Acta Physiol. Pharmacol. Neerl. 6 1957 795 802
11. G.C. Brown, and C.E. Cooper Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase FEBS Lett. 356 1994 295 298
12. 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, and M. Feelisch Nitrite is a signaling molecule and regulator of gene expression in mammalian tissues Nat. Chem. Biol. 1 2005 290 297
13. N.S. Bryan, J.W. Calvert, J.W. Elrod, S. Gundewar, S.Y. Ji, and D.J. Lefer Dietary nitrite supplementation protects against myocardial ischemia-reperfusion injury Proc. Natl. Acad. Sci. USA 104 2007 19144 19149
14. C.B. Cairns, J. Walther, A.H. Harken, and A. Banerjee Mitochondrial oxidative phosphorylation thermodynamic efficiencies reflect physiological organ roles Am. J. Physiol. 274 1998 R1376 R1383
15. M. Carlstrom, F.J. Larsen, T. Nystrom, M. Hezel, S. Borniquel, E. Weitzberg, and J.O. Lundberg Dietary inorganic nitrate reverses features of metabolic syndrome in endothelial nitric oxide synthase-deficient mice Proc. Natl. Acad. Sci. USA 107 2010 17716 17720
16. P.R. Castello, P.S. David, T. McClure, Z. Crook, and R.O. Poyton Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes Cell Metab. 3 2006 277 287
17. K.S. Echtay, D. Roussel, J. St-Pierre, M.B. Jekabsons, S. Cadenas, J.A. Stuart, J.A. Harper, S.J. Roebuck, A. Morrison, and S. Pickering Superoxide activates mitochondrial uncoupling proteins Nature 415 2002 96 99
18. M. Fernstrom, M. Tonkonogi, and K. Sahlin Effects of acute and chronic endurance exercise on mitochondrial uncoupling in human skeletal muscle J. Physiol. 554 2004 755 763
19. M.T. Gladwin, A.N. Schechter, D.B. Kim-Shapiro, R.P. Patel, N. Hogg, S. Shiva, R.O. Cannon 3rd, M. Kelm, D.A. Wink, and M.G. Espey The emerging biology of the nitrite anion Nat. Chem. Biol. 1 2005 308 314
20. E. Gnaiger Oxygen conformance of cellular respiration. A perspective of mitochondrial physiology Adv. Exp. Med. Biol. 543 2003 39 55
21. E. Gnaiger, G. Mendez, and S.C. Hand High phosphorylation efficiency and depression of uncoupled respiration in mitochondria under hypoxia Proc. Natl. Acad. Sci. USA 97 2000 11080 11085
22. M. Govoni, E.A. Jansson, E. Weitzberg, and J.O. Lundberg The increase in plasma nitrite after a dietary nitrate load is markedly attenuated by an antibacterial mouthwash Nitric Oxide 19 2008 333 337
23. B.H. Groen, J.A. Berden, and K. van Dam Differentiation between leaks and slips in oxidative phosphorylation Biochim. Biophys. Acta 1019 1990 121 127
24. P.C. Hinkle P/O ratios of mitochondrial oxidative phosphorylation Biochim. Biophys. Acta 1706 2005 1 11
25. L.J. Ignarro, G.M. Buga, K.S. Wood, R.E. Byrns, and G. Chaudhuri Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide Proc. Natl. Acad. Sci. USA 84 1987 9265 9269
26. S. Iossa, M.P. Mollica, L. Lionetti, R. Crescenzo, R. Tasso, and G. Liverini A possible link between skeletal muscle mitochondrial efficiency and age-induced insulin resistance Diabetes 53 2004 2861 2866
27. M. Klingenberg Mitochondria metabolite transport FEBS Lett. 6 1970 145 154
28. A.V. Kozlov, K. Staniek, and H. Nohl Nitrite reductase activity is a novel function of mammalian mitochondria FEBS Lett. 454 1999 127 130
29. A.V. Kuznetsov, T. Tiivel, P. Sikk, T. Kaambre, L. Kay, Z. Daneshrad, A. Rossi, L. Kadaja, N. Peet, and E. Seppet Striking differences between the kinetics of regulation of respiration by ADP in slow-twitch and fast-twitch muscles in vivo Eur. J. Biochem. 241 1996 909 915
30. F.J. Larsen, B. Ekblom, K. Sahlin, J.O. Lundberg, and E. Weitzberg Effects of dietary nitrate on blood pressure in healthy volunteers N. Engl. J. Med. 355 2006 2792 2793
31. F.J. Larsen, E. Weitzberg, J.O. Lundberg, and B. Ekblom Effects of dietary nitrate on oxygen cost during exercise Acta Physiol. (Oxf.) 191 2007 59 66
32. F.J. Larsen, E. Weitzberg, J.O. Lundberg, and B. Ekblom Dietary nitrate reduces maximal oxygen consumption while maintaining work performance in maximal exercise Free Radic. Biol. Med. 48 2010 342 347
33. C.Y. Li, J.Z. Liu, L.P. Wu, B. Li, and L.F. Chen Effects of hypobaric hypoxia on adenine nucleotide pools, adenine nucleotide transporter activity and protein expression in rat liver World J. Gastroenterol. 12 2006 2120 2124
34. A.D. Liese, M. Nichols, X. Sun, R.B. D'Agostino Jr., and S.M. Haffner Adherence to the DASH diet is inversely associated with incidence of type 2 diabetes: the insulin resistance atherosclerosis study Diabetes Care 32 2009 1434 1436
35. J.O. Lundberg, and M. Govoni Inorganic nitrate is a possible source for systemic generation of nitric oxide Free Radic. Biol. Med. 37 2004 395 400
36. J.O. Lundberg, E. Weitzberg, J.A. Cole, and N. Benjamin Nitrate, bacteria and human health Nat. Rev. Microbiol. 2 2004 593 602
37. J.O. Lundberg, E. Weitzberg, and M.T. Gladwin The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics Nat. Rev. Drug Discov. 7 2008 156 167
38. J.O. Lundberg, M.T. Gladwin, A. Ahluwalia, N. Benjamin, N.S. Bryan, A. Butler, P. Cabrales, A. Fago, M. Feelisch, and P.C. Ford Nitrate and nitrite in biology, nutrition and therapeutics Nat. Chem. Biol. 5 2009 865 869
39. A. Modin, H. Bjorne, M. Herulf, K. Alving, E. Weitzberg, and J.O. Lundberg Nitrite-derived nitric oxide: a possible mediator of 'acidic-metabolic' vasodilation Acta Physiol. Scand. 171 2001 9 16
40. M. Mogensen, M. Bagger, P.K. Pedersen, M. Fernstrom, and K. Sahlin Cycling efficiency in humans is related to low UCP3 content and to type I fibres but not to mitochondrial efficiency J. Physiol. 571 2006 669 681
41. S. Moncada, and A. Higgs The L-arginine-nitric oxide pathway N. Engl. J. Med. 329 1993 2002 2012
42. L. Moseley, J. Achten, J.C. Martin, and A.E. Jeukendrup No differences in cycling efficiency between world-class and recreational cyclists Int. J. Sports Med. 25 2004 374 379
43. E. Nisoli, E. Clementi, C. Paolucci, V. Cozzi, C. Tonello, C. Sciorati, R. Bracale, A. Valerio, M. Francolini, and S. Moncada Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide Science 299 2003 896 899
44. H. Nohl, K. Staniek, B. Sobhian, S. Bahrami, H. Redl, and A.V. Kozlov Mitochondria recycle nitrite back to the bioregulator nitric monoxide Acta Biochim. Pol. 47 2000 913 921
45. M. Palacios-Callender, V. Hollis, N. Frakich, J. Mateo, and S. Moncada Cytochrome c oxidase maintains mitochondrial respiration during partial inhibition by nitric oxide J. Cell Sci. 120 2007 160 165
46. N. Parker, C. Affourtit, A. Vidal-Puig, and M.D. Brand Energization-dependent endogenous activation of proton conductance in skeletal muscle mitochondria Biochem. J. 412 2008 131 139
47. A.S. Reisch, and O. Elpeleg Biochemical assays for mitochondrial activity: assays of TCA cycle enzymes and PDHc Methods Cell Biol. 80 2007 199 222
48. R.S. Richardson, S. Duteil, C. Wary, D.W. Wray, J. Hoff, and P.G. Carlier Human skeletal muscle intracellular oxygenation: the impact of ambient oxygen availability J. Physiol. 571 2006 415 424
49. D.F. Rolfe, A.J. Hulbert, and M.D. Brand Characteristics of mitochondrial proton leak and control of oxidative phosphorylation in the major oxygen-consuming tissues of the rat Biochim. Biophys. Acta 1188 1994 405 416
50. S. Shiva, M.N. Sack, J.J. Greer, M. Duranski, L.A. Ringwood, L. Burwell, X. Wang, P.H. MacArthur, A. Shoja, and N. Raghavachari Nitrite augments tolerance to ischemia/reperfusion injury via the modulation of mitochondrial electron transfer J. Exp. Med. 204 2007 2089 2102
51. S. Soboll, and J. Stucki Regulation of the degree of coupling of oxidative phosphorylation in intact rat liver Biochim. Biophys. Acta 807 1985 245 254
52. R. Steinlechner-Maran, T. Eberl, M. Kunc, R. Margreiter, and E. Gnaiger Oxygen dependence of respiration in coupled and uncoupled endothelial cells Am. J. Physiol. 271 1996 C2053 C2061
53. J.W. Stucki The optimal efficiency and the economic degrees of coupling of oxidative phosphorylation Eur. J. Biochem. 109 1980 269 283
54. S.R. Tannenbaum, and P. Correa Nitrate and gastric cancer risks Nature 317 1985 675 676
55. D.D. Thomas, X. Liu, S.P. Kantrow, and J.R. Lancaster Jr. The biological lifetime of nitric oxide: implications for the perivascular dynamics of NO and O2 Proc. Natl. Acad. Sci. USA 98 2001 355 360
56. M. Tonkonogi, and K. Sahlin Rate of oxidative phosphorylation in isolated mitochondria from human skeletal muscle: effect of training status Acta Physiol. Scand. 161 1997 345 353
57. M. Tonkonogi, B. Walsh, T. Tiivel, V. Saks, and K. Sahlin Mitochondrial function in human skeletal muscle is not impaired by high intensity exercise Pflugers Arch. 437 1999 562 568
58. E.E. van Faassen, S. Bahrami, M. Feelisch, N. Hogg, M. Kelm, D.B. Kim-Shapiro, A.V. Kozlov, H. Li, J.O. Lundberg, and R. Mason Nitrite as regulator of hypoxic signaling in mammalian physiology Med. Res. Rev. 29 2009 683 741
59. A.J. Webb, N. Patel, S. Loukogeorgakis, M. Okorie, Z. Aboud, S. Misra, R. Rashid, P. Miall, J. Deanfield, and N. Benjamin Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite Hypertension 51 2008 784 790
60. R. Wibom, L. Hagenfeldt, and U. von Dobeln Measurement of ATP production and respiratory chain enzyme activities in mitochondria isolated from small muscle biopsy samples Anal. Biochem. 311 2002 139 151
61. W.C. Willett Diet and health: what should we eat? Science 264 1994 532 537
62. M. Zackova, and P. Jezek Reconstitution of novel mitochondrial uncoupling proteins UCP2 and UCP3 Biosci. Rep. 22 2002 33 46
63. J.L. Zweier, P. Wang, A. Samouilov, and P. Kuppusamy Enzyme-independent formation of nitric oxide in biological tissues Nat. Med. 1 1995 804 809