Inorganic nitrate promotes the browning of white adipose tissue through the nitrate-nitrite-nitric oxide pathway

Diabetes

Volumn 64, Issue 2, 2015, Pages 471-484

  Roberts, Lee D ^a,b   Ashmore, Tom ^b,c   Kotwica, Aleksandra O ^c   Murfitt, Steven A ^b   Fernandez, Bernadette O ^d   Feelisch, Martin ^d   Murray, Andrew J ^c   Griffin, Julian L ^a,b  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A DEHYDROGENASE; CARNITINE PALMITOYLTRANSFERASE I; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYTOCHROME C; LONG CHAIN FATTY ACID; MEMBRANE PROTEIN; MOLECULAR MARKER; NITRATE; NITRIC OXIDE; NITRITE; OXYGEN; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TBX1; TRANSMEMBRANE PROTEIN 26; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1; NITRIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASAL METABOLIC RATE; BROWN ADIPOCYTE; CONTROLLED STUDY; ENERGY EXPENDITURE; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; GENE EXPRESSION; HUMAN; MALE; MASS FRAGMENTOGRAPHY; METABOLOMICS; MOUSE; NONHUMAN; OXYGEN CONCENTRATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; RESPIRATORY CHAIN; TISSUE METABOLISM; WHITE ADIPOCYTE; ANIMAL; BROWN ADIPOSE TISSUE; C57BL MOUSE; CELL CULTURE; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; WHITE ADIPOSE TISSUE; WISTAR RAT;

ADIPOCYTES, BROWN; ADIPOCYTES, WHITE; ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ANIMALS; CELLS, CULTURED; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DOSE-RESPONSE RELATIONSHIP, DRUG; MALE; MICE; MICE, INBRED C57BL; NITRATES; NITRIC OXIDE; NITRITES; RATS; RATS, WISTAR;

EID: 84921924044     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0496     Document Type: Article

References (48)

1. Huang PL. eNOS, metabolic syndrome and cardiovascular disease. Trends Endocrinol Metab 2009;20:295-302
2. Monti LD, Barlassina C, Citterio L, et al. Endothelial nitric oxide synthase polymorphisms are associated with type 2 diabetes and the insulin resistance syndrome. Diabetes 2003;52:1270-1275
3. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 1993;329:2002-2012
4. Jansson EA, Huang L, Malkey R, et al. A mammalian functional nitrate reductase that regulates nitrite and nitric oxide homeostasis. Nat Chem Biol 2008;4:411-417
5. 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;355:2792-2793
6. Carlström M, Larsen FJ, Nyström T, et al. Dietary inorganic nitrate reverses features of metabolic syndrome in endothelial nitric oxide synthase-deficient mice. Proc Natl Acad Sci U S A 2010;107:17716-17720
7. Kapil V, Milsom AB, Okorie M, et al. Inorganic nitrate supplementation lowers blood pressure in humans: role for nitrite-derived NO. Hypertension 2010;56:274-281
8. Bryan NS, Fernandez BO, Bauer SM, et al. Nitrite is a signaling molecule and regulator of gene expression in mammalian tissues. Nat Chem Biol 2005;1:290-297
9. Mitschke MM, Hoffmann LS, Gnad T, et al. Increased cGMP promotes healthy expansion and browning of white adipose tissue. FASEB J 2013;27:1621-1630
10. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 2004;84:277-359
11. Lowell BB, Spiegelman BM. Towards a molecular understanding of adaptive thermogenesis. Nature 2000;404:652-660
12. Wu Z, Puigserver P, Andersson U, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999;98:115-124
13. Enerbäck S, Jacobsson A, Simpson EM, et al. Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 1997;387:90-94
14. Ishibashi J, Seale P. Medicine. Beige can be slimming. Science 2010;328:1113-1114
15. Petrovic N, Walden TB, Shabalina IG, Timmons JA, Cannon B, Nedergaard J. Chronic peroxisome proliferator-activated receptor gamma (PPARgamma) activation of epididymally derived white adipocyte cultures reveals a population of thermogenically competent, UCP1-containing adipocytes molecularly distinct from classic brown adipocytes. J Biol Chem 2010;285:7153-7164
16. Cousin B, Cinti S, Morroni M, et al. Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization. J Cell Sci 1992;103:931-942
17. Oberkofler H, Dallinger G, Liu YM, Hell E, Krempler F, Patsch W. Uncoupling protein gene: quantification of expression levels in adipose tissues of obese and non-obese humans. J Lipid Res 1997;38:2125-2133
18. Melnyk A, Harper ME, Himms-Hagen J. Raising at thermoneutrality prevents obesity and hyperphagia in BAT-ablated transgenic mice. Am J Physiol 1997;272:R1088-R1093
19. Kopecky J, Clarke G, Enerbäck S, Spiegelman B, Kozak LP. Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. J Clin Invest 1995;96:2914-2923
20. Roberts LD, Boström P, O'Sullivan JF, et al. β-Aminoisobutyric acid induces browning of white fat and hepatic β-oxidation and is inversely correlated with cardiometabolic risk factors. Cell Metab 2014;19:96-108
21. Rassaf T, Bryan NS, Kelm M, Feelisch M. Concomitant presence of N-nitroso and S-nitroso proteins in human plasma. Free Radic Biol Med 2002;33:1590-1596
22. Boström P, Wu J, Jedrychowski MP, et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 2012;481:463-468
23. Seale P, Conroe HM, Estall J, et al. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest 2011;121:96-105
24. Roberts LD, Murray AJ, Menassa D, Ashmore T, Nicholls AW, Griffin JL. The contrasting roles of PPARd and PPARg in regulating the metabolic switch between oxidation and storage of fats in white adipose tissue. Genome Biol 2011;12:R75
25. Morash AJ, Kotwica AO, Murray AJ. Tissue-specific changes in fatty acid oxidation in hypoxic heart and skeletal muscle. Am J Physiol Regul Integr Comp Physiol 2013;305:R534-R541
26. Houle-Leroy P, Garland T Jr, Swallow JG, Guderley H. Effects of voluntary activity and genetic selection on muscle metabolic capacities in house mice Mus domesticus. J Appl Physiol (1985) 2000;89:1608-1616
27. Charalambous M, Ferron SR, Da Rocha ST, et al. Imprinted gene dosage is critical for the transition to independent life. Cell Metab 2012;15:209-221
28. Roberts LD, Souza AL, Gerszten RE, Clish CB. Targeted metabolomics. Curr Protoc Mol Biol 2012;30:30.2.1-30.2.24
29. Wu J, Boström P, Sparks LM, et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 2012;150:366-376
30. Lundberg JO, Gladwin MT, Ahluwalia A, et al. Nitrate and nitrite in biology, nutrition and therapeutics. Nat Chem Biol 2009;5:865-869
31. Cheung KJ, Tzameli I, Pissios P, et al. Xanthine oxidoreductase is a regulator of adipogenesis and PPARgamma activity. Cell Metab 2007;5:115-128
32. Haas B, Mayer P, Jennissen K, et al. Protein kinase G controls brown fat cell differentiation and mitochondrial biogenesis. Sci Signal 2009;2:ra78
33. Castello PR, David PS, McClure T, Crook Z, Poyton RO. Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab 2006;3:277-287
34. Lundberg JO, Weitzberg E, Gladwin MT. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 2008;7:156-167
35. Van Faassen EE, Bahrami S, Feelisch M, et al. Nitrite as regulator of hypoxic signaling in mammalian physiology. Med Res Rev 2009;29:683-741
36. Ye J, Gao Z, Yin J, He Q. Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am J Physiol Endocrinol Metab 2007;293:E1118-E1128
37. Hosogai N, Fukuhara A, Oshima K, et al. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes 2007;56:901-911
38. Krishnan J, Danzer C, Simka T, et al. Dietary obesity-associated Hif1α activation in adipocytes restricts fatty acid oxidation and energy expenditure via suppression of the Sirt2-NAD+ system. Genes Dev 2012;26:259-270
39. Wellen KE, Thompson CB. Cellular metabolic stress: considering how cells respond to nutrient excess. Mol Cell 2010;40:323-332
40. Webb AJ, Patel N, Loukogeorgakis S, et al. Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite. Hypertension 2008;51:784-790
41. Larsen FJ, Schiffer TA, Borniquel S, et al. Dietary inorganic nitrate improves mitochondrial efficiency in humans. Cell Metab 2011;13:149-159
42. Essawy SS, Abdel-Sater KA, Elbaz AA. Comparing the effects of inorganic nitrate and allopurinol in renovascular complications of metabolic syndrome in rats: role of nitric oxide and uric acid. Arch Med Sci 2014;10:537-545
43. Bordicchia M, Liu D, Amri EZ, et al. Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human. J Clin Invest 2012;122:1022-1036
44. Nisoli E, Clementi E, Paolucci C, et al. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 2003;299:896-899
45. Seale P, Kajimura S, Yang W, et al. Transcriptional control of brown fat determination by PRDM16. Cell Metab 2007;6:38-54
46. Siervo M, Jackson SJ, Bluck LJC. In-vivo nitric oxide synthesis is reduced in obese patients with metabolic syndrome: application of a novel stable isotopic method. J Hypertens 2011;29:1515-1527
47. Liese AD, Nichols M, Sun X, D'Agostino RB Jr, Haffner SM. Adherence to the DASH Diet is inversely associated with incidence of type 2 diabetes: the insulin resistance atherosclerosis study. Diabetes Care 2009;32:1434-1436
48. Carter P, Gray LJ, Troughton J, Khunti K, Davies MJ. Fruit and vegetable intake and incidence of type 2 diabetes mellitus: systematic review and metaanalysis. BMJ 2010;341:c4229