Deletion of inducible nitric-oxide synthase in leptin-deficient mice improves brown adipose tissue function

PLoS ONE

Volumn 5, Issue 6, 2010, Pages

  Becerril, Sara ^a,b   Rodríguez, Amaia ^a,b   Catalán, Victoria ^a,b   Sáinz, Neira ^a,b   Ramaaírez, Beatriz ^a,b   Collantes, María ^a   Peñuelas, Iván ^a   Gómez Ambrosi, Javier ^a,b   Frühbeck, Gema ^a,b  

^a UNIVERSITY CLINIC OF NAVARRA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; INDUCIBLE NITRIC OXIDE SYNTHASE; LEPTIN; LIPID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SIRTUIN 1; SIRTUIN 3; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 3;

ADIPOCYTE; ADIPOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BROWN ADIPOSE TISSUE; CARBOHYDRATE METABOLISM; CELL FUNCTION; CONTROLLED STUDY; ENERGY BALANCE; FOOD INTAKE; GENE DELETION; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; LIPID METABOLISM; MALE; MITOCHONDRION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN DEFICIENCY; REAL TIME POLYMERASE CHAIN REACTION; RECTUM TEMPERATURE; STRAIN DIFFERENCE; THERMOGENESIS; WESTERN BLOTTING;

ADIPOSE TISSUE, BROWN; ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; BODY TEMPERATURE; CARBOHYDRATE METABOLISM; DNA PRIMERS; ENERGY METABOLISM; IMMUNOHISTOCHEMISTRY; LEPTIN; LIPID METABOLISM; MICE; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE II; POLYMERASE CHAIN REACTION;

MUS; RODENTIA;

EID: 77956214423     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010962     Document Type: Article

References (70)

1. Galgani J, Ravussin E (2008) Energy metabolism, fuel selection and body weight regulation. Int J Obes 32 Suppl 7: S109-119.
2. Webber J (2003) Energy balance in obesity. Proc Nutr Soc 62: 539-543.
3. Frühbeck G (2005) Does a NEAT difference in energy expenditure lead to obesity? Lancet 366: 615-616.
4. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84: 277-359.
5. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, et al. (2009) Functional brown adipose tissue in healthy adults. N Engl J Med 360: 1518-1525.
6. Frühbeck G, Becerril S, Sáinz N, Garrastachu P, García-Velloso MJ (2009) BAT: a new target for human obesity? Trends Pharmacol Sci 30: 387-396.
7. Klingenberg M (1990) Mechanism and evolution of the uncoupling protein of brown adipose tissue. Trends Biochem Sci 15: 108-112.
8. Handschin C, Spiegelman BM (2006) Peroxisome proliferator-activated receptor c coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev 27: 728-735.
9. Gómez-Ambrosi J, Frühbeck G, Martínez JA (2001) Rapid in vivo PGC-1 mRNA upregulation in brown adipose tissue of Wistar rats by a b3-adrenergic agonist and lack of effect of leptin. Mol Cell Endocrinol 176: 85-90.
10. Seale P, Kajimura S, Yang W, Chin S, Rohas LM, et al. (2007) Transcriptional control of brown fat determination by PRDM16. Cell Metab 6: 38-54.
11. Frühbeck G, Sesma P, Burrell MA (2009) PRDM16: the interconvertible adipomyocyte switch. Trends Cell Biol 19: 141-146.
12. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, et al. (2005) Nutrient control of glucose homeostasis through a complex of PGC-1a and SIRT1. Nature 434: 113-118.
13. Feige JN, Lagouge M, Canto C, Strehle A, Houten SM, et al. (2008) Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Metab 8: 347-358.
14. Christian M, Kiskinis E, Debevec D, Leonardsson G, White R, et al. (2005) RIP140-targeted repression of gene expression in adipocytes. Mol Cell Biol 25: 9383-9391.
15. White R, Morganstein D, Christian M, Seth A, Herzog B, et al. (2008) Role of RIP140 in metabolic tissues: connections to disease. FEBS Lett 582: 39-45.
16. Ahima RS, Flier JS (2000) Leptin. Annu Rev Physiol 62: 413-437.
17. Sahu A (2004) Minireview: A hypothalamic role in energy balance with special emphasis on leptin. Endocrinology 145: 2613-2620.
18. Scarpace PJ, Matheny M, Pollock BH, Tumer N (1997) Leptin increases uncoupling protein expression and energy expenditure. Am J Physiol 273: E226-230.
19. Scarpace PJ, Matheny M (1998) Leptin induction of UCP1 gene expression is dependent on sympathetic innervation. Am J Physiol 275: E259-264.
20. Kakuma T, Wang ZW, Pan W, Unger RH, Zhou YT (2000) Role of leptin in peroxisome proliferator-activated receptor c coactivator-1 expression. Endocrinology 141: 4576-4582.
21. Gullicksen PS, Flatt WP, Dean RG, Hartzell DL, Baile CA (2002) Energy metabolism and expression of uncoupling proteins 1, 2, and 3 after 21 days of recovery from intracerebroventricular mouse leptin in rats. Physiol Behav 75: 473-482.
22. Commins SP, Watson PM, Padgett MA, Dudley A, Argyropoulos G, et al. (1999) Induction of uncoupling protein expression in brown and white adipose tissue by leptin. Endocrinology 140: 292-300.
23. Nisoli E, Tonello C, Briscini L, Carruba MO (1997) Inducible nitric oxide synthase in rat brown adipocytes: implications for blood flow to brown adipose tissue. Endocrinology 138: 676-682.
24. Nathan C (1997) Inducible nitric oxide synthase: what difference does it make? J Clin Invest 100: 2417-2423.
25. Giordano A, Tonello C, Bulbarelli A, Cozzi V, Cinti S, et al. (2002) Evidence for a functional nitric oxide synthase system in brown adipocyte nucleus. FEBS Lett 514: 135-140.
26. Perreault M, Marette A (2001) Targeted disruption of inducible nitric oxide synthase protects against obesity-linked insulin resistance in muscle. Nat Med 7: 1138-1143.
27. Frühbeck G (1999) Pivotal role of nitric oxide in the control of blood pressure after leptin administration. Diabetes 48: 903-908.
28. Frühbeck G, Gómez-Ambrosi J (2001) Modulation of the leptin-induced white adipose tissue lipolysis by nitric oxide. Cell Signal 13: 827-833.
29. Rodríguez A, Fortuño A, Gómez-Ambrosi J, Zalba G, Díez J, et al. (2007) The inhibitory effect of leptin on angiotensin II-induced vasoconstriction in vascular smooth muscle cells is mediated via a nitric oxide-dependent mechanism. Endocrinology 148: 324-331.
30. Shiuchi T, Nakagami H, Iwai M, Takeda Y, Cui T, et al. (2001) Involvement of bradykinin and nitric oxide in leptin-mediated glucose uptake in skeletal muscle. Endocrinology 142: 608-612.
31. Dixit VD, Mielenz M, Taub DD, Parvizi N (2003) Leptin induces growth hormone secretion from peripheral blood mononuclear cells via a protein kinase C- and nitric oxide-dependent mechanism. Endocrinology 144: 5595-5603.
32. Chehab FF, Mounzih K, Lu R, Lim ME (1997) Early onset of reproductive function in normal female mice treated with leptin. Science 275: 88-90.
33. Gómez-Ambrosi J, Becerril S, Oroz P, Zabalza S, Rodríguez A, et al. (2004) Reduced adipose tissue mass and hypoleptinemia in iNOS deficient mice: effect of LPS on plasma leptin and adiponectin concentrations. FEBS Lett 577: 351-356.
34. Laubach VE, Shesely EG, Smithies O, Sherman PA (1995) Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc Natl Acad Sci U S A 92: 10688-10692.
35. Densmore VS, Morton NM, Mullins JJ, Seckl JR (2006) 11 b-hydroxysteroid dehydrogenase type 1 induction in the arcuate nucleus by high-fat feeding: A novel constraint to hyperphagia? Endocrinology 147: 4486-4495.
36. Mazo M, Planat-Bénard V, Abizanda G, Pelacho B, Léobon B, et al. (2008) Transplantation of adipose derived stromal cells is associated with functional improvement in a rat model of chronic myocardial infarction. Eur J Heart Fail 10: 454-462.
37. Rodríguez A, Catalán V, Becerril S, Gil MJ, Mugueta C, et al. (2008) Impaired adiponectin-AMPK signalling in insulin-sensitive tissues of hypertensive rats. Life Sci 83: 540-549.
38. Gómez-Ambrosi J, Catalán V, Ramírez B, Rodríguez A, Colina I, et al. (2007) Plasma osteopontin levels and expression in adipose tissue are increased in obesity. J Clin Endocrinol Metab 92: 3719-3727.
39. Catalán V, Gómez-Ambrosi J, Rotellar F, Silva C, Rodríguez A, et al. (2007) Validation of endogenous control genes in human adipose tissue: relevance to obesity and obesity-associated type 2 diabetes mellitus. Horm Metab Res 39: 495-500.
40. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, et al. (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372: 425-432.
41. Ueno N, Oh-ishi S, Segawa M, Nishida M, Fukuwatari Y, et al. (1998) Effect of age on brown adipose tissue activity in the obese (ob/ob) mouse. Mech Ageing Dev 100: 67-76.
42. Brown GC (2001) Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim Biophys Acta 1504: 46-57.
43. Brown GC, Borutaite V (2002) Nitric oxide inhibition of mitochondrial respiration and its role in cell death. Free Radic Biol Med 33: 1440-1450.
44. Nisoli E, Clementi E, Paolucci C, Cozzi V, Tonello C, et al. (2003) Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299: 896-899.
45. Merial C, Bouloumie A, Trocheris V, Lafontan M, Galitzky J (2000) Nitric oxide-dependent downregulation of adipocyte UCP-2 expression by tumor necrosis factor-alpha. Am J Physiol Cell Physiol 279: C1100-1106.
46. Zarrindast MR, Gholami A, Sahraei H, Haeri-Rohani A (2003) Role of nitric oxide in the acquisition and expression of apomorphine- or morphine-induced locomotor sensitization. Eur J Pharmacol 482: 205-213.
47. Nicholls DG, Locke RM (1984) Thermogenic mechanisms in brown fat. Physiol Rev 64: 1-64.
48. Tseng YH, Kokkotou E, Schulz TJ, Huang TL, Winnay JN, et al. (2008) New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454: 1000-1004.
49. Debevec D, Christian M, Morganstein D, Seth A, Herzog B, et al. (2007) Receptor interacting protein 140 regulates expression of uncoupling protein 1 in adipocytes through specific peroxisome proliferator activated receptor isoforms and estrogen-related receptor a. Mol Endocrinol 21: 1581-1592.
50. Catalán V, Gómez-Ambrosi J, Lizanzu A, Rodríguez A, Silva C, et al. (2009) RIP140 Gene and protein expression levels are downregulated in visceral adipose tissue in human morbid obesity. Obes Surg 19: 771-776.
51. Uldry M, Yang W, St-Pierre J, Lin J, Seale P, et al. (2006) Complementary action of the PGC-1a coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab 3: 333-341.
52. Nemoto S, Fergusson MM, Finkel T (2005) SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1a. J Biol Chem 280: 16456-16460.
53. Chen W, Yang Q, Roeder RG (2009) Dynamic interactions and cooperative functions of PGC-1a and MED1 in TRa-mediated activation of the brown-fatspecific UCP-1 gene. Mol Cell 35: 755-768.
54. Shi T, Wang F, Stieren E, Tong Q (2005) SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J Biol Chem 280: 13560-13567.
55. Puigserver P, Spiegelman BM (2003) Peroxisome proliferator-activated receptorc coactivator 1 a (PGC-1a): transcriptional coactivator and metabolic regulator. Endocr Rev 24: 78-90.
56. Villarroya F, Brun S, Giralt M, Camara Y, Solanes G, et al. (2001) Gene expression of leptin and uncoupling proteins: molecular end-points of fetal development. Biochem Soc Trans 29: 76-80.
57. Nau K, Fromme T, Meyer CW, von Praun C, Heldmaier G, et al. (2008) Brown adipose tissue specific lack of uncoupling protein 3 is associated with impaired cold tolerance and reduced transcript levels of metabolic genes. J Comp Physiol 178: 269-277.
58. Finocchietto PV, Franco MC, Holod S, González AS, Converso DP, et al. (2009) Mitochondrial nitric oxide synthase: a masterpiece of metabolic adaptation, cell growth, transformation, and death. Exp Biol Med (Maywood) 234: 1020-1028.
59. Soszynski D, Chelminiak M (2007) Intracerebroventricular injection of neuronal and inducible nitric oxide synthase inhibitors does not influence febrile response in rats during turpentine abscess. J Physiol Pharmacol 58: 657-667.
60. Fortuño A, Rodríguez A, Gómez-Ambrosi J, Múniz P, Salvador J, et al. (2002) Leptin inhibits angiotensin II-induced intracellular calcium increase and vasoconstriction in the rat aorta. Endocrinology 143: 3555-3560.
61. Rodríguez A, Frühbeck G, Gómez-Ambrosi J, Catalán V, Sainz N, et al. (2006) The inhibitory effect of leptin on angiotensin II-induced vasoconstriction is blunted in spontaneously hypertensive rats. J Hypertens 24: 1589-1597.
62. White V, González E, Pustovrh C, Capobianco E, Martínez N, et al. (2007) Leptin in embryos from control and diabetic rats during organogenesis: a modulator of nitric oxide production and lipid homeostasis. Diabetes Metab Res Rev 23: 580-588.
63. Raso GM, Pacilio M, Esposito E, Coppola A, Di Carlo R, et al. (2002) Leptin potentiates IFN-c-induced expression of nitric oxide synthase and cyclooxygenase- 2 in murine macrophage J774A.1. Br J Pharmacol 137: 799-804.
64. Frühbeck G (2006) Intracellular signalling pathways activated by leptin. Biochem J 393: 7-20.
65. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, et al. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808.
66. MacLean A, Wei XQ, Huang FP, Al-Alem UA, Chan WL, et al. (1998) Mice lacking inducible nitric-oxide synthase are more susceptible to herpes simplex virus infection despite enhanced Th1 cell responses. J Gen Virol 79 (Pt 4): 825-830.
67. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444: 860-867.
68. Sugita H, Kaneki M, Tokunaga E, Sugita M, Koike C, et al. (2002) Inducible nitric oxide synthase plays a role in LPS-induced hyperglycemia and insulin resistance. Am J Physiol Endocrinol Metab 282: E386-394.
69. Sugita H, Fujimoto M, Yasukawa T, Shimizu N, Sugita M, et al. (2005) Inducible nitric-oxide synthase and NO donor induce insulin receptor substrate- 1 degradation in skeletal muscle cells. J Biol Chem 280: 14203-14211.
70. Fujimoto M, Shimizu N, Kunii K, Martyn JA, Ueki K, et al. (2005) A role for iNOS in fasting hyperglycemia and impaired insulin signaling in the liver of obese diabetic mice. Diabetes 54: 1340-1348.