Brown adipose tissue redox status in response to dietary-induced obesity-associated oxidative stress in male and female rats

Stress

Volumn 14, Issue 2, 2011, Pages 174-184

  Nadal Casellas, A ^a,b   Proenza, A M ^a,b   Gianotti, M ^a,b   Llado I ^a,b  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b Instituto de Salud Carlos III   (Spain)

Author keywords

Brown adipose tissue; gender differences; mitochondria; obesity; oxidative stress; redox status

Indexed keywords

GLUTATHIONE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; UNCOUPLING PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; BODY WEIGHT; BROWN ADIPOSE TISSUE; CALORIC INTAKE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; LIPID DIET; MALE; MITOCHONDRION; NONHUMAN; OBESITY; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RAT; SEX DIFFERENCE;

ADIPOSE TISSUE, BROWN; ANIMALS; DIETARY FATS; FEMALE; GLUTATHIONE; INSULIN; MALE; MITOCHONDRIA; OBESITY; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; RATS, WISTAR; SEX FACTORS; SUPEROXIDE DISMUTASE;

EID: 79551645212     PISSN: 10253890     EISSN: 16078888     Source Type: Journal    
DOI: 10.3109/10253890.2010.524681     Document Type: Article

References (66)

1. Bachman ES, Dhillon H, Zhang CY, Cinti S, Bianco AC, Kobilka BK, Lowell BB. 2002. betaAR signaling required for diet-induced thermogenesis and obesity resistance. Science 297: 843-845.
2. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
3. Brooks SL, Rothwell NJ, Stock MJ, Goodbody AE, Trayhurn P. 1980. Increased proton conductance pathway in brown adipose tissue mitochondria of rats exhibiting diet-induced thermogen-esis. Nature 286:274-276.
4. Cannon B, Shabalina IG, Kramarova TV, Petrovic N, Nedergaard J. 2006. Uncoupling proteins: A role in protection against reactive oxygen species-Or not? Biochem Biophys Acta 1757:449-458.
5. Carriere A, Carmona MC, Fernandez Y, Rigoulet M, Wenger RH, Penicaud L, Casteilla L. 2004. Mitochondrial reactive oxygen species control the transcription factor CHOP-10/GADD153 and adipocyte differentiation: A mechanism for hypoxia-dependent effect. J Biol Chem 279:40462-40469.
6. Catala-Niell A, Estrany ME, Proenza AM, Gianotti M, Llado I. 2008. Skeletal muscle and liver oxidative metabolism in response to a voluntary isocaloric intake of a high fat diet in male and female rats. Cell Physiol Biochem 22:327-336.
7. Chen JQ, Cammarata PR, Baines CP, Yager JD. 2009. Regulation of mitochondrial respiratory chain biogenesis by estrogens/estrogen receptors and physiological, pathological and pharmacological implications. Biochim Biophys Acta 1793:1540-1570.
8. Chrzanowska-Lightowlers ZM, Turnbull DM, Lightowlers RN. 1993. A microtiter plate assay for cytochrome c oxidase in permeabilized whole cells. Anal Biochem 214:45-49.
9. Colom B, Alcolea MP, Valle A, Oliver J, Roca P, Garcia-Palmer FJ. 2007. Skeletal muscle of female rats exhibit higher mitochondrial mass and oxidative-phosphorylative capacities compared to males. Cell Physiol Biochem 19:205-212.
10. Dandona P, Aljada A, Bandyopadhyay A. 2004. Inflammation: The link between insulin resistance, obesity and diabetes. Trends Immunol 25:4-7.
11. Echtay KS. 2007. Mitochondrial uncoupling proteins-What is their physiological role? Free Radic Biol Med 43:1351-1371.
12. Enerback S, Jacobsson A, Simpson EM, Guerra C, Yamashita H, Harper ME, Kozak LP. 1997. Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387: 90-94.
13. Feldmann HM, Golozoubova V, Cannon B, Nedergaard J. 2009. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab 9:203-209.
14. Fisler JS, Warden CH. 2006. Uncoupling proteins, dietary fat and the metabolic syndrome. Nutr Metab (Lond) 3:38.
15. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I. 2004. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 114: 1752-1761.
16. Galinier A, Carriere A, Fernandez Y, Carpene C, Andre M, Caspar-Bauguil S, Thouvenot JP, Periquet B, Penicaud L, Casteilla L. 2006a. Adipose tissue proadipogenic redox changes in obesity. J Biol Chem 281:12682-12687.
17. Galinier A, Carriere A, Fernandez Y, Caspar-Bauguil S, Periquet B, Periquet A, Penicaud L, Casteilla L. 2006b. Site specific changes of redox metabolism in adipose tissue of obese Zucker rats. FEBS Lett 580:6391-6398.
18. Gomez-Perez Y, Amengual-Cladera E, Catala-Niell A, Thomas-Moya E, Gianotti M, Proenza AM, Llado I. 2008. Gender dimorphism in high-fat-diet- induced insulin resistance in skeletal muscle of aged rats. Cell Physiol Biochem 22: 539-548.
19. Granneman JG, Burnazi M, Zhu Z, Schwamb LA. 2003. White adipose tissue contributes to UCP1-independent thermogenesis. Am J Physiol Endocrinol Metab 285:E1230-E1236.
20. Guevara R, Santandreu FM, Valle A, Gianotti M, Oliver J, Roca P. 2009. Sex-dependent differences in aged rat brain mitochondrial function and oxidative stress. Free Radic Biol Med 46:169-175.
21. Halliwell B, Gutteridge JM, Cross CE. 1992. Free radicals, antioxidants, and human disease: Where are we now? J Lab Clin Med 119:598-620.
22. Heaton GM, Wagenvoord RJ, Kemp A, Jr, Nicholls DG. 1978. Brown-adipose-tissue mitochondria: Photoaffinity labelling of the regulatory site of energy dissipation. Eur J Biochem 82: 515-521.
23. Himms-Hagen J. 1984. Brown adipose tissue thermogenesis, energy balance, and obesity. Can J Biochem Cell Biol 62:610-617.
24. Inokuma K, Okamatsu-Ogura Y, Omachi A, Matsushita Y, Kimura K, Yamashita H, Saito M. 2006. Indispensable role of mitochondrial UCP1 for antiobesity effect of beta3-adrenergic stimulation. Am J Physiol Endocrinol Metab 290: E1014-E1021.
25. James AM, Murphy MP. 2002. How mitochondrial damage affects cell function. J Biomed Sci 9:475-487.
26. Johnson P. 2002. Antioxidant enzyme expression in health and disease: Effects of exercise and hypertension. Comp Biochem Physiol C Toxicol Pharmacol 133:493-505.
27. Justo R, Frontera M, Pujol E, Rodriguez-Cuenca S, Llado I, Garcia-Palmer FJ, Roca P, Gianotti M. 2005. Gender-related differences in morphology and thermogenic capacity of brown adipose tissue mitochondrial subpopulations. Life Sci 76: 1147-1158. (Pubitemid 40037536)
28. Keaney JF, Jr, Larson MG, Vasan RS, Wilson PW, Lipinska I, Corey D, Massaro JM, Sutherland P, Vita JA, Benjamin EJ. 2003. Obesity and systemic oxidative stress: Clinical correlates of oxidative stress in the Framingham Study. Arterioscler Thromb Vasc Biol 23:434-439.
29. Lindberg O, de Pierre J, Rylander E, Afzelius BA. 1967. Studies of the mitochondrial energy-transfer system of brown adipose tissue. J Cell Biol 34:293-310.
30. Liu X, Rossmeisl M, McClaine J, Riachi M, Harper ME, Kozak LP. 2003. Paradoxical resistance to diet-induced obesity in UCP1-deficient mice. J Clin Invest 111:399-407.
31. Lopez-Torres M, Gredilla R, Sanz A, Barja G. 2002. Influence of aging and long-term caloric restriction on oxygen radical generation and oxidative DNA damage in rat liver mitochondria. Free Radic Biol Med 32:882-889.
32. Lowell BB, Spiegelman BM. 2000. Towards a molecular understanding of adaptive thermogenesis. Nature 404:652-660.
33. Ma SW, Foster DO. 1989. Brown adipose tissue, liver, and diet-induced thermogenesis in cafeteria diet-fed rats. Can J Physiol Pharmacol 67:376-381.
34. Ma SW, Foster DO, Nadeau BE, Triandafillou J. 1988. Absence of increased oxygen consumption in brown adipose tissue of rats exhibiting "cafeteria" diet-induced thermogenesis. Can J Physiol Pharmacol 66:1347-1354.
35. Matamala JC, Gianotti M, Pericas J, Quevedo S, Roca P, Palou A, Garcia-Palmer FJ. 1996. Changes induced by fasting and dietetic obesity in thermogenic parameters of rat brown adipose tissue mitochondrial subpopulations. Biochem J 319(Pt 2): 529-534.
36. McClung JP, Roneker CA, Mu W, Lisk DJ, Langlais P, Liu F, Lei XG. 2004. Development of insulin resistance and obesity in mice overexpressing cellular glutathione peroxidase. Proc Natl Acad Sci USA 101:8852-8857.
37. Muller FL, Liu Y, Van Remmen H. 2004. Complex III releases superoxide to both sides of the inner mitochondrial membrane. J Biol Chem 279:49064-49073.
38. Nakano K, Tarashima M, Tachikawa E, Noda N, Nakayama T, Sasaki K, Mizoguchi E, Matsuzaki M, Osawa M. 2005. Platelet mitochondrial evaluation during cytochrome c and dichloroace-tate treatments of MELAS. Mitochondrion 5:426-433.
39. Navarro A, Boveris A. 2007. The mitochondrial energy transduction system and the aging process. Am J Physiol Cell Physiol 292: C670-C686.
40. Nedergaard J, Cannon B. 2010. The changed metabolic world with human brown adipose tissue: Therapeutic visions. Cell Metab 11:268-272.
41. Olusi SO. 2002. Obesity is an independent risk factor for plasma lipid peroxidation and depletion of erythrocyte cytoprotectic enzymes in humans. Int J Obes Relat Metab Disord 26: 1159-1164.
42. Paglia DE, Valentine WN. 1967. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxi-dase. J Lab Clin Med 70:158-169.
43. Pedersen SB, Bruun JM, Kristensen K, Richelsen B. 2001. Regulation of UCP1, UCP2, and UCP3 mRNA expression in brown adipose tissue, white adipose tissue, and skeletal muscle in rats by estrogen. Biochem Biophys Res Commun 288:191-197.
44. Pichon L, Huneau JF, Fromentin G, Tome D. 2006. A high-protein, high-fat, carbohydrate-free diet reduces energy intake, hepatic lipogenesis, and adiposity in rats. J Nutr 136:1256-1260.
45. Porter RK. 2008. Uncoupling protein 1: A short-circuit in the chemiosmotic process. J Bioenerg Biomembr 40:457-461.
46. Quevedo S, Roca P, Pico C, Palou A. 1998. Sex-associated differences in cold-induced UCP1 synthesis in rodent brown adipose tissue. Pflugers Arch 436:689-695.
47. Quick KL, Hardt JI, Dugan LL. 2000. Rapid microplate assay for superoxide scavenging efficiency. J Neurosci Methods 97: 139-144.
48. Rebolledo OR, Marra CA, Raschia A, Rodriguez S, Gagliardino JJ. 2008. Abdominal adipose tissue: Early metabolic dysfunction associated to insulin resistance and oxidative stress induced by an unbalanced diet. Horm Metab Res 40:794-800.
49. Reitman A, Friedrich I, Ben-Amotz A, Levy Y. 2002. Low plasma antioxidants and normal plasma B vitamins and homocysteine in patients with severe obesity. Isr Med Assoc J 4:590-593.
50. Richard D. 1986. Effects of ovarian hormones on energy balance and brown adipose tissue thermogenesis. Am J Physiol 250: R245-R249.
51. Roca P, Rodriguez AM, Oliver P, Bonet ML, Quevedo S, Pico C, Palou A. 1999. Brown adipose tissue response to cafeteria diet-feeding involves induction of the UCP2 gene and is impaired in female rats as compared to males. Pflugers Arch 438:628-634.
52. Rodriguez-Cuenca S, Pujol E, Justo R, Frontera M, Oliver J, Gianotti M, Roca P. 2002. Sex-dependent thermogenesis, differences in mitochondrial morphology and function, and adrenergic response in brown adipose tissue. J Biol Chem 277: 42958-42963.
53. Rodriguez-Cuenca S, Monjo M, Gianotti M, Proenza AM, Roca P. 2007. Expression of mitochondrial biogenesis-signaling factors in brown adipocytes is influenced specifically by 17beta-estradiol, testosterone, and progesterone. Am J Physiol Endocrinol Metab 292:E340-E346.
54. Rothwell NJ, Stock MJ. 1979. A role for brown adipose tissue in diet-induced thermogenesis. Nature 281:31-35.
55. Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J, Iwanaga T, Miyagawa M, Kameya T, Nakada K, Kawai Y, Tsujisaki M. 2009. High incidence of metabolically active brown adipose tissue in healthy adult humans: Effects of cold exposure and adiposity. Diabetes 58:1526-1531.
56. Schmid GM, Converset V, Walter N, Sennitt MV, Leung KY, Byers H, Ward M, Hochstrasser DF, Cawthorne MA, Sanchez JC. 2004. Effect of high-fat diet on the expression of proteins in muscle, adipose tissues, and liver of C57BL/6 mice. Proteomics 4:2270-2282.
57. Sclafani A, Springer D. 1976. Dietary obesity in adult rats: Similarities to hypothalamic and human obesity syndromes. Physiol Behav 17:461-471.
58. Shabalina IG, Petrovic N, Kramarova TV, Hoeks J, Cannon B, Nedergaard J. 2006. UCP1 and defense against oxidative stress. 4-Hydroxy-2-nonenal effects on brown fat mitochondria are uncoupling protein 1-independent. J Biol Chem 281: 13882-13893.
59. Slater TF, Sawyer BC. 1971. The stimulatory effects of carbon tetrachloride on peroxidative reactions in rat liver fractions in vitro. Inhibitory effects of free-radical scavengers and other agents. Biochem J 123:823-828.
60. Terauchi Y, Takamoto I, Kubota N, Matsui J, Suzuki R, Komeda K, Hara A, Toyoda Y, MiwaI, AizawaS,Tsutsumi S, Tsubamoto Y, Hashimoto S, Eto K, Nakamura A, Noda M, Tobe K, Aburatani H, Nagai R, Kadowaki T. 2007. Glucokinase and IRS-2 are required for compensatory beta cell hyperplasia in response to high-fat diet-induced insulin resistance. J Clin Invest 117:246-257.
61. Thomas PS, Farquhar MN. 1978. Specific measurement of DNA in nuclei and nucleic acids using diaminobenzoic acid. Anal Biochem 89:35-44.
62. Valle A, Guevara R, Garcia-Palmer FJ, Roca P, Oliver J. 2007. Sexual dimorphism in liver mitochondrial oxidative capacity is conserved under caloric restriction conditions. Am J Physiol Cell Physiol 293:C1302-C1308.
63. Valle A, Santandreu FM, Garcia-Palmer FJ, Roca P, Oliver J. 2008. The serum levels of 17beta-estradiol, progesterone and triiodothyronine correlate with brown adipose tissue thermo-genic parameters during aging. Cell Physiol Biochem 22: 337-346.
64. Villena JA, Hock MB, Chang WY, Barcas JE, Giguere V, Kralli A. 2007. Orphan nuclear receptor estrogen-related receptor alpha is essential for adaptive thermogenesis. Proc Natl Acad Sci USA 104:1418-1423.
65. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerback S, Nuutila P. 2009. Functional brown adipose tissue in healthy adults. N Engl J Med 360:1518-1525.
66. Zingaretti MC, Crosta F, Vitali A, Guerrieri M, Frontini A, Cannon B, Nedergaard J, Cinti S. 2009. The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. Faseb J 23:3113-3120.