Brown adipose tissue and its modulation by a mitochondria-targeted peptide in rat burn injury-induced hypermetabolism

American Journal of Physiology - Endocrinology and Metabolism

Volumn 304, Issue 4, 2013, Pages

  Yo, Kikuo ^a,b   Yu, Yong Ming ^a,b   Zhao, Gaofeng ^a,b   Bonab, Ali A ^a,b   Aikawa, Naoki ^c   Tompkins, Ronald G ^a,b   Fischman, Alan J ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c KEIO UNIVERSITY   (Japan)

Author keywords

Brown adipose tissue; Burn injury induced hypermetabolism; Mitochondria dysfunction

Indexed keywords

UNCOUPLING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; BROWN ADIPOSE TISSUE; BURN; BURN INJURY INDUCED HYPERMETABOLISM; CONTROLLED STUDY; ENERGY EXPENDITURE; HYPERMETABOLISM; MALE; MITOCHONDRION; MORPHOLOGICAL TRAIT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RESTING METABOLIC RATE; SHAM PROCEDURE; SPRAGUE DAWLEY RAT;

ADIPOSE TISSUE, BROWN; ANIMALS; BURNS; DOWN-REGULATION; ENERGY METABOLISM; FREE RADICAL SCAVENGERS; ION CHANNELS; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL TURNOVER; MOLECULAR TARGETED THERAPY; OLIGOPEPTIDES; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SCAPULA; SPECIFIC PATHOGEN-FREE ORGANISMS; UP-REGULATION;

EID: 84874036488     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00098.2012     Document Type: Article

References (47)

1. Astrup A, Bülow J, Madsen J, Christensen NJ. Contribution of BAT and skeletal muscle to thermogenesis induced by ephedrine in man. Am J Physiol Endocrinol Metab 248: E507-E515, 1985.
2. Beffa DC, Carter EA, Lu XM, Yu YM, Prelack K, Sheridan RL, Young VR, Fischman AJ, Tompkins RG. Negative chemical ionization gas chromatography/mass spectrometry to quantify urinary 3-methylhistidine: application to burn injury. Anal Biochem 355: 95-101, 2006.
3. Bonab AA, Carter EA, Paul K, Kaneki M, Yu YM, Tompkins RG, Fischman AJ. Effect of simvastatin on burn-induced alterations in tissue specific glucose metabolism: implications for burn associated insulin resistance. Int J Mol Med 26: 311-316, 2010.
4. Carter EA, Bonab AA, Hamrahi V, Pitman J, Winter D, Macintosh LJ, Cyr EM, Paul K, Yerxa J, Jung W, Tompkins RG, Fischman AJ. Effects of burn injury, cold stress and cutaneous wound injury on the morphology and energy metabolism of murine brown adipose tissue (BAT) in vivo. Life Sci 89: 78-85, 2011.
5. Carter EA, Bonab AA, Paul K, Yerxa J, Tompkins RG, Fischman AJ. Association of heat production with 18F-FDG accumulation in murine brown adipose tissue after stress. J Nucl Med 52: 1616-1620, 2011.
6. Carter EA, Tompkins RG, Babich JW, Correia JA, Fischman AJ. Decreased cerebral glucose utilization in rats during the ebb phase of thermal injury. J Trauma 40: 930-935, 1996.
7. Carter EA, Tompkins RG, Hsu H, Christian B, Alpert NM, Weise S, Fischman AJ. Metabolic alterations in muscle of thermally injured rabbits, measured by positron emission tomography. Life Sci 61: 39-44, 1997.
8. Chang DW, DeSanti L, Demling RH. Anticatabolic and anabolic strategies in critical illness: a review of current treatment modalities. Shock 10: 155-160, 1998.
9. Cho J, Won K, Wu D, Soong Y, Liu S, Szeto HH, Hong MK. Potent mitochondria-targeted peptides reduce myocardial infarction in rats. Coron Artery Dis 18: 215-220, 2007.
10. Cho S, Szeto HH, Kim E, Kim H, Tolhurst AT, Pinto JT. A novel cell-permeable antioxidant peptide, SS31, attenuates ischemic brain injury by down-regulating CD36. J Biol Chem 282: 4634-4642, 2007.
11. Crisan M, Casteilla L, Lehr L, Carmona M, Paoloni-Giacobino A, Yap S, Sun B, Leger B, Logar A, Penicaud L, Schrauwen P, Cameron-Smith D, Russell AP, Peault B, Giacobino JP. A reservoir of brown adipocyte progenitors in human skeletal muscle. Stem Cells 26: 2425-2433, 2008.
12. Cypess AM, Kahn CR. Brown fat as a therapy for obesity and diabetes. Curr Opin Endocrinol Diabetes Obes 17: 143-149, 2010.
13. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng YH, Doria A, Kolodny GM, Kahn CR. Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360: 1509-1517, 2009.
14. Echtay KS. Mitochondrial uncoupling proteins-what is their physiological role? Free Radic Biol Med 43: 1351-1371, 2007.
15. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, Clapham JC, Brand MD. Superoxide activates mitochondrial uncoupling proteins. Nature 415: 96-99, 2002.
16. Fruhbeck G, Becerril S, Sainz N, Garrastachu P, Garcia-Velloso MJ. BAT: a new target for human obesity? Trends Pharmacol Sci 30: 387-396, 2009.
17. Golozoubova V, Cannon B, Nedergaard J. UCP1 is essential for adaptive adrenergic nonshivering thermogenesis. Am J Physiol Endocrinol Metab 291: E350-E357, 2006.
18. Herndon DN, Hart DW, Wolf SE, Chinkes DL, Wolfe RR. Reversal of catabolism by beta-blockade after severe burns. N Engl J Med 345: 1223-1229, 2001.
19. Herndon DN, Tompkins RG. Support of the metabolic response to burn injury. Lancet 363: 1895-1902, 2004.
20. Kelso GF, Porteous CM, Coulter CV, Hughes G, Porteous WK, Ledgerwood EC, Smith RA, Murphy MP. Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties. J Biol Chem 276: 4588-4596, 2001.
21. Kopecky J, Clarke G, Enerback S, Spiegelman B, Kozak LP. Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. J Clin Invest 96: 2914-2923, 1995.
22. Kopecky J, Hodny Z, Rossmeisl M, Syrovy I, Kozak LP. Reduction of dietary obesity in aP2-Ucp transgenic mice: physiology and adipose tissue distribution. Am J Physiol Endocrinol Metab 270: E768-E775, 1996.
23. Kozak LP. and Anunciado-Koza R. UCP1: its involvement and utility in obesity. Int J Obes (Lond) 32, Suppl 7: S32-S38, 2008.
24. Lidell ME, Enerback S. Brown adipose tissue-a new role in humans? Nat Rev Endocrinol 6: 319-325, 2010.
25. Murphy MP. Selective targeting of bioactive compounds to mitochondria. Trends Biotechnol 15: 326-330, 1997.
26. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 293: E444-E452, 2007.
27. Nedergaard J, Cannon B. The changed metabolic world with human brown adipose tissue: therapeutic visions. Cell Metab 11: 268-272, 2010.
28. Nedergaard J, Golozoubova V, Matthias A, Asadi A, Jacobsson A, Cannon B. UCP1: the only protein able to mediate adaptive non-shivering thermogenesis and metabolic inefficiency. Biochim Biophys Acta 1504: 82-106, 2001.
29. Parihar A, Parihar MS, Milner S, Bhat S. Oxidative stress and antioxidative mobilization in burn injury. Burns 34: 6-17, 2008.
30. Parysow O, Mollerach AM, Jager V, Racioppi S, San Roman J, Gerbaudo VH. Low-dose oral propranolol could reduce brown adipose tissue F-18 FDG uptake in patients undergoing PET scans. Clin Nucl Med 32: 351-357, 2007.
31. Petri S, Kiaei M, Damiano M, Hiller A, Wille E, Manfredi G, Calingasan NY, Szeto HH, Beal MF. Cell-permeable peptide antioxidants as a novel therapeutic approach in a mouse model of amyotrophic lateral sclerosis. J Neurochem 98: 1141-1148, 2006.
32. Ruan X, Li Z, Zhang Y, Yang L, Pan Y, Wang Z, Feng GS, Chen Y. Apolipoprotein A-I possesses an anti-obesity effect associated with increase of energy expenditure and upregulation of UCP1 in brown fat. J Cell Mol Med 15: 763-772, 2011.
33. 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. High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58: 1526-1531, 2009.
34. Simonsen L, Stallknecht B, Bulow J. Contribution of skeletal muscle and adipose tissue to adrenaline-induced thermogenesis in man. Int J Obes Relat Metab Disord 17, Suppl 3: S47-S51; discussion S68, 1993.
35. Smith RA, Porteous CM, Coulter CV, Murphy MP. Selective targeting of an antioxidant to mitochondria. Eur J Biochem 263: 709-716, 1999.
36. Soderlund V, Larsson SA, Jacobsson H. Reduction of FDG uptake in brown adipose tissue in clinical patients by a single dose of propranolol. Eur J Nucl Med Mol Imaging 34: 1018-1022, 2007.
37. Szeto HH. Mitochondria-targeted cytoprotective peptides for ischemiareperfusion injury. Antioxid Redox Signal 10: 601-619, 2008.
38. Tai C, Chatziioannou A, Siegel S, Young J, Newport D, Goble RN, Nutt RE, Cherry SR. Performance evaluation of the microPET P4: a PET system dedicated to animal imaging. Phys Med Biol 46: 1845-1862, 2001.
39. Thomas DA, Stauffer C, Zhao K, Yang H, Sharma VK, Szeto HH, Suthanthiran M. Mitochondrial targeting with antioxidant peptide SS-31 prevents mitochondrial depolarization, reduces islet cell apoptosis, increases islet cell yield, and improves posttransplantation function. J Am Soc Nephrol 18: 213-222, 2007.
40. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P, Teule GJ. Cold-activated brown adipose tissue in healthy men. N Engl J Med 360: 1500-1508, 2009.
41. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerback S, Nuutila P. Functional brown adipose tissue in healthy adults. N Engl J Med 360: 1518-1525, 2009.
42. Wijers SL, Schrauwen P, Saris WH, van Marken Lichtenbelt WD. Human skeletal muscle mitochondrial uncoupling is associated with cold induced adaptive thermogenesis. PLoS One 3: e1777, 2008.
43. Yu YM, Tompkins RG, Ryan CM, Young VR. The metabolic basis of the increase of the increase in energy expenditure in severely burned patients. J Parenter Enteral Nutr 23: 160-168, 1999.
44. Zang Q, Maass DL, White J, Horton JW. Cardiac mitochondrial damage and loss of ROS defense after burn injury: the beneficial effects of antioxidant therapy. J Appl Physiol 102: 103-112, 2007.
45. Zhang Q, Ma B, Fischman AJ, Tompkins RG, Carter EA. Increased uncoupling protein 1 mRNA expression in mice brown adipose tissue after burn injury. J Burn Care Res 29: 358-362, 2008.
46. Zhao K, Luo G, Giannelli S, Szeto HH. Mitochondria-targeted peptide prevents mitochondrial depolarization and apoptosis induced by tert-butyl hydroperoxide in neuronal cell lines. Biochem Pharmacol 70: 1796-1806, 2005.
47. Zhao K, Zhao GM, Wu D, Soong Y, Birk AV, Schiller PW, Szeto HH. Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury. J Biol Chem 279: 34682-34690, 2004.