Severe Burn Injury Induces Thermogenically Functional Mitochondria in Murine White Adipose Tissue

Shock

Volumn 44, Issue 3, 2015, Pages 258-264

  Porter, Craig ^a,b   Herndon, David N ^a,b   Bhattarai, Nisha ^a,b   Ogunbileje, John O ^a,b   Szczesny, Bartosz ^c   Szabo, Csaba ^c   Toliver Kinsky, Tracy ^c   Sidossis, Labros S ^a,b  

^a SHRINERS HOSPITALS FOR CHILDREN   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^c Departments of Anesthesiology   (United States)

Author keywords

Adipose tissue; burn injury; hypermetabolism; mitochondria; thermogenesis

Indexed keywords

CITRATE SYNTHASE; FAT DROPLET; UNCOUPLING PROTEIN 1; ION CHANNEL; MITOCHONDRIAL PROTEIN; UCP1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY SURFACE; BURN; CONTROLLED STUDY; ENZYME ACTIVITY; HYPERMETABOLISM; IMMUNOHISTOCHEMISTRY; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MORPHOLOGY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RESPIROMETRY; SCALD; SKINFOLD THICKNESS; THERMOGENESIS; WHITE ADIPOSE TISSUE; ANIMAL; BAGG ALBINO MOUSE; COMPLICATION; METABOLISM; MITOCHONDRIAL DISEASES; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADIPOSE TISSUE, WHITE; ANIMALS; BURNS; CITRATE (SI)-SYNTHASE; ION CHANNELS; MALE; MICE, INBRED BALB C; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MITOCHONDRIAL PROTEINS; THERMOGENESIS; UNCOUPLING PROTEIN 1;

EID: 84938643185     PISSN: 10732322     EISSN: 15400514     Source Type: Journal    
DOI: 10.1097/SHK.0000000000000410     Document Type: Article

References (45)

1. Goran MI, Peters EJ, Herndon DN, Wolfe RR. Total energy expenditure in burned children using the doubly labeled water technique. Am J Physiol 259: 576-585, 1990.
2. Wilmore D, Long J, Mason AJ, Skreen RW, Pruitt BJ Jr. Catecholamines: mediator of the hypermetabolic response to thermal injury. Ann Surg 180: 653-669, 1974.
3. Jeschke MG, Gauglitz GG, Kulp GA, Finnerty CC, Williams FN, Kraft R, Suman OE, Mlcak RP, Herndon DN. Long-term persistance of the pathophysiologic response to severe burn injury. PLoS One 6: e21245, 2011.
4. Yu YM, Tompkins RG, Ryan CM, Young VR. The metabolic basis of the increase of the increase in energy expenditure in severely burned patients. JPEN J Parenter Enteral Nutr 23: 160-168, 1999.
5. Cousin B, Cinti S, Morroni M, Raimbault S, Ricquier D, Pénicaud L, Casteilla L. Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization. J Cell Sci 103: 931-942, 1992.
6. Young P, Arch J, Ashwell M. Brown adipose tissue in the parametrial fat pad of the mouse. FEBS Lett 167: 10-14, 1984.
7. Porter C, Malagaris I, Sidossis L. Is the heat surrounding adipose tissue mitochondria warranted? Curr Opin Clin Nutr Metab Care 17: 503-508, 2014.
8. Shabalina I, Petrovic N, de Jong J, Kalinovich A, Cannon B, Nedergaard J. UCP1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Rep 5: 1196-1203, 2013.
9. Finnerty CC, Herndon DN, Przkora R, Pereira CT, Oliveira HM, Queiroz DM, Rocha AM, Jeschke MG. Cytokine expression profile over time in severely burned pediatric patients. Shock 26: 13-19, 2006.
10. Gauglitz G, Song J, Herndon D, Finnerty C, Boehning D, Barral J, Jeschke M. Characterization of the inflammatory response during acute and post-acute phases after severe burn. Shock 30: 503-507, 2008.
11. Jeschke MG, Chinkes DL, Finnerty CC, Kulp G, Suman OE, Norbury WB, Branski LK, Gauglitz GG, Mlcak RP, Herndon DN. Pathophysiologic response to severe burn injury. Ann Surg 248: 387-401, 2008.
12. Norbury WB, Hserndon DN, Branski LK, Chinkes DL, Jeschke MG. Urinary cortisol and catecholamine excretion after burn injury in children. J Clin Endocrinol Metab 93: 1270-1275, 2008.
13. Kulp GA, Herndon DN, Lee JO, Suman OE, Jeschke MG. Extent and magnitude of catecholamine surge in pediatric burned patients. Shock 33: 369-374, 2010.
14. Caldwell FJ, Bowser B, Crabtree J. The effect of occlusive dressings on the energy metabolism of severely burned children. Ann Surg 193: 579-591, 1981.
15. Caldwell FJ, Wallace B, Cone J, Manuel L. Control of the hypermetabolic response to burn injury using environmental factors. Ann Surg 215: 485-490, 1992.
16. Carter E, Bonab A, Hamrahi V, Pitman J, Winter D, Macintosh L, Cyr E, Paul K, Yerxa J, Jung W. 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.
17. Carter E, Winter D, Tolman C, Paul K, Hamrahi V, Tompkins R, Fischman A. Combination of radiation and burn injury alters [18F] 2-fluoro-2-deoxy-D-glucose uptake in mice. J Burn Care Res 33: 723-730, 2012.
18. Yo K, Yu Y, Zhao G, Bonab A, Aikawa N, Tompkins R, Fischman A. Brown adipose tissue and its modulation by a mitochondria-targeted peptide in rat burn injury induced hypermetabolism. Am J Physiol Endocrinol Metab 304: 331-341, 2013.
19. Bohannon J, Cui W, Sherwood E, Toliver-Kinsky T. Dendritic cell modification of neutrophil responses to infection after burn injury. J Immunol 185: 2847-2853, 2010.
20. Toliver-Kinsky T, Lin C, Herndon D, Sherwood E. Stimulation of hematopoiesis by the Fms-like tyrosine kinase 3 ligand restores bacterial induction of TH1 cytokines in thermally injured mice. Infect Immun 71: 3058-3067, 2003.
21. Toliver-Kinsky T, Varma T, Lin C, Herndon D, Sherwood E. Interferon-gamma production is suppressed in thermally injured mice: decreased production of regulatory cytokines and corresponding receptors. Shock 18: 322-330, 2002.
22. Gnaiger E. Capacity of oxidative phosphorylation in human skeletal muscle: new perspectives of mitochondrial physiology. Int J Biochem Cell Biol 41: 1837-1845, 2009.
23. Gnaiger E. Mitochondrial pathways and respiratory control. In: An Introduction to OXPHOS Analysis. OROBOROS MiPNet Publications. 4th ed. (Mitochondr Physiol Network 19.12). Innsbruck, Austria: OROBOROS MiPNet Publications, 2014.
24. Pesta D, Gnaiger E. High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle. Methods Mol Biol 810: 25-58, 2012.
25. Cannon B, Nedergaard J. Studies of thermogenesis and mitochondrial function in adipose tissues. Methods Mol Biol 456: 109-121, 2008.
26. Cannon B, Nedergaard J. Respiratory and thermogenic capacities of cells and mitochondria from brown and white adipose tissue. Methods Mol Biol 155: 295-303, 2001.
27. Cannon B, Nedergaard J. Nonshivering thermogenesis and its adequate measurement in metabolic studies. J Exp Biol 214: 242-253, 2011.
28. Matthias A, Ohlson K, Fredriksson J, Jacobsson A, Nedergaard J, Cannon B. Thermogenic responses in brown fat cells are fully UCP1-dependent. J Biol Chem 275: 25073-25081, 2000.
29. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 84: 277-359, 2004.
30. Nedergaard J, Matthias A, Golozoubova V, Jacobsson A, Cannon B. UCP1: the original uncoupling protein-and perhaps the only one? J Bioenerg Biomembr 31: 475-491, 1999.
31. Rolfe D, Brown G. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77: 731-758, 1997.
32. Larsen S, Nielsen J, Hansen CN, Nielsen LB, Wibrand F, Stride N, Schroder HD, Boushel R, Helge JW, Dela F. Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol 590: 3349-3360, 2012.
33. Yin X, Lanza I, Swain J, Sarr M, Nair K, Jensen M. Adipocyte mitochondrial function is reduced in human obesity independent of fat cell size. J Clin Endocrinol Metab 99: 209-216, 2014.
34. Srere P. Citrate synthase. Methods Enzymol 13: 3-11, 1969.
35. Hart DW, Wolf SE, Chinkes DL, Gore DC, Mlcak RP, Beauford RB, Obeng MK, Lal S, Gold WF, Wolfe RR. Determinants of skeletal muscle catabolism after severe burn. Ann Surg 232: 455-465, 2000.
36. 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.
37. Herndon DN, Nguyen TT, Wolfe RR, Maggi SP, Biolo G, Muller M, Barrow RE. Lipolysis in burned patients is stimulated by the beta 2-receptor for catecholamines. Arch Surg 129: 1301-1304, 1994.
38. Herndon DN, Rodriguez NA, Diaz EC, Hegde S, Jennings K, Mlcak RP, Suri JS, Lee JO, Williams FN, Meyer W. Long-term propranolol use in severely burned pediatric patients: a randomized controlled study. Ann Surg 256: 402-411, 2012.
39. 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.
40. Young P, Wilson S, Arch JR. Prolonged beta-adrenoceptor stimulation increases the amount of GDP-binding protein in brown adipose tissue mitochondria. Life Sci 34: 1111-1117, 1984.
41. Boushel R, Gnaiger E, Schjerling P, Skovbro M, Kraunsøe R, Dela F. Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50: 790-796, 2007.
42. Porter C, Herndon DN, Borscheim E, Chao T, Reidy PT, Borack MS, Rasmussen BB, Chondonikola M, Saraf MK, Sidossis LS. Uncoupled skeletal muscle mitochondria contribute to hypermetabolism in severely burned adults. Am J Physiol Endocrinol Metab 307: 462-467, 2014.
43. Rabøl R, Larsen S, Højberg PM, Almdal T, Boushel R, Haugaard SB, Andersen JL, Madsbad S, Dela F. Regional anatomic differences in skeletal muscle mitochondrial respiration in type 2 diabetes and obesity. J Clin Endocrinol Metab 95: 857-863, 2010.
44. Short KR, Bigelow ML, Kahl J, Singh R, Coenen-Schimke J, Raghavakaimal S, Nair KS. Decline in skeletal muscle mitochondrial function with aging in humans. Proc Natl Acad Sci USA 102: 5618-5623, 2005.
45. Nedergaard J, Cannon B. UCP1 mRNA does not produce heat. Biochim Biophys Acta 1831: 943-949, 2013.