Expression of uncoupling protein 3 is upregulated in skeletal muscle during sepsis

American Journal of Physiology - Endocrinology and Metabolism

Volumn 285, Issue 3 48-3, 2003, Pages

  Sun, Xiaoyan ^a,b   Wray, Curtis ^a   Tian, Xintian ^a   Hasselgren, Per Olof ^c   Lu, James ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cachexia; Free fatty acids; Glucocorticoids

Indexed keywords

DEXAMETHASONE; FATTY ACID; GLUCOCORTICOID; LIPOPOLYSACCHARIDE; MIFEPRISTONE; UNCOUPLING PROTEIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CACHEXIA; CONTROLLED STUDY; DENERVATION; ENERGY BALANCE; MALE; MEDIATOR RELEASE; MUSCLE ATROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN RNA BINDING; RAT; RECEPTOR UPREGULATION; SEPSIS; SKELETAL MUSCLE; THERMOGENESIS;

EID: 0042967629     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.00446.2002     Document Type: Article

References (60)

1. Angerås U, Hall-Angerås M, Wagner KR, James H, Hasselgren PO, and Fischer JE. Tissue metabolite levels in different types of skeletal muscle during sepsis. Metabolism 40: 1147-1151, 1991.
2. Bagby GJ, Corll CB, and Martinez RR. Triacylglycerol kinetics in endotoxic rats with suppressed lipoprotein lipase activity. Am J Physiol Endocrinol Metab 253: E59-E64, 1987.
3. Baracos VE, DeVivo C, Hoyle DH, and Goldberg AL. Activation of the ATP-ubiquitin-proteasome pathway in skeletal muscle of cachectic rats bearing a hepatoma. Am J Physiol Endocrinol Metab 268: E996-E1006, 1995.
4. Baracos VE and Goldberg AL. Maintenance of normal length improves protein balance and energy status in isolated rat skeletal muscles. Am J Physiol Cell Physiol 251: C588-C596, 1986.
5. Boss O, Muzzin P, and Giacobino JP. The uncoupling proteins, a review. Eur J Endocrinol 139: 1-9, 1998.
6. Boss O, Samec S, Paoloni-Giacobino A, Rossier C, Dulloo A, Seydoux J, Muzzin P, and Giacobino JP. Uncoupling protein-3: a new member of the mitochondrial carrier family with tissue-specific expression. FEBS Lett 408: 39-42, 1997.
7. Cadenas S, Bukingham JA, Samec S, Seydoux J, Din N, Dulloo AG, and Brand MD. UCP2 and UCP3 rise in starved rat skeletal muscle but mitochondrial proton conductance is unchanged. FEBS Lett 462: 257-260, 1999.
8. Chaudry IH, Wichterman LA, and Baue AE. Effect of sepsis on tissue adenine nucleotide levels. Surgery 85: 205-211, 1979.
9. Chen WJ. Utilization of exogenous fat emulsion (Intralipid) in septic rats. J Parenter Enteral Nutr 8: 14-17, 1984.
10. Chomczynski P and Sacci N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
11. Clapham JC, Arch JR, Chapman H, Haynes A, Lister C, Moore GB, Piercy V, Carter SA, Lehner I, Smith SA, Beeley LJ, Godden RJ, Herrity N, Skehel M, Changani KK, Hockings PD, Reid DG, Squires SM, Hatcher J, Trail B, Latcham J, Rastan S, Harper AJ, Cadenas S, Buckingham JA, Brand MD, and Abuin A. Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature 406: 415-418, 2000.
12. Cortright RN, Zheng D, Jones JP, Fluckey JD, DiCarlo SE, Grujic D, Lowell BB, and Dohm GL. Regulation of skeletal muscle UCP-2 and UCP-3 gene expression by exercise and denervation. Am J Physiol Endocrinol Metab 276: E217-E221, 1999.
13. Denjean F, Desplanches D, Lachuer J, Cohen-Adad F, Mayet MH, and Duchamp C. Muscle-specific up-regulation of rat UCP3 mRNA expression by long-term hindlimb unloading. Biochem Biophys Res Commun 266: 518-522, 1999.
14. Dux L. Muscle relaxation and sarcoplasmic reticulum function in different muscle types. Rev Physiol Biochem Pharmacol 122: 69-147, 1993.
15. Fang CH, Sun X, Li BG, Fischer DR, Pritts TA, Penner G, and Hasselgren PO. Burn injuries in rats upregulate the gene expression of the ubiquitin-conjugating enzyme E2(14k) in skeletal muscle. J Burn Care Rehabil 21: 528-534, 2000.
16. Fischer D, Sun X, Gang G, Pritts T, and Hasselgren PO. The gene expression of ubiquitin ligase E3alpha is upregulated in skeletal muscle during sepsis in rats - potential role of glucocorticoids. Biochem Biophys Res Commun 267: 504-508, 2000.
17. Gong DW, He Y, Karas M, and Reitman M. Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, beta3-adrenergic agonists, and leptin. J Biol Chem 272: 24129-24132, 1997.
18. Hall-Angerås M, Angerås U, Zamir O, Hasselgren PO, and Fischer JE. Effect of the glucocorticoid receptor antagonist RU 38486 on muscle protein breakdown in sepsis. Surgery 109: 468-473, 1991.
19. Hasselgren PO and Fischer JE. Muscle cachexia: current concepts of intracellular mechanisms and molecular regulation. Ann Surg 233: 9-17, 2001.
20. Hasselgren PO, Hall-Angerås M, Angerås U, Benson DW, James JH, and Fischer JE. Regulation of total and myofibrillar protein breakdown in rat extensor digitorum longus and soleus muscle incubated flaccid or at resting length. Biochem J 267: 37-44, 1990.
21. Hasselgren PO, James JH, Benson DW, Hall-Angerås M, Angerås U, Hiyama DT, Li S, and Fischer JE. Total and myofibrillar protein breakdown in different types of rat skeletal muscle: effects of sepsis and regulation by insulin. Metabolism 38: 634-640, 1989.
22. Hesselink MKC, Keizer HA, Borghouts LB, Schaart G, Kornips CFP, Slieker LJ, Sloop KW, Saris WHM, and Schrauwen P. Protein expression of UCP3 differs between human type 1, type 2a, and type 2b fibers. FASEB J 15: 1071-1073, 2001.
23. Hildebrandt AL and Neufer PD. Exercise attenuates the fasting-induced transcriptional activation of metabolic genes in skeletal muscle. Am J Physiol Endocrinol Metab 278: E1078-E1086, 2000.
24. Hobler SC, Wang JJ, Williams AB, Melandri F, Sun X, Fischer JE, and Hasselgren PO. Sepsis is associated with increased ubiquitin-conjugating enzyme E214k mRNA in skeletal muscle. Am J Physiol Regul Integr Comp Physiol 276: R468-R473, 1999.
25. Huppertz C, Fischer BM, Kim YB, Kotani K, Vidal-Puig A, Slieker LJ, Sloop KW, Lowell BB, and Kahn BB. Uncoupling protein 3 (UCP3) stimulates glucose uptake in muscle cells through a phosphoinositide 3-kinase-dependent mechanism. J Biol Chem 276: 12520-12529, 2001.
26. Hwang CS and Lane MD. Up-regulation of uncoupling protein-3 by fatty acid in C2C12 myotubes. Biochem Biophys Res Commun 258: 464-469, 1999.
27. Idstrom JP, Soussi B, Elander A, and Bylund-Fellenius AC. Purine metabolism after in vivo ischemia and reperfusion in rat skeletal muscle. Am J Physiol Heart Circ Physiol 258: H1668-H1673, 1990.
28. James HJ, Fang CH, Schrantz SJ, Hasselgren PO, Paul RJ, and Fischer JE. Linkage of aerobic glycolysis to sodium-potassium transport in rat skeletal muscle. Implications for increased muscle lactate production in sepsis. J Clin Invest 98: 2388-2397, 1996.
29. James HJ, Hasselgren PO, King JK, James LE, and Fischer JE. Intracellular glutamine concentration does not decrease in all muscles during sepsis. J Surg Res 54: 558-564, 1993.
30. Jimenez M, Yvon C, Lehr L, Leger B, Keller P, Russell A, Kuhne F, Flandin P, Giacobino JP, and Muzzin P. Expression of uncoupling protein-3 in subsarcolemmal and intermyofibrillar mitochondria of various mouse muscle types and its modulation by fasting. Eur J Biochem 269: 2878-2884, 2002.
31. Jucker BM, Ren J, Dufou S, Cao X, Previs SF, Cadman KS, and Shulman GI. 13C/31P NMR assessment of mitochondrial energy coupling in skeletal muscle of awake fed and fasted rats. Relationship with uncoupling protein 3 expression. J Biol Chem 275: 39279-39286, 2000.
32. Kelly FJ and Goldspink DF. The differing responses of four muscle types to dexamethasone treatment in the rat. Biochem J 208: 147-151, 1982.
33. Konagaya M, Bernard PA, and Max SR. Blockade of glucocorticoid receptor binding and inhibition of dexamethasone-induced muscle atrophy in the rat by RU 38486, a potent glucocorticoid antagonist. Endocrinology 119: 375-380, 1986.
34. Lanza-Jacoby S and Tabares A. Triglyceride kinetics, tissue lipoprotein lipase, and liver lipogenesis in septic rats. Am J Physiol Endocrinol Metab 258: E678-E685, 1990.
35. Lin E, Lowry SF, and Calvano SE. Endocrine and metabolic responses to injury. In: Principles of Surgery (7th ed.), edited by Schwartz SI, Shires GT, Spencer FC, Daly JM, Fischer JE, and Galloway AC. New York: McGraw-Hill, 1999, p. 3-51.
36. Linz DN, Garcia VF, Arya G, Hug G, Tombragel E, Landrigan E, Chuck G, Tsoras M, Ryan M, and Ziegler MM. Weanling and adult rats differ in fatty acid and carnitine metabolism during sepsis. J Pediatr Surg 30: 959-966, 1995.
37. Llovera M, Garcia-Martinez C, Agell N, Marzabal M, Lopez-Soriano FJ, and Argiles JM. Ubiquitin gene expression is increased in skeletal muscle of tumour-bearing rats. FEBS Lett 338: 311-318, 1994.
38. Matsuda J, Hosoda K, Itoh H, Son C, Doi K, Tanaka T, Fukunaga Y, Inone G, Nishimura H, Yoshimasa Y, Yamori Y, and Nakao K. Cloning of rat uncoupling protein-3 and uncoupling protein-2 cDNAs: their gene expression in rats fed high-fat diet. FEBS Lett 418: 200-204, 1997.
39. McGrath JA and Goldspink DF. Glucocorticoid action on protein synthesis and protein breakdown in isolated skeletal muscles. Biochem J 206: 641-645, 1982.
40. Medina R, Wing SS, Haas A, and Goldberg AL. Activation of the ubiquitin-ATP-dependent proteolytic system in skeletal muscle during fasting and denervation atrophy. Biomed Biophys Acta 50: 347-356, 1991.
41. Nagase I, Yoshida S, Canas X, Irie Y, Kimura K, Yoshida T, and Saito M. Up-regulation of uncoupling protein 3 by thyroid hormone, peroxisome proliferator-activated receptor ligands and 9-cis retinoic acid in L6 myotubes. FEBS Lett 461: 319-322, 1999.
42. Ohtsuka A, Tanaka H, Hizaki K, and Hayashi K. Chick skeletal muscle proteolysis in vitro increased by corticosterone. Biosci Biotechnol Biochem 62: 1781-1783, 1998.
43. Rannels SR and Jefferson LS. Effects of glucocorticoids on muscle protein turnover in perfused rat hemicorpus. Am J Physiol Endocrinol Metab 238: E564-E572, 1980.
44. Sabina RL, Kernstine KH, Boyd RL, Holmes EW, and Swain JL. Metabolism of 5-amino-4-imidazolecarboxamide riboside in cardiac and skeletal muscle. Effects on purine nucleotide synthesis. J Biol Chem 257: 10178-10183, 1982.
45. Samec S, Seydoux J, and Dulloo AG. Role of UCP homologues in skeletal muscles and brown adipose tissue: mediators of thermogenesis or regulators of lipids as fuel substrate? FASEB J 12: 715-724, 1998.
46. Sanchis D, Busquets S, Alvarez B, Ricquier D, Lopez-Soriano FJ, and Argiles JM. Skeletal muscle UCP2 and UCP3 gene expression in a rat cancer cachexia model. FEBS Lett 436: 415-418, 1998.
47. Sayeed MM. Alterations in calcium signaling and cellular responses in septic injury. New Horiz 4: 72-86, 1996.
48. Schrauwen P, Schaart G, Saris WHM, Slieker LJ, Glatz JFC, Vidal H, and Black EE. The effect of weight reduction on skeletal muscle UCP2 and UCP3 mRNA expression and UCP3 protein content in Type II diabetic subjects. Diabetologia 43: 1408-1416, 2000.
49. Simonsen L, Stallknecht B, and Bülow J. Contribution of skeletal muscle and adipose tissue to adrenaline-induced thermogenesis in man. Int J Obes 17: 547-551, 1993.
50. Solanes G, Vidal-Puig A, Grujic D, Flier JS, and Lowell BB. The human uncoupling protein-3 gene. Genomic structure, chromosomal localization, and genetic basis for short and long form transcripts. J Biol Chem 272: 25433-25436, 1997.
51. Son C, Hosoda K, Matsuda J, Fujikura J, Yonemitsu S, Iwakura H, Masuxaki H, Ogawa Y, Hayashi T, Itoh H, Nishimura H, Inoue G, Yoshimasa Y, Yamori Y, and Nakao K. Up-regulation of uncoupling protein 3 gene expression by fatty acids and agonists for PPARs in L6 myotubes. Endocrinology 142: 4189-4194, 2001.
52. Sun X, Fischer DR, Pritts TA, Wray CJ, and Hasselgren PO. Expression and binding activity of the glucocorticoid receptor are upregulated in septic muscle. Am J Physiol Regul Integr Comp Physiol 282: R509-R518, 2002.
53. Tiao G, Fagan J, Roegner V, Lieberman M, Wang JJ, Fischer JE, and Hasselgren PO. Energy-ubiquitin-dependent muscle proteolysis during sepsis in rats is regulated by glucocorticoids. J Clin Invest 97: 339-348, 1996.
54. Tiao G, Fagan JM, Samuels N, James JH, Hudson K, Lieberman M, Fischer JE, and Hasselgren PO. Sepsis stimulates nonlysosomal, energy-dependent proteolysis and increases ubiquitin mRNA levels in rat skeletal muscle. J Clin Invest 94: 2255-2264, 1994.
55. Weigle DS, Selfridge LE, Schwartz MW, Seeley RJ, Cummings DE, Havel PJ, Kuijper JL, and BertrandelRio H. Elevated free fatty acids induce uncoupling protein 3 expression in muscle: a potential explanation for the effect of fasting. Diabetes 47: 298-302, 1998.
56. Wicklmayr M, Rett K, Schwiegelshohn B, Wolfram G, Hailer S, and Dietze G. Inhibition of muscular amino acid release by lipid infusion in man. Eur J Clin Invest 17: 301-305, 1987.
57. Wing SS and Goldberg AL. Glucocorticoids activate the ATP-ubiquitin-dependent proteolytic system in skeletal muscle during fasting. Am J Physiol Endocrinol Metab 264: E668-E676, 1993.
58. Yoshitomi H, Yamazaki K, and Tanaka L. Mechanism of ubiquitous expression of mouse uncoupling protein 2 mRNA: control by cis-acting DNA element in 5′-flanking region. Biochem J 340: 397-404, 1999.
59. Yu X, Barger JL, Boyer BB, Brand MD, Pan G, and Adams SH. Impact of endotoxin on UCP homolog mRNA abundance, thermoregulation, and mitochondrial proton leak kinetics. Am J Physiol Endocrinol Metab 279: E433-E446, 2000.
60. Zamir O, Hasselgren PO, Frederick JA, and Fischer JE. Is the metabolic response to sepsis in skeletal muscle different in infants and adults? An experimental study in rats. J Pediatr Surg 27: 1399-1403, 1992.