Increased uncoupling protein 3 content does not affect mitochondrial function in human skeletal muscle in vivo

Journal of Clinical Investigation

Volumn 111, Issue 4, 2003, Pages 479-486

  Hesselink, Matthijs K C ^a   Greenhaff, Paul L ^b   Constantin Teodosiu, Dimitru ^b   Hultman, Eric ^c   Saris, Wim H M ^a   Nieuwlaat, Robby ^a   Schaart, Gert ^a   Kornips, Esther ^a   Schrauwen, Patrick ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b QUEEN S MEDICAL CENTRE   (United Kingdom)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCARNITINE; CREATINE; CREATINE PHOSPHATE; LACTIC ACID; UNCOUPLING PROTEIN 3;

ADULT; ANOXIA; ARTICLE; DIET; HUMAN; HUMAN EXPERIMENT; IN VIVO STUDY; LIMB BLOOD FLOW; LIPID DIET; LOW FAT DIET; MALE; MITOCHONDRIAL RESPIRATION; MUSCLE CONTRACTION; NORMAL HUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; SKELETAL MUSCLE;

EID: 0037327114     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI16653     Document Type: Article

References (52)

1. Boss, O., et al. 1997. Uncoupling protein-3: a new member of the mirochondrial carrier family with tissue-specific expression. FEBS Lett. 408:39-42.
2. Ricquier, D., and Bouillaud, F. 2000. The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem. J. 345:161-179.
3. Bouchard, C., Perusse, L., Chagnon, Y.C., Warden, C., and Ricquier, D. 1997. Linkage between markers in the vicinity of the uncoupling protein 2 gene and resting metabolic rate in humans. Hum. Mol. Genet. 6:1887-1889.
4. Schrauwen, P., Xia, J., Bogardus, C., Pratley, R.E., and Ravussin, E. 1999. Skeletal muscle uncoupling protein 3 expression is a determinant of energy expenditure in Pima Indians. Diabetes. 48:146-149.
5. Stuart, J.A., Harper, J.A., Brindle, K.M., Jekabsons, M.B., and Brand, M.D. 2001. A mitochondrial uncoupling artifact can be caused by expression of uncoupling protein 1 in yeast. Biochem. J. 356:779-789.
6. Cadenas, S., et al. 2002. The basal proton conductance of skeletal muscle mitochondria from transgenic mice overexpressing or lacking uncoupling protein-3. J. Biol. Chem. 277:2773-2778.
7. Harper, J.A., et al. 2002. Artifactual uncoupling by uncoupling protein 3 in yeast mitochondria at the concentrations found in mouse and rat skeletal-muscle mitochondria. Biochem. J. 361:49-56.
8. Gong, D.W., He, Y., Karas, M., and Reitman, M. 1997. Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, β3-adrenergic agonists, and leptin. J. Biol. Chem. 272:24129-24132.
9. Zhang, C.Y., Hagen, T., Mootha, V.K., Slieker, L.J., and Lowell, B.B. 1999. Assessment of uncoupling activity of uncoupling protein 3 using a yeast heterologous expression system. FEBS Lett. 449:129-134.
10. Clapham, J.C., et al. 2000. Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature. 406:415-418.
11. Vidal-Puig, A.J., et al. 2000. Energy metabolism in uncoupling protein 3 gene knockout mice. J. Biol. Chem. 275:16258-16266.
12. Gong, D.W., et al. 2000. Lack of obesity and normal response to fasting and thyroid hormone in mice lacking uncoupling protein-3. J. Biol. Chem. 275:16251-16257.
13. Cline, G.W., et al. 2001. In vivo effects of uncoupling protein-3 gene disruption on mitochondrial energy metabolism. J. Biol. Chem. 276:20240-20244.
14. Cadenas, S., et al. 1999. UCP2 and UCP3 rise in starved rat skeletal muscle but mitochondrial proton conductance is unchanged. FEBS Lett. 462:257-260.
15. Jucker, B.M., et al. 2000. 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.
16. Jucker, B.M., et al. 2000. Assessment of mitochondrial energy coupling in vivo by 13C/31P NMR. Proc. Natl. Acad. Sci. USA. 97:6880-6884.
17. de Lange, P., et al. 2001. Uncoupling protein-3 is a molecular determinant for the regulation of resting metabolic rate by thyroid hormone. Endocrinology. 142:3414-3420.
18. Boehm, E.A., Jones, B.E., Radda, G.K., Veech, R.L., and Clarke, K. 2001. Increased uncoupling proteins and decreased efficiency in palmitateperfused hyperthyroid rat heart. Am. J. Physiol. Heart Circ. Physiol. 280:H977-H983.
19. Lanni, A., et al. 1999. Expression of uncoupling protein-3 and mirochondrial activity in the transition from hypothyroid to hyperthyroid state in rat skeletal muscle. FEBS Lett. 444:250-254.
20. Surwit, R.S., et al. 1998. Diet-induced changes in uncoupling proteins in obesity-prone and obesity-resistant strains of mice. Proc. Natl. Acad. Sci. USA. 95:4061-4065.
21. Samec, S., Seydoux, J., and Dulloo, A.G. 1999. Post-starvation gene expression of skeletal muscle uncoupling protein 2 and uncoupling protein 3 in response to dietary fat levels and fatty acid composition: a link with insulin resistance. Diabetes. 48:436-441.
22. Schrauwen, P., Hoppeler, H., Billeter, R., Bakker, A., and Pendergast, D. 2001. Fiber type dependent upregulation of human skeletal muscle UCP2 and UCP3 mRNA expression by high-fat diet. Int. J. Obes. Relat. Metab. Disord. 25:449-456.
23. Bergström, J., and Hultman, E. 1966. Muscle glycogen synthesis after exercise: an enhancing factor localized to the muscle cells in man. Nature. 210:309-310.
24. Greenhaff, P.L., Bodin, K., Soderlund, K., and Hultman, E. 1994. Effect of oral creatine supplementation on skeletal muscle phosphocreatine resynthesis. Am. J. Physiol. 266:E725-E730.
25. Siri, W.R. 1956. The gross composition of the body. Adv. Biol. Med. Physiol. 4:239-280.
26. Stichting-Nederlandse-Voedingsstoffenbestand. 1996. NEVO table. Voorlichtingsbureau voor de voeding. The Hague, The Netherlands. 235 pp.
27. Harris, J.A., and Benedict, F.G.A. 1919. A biometric study of basal metabolism in man. Carnegie Institution of Washington. Washington, DC, USA. 223-251.
28. Westerterp, K.R. 2001. Pattern and intensity of physical activity. Nature. 410:539.
29. Harris, R.C., Hultman, E., and Nordesjo, L.O. 1974. Glycogen, glycolytic intermediates and high-energy phosphates determined in biopsy samples ofmusculus quadriceps femoris of man at rest. Methods and variance of values. Scand. J. Clin. Lab. Invest. 33:109-120.
30. Cederblad, G., Carlin, J.I., Constantin-Teodosiu, D., Harper, P., and Hultman, E. 1990. Radioisotopic assays of CoASH and carnitine and their acetylated forms in human skeletal muscle. Anal. Biochem. 185:274-278.
31. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
32. Hesselink, M.K., et al. 2001. Protein expression of UCP3 differs between human type 1, type 2a, and type 2b fibers. FASEB J. 15:1071-1073.
33. Bezaite, V., Hofmann, W., Kramer, J.K., Kozak, L.P., and Harper, M.E. 2001. Effects of fasting on muscle mitochondrial energetics and fatty acid metabolism in Ucp3(-/-) and wild-type mice. Am. J. Physiol. Endocrinol. Metab. 281:E975-E982.
34. Harris, R.C., et al. 1976. The time course of phosphorylcreatine resynthesis during recovery of the quadriceps muscle in man. Pflügers Arch. 367:137-142.
35. Erickson-Viitanen, S., Viitanen, P., Geiger, P.J., Yang, W.C., and Bessman, S.P. 1982. Compartmentation of mitochondrial creatine phosphokinase. I. Direct demonstration of compartmentation with the use of labeled precursors. J. Biol. Chem. 257:14395-14404.
36. Constantin-Teodosiu, D., Cederblad, G., and Hultman, E. 1993. PDC activity and acetyl group accumulation in skeletal muscle during isometric contraction. J. Appl. Physiol. 74:1712-1718.
37. Kariman, K., Chance, B., Burkhart, D.S., and Bolinger, L.A. 1986. Uncoupling effects of 2,4-dinitrophenol on electron transfer reactions and cell bioenergetics in rat brain in situ. Brain Res. 366:300-306.
38. Ren, J.M., and Hultman, E. 1989. Regulation of glycogenolysis in human skeletal muscle. J. Appl. Physiol. 67:2243-2248.
39. Söderlund, K., and Hultman, E. 1990. ATP content in single muscle fibers from human skeletal muscle after electrical stimulation and during recovery. Acta Physiol. Scand. 139:459-466.
40. Jones, S., Constantin-Teodosiu, D., Hultman, E., and Greenhaff, P.L. 2001. The creatine-mediated increase in muscle phosphocreatine resynthesis during recovery from maximal exercise in humans is associated with increased mitochondrial acetyl group utilisation. J. Physiol. 531P:66P.
41. Campbell, S.P., Hultman, E., Constantin-Teodosiu, D., and Greenhaff, P.L. 2000. Acetyl group delivery limits mitochondrial flux in human skeletal muscle. J. Physiol. 523P:189P.
42. Echtay, K.S., et al. 2002. Superoxide activates mitochondrial uncoupling proteins. Nature. 415:96-99.
43. Pecqueut, C., et al. 2001. Uncoupling protein 2, in vivo distribution, induction upon oxidative stress, and evidence for translational regulation. J. Biol. Chem. 276:8705-8712.
44. Millet, L., et al. 1997. Increased uncoupling protein-2 and -3 mRNA expression during fasting in obese and lean humans. J. Clin. Invest. 100:2665-2670.
45. Schrauwen, P., Troost, F.J., Xia, J., Ravussin, E., and Satis, W.H. 1999. Skeletal muscle UCP2 and UCP3 expression in trained and untrained male subjects. Int. J. Obes. Relat. Metab. Disord. 23:966-972.
46. Walder, K., et al. 1998. Association between uncoupling protein polymorphisms (UCP2-UCP3) and energy metabolism/obesity in Pima Indians. Hum. Mol. Genet. 7:1431-1435.
47. Harper, M.E., et al. 2002. Decreased mitochondrial proton leak and reduced expression of uncoupling protein 3 in skeletal muscle of obese diet-resistant women. Diabetes. 51:2459-2466.
48. Chung, W.K., et al. 1999. Genetic and physiologic analysis of the role of uncoupling protein 3 in human energy homeostasis. Diabetes. 48:1890-1895.
49. Schtauwen, P., Saris, W.H., and Hesselink, M.K. 2001. An alternative function for human uncoupling protein 3: protection of mitochondria against accumulation of nonesterified fatty acids inside the mitochondrial matrix. FASEB J. 15:2497-2502.
50. Argyropoulos, G., et al. 1998. Effects of mutations in the human uncoupling protein 3 gene on the respiratory quotient and fat oxidation in severe obesity and type 2 diabetes. J. Clin. Invest. 102:1345-1351.
51. Hamilton, J.A., and Kamp, F. 1999. How are free fatty acids transported in membranes? Is it by proteins or by free diffusion through the lipids? Diabetes. 48:2255-2269.
52. Jezek, P., Orosz, D.E., Modriansky, M., and Garlid, K.D. 1994. Transport of anions and protons by the mitochondrial uncoupling protein and its regulation by nucleotides and fatty acids. A new look at old hypotheses. J. Biol. Chem. 269:26184-26190.