Absence of UCP3 in brown adipose tissue does not impair nonshivering thermogenesis

Physiological and Biochemical Zoology

Volumn 77, Issue 1, 2004, Pages 116-126

  Liebig, Michaela ^a   Von Praun, Christa ^a   Heldmaier, Gerhard ^a   Klingenspor, Martin ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CELL RECEPTOR; CYTOCHROME C OXIDASE; ION CHANNEL; LIGAND; MEMBRANE PROTEIN; MESSENGER RNA; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN 2; MITOCHONDRIAL UNCOUPLING PROTEIN 3; NORADRENALIN; PRIMER DNA; TRANSCRIPTION FACTOR;

PROTEIN; RODENT; THERMOREGULATION;

ACCLIMATIZATION; ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; BASAL METABOLIC RATE; BROWN ADIPOSE TISSUE; COLD; COMPARATIVE STUDY; GENE EXPRESSION; GENETICS; HAMSTER; METABOLISM; NORTHERN BLOTTING; PHODOPUS; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; THERMOGENESIS; WESTERN BLOTTING;

ACCLIMATIZATION; ADIPOSE TISSUE, BROWN; ANALYSIS OF VARIANCE; ANIMALS; BASAL METABOLISM; BLOTTING, NORTHERN; BLOTTING, WESTERN; CARRIER PROTEINS; COLD; CRICETINAE; DNA PRIMERS; ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION; ION CHANNELS; LIGANDS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; NOREPINEPHRINE; PHODOPUS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; THERMOGENESIS; TRANSCRIPTION FACTORS;

ANIMALIA; CRICETINAE; PHODOPUS; PHODOPUS SUNGORUS; RODENTIA;

EID: 1942453834     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/381464     Document Type: Article

References (45)

1. Acin A., M. Rodriguez, H. Rique, E. Canet, J.A. Boutin, and J.P. Galizzi. 1999. Cloning and characterization of the 5′ flanking region of the human uncoupling protein 3 (UCP3) gene. Biochem Biophys Res Commun 258:278-283.
2. Arsenijevic D., H. Onuma, C. Pecqueur, S. Raimbault, B.S. Manning, B. Miroux, E. Couplan, et al. 2000. Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat Genet 26:435-439.
3. Bouillaud F., E. Couplan, C. Pecqueur, and D. Ricquier. 2001. Homologues of the uncoupling protein from brown adipose tissue (UCP1): UCP2, UCP3, BMCP1 and UCP4. Biochim Biophys Acta 1504:107-119.
4. Brand M.D., R. Pamplona, M. Portero-Otin, J.R. Requena, S.J. Roebuck, J.A. Buckingham, J.C. Clapham, and S. Cadenas. 2002. Oxidative damage and phospholipid fatty acyl composition in skeletal muscle mitochondria from mice underexpressing or overexpressing uncoupling protein 3. Biochem J 368:597-603.
5. Cadenas S., J.A. Buckingham, S. Samec, J. Seydoux, N. Din, A.G. Dulloo, and M.D. Brand. 1999. UCP2 and UCP3 rise in starved rat skeletal muscle but mitochondrial proton conductance is unchanged. FEBS Lett 462:257-260.
6. Clapham J.C., J.R. Arch, H. Chapman, A. Haynes, C. Lister, G.B. Moore, V. Piercy, et al. 2000. Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature 406:415-418.
7. Cunningham S.A., H. Wiesinger, and D.G. Nicholls. 1986. Quantification of fatty acid activation of the uncoupling protein in brown adipocytes and mitochondria from the guineapig. Eur J Biochem 157:415-420.
8. Echtay K.S., D. Roussel, J. St. Pierre, M.B. Jekabsons, S. Cadenas, J.A. Stuart, J.A. Harper, et al. 2002. Superoxide activates mitochondrial uncoupling proteins. Nature 415:96-99.
9. Echtay K.S., E. Winkler, K. Frischmuth, and M. Klingenberg. 2001. Uncoupling proteins 2 and 3 are highly active H(+) transporters and highly nucleotide sensitive when activated by coenzyme Q (ubiquinone). Proc Natl Acad Sci USA 98:1416-1421.
10. Encke D., M. Ely, G. Heldmaier, and S. Klaus. 1997. Physiological approach to maturation of brown adipocytes in primary cell culture. Biochim Biophys Acta 1357:339-347.
11. Enerbäck S., A. Jacobsson, E.M. Simpson, C. Guerra, H. Yamashita, M.E. Harper, and L.P. Kozak. 1997. Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387:90-94.
12. Garcia-Martinez C., B. Sibille, G. Solanes, C. Darimont, K. Mace, F. Villarroya, and A.M. Gomez-Foix. 2001. Overexpression of UCP3 in cultured human muscle lowers mitochondrial membrane potential, raises ATP/ADP ratio, and favors fatty acid vs. glucose oxidation. FASEB (Fed Am Soc Exp Biol) J 15:2033-2035.
13. Gong D.W., Y.F. He, M. Karas, and M. Reitman. 1997. Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, beta 3-adrenergic agonists, and leptin. J Biol Chem 272:24129-24132.
14. Gong D.W., S. Monemdjou, O. Gavrilova, L.R. Leon, B. Marcus-Samuels, C.J. Chou, C. Everett, 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.
15. Hanak P. and P. Jezek. 2001. Mitochondrial uncoupling proteins and phylogenesis: UCP4 as the ancestral uncoupling protein. FEBS Lett 495:137-141.
16. Harper J.A., J.A. Stuart, M.B. Jekabsons, D. Roussel, K.M. Brindle, K. Dickinson, R.B. Jones, and M.D. Brand. 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.
17. Heldmaier G., A. Buchberger, and K. Seidl. 1983. Contribution of brown adipose tissue to thermoregulatory heat production in the Djungarian hamster. J Therm Biol 8:413-415.
18. Heldmaier G. and T.P. Ruf. 1992. Body temperature and metabolic rate during natural hypothermia in endotherms. J Comp Physiol B 162:696-706.
19. Heldmaier G., S. Steinlechner, and J. Rafael. 1982. Nonshivering thermogenesis and cold resistance during seasonal acclimatization in the Djungarian hamster. J Comp Physiol 149:1-9.
20. Himms-Hagen J. and M.E. Harper. 2001. Physiological role of UCP3 may be export of fatty acids from mitochondria when fatty acid oxidation predominates: an hypothesis. Exp Biol Med 226:78-84.
21. Hong Y., B.D. Fink, J.S. Dillon, and W.I. Sivitz. 2001. Effects of adenoviral overexpression of uncoupling protein-2 and -3 on mitochondrial respiration in insulinoma cells. Endocrinology 142:249-256.
22. Jaburek M., M. Varecha, R.E. Gimeno, M. Dembski, P. Jezek, M. Zhang, P. Burn, L.A. Tartaglia, and K.D. Garlid. 1999. Transport function and regulation of mitochondrial uncoupling proteins 2 and 3. J Biol Chem 274:26003-26007.
23. Klaus S. 1991. Development of Phodopus sungorus brown preadipocytes in primary cell culture: effect of an atypical beta-adrenergic agonist, insulin and triiodothyronin on differentiation, mitochondrial development and expression of the uncoupling protein UCP. J Cell Biol 115:1783-1790.
24. Klingenberg M., K.S. Echtay, M. Bienengraeber, E. Winkler, and S.G. Huang. 1999. Structure-function relationship in UCP1. Int J Obesity 23:S24-S29.
25. Klingenspor M. 2003. Cold-induced recruitment of brown adipose tissue thermogenesis. Exp Physiol 88:141-148.
26. Klingenspor M., C. Ebbinghaus, G. Hülshorst, S. Stöhr, F. Spiegelhalter, K. Haas, and G. Heldmaier. 1996. Multiple regulatory steps are involved in the control of lipoprotein lipase activity in brown adipose tissue. J Lipid Res 37:1685-1695.
27. Mao W., X.X. Yu, A. Zhong, W. Li, J. Brush, S.W. Sherwood, S.H. Adams, and G.Pan. 1999. UCP4, a novel brain-specific mitochondrial protein that reduces membrane potential in mammalian cells. FEBS Lett 443:326-330.
28. Matthias A., A. Jacobsson, B. Cannon, and J. Nedergaard. 1999. The bioenergetics of brown fat mitochondria from UCP1-ablated mice: UCP1 is not involved in fatty acid-induced deenergization ("uncoupling"). J Biol Chem 274:28150-28160.
29. Moore G.B., J. Himms-Hagen, M.E. Harper, and J.C. Clapham. 2001. Overexpression of UCP-3 in skeletal muscle of mice results in increased expression of mitochondrial thioesterase mRNA. Biochem Biophys Res Commun 283:785-790.
30. Nagase I., S. Yoshida, X. Canas, Y. Irie, K. Kimura, T. Yoshida, and M. Saito. 1999. 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.
31. Nedergaard J. and B. Cannon. 2003. Pros and cons for suggested functions. Exp Physiol 88:65-84.
32. Nicholls D.G. and R.M. Locke. 1984. Thermogenic mechanisms in brown fat. Physiol Rev 64:1-64.
33. Paradies G., G. Petrosillo, M. Pistolese, and F.M. Ruggiero. 2000. The effect of reactive oxygen species generated from the mitochondrial electron transport chain on the cytochrome c oxidase activity and on the cardiolipin content in bovine heart submitochondrial particles. FEBS Lett 466:323-326.
34. Pecqueur C., M.C. Alves-Guerra, C. Gelly, C. Levi-Meyrueis, E. Couplan, S. Collins, D. Ricquier, F. Bouillaud, and B. Miroux. 2001. Uncoupling protein 2, in vivo distribution, induction upon oxidative stress, and evidence for translational regulation. J Biol Chem 276:8705-8712.
35. Puchalski W., H. Böckler, G. Heldmaier, and M. Langefeld. 1987. Organ blood flow and brown adipose tissue oxygen consumption during noradrenaline-induced nonshivering thermogenesis in the Djungarian hamster. J Exp Zool 242:263-271.
36. Rafael J., P. Vsiansky, and G. Heldmaier. 1985. Increased contribution of brown adipose tissue to nonshivering thermogenesis in the Djungarian hamster during cold-adaptation. J Comp Physiol B 155:717-722.
37. Sambrook J. and D.W. Russell. 2001. Calcium-phosphate-mediated transfection of eucaryotic cells with plasmid DNAs. Pp. 14-20 in J. Argentine, N. Irwin, and K.A. Janssen, eds. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
38. Sanchis D., C. Fleury, N. Chomiki, M. Goubern, Q. Huang, M. Neverova, F.M. Gregoire, et al. 1998. BMCP1, a novel mitochondrial carrier with high expression in the central nervous system of humans and rodents, and respiration uncoupling activity in recombinant yeast. J Biol Chem 273:34611-34615.
39. Son C., K. Hosoda, J. Matsuda, J. Fujikura, S. Yonemitsu, H. Iwakura, H. Masuzaki, et al. 2001. Up-regulation of uncoupling protein 3 gene expression by fatty acids and agonists for PPARs in L6 myotubes. Endocrinology 142:4189-4194.
40. Stieglitz A., F. Spiegelhalter, G. Klante, and G. Heldmaier. 1995. Urinary 6-sulphatoxymelatonin excretion reflects pineal melatonin secretion in the Djungarian hamster (Phodopus sungorus). J Pineal Res 18:69-76.
41. Stuart J.A., J.A. Harper, K.M. Brindle, M.B. Jekabsons, and M.D. Brand. 2001. Physiological levels of mammalian uncoupling protein 2 do not uncouple yeast mitochondria. J Biol Chem 276:18633-18639.
42. Teruel T., S.A. Smith, J. Peterson, and J.C. Clapham. 2000. Synergistic activation of UCP-3 expression in cultured fetal rat brown adipocytes by PPARalpha and PPARgamma ligands. Biochem Biophys Res Commun 273:560-564.
43. Vidal-Puig A.J., D. Grujic, C.Y. Zhang, T. Hagen, O. Boss, Y. Ido, A. Szczepanik, et al. 2000. Energy metabolism in uncoupling protein 3 gene knockout mice. J Biol Chem 275:16258-16266.
44. von Praun C., M. Burkert, M. Gessner, and M. Klingenspor. 2001. Tissue-specific expression and cold-induced mRNA levels of uncoupling proteins in the Djungarian hamster. Physiol Biochem Zool 74:203-211.
45. Weigle D.S., L.E. Selfridge, M.W. Schwartz, R.J. Seeley, D.E. Cummings, P.J. Havel, J.L. Kuijper, and H. Beltrandelrio. 1998. Elevated free fatty acids induce uncoupling protein 3 expression in muscle: a potential explanation for the effect of fasting. Diabetes 47:298-302.