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. 1994 Jun 1;300(Pt 2):463–468. doi: 10.1042/bj3000463

Cold exposure induces different uncoupling-protein thermogenin masking/unmasking processes in brown adipose tissue depending on mitochondrial subtypes.

M Moreno 1, P Puigserver 1, J Llull 1, M Gianotti 1, A Lanni 1, F Goglia 1, A Palou 1
PMCID: PMC1138185  PMID: 8002952

Abstract

The effect of cold exposure on thermogenic parameters such as mitochondrial protein content, GDP-binding and uncoupling protein (UCP) levels in different mitochondrial fractions from rat brown adipose tissue has been investigated. Rats were exposed from 12 h to 5 days at 4 degrees C, and three mitochondrial fractions were isolated by differential centrifugation: the M1 fraction (1000 g), the M3 fraction (3000 g) and the M15 fraction (15,000 g). Cytochrome c oxidase activity as an index of mitochondrial mass showed an increase during cold exposure. During the first 24 h of cold exposure UCP was incorporated specifically into the M3 and M15 mitochondrial fractions, and thereafter UCP appeared in the heaviest M1 fraction. However, specific GDP binding was increased during the first 24 h in the same way in all subpopulations, and this increase continued up to 72 h of cold exposure. Results suggest that different molecular events are involved during acute and chronic adaptation to cold: during the first 24 h of cold acclimatization, thermogenic activity is increased by an unmasking process of the UCP binding sites in the M1 mitochondrial fraction as UCP levels were constant and GDP binding increased, but in the M3 and M15 fraction the increase in thermogenic activity was completely due to an increase in GDP binding induced by a specific incorporation of UCP targeted to these mitochondria. Thus thermogenic parameters change in a different way in the brown-fat mitochondrial subpopulations during cold acclimatization.

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Selected References

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  1. Ashwell M., Jennings G., Richard D., Stirling D. M., Trayhurn P. Effect of acclimation temperature on the concentration of the mitochondrial 'uncoupling' protein measured by radioimmunoassay in mouse brown adipose tissue. FEBS Lett. 1983 Sep 5;161(1):108–112. doi: 10.1016/0014-5793(83)80740-6. [DOI] [PubMed] [Google Scholar]
  2. Bouillaud F., Ricquier D., Mory G., Thibault J. Increased level of mRNA for the uncoupling protein in brown adipose tissue of rats during thermogenesis induced by cold exposure or norepinephrine infusion. J Biol Chem. 1984 Sep 25;259(18):11583–11586. [PubMed] [Google Scholar]
  3. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  4. Cannon B., Nedergaard J. The biochemistry of an inefficient tissue: brown adipose tissue. Essays Biochem. 1985;20:110–164. [PubMed] [Google Scholar]
  5. Desautels M., Zaror-Behrens G., Himms-Hagen J. Increased purine nucleotide binding, altered polypeptide composition, and thermogenesis in brown adipose tissue mitochondria of cold-acclimated rats. Can J Biochem. 1978 Jun;56(6):378–383. doi: 10.1139/o78-060. [DOI] [PubMed] [Google Scholar]
  6. Goglia F., Liverini G., Lanni A., Iossa S., Barletta A. Light mitochondria and cellular thermogenesis. Biochem Biophys Res Commun. 1988 Mar 30;151(3):1241–1249. doi: 10.1016/s0006-291x(88)80499-6. [DOI] [PubMed] [Google Scholar]
  7. Goglia F., Liverini G., Lanni A., Iossa S., Barletta A. Tri-iodothyronine enhances the formation of light mitochondria during cold exposure. Comp Biochem Physiol B. 1986;85(4):869–873. doi: 10.1016/0305-0491(86)90189-6. [DOI] [PubMed] [Google Scholar]
  8. Gribskov C. L., Henningfield M. F., Swick A. G., Swick R. W. Evidence for unmasking of rat brown-adipose-tissue mitochondrial GDP-binding sites in response to acute cold exposure. Effects of washing with albumin on GDP binding. Biochem J. 1986 Feb 1;233(3):743–747. doi: 10.1042/bj2330743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Herron D., Rehnmark S., Néchad M., Loncar D., Cannon B., Nedergaard J. Norepinephrine-induced synthesis of the uncoupling protein thermogenin (UCP) and its mitochondrial targeting in brown adipocytes differentiated in culture. FEBS Lett. 1990 Jul 30;268(1):296–300. doi: 10.1016/0014-5793(90)81031-i. [DOI] [PubMed] [Google Scholar]
  10. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  11. Liu X. Q., Freeman K. B., Shore G. C. An amino-terminal signal sequence abrogates the intrinsic membrane-targeting information of mitochondrial uncoupling protein. J Biol Chem. 1990 Jan 5;265(1):9–12. [PubMed] [Google Scholar]
  12. Milner R. E., Trayhurn P. Cold-induced changes in uncoupling protein and GDP binding sites in brown fat of ob/ob mice. Am J Physiol. 1989 Aug;257(2 Pt 2):R292–R299. doi: 10.1152/ajpregu.1989.257.2.R292. [DOI] [PubMed] [Google Scholar]
  13. Milner R. E., Trayhurn P. Evidence that the acute unmasking of GDP-binding sites in brown adipose tissue mitochondria is not dependent on mitochondrial swelling. Biochem Cell Biol. 1988 Nov;66(11):1226–1230. doi: 10.1139/o88-140. [DOI] [PubMed] [Google Scholar]
  14. Milner R. E., Wilson S., Arch J. R., Trayhurn P. Acute effects of a beta-adrenoceptor agonist (BRL 26830A) on rat brown-adipose-tissue mitochondria. Increased GDP binding and GDP-sensitive proton conductance without changes in the concentration of uncoupling protein. Biochem J. 1988 Feb 1;249(3):759–763. doi: 10.1042/bj2490759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Nedergaard J., Cannon B. Apparent unmasking of [3H]GDP binding in rat brown-fat mitochondria is due to mitochondrial swelling. Eur J Biochem. 1987 May 4;164(3):681–686. doi: 10.1111/j.1432-1033.1987.tb11180.x. [DOI] [PubMed] [Google Scholar]
  16. Nedergaard J., Cannon B. [3H]GDP binding and thermogenin amount in brown adipose tissue mitochondria from cold-exposed rats. Am J Physiol. 1985 Mar;248(3 Pt 1):C365–C371. doi: 10.1152/ajpcell.1985.248.3.C365. [DOI] [PubMed] [Google Scholar]
  17. Nedergaard J., Raasmaja A., Cannon B. Parallel increases in amount of (3H)GDP binding and thermogenin antigen in brown-adipose-tissue mitochondria of cafeteria-fed rats. Biochem Biophys Res Commun. 1984 Aug 16;122(3):1328–1336. doi: 10.1016/0006-291x(84)91237-3. [DOI] [PubMed] [Google Scholar]
  18. Peachey T., French R. R., York D. A. Regulation of GDP binding and uncoupling-protein concentration in brown-adipose-tissue mitochondria. The effects of cold-acclimation, warm-reacclimation and noradrenaline. Biochem J. 1988 Jan 15;249(2):451–457. doi: 10.1042/bj2490451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Puigserver P., Gianotti M., Palou A. Impaired starvation-induced loss of mitochondrial protein in the brown adipose tissue of dietary obese rats. Int J Obes Relat Metab Disord. 1992 Apr;16(4):255–261. [PubMed] [Google Scholar]
  20. Puigserver P., Herron D., Gianotti M., Palou A., Cannon B., Nedergaard J. Induction and degradation of the uncoupling protein thermogenin in brown adipocytes in vitro and in vivo. Evidence for a rapidly degradable pool. Biochem J. 1992 Jun 1;284(Pt 2):393–398. doi: 10.1042/bj2840393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Puigserver P., Lladó I., Palou A., Gianotti M. Evidence for masking of brown adipose tissue mitochondrial GDP-binding sites in response to fasting in rats made obese by dietary manipulation. Effects of reversion to standard diet. Biochem J. 1991 Oct 15;279(Pt 2):575–579. doi: 10.1042/bj2790575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ridley R. G., Patel H. V., Gerber G. E., Morton R. C., Freeman K. B. Complete nucleotide and derived amino acid sequence of cDNA encoding the mitochondrial uncoupling protein of rat brown adipose tissue: lack of a mitochondrial targeting presequence. Nucleic Acids Res. 1986 May 27;14(10):4025–4035. doi: 10.1093/nar/14.10.4025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Swick A. G., Kemnitz J. W., Houser W. D., Swick R. W. Norepinephrine stimulates activity of brown adipose tissue in rhesus monkeys. Int J Obes. 1986;10(3):241–244. [PubMed] [Google Scholar]
  24. Swick A. G., Swick R. W. Rapid changes in number of GDP binding sites on brown adipose tissue mitochondria. Am J Physiol. 1986 Aug;251(2 Pt 1):E192–E195. doi: 10.1152/ajpendo.1986.251.2.E192. [DOI] [PubMed] [Google Scholar]
  25. Trayhurn P., Ashwell M., Jennings G., Richard D., Stirling D. M. Effect of warm or cold exposure on GDP binding and uncoupling protein in rat brown fat. Am J Physiol. 1987 Feb;252(2 Pt 1):E237–E243. doi: 10.1152/ajpendo.1987.252.2.E237. [DOI] [PubMed] [Google Scholar]

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