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. 1988 Jun 15;252(3):843–849. doi: 10.1042/bj2520843

Amino acid and glucose uptake by rat brown adipose tissue. Effect of cold-exposure and acclimation.

F J López-Soriano 1, J A Fernández-López 1, T Mampel 1, F Villarroya 1, R Iglesias 1, M Alemany 1
PMCID: PMC1149224  PMID: 3421924

Abstract

The net uptake/release of glucose, lactate and amino acids from the bloodstream by the interscapular brown adipose tissue of control, cold-exposed and cold-acclimated rats was estimated by measurement of arteriovenous differences in their concentrations. In the control animals amino acids contributed little to the overall energetic needs of the tissue; glucose uptake was more than compensated by lactate efflux. Cold-exposure resulted in an enhancement of amino acid utilization and of glucose uptake, with high lactate efflux. There was a net glycine and proline efflux that partly compensated the positive nitrogen balance of the tissue; amino acids accounted for about one-third of the energy supplied by glucose to the tissue. Cold-acclimation resulted in a very high increase in glucose uptake, with a parallel decrease in lactate efflux and amino acid consumption. Branched-chain amino acids, however, were more actively utilized. This was related with a much higher alanine efflux, in addition to that of glycine and proline. It is suggested that most of the glucose used during cold-exposure is returned to the bloodstream as lactate under conditions of active lipid utilization, amino acids contributing their skeletons largely in anaplerotic pathways. On the other hand, cold-acclimation resulted in an important enhancement of glucose utilization, with lowered amino acid oxidation. Amino acids are thus used as metabolic substrates by the brown adipose tissue of rats under conditions of relatively scarce substrate availability, but mainly as anaplerotic substrates, in parallel to glucose. Cold-acclimation results in a shift of the main substrates used in thermogenesis from lipid to glucose, with a much lower need for amino acids.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abrahams S. L., Younathan E. S. Modulation of the kinetic properties of phosphofructokinase by ammonium ions. J Biol Chem. 1971 Apr 25;246(8):2464–2467. [PubMed] [Google Scholar]
  2. Aikawa T., Matsutaka H., Yamamoto H., Okuda T., Ishikawa E. Gluconeogenesis and amino acid metabolism. II. Inter-organal relations and roles of glutamine and alanine in the amino acid metabolism of fasted rats. J Biochem. 1973 Nov;74(5):1003–1017. [PubMed] [Google Scholar]
  3. Brosnan J. T., Man K. C., Hall D. E., Colbourne S. A., Brosnan M. E. Interorgan metabolism of amino acids in streptozotocin-diabetic ketoacidotic rat. Am J Physiol. 1983 Feb;244(2):E151–E158. doi: 10.1152/ajpendo.1983.244.2.E151. [DOI] [PubMed] [Google Scholar]
  4. Carneheim C., Nedergaard J., Cannon B. Beta-adrenergic stimulation of lipoprotein lipase in rat brown adipose tissue during acclimation to cold. Am J Physiol. 1984 Apr;246(4 Pt 1):E327–E333. doi: 10.1152/ajpendo.1984.246.4.E327. [DOI] [PubMed] [Google Scholar]
  5. Cooney G. J., Newsholme E. A. The maximum capacity of glycolysis in brown adipose tissue and its relationship to control of the blood glucose concentration. FEBS Lett. 1982 Nov 8;148(2):198–200. doi: 10.1016/0014-5793(82)80807-7. [DOI] [PubMed] [Google Scholar]
  6. Cooney G., Curi R., Mitchelson A., Newsholme P., Simpson M., Newsholme E. A. Activities of some key enzymes of carbohydrate, ketone body, adenosine and glutamine metabolism in liver, and brown and white adipose tissues of the rat. Biochem Biophys Res Commun. 1986 Jul 31;138(2):687–692. doi: 10.1016/s0006-291x(86)80551-4. [DOI] [PubMed] [Google Scholar]
  7. Czech M. P., Lawrence J. C., Jr, Lynn W. S. Hexose transport in isolated brown fat cells. A model system for investigating insulin action on membrane transport. J Biol Chem. 1974 Sep 10;249(17):5421–5427. [PubMed] [Google Scholar]
  8. Desautels M., Himms-Hagen J. Roles of noradrenaline and protein synthesis in the cold-induced increase in purine nucleotide binding by rat brown adipose tissue mitochondria. Can J Biochem. 1979 Jun;57(6):968–976. doi: 10.1139/o79-118. [DOI] [PubMed] [Google Scholar]
  9. Felig P. The glucose-alanine cycle. Metabolism. 1973 Feb;22(2):179–207. doi: 10.1016/0026-0495(73)90269-2. [DOI] [PubMed] [Google Scholar]
  10. Fernandez J. A., Mampel T., Villarroya F., Iglesias R. Direct assessment of brown adipose tissue as a site of systemic tri-iodothyronine production in the rat. Biochem J. 1987 Apr 1;243(1):281–284. doi: 10.1042/bj2430281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ferré P., Burnol A. F., Leturque A., Terretaz J., Penicaud L., Jeanrenaud B., Girard J. Glucose utilization in vivo and insulin-sensitivity of rat brown adipose tissue in various physiological and pathological conditions. Biochem J. 1986 Jan 1;233(1):249–252. doi: 10.1042/bj2330249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Foster D. O., Frydman M. L. Nonshivering thermogenesis in the rat. II. Measurements of blood flow with microspheres point to brown adipose tissue as the dominant site of the calorigenesis induced by noradrenaline. Can J Physiol Pharmacol. 1978 Feb;56(1):110–122. doi: 10.1139/y78-015. [DOI] [PubMed] [Google Scholar]
  13. Foster D. O., Frydman M. L. Tissue distribution of cold-induced thermogenesis in conscious warm- or cold-acclimated rats reevaluated from changes in tissue blood flow: the dominant role of brown adipose tissue in the replacement of shivering by nonshivering thermogenesis. Can J Physiol Pharmacol. 1979 Mar;57(3):257–270. doi: 10.1139/y79-039. [DOI] [PubMed] [Google Scholar]
  14. Foster D. O. Quantitative contribution of brown adipose tissue thermogenesis to overall metabolism. Can J Biochem Cell Biol. 1984 Jul;62(7):618–622. doi: 10.1139/o84-082. [DOI] [PubMed] [Google Scholar]
  15. Hensgens H. E., Meijer A. J., Williamson J. R., Gimpel J. A., Tager J. M. Prolone metabolism in isolated rat liver cells. Biochem J. 1978 Mar 15;170(3):699–707. doi: 10.1042/bj1700699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. JOHNSON A. B., STRECKER H. J. The interconversion of glutamic acid and proline. IV. The oxidation of proline by rat liver mitochondria. J Biol Chem. 1962 Jun;237:1876–1882. [PubMed] [Google Scholar]
  17. James D. E., Burleigh K. M., Storlien L. H., Bennett S. P., Kraegen E. W. Heterogeneity of insulin action in muscle: influence of blood flow. Am J Physiol. 1986 Oct;251(4 Pt 1):E422–E430. doi: 10.1152/ajpendo.1986.251.4.E422. [DOI] [PubMed] [Google Scholar]
  18. Jones R. G., Williamson D. H. Alterations in mammary-gland blood flow and glucose metabolism in the lactating rat induced by short-term starvation and refeeding. Biosci Rep. 1984 May;4(5):421–426. doi: 10.1007/BF01122507. [DOI] [PubMed] [Google Scholar]
  19. Lee K. S., Drescher D. G. Fluorometric amino-acid analysis with o-phthaldialdehyde (OPA). Int J Biochem. 1978;9(7):457–467. doi: 10.1016/0020-711x(78)90075-7. [DOI] [PubMed] [Google Scholar]
  20. López-Soriano F. J., Alemany M. Activities of enzymes of amino acid metabolism in rat brown adipose tissue. Biochem Int. 1986 Mar;12(3):471–478. [PubMed] [Google Scholar]
  21. López-Soriano F. J., Alemany M. Effect of cold-temperature exposure and acclimation on amino acid pool changes and enzyme activities of rat brown adipose tissue. Biochim Biophys Acta. 1987 Sep 11;925(3):265–271. doi: 10.1016/0304-4165(87)90191-7. [DOI] [PubMed] [Google Scholar]
  22. Ma S. W., Foster D. O. Uptake of glucose and release of fatty acids and glycerol by rat brown adipose tissue in vivo. Can J Physiol Pharmacol. 1986 May;64(5):609–614. doi: 10.1139/y86-101. [DOI] [PubMed] [Google Scholar]
  23. Nicholls D. G. Brown adipose tissue mitochondria. Biochim Biophys Acta. 1979 Jul 3;549(1):1–29. doi: 10.1016/0304-4173(79)90016-8. [DOI] [PubMed] [Google Scholar]
  24. PITTS R. F. RENAL PRODUCTION AND EXCRETION OF AMMONIA. Am J Med. 1964 May;36:720–742. doi: 10.1016/0002-9343(64)90182-2. [DOI] [PubMed] [Google Scholar]
  25. Robinson J. D. Interactions between monovalent cations and the (Na+ + K+)-dependent adenosine triphosphatase. Arch Biochem Biophys. 1970 Jul;139(1):17–27. doi: 10.1016/0003-9861(70)90040-8. [DOI] [PubMed] [Google Scholar]
  26. Rothwell N. J., Stock M. J. Influence of noradrenaline on blood flow to brown adipose tissue in rats exhibiting diet-induced thermogenesis. Pflugers Arch. 1981 Mar;389(3):237–242. doi: 10.1007/BF00584784. [DOI] [PubMed] [Google Scholar]
  27. Ruderman N. B. Muscle amino acid metabolism and gluconeogenesis. Annu Rev Med. 1975;26:245–258. doi: 10.1146/annurev.me.26.020175.001333. [DOI] [PubMed] [Google Scholar]
  28. Shimazu T., Takahashi A. Stimulation of hypothalamic nuclei has differential effects on lipid synthesis in brown and white adipose tissue. Nature. 1980 Mar 6;284(5751):62–63. doi: 10.1038/284062a0. [DOI] [PubMed] [Google Scholar]
  29. Snell K., Duff D. A. Alanine release by rat adipose tissue in vitro. Biochem Biophys Res Commun. 1977 Aug 8;77(3):925–931. doi: 10.1016/s0006-291x(77)80066-1. [DOI] [PubMed] [Google Scholar]
  30. Thurlby P. L., Trayhurn P. Regional blood flow in genetically obese (ob/ob) mice. The importance of brown adipose tissue to the reduced energy expenditure on non-shivering thermogenesis. Pflugers Arch. 1980 Jun;385(3):193–201. doi: 10.1007/BF00647457. [DOI] [PubMed] [Google Scholar]
  31. Wilson S., Thurlby P. L., Arch J. R. Substrate supply for thermogenesis induced by the beta-adrenoceptor agonist BRL 26830A. Can J Physiol Pharmacol. 1987 Feb;65(2):113–119. doi: 10.1139/y87-023. [DOI] [PubMed] [Google Scholar]
  32. Windmueller H. G., Spaeth A. E. Uptake and metabolism of plasma glutamine by the small intestine. J Biol Chem. 1974 Aug 25;249(16):5070–5079. [PubMed] [Google Scholar]
  33. Yamamoto H., Aikawa T., Matsutaka H., Okuda T., Ishikawa E. Interorganal relationships of amino acid metabolism in fed rats. Am J Physiol. 1974 Jun;226(6):1428–1433. doi: 10.1152/ajplegacy.1974.226.6.1428. [DOI] [PubMed] [Google Scholar]
  34. Young P., Cawthorne M. A., Smith S. A. Brown adipose tissue is a major site of glucose utilisation in C57Bl/6 ob/ob mice treated with a thermogenic beta-adrenoceptor agonist. Biochem Biophys Res Commun. 1985 Jul 16;130(1):241–248. doi: 10.1016/0006-291x(85)90408-5. [DOI] [PubMed] [Google Scholar]

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