Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1992 Jan 15;281(Pt 2):407–411. doi: 10.1042/bj2810407

Differential sensitivity of insulin- and adaptive-regulation-induced system A activation to microtubular function in skeletal muscle.

A Gumà 1, A Castelló 1, X Testar 1, M Palacín 1, A Zorzano 1
PMCID: PMC1130699  PMID: 1736891

Abstract

1. Insulin and adaptive regulation are known to stimulate system A amino acid transport activity in skeletal muscle. The present study was designed to investigate whether activation of system A in muscle is a consequence of processes which rely on microtubule or microfilament function. To that end, extensor digitorum longus (EDL) muscles were incubated in the presence of colchicine and cytochalasin D, well-known inhibitors of microtubule and microfilament activity respectively. 2. Basal alpha-(methyl)aminoisobutyric acid (MeAIB) uptake decreased after incubation with 5 microM-colchicine in a time-dependent manner. In keeping with this, adaptive regulation of MeAIB uptake caused by prolonged incubation in the absence of amino acids was substantially decreased in the presence of colchicine. 3. Under these conditions, stimulation of MeAIB uptake by insulin was unaltered in muscle in the presence of colchicine. This contrasted with the insulin-induced stimulation of MeAIB uptake by isolated rat hepatocytes, which was markedly decreased by colchicine. 4. Cytochalasin D, an agent that disrupts microfilaments, did not inhibit basal or insulin-stimulated MeAIB uptake by the incubated muscle. 5. Neither colchicine nor cytochalasin D modified the stimulatory effect of insulin on 3-O-methylglucose uptake by EDL muscle. 6. We conclude that up-regulation of system A by synthesis of new carriers depends on the integrity of microtubular function both in skeletal muscle and in hepatocytes. Microtubules might play a role in the movement of system A-containing vesicles from the Golgi network to the plasma membrane.

Full text

PDF
407

Selected References

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

  1. Bertran J., Roca A., Pola E., Testar X., Zorzano A., Palacín M. Modification of system A amino acid carrier by diethyl pyrocarbonate. J Biol Chem. 1991 Jan 15;266(2):798–802. [PubMed] [Google Scholar]
  2. Bracy D. S., Schenerman M. A., Kilberg M. S. Solubilization and reconstitution of hepatic System A-mediated amino acid transport. Preparation of proteoliposomes containing glucagon-stimulated transport activity. Biochim Biophys Acta. 1987 May 12;899(1):51–58. doi: 10.1016/0005-2736(87)90238-0. [DOI] [PubMed] [Google Scholar]
  3. Díez J. C., Avila J., Nieto J. M., Andreu J. M. Reversible inhibition of microtubules and cell growth by the bicyclic colchicine analogue MTC. Cell Motil Cytoskeleton. 1987;7(2):178–186. doi: 10.1002/cm.970070210. [DOI] [PubMed] [Google Scholar]
  4. Elsas L. J., Albrecht I., Rosenberg L. E. Insulin stimulation of amino acid uptake in rat diaphragm. Relationship to protein sythesis. J Biol Chem. 1968 Apr 25;243(8):1846–1853. [PubMed] [Google Scholar]
  5. Fehlmann M., Le Cam A., Freychet P. Insulin and glucagon stimulation of amino acid transport in isolated rat hepatocytes. Synthesis of a high affinity component of transport. J Biol Chem. 1979 Oct 25;254(20):10431–10437. [PubMed] [Google Scholar]
  6. Goshima K., Masuda A., Owaribe K. Insulin-induced formation of ruffling membranes of KB cells and its correlation with enhancement of amino acid transport. J Cell Biol. 1984 Mar;98(3):801–809. doi: 10.1083/jcb.98.3.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Greene W. C., Parker C. M., Parker C. W. Colchicine-sensitive structures and lymphocyte activation. J Immunol. 1976 Sep;117(3):1015–1022. [PubMed] [Google Scholar]
  8. Griffin J. F., Rampal A. L., Jung C. Y. Inhibition of glucose transport in human erythrocytes by cytochalasins: A model based on diffraction studies. Proc Natl Acad Sci U S A. 1982 Jun;79(12):3759–3763. doi: 10.1073/pnas.79.12.3759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Guidotti G. G., Gazzola G. C., Borghetti A. F., Franchi-Gazzola R. Adaptive regulation of amino acid transport across the cell membrane in avian and mammalian tissues. Biochim Biophys Acta. 1975 Oct 6;406(2):264–279. doi: 10.1016/0005-2736(75)90009-7. [DOI] [PubMed] [Google Scholar]
  10. Gumà A., Testar X., Palacín M., Zorzano A. Insulin-stimulated alpha-(methyl)aminoisobutyric acid uptake in skeletal muscle. Evidence for a short-term activation of uptake independent of Na+ electrochemical gradient and protein synthesis. Biochem J. 1988 Aug 1;253(3):625–629. doi: 10.1042/bj2530625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Handlogten M. E., Weissbach L., Kilberg M. S. Heterogeneity of Na+-independent 2-aminobicyclo-(2,2,1)-heptane-2-carboxylic acid and L-leucine transport in isolated rat hepatocytes in primary culture. Biochem Biophys Res Commun. 1982 Jan 15;104(1):307–313. doi: 10.1016/0006-291x(82)91975-1. [DOI] [PubMed] [Google Scholar]
  12. Hirshman M. F., Goodyear L. J., Wardzala L. J., Horton E. D., Horton E. S. Identification of an intracellular pool of glucose transporters from basal and insulin-stimulated rat skeletal muscle. J Biol Chem. 1990 Jan 15;265(2):987–991. [PubMed] [Google Scholar]
  13. Huleux C., Dreux C., Imhoff V., Chambaut-Guerin A. M., Rossignol B. Microfilaments and cellular signal transduction: effect of cytochalasin D on the production of cAMP, inositol phosphates, and on calcium movements in rat parotid glands. Biol Cell. 1989;67(1):61–65. doi: 10.1111/j.1768-322x.1989.tb03010.x. [DOI] [PubMed] [Google Scholar]
  14. Häring H. U., Kemmler W., Hepp K. D. Effect of colchicine and vinblastine on the coupling of insulin binding and insulin action in fat cells. FEBS Lett. 1979 Sep 15;105(2):329–332. doi: 10.1016/0014-5793(79)80641-9. [DOI] [PubMed] [Google Scholar]
  15. James D. E., Brown R., Navarro J., Pilch P. F. Insulin-regulatable tissues express a unique insulin-sensitive glucose transport protein. Nature. 1988 May 12;333(6169):183–185. doi: 10.1038/333183a0. [DOI] [PubMed] [Google Scholar]
  16. KIPNIS D. M., NOALL M. W. Stimulation of amino acid transport by insulin in the isolated rat diaphragm. Biochim Biophys Acta. 1958 Apr;28(1):226–227. doi: 10.1016/0006-3002(58)90466-9. [DOI] [PubMed] [Google Scholar]
  17. Katz J., Wals P. A., Golden S., Rognstad R. Recycling of glucose by rat hepatocytes. Eur J Biochem. 1975 Dec 1;60(1):91–101. doi: 10.1111/j.1432-1033.1975.tb20979.x. [DOI] [PubMed] [Google Scholar]
  18. Kelley D. S., Potter V. R. Regulation of amino acid transport systems by amino acid depletion and supplementation in monolayer cultures of rat hepatocytes. J Biol Chem. 1978 Dec 25;253(24):9009–9017. [PubMed] [Google Scholar]
  19. Kilberg M. S., Handlogten M. E., Christensen H. N. Characteristics of system ASC for transport of neutral amino acids in the isolated rat hepatocyte. J Biol Chem. 1981 Apr 10;256(7):3304–3312. [PubMed] [Google Scholar]
  20. Kletzien R. F., Pariza M. W., Becker J. E., Potter V. R., Butcher F. R. Induction of amino acid transport in primary cultures of adult rat liver parenchymal cells by insulin. J Biol Chem. 1976 May 25;251(10):3014–3020. [PubMed] [Google Scholar]
  21. Klip A., Ramlal T., Young D. A., Holloszy J. O. Insulin-induced translocation of glucose transporters in rat hindlimb muscles. FEBS Lett. 1987 Nov 16;224(1):224–230. doi: 10.1016/0014-5793(87)80452-0. [DOI] [PubMed] [Google Scholar]
  22. Le Marchand-Brustel Y., Moutard N., Freychet P. Aminoisobutyric acid transport in soleus muscles of lean and gold thioglucose-obese mice. Am J Physiol. 1982 Jul;243(1):E74–E79. doi: 10.1152/ajpendo.1982.243.1.E74. [DOI] [PubMed] [Google Scholar]
  23. Logan W. J., Klip A., Gagalang E. Regulation of amino acid transport in L6 muscle cells: I. Stimulation of transport system A by amino acid deprivation. J Cell Physiol. 1982 Aug;112(2):229–236. doi: 10.1002/jcp.1041120211. [DOI] [PubMed] [Google Scholar]
  24. Maizels E. Z., Ruderman N. B., Goodman M. N., Lau D. Effect of acetoacetate on glucose metabolism in the soleus and extensor digitorum longus muscles of the rat. Biochem J. 1977 Mar 15;162(3):557–568. doi: 10.1042/bj1620557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Palacin M., Werner A., Dittmer J., Murer H., Biber J. Expression of rat liver Na+/L-alanine co-transport in Xenopus laevis oocytes. Effect of glucagon in vivo. Biochem J. 1990 Aug 15;270(1):189–195. doi: 10.1042/bj2700189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pola E., Bertran J., Roca A., Palacín M., Zorzano A., Testar X. Sensitivity of system A and ASC transport activities to thiol-group-modifying reagents in rat liver plasma-membrane vesicles. Evidence for a direct binding of N-ethylmaleimide and iodoacetamide on A and ASC carriers. Biochem J. 1990 Oct 15;271(2):297–303. doi: 10.1042/bj2710297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Prentki M., Crettaz M., Jeanrenaud B. Role of microtubules in insulin and glucagon stimulation of amino acid transport in isolated rat hepatocytes. J Biol Chem. 1981 May 10;256(9):4336–4340. [PubMed] [Google Scholar]
  28. Shanahan M. F., Olson S. A., Weber M. J., Lienhard G. E., Gorga J. C. Photolabeling of glucose-sensitive cytochalasin B binding proteins in erythrocyte, fibroblast and adipocyte membranes. Biochem Biophys Res Commun. 1982 Jul 16;107(1):38–43. doi: 10.1016/0006-291x(82)91666-7. [DOI] [PubMed] [Google Scholar]
  29. Tarnuzzer R. W., Campa M. J., Qian N. X., Englesberg E., Kilberg M. S. Expression of the mammalian system A neutral amino acid transporter in Xenopus oocytes. J Biol Chem. 1990 Aug 15;265(23):13914–13917. [PubMed] [Google Scholar]
  30. Tauber R., Reutter W. A colchicine-sensitive uptake system in Morris hepatomas. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5282–5286. doi: 10.1073/pnas.77.9.5282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Vandenburgh H. H., Kaufman S. Coupling of voltage-sensitive sodium channel activity to stretch-induced amino acid transport in skeletal muscle in vitro. J Biol Chem. 1982 Nov 25;257(22):13448–13454. [PubMed] [Google Scholar]
  32. Walker P. R., Whitfield J. F. Inhibition by colchicine of changes in amino acid transport and initiation of DNA synthesis in regenerating rat liver. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1394–1398. doi: 10.1073/pnas.75.3.1394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wardzala L. J., Jeanrenaud B. Identification of the D-glucose-inhibitable cytochalasin B binding site as the glucose transporter in rat diaphragm plasma and microsomal membranes. Biochim Biophys Acta. 1983 Apr 21;730(1):49–56. doi: 10.1016/0005-2736(83)90315-2. [DOI] [PubMed] [Google Scholar]
  34. Wardzala L. J., Jeanrenaud B. Potential mechanism of insulin action on glucose transport in the isolated rat diaphragm. Apparent translocation of intracellular transport units to the plasma membrane. J Biol Chem. 1981 Jul 25;256(14):7090–7093. [PubMed] [Google Scholar]
  35. Wheeler T. J., Simpson I. A., Sogin D. C., Hinkle P. C., Cushman S. W. Detection of the rat adipose cell glucose transporter with antibody against the human red cell glucose transporter. Biochem Biophys Res Commun. 1982 Mar 15;105(1):89–95. doi: 10.1016/s0006-291x(82)80014-4. [DOI] [PubMed] [Google Scholar]
  36. Zorzano A., Balon T. W., Garetto L. P., Goodman M. N., Ruderman N. B. Muscle alpha-aminoisobutyric acid transport after exercise: enhanced stimulation by insulin. Am J Physiol. 1985 May;248(5 Pt 1):E546–E552. doi: 10.1152/ajpendo.1985.248.5.E546. [DOI] [PubMed] [Google Scholar]
  37. Zorzano A., Balon T. W., Goodman M. N., Ruderman N. B. Insulin and exercise stimulate muscle alpha-aminoisobutyric acid transport by a Na+-K+-ATPase independent pathway. Biochem Biophys Res Commun. 1986 Feb 13;134(3):1342–1349. doi: 10.1016/0006-291x(86)90397-9. [DOI] [PubMed] [Google Scholar]
  38. Zorzano A., Wilkinson W., Kotliar N., Thoidis G., Wadzinkski B. E., Ruoho A. E., Pilch P. F. Insulin-regulated glucose uptake in rat adipocytes is mediated by two transporter isoforms present in at least two vesicle populations. J Biol Chem. 1989 Jul 25;264(21):12358–12363. [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES