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. 1994 Jan 15;297(Pt 2):289–295. doi: 10.1042/bj2970289

Structural disruption of the trans-Golgi network does not interfere with the acute stimulation of glucose and amino acid uptake by insulin-like growth factor I in muscle cells.

H S Hundal 1, P J Bilan 1, T Tsakiridis 1, A Marette 1, A Klip 1
PMCID: PMC1137827  PMID: 8297333

Abstract

The effects of insulin-like growth factor I (IGF-I) on glucose and amino acid uptake were investigated in fully differentiated L6 muscle cells, in order to determine whether the two processes are functionally related. Transport of both glucose and amino acid (methylaminoisobutyric acid, MeAIB) was activated rapidly in response to IGF-I. Stimulation reached a peak within 30 min and was sustained for up to 90 min. Maximal activation of either glucose or MeAIB transport was achieved at 3 nM IGF-I; the half-maximal activation (ED50) of glucose transport was at 107 pM and that of MeAIB transport was at 36 pM. Stimulation of amino acid uptake occurred in the absence or presence of glucose, suggesting that this response is not secondary to increased glucose intake. Incubation of cells for 1 h with Brefeldin A (5 micrograms/ml), which disassembles the Golgi apparatus and inhibits the secretory pathway in eukaryotic cells, had no effect on the acute IGF-I activation of glucose and MeAIB transport. Moreover, Brefeldin A caused wide redistribution of the trans-Golgi antigen TGN38, as assessed by subcellular fractionation, without affecting the distribution of glucose transporters. The finding that the degree of activation, time response and sensitivity to IGF-I and Brefeldin A were similar for both glucose and MeAIB transport suggests commonalities in the IGF-I mechanism of recruitment of glucose transporters and stimulation of amino acid transport through System A. An integral trans-Golgi network does not appear to be required for the acute IGF-I stimulation of glucose or amino acid transport, even though stimulation of glucose transport occurs through recruitment of glucose transporters from intracellular stores in these cells. We propose that the donor site of glucose transporters (and perhaps of amino acid transporters) involved in the acute response to IGF-I lies beyond the trans-Golgi network, perhaps in an endosomal compartment in close proximity to the plasma membrane.

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Selected References

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  1. Beguinot F., Kahn C. R., Moses A. C., Smith R. J. Distinct biologically active receptors for insulin, insulin-like growth factor I, and insulin-like growth factor II in cultured skeletal muscle cells. J Biol Chem. 1985 Dec 15;260(29):15892–15898. [PubMed] [Google Scholar]
  2. Bilan P. J., Mitsumoto Y., Maher F., Simpson I. A., Klip A. Detection of the GLUT3 facilitative glucose transporter in rat L6 muscle cells: regulation by cellular differentiation, insulin and insulin-like growth factor-I. Biochem Biophys Res Commun. 1992 Jul 31;186(2):1129–1137. doi: 10.1016/0006-291x(92)90864-h. [DOI] [PubMed] [Google Scholar]
  3. Bilan P. J., Ramlal T., Klip A. IGF-I mediated recruitment of glucose transporters from intracellular membranes to plasma membranes in L6 muscle cells. Adv Exp Med Biol. 1991;293:273–288. doi: 10.1007/978-1-4684-5949-4_25. [DOI] [PubMed] [Google Scholar]
  4. Blok J., Gibbs E. M., Lienhard G. E., Slot J. W., Geuze H. J. Insulin-induced translocation of glucose transporters from post-Golgi compartments to the plasma membrane of 3T3-L1 adipocytes. J Cell Biol. 1988 Jan;106(1):69–76. doi: 10.1083/jcb.106.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Burant C. F., Treutelaar M. K., Allen K. D., Sens D. A., Buse M. G. Comparison of insulin and insulin-like growth factor I receptors from rat skeletal muscle and L-6 myocytes. Biochem Biophys Res Commun. 1987 Aug 31;147(1):100–107. doi: 10.1016/s0006-291x(87)80092-x. [DOI] [PubMed] [Google Scholar]
  7. Christensen H. N. Role of amino acid transport and countertransport in nutrition and metabolism. Physiol Rev. 1990 Jan;70(1):43–77. doi: 10.1152/physrev.1990.70.1.43. [DOI] [PubMed] [Google Scholar]
  8. Cushman S. W., Wardzala L. J. Potential mechanism of insulin action on glucose transport in the isolated rat adipose cell. Apparent translocation of intracellular transport systems to the plasma membrane. J Biol Chem. 1980 May 25;255(10):4758–4762. [PubMed] [Google Scholar]
  9. Douen A. G., Ramlal T., Rastogi S., Bilan P. J., Cartee G. D., Vranic M., Holloszy J. O., Klip A. Exercise induces recruitment of the "insulin-responsive glucose transporter". Evidence for distinct intracellular insulin- and exercise-recruitable transporter pools in skeletal muscle. J Biol Chem. 1990 Aug 15;265(23):13427–13430. [PubMed] [Google Scholar]
  10. Friedman J. E., Dudek R. W., Whitehead D. S., Downes D. L., Frisell W. R., Caro J. F., Dohm G. L. Immunolocalization of glucose transporter GLUT4 within human skeletal muscle. Diabetes. 1991 Jan;40(1):150–154. doi: 10.2337/diab.40.1.150. [DOI] [PubMed] [Google Scholar]
  11. Fujiwara T., Oda K., Yokota S., Takatsuki A., Ikehara Y. Brefeldin A causes disassembly of the Golgi complex and accumulation of secretory proteins in the endoplasmic reticulum. J Biol Chem. 1988 Dec 5;263(34):18545–18552. [PubMed] [Google Scholar]
  12. 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]
  13. Hendricks L. C., McClanahan S. L., Palade G. E., Farquhar M. G. Brefeldin A affects early events but does not affect late events along the exocytic pathway in pancreatic acinar cells. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7242–7246. doi: 10.1073/pnas.89.15.7242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Hundal H. S., Ramlal T., Reyes R., Leiter L. A., Klip A. Cellular mechanism of metformin action involves glucose transporter translocation from an intracellular pool to the plasma membrane in L6 muscle cells. Endocrinology. 1992 Sep;131(3):1165–1173. doi: 10.1210/endo.131.3.1505458. [DOI] [PubMed] [Google Scholar]
  16. Hunziker W., Whitney J. A., Mellman I. Brefeldin A and the endocytic pathway. Possible implications for membrane traffic and sorting. FEBS Lett. 1992 Jul 27;307(1):93–96. doi: 10.1016/0014-5793(92)80908-y. [DOI] [PubMed] [Google Scholar]
  17. Klausner R. D., Donaldson J. G., Lippincott-Schwartz J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol. 1992 Mar;116(5):1071–1080. doi: 10.1083/jcb.116.5.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Koivisto U. M., Martinez-Valdez H., Bilan P. J., Burdett E., Ramlal T., Klip A. Differential regulation of the GLUT-1 and GLUT-4 glucose transport systems by glucose and insulin in L6 muscle cells in culture. J Biol Chem. 1991 Feb 5;266(4):2615–2621. [PubMed] [Google Scholar]
  19. Kong C. T., Yet S. F., Lever J. E. Cloning and expression of a mammalian Na+/amino acid cotransporter with sequence similarity to Na+/glucose cotransporters. J Biol Chem. 1993 Jan 25;268(3):1509–1512. [PubMed] [Google Scholar]
  20. Ladinsky M. S., Howell K. E. The trans-Golgi network can be dissected structurally and functionally from the cisternae of the Golgi complex by brefeldin A. Eur J Cell Biol. 1992 Oct;59(1):92–105. [PubMed] [Google Scholar]
  21. Lamphere L., Lienhard G. E. Components of signaling pathways for insulin and insulin-like growth factor-I in muscle myoblasts and myotubes. Endocrinology. 1992 Nov;131(5):2196–2202. doi: 10.1210/endo.131.5.1385098. [DOI] [PubMed] [Google Scholar]
  22. Lippincott-Schwartz J., Yuan L., Tipper C., Amherdt M., Orci L., Klausner R. D. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell. 1991 Nov 1;67(3):601–616. doi: 10.1016/0092-8674(91)90534-6. [DOI] [PubMed] [Google Scholar]
  23. Luzio J. P., Brake B., Banting G., Howell K. E., Braghetta P., Stanley K. K. Identification, sequencing and expression of an integral membrane protein of the trans-Golgi network (TGN38). Biochem J. 1990 Aug 15;270(1):97–102. doi: 10.1042/bj2700097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mitsumoto Y., Burdett E., Grant A., Klip A. Differential expression of the GLUT1 and GLUT4 glucose transporters during differentiation of L6 muscle cells. Biochem Biophys Res Commun. 1991 Mar 15;175(2):652–659. doi: 10.1016/0006-291x(91)91615-j. [DOI] [PubMed] [Google Scholar]
  25. Mitsumoto Y., Klip A. Development regulation of the subcellular distribution and glycosylation of GLUT1 and GLUT4 glucose transporters during myogenesis of L6 muscle cells. J Biol Chem. 1992 Mar 5;267(7):4957–4962. [PubMed] [Google Scholar]
  26. Ramlal T., Sarabia V., Bilan P. J., Klip A. Insulin-mediated translocation of glucose transporters from intracellular membranes to plasma membranes: sole mechanism of stimulation of glucose transport in L6 muscle cells. Biochem Biophys Res Commun. 1988 Dec 30;157(3):1329–1335. doi: 10.1016/s0006-291x(88)81020-9. [DOI] [PubMed] [Google Scholar]
  27. Reaves B., Wilde A., Banting G. Identification, molecular characterization and immunolocalization of an isoform of the trans-Golgi-network (TGN)-specific integral membrane protein TGN38. Biochem J. 1992 Apr 15;283(Pt 2):313–316. doi: 10.1042/bj2830313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Robinson L. J., James D. E. Insulin-regulated sorting of glucose transporters in 3T3-L1 adipocytes. Am J Physiol. 1992 Aug;263(2 Pt 1):E383–E393. doi: 10.1152/ajpendo.1992.263.2.E383. [DOI] [PubMed] [Google Scholar]
  29. Rodnick K. J., Slot J. W., Studelska D. R., Hanpeter D. E., Robinson L. J., Geuze H. J., James D. E. Immunocytochemical and biochemical studies of GLUT4 in rat skeletal muscle. J Biol Chem. 1992 Mar 25;267(9):6278–6285. [PubMed] [Google Scholar]
  30. Rosa P., Barr F. A., Stinchcombe J. C., Binacchi C., Huttner W. B. Brefeldin A inhibits the formation of constitutive secretory vesicles and immature secretory granules from the trans-Golgi network. Eur J Cell Biol. 1992 Dec;59(2):265–274. [PubMed] [Google Scholar]
  31. Sargeant R., Mitsumoto Y., Sarabia V., Shillabeer G., Klip A. Hormonal regulation of glucose transporters in muscle cells in culture. J Endocrinol Invest. 1993 Feb;16(2):147–162. doi: 10.1007/BF03347669. [DOI] [PubMed] [Google Scholar]
  32. Shainberg A., Yagil G., Yaffe D. Alterations of enzymatic activities during muscle differentiation in vitro. Dev Biol. 1971 May;25(1):1–29. doi: 10.1016/0012-1606(71)90017-0. [DOI] [PubMed] [Google Scholar]
  33. Shite S., Seguchi T., Shimada T., Ono M., Kuwano M. Rapid turnover of low-density lipoprotein receptor by a non-lysosomal pathway in mouse macrophage J774 cells and inhibitory effect of brefeldin A. Eur J Biochem. 1990 Jul 31;191(2):491–497. doi: 10.1111/j.1432-1033.1990.tb19148.x. [DOI] [PubMed] [Google Scholar]
  34. Suzuki K., Kono T. Evidence that insulin causes translocation of glucose transport activity to the plasma membrane from an intracellular storage site. Proc Natl Acad Sci U S A. 1980 May;77(5):2542–2545. doi: 10.1073/pnas.77.5.2542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Yaffe D. Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc Natl Acad Sci U S A. 1968 Oct;61(2):477–483. doi: 10.1073/pnas.61.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]

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