Increased expression of the SNARE accessory protein Munc18c in lipid-mediated insulin resistance

Journal of Lipid Research

Volumn 44, Issue 6, 2003, Pages 1174-1181

  Schlaepfer, Isabel R ^a   Pulawa, Leslie K ^a   Ferreira, Luis D M C B ^a,c   James, David E ^b,d   Capell, Warren H ^a   Eckel, Robert H ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

GLUT4; Muscle; Soluble N ethylmaleimide sensitive factor attachment protein receptor

Indexed keywords

N ETHYLMALEIMIDE; PROTEIN MUNC18C; SNARE PROTEIN; SYNTAXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FATTY ACID METABOLISM; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; INSULIN RESISTANCE; LIPID METABOLISM; MAMMAL CELL; MEMBRANE VESICLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; TRANSCRIPTION REGULATION;

ANIMALS; BLOOD GLUCOSE; CELLS, CULTURED; DIETARY FATS; INSULIN RESISTANCE; LIPID METABOLISM; LIPOPROTEIN LIPASE; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MUNC18 PROTEINS; MUSCLE FIBERS; MUSCLE, SKELETAL; NERVE TISSUE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SNARE PROTEINS; TRANSFECTION; VESICULAR TRANSPORT PROTEINS;

EID: 0142105867     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.M300003-JLR200     Document Type: Article

References (45)

1. Mokdad, A. H., E. S. Ford, B. A. Bowman, D. E. Nelson, M. M. Engelgau, F. Vinicor, and J. S. Marks. 2001. The continuing increase of diabetes in the US. Diabetes Care. 24: 412.
2. Shulman, G. I. 2000. Cellular mechanisms of insulin resistance. J. Clin. Invest. 106: 171-176.
3. Eckel, R. H. 1989. Lipoprotein lipase. A multifunctional enzyme relevant to common metabolic diseases. N. Engl. J. Med. 320: 1060-1068.
4. Jensen, D. R., I. R. Schlaepfer, C. L. Morin, D. S. Pennington, T. Marcell, S. M. Ammon, A. Gutierrez-Hartmann, and R. H. Eckel. 1997. Prevention of diet-induced obesity in transgenic mice overexpressing skeletal muscle lipoprotein lipase. Am. J. Physiol. 273: R683-R689.
5. Ferreira, L. D. M. C. B., L. K. Pulawa, D. R. Jensen, and R. H. Eckel. 2001. Overexpressing human lipoprotein lipase in mouse skeletal muscle is associated with insulin resistance. Diabetes. 50: 1064-1068.
6. Douen, A. G., T. Ramlal, S. Rastogi, P. J. Bilan, G. D. Cartee, M. Vranic, J. O. Holloszy, and A. Klip. 1990. 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. 265: 13427-13430.
7. Foster, L. J., and A. Klip. 2000. Mechanism and regulation of GLUT-4 vesicle fusion in muscle and fat cells. Am. J. Physiol. Cell Physiol. 279: C877-C890.
8. Tellam, J. T., S. McIntosh, and D. E. James. 1995. Molecular identification of two novel Munc-18 isoforms expressed in non-neuronal tissues. J. Biol. Chem. 270: 5857-5863.
9. Khan, A. H., D. C. Thurmond, C. Yang, C. D. Sigmund, and J. E. Pessin. 2001. Munc18c regulates insulin-stimulated GLUT4 translocation to the transverse tubules in skeletal muscle. J. Biol. Chem. 276:4063-4069.
10. Roden, M., T. B. Price, G. Perseghin, K. F. Petersen, D. L. Rothman, G. W. Cline, and G. I. Shulman. 1996. Mechanism of free fatty acid-induced insulin resistance in humans. J. Clin. Invest. 97: 2859-2865.
11. Goodpaster, B. H., J. He, S. Watkins, and D. E. Kelley. 2001. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J. Clin. Endocrinol. Metab. 86: 5755-5761.
12. Greco, A. V., G. Mingrone, A. Giancaterini, M. Manco, M. Morroni, S. Cinti, M. Granzotto, R. Vettor, S. Camastra, and E. Ferrannini. 2002. Insulin resistance in morbid obesity: reversal with intramyocellular fat depletion. Diabetes. 51: 144-151.
13. Poirier, P., T. Marcell, P. U. Huey, I. R. Schlaepfer, G. C. Orwens, D. R. Jensen, and R. H. Eckel. 2000. Increased intracellular triglyceride in C(2)C(12) muscle cells transfected with human lipoprotein lipase. Biochem. Biophys. Res. Commun. 270: 997-1001.
14. Lockhart, D. J., H. Dong, M. C. Byrne, M. T. Follettie, M. V. Gallo, M. S. Chee, M. Mittmann, C. Wang, M. Kobayashi, H. Horton, and E. L. Brown. 1996. Expression monitoring by hybridization to high-density oligonucleotide arrays. Nat. Biotechnol. 14: 1675-1680.
15. Bender, T. P., and M. E. Greenberg. 1989. Current Protocols in Molecular Biology. Wiley and Sons, New York. 4.10.1-4.10.11.
16. Zhang, J., D. Chrysis, and L. E. Underwood. 1998. Reduction of hepatic insulin-like growth factor I (IGF-I) messenger ribonucleic acid (mRNA) during fasting is associated with diminished splicing of IGF-I pre-mRNA and decreased stability of cytoplasmic IGF-I mRNA. Endocrinology. 139: 4523-4530.
17. Gotoh, K., H. Yokota, E. Kikuya, T. Watanabe, and M. Oishi. 1998. Genomic structure of MUNC18-1 protein, which is involved in docking and fusion of synaptic vesicles in brain. J. Biol. Chem. 273: 21642-21647.
18. Schlaepfer, I. R., and R. H. Eckel. 1999. Plasma triglyceride reduction in mice after direct injections of muscle-specific lipoprotein lipase DNA. Diabetes. 48: 223-227.
19. Han, D. H., P. A. Hansen, H. H. Host, and J. O. Holloszy. 1997. Insulin resistance of muscle glucose transport in rats fed a high-fat diet: a reevaluation. Diabetes. 46: 1761-1767.
20. Kraegen, E. W., P. W. Clark, A. B. Jenkins, E. A. Daley, D.J. Chisholm, and L. H. Storlien. 1991. Development of muscle insulin resistance after liver insulin resistance in high-fat-fed rats. Diabetes. 40:1397-1403.
21. Zierath, J. R., K. L. Houseknecht, L. Gnudi, and B. B. Kahn. 1997. High-fat feeding impairs insulin-stimulated GLUT4 recruitment via an early insulin-signaling defect. Diabetes. 46: 215-223.
22. Rea, S., L. B. Martin, S. McIntosh, S. L. Macaulay, T. Ramsdale, G. Baldini, and D. E. James. 1998. Syndet, an adipocyte target SNARE involved in the insulin-induced translocation of GLUT4 to the cell surface. J. Biol. Chem. 273: 18784-18792.
23. Pessin, J. E., and A. R. Saltiel. 2000. Signaling pathways in insulin action: molecular targets of insulin resistance. J. Clin. Invest. 106: 165-169.
24. St. Denis, J. F., and S. W. Cushman. 1998. Role of SNAREs in the GLUT4 translocation response to insulin in adipose cells and muscle. J. Basic Clin. Physiol. Pharmacol. 9: 153-165.
25. Pevsner, J., S. C. Hsu, J. E. Braun, N. Calakos, A. E. Ting, M. K. Bennett, and R. H. Scheller. 1994. Specificity and regulation of a synaptic vesicle docking complex. Neuron. 13: 353-361.
26. Tellam, J. T., S. L. Macaulay, S. McIntosh, D. R. Hewish, C. W. Ward, and D. E. James. 1997. Characterization of Munc-18c and syntaxin-4 in 3T3-L1 adipocytes. Putative role in insulin-dependent movement of GLUT-4. J. Biol. Chem. 272: 6179-6186.
27. Egerton, M., J. Zueco, and A. Boyd. 1993. Molecular characterization of the SEC1 gene of Saccharomyces cerevisiae: subcellular distribution of a protein required for yeast protein secretion. Yeast. 9: 703-713.
28. Verhage, M., A. S. Maia, J. J. Plomp, A. B. Brussaard, J. H. Heeroma, H. Vermeer, R. F. Toonen, R. E. Hammer, T. K. van den Berg, M. Missler, H. J. Geuze, and T. C. Sudhof. 2000. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science. 287: 864-869.
29. Thurmond, D. C., and J. E. Pessin. 2000. Discrimination of GLUT4 vesicle trafficking from fusion using a temperature-sensitive Munc18c mutant. EMBO J. 19: 3565-3575.
30. Bryant, N. J., and D. E. James. 2001. Vps45p stabilizes the syntaxin homologue Tlg2p and positively regulates SNARE complex formation. EMBO J. 20: 3380-3388.
31. Hickson, G. R., L. H. Chamberlain, V. H. Maier, and G. W. Gould. 2000. Quantification of SNARE protein levels in 3T3-L1 adipocytes: implications for insulin-stimulated glucose transport. Biochem. Biophys. Res. Commun. 270: 841-845.
32. Levak-Frank, S., P. H. Weinstock, T. Hayek, R. Verdery, W. Hofmann, R. Ramakrishnan, W. Sattler, J. L. Breslow, and R. Zechner. 1997. Induced mutant mice expressing lipoprotein lipase exclusively in muscle have subnormal triglycerides yet reduced high density lipoprotein cholesterol levels in plasma. J. Biol. Chem. 272: 17182-17190.
33. Kim, K. K., J. J. Fillmore, Y. Chen, C. Yu, I. K. Moore, M. Pypaert, E. P. Lutz, Y. Kako, W. Velez-Carrasco, I. J. Goldberg, J. L. Breslow, and G. I. Shulman. 2001. Tissue-specific overexpression of lipoprotein lipase causes tissue- specific insulin resistance. Proc. Natl. Acad. Sci. USA. 98: 7522-7527.
34. Thurmond, D. C., M. Kanzaki, A. H. Khan, and J. E. Pessin. 2000. Munc18c function is required for insulin-stimulated plasma membrane fusion of GLUT4 and insulin-responsive amino peptidase storage vesicles. Mol. Cell. Biol. 20: 379-388.
35. Thurmond, D. C., B. P. Ceresa, S. Okada, J. S. Elmendorf, K. Coker, and J. E. Pessin. 1998. Regulation of insulin-stimulated GLUT4 translocation by Munc18c in 3T3L1 adipocytes. J. Biol. Chem. 273: 33876-33883.
36. Fujita, H., P. L. Tuma, C. M. Finnegan, L. Locco, and A. L. Hubbard. 1998. Endogenous syntaxins 2, 3 and 4 exhibit distinct but overlapping patterns of expression at the hepatocyte plasma membrane. Biochem. J. 329: 527-538.
37. Foster, L.J., K. Yaworsky, W. S. Trimble, and A. Klip. 1999. SNAP23 promotes insulin-dependent glucose uptake in 3T3-L1 adipocytes: possible interaction with cytoskeleton. Am. J. Physiol. 276: C1108-C1114.
38. Sarabia, V., T. Ramlal, and A. Klip. 1990. Glucose uptake in human and animal muscle cells in culture. Biochem. Cell Biol. 68: 536-542.
39. Michael, L. F., Z. Wu, R. B. Cheatham, P. Puigserver, G. Adelmant, J. J. Lehman, D. P. Kelly, and B. M. Spiegelman. 2001. Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC1. Proc. Natl. Acad. Sci. USA. 98: 3820-3825.
40. Tortorella, L. L., and P. F. Pilch. 2002. C2C12 myocytes lack an insulin-responsive vesicular compartment despite dexamethasone-induced GLUT4 expression. Am. J. Physiol. Endocrinol. Metab. 283: E514-E524.
41. Griffin, M. E., M.J. Marcucci, G. W. Cline, K. Bell, N. Barucci, D. Lee, L. J. Goodyear, E. W. Kraegen, M. F. White, and G. I. Shulman. 1999. Free fatty acid-induced insulin resistance is associated with activation of protein kinase C theta and alterations in the insulin signaling cascade. Diabetes. 48: 1270-1274.
42. Schmitz-Peiffer, C. 2000. Signalling aspects of insulin resistance in skeletal muscle: mechanisms induced by lipid oversupply. Cell. Signal. 12: 583-594.
43. Kelley, D. E., and L. J. Mandarino. 2000. Fuel selection in human skeletal muscle in insulin resistance-A reexamination. Diabetes. 49:677-683.
44. Abel, E. D., O. Peroni, J. K. Kim, Y. B. Kim, O. Boss, E. Hadro, T. Minnemann, G. I. Shulman, and B. B. Kahn. 2001. Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature. 409: 729-733.
45. Summers, S. A., L. A. Garza, H. L. Zhou, and M. J. Birnbaum. 1998. Regulation of insulin-stimulated glucose transporter GLUT4 translocation and Akt kinase activity by ceramide. Mol. Cell. Biol. 18: 5457-5464.