DHHC7 palmitoylates glucose transporter 4 (Glut4) and regulates Glut4 membrane translocation

Journal of Biological Chemistry

Volumn 292, Issue 7, 2017, Pages 2979-2991

  Du, Keyong ^a   Murakami, Shoko ^b   Sun, Yingmin ^a   Kilpatrick, Casey L ^b   Luscher, Bernhard ^b  

^a TUFTS MEDICAL CENTER   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLATION; CELL MEMBRANES; INSULIN; MAMMALS;

3T3-L1 ADIPOCYTES; ACYLTRANSFERASE; DYNAMIC REGULATION; ECTOPIC EXPRESSIONS; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE TRANSPORTER 4; MEMBRANE TRANSLOCATION;

GLUCOSE;

DHHC7 PROTEIN; GLUCOSE TRANSPORTER 4; INSULIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ACYLTRANSFERASE; DHHC7 PROTEIN, MOUSE; PALMITIC ACID; SLC2A4 PROTEIN, MOUSE;

3T3-L1 CELL LINE; ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; HORMONE ACTION; HYPERGLYCEMIA; MAMMAL; MOUSE; NONHUMAN; PALMITOYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; ANIMAL; C57BL MOUSE; CELL MEMBRANE; GENETICS; GLUCOSE TOLERANCE TEST; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM;

3T3-L1 CELLS; ACYLTRANSFERASES; ADIPOCYTES; ANIMALS; CELL MEMBRANE; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORTER TYPE 4; HEK293 CELLS; HUMANS; HYPERGLYCEMIA; INSULIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PALMITIC ACID; PROTEIN TRANSPORT;

EID: 85013632747     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.747139     Document Type: Article

References (56)

1. Mitchell, D. A., Vasudevan, A., Linder, M. E., and Deschenes, R. J. (2006) Protein palmitoylation by a family of DHHC protein S-acyltransferases. J. Lipid Res. 47, 1118-1127
2. Nadolski, M. J., and Linder, M. E. (2007) Protein lipidation. FEBS J. 274, 5202-5210
3. Sorek, N., Bloch, D., and Yalovsky, S. (2009) Protein lipid modifications in signaling and subcellular targeting. Curr. Opin. Plant Biol. 12, 714-720
4. Aicart-Ramos, C., Valero, R. A., and Rodriguez-Crespo, I. (2011) Protein palmitoylation and subcellular trafficking. Biochim. Biophys. Acta. 1808, 2981-2994
5. Hornemann, T. (2015) Palmitoylation and depalmitoylation defects. J. Inherited Metab. Dis. 38, 179-186
6. Korycka, J., Lach, A., Heger, E., Boguslawska, D. M., Wolny, M., Toporkiewicz, M., Augoff, K., Korzeniewski, J., and Sikorski, A. F. (2012) Human DHHC proteins: a spotlight on the hidden player of palmitoylation. Eur. J. Cell Biol. 91, 107-117
7. Greaves, J., and Chamberlain, L. H. (2011) DHHC palmitoyl transferases: substrate interactions and (patho)physiology. Trends Biochem. Sci. 36, 245-253
8. Roth, A. F., Feng, Y., Chen, L., and Davis, N. G. (2002) The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase. J. Cell Biol. 159, 23-28
9. Lobo, S., Greentree, W. K., Linder, M. E., and Deschenes, R. J. (2002) Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J. Biol. Chem. 277, 41268-41273
10. Keller, C. A., Yuan, X., Panzanelli, P., Martin, M. L., Alldred, M., Sassoe-Pognetto, M., and Luscher, B. (2004) The γ2 subunit of GABA(A) receptors is a substrate for palmitoylation by GODZ. J. Neurosci. 24, 5881-5891
11. Fukata, M., Fukata, Y., Adesnik, H., Nicoll, R. A., and Bredt, D. S. (2004) Identification of PSD-95 palmitoylating enzymes. Neuron 44, 987-996
12. Martin, B. R. (2013) Chemical approaches for profiling dynamic palmitoylation. Biochem. Soc. Trans. 41, 43-49
13. Chaudhary, J., and Skinner, M. K. (2002) Identification of a novel gene product, Sertoli cell gene with a zinc finger domain, that is important for FSH activation of testicular Sertoli cells. Endocrinology 143, 426-435
14. Fang, C., Deng, L., Keller, C. A., Fukata, M., Fukata, Y., Chen, G., and Luscher, B. (2006) GODZ-mediated palmitoylation of GABA(A) receptors is required for normal assembly and function of GABAergic inhibitory synapses. J. Neurosci. 26, 12758-12768
15. Kilpatrick, C. L., Murakami, S., Feng, M., Wu, X., Lal, R., Chen, G., Du, K., and Luscher, B. (2016) Dissociation of Golgi-associated DHHC-type zinc finger protein (GODZ) and Sertoli cell gene with a zinc finger domainbeta (SERZ-β)-mediated palmitoylation by loss of function analyses in knockout mice. J. Biol. Chem. 291, 27371-27386
16. Thorens, B., and Mueckler, M. (2010) Glucose transporters in the 21st Century. Am. J. Physiol. Endocrinol. Metab. 298, E141-145
17. Adekola, K., Rosen, S. T., and Shanmugam, M. (2012) Glucose transporters in cancer metabolism. Curr. Opin. Oncol. 24, 650-654
18. Leto, D., and Saltiel, A. R. (2012) Regulation of glucose transport by insulin: traffic control of GLUT4. Nat. Rev. Mol. Cell Biol. 13, 383-396
19. Graham, T. E., and Kahn, B. B. (2007) Tissue-specific alterations of glucose transport and molecular mechanisms of intertissue communication in obesity and type 2 diabetes. Horm. Metab. Res. 39, 717-721
20. Shulman, G. I. (2000) Cellular mechanisms of insulin resistance. J. Clin. Invest. 106, 171-176
21. Nandi, A., Kitamura, Y., Kahn, C. R., and Accili, D. (2004) Mouse models of insulin resistance. Physiol. Rev. 84, 623-647
22. Bryant, N. J., Govers, R., and James, D. E. (2002) Regulated transport of the glucose transporter GLUT4. Nat. Rev. Mol. Cell Biol. 3, 267-277
23. Cheatham, B. (2000) GLUT4 and company: SNAREing roles in insulinregulated glucose uptake. Trends Endocrinol. Metab. 11, 356-361
24. Hoffman, N. J., and Elmendorf, J. S. (2011) Signaling, cytoskeletal, and membrane mechanisms regulating GLUT4 exocytosis. Trends Endocrinol. Metab. 22, 110-116
25. Foley, K., Boguslavsky, S., and Klip, A. (2011) Endocytosis, recycling, and regulated exocytosis of glucose transporter 4. Biochemistry 50, 3048-3061
26. Fukata, Y., and Fukata, M. (2010) Protein palmitoylation in neuronal development and synaptic plasticity. Nat. Rev. Neurosci. 11, 161-175
27. Galic, S., Oakhill, J. S., and Steinberg, G. R. (2010) Adipose tissue as an endocrine organ. Mol. Cell. Endocrinol. 316, 129-139
28. Kajimura, S., and Saito, M. (2014) A new era in brown adipose tissue biology: molecular control of brown fat development and energy homeostasis. Annu. Rev. Physiol. 76, 225-249
29. Ren, W., Jhala, U. S., and Du, K. (2013) Proteomic analysis of protein palmitoylation in adipocytes. Adipocyte 2, 17-28
30. Ren, W., Sun, Y., and Du, K. (2015) Glut4 palmitoylation at Cys-223 plays a critical role in Glut4 membrane trafficking. Biochem. Biophys. Res. Commun. 460, 709-714
31. Martin, B. R., and Cravatt, B. F. (2009) Large-scale profiling of protein palmitoylation in mammalian cells. Nat. Methods 6, 135-138
32. Mitchell, D. A., Hamel, L. D., Ishizuka, K., Mitchell, G., Schaefer, L. M., and Deschenes, R. J. (2012) The Erf4 subunit of the yeast Ras palmitoyl acyltransferase is required for stability of the Acyl-Erf2 intermediate and palmitoyl transfer to a Ras2 substrate. J. Biol. Chem. 287, 34337-34348
33. Ebina, Y., Edery, M., Ellis, L., Standring, D., Beaudoin, J., Roth, R. A., and Rutter, W. J. (1985) Expression of a functional human insulin receptor from a cloned cDNA in Chinese hamster ovary cells. Proc. Natl. Acad. Sci. U.S.A. 82, 8014-8018
34. Bogan, J. S., Hendon, N., McKee, A. E., Tsao, T. S., and Lodish, H. F. (2003) Functional cloning of TUG as a regulator of GLUT4 glucose transporter trafficking. Nature 425, 727-733
35. Omata, W., Shibata, H., Suzuki, Y., Tanaka, S., Suzuki, T., Takata, K., and Kojima, I. (1997) Subcellular distribution of GLUT4 in Chinese hamster ovary cells overexpressing mutant dynamin: evidence that dynamin is a regulatory GTPase in GLUT4 endocytosis. Biochem. Biophys. Res. Commun. 241, 401-406
36. Lampson, M. A., Racz, A., Cushman, S. W., and McGraw, T. E. (2000) Demonstration of insulin-responsive trafficking of GLUT4 and vpTR in fibroblasts. J. Cell Sci. 113, 4065-4076
37. Bell, G. I., Kayano, T., Buse, J. B., Burant, C. F., Takeda, J., Lin, D., Fukumoto, H., and Seino, S. (1990) Molecular biology of mammalian glucose transporters. Diabetes Care 13, 198-208
38. Green, H., and Meuth, M. (1974) An established pre-adipose cell line and its differentiation in culture. Cell 3, 127-133
39. Ross, S. A., Herbst, J. J., Keller, S. R., and Lienhard, G. E. (1997) Trafficking kinetics of the insulin-regulated membrane aminopeptidase in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 239, 247-251
40. Gonzalez Montoro, A., Quiroga, R., and Valdez Taubas, J. (2013) Zinc co-ordination by the DHHC cysteine-rich domain of the palmitoyltransferase Swf1. Biochem. J. 454, 427-435
41. Ohno, Y., Kashio, A., Ogata, R., Ishitomi, A., Yamazaki, Y., and Kihara, A. (2012) Analysis of substrate specificity of human DHHC protein acyltransferases using a yeast expression system. Mol. Biol. Cell 23, 4543-4551
42. Lai, J., and Linder, M. E. (2013) Oligomerization of DHHC protein Sacyltransferases. J. Biol. Chem. 288, 22862-22870
43. Pouliot, J. F., and Beliveau, R. (1995) Palmitoylation of the glucose transporter in blood-brain barrier capillaries. Biochim. Biophys. Acta 1234, 191-196
44. Wei, X., Song, H., and Semenkovich, C. F. (2014) Insulin-regulated protein palmitoylation impacts endothelial cell function. Arterioscler. Thromb. Vasc. Biol. 34, 346-354
45. Lievens, P. M., Kuznetsova, T., Kochlamazashvili, G., Cesca, F., Gorinski, N., Galil, D. A., Cherkas, V., Ronkina, N., Lafera, J., Gaestel, M., Ponimaskin, E., and Dityatev, A. (2016) ZDHHC3 tyrosine phosphorylation regulates NCAM palmitoylation. Mol. Cell. Biol. 36, 2208-2225
46. Yang, W., Di Vizio, D., Kirchner, M., Steen, H., and Freeman, M. R. (2010) Proteome scale characterization of human S-acylated proteins in lipid raft-enriched and non-raft membranes. Mol. Cell. Proteomics 9, 54-70
47. Kang, R., Wan, J., Arstikaitis, P., Takahashi, H., Huang, K., Bailey, A. O., Thompson, J. X., Roth, A. F., Drisdel, R. C., Mastro, R., Green, W. N., Yates, J. R., 3rd, Davis, N. G., and El-Husseini, A. (2008) Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation. Nature 456, 904-909
48. Greaves, J., and Chamberlain, L. H. (2010) S-Acylation by the DHHC protein family. Biochem. Soc. Trans. 38, 522-524
49. Ren, W., Cheema, S., and Du, K. (2012) The association of ClipR-59 protein with AS160 modulates AS160 protein phosphorylation and adipocyte Glut4 protein membrane translocation. J. Biol. Chem. 287, 26890-26900
50. Stenkula, K. G., Lizunov, V. A., Cushman, S. W., and Zimmerberg, J. (2010) Insulin controls the spatial distribution of GLUT4 on the cell surface through regulation of its postfusion dispersal. Cell Metab. 12, 250-259
51. Shmueli, A., Segal, M., Sapir, T., Tsutsumi, R., Noritake, J., Bar, A., Sapoznik, S., Fukata, Y., Orr, I., Fukata, M., and Reiner, O. (2010) Ndel1 palmitoylation: a new mean to regulate cytoplasmic dynein activity. EMBO J. 29, 107-119
52. Du, K., Herzig, S., Kulkarni, R. N., and Montminy, M. (2003) TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 300, 1574-1577
53. Ren, W., Sun, Y., and Du, K. (2013) DHHC17 palmitoylates ClipR-59 and modulates ClipR-59 association with the plasma membrane. Mol. Cell. Biol. 33, 4255-4265
54. Ding, J., and Du, K. (2009) ClipR-59 interacts with Akt and regulates Akt cellular compartmentalization. Mol. Cell Biol. 29, 1459-1471
55. Ren, W., Sun, Y., Cheema, S., and Du, K. (2013) Interaction of constitutive photomorphogenesis 1 protein with protein-tyrosine phosphatase 1B suppresses protein-tyrosine phosphatase 1B activity and enhances insulin signaling. J. Biol. Chem. 288, 10902-10913
56. Du, K., and Yingmin, S. (2015) ClipR-59 plays a critical role in the regulation of body glucose homeostasis. Adipocyte 4, 286-294