Phosphoinositides in insulin action on GLUT4 dynamics: Not just PtdIns(3,4,5)P3

American Journal of Physiology - Endocrinology and Metabolism

Volumn 295, Issue 3, 2008, Pages

  Shisheva, Assia ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Fat and muscle cells; Glucose transport; Glucose transporter 4; Phosphatidylinositol bisphosphates; Phosphatidylinositol monophosphates

Indexed keywords

FAT; GLUCOSE; GLUCOSE TRANSPORTER 4; INSULIN; INSULIN RECEPTOR; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; WORTMANNIN; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 3,4,5-TRIPHOSPHATE; POLYPHOSPHOINOSITIDE;

CELL MEMBRANE; CELL SURFACE; ENZYME ACTIVATION; ENZYME REGULATION; GLUCOSE TRANSPORT; MOLECULAR DYNAMICS; MUSCLE CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; REVIEW; ANIMAL; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALS; GLUCOSE TRANSPORTER TYPE 4; HUMANS; INSULIN; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHATIDYLINOSITOLS;

EID: 53149105150     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.90353.2008     Document Type: Review

References (76)

1. Berwick DC, Dell GC, Welsh GI, Heesom KJ, Hers I, Fletcher LM, Cook FT, Tavaré JM. Protein kinase B phosphorylation of PIKfyve regulates the trafficking of GLUT4 vesicles. J Cell Sci 117: 5985-5993, 2004.
2. Bose A, Guilherme A, Robida SI, Nicoloro SM, Zhou QL, Jiang ZY, Pomerleau DP, Czech MP. Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c. Nature 420: 821-824, 2002.
3. Bose A, Robida S, Furcinitti PS, Chawla A, Fogarty K, Corvera S, Czech MP. Unconventional myosin Myo1c promotes membrane fusion in a regulated exocytic pathway. Mol Cell Biol 24: 5447-5458, 2004.
4. Brown RA, Domin J, Acaro A, Waterfield MD, Shepherd PR. Insulin activates the alpha isoform of class II phosphoinositide 3-kinases. J Biol Chem 274: 14529-14532, 1999.
5. Carricaburu V, Lamia KA, Lo E, Lavereaux L, Payrastre B, Cantley LC, Rameh LE. The phosphatidylinositol (PI)-5-phosphate 4-kinase type II enzyme controls insulin signaling by regulating PI-3,4,5-trisphosphate degradation. Proc Natl Acad Sci USA 100: 9867-9872, 2003.
6. Chang L, Chiang SH, Saltiel AR. TC10α is required for insulin-stimulated glucose uptake in adipocytes. Endocrinology 148: 27-33, 2007.
7. Chaussade C, Pirola L, Bonnafous S, Blondeau F, Brenz-Verca S, Tronchère H, Portis F, Rusconi S, Payrastre B, Laporte J, Van Obberghen E. Expression of myotubularin by an adenoviral vector demonstrates its function as a phosphatidylinositol 3-phosphate [PtdIns(3)P] phosphatase in muscle cell lines: involvement of PtdIns(3)P in insulin-stimulated glucose transport. Mol Endocrinol 17: 2448-2460, 2003.
8. Chen XW, Leto D, Chiang SH, Wang Q, Saltiel AR. Activation of RalA is required for insulin-stimulated Glut4 trafficking to the plasma membrane via the exocyst and the motor protein Myo1c. Dev Cell 3: 391-404, 2007.
9. Chen G, Raman P, Bhonagiri P, Strawbridge AB, Pattar GR, Elmendorf JS. Protective effect of phosphatidylinositol 4,5-bisphosphate against cortical filamentous actin loss and insulin resistance induced by sustained exposure of 3T3-L1 adipocytes to insulin. J Biol Chem 279: 39705-39709, 2004.
10. Czech MP. Dynamics of phosphoinositides in membrane retrieval and insertion. Annu Rev Physiol 65: 791-815, 2003.
11. Del Vecchio RL, Pilch PF. Phosphatidylinositol 4-kinase is a component of glucose transporter (GLUT4)-containing vesicles. J Biol Chem 266: 13278-13283, 1991.
12. Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 443: 651-657, 2006.
13. Dugani CB, Klip A. Glucose transporter 4: cycling, compartments and controversies. EMBO Rep 6: 1137-1142, 2005.
14. Falasca M, Hughes WE, Dominguez V, Sala G, Fostira F, Fang MQ, Cazzolli R, Shepherd PR, James DE, Maffucci T. The role of phosphoinositide 3-kinase C2α in insulin signaling. J Biol Chem 282: 28226-28236, 2007.
15. Foster LJ, Li D, Randhawa VK, Klip A. Insulin accelerates inter-endosomal GLUT4 traffic via phosphatidylinositol 3-kinase and protein kinase B. J Biol Chem 276: 44212-44221, 2001.
16. Funaki M, DiFransico L, Janmey PA. PI 4,5-P2 stimulates glucose transport activity of GLUT4 in the plasma membrane of 3T3-L1 adipocytes. Biochim Biophys Acta 1763: 889-899, 2006.
17. Furtado LM, Poon V, Klip A. GLUT4 activation: thoughts on possible mechanisms. Acta Physiol Scand 178: 287-296, 2003.
18. Huang S, Lifshitz L, Patki-Kamath V, Ruft R, Fogarty K, Czech MP. Phosphatidylinositol-4,5-bisphosphate-rich plasma membrane patches organize active zones of endocytosis and ruffling in cultured adipocytes. Mol Cell Biol 24: 9102-9123, 2004.
19. Huang S, Czech MP. The GLUT4 glucose transporter. Cell Metab 5: 237-252, 2007.
20. Ikonomov OC, Sbrissa D, Shisheva A. Mammalian cell morphology and endocytic membrane homeostasis require enzymatically active phosphoinositide 5-kinase PIKfyve. J Biol Chem 276: 26141-26147, 2001.
21. Ikonomov OC, Sbrissa D, Mlak K, Shisheva A. Requirement for PIKfyve enzymatic activity in acute and long-term insulin cellular effects. Endocrinology 143: 4742-4754, 2002.
22. 2 synthesis to regulate early endosome dynamics and fusion. Am J Physiol Cell Physiol 291: C393-C404, 2006.
23. Ikonomov OC, Sbrissa D, Dondapati R, Shisheva A. ArPIKfyve-PIKfyve interaction and role in insulin-regulated GLUT4 translocation and glucose transport in 3T3-L1 adipocytes. Exp Cell Res 313: 2404-2416, 2007.
24. Ikonomov OC, Sbrissa D, Fligger J, Foti M, Carpentier JL, Shisheva A. PIKfyve controls fluid-phase endocytosis but not recycling/degradation of endocytosed receptors or sorting of procathepsin D by regulating multivesicular body morphogenesis. Mol Biol Cell 14: 4581-4591, 2003.
25. Inoue M, Chiang SH, Chang L, Chen XW, Saltiel AR. Compartmentalization of the exocyst complex in lipid rafts controls Glut4 vesicle tethering. Mol Biol Cell 17: 2303-2311, 2006.
26. Ishiki M, Randhawa VK, Poon V, JeBailey L, Klip A. Insulin regulates the membrane arrival, fusion, and C-terminal unmasking of glucose transporter-4 via distinct phosphoinositides. J Biol Chem 280: 28792-28802, 2005.
27. JeBailey L, Rudich A, Huang X, Di Ciano-Oliveira C, Kapus A, Klip A. Skeletal muscle cells and adipocytes differ in their reliance on TC10 and Rac for insulin-induced actin remodeling. Mol Endocrinol 18: 359-372, 2004.
28. Jiang ZY, Chawla A, Bose A, Way M, Czech MP. A phosphatidylinositol 3-kinase-independent insulin signaling pathway to N-WASP/Arp2/3/F-actin required for GLUT4 glucose transporter recycling. J Biol Chem 277: 509-515, 2002.
29. Kanda H, Tamori Y, Shinoda H, Yoshikawa M, Sakaue M, Udagawa J, Otani H, Tashiro F, Miyazaki JI, Kasuga M. Adipocytes from Munc18c-null mice show increased sensitivity to insulin-stimulated GLUT4 externalization. J Clin Invest 115: 291-301, 2005.
30. Kanzaki M, Furukawa M, Raab W, Pessin JE. Phosphatidylinositol 4,5-bisphosphate regulates adipocyte actin dynamics and GLUT4 vesicle recycling. J Biol Chem 279: 30622-30633, 2004.
31. Kanzaki M, Watson RT, Hou JC, Stamnes M, Saltiel AR, Pessin JE. Small GTP-binding protein TC10 differentially regulates two distinct populations of filamentous actin in 3T3L1 adipocytes. Mol Biol Cell 13: 2334-2346, 2002.
32. Kanzaki M, Watson RT, Khan AH, Pessin JE. Insulin stimulates actin comet tails on intracellular GLUT4-containing compartments in differentiated 3T3L1 adipocytes. J Biol Chem 276: 49331-49336, 2001.
33. Kelly KL, Ruderman NB. Insulin-stimulated phosphatidylinositol 3-kinase. J Biol Chem 268: 4391-4398, 1993.
34. Kong AM, Horan KA, Sriratana A, Bailey CG, Collyer LJ, Nandurkar HH, Shisheva A, Layton MJ, Rasko JE, Rowe T, Mitchell CA. Phosphatidylinositol 3-phosphate [PtdIns3P] is generated at the plasma membrane by an inositol polyphosphate 5-phosphatase: endogenous PtdIns3P can promote GLUT4 translocation to the plasma membrane. Mol Cell Biol 26: 6065-6081, 2006.
35. Kristiansen S, Ramlal T, Klip A. Phosphatidylinositol 4-kinase, but not phosphatidylinositol 3-kinase, is present in GLUT4-containing vesicles isolated from rat skeletal muscle. Biochem J 335: 351-356, 1998.
36. -/- mice. Mol Cell Biol 24: 5080-5087, 2004.
37. Larance M, Ramm G, James DE. The GLUT4 code. Mol Endocrinol 22: 226-233, 2008.
38. Maffucci T, Brancaccio A, Piccolo E, Stein RC, Falasca M. Insulin induces phosphatidinylinositol-3-phosphate formation through TC10 activation. EMBO J 22: 4178-4189, 2003.
39. Martin TF. PI(4,5)P(2) regulation of surface membrane traffic. Curr Opin Cell Biol 13: 493-499, 2001.
40. McCarthy AM, Spisak KO, Brozinick JT, Elmendorf JS. Loss of cortical actin filaments in insulin-resistant skeletal muscle cells impairs GLUT4 vesicle trafficking and glucose transport. Am J Physiol Cell Physiol 291: C860-C868, 2006.
41. Minokoshi Y, Kahn CR, Kahn BB. Tissue-specific ablation of the GLUT4 glucose transporter or the insulin receptor challenges assumptions about insulin action and glucose homeostasis. J Biol Chem 278: 33609-33612, 2003.
42. Mora S, Durham PL, Smith JR, Russo AF, Jeromin A, Pessin JE. NCS-1 inhibits insulin-stimulated GLUT4 translocation in 3T3L1 adipocytes through a phosphatidylinositol 4-kinase-dependent pathway. J Biol Chem 277: 27494-27500, 2002.
43. Navé BT, Siddle K, Shepherd PR. Phorbol esters stimulate phosphatidylinositol 3,4,5-trisphosphate production in 3T3-L1 adipocytes: implications for stimulation of glucose transport. Biochem J 318: 203-205, 1996.
44. Nicot AS, Fares H, Payrastre B, Chisholm AD, Labouesse M, Laporte J. The phosphoinositide kinase PIKfyve/Fab1p regulates terminal lysosome maturation in Caenorhabditis elegans. Mol Biol Cell 17: 3052-3074, 2006.
45. Niebuhr K, Giuriato S, Pedron T, Philpott DJ, Gaits F, Sable J, Sheetz MP, Parsot C, Sansonetti PJ, Payrastre B. Conversion of PtdIns(4,5)P(2) into PtdIns(5)P by the S. flexneri effector IpgD reorganizes host cell morphology. EMBO J 21: 5069-5078, 2002.
46. Omata W, Shibata H, Li L, Takata K, Kojima I. Actin filaments play a critical role in insulin-induced exocytotic recruitment but not in endocytosis of GLUT4 in isolated rat adipocytes. Biochem J 346: 321-328, 2000.
47. Patel N, Huang C, Klip A. Cellular location of insulin-triggered signals and implications for glucose uptake. Pflügers Arch 451: 499-510, 2006.
48. Patki V, Buxton J, Chawla A, Lifshitz L, Fogarty K, Carrington W, Tuft R, Corvera S. Insulin action on GLUT4 traffic visualized in single 3T3-L1 adipocytes by using ultra-fast microscopy. Mol Biol Cell 12: 129-141, 2001.
49. Pendaries C, Tronchère JM, Arbibe L, Mounier J, Gozani O, Cantley L, Fry MJ, Gaits-Iacovoni F, Sansonetti PJ, Payrastre B. PtdIns(5)P activates the host cell PI3-kinase/Akt pathway during Shigella flexneri infection. EMBO J 25: 1024-1034, 2006.
50. Pilch PF. The mass action hypothesis: formation of Glut4 storage vesicles, a tissue-specific, regulated exocytic compartment. Acta Physiol (Oxf) 192: 89-101, 2008.
51. Rusten TE, Rodahl LNW, Pattni K, Englund C, Samakovlis C, Dove S, Brech A, Stenmark H. Fab1 phosphatidylinositol 3-phosphate 5-kinase controls trafficking but not silencing of endocytosed receptors. Mol Biol Cell 17: 3989-4001, 2006.
52. Rutherford AC, Traer C, Wassmer T, Pattni K, Bujny MV, Carlton JG, Stenmark H, Cullen PJ. The mammalian phosphatidylinositol 3-phosphate 5-kinase (PIKfyve) regulates endosome-to-TGN retrograde transport. J Cell Sci 119: 3944-3957, 2006.
53. Sasaoka T, Wada T, Tsuneki H. Lipid phosphatases as a possible therapeutic target in cases of type 2 diabetes and obesity. Pharmacol Ther 112: 799-809, 2006.
54. Sbrissa D, Shisheva A. Acquisition of unprecedented phosphatidylinositol 3,5-bisphosphate rise in hyperosmotically stressed 3T3-L1 adipocytes, mediated by ArPIKfyve-PIKfyve pathway. J Biol Chem 280: 7883-7889, 2005.
55. Sbrissa D, Ikonomov OC, Shisheva A. PIKfyve, a mammalian ortholog of yeast Fab1p lipid kinase, synthesizes 5-phosphoinositides. Effect of insulin. J Biol Chem 274: 21589-21597, 1999.
56. Sbrissa D, Ikonomov O, Shisheva A. Selective insulin-induced activation of class IA phosphoinositide 3-kinase in PIKfyve immune complexes from 3T3-L1 adipocytes. Mol Cell Endocrinol 181: 35-46, 2001.
57. Sbrissa D, Ikonomov O, Shisheva A. PtdIns 3-P-binding domains in PIKfyve: binding specificity and consequences to the protein endomembrane localization. J Biol Chem 277: 6073-6079, 2002.
58. Sbrissa D, Ikonomov OC, Deeb R, Shisheva A. Phosphatidylinositol 5-phosphate biosynthesis is linked to PIKfyve and is involved in osmotic response pathway in mammalian cells. J Biol Chem 277: 47276-47284, 2002.
59. Sbrissa D, Ikonomov OC, Fu Z, Ijuin T, Gruenberg J, Takenawa T, Shisheva A. Core protein machinery for mammalian phosphatidylinositol 3,5-bisphosphate synthesis and turnover that regulates the progression of endosomal transport. Novel Sac phosphatase joins the ArPIKfyve-PIKfyve complex. J Biol Chem 282: 23878-23891, 2007.
60. Sbrissa D, Ikonomov OC, Strakova J, Dondapati R, Mlak K, Deeb R, Silver R, Shisheva A. A mammalian ortholog of Saccharomyces cerevisiae Vac14 that associates with and up-regulates PIKfyve phosphoinositide 5-kinase activity. Mol Cell Biol 24: 10437-10447, 2004.
61. Sbrissa D, Ikonomov OC, Strakova J, Shisheva A. Role for a novel signaling intermediate, phosphatidylinositol 5-phosphate, in insulin-regulated F-actin stress fiber breakdown and GLUT4 translocation. Endocrinology 145: 4853-4865, 2004.
62. Seebohm G, Strutz-Seebohm N, Birkin R, Dell G, Bucci C, Spinosa MR, Tavaré JM, Lang F. Regulation of endocytic recycling of KCNQ1/KCNE1 potassium channels. Circ Res 100: 686-692, 2007.
63. Shisheva A. PIKfyve: partners, significance, debates and paradoxes. Cell Biol Int 32: 591-604, 2008.
64. Shisheva A. Regulating GLUT4 vesicle dynamics by phosphoinositide kinases and phosphoinositide phosphatases. Front Biosci 8: s945-s967, 2003.
65. Shisheva A, Ikonomov O, Sbrissa D. Novel Sac3 phosphatase associates with PtdIns 3,5-P2-synthesizing PIKfyve and functions as a negative regulator of insulin responsiveness in 3T3-L1 adipocytes. In: Xth International Symposium on Insulin Receptors and Insulin Action. Stockholm, Sweden: May 2-6, 2007, p. 46.
66. Shisheva A, Rusin B, Ikonomov OC, DeMarco C, Sbrissa D. Localization and insulin-regulated relocation of 5-′-phosphoinositide kinase PIKfyve in 3T3-L1 adipocytes. J Biol Chem 276: 11859-11869, 2001.
67. 2+-binding FYVE finger-containing phosphoinositide kinase in insulin-sensitive cells. Mol Cell Biol 19: 623-634, 1999.
68. Sweeney G, Garg RR, Ceddia RB, Li D, Ishiki M, Somwar R, Foster LJ, Neilsen PO, Prestwich GD, Rudich A, Klip A. Intracellular delivery of phosphatidylinositol (3,4,5)-trisphosphate causes incorporation of glucose transporter 4 into the plasma membrane of muscle and fat cells without increasing glucose uptake. J Biol Chem 279: 32233-32242, 2004.
69. Takenawa T, Itoh T. Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane. Biochim Biophys Acta 1533: 190-206, 2001.
70. Taniguchi CM, Emanuelli B, Kahn CR. Critical nodes in signaling pathways: insights into insulin action. Mol Cell Biol 7: 85-96, 2006.
71. Tong P, Khayat ZA, Huang C, Patel N, Ueyama A, Klip A. Insulin-induced cortical actin remodeling promotes GLUT4 insertion at muscle cell membrane ruffles. J Clin Invest 108: 371-381, 2001.
72. Vinciguerra M, Foti M. PTEN and SHIP2 phosphoinositide phosphatases as negative regulators of insulin signaling. Arch Physiol Biochem 112: 89-104, 2006.
73. Watson RT, Kanzaki M, Pessin JE. Regulated membrane trafficking of the insulin-responsive glucose transporter 4 in adipocytes. Endocr Rev 25: 177-204, 2004.
74. Watson RT, Pessin JE. GLUT4 translocation: the last 200 nanometers. Cell Signal 19: 2209-2217, 2007.
75. Xu Z, Huang G, Kandror KV. Phosphatidylinositol 4-kinase type IIalpha is targeted specifically to cellugyrin-positive glucose transporter 4 vesicles. Mol Endocrinol 20: 2890-2897, 2006.
76. Xu Z, Kandror KV. Translocation of small preformed vesicles is responsible for the insulin activation of glucose transport in adipose cells. Evidence from the in vitro reconstitution assay. J Biol Chem 277: 47972-47975, 2002.