Inositol pyrophosphates inhibit akt signaling, thereby regulating insulin sensitivity and weight gain

Cell

Volumn 143, Issue 6, 2010, Pages 897-910

  Chakraborty, Anutosh ^a   Koldobskiy, Michael A ^a   Bello, Nicholas T ^a   Maxwell, Micah ^a   Potter, James J ^a   Juluri, Krishna R ^a   Maag, David ^a   Kim, Seyun ^a   Huang, Alex S ^a   Dailey, Megan J ^a   Saleh, Masoumeh ^a   Snowman, Adele M ^a   Moran, Timothy H ^a   Mezey, Esteban ^a   Snyder, Solomon H ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INOSITOL PENTAKISPHOSPHATE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; INSULIN SENSITIVITY; LIVER; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; WEIGHT GAIN; WHITE ADIPOSE TISSUE;

MUS;

EID: 78649961357     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.11.032     Document Type: Article

References (81)

1. D.R. Alessi, S.R. James, C.P. Downes, A.B. Holmes, P.R. Gaffney, C.B. Reese, and P. Cohen Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha Curr. Biol. 7 1997 261 269
2. M. Andjelković, D.R. Alessi, R. Meier, A. Fernandez, N.J. Lamb, M. Frech, P. Cron, P. Cohen, J.M. Lucocq, and B.A. Hemmings Role of translocation in the activation and function of protein kinase B J. Biol. Chem. 272 1997 31515 31524
3. C.J. Barker, C. Illies, G.C. Gaboardi, and P.O. Berggren Inositol pyrophosphates: structure, enzymology and function Cell. Mol. Life Sci. 66 2009 3851 3871
4. M. Bennett, S.M. Onnebo, C. Azevedo, and A. Saiardi Inositol pyrophosphates: metabolism and signaling Cell. Mol. Life Sci. 63 2006 552 564
5. M.J. Berridge, P. Lipp, and M.D. Bootman The versatility and universality of calcium signalling Nat. Rev. Mol. Cell Biol. 1 2000 11 21
6. R. Bhandari, A. Saiardi, Y. Ahmadibeni, A.M. Snowman, A.C. Resnick, T.Z. Kristiansen, H. Molina, A. Pandey, J.K. Werner Jr., and K.R. Juluri Protein pyrophosphorylation by inositol pyrophosphates is a posttranslational event Proc. Natl. Acad. Sci. USA 104 2007 15305 15310
7. R. Bhandari, K.R. Juluri, A.C. Resnick, and S.H. Snyder Gene deletion of inositol hexakisphosphate kinase 1 reveals inositol pyrophosphate regulation of insulin secretion, growth, and spermiogenesis Proc. Natl. Acad. Sci. USA 105 2008 2349 2353
8. V. Calleja, D. Alcor, M. Laguerre, J. Park, B. Vojnovic, B.A. Hemmings, J. Downward, P.J. Parker, and B. Larijani Intramolecular and intermolecular interactions of protein kinase B define its activation in vivo PLoS Biol. 5 2007 e95
9. A. Chakraborty, M.A. Koldobskiy, K.M. Sixt, K.R. Juluri, A.K. Mustafa, A.M. Snowman, D.B. van Rossum, R.L. Patterson, and S.H. Snyder HSP90 regulates cell survival via inositol hexakisphosphate kinase-2 Proc. Natl. Acad. Sci. USA 105 2008 1134 1139
10. T.O. Chan, S.E. Rittenhouse, and P.N. Tsichlis AKT/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide- dependent phosphorylation Annu. Rev. Biochem. 68 1999 965 1014
11. H. Cho, J. Mu, J.K. Kim, J.L. Thorvaldsen, Q. Chu, E.B. Crenshaw III, K.H. Kaestner, M.S. Bartolomei, G.I. Shulman, and M.J. Birnbaum Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta) Science 292 2001 1728 1731
12. D. Cota, K. Proulx, K.A. Smith, S.C. Kozma, G. Thomas, S.C. Woods, and R.J. Seeley Hypothalamic mTOR signaling regulates food intake Science 312 2006 927 930
13. D.A. Cross, D.R. Alessi, P. Cohen, M. Andjelkovich, and B.A. Hemmings Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B Nature 378 1995 785 789
14. R.A. Currie, K.S. Walker, A. Gray, M. Deak, A. Casamayor, C.P. Downes, P. Cohen, D.R. Alessi, and J. Lucocq Role of phosphatidylinositol 3,4,5-trisphosphate in regulating the activity and localization of 3-phosphoinositide-dependent protein kinase-1 Biochem. J. 337 1999 575 583
15. G. Di Paolo, and P. De Camilli Phosphoinositides in cell regulation and membrane dynamics Nature 443 2006 651 657
16. C.P. Downes, A. Gray, A. Fairservice, S.T. Safrany, I.H. Batty, and I. Fleming The regulation of membrane to cytosol partitioning of signalling proteins by phosphoinositides and their soluble headgroups Biochem. Soc. Trans. 33 2005 1303 1307
17. M. Elchebly, P. Payette, E. Michaliszyn, W. Cromlish, S. Collins, A.L. Loy, D. Normandin, A. Cheng, J. Himms-Hagen, and C.C. Chan Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene Science 283 1999 1544 1548
18. S.R. Farmer Regulation of PPARgamma activity during adipogenesis Int J Obes (Lond) 29 Suppl 1 2005 S13 S16
19. D.A. Fruman, S.B. Snapper, C.M. Yballe, F.W. Alt, and L.C. Cantley Phosphoinositide 3-kinase knockout mice: role of p85alpha in B cell development and proliferation Biochem. Soc. Trans. 27 1999 624 629
20. K. Funai, J.D. Parkington, S. Carambula, and R.A. Fielding Age-associated decrease in contraction-induced activation of downstream targets of Akt/mTor signaling in skeletal muscle Am. J. Physiol. Regul. Integr. Comp. Physiol. 290 2006 R1080 R1086
21. C.E. Hand, and J.F. Honek Phosphate transfer from inositol pyrophosphates InsP5PP and InsP4(PP)2: a semi-empirical investigation Bioorg. Med. Chem. Lett. 17 2007 183 188
22. J. Hirosumi, G. Tuncman, L. Chang, C.Z. Görgün, K.T. Uysal, K. Maeda, M. Karin, and G.S. Hotamisligil A central role for JNK in obesity and insulin resistance Nature 420 2002 333 336
23. U. Hoffler, K. Hobbie, R. Wilson, R. Bai, A. Rahman, D. Malarkey, G. Travlos, and B.I. Ghanayem Diet-induced obesity is associated with hyperleptinemia, hyperinsulinemia, hepatic steatosis, and glomerulopathy in C57Bl/6J mice Endocrine 36 2009 311 325
24. M.K. Holz, B.A. Ballif, S.P. Gygi, and J. Blenis mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events Cell 123 2005 569 580
25. C. Illies, J. Gromada, R. Fiume, B. Leibiger, J. Yu, K. Juhl, S.N. Yang, D.K. Barma, J.R. Falck, and A. Saiardi Requirement of inositol pyrophosphates for full exocytotic capacity in pancreatic beta cells Science 318 2007 1299 1302
26. R.F. Irvine, and M.J. Schell Back in the water: the return of the inositol phosphates Nat. Rev. Mol. Cell Biol. 2 2001 327 338
27. M. Ito, A. Gomori, J. Suzuki, S. Tsujioka, M. Sasaki, M. Matsuda, M.A. Bednarek, M. Ito, A. Ishihara, and H. Iwaasa Antagonism of central melanin-concentrating hormone 1 receptor alleviates steatohepatitis in mice J. Endocrinol. 198 2008 309 315
28. Y. Izumiya, T. Hopkins, C. Morris, K. Sato, L. Zeng, J. Viereck, J.A. Hamilton, N. Ouchi, N.K. LeBrasseur, and K. Walsh Fast/Glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice Cell Metab. 7 2008 159 172
29. J.R. Jones, C. Barrick, K.A. Kim, J. Lindner, B. Blondeau, Y. Fujimoto, M. Shiota, R.A. Kesterson, B.B. Kahn, and M.A. Magnuson Deletion of PPARgamma in adipose tissues of mice protects against high fat diet-induced obesity and insulin resistance Proc. Natl. Acad. Sci. USA 102 2005 6207 6212
30. S.E. Kahn, R.L. Hull, and K.M. Utzschneider Mechanisms linking obesity to insulin resistance and type 2 diabetes Nature 444 2006 840 846
31. O. Kaidanovich, and H. Eldar-Finkelman The role of glycogen synthase kinase-3 in insulin resistance and type 2 diabetes Expert Opin. Ther. Targets 6 2002 555 561
32. K.J. Kaiyala, G.J. Morton, B.G. Leroux, K. Ogimoto, B. Wisse, and M.W. Schwartz Identification of body fat mass as a major determinant of metabolic rate in mice Diabetes 59 2010 1657 1666
33. M.A. Koldobskiy, A. Chakraborty, J.K. Werner Jr., A.M. Snowman, K.R. Juluri, M.S. Vandiver, S. Kim, S. Heletz, and S.H. Snyder p53-mediated apoptosis requires inositol hexakisphosphate kinase-2 Proc. Natl. Acad. Sci. USA 2010 10.1073/pnas.1015671107 in press. Published online November 15, 2010
34. D. Komander, A. Fairservice, M. Deak, G.S. Kular, A.R. Prescott, C. Peter Downes, S.T. Safrany, D.R. Alessi, and D.M. van Aalten Structural insights into the regulation of PDK1 by phosphoinositides and inositol phosphates EMBO J. 23 2004 3918 3928
35. K.F. Leavens, R.M. Easton, G.I. Shulman, S.F. Previs, and M.J. Birnbaum Akt2 is required for hepatic lipid accumulation in models of insulin resistance Cell Metab. 10 2009 405 418
36. Y.S. Lee, S. Mulugu, J.D. York, and E.K. O'Shea Regulation of a cyclin-CDK-CDK inhibitor complex by inositol pyrophosphates Science 316 2007 109 112
37. M.A. Lemmon Membrane recognition by phospholipid-binding domains Nat. Rev. Mol. Cell Biol. 9 2008 99 111
38. H. Lin, P.C. Fridy, A.A. Ribeiro, J.H. Choi, D.K. Barma, G. Vogel, J.R. Falck, S.B. Shears, J.D. York, and G.W. Mayr Structural analysis and detection of biological inositol pyrophosphates reveal that the family of VIP/diphosphoinositol pentakisphosphate kinases are 1/3-kinases J. Biol. Chem. 284 2009 1863 1872
39. H.R. Luo, Y.E. Huang, J.C. Chen, A. Saiardi, M. Iijima, K. Ye, Y. Huang, E. Nagata, P. Devreotes, and S.H. Snyder Inositol pyrophosphates mediate chemotaxis in Dictyostelium via pleckstrin homology domain-PtdIns(3,4,5)P3 interactions Cell 114 2003 559 572
40. B.D. Manning, and L.C. Cantley AKT/PKB signaling: navigating downstream Cell 129 2007 1261 1274
41. R.M. Memmott, and P.A. Dennis Akt-dependent and -independent mechanisms of mTOR regulation in cancer Cell. Signal. 21 2009 656 664
42. S. Mulugu, W. Bai, P.C. Fridy, R.J. Bastidas, J.C. Otto, D.E. Dollins, T.A. Haystead, A.A. Ribeiro, and J.D. York A conserved family of enzymes that phosphorylate inositol hexakisphosphate Science 316 2007 106 109
43. M.G. Myers, M.A. Cowley, and H. Münzberg Mechanisms of leptin action and leptin resistance Annu. Rev. Physiol. 70 2008 537 556
44. U. Padmanabhan, D.E. Dollins, P.C. Fridy, J.D. York, and C.P. Downes Characterization of a selective inhibitor of inositol hexakisphosphate kinases: use in defining biological roles and metabolic relationships of inositol pyrophosphates J. Biol. Chem. 284 2009 10571 10582
45. X.D. Peng, P.Z. Xu, M.L. Chen, A. Hahn-Windgassen, J. Skeen, J. Jacobs, D. Sundararajan, W.S. Chen, S.E. Crawford, K.G. Coleman, and N. Hay Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2 Genes Dev. 17 2003 1352 1365
46. F. Pinto Lde, C.M. Compri, J.V. Fornari, W. Bartchewsky, D.E. Cintra, M. Trevisan, Pde.O. Carvalho, M.L. Ribeiro, L.A. Velloso, and M.J. Saad The immunosuppressant drug, thalidomide, improves hepatic alterations induced by a high-fat diet in mice Liver Int. 30 2010 603 610
47. J.K. Reddy, and M.S. Rao Lipid metabolism and liver inflammation. II. Fatty liver disease and fatty acid oxidation Am. J. Physiol. Gastrointest. Liver Physiol. 290 2006 G852 G858
48. C. Rommel, S.C. Bodine, B.A. Clarke, R. Rossman, L. Nunez, T.N. Stitt, G.D. Yancopoulos, and D.J. Glass Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways Nat. Cell Biol. 3 2001 1009 1013
49. S.E. Ross, N. Hemati, K.A. Longo, C.N. Bennett, P.C. Lucas, R.L. Erickson, and O.A. MacDougald Inhibition of adipogenesis by Wnt signaling Science 289 2000 950 953
50. D. Ruggero, and N. Sonenberg The Akt of translational control Oncogene 24 2005 7426 7434
51. A. Saiardi, H. Erdjument-Bromage, A.M. Snowman, P. Tempst, and S.H. Snyder Synthesis of diphosphoinositol pentakisphosphate by a newly identified family of higher inositol polyphosphate kinases Curr. Biol. 9 1999 1323 1326
52. A. Saiardi, E. Nagata, H.R. Luo, A.M. Snowman, and S.H. Snyder Identification and characterization of a novel inositol hexakisphosphate kinase J. Biol. Chem. 276 2001 39179 39185
53. A. Saiardi, C. Sciambi, J.M. McCaffery, B. Wendland, and S.H. Snyder Inositol pyrophosphates regulate endocytic trafficking Proc. Natl. Acad. Sci. USA 99 2002 14206 14211
54. A. Saiardi, R. Bhandari, A.C. Resnick, A.M. Snowman, and S.H. Snyder Phosphorylation of proteins by inositol pyrophosphates Science 306 2004 2101 2105
55. A. Saiardi, A.C. Resnick, A.M. Snowman, B. Wendland, and S.H. Snyder Inositol pyrophosphates regulate cell death and telomere length through phosphoinositide 3-kinase-related protein kinases Proc. Natl. Acad. Sci. USA 102 2005 1911 1914
56. D.D. Sarbassov, D.A. Guertin, S.M. Ali, and D.M. Sabatini Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex Science 307 2005 1098 1101
57. J. Shao, H. Yamashita, L. Qiao, and J.E. Friedman Decreased Akt kinase activity and insulin resistance in C57BL/KsJ-Leprdb/db mice J. Endocrinol. 167 2000 107 115
58. K.P. Shay, and T.M. Hagen Age-associated impairment of Akt phosphorylation in primary rat hepatocytes is remediated by alpha-lipoic acid through PI3 kinase, PTEN, and PP2A Biogerontology 10 2009 443 456
59. S.B. Shears Understanding the biological significance of diphosphoinositol polyphosphates ('inositol pyrophosphates') Biochem. Soc. Symp. 74 2007 211 221
60. Q.Q. Tang, M. Grønborg, H. Huang, J.W. Kim, T.C. Otto, A. Pandey, and M.D. Lane Sequential phosphorylation of CCAAT enhancer-binding protein beta by MAPK and glycogen synthase kinase 3beta is required for adipogenesis Proc. Natl. Acad. Sci. USA 102 2005 9766 9771
61. C.M. Taniguchi, B. Emanuelli, and C.R. Kahn Critical nodes in signalling pathways: insights into insulin action Nat. Rev. Mol. Cell Biol. 7 2006 85 96
62. J.C. Tou, and C.E. Wade Determinants affecting physical activity levels in animal models Exp. Biol. Med. (Maywood) 227 2002 587 600
63. S.H. Um, F. Frigerio, M. Watanabe, F. Picard, M. Joaquin, M. Sticker, S. Fumagalli, P.R. Allegrini, S.C. Kozma, J. Auwerx, and G. Thomas Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity Nature 431 2004 200 205
64. G.I. Welsh, I. Hers, D.C. Berwick, G. Dell, M. Wherlock, R. Birkin, S. Leney, and J.M. Tavaré Role of protein kinase B in insulin-regulated glucose uptake Biochem. Soc. Trans. 33 2005 346 349
65. W. Ye, N. Ali, M.E. Bembenek, S.B. Shears, and E.M. Lafer Inhibition of clathrin assembly by high affinity binding of specific inositol polyphosphates to the synapse-specific clathrin assembly protein AP-3 J. Biol. Chem. 270 1995 1564 1568
66. S.J. York, B.N. Armbruster, P. Greenwell, T.D. Petes, and J.D. York Inositol diphosphate signaling regulates telomere length J. Biol. Chem. 280 2005 4264 4269
67. Bhandari, R., Juluri, K.R., Resnick, A.C., and Snyder, S.H. (2008). Gene deletion of inositol hexakisphosphate kinase 1 reveals inositol pyrophosphate regulation of insulin secretion, growth, and spermiogenesis. Proc. Natl. Acad. Sci. USA 105, 2349-2353.
68. Chakraborty, A., Koldobskiy, M.A., Sixt, K.M., Juluri, K.R., Mustafa, A.K., Snowman, A.M., van Rossum, D.B., Patterson, R.L., and Snyder, S.H. (2008). HSP90 regulates cell survival via inositol hexakisphosphate kinase-2. Proc. Natl. Acad. Sci. USA 105, 1134-1139.
69. Fueger, P.T., Bracy, D.P., Malabanan, C.M., Pencek, R.R., Granner, D.K., and Wasserman, D.H. (2004). Hexokinase II overexpression improves exercise-stimulated but not insulin-stimulated muscle glucose uptake in high-fat-fed C57BL/6J mice. Diabetes 53, 306-314.
70. Kim, E.K., Miller, I., Aja, S., Landree, L.E., Pinn, M., McFadden, J., Kuhajda, F.P., Moran, T.H., and Ronnett, G.V. (2004). C75, a fatty acid synthase inhibitor, reduces food intake via hypothalamic AMP-activated protein kinase. J. Biol. Chem. 279, 19970-19976.
71. Knight, Z.A., Feldman, M.E., Balla, A., Balla, T., and Shokat, K.M. (2007). A membrane capture assay for lipid kinase activity. Nat. Protoc. 2, 2459-2466.
72. Komander, D., Fairservice, A., Deak, M., Kular, G.S., Prescott, A.R., Peter Downes, C., Safrany, S.T., Alessi, D.R., and van Aalten, D.M. (2004). Structural insights into the regulation of PDK1 by phosphoinositides and inositol phosphates. EMBO J. 23, 3918-3928.
73. Kraegen, E.W., James, D.E., Jenkins, A.B., and Chisholm, D.J. (1985). Dose-response curves for in vivo insulin sensitivity in individual tissues in rats. Am. J. Physiol. 248, E353-E362.
74. Resnick, A.C., Snowman, A.M., Kang, B.N., Hurt, K.J., Snyder, S.H., and Saiardi, A. (2005). Inositol polyphosphate multikinase is a nuclear PI3-kinase with transcriptional regulatory activity. Proc. Natl. Acad. Sci. USA 102, 12783-12788.
75. Saiardi, A., Erdjument-Bromage, H., Snowman, A.M., Tempst, P., and Snyder, S.H. (1999). Synthesis of diphosphoinositol pentakisphosphate by a newly identified family of higher inositol polyphosphate kinases. Curr. Biol. 9, 1323-1326.
76. Saiardi, A., Sciambi, C., McCaffery, J.M., Wendland, B., and Snyder, S.H. (2002). Inositol pyrophosphates regulate endocytic trafficking. Proc. Natl. Acad. Sci. USA 99, 14206-14211.
77. Sarbassov, D.D., Ali, S.M., Kim, D.H., Guertin, D.A., Latek, R.R., Erdjument-Bromage, H., Tempst, P., and Sabatini, D.M. (2004). Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr. Biol. 14, 1296-1302.
78. Schalm, S.S., Fingar, D.C., Sabatini, D.M., and Blenis, J. (2003). TOS motif-mediated raptor binding regulates 4E-BP1 multisite phosphorylation and function. Curr. Biol. 13, 797-806.
79. Shin, S., Wakabayashi, J., Yates, M.S., Wakabayashi, N., Dolan, P.M., Aja, S., Liby, K.T., Sporn, M.B., Yamamoto, M., and Kensler, T.W. (2009). Role of Nrf2 in prevention of high-fat diet-induced obesity by synthetic triterpenoid CDDO-imidazolide. Eur. J. Pharmacol. 620, 138-144.
80. van den Hoek, A.M., Heijboer, A.C., Corssmit, E.P., Voshol, P.J., Romijn, J.A., Havekes, L.M., and Pijl, H. (2004). PYY3-36 reinforces insulin action on glucose disposal in mice fed a high-fat diet. Diabetes 53, 1949-1952.
81. Voshol, P.J., Jong, M.C., Dahlmans, V.E., Kratky, D., Levak-Frank, S., Zechner, R., Romijn, J.A., and Havekes, L.M. (2001). In muscle-specific lipoprotein lipase-overexpressing mice, muscle triglyceride content is increased without inhibition of insulin-stimulated whole-body and muscle-specific glucose uptake. Diabetes 50, 2585-2590.