Amino Acids Activate mTOR Complex 1 via Ca2+/CaM Signaling to hVps34

Cell Metabolism

Volumn 7, Issue 5, 2008, Pages 456-465

  Gulati, Pawan ^a   Gaspers, Lawrence D ^b   Dann, Stephen G ^a   Joaquin, Manel ^c   Nobukuni, Takahiro ^a   Natt, Francois ^d   Kozma, Sara C ^a   Thomas, Andrew P ^b   Thomas, George ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d NOVARTIS PHARMA AG   (Switzerland)

Author keywords

HUMDISEASE

Indexed keywords

AMINO ACID; CALCIUM ION; CALMODULIN; CELL PROTEIN; HUMAN VACUOLAR PROTEIN SORTING 34; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROTEIN KINASE (CALCIUM,CALMODULIN);

ARTICLE; BINDING SITE; CALCIUM CELL LEVEL; CANCER GROWTH; CELL STRAIN HEK293; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVITY; HELA CELL; HUMAN; HUMAN CELL; METABOLIC DISORDER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN MOTIF; SIGNAL TRANSDUCTION;

BINDING SITES; BLOTTING, WESTERN; CALCIUM; CALMODULIN; CELLS, CULTURED; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; KIDNEY; LEUCINE; MUTAGENESIS, SITE-DIRECTED; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TRANSFECTION; VESICULAR TRANSPORT PROTEINS;

MAMMALIA;

EID: 42649112409     PISSN: 15504131     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cmet.2008.03.002     Document Type: Article

References (42)

1. Bai X., Ma D., Liu A., Shen X., Wang Q.J., Liu Y., and Jiang Y. Rheb activates mTOR by antagonizing its endogenous inhibitor, FKBP38. Science 318 (2007) 977-980
2. Byfield M.P., Murray J.T., and Backer J.M. hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. J. Biol. Chem. 280 (2005) 33076-33082
3. Calle E.E., and Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat. Rev. Cancer 4 (2004) 579-591
4. Conus N.M., Hemmings B.A., and Pearson R.B. Differential regulation by calcium reveals distinct signaling requirements for the activation of Akt and p70S6k. J. Biol. Chem. 273 (1998) 4776-4782
5. Dann S.G., Selvaraj A., and Thomas G. mTOR Complex1-S6K1 signaling: at the crossroads of obesity, diabetes and cancer. Trends Mol. Med. 13 (2007) 252-259
6. Finkelstein E.A., Ruhm C.J., and Kosa K.M. Economic causes and consequences of obesity. Annu. Rev. Public Health 26 (2005) 239-257
7. Gingras A.C., Gygi S.P., Raught B., Polakiewicz R.D., Abraham R.T., Hoekstra M.F., Aebersold R., and Sonenberg N. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev. 13 (1999) 1422-1437
8. Gordon P.B., Holen I., Fosse M., Rotnes J.S., and Seglen P.O. Dependence of hepatocytic autophagy on intracellularly sequestered calcium. J. Biol. Chem. 268 (1993) 26107-26112
9. Hall R.A. Studying protein-protein interactions via blot overlay or Far Western blot. Methods Mol. Biol. 261 (2004) 167-174
10. Hannan K.M., Thomas G., and Pearson R.B. Activation of S6K1 (p70 ribosomal protein S6 kinase 1) requires an initial calcium-dependent priming event involving formation of a high-molecular-mass signalling complex. Biochem. J. 370 (2003) 469-477
11. Hara K., Yonezawa K., Weng Q.P., Kozlowski M.T., Belham C., and Avruch J. Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J. Biol. Chem. 273 (1998) 14484-14494
12. Harrington L.S., Findlay G.M., Gray A., Tolkacheva T., Wigfield S., Rebholz H., Barnett J., Leslie N.R., Cheng S., Shepherd P.R., et al. The TSC1-2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS proteins. J. Cell Biol. 166 (2004) 213-223
13. Hoyer-Hansen M., Bastholm L., Szyniarowski P., Campanella M., Szabadkai G., Farkas T., Bianchi K., Fehrenbacher N., Elling F., Rizzuto R., et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 25 (2007) 193-205
14. Kahl C.R., and Means A.R. Regulation of cell cycle progression by calcium/calmodulin-dependent pathways. Endocr. Rev. 24 (2003) 719-736
15. Kihara A., Kabeya Y., Ohsumi Y., and Yoshimori T. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep. 2 (2001) 330-335
16. Kihara A., Noda T., Ishihara N., and Ohsumi Y. Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J. Cell Biol. 152 (2001) 519-530
17. Kim D.H., Sarbassov D.D., Ali S.M., King J.E., Latek R.R., Erdjument-Bromage H., Tempst P., and Sabatini D.M. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110 (2002) 163-175
18. Krebs M. Amino acid-dependent modulation of glucose metabolism in humans. Eur. J. Clin. Invest. 35 (2005) 351-354
19. Long X., Ortiz-Vega S., Lin Y., and Avruch J. Rheb binding to mammalian target of rapamycin (mTOR) is regulated by amino acid sufficiency. J. Biol. Chem. 280 (2005) 23433-23436
20. Means A.R., Tash J.S., and Chafouleas J.G. Physiological implications of the presence, distribution, and regulation of calmodulin in eukaryotic cells. Physiol. Rev. 62 (1982) 1-39
21. Meyer T., Hanson P.I., Stryer L., and Schulman H. Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science 256 (1992) 1199-1202
22. Morgan A.J., and Thomas A.P. Single cell and subcellular measurement of intracellular Ca2+ concentration ([Ca2+]i). Methods Mol. Biol. 114 (1999) 93-123
23. Nobukuni T., Joaquin M., Roccio M., Dann S.G., Kim S.Y., Gulati P., Byfield M.P., Backer J.M., Natt F., Bos J.L., et al. Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Proc. Natl. Acad. Sci. USA 102 (2005) 14238-14243
24. Nobukuni T., Kozma S.C., and Thomas G. hvps34, an ancient player, enters a growing game: mTOR Complex1/S6K1 signaling. Curr. Opin. Cell Biol. 19 (2007) 135-141
25. Patti M.E., and Kahn B.B. Nutrient sensor links obesity with diabetes risk. Nat. Med. 10 (2004) 1049-1050
26. Pearce L.R., Huang X., Boudeau J., Pawlowski R., Wullschleger S., Deak M., Ibrahim A.F., Gourlay R., Magnuson M.A., and Alessi D.R. Identification of Protor as a novel Rictor-binding component of mTOR complex-2. Biochem. J. 405 (2007) 513-522
27. Peyrollier K., Hajduch E., Blair A.S., Hyde R., and Hundal H.S. L-leucine availability regulates phosphatidylinositol 3-kinase, p70 S6 kinase and glycogen synthase kinase-3 activity in L6 muscle cells: evidence for the involvement of the mammalian target of rapamycin (mTOR) pathway in the L-leucine-induced up-regulation of system A amino acid transport. Biochem. J. 350 (2000) 361-368
28. Resnick L.M. Therapeutic implications of calcium intake in hypertension: more analyses, a little progress, and a different approach. Am. J. Hypertens. 12 (1999) 82-83
29. Rhoads A.R., and Friedberg F. Sequence motifs for calmodulin recognition. FASEB J. 11 (1997) 331-340
30. Rooney T.A., Sass E.J., and Thomas A.P. Characterization of cytosolic calcium oscillations induced by phenylephrine and vasopressin in single fura-2-loaded hepatocytes. J. Biol. Chem. 264 (1989) 17131-17141
31. Sancak Y., Thoreen C.C., Peterson T.R., Lindquist R.A., Kang S.A., Spooner E., Carr S.A., and Sabatini D.M. PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol. Cell 25 (2007) 903-915
32. Thastrup O., Cullen P.J., Drobak B.K., Hanley M.R., and Dawson A.P. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc. Natl. Acad. Sci. USA 87 (1990) 2466-2470
33. Thomas A.P., Bird G.S., Hajnoczky G., Robb-Gaspers L.D., and Putney Jr. J.W. Spatial and temporal aspects of cellular calcium signaling. FASEB J. 10 (1996) 1505-1517
34. Tremblay F., Jacques H., and Marette A. Modulation of insulin action by dietary proteins and amino acids: role of the mammalian target of rapamycin nutrient sensing pathway. Curr. Opin. Clin. Nutr. Metab. Care 8 (2005) 457-462
35. Tremblay F., Krebs M., Dombrowski L., Brehm A., Bernroider E., Roth E., Nowotny P., Waldhausl W., Marette A., and Roden M. Overactivation of S6 kinase 1 as a cause of human insulin resistance during increased amino acid availability. Diabetes 54 (2005) 2674-2684
36. Tremblay F., Brule S., Hee Um S., Li Y., Masuda K., Roden M., Sun X.J., Krebs M., Polakiewicz R.D., Thomas G., and Marette A. Identification of IRS-1 Ser-1101 as a target of S6K1 in nutrient- and obesity-induced insulin resistance. Proc. Natl. Acad. Sci. USA 104 (2007) 14056-14061
37. Tzatsos A., and Kandror K.V. Nutrients suppress phosphatidylinositol 3-kinase/Akt signaling via raptor-dependent mTOR-mediated insulin receptor substrate 1 phosphorylation. Mol. Cell. Biol. 26 (2006) 63-76
38. Um S.H., Frigerio F., Watanabe M., Picard F., Joaquin M., Sticker M., Fumagalli S., Allegrini P.R., Kozma S.C., Auwerx J., and Thomas G. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431 (2004) 200-205
39. Um S.H., D'Alessio D., and Thomas G. Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab. 3 (2006) 393-402
40. Vergne I., Chua J., and Deretic V. Tuberculosis toxin blocking phagosome maturation inhibits a novel Ca2+/calmodulin-PI3K hVPS34 cascade. J. Exp. Med. 198 (2003) 653-659
41. Wullschleger S., Loewith R., and Hall M.N. TOR signaling in growth and metabolism. Cell 124 (2006) 471-484
42. Zhang H.H., Lipovsky A.I., Dibble C.C., Sahin M., and Manning B.D. S6K1 regulates GSK3 under conditions of mTOR-dependent feedback inhibition of Akt. Mol. Cell 24 (2006) 185-197