HVps15, but not Ca2+/CaM, is required for the activity and regulation of hVps34 in mammalian cells

Biochemical Journal

Volumn 417, Issue 3, 2009, Pages 747-755

  Yan, Ying ^a   Flinn, Rory J ^a   Wu, Haiyan ^a   Schnur, Rachel S ^a   Backer, Joathan M ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Autophagy; Beclin 1; Mammalian target of rapamycin (mTOR); Mammalian vacuolar protein sorting 34 (Vps34); UV radiation resistance associated gene (UVRAG); Vacuolar protein sorting 15 (Vps15)

Indexed keywords

AUTOPHAGY; BECLIN-1; MAMMALIAN TARGET OF RAPAMYCIN (MTOR); MAMMALIAN VACUOLAR PROTEIN SORTING 34 (VPS34); UV RADIATION RESISTANCE-ASSOCIATED GENE (UVRAG); VACUOLAR PROTEIN SORTING 15 (VPS15);

ANTIBIOTICS; CALCIUM; CAMS; ESTERS; ETHANE; NUTRIENTS; ULTRAVIOLET RADIATION;

MAMMALS;

BECLIN 1; CALCIUM ION; CALMODULIN; EDETIC ACID; EGTAZIC ACID; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; MAMMALIAN VACUOLAR PROTEIN SORTING 15 HOMOLOG; MAMMALIAN VACUOLAR PROTEIN SORTING 34 HOMOLOG; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; REGULATOR PROTEIN; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, HUMAN; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SERINE THREONINE KINASE; TUMOR SUPPRESSOR PROTEIN; UVRAG PROTEIN, HUMAN; VPS15 PROTEIN KINASE; VPS15 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CALCIUM SIGNALING; CELL ACTIVATION; CHELATION; CONTROLLED STUDY; EMBRYO; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MAMMAL CELL; METABOLIC REGULATION; NONHUMAN; NUTRITIONAL STATUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; ANIMAL; BINDING SITE; CHO CELL; CRICETULUS; GENETICS; HAMSTER; METABOLISM; SIGNAL TRANSDUCTION;

MAMMALIA; TETRA;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS REGULATORY PROTEINS; BINDING SITES; CALMODULIN; CHO CELLS; CRICETINAE; CRICETULUS; HUMANS; MEMBRANE PROTEINS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 59849113021     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20081865     Document Type: Article

References (29)

1. Backer, J. M. (2008) The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem. J. 410, 1-17
2. Schu, P. V., Takegawa, K., Fry, M. J., Stack, J. H., Waterfield, M. D. and Emr, S. D. (1993) Phosphatidylinositol 3-kinase encoded by yeast VPS 34 gene essential for protein sorting. Science 260, 88-91
3. Volinia, S., Dhand, R., Vanhaesebroeck, B., MacDougall, L. K., Stein, R., Zvelebil, M. J., Domin, J., Panaretou, C. and Waterfield, M. D. (1995) A human phosphatidylinositol 3-kinase complex related to the yeast Vps34p-Vps15p protein sorting system. EMBO J. 14, 3339-3348
4. Stenmark, H. and Aasland, R. (1999) FYVE-finger proteins: effectors of an inositol lipid. J. Cell Sci. 112, 4175-4183
5. Lemmon, M. A. (2003) Phosphoinositide recognition domains. Traffic 4, 201-213
6. Vanhaesebroeck, B., Leevers, S. J., Ahmadi, K., Timms, J., Katso, R., Driscoll, P. C., Woscholski, R., Parker, P. J. and Waterfield, M. D. (2001) Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 70, 535-602
7. Christoforidis, S., Miaczynska, M., Ashman, K., Wilm, M., Zhao, L., Yip, S.-C., Waterfield, M. D., Backer, J. M. and Zerial, M. (1999) Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat. Cell Biol. 1, 249-252
8. Murray, J. T., Panaretou, C., Stenmark, H., Miaczynska, M. and Backer, J. M. (2002) Role of Rab5 in the recruitment of hVps34/p150 to the early endosome. Traffic 3, 416-427
9. Futter, C. E., Collinson, L. M., Backer, J. M. and Hopkins, C. R. (2001) Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J. Cell Biol. 155, 1251-1264
10. Stein, M. P., Feng, Y., Cooper, K. L., Welford, A. M. and Wandinger-Ness, A. (2003) Human VPS34 and p150 are Rab7 interacting partners. Traffic 4, 754-771
11. Kihara, A., Noda, T., Ishihara, N. and Ohsumi, Y. (2001) Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J. Cell Biol. 152, 519-530
12. Furuya, N., Yu, J., Byfield, M., Pattingre, S. and Levine, B. (2005) The evolutionarily conserved domain of Beclin 1 is required for Vps34 binding, autophagy and tumor suppressor function. Autophagy 1, 46-52
13. Liang, C., Feng, P., Ku, B., Dotan, I., Canaani, D., Oh, B. H. and Jung, J. U. (2006) Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat. Cell Biol. 8, 688-699
14. Takahashi, Y., Coppola, D., Matsushita, N., Cualing, H. D., Sun, M., Sato, Y., Liang, C., Jung, J. U., Cheng, J. Q., Mul, J. J. et al. (2007) Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat. Cell Biol. 9, 1142-1151
15. Byfield, M. P., Murray, J. T. and Backer, J. M. (2005) hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. J. Biol. Chem. 280, 33076-33082
16. 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. (2005) Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Proc. Natl. Acad. Sci. U.S.A. 102, 14238-14243
17. 2+/CaM signaling to hVps34. Cell Metab. 7, 456-465
18. Juhasz, G., Hill, J. H., Yan, Y., Sass, M., Baehrecke, E. H., Backer, J. M. and Neufeld, T. P. (2008) The class III PI3K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J. Cell Biol. 181, 655-666
19. Stack, J. H., Herman, P. K., Schu, P. V. and Emr, S. D. (1993) A membrane-associated complex containing the Vps15 protein kinase and the Vps34 PI 3-kinase is essential for protein sorting to the yeast lysosome-like vacuole. EMBO J. 12, 2195-2204
20. Panaretou, C., Domin, J., Cockcroft, S. and Waterfield, M. D. (1997) Characterization of p150, an adaptor protein for the human phosphatidylinositol (PtdIns) 5-kinase: substrate presentation by phosphatidylinositol transfer protein to the p150-PtdIns 3-kinase complex. J. Biol. Chem. 272, 2477-2485
21. Stack, J. H., DeWald, D. B., Takegawa, K. and Emr, S. D. (1995) Vesicle-mediated protein transport: regulatory interactions between the Vps15 protein kinase and the Vps34 PtdIns 3-kinase essential for protein sorting to the vacuole in yeast. J. Cell Biol. 129, 321-334
22. Stack, J. H. and Emr, S. D. (1994) Vps34p required for yeast vacuolar protein sorting is a multiple specificity kinase that exhibits both protein kinase and phosphatidylinositolspecific PI3-kinase activities. J. Biol. Chem. 269, 31552-31562
23. Cao, C., Laporte, J., Backer, J. M., Wandinger-Ness, A. and Stein, M. P. (2007) Myotubularin lipid phosphatase binds the hVPS15/hVPS34 lipid kinase complex on endosomes. Traffic 8, 1052-1067
24. Cao, C., Backer, J. M., Laporte, J., Bedrick, E. J. and Wandinger-Ness, A. (2008) Sequential actions of myotubularin lipid phosphatases regulate endosomal PI(3)P and growth factor receptor trafficking. Mol. Biol. Cell 19, 3334-3346
25. Lindmo, K., Brech, A., Finley, K. D., Gaumer, S., Contamine, D., Rusten, T. E. and Stenmark, H. (2008) The PI 3-kinase regulator Vps15 is required for autophagic clearance of protein aggregates. Autophagy 4, 500-506
26. Pollard, J. W. and Stanners, C. P. (1979) Characterization of cell lines showing growth control isolated from both the wild-type and a leucyl-tRNA synthetase mutant of Chinese hamster ovary cells. J. Cell. Physiol. 98, 571-585
27. Siddhanta, U., McIlroy, J., Shah, A., Zhang, Y. and Backer, J. M. (1998) Distinct roles for the p110a and hVPS34 phosphatidylinositol 3′-kinases in vesicular trafficking, regulation of the actin cytoskeleton, and mitogenesis. J. Cell Biol. 143, 1647-1659
28. Vergne, I., Chua, J. and Deretic, V. (2003) Tuberculosis toxin blocking phagosome maturation inhibits a novel Ca2+/calmodulin-PI3K hVPS34 cascade. J. Exp. Med. 198, 653-659
29. Herman, P. K., Stack, J. H., DeModena, J. A. and Emr, S. D. (1991) A novel protein kinase homolog essential for protein sorting to the yeast lysosome-like vacuole. Cell 64, 425-437