How phosphoinositide 3-phosphate controls growth downstream of amino acids and autophagy downstream of amino acid withdrawal

Biochemical Society Transactions

Volumn 40, Issue 1, 2012, Pages 37-43

  Ktistakis, Nicholas T ^a   Manifava, Maria ^a   Schoenfelder, Priya ^a   Rotondo, Sergio ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

Amino acid; Autophagy; Growth control; Phosphatidylinositol 3 phosphate (PtdIns3P); Target of rapamycin (TOR); Vacuolar protein sorting 34 (Vps34)

Indexed keywords

AMINO ACID; BECLIN 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PROTEIN BCL 2; RAB PROTEIN; RAB7 PROTEIN;

AUTOPHAGOSOME; AUTOPHAGY; COMPLEX FORMATION; CRYSTAL STRUCTURE; DOWN REGULATION; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; LYSOSOME; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION;

AMINO ACIDS; ANIMALS; AUTOPHAGY; CELL PROLIFERATION; CLASS III PHOSPHATIDYLINOSITOL 3-KINASES; HUMANS; PHOSPHATIDYLINOSITOLS; PROTEINS; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 84856249448     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20110684     Document Type: Review

References (71)

1. Kim, J. and Guan, K.L. (2011) Amino acid signaling in TOR activation. Annu. Rev. Biochem. 80, 1001-1032
2. Wullschleger, S., Loewith, R. and Hall, M.N. (2006) TOR signaling in growth and metabolism. Cell 124, 471-484 (Pubitemid 43199434)
3. Weidberg, H., Shvets, E. and Elazar, Z. (2011) Biogenesis and cargo selectivity of autophagosomes. Annu. Rev. Biochem. 80, 125-156
4. Mizushima, N. (2007) Autophagy: process and function. Genes Dev. 21, 2861-2873
5. Burman, C. and Ktistakis, N.T. (2010) Regulation of autophagy by phosphatidylinositol 3-phosphate. FEBS Lett. 584, 1302-1312
6. Backer, J.M. (2008) The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem. J. 410, 1-17
7. Nobukuni, T., Kozma, S.C. and Thomas, G. (2007) hvps34, an ancient player, enters a growing game: mTOR Complex1/S6K1 signaling. Curr. Opin. Cell Biol. 19, 135-141 (Pubitemid 46386413)
8. Falasca, M. and Maffucci, T. (2007) Role of class II phosphoinositide 3-kinase in cell signalling. Biochem. Soc. Trans. 35, 211-214 (Pubitemid 46596470)
9. Arcaro, A., Zvelebil, M.J., Wallasch, C., Ullrich, A., Waterfield, M.D. and Domin, J. (2000) Class II phosphoinositide 3-kinases are downstream targets of activated polypeptide growth factor receptors. Mol. Cell. Biol. 20, 3817-3830 (Pubitemid 30314481)
10. Dominguez, V., Raimondi, C., Somanath, S., Bugliani, M., Loder, M.K., Edling, C.E., Divecha, N., da Silva-Xavier, G., Marselli, L., Persaud, S.J. et al. (2011) Class II phosphoinositide 3-kinase regulates exocytosis of insulin granules in pancreatic β cells. J. Biol. Chem. 286, 4216-4225
11. Maffucci, T., Cooke, F.T., Foster, F.M., Traer, C.J., Fry, M.J. and Falasca, M. (2005) Class II phosphoinositide 3-kinase defines a novel signaling pathway in cell migration. J. Cell Biol. 169, 789-799 (Pubitemid 41002884)
12. Misawa, H., Ohtsubo, M., Copeland, N.G., Gilbert, D.J., Jenkins, N.A. and Yoshimura, A. (1998) Cloning and characterization of a novel class II phosphoinositide 3-kinase containing C2 domain. Biochem. Biophys. Res. Commun. 244, 531-539 (Pubitemid 28414116)
13. 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 VPS34 gene essential for protein sorting. Science 260, 88-91 (Pubitemid 23122750)
14. Stenmark, H. (2010) The Sir Hans Krebs Lecture. How a lipid mediates tumour suppression. Delivered on 29 June 2010 at the 35th FEBS Congress in Gothenburg, Sweden. FEBS J. 277, 4837-4848
15. Lindmo, K. and Stenmark, H. (2006) Regulation of membrane traffic by phosphoinositide 3-kinases. J. Cell Sci. 119, 605-614
16. 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 (Pubitemid 34280235)
17. Obara, K. and Ohsumi, Y. (2011) PtdIns 3-kinase orchestrates autophagosome formation in yeast. J. Lipids 2011, 498768
18. Itakura, E., Kishi, C., Inoue, K. and Mizushima, N. (2008) Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol. Biol. Cell 19, 5360-5372
19. Liang, X.H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H. and Levine, B. (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672-676 (Pubitemid 129516338)
20. 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
21. Zhong, Y., Wang, Q.J., Li, X., Yan, Y., Backer, J.M., Chait, B.T., Heintz, N. and Yue, Z. (2009) Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat. Cell Biol. 11, 468-476
22. Takahashi, Y., Coppola, D., Matsushita, N., Cualing, H.D., Sun, M., Sato, Y., Liang, C., Jung, J.U., Cheng, J.Q., Mule, J.J. et al. (2007) Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat. Cell Biol. 9, 1142-1151 (Pubitemid 47500490)
23. Matsunaga, K., Saitoh, T., Tabata, K., Omori, H., Satoh, T., Kurotori, N., Maejima, I., Shirahama-Noda, K., Ichimura, T., Isobe, T. et al. (2009) Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat. Cell Biol. 11, 385-396
24. Pattingre, S., Tassa, A., Qu, X., Garuti, R., Liang, X.H., Mizushima, N., Packer, M., Schneider, M.D. and Levine, B. (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927-939 (Pubitemid 41345209)
25. Fimia, G.M., Stoykova, A., Romagnoli, A., Giunta, L., Di Bartolomeo, S., Nardacci, R., Corazzari, M., Fuoco, C., Ucar, A., Schwartz, P. et al. (2007) Ambra1 regulates autophagy and development of the nervous system. Nature 447, 1121-1125 (Pubitemid 47014434)
26. Miller, S., Tavshanjian, B., Oleksy, A., Perisic, O., Houseman, B.T., Shokat, K.M. and Williams, R.L. (2010) Shaping development of autophagy inhibitors with the structure of the lipid kinase Vps34. Science 327, 1638-1642
27. phox bind to lipid products of PI(3)K. Nat. Cell Biol. 3, 675-678
28. Gaullier, J.M., Simonsen, A., D'Arrigo, A., Bremnes, B., Stenmark, H. and Aasland, R. (1998) FYVE fingers bind PtdIns(3)P. Nature 394, 432-433
29. Ellson, C.D., Gobert-Gosse, S., Anderson, K.E., Davidson, K., Erdjument-Bromage, H., Tempst, P., Thuring, J.W., Cooper, M.A., Lim, Z.Y., Holmes, A.B. et al. (2001) PtdIns(3)P regulates the neutrophil oxidase complex by binding to the PX domain of p40phox. Nat. Cell Biol. 3, 679-682 (Pubitemid 32624425)
30. Juhasz, G., Hill, J.H., Yan, Y., Sass, M., Baehrecke, E.H., Backer, J.M. and Neufeld, T.P. (2008) The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J. Cell Biol. 181, 655-666 (Pubitemid 351717512)
31. Burman, C. and Ktistakis, N.T. (2010) Autophagosome formation in mammalian cells. Semin. Immunopathol. 32, 397-413
32. Zhou, X., Takatoh, J. and Wang, F. (2011) The mammalian class 3 PI3K (PIK3C3) is required for early embryogenesis and cell proliferation. PLoS ONE 6, e16358
33. Zhou, X., Wang, L., Hasegawa, H., Amin, P., Han, B.X., Kaneko, S., He, Y. and Wang, F. (2010) Deletion of PIK3C3/Vps34 in sensory neurons causes rapid neurodegeneration by disrupting the endosomal but not the autophagic pathway. Proc. Natl. Acad. Sci. U.S.A. 107, 9424-9429
34. Proikas-Cezanne, T. and Codogno, P. (2011) Beclin 1 or not Beclin 1. Autophagy 7, 671-672
35. Vergne, I., Roberts, E., Elmaoued, R.A., Tosch, V., Delgado, M.A., Proikas-Cezanne, T., Laporte, J. and Deretic, V. (2009) Control of autophagy initiation by phosphoinositide 3-phosphatase Jumpy. EMBO J. 28, 2244-2258
36. Taguchi-Atarashi, N., Hamasaki, M., Matsunaga, K., Omori, H., Ktistakis, N.T., Yoshimori, T. and Noda, T. (2010) Modulation of local PtdIns3P levels by the PI phosphatase MTMR3 regulates constitutive autophagy. Traffic 11, 468-478
37. Martin, K.R., Xu, Y., Looyenga, B.D., Davis, R.J., Wu, C.L., Tremblay, M.L., Xu, H.E. and MacKeigan, J.P. (2011) Identification of PTPσ as an autophagic phosphatase. J. Cell Sci. 124, 812-819
38. Obara, K., Sekito, T., Niimi, K. and Ohsumi, Y. (2008) The Atg18-Atg2 complex is recruited to autophagic membranes via phosphatidylinositol 3-phosphate and exerts an essential function. J. Biol. Chem. 283, 23972-23980
39. Proikas-Cezanne, T., Waddell, S., Gaugel, A., Frickey, T., Lupas, A. and Nordheim, A. (2004) WIPI-1β (WIPI49), a member of the novel 7-bladed WIPI protein family, is aberrantly expressed in human cancer and is linked to starvation-induced autophagy. Oncogene 23, 9314-9325 (Pubitemid 40069664)
40. Polson, H.E., de Lartigue, J., Rigden, D.J., Reedijk, M., Urbé, S., Clague, M.J. and Tooze, S.A. (2010) Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6, 506-522
41. Obara, K., Noda, T., Niimi, K. and Ohsumi, Y. (2008) Transport of phosphatidylinositol 3-phosphate into the vacuole via autophagic membranes in Saccharomyces cerevisiae. Genes Cells 13, 537-547 (Pubitemid 351761772)
42. Axe, E.L., Walker, S.A., Manifava, M., Chandra, P., Roderick, H.L., Habermann, A., Griffiths, G. and Ktistakis, N.T. (2008) Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 182, 685-701
43. Huang, J., Birmingham, C.L., Shahnazari, S., Shiu, J., Zheng, Y.T., Smith, A.C., Campellone, K.G., Heo, W.D., Gruenheid, S., Meyer, T. et al. (2011) Antibacterial autophagy occurs at PI(3)P-enriched domains of the endoplasmic reticulum and requires Rab1 GTPase. Autophagy 7, 17-26
44. Cottam, E.M., Maier, H.J., Manifava, M., Vaux, L.C., Chandra- Schoenfelder, P., Gerner, W., Britton, P., Ktistakis, N.T. and Wileman, T. (2011) Coronavirus nsp6 proteins generate autophagosomes from the endoplasmic reticulum via an omegasome intermediate. Autophagy 7, 12-24
45. Hayashi-Nishino, M., Fujita, N., Noda, T., Yamaguchi, A., Yoshimori, T. and Yamamoto, A. (2009) A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell Biol. 11, 1433-1437
46. Ylä-Anttila, P., Vihinen, H., Jokitalo, E. and Eskelinen, E.L. (2009) 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 5, 1180-1185
47. Matsunaga, K., Morita, E., Saitoh, T., Akira, S., Ktistakis, N.T., Izumi, T., Noda, T. and Yoshimori, T. (2010) Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J. Cell Biol. 190, 511-521
48. Fan, W., Nassiri, A. and Zhong, Q. (2011) Autophagosome targeting and membrane curvature sensing by Barkor/Atg14(L). Proc. Natl. Acad. Sci. U.S.A. 108, 7769-7774
49. Wilz, L., Fan, W. and Zhong, Q. (2011) Membrane curvature response in autophagy. Autophagy 7, 1249-1250
50. Hailey, D.W., Rambold, A.S., Satpute-Krishnan, P., Mitra, K., Sougrat, R., Kim, P.K. and Lippincott-Schwartz, J. (2010) Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141, 656-667
51. Ravikumar, B., Moreau, K., Jahreiss, L., Puri, C. and Rubinsztein, D.C. (2010) Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat. Cell Biol. 12, 747-757
52. Bodemann, B.O., Orvedahl, A., Cheng, T., Ram, R.R., Ou, Y.H., Formstecher, E., Maiti, M., Hazelett, C.C., Wauson, E.M., Balakireva, M. et al. (2011) RalB and the exocyst mediate the cellular starvation response by direct activation of autophagosome assembly. Cell 144, 253-267
53. Manning, B.D. and Cantley, L.C. (2003) Rheb fills a GAP between TSC and TOR. Trends Biochem. Sci. 28, 573-576 (Pubitemid 38352801)
54. Long, X., Ortiz-Vega, S., Lin, Y. and Avruch, J. (2005) Rheb binding to mammalian target of rapamycin (mTOR) is regulated by amino acid sufficiency. J. Biol. Chem. 280, 23433-23436 (Pubitemid 40884818)
55. Sancak, Y., Peterson, T.R., Shaul, Y.D., Lindquist, R.A., Thoreen, C.C., Bar-Peled, L. and Sabatini, D.M. (2008) The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320, 1496-1501 (Pubitemid 351929429)
56. Kim, E., Goraksha-Hicks, P., Li, L., Neufeld, T.P. and Guan, K.L. (2008) Regulation of TORC1 by Rag GTPases in nutrient response. Nat. Cell Biol. 10, 935-945
57. Sancak, Y., Bar-Peled, L., Zoncu, R., Markhard, A.L., Nada, S. and Sabatini, D.M. (2010) Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141, 290-303
58. Hosokawa, N., Hara, T., Kaizuka, T., Kishi, C., Takamura, A., Miura, Y., Iemura, S., Natsume, T., Takehana, K., Yamada, N. et al. (2009) Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol. Biol. Cell 20, 1981-1991
59. Jung, C.H., Jun, C.B., Ro, S.H., Kim, Y.M., Otto, N.M., Cao, J., Kundu, M. and Kim, D.H. (2009) ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol. Biol. Cell 20, 1992-2003
60. Ganley, I.G., Lam du, H., Wang, J., Ding, X., Chen, S. and Jiang, X. (2009) ULK1·ATG13·FIP200 complex mediates mTOR signaling and is essential for autophagy. J. Biol. Chem. 284, 12297-12305
61. 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 (Pubitemid 41429682)
62. 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 (Pubitemid 41368357)
63. 2+ /CaM signaling to hVps34. Cell Metab. 7, 456-465
64. 2+ /CaM, is required for the activity and regulation of hVps34 in mammalian cells. Biochem. J. 417, 747-755
65. Flinn, R.J., Yan, Y., Goswami, S., Parker, P.J. and Backer, J.M. (2010) The late endosome is essential for mTORC1 signaling. Mol. Biol. Cell 21, 833-841
66. Li, L., Kim, E., Yuan, H., Inoki, K., Goraksha-Hicks, P., Schiesher, R.L., Neufeld, T.P. and Guan, K.L. (2010) Regulation of mTORC1 by the Rab and Arf GTPases. J. Biol. Chem. 285, 19705-19709
67. 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 (Pubitemid 34746409)
68. 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 (Pubitemid 129500945)
69. 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 (Pubitemid 37361856)
70. Korolchuk, V.I., Saiki, S., Lichtenberg, M., Siddiqi, F.H., Roberts, E.A., Imarisio, S., Jahreiss, L., Sarkar, S., Futter, M., Menzies, F.M. et al. (2011) Lysosomal positioning coordinates cellular nutrient responses. Nat. Cell Biol. 13, 453-460
71. Yu, L., McPhee, C.K., Zheng, L., Mardones, G.A., Rong, Y., Peng, J., Mi, N., Zhao, Y., Liu, Z., Wan, F. et al. (2010) Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 465, 942-946