Class III phosphoinositide 3-kinase-Beclin1 complex mediates the amino acid-dependent regulation of autophagy in C2C12 myotubes

Biochemical Journal

Volumn 376, Issue 3, 2003, Pages 577-586

  Tassa, Amina ^a   Roux, Marie Paule ^a   Attaix, Didier ^a   Bechet, Daniel M ^a  

^a CEMAGREF   (France)

Author keywords

Apg protein; Macroautophagy; Muscle cell; Phosphatidylinositol 3 kinase; Proteolysis; Signal transduction

Indexed keywords

AMINO ACIDS; IMMUNOLOGY; PRECIPITATION (CHEMICAL); PROTEINS;

CYTOPLASMIC COMPONENTS; PROTEOLYSIS;

BIOCHEMISTRY;

AMINO ACID; GLYCOGEN SYNTHASE KINASE; GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; PROTEIN BECLIN1; PROTEIN KINASE B; PROTEIN P44; PROTEIN S6; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL ORGANELLE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ENZYME DEGRADATION; ENZYME REGULATION; IMMUNOPRECIPITATION; INCUBATION TIME; LYSOSOME; MOUSE; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN MALNUTRITION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMINO ACIDS; ANDROSTADIENES; ANIMALS; ANTIBODIES; AUTOPHAGY; CELL LINE; ENZYME INHIBITORS; MACROMOLECULAR SUBSTANCES; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLE FIBERS; PROTEINS; TRANSFECTION;

ANIMALIA;

EID: 0347986620     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20030826     Document Type: Article

References (50)

1. Proud, C. G. (2002) Regulation of mammalian translation factors by nutrients. Eur. J. Biochem. 269, 5338-5349
2. 2+-activated and ATP-ubiquitin dependent proteinases in the unweighted rat soleus muscle. Biochem. J. 316, 65-72
3. Blommaart, E. F., Luiken, J. J. and Meijer, A. J. (1997) Autophagic proteolysis: control and specificity. Histochem. J. 29, 365-385
4. Mortimore, G. E., Poso, A. R. and Lardeux, B. R. (1989) Mechanism and regulation of protein degradation in liver. Diabetes Metab. Rev. 5, 49-70
5. Mordier, S., Deval, C., Bechet, D., Tassa, A. and Ferrara, M. (2000) Leucine limitation induces autophagy and activation of lysosome-dependent proteolysis in C2C12 myotubes through a mammalian target of rapamycin- independent signaling pathway. J. Biol. Chem. 275, 29900-29906
6. Ohsumi, Y. (2001) Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev Mol. Cell Biol. 2, 211-216
7. Mizushima, N., Sugita, H., Yoshimori, T. and Ohsumi, Y. (1998) A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J. Biol. Chem. 273, 33889-33892
8. Yan, J., Kuroyanagi, H., Kuroiwa, A., Matsuda, Y., Tokumitsu, H., Tomoda, T., Shirasawa, T. and Muramatsu, M. (1998) Identification of mouse ULK1, a novel protein kinase structurally related to C. elegans UNC-51. Biochem. Biophys. Res. Commun. 246, 222-227
9. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y. and Yoshimori, T. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728
10. Kamada, Y., Funakoshi, T., Shintani, T., Nagano, K., Ohsumi, M. and Ohsumi, Y. (2000) Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J. Cell Biol. 150, 1507-1513
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. Kihara, A., Kabeya, Y., Ohsumi, Y. and Yoshimori, T. (2001) Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep. 2, 330-335
13. Suzuki, K., Kirisako, T., Kamada, Y., Mizushima, N., Noda, T. and Ohsumi, Y. (2001) The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 20, 5971-5981
14. Mizushima, N., Yamamoto, A., Hatano, M., Kobayashi, Y., Kabeya, Y., Suzuki, K., Tokuhisa, T., Ohsumi, Y. and Yoshimori, T. (2001) Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 152, 657-668
15. Ogier-Denis, E., Pattingre, S., El Benna, J. and Codogno, P. (2000) Erk1/2-dependent phosphorylation of Galpha-interacting protein stimulates its GTPase accelerating activity and autophagy in human colon cancer cells. J. Biol. Chem. 275, 39090-39095
16. vom Dahl, S., Dombrowski, F., Schmitt, M., Schliess, F., Pfeifer, U. and Haussinger, D. (2001) Cell hydration controls autophagosome formation in rat liver in a microtubule-dependent way downstream from p38MAPK activation. Biochem. J. 354, 31-36
17. Petiot, A., Ogier-Denis, E., Blommaart, E. F., Meijer, A. J. and Codogno, P. (2000) Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275, 992-998
18. van Sluijters, D. A., Dubbelhuis, P. F., Blommaart, E. F. and Meijer, A. J. (2000) Amino-acid-dependent signal transduction. Biochem. J. 351, 545-550
19. Gao, X., Zhang, Y., Arrazola, P., Hino, O., Kobayashi, T., Yeung, R. S., Ru, B. and Pan, D. (2002) Tsc tumour suppressor proteins antagonize amino-acid-TOR signalling. Nat. Cell Biol. 4, 699-704
20. Kimball, S. R., Horetsky, R. L. and Jefferson, L. S. (1998) Implication of elF2B rather than elF4E in the regulation of global protein synthesis by amino acids in L6 myoblasts. J. Biol. Chem. 273, 30945-30953
21. Krause, U., Rider, M. H. and Hue, L. (1996) Protein kinase signaling pathway triggered by cell swelling and involved in the activation of glycogen synthase and acetyl-CoA carboxylase in isolated rat hepatocytes. J. Biol. Chem. 271, 16668-16673
22. Tournu, C., Obled, A., Ferrara, M., Omura, S. and Bechet, D. (2001) Glucose regulates protein catabolism in ras-transformed fibroblasts through a lysosomal-dependent proteolytic pathway. Biochem. J. 357, 255-261
23. Siddhanta, U., McIlroy, J., Shah, A., Zhang, Y. and Backer, J. M. (1998) Distinct roles for the p110alpha and hVPS34 phosphatidylinositol 3′-kinases in vesicular trafficking, regulation of the actin cytoskeleton, and mitogenesis. J. Cell Biol.143, 1647-1659
24. Bechet, D., Ferrara, M., Mordier, S., Roux, M. P., Deval, C. and Obled, A. (1991) Expression of lysosomal cathepsins during calf myoblast-myotube differentiation: characterization of a cDNA encoding bovine cathepsin B. J. Biol. Chem. 266, 14104-14112
25. Yasuda, Y., Kageyama, T., Akamine, A., Shibata, M., Kominami, E., Uchiyama, Y. and Yamamoto, K. (1999) Characterization of new fluorogenic substrates for the rapid and sensitive assay of cathepsin E and cathepsin D. J. Biochem. 125, 1137-1143
26. Kopitz, J., Kisen, G. O., Gordon, P. B., Bohley, P. and Seglen, P. O. (1990) Nonselective autophagy of cytosolic enzymes by isolated rat hepatocytes. J. Cell Biol. 111, 941-953
27. Rommel, C., Bodine, S. C., Clarke, B. A., Rossman, R., Nunez, L., Stitt, T. N., Yancopoulos, G. D. and Glass, D. J. (2001) 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, 1009-1013
28. Davies, S. P., Reddy, H., Caivano, M. and Cohen, P. (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95-105
29. Djordjevic, S. and Driscoll, P. C. (2002) Structural insight into substrate specificity and regulatory mechanisms of phosphoinositide 3-kinases. Trends Biochem. Sci. 27, 426-432
30. Fruman, D. A., Meyers, R. E. and Cantley, L. C. (1998) Phosphoinositide kinases. Annu. Rev. Biochem. 67, 481-507
31. Rameh, L. E. and Cantley, L. C. (1999) The role of phosphoinositide 3-kinase lipid products in cell function. J. Biol. Chem. 274, 8347-8350
32. 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
33. Vanhaesebroeck, B., Welham, M. J., Kotani, K., Stein, R., Warne, P. H., Zvelebil, M. J., Higashi, K., Volinia, S., Downward, J. and Waterfield, M. D. (1997) P110delta, a novel phosphoinositide 3-kinase in leukocytes. Proc. Natl. Acad. Sci. U.S.A. 94, 4330-4335
34. Inoki, K., Li, Y., Zhu, T., Wu, J. and Guan, K. L. (2002) TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 4, 648-657
35. Arcaro, A., Volinia, S., Zvelebil, M. J., Stein, R., Watton, S. J., Layton, M. J., Gout, I., Ahmadi, K., Downward, J. and Waterfield, M. D. (1998) Human phosphoinositide 3-kinase C2beta, the role of calcium and the C2 domain in enzyme activity. J. Biol. Chem. 273, 33082-33090
36. Fratti, R. A., Backer, J. M., Gruenberg, J., Corvera, S. and Deretic, V. (2001) Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J. Cell Biol. 154, 631-644
37. Franke, T. F., Kaplan, D. R., Cantley, L. C. and Toker, A. (1997) Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4- bisphosphate. Science 275, 665-668
38. Morris, M. C., Depollier, J., Mery, J., Heitz, F. and Divita, G. (2001) A peptide carrier for the delivery of biologically active proteins into mammalian cells. Nat. Biotechnol. 19, 1173-1176
39. Patti, M. E., Brambilla, E., Luzi, L., Landaker, E. J. and Kahn, C. R. (1998) Bidirectional modulation of insulin action by amino acids. J. Clin. Invest. 101, 1519-1529
40. Peyrollier, K., Hajduch, E., Blair, A. S., Hyde, R. and Hundal, H. S. (2000) 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, 361-368
41. Brunn, G. J., Williams, J., Sabers, C., Wiederrecht, G., Lawrence, Jr, J. C. and Abraham, R. T. (1996) Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J. 15, 5256-5267
42. Dennis, P. B., Jaeschke, A., Saitoh, M., Fowler, B., Kozma, S. C. and Thomas, G. (2001) Mammalian TOR: a homeostatic ATP sensor. Science 294, 1102-1105
43. Stenmark, H., Aasland, R. and Driscoll, P. C. (2002) The phosphatidylinositol 3-phosphate-binding FYVE finger. FEBS Lett. 513, 77-64
44. Panaretou, C., Domin, J., Cockcroft, S. and Waterfield, M. D. (1997) Characterization of p150, an adaptor protein for the human phosphatidylinositol (Ptdlns) 3-kinase. Substrate presentation by phosphatidylinositol transfer protein to the p150.Ptdins 3-kinase complex. J. Biol. Chem. 272, 2477-2485
45. Deval, C., Mordier, S., Obled, C., Bechet, D., Combaret, L., Attaix, D. and Ferrara, M. (2001) Identification of cathepsin L as a differientally expressed message associated with muscle wasting. Biochem. J. 360, 143-150
46. Auranen, M., Villanova, M., Muntoni, F., Fardeau, M., Scherer, S. W., Kalino, H. and Minassian, B. A. (2000) X-linked vacuolar myopathies: two separate loci and refined genetic mapping. Ann. Neurol. 47, 666-669
47. Tanaka, Y., Guhde, G., Suter, A., Eskelinen, E. L., Hartmann, D., Lullmann-Rauch, R., Janssen, P. M., Blanz, J., von Figura, K. and Saftig, P. (2000) Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature (London) 406, 902-906
48. Larsen, K. E. and Sulzer, D. (2002) Autophagy in neurons: a review. Histol. Histopathol. 17, 897-908
49. 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 (London) 402, 672-676
50. Donati, A., Cavallini, G., Paradiso, C., Vittorini, S., Pollera, M., Gori, Z. and Bergamini, E. (2001) Age-related changes in the autophagic proteolysis of rat isolated liver cells: effects of antiaging dietary restrictions. J. Gerontol. A Biol. Sci. Med. Sci. 56, B375-B383