The role of mammalian autophagy in protein metabolism

Proceedings of the Japan Academy Series B: Physical and Biological Sciences

Volumn 83, Issue 2, 2007, Pages 39-46

  Mizushima, Noboru ^a,b  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Aggregation; Amino acids; Protein degradation; Starvation

Indexed keywords

BACTERIA (MICROORGANISMS); EUKARYOTA; MAMMALIA;

EID: 33947288435     PISSN: 03862208     EISSN: 13492896     Source Type: Journal    
DOI: 10.2183/pjab.83.39     Document Type: Review

References (50)

1. Cuervo, A.M. (2004) Autophagy: in sickness and in health. Trends Cell Biol. 14, 70-77.
2. Levine, B. and Klionsky, D.J. (2004) Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6, 463-477.
3. Klionsky, D.J. (2005) The molecular machinery of autophagy: unanswered questions. J. Cell Sci. 118, 7-18.
4. Mizushima, N. (2005) The pleiotropic role of autophagy: from protein metabolism to bactericide. Cell Death Differ. 12 (Suppl. 2), 1535-1541.
5. Ohsumi, Y. (2001) Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. Mol. Cell Biol. 2, 211-216.
6. Klionsky, D.J., Cregg, J.M., Dunn, W.A., Jr., Emr, S.D., Sakai, Y., Sandoval, I.V., Sibirny, A., Subramani, S., Thumm, M., Veenhuis, M. et al. (2003) A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5, 539-545.
7. 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.
8. Noda, T., Suzuki, K. and Ohsumi, Y. (2002) Yeast autophagosomes: de novo formation of a membrane structure. Trends Cell Biol. 12, 231-235.
9. 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.
10. Liang, X.H., Kleeman, L.K., Jiang, H.H., Gordon, G., Goldman, J.E., Berry, G., Herman, B. and Levine, B. (1998) Protection against fatal Sindbis virus encephalitis by Beclin, a novel Bcl-2-interacting protein. J. Virol. 72, 8586-8596.
11. Kihara, A., Kabeya, Y., Ohsumi, Y. and Yoshimori, T. (2001) Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Reports 2, 330-335.
12. 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.
13. 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.
14. Mizushima, N., Noda, T., Yoshimori, T., Tanaka, Y., Ishii, T., George, M.D., Klionsky, D.J., Ohsumi, M. and Ohsumi, Y. (1998) A protein conjugation system essential for autophagy. Nature 395, 395-398.
15. 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.
16. 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, 657-667.
17. Mizushima, N., Yoshimori, T. and Ohsumi, Y. (2003) Role of the Apg12 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 35, 553-561.
18. Mizushima, N., Noda, T. and Ohsumi, Y. (1999) Apg16p is required for the function of the Apg12p-Apg5p conjugate in the yeast autophagy pathway. EMBO J. 18, 3888-3896.
19. Kuma, A., Mizushima, N., Ishihara, N. and Ohsumi, Y. (2002) Formation of the ∼350-kDa Apg12-Apg5·Apg16 multimeric complex, mediated by Apg16 oligomerization, is essential for autophagy in yeast. J. Biol. Chem. 277, 18619-18625.
20. Mizushima, N., Kuma, A., Kobayashi, Y., Yamamoto, A., Matsubae, M., Takao, T., Natsume, T., Ohsumi, Y. and Yoshimori, T. (2003) Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J. Cell Sci. 116, 1679-1688.
21. Ichimura, Y., Kirisako, T., Takao, T., Satomi, Y., Shimonishi, Y., Ishihara, N., Mizushima, N., Tanida, I., Kominami, E., Ohsumi, M. et al. (2000) A ubiquitin-like system mediates protein lipidation. Nature 408, 488-492.
22. 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.
23. Kirisako, T., Ichimura, Y., Okada, H., Kabeya, Y., Mizushima, N., Yoshimori, T., Ohsumi, M., Takao, T., Noda, T. and Ohsumi, Y. (2000) The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J. Cell Biol. 151, 263-275.
24. Marin∼o, G., Uria, J.A., Puente, X.S., Quesada, V., Bordallo, J. and López-Otin, C. (2003) Human autophagins, a family of cysteine proteinases potentially implicated in cell degradation by autophagy. J. Biol. Chem. 278, 3671-3678.
25. Kabeya, Y., Mizushima, N., Yamamoto, A., Oshitani-Okamoto, S., Ohsumi, Y. and Yoshimori, T. (2004) LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell. Sci. 117, 2805-2812.
26. Tanida, I., Sou, Y.S., Ezaki, J., Minematsu-Ikeguchi, N., Ueno, T. and Kominami, E. (2004) HsAtg4B/HsApg4B/autophagin-1 cleaves the carboxyl termini of three human Atg8 homologues and delipidates microtubule-associated protein light chain 3- and GABAA receptor-associated protein-phospholipid conjugates. J. Biol. Chem. 279, 36268-36276 (Epub 2004 Jun 8).
27. Mizushima, N. (2004) Methods for monitoring autophagy. Int. J. Biochem. Cell Biol. 36, 2491-2502.
28. Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T. and Ohsumi, Y. (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15, 1101-1111.
29. Takeshige, K., Baba, M., Tsuboi, S., Noda, T. and Ohsumi, Y. (1992) Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J. Cell Biol. 119, 301-311.
30. Munz, C. (2006) Autophagy and antigen presentation. Cell. Microbiol. 8, 891-898.
31. Tsukada, M. and Ohsumi, Y. (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333, 169-174.
32. Otto, G.P., Wu, M.Y., Kazgan, N., Anderson, O.R. and Kessin, R.H. (2003) Macroautophagy is required for multicellular development of the social amoeba Dictyostelium discoideum. J. Biol. Chem. 278, 17636-17645.
33. Scott, R.C., Schuldiner, O. and Neufeld, T.P. (2004) Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell 7, 167-178.
34. Kuma, A., Hatano, M., Matsui, M., Yamamoto, A., Nakaya, H., Yoshimori, T., Ohsumi, Y., Tokuhisa, T. and Mizushima, N. (2004) The role of autophagy during the early neonatal starvation period. Nature 432, 1032-1036.
35. Lum, J.J., Bauer, D.E., Kong, M., Harris, M.H., Li, C., Lindsten, T. and Thompson, C.B. (2005) Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120, 237-248.
36. Onodera, J. and Ohsumi, Y. (2005) Autophagy is required for maintenance of amino acid levels and protein synthesis under nitrogen starvation. J. Biol. Chem. 280, 31582-31586.
37. Fingar, D.C. and Blenis, J. (2004) Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 23, 3151-3171.
38. Codogno, P. and Meijer, A.J. (2005) Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ. 12 (Suppl. 2), 1509-1518.
39. Noda, T. and Ohsumi, Y. (1998) Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 273, 3963-3966.
40. Hosokawa, N., Hara, Y. and Mizushima, N. (2006) Generation of cell lines with tetracycline-regulated autophagy and a role for autophagy in controlling cell size. FEBS Lett. 580, 2623-2629.
41. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H. et al. (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885-889.
42. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J.I., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E. et al. (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441, 880-884.
43. Komatsu, M., Waguri, S., Ueno, T., Iwata, J., Murata, S., Tanida, I., Ezaki, J., Mizushima, N., Ohsumi, Y., Uchiyama, Y. et al. (2005) Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169, 425-434.
44. Arrasate, M., Mitra, S., Schweitzer, E.S., Segal, M.R. and Finkbeiner, S. (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431, 805-810.
45. Bjorkoy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Overvatn, A., Stenmark, H. and Johansen, T. (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171, 603-614.
46. Wang, Q.J., Ding, Y., Kohtz, S., Mizushima, N., Cristea, I.M., Rout, M.P., Chait, B.T., Zhong, Y., Heintz, N. and Yue, Z. (2006) Induction of autophagy in axonal dystrophy and degeneration. J. Neurosci. 26, 8057-8068.
47. Iwata, J., Ezaki, J., Komatsu, M., Yokota, S., Ueno, T., Tanida, I., Chiba, T., Tanaka, K. and Kominami, E. (2006) Excess peroxisomes are degraded by autophagic machinery in mammals. J. Biol. Chem. 281, 4035-4041.
48. David, L.L. and Shearer, T.R. (1989) Role of proteolysis in lenses: a review. Lens Eye Toxic. Res. 6, 725-747.
49. Bassnett, S. (2002) Lens organelle degradation. Exp. Eye Res. 74, 1-6.
50. Matsui, M., Yamamoto, A., Kuma, A., Ohsumi, Y. and Mizushima, N. (2006) Organelle degradation during the lens and erythroid differentiation is independent of autophagy. Biochem. Biophys. Res. Commun. 339, 485-489.