Eaten alive: A history of macroautophagy

Nature Cell Biology

Volumn 12, Issue 9, 2010, Pages 814-822

  Yang, Zhifen ^a,b   Klionsky, Daniel J ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b Department of Molecular Cellular and Developmental Biology Natural Science Building ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; AGING; AUTOPHAGY; CARCINOGENESIS; CELL DEATH; CELL MATURATION; CELL ORGANELLE; CELL SURVIVAL; HOMEOSTASIS; IMMUNE RESPONSE; INFECTION; INNATE IMMUNITY; LIFESPAN; LONGEVITY; MACROAUTOPHAGY; METABOLIC STRESS; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; HISTORY; HUMAN; PHYSIOLOGY;

ANIMALS; AUTOPHAGY; CELL BIOLOGY; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; MODELS, BIOLOGICAL;

EID: 77956404377     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb0910-814     Document Type: Review

References (119)

1. Clark, S. L. Jr. Cellular differentiation in the kidneys of newborn mice studied with the electron microscope. J. Biophys. Biochem. Cytol. 3, 349-362 (1957).
2. Novikoff, A. B. The proximal tubule cell in experimental hydronephrosis. J. Biophys. Biochem. Cytol. 6, 136-138 (1959).
3. Ashford, T. P. & Porter, K. R. Cytoplasmic components in hepatic cell lysosomes. J. Cell Biol. 12, 198-202 (1962).
4. Novikoff, A. B. & Essner, E. Cytolysomes and mitochondrial degeneration. J. Cell Biol. 15, 140-146 (1962).
5. de Duve, C. & Wattiaux, R. Functions of lysosomes. Annu. Rev. Physiol. 28, 435-492 (1966).
6. Novikoff, A. B., Essner, E. & Quintana, N. Golgi apparatus and lysosomes. Fed. Proc. 23, 1010-1022 (1964).
7. Deter, R. L., Baudhuin, P. & de Duve, C. Participation of lysosomes in cellular autophagy induced in rat liver by glucagon. J. Cell Biol. 35, C11-16 (1967).
8. Pfeifer, U. Inhibition by insulin of the physiological autophagic breakdown of cell organelles. Acta Biol. Med. Ger. 36, 1691-1694 (1977).
9. Mortimore, G. E. & Schworer, C. M. Induction of autophagy by amino-acid deprivation in perfused rat liver. Nature 270, 174-176 (1977).
10. Seglen, P. O. & Gordon, P. B. 3-methyladenine: specific inhibitor of autophagic/lyso-somal protein degradation in isolated rat hepatocytes. Proc. Natl Acad. Sci. USA 79, 1889-1892 (1982).
11. Holen, I., Gordon, P. B. & Seglen, P. O. Protein kinase-dependent effects of okadaic acid on hepatocytic autophagy and cytoskeletal integrity. Biochem. J. 284, 633-636 (1992).
12. Gordon, P. B. & Seglen, P. O. Prelysosomal convergence of autophagic and endocytic pathways. Biochem. Biophys. Res. Commun. 151, 40-47 (1988).
13. Bolender, R. P. & Weibel, E. R. A morphometric study of the removal of phenobarbital-induced membranes from hepatocytes after cessation of treatment. J. Cell Biol. 56, 746-761 (1973).
14. Beaulaton, J. & Lockshin, R. A. Ultrastructural study of the normal degeneration of the intersegmental muscles of Anthereae polyphemus and Manduca sexta (Insecta, Lepidoptera) with particular reference of cellular autophagy. J. Morphol. 154, 39-57 (1977).
15. Veenhuis, M., Douma, A., Harder, W. & Osumi, M. Degradation and turnover of peroxi-somes in the yeast Hansenula polymorpha induced by selective inactivation of peroxi-somal enzymes. Arch. Microbiol. 134, 193-203 (1983).
16. Lemasters, J. J. et al. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta 1366, 177-196 (1998).
17. Takeshige, K., Baba, M., Tsuboi, S., Noda, T. & Ohsumi, Y. Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J. Cell Biol. 119, 301-311 (1992).
18. Tsukada, M. & Ohsumi, Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333, 169-174 (1993).
19. Titorenko, V. I., Keizer, I., Harder, W. & Veenhuis, M. Isolation and characterization of mutants impaired in the selective degradation of peroxisomes in the yeast Hansenula polymorpha. J. Bacteriol. 177, 357-363 (1995).
20. Harding, T. M., Morano, K. A., Scott, S. V. & Klionsky, D. J. Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J. Cell Biol. 131, 591-602 (1995).
21. Klionsky, D. J. et al. A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5, 539-545 (2003).
22. Matsuura, A., Tsukada, M., Wada, Y. & Ohsumi, Y. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 192, 245-250 (1997).
23. Kanki, T. et al. A genomic screen for yeast mutants defective in selective mitochondria autophagy. Mol. Biol. Cell 20, 4730-4738 (2009).
24. Okamoto, K., Kondo-Okamoto, N. & Ohsumi, Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 17, 87-97 (2009).
25. Klionsky, D. J., Cueva, R. & Yaver, D. S. Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J. Cell Biol. 119, 287-299 (1992).
26. Hutchins, M. U. & Klionsky, D. J. Vacuolar localization of oligomeric α-mannosidase requires the cytoplasm to vacuole targeting and autophagy pathway components in Saccharomyces cerevisiae. J. Biol. Chem. 276, 20491-20498 (2001).
27. Xie, Z. & Klionsky, D. J. Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9, 1102-1109 (2007).
28. Suzuki, K. et al. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 20, 5971-5981 (2001).
29. Kim, J., Huang, W.-P., Stromhaug, P. E. & Klionsky, D. J. Convergence of multiple autophagy and cytoplasm to vacuole targeting components to a perivacuolar membrane compartment prior to de novo vesicle formation. J. Biol. Chem. 277, 763-773 (2002).
30. Teter, S. A. et al. Degradation of lipid vesicles in the yeast vacuole requires function of Cvt17, a putative lipase. J. Biol. Chem. 276, 2083-2087 (2001).
31. Epple, U. D., Suriapranata, I., Eskelinen, E.-L. & Thumm, M. Aut5/Cvt17p, a putative lipase essential for disintegration of autophagic bodies inside the vacuole. J. Bacteriol. 183, 5942-5955 (2001).
32. Yang, Z., Huang, J., Geng, J., Nair, U. & Klionsky, D. J. Atg22 recycles amino acids to link the degradative and recycling functions of autophagy. Mol. Biol. Cell 17, 5094-5104 (2006).
33. Mizushima, N., Sugita, H., Yoshimori, T. & Ohsumi, Y. A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J. Biol. Chem. 273, 33889-33892 (1998).
34. Kabeya, Y. et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728 (2000).
35. Klionsky, D. J. et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4, 151-175 (2008).
36. Yang, Z. & Klionsky, D. J. Mammalian autophagy: core molecular machinery and signaling regulation. Curr. Opin. Cell Biol. 22, 124-131 (2009).
37. Mizushima, N. et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 152, 657-668 (2001).
38. Tian, Y. et al. C. elegans screen identifies autophagy genes specific to multicellular organisms. Cell 141, 1042-1055 (2010).
39. Behrends, C., Sowa, M. E., Gygi, S. P. & Harper, J. W. Network organization of the human autophagy system. Nature 466, 68-76 (2010).
40. Lipinski, M. M. et al. A genome-wide siRNA screen reveals multiple mTORC1 independent signaling pathways regulating autophagy under normal nutritional conditions. Dev. Cell 18, 1041-1052 (2010).
41. Axe, E. L. et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 182, 685-701 (2008).
42. Hayashi-Nishino, M. et al. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell Biol. 11, 1433-1437 (2009).
43. Yla-Anttila, P., Vihinen, H., Jokitalo, E. & Eskelinen, E.-L. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 5, 1180-1185 (2009).
44. Hailey, D. W. et al. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141, 656-667 (2010).
45. Ravikumar, B., Moreau, K., Jahreiss, L., Puri, C. & Rubinsztein, D. C. Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat. Cell Biol. 12, 747-757 (2010).
46. Tooze, S. A & Yoshimori, T. The origin of the autophagosomal membrane. Nat. Cell Biol. 12, 831-835 (2010).
47. Bavro, V. N. et al. Crystal structure of the GABAA-receptor-associated protein, GABARAP. EMBO Rep. 3, 183-189 (2002).
48. Sugawara, K. et al. The crystal structure of microtubule-associated protein light chain 3, a mammalian homologue of Saccharomyces cerevisiae Atg8. Genes Cells 9, 611-618 (2004).
49. Miller, S. et al. Shaping development of autophagy inhibitors with the structure of the lipid kinase Vps34. Science 327, 1638-1642 (2010).
50. Kunz, J. et al. Target of rapamycin in yeast, TOR2, is an essential phosphatidylinositol kinase homolog required for G1 progression. Cell 73, 585-596 (1993).
51. Brown, E. J. et al. A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 369, 756-758 (1994).
52. Blommaart, E. F., Luiken, J. J., Blommaart, P. J., van Woerkom, G. M. & Meijer, A. J. Phosphorylation of ribosomal protein S6 is inhibitory for autophagy in isolated rat hepatocytes. J. Biol. Chem. 270, 2320-2326 (1995).
53. Noda, T. & Ohsumi, Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 273, 3963-3966 (1998).
54. Blommaart, E. F. , Krause, U., Schellens, J. P., Vreeling-Sindelarova, H. & Meijer, A. J. The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur. J. Biochem. 243, 240-246 (1997).
55. Petiot, A., Ogier-Denis, E., Blommaart, E. F. , Meijer, A. J. & Codogno, P. Distinct classes of phosphatidylinositol 3'-kinases are involved in signaling pathways that control mac-roautophagy in HT-29 cells. J. Biol. Chem. 275, 992-998 (2000).
56. Arico, S. et al. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J. Biol. Chem. 276, 35243-35246 (2001).
57. Meijer, A. J. & Codogno, P. Regulation and role of autophagy in mammalian cells. Int. J. Biochem. Cell Biol. 36, 2445-2462 (2004).
58. Wei, Y., Pattingre, S., Sinha, S., Bassik, M. & Levine, B. JNK1-mediated phospho-rylation of Bcl-2 regulates starvation-induced autophagy. Mol. Cell 30, 678-688 (2008).
59. Zalckvar, E. et al. DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy. EMBO Rep. 10, 285-292 (2009).
60. Liang, X. H. et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672-676 (1999).
61. Pattingre, S. et al. Bcl-2 anti-apoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927-939 (2005).
62. Aita, V. M. et al. Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 59, 59-65 (1999).
63. Qu, X. et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 112, 1809-1820 (2003).
64. Yue, Z., Jin, S., Yang, C., Levine, A. J. & Heintz, N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl Acad. Sci. USA 100, 15077-15082 (2003).
65. Marino, G. et al. Tissue-specific autophagy alterations and increased tumorigenesis in mice deficient in Atg4C/autophagin-3. J. Biol. Chem. 282, 18573-18583 (2007).
66. Degenhardt, K. et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10, 51-64 (2006).
67. Mathew, R. et al. Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev. 21, 1367-1381 (2007).
68. Mathew, R. et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 137, 1062-1075 (2009).
69. Amaravadi, R. K. et al. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J. Clin. Invest. 117, 326-336 (2007).
70. Carew, J. S. et al. Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHA to overcome Bcr-Abl-mediated drug resistance. Blood 110, 313-322 (2007).
71. Ravikumar, B., Duden, R. & Rubinsztein, D. C. Aggregate-prone proteins with poly-glutamine and polyalanine expansions are degraded by autophagy. Hum. Mol. Genet. 11, 1107-1117 (2002).
72. Ravikumar, B. et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 36, 585-595 (2004).
73. Webb, J. L., Ravikumar, B., Atkins, J., Skepper, J. N. & Rubinsztein, D. C. α-Synuclein is degraded by both autophagy and the proteasome. J. Biol. Chem. 278, 25009-25013 (2003).
74. Yu, W. H. et al. Macroautophagy - a novel β-amyloid peptide-generating pathway activated in Alzheimer's disease. J. Cell Biol. 171, 87-98 (2005).
75. Komatsu, M. et al. Loss of autophagy in the central nervous system causes neurode-generation in mice. Nature 441, 880-884 (2006).
76. Hara, T. et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885-889 (2006).
77. Bjørkøy, G. et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell. Biol. 171, 603-614 (2005).
78. Iwata, A., Riley, B. E., Johnston, J. A. & Kopito, R. R. HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J. Biol. Chem. 280, 40282-40292 (2005).
79. Komatsu, M. et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131, 1149-1163 (2007).
80. Kirkin, V. et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 33, 505-516 (2009).
81. Nezis, I. P. et al. Ref(2)P, the Drosophila melanogaster homologue of mammalian p62, is required for the formation of protein aggregates in adult brain. J. Cell Biol. 180, 1065-1071 (2008).
82. Pankiv, S. et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24131-24145 (2007).
83. Kim, P. K., Hailey, D. W., Mullen, R. T. & Lippincott-Schwartz, J. Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc. Natl Acad. Sci. USA 105, 20567-20574 (2008).
84. Kraft, C., Peter, M. & Hoffman, K. Selective autophagy: ubiquitin-mediated recognition and beyond. Nat. Cell Biol. 12, 836-841 (2010).
85. Rikihisa, Y. Glycogen autophagosomes in polymorphonuclear leukocytes induced by rickettsiae. Anat. Rec. 208, 319-327 (1984).
86. Gutierrez, M. G. et al. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753-766 (2004).
87. Nakagawa, I. et al. Autophagy defends cells against invading group A Streptococcus. Science 306, 1037-1040 (2004).
88. Andrade, R. M., Wessendarp, M., Gubbels, M. J., Striepen, B. & Subauste, C. S. CD40 induces macrophage anti-Toxoplasma gondii activity by triggering autophagy-dependent fusion of pathogen-containing vacuoles and lysosomes. J. Clin. Invest. 116, 2366-2377 (2006).
89. Singh, S. B., Davis, A. S., Taylor, G. A. & Deretic, V. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 313, 1438-1441 (2006).
90. Ogawa, M. et al. Escape of intracellular Shigella from autophagy. Science 307, 727-731 (2005).
91. Yano, T. et al. Autophagic control of Listeria through intracellular innate immune recognition in Drosophila. Nat. Immunol. 9, 908-916 (2008).
92. Thurston, T. L., Ryzhakov, G., Bloor, S., von Muhlinen, N. & Randow, F. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 10, 1215-1221 (2009).
93. Liang, X. H. et al. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J. Virol. 72, 8586-8596 (1998).
94. Tallóczy, Z., Virgin, H. W. IV. & Levine, B. PKR-dependent autophagic degradation of herpes simplex virus type 1. Autophagy 2, 24-29 (2006).
95. Orvedahl, A. et al. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1, 23-35 (2007).
96. Paludan, C. et al. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307, 593-596 (2005).
97. English, L. et al. Autophagy enhances the presentation of endogenous viral antigens on MHC class I molecules during HSV-1 infection. Nat. Immunol. 10, 480-487 (2009).
98. Del Roso, A. et al. Ageing-related changes in the in vivo function of rat liver macroau-tophagy and proteolysis. Exp. Gerontol. 38, 519-527 (2003).
99. Donati, A. et al. Age-related changes in the regulation of autophagic proteolysis in rat isolated hepatocytes. J. Gerontol. A Biol. Sci. Med. Sci. 56, B288-293 (2001).
100. Cavallini, G., Donati, A., Gori, Z. & Bergamini, E. Towards an understanding of the anti-aging mechanism of caloric restriction. Curr. Aging Sci. 1, 4-9 (2008).
101. Meléndez, A. et al. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301, 1387-1391 (2003).
102. Juhasz, G., Erdi, B., Sass, M. & Neufeld, T. P. Atg7-dependent autophagy promotes neuronal health, stress tolerance and longevity but is dispensable for metamorphosis in Drosophila. Genes Dev. 21, 3061-3066 (2007).
103. Simonsen, A. et al. Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy 4, 176-184 (2008).
104. Madeo, F. , Tavernarakis, N. & Kroemer, G. Can autophagy promote longevity? Nat Cell Biol. 12, 842-846 (2010).
105. Bergamini, E. Targets for antiageing drugs. Expert Opin. Ther. Targets 9, 77-82 (2005).
106. Eisenberg, T. et al. Induction of autophagy by spermidine promotes longevity. Nat Cell Biol. 11, 1305-1314 (2009).
107. Otto, G. P., Wu, M. Y., Kazgan, N., Anderson, O. R. & Kessin, R. H. Macroautophagy is required for multicellular development of the social amoeba Dictyostelium discoideum J. Biol. Chem. 278, 17636-17645 (2003).
108. Juhasz, G., Csikos, G., Sinka, R., Erdelyi, M. & Sass, M. The Drosophila homolog of Aut1 is essential for autophagy and development. FEBS Lett. 543, 154-158 (2003).
109. Kuma, A. et al. The role of autophagy during the early neonatal starvation period. Nature 432, 1032-1036 (2004).
110. Komatsu, M. et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169, 425-434 (2005).
111. Tsukamoto, S. et al. Autophagy is essential for pre-implantation development of mouse embryos. Science 321, 117-120 (2008).
112. Mizushima, N. & Levine, B. Autophagy in mammalian development and differentiation. Nat. Cell Biol. 12, 823-830 (2010).
113. Schin, K. S. & Clever, U. Lysosomal and free acid phosphatase in salivary glands of Chironomus tentans. Science 150, 1053-1055 (1965).
114. Nopanitaya, W. & Misch, D. W. Developmental cytology of the midgut in the flesh-fly, Sarcophaga bullata (Parker). Tissue Cell 6, 487-502 (1974).
115. Yu, L. et al. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304, 1500-1502 (2004).
116. Shimizu, S. et al. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 6, 1221-1228 (2004).
117. Berry, D. L. & Baehrecke, E. H. Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 131, 1137-1148 (2007).
118. McPhee, C. K., Logan, M. A., Freeman, M. R. & Baehrecke, E. H. Activation of autophagy during cell death requires the engulfment receptor Draper. Nature 465, 1093-1096 (2010).
119. Mathew, R., Karantza-Wadsworth, V. & White, E. Role of autophagy in cancer. Nat. Rev. Cancer 7, 961-967 (2007).