Regulation and function of autophagy during cell survival and cell death

Cold Spring Harbor Perspectives in Biology

Volumn 4, Issue 6, 2012, Pages 1-14

  Das, Gautam ^a   Shravage, Bhupendra V ^a   Baehrecke, Eric H ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; METAZOA;

CASPASE;

ANIMAL; AUTOPHAGY; CELL DEATH; CELL SURVIVAL; GENETICS; METABOLISM; REVIEW;

ANIMALS; AUTOPHAGY; CASPASES; CELL DEATH; CELL SURVIVAL;

EID: 84863954409     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a008813     Document Type: Article

References (124)

1. Ashford TP, Porter KR. 1962. Cytoplasmic components in hepatic cell lysosomes. J Cell Biol 12: 198-202.
2. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT. 2008. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182: 685-701.
3. Baehrecke EH. 2005. Autophagy: Dual roles in life and death? Nat Rev Mol Cell Biol 6: 505-510.
4. Behrends C, Sowa ME, Gygi SP, Harper JW. 2010. Network organization of the human autophagy system. Nature 466: 68-76.
5. Berry DL, Baehrecke EH. 2007. Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 131: 1137-1148.
6. Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, 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.
7. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Yoshimori T, et al. 2005. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25: 1025-1040.
8. Bursch W, Ellinger A, Kienzl H, Torok L, Pandey S, Sikorska M, Walker R, Hermann RS. 1996. Active cell death induced by the anti-estrogens tamoxifen and ICI164384 in human mammary carcinoma cells (MCF-7) in culture: The role of autophagy. Carcinogenesis 17: 1595-1607.
9. Byfield MP, Murray JT, Backer JM. 2005. hVps34 is a nutrient- regulated lipid kinase required for activation of p70 S6 kinase. J Biol Chem 280: 33076-33082.
10. Chan EY, Longatti A, McKnight NC, Tooze SA. 2009. Kinase- inactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13-independent mechanism. Mol Cell Biol 29: 157-171.
11. Clark SLJ. 1957. Cellular differentiation in the kidneys of newborn mice studied with the electron microscope. J Biophys Biochem Cytol 3: 349-362.
12. Clarke PGH. 1990. Developmental cell death: Morphological diversity and multiple mechanisms. Anat Embryol 181: 195-213.
13. Crighton D, Wilkinson S, O'Prey J, Syed N, Smith P, Harrison PR, Gasco M, Garrone O, Crook T, Ryan KM. 2006. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126: 121-134.
14. Cuervo AM. 2008. Autophagy and aging: Keeping that old broom working. Trends Genet 24: 604-612.
15. de Duve C, Wattiaux R. 1966. Functions of lysosomes. Annu Rev Physiol 28: 435-492.
16. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gélinas C, Fan Y, et al. 2006. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10: 51-64.
17. Denton D, Shravage B, Simin R, Mills K, Berry DL, Baehrecke EH, Kumar S. 2009. Autophagy, not apoptosis, is essential for midgut cell death in Drosophila. Curr Biol 19: 1741-1746.
18. Deretic V. 2011. Autophagy in immunity and cell-autonomous defense against intracellular microbes. Immunol Rev 240: 92-104.
19. Dunn WAJ. 1990. Studies on the mechanisms of autophagy: Formation of the autophagic vacuole. J Cell Biol 110: 1923-1933.
20. Dusetti NJ, Jiang Y, Vaccaro MI, Tomasini R, Azizi Samir A, Calvo EL, Ropolo A, Fiedler F, Mallo GV, Dagorn JC, et al. 2002. Cloning and expression of the rat vacuole membrane protein 1 (VMP1), a newgene activated in pancreas with acute pancreatitis, which promotes vacuole formation. Biochem Biophys Res Commun 290: 641-649.
21. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R, et al. 2011. Phosphorylation of ULK1 (hATG1) by AMPactivated protein kinase connects energy sensing to mitophagy. Science 331: 456-461.
22. Elgendy M, Sheridan C, Brumatti G, Martin SJ. 2011. Oncogenic Ras-induced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival. Mol Cell 42: 23-35.
23. Elmore SP, Qian T, Grissom SF, Lemasters JJ. 2001. The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J 15: 2286-2287.
24. Filimonenko M, Isakson P, Finley KD, Anderson M, Jeong H, Melia TJ, Bartlett BJ, Myers KM, Birkeland HC, Lamark T, et al. 2010. The selective macroautophagic degradation of aggregated proteins requires the PI3P-binding protein Alfy. Mol Cell 38: 265-279.
25. Fimia GM, 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.
26. Fleming A, Noda T, Yoshimori T, Rubinsztein DC. 2011. Chemical modulators of autophagy as biological probes and potential therapeutics. Nat Chem Biol 7: 9-17.
27. Gu Z, Flemington C, Chittenden T, Zambetti GP. 2000. ei24, a p53 response gene involved in growth suppression and apoptosis. Mol Cell Biol 20: 233-241.
28. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ. 2008. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30: 214-226.
29. Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK, Lippincott-Schwartz J. 2010. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141: 656-667.
30. Hamed HA, Yacoub A, Park MA, Eulitt P, Sarkar D, Dimitrie IP, Chen CS, Grant S, Curiel DT, Fisher PB, et al. 2010. OSU-03012 enhances Ad.7-induced GBM cell killing via ER stress and autophagy and by decreasing expression of mitochondrial protective proteins. Cancer Biol Ther 9: 526-536.
31. 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.
32. Harding TM, Morano KA, Scott SV, Klionsky DJ. 1995. Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J Cell Bio 131: 591-602.
33. Harding TM, Hefner-Gravink A, Thumm M, Klionsky DJ. 1996. Genetic and phenotypic overlap between autophagy and the cytoplasm to vacuole protein. J Biol Chem 271: 17621-17624.
34. Hars ES, Qi H, Ryazanov AG, Jin S, Cai L, Hu C, Liu LF. 2007. Autophagy regulates ageing in C. elegans. Autophagy 3: 93-95.
35. Hou YC, Chittaranjan S, Barbosa SG, McCall K, Gorski SM. 2008. Effector caspase Dcp-1 and IAP protein Bruce regulate starvation-induced autophagy during Drosophila melanogaster oogenesis. J Cell Biol 182: 1127-1139.
36. Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, et al. 2000. A ubiquitin-like system mediates protein lipidation. Nature 408: 488-492.
37. Inoki K, Zhu T, Guan KL. 2003. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115: 577-590.
38. Jaber N, Dou Z, Chen JS, Catanzaro J, Jiang YP, Ballou LM, Selinger E, Ouyang X, Lin RZ, Zhang J, et al. 2012. Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function. Proc Natl Acad Sci 109: 2003-2008.
39. Jiang C, Baehrecke EH, Thummel CS. 1997. Steroid regulated programmed cell death during Drosophila metamorphosis. Development 124: 4673-4683.
40. Johansen T, Lamark T. 2011. Selective autophagy mediated by autophagic adapter proteins. Autophagy 7: 279-296.
41. Juhász G, Erdi B, Sass M, Neufeld TP. 2007. Atg7-dependent autophagy promotes neuronal health, stress tolerance, and longevity but is dispensable for metamorphosis in Drosophila. Genes Dev 21: 3061-3066.
42. Juhász G, Hill JH, Yan Y, Sass M, Baehrecke EH, Backer JM, Neufeld TP. 2008. The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J Cell Biol 181: 2347-2360.
43. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728.
44. Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y. 2000. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 150: 1507-1513.
45. Kang C, You YJ, Avery L. 2007. Dual roles of autophagy in the survival of Caenorhabditis elegans during starvation. Genes Dev 21: 2161-2171.
46. Kanki T, Wang K, Cao Y, Baba M, Klionsky DJ. 2009. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell 17: 98-109.
47. Kim J, Kundu M, Viollet B, Guan KL. 2011. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13: 132-141.
48. Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, Yoshimori T, Ohsumi M, Takao T, Noda T, 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: 263-276.
49. Kirkin V, Lamark T, Sou YS, Bjørkøy G, Nunn JL, Bruun JA, Shvets E, McEwan DG, Clausen TH, Wild P, et al. 2009. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell 33: 505-516.
50. Klionsky DJ. 2008. Autophagy revisited: A conversation with Christian de Duve. Autophagy 4: 740-743.
51. Klionsky DJ, Cregg JM, Dunn WAJ, Emr SD, Sakai Y, Sandoval IV, Sibirny A, Subramani S, Thumm M, Veenhuis M, et al. 2003. A unified nomenclature for yeast autophagy- related genes. Dev Cell 5: 539-545.
52. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, 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.
53. Kosta A, Roisin-Bouffay C, Luciani MF, Otto GP, Kessin RH, Golstein P. 2004. Autophagy gene disruption reveals a non-vacuolar cell death pathway in Dictyostelium. J Biol Chem 279: 48404-48409.
54. Kraft C, Deplazes A, Sohrmann M, Peter M. 2008. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat Cell Biol 10: 602-610.
55. Kuma A, Mizushima N, Ishihara N, Ohsumi Y. 2002. Formation of the approximately 350-kDa Apg12-Apg5. Apg16 multimeric complex, mediated by Apg16 oligomerization, is essential for autophagy in yeast. J Biol Chem 277: 18619-18625.
56. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N. 2004. The role of autophagy during the early neonatal starvation period. Nature 432: 1032-1036.
57. Lee C-Y, Baehrecke EH. 2001. Steroid regulation of autophagic programmed cell death during development. Development 128: 1443-1455.
58. Lee C-Y, Cooksey BAK, Baehrecke EH. 2002. Steroid regulation of midgut cell death during Drosophila development. Dev Biol 250: 101-111.
59. Lee C-Y, Clough EA, Yellon P, Teslovich TM, Stephan DA, Baehrecke EH. 2003. Genome-wide analyses of steroidand radiation-triggered programmed cell death in Drosophila. Curr Biol 13: 350-357.
60. Lee JW, Park S, Takahashi Y, Wang HG. 2010. The association of AMPK with ULK1 regulates autophagy. PLoS ONE 5: e15394.
61. Levine B, Kroemer G. 2009. Autophagy in aging, disease and death: The true identity of a cell death impostor. Cell Death Differ 16: 1-2.
62. Levine B, Yuan J. 2005.Autophagy in cell death: An innocent convict? J Clin Invest 115: 2679-2688.
63. Li TR, White KP. 2003. Tissue-specific gene expression and ecdysone-regulated genomic networks in Drosophila. Dev Cell 5: 59-72.
64. Liang XH, Kleeman LK, Jiang HH, Gordon G, Goldman JE, Berry G, Herman B, Levine B. 1998. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2- interacting protein. J Virol 72: 8586-8596.
65. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402: 672-676.
66. Lipinski MM, Hoffman G, Ng A, Zhou W, Py BF, Hsu E, Liu X, Eisenberg J, Liu J, Blenis J, et al. 2010. A genome-wide siRNA screen reveals multiple mTORC1 independent signaling pathways regulating autophagy under normal nutritional conditions. Dev Cell 18: 1041-1052.
67. Lum JJ, DeBerardinis RJ, Thompson CB. 2005. Autophagy in metazoans: Cell survival in the land of plenty. Nat Rev Mol Cell Biol 6: 439-448.
68. Mah LY, Ryan KM. 2012. Autophagy and cancer. Cold Spring Harb Perspect Biol 4: a008821.
69. Manjithaya R, Nazarko TY, Farré JC, Subramani S. 2010. Molecular mechanism and physiological role of pexophagy. FEBS Lett 584: 1367-1373.
70. Martin AP, Mitchell C, Rahmani M, Nephew KP, Grant S, Dent P. 2009. Inhibition of MCL-1 enhances lapatinib toxicity and overcomes lapatinib resistance via BAK-dependent autophagy. Cancer Biol Ther 8: 2084-2096.
71. Mathew R, Karp CM, Beaudoin B, Vuong N, Chen G, Chen HY, Bray K, Reddy A, Bhanot G, Gelinas C, et al. 2009. Autophagy suppresses tumorigenesis through elimination of p62. Cell 137: 1062-1075.
72. Matsuura A, Tsukada M, Wada Y, Ohsumi Y. 1997. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 192: 245-250.
73. McPhee CK, Baehrecke EH. 2009. Autophagy in Drosophila melanogaster. Biochim Biophys Acta 1793: 1452-1460.
74. McPhee CK, Logan MA, Freeman MR, Baehrecke EH. 2010. Activation of autophagy during cell death requires the engulfment receptor Draper. Nature 465: 1093-1096.
75. Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, Levine B. 2003. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301: 1387-1391.
76. Meley D, Bauvy C, Houben-Weerts JH, Dubbelhuis PF, Helmond MT, Codogno P, Meijer AJ. 2006. AMP-activated protein kinase and the regulation of autophagic proteolysis. J Biol Chem 281: 34870-34879.
77. Menzies FM, Moreau K, Rubinsztein DC. 2011. Protein misfolding disorders and macroautophagy. Curr Opin Cell Biol 23: 190-197.
78. Mizushima N, Komatsu M. 2011. Autophagy: Renovation of cells and tissues. Cell 147: 728-741.
79. Mohseni N, McMillan SC, Chaudhary R, Mok J, Reed BH. 2009. Autophagy promotes caspase-dependent cell death during Drosophila development. Autophagy 5: 329-338.
80. Mortensen M, Soilleux EJ, Djordjevic G, Tripp R, Lutteropp M, Sadighi-Akha E, Stranks AJ, Glanville J, Knight S, Jacobsen SE, et al. 2011. The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance. J Exp Med 208: 455-467.
81. Nair U, Jotwani A, Geng J, Gammoh N, Richerson D, Yen WL, Griffith J, Nag S, Wang K, Moss T, et al. 2011. SNARE proteins are required for macroautophagy. Cell 146: 290-302.
82. Narendra D, Tanaka A, Suen DF, Youle RJ. 2008. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183: 795-803.
83. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, Youle RJ. 2010. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 8: e1000298.
84. Nezis IP, Lamark T, Velentzas AD, Rusten TE, Bjørkøy G, Johansen T, Papassideri IS, Stravopodis DJ, Margaritis LH, Stenmark H, et al. 2009.Cell death during Drosophila melanogaster early oogenesis is mediated through autophagy. Autophagy 5: 298-302.
85. Nezis IP, Shravage BV, Sagona AP, Lamark T, Bjørkøy G, Johansen T, Rusten TE, Brech A, Baehrecke EH, Stenmark H. 2010. Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis. J Cell Biol 190: 523-531.
86. Nixon RA, Yang D.-S. 2012. Autophagy and neuronal cell death in neurological disorders. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a008839.
87. Nobukuni T, Joaquin M, Roccio M, Dann SG, Kim SY, Gulati P, Byfield MP, Backer JM, Natt F, Bos JL, et al. 2005. Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Proc Natl Acad Sci 102: 14238-14243.
88. Novak I, Kirkin V, McEwan DG, Zhang J, Wild P, Rozenknop A, Rogov V, Löhr F, Popovic D, Occhipinti A, et al. 2010. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 11: 45-51.
89. Novikoff AB, Essner E. 1962. Cytolysomes and mitochondrial degeneration. J Cell Biol 15: 140-146.
90. Ohsumi Y. 2001. Molecular dissection of autophagy: Two ubiquitin-like systems. Nat Rev Mol Cell Biol 2: 211-216.
91. Okamoto K, Kondo-Okamoto N, Ohsumi Y. 2009. Mitochondria- anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 17: 87-97.
92. Otto GP, Wu MY, Kazgan N, Anderson OR, Kessin RH. 2003. Macroautophagy is required for multicellular development of the social amoeba Dictyostelium discoideum. J Biol Chem 278: 17636-17645.
93. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. 2005. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122: 927-939.
94. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen EL, Mizushima N, Ohsumi Y, et al. 2003. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 112: 1809-1820.
95. Qu X, Zou Z, Sun Q, Luby-Phelps K, Cheng P, Hogan RN, Gilpin C, Levine B. 2007. Autophagy gene-dependent clearance of apoptotic cells during embryonic development. Cell 128: 931-946.
96. Radoshevich L, Murrow L, Chen N, Fernandez E, Roy S, Fung C, Debnath J. 2010. ATG12 conjugation to ATG3 regulates mitochondrial homeostasis and cell death. Cell 142: 590-600.
97. Ravikumar B, Moreau K, Jahreiss L, Puri C, Rubinsztein DC. 2010. Plasma membrane contributes to the formation of pre-autophagosomal structures. NatCell Biol 12: 747-757.
98. Ryoo HD, Baehrecke EH. 2010. Distinct death mechanisms in Drosophila development. Curr Opin Cell Biol 22: 889-895.
99. Samari HR, Seglen PO. 1998. Inhibition of hepatocytic autophagy by adenosine, aminoimidazole-4-carboxamide riboside, and N6-mercaptopurine riboside. Evidence for involvement of amp-activated protein kinase. J Biol Chem 273: 23758-23763.
100. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. 2010. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141: 290-303.
101. Schweichel J-U, Merker H-J. 1973. The morphology of various types of cell death in prenatal tissues. Teratology 7: 253-266.
102. Scott RC, Schuldiner O, Neufeld TP. 2004. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev Cell 7: 167-178.
103. Scott RC, Juhász G, Neufeld TP. 2007. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr Biol 17: 1-11.
104. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa- Kobayashi S, Thompson CB, Tsujimoto Y. 2004. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6: 1221-1228.
105. Simonsen A, Tooze SA. 2009. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J Cell Biol 186: 773-782.
106. Simonsen A, Cumming RC, Brech A, Isakson P, Schubert DR, Finley KD. 2007. Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy 4: 176-184.
107. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ. 2009. Autophagy regulates lipid metabolism. Nature 458: 1131-1135.
108. Sjöblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, Mandelker D, Leary RJ, Ptak J, Silliman N, et al. 2006. The consensus coding sequences of human breast and colorectal cancers. Science 314: 268-274.
109. Takamura A, Komatsu M, Hara T, Sakamoto A, Kishi C, Waguri S, Eishi Y, Hino O, Tanaka K, Mizushima N. 2011. Autophagy-deficient mice develop multiple liver tumors. Genes Dev 25: 795-800.
110. Tanida I, Mizushima N, Kiyooka M, Ohsumi M, Ueno T, Ohsumi Y, Kominami E. 1999. Apg7p/Cvt2p: A novel protein-activating enzyme essential for autophagy. Mol Biol Cell 10: 1367-1379.
111. Thumm M, Egner R, Koch B, Schlumpberger M, Straub M, Veenhuis M, Wolf DH. 1994. Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett 349: 275-280.
112. Tian Y, Li Z, Hu W, Ren H, Tian E, Zhao Y, Lu Q, Huang X, Yang P, Li X, et al. 2010. C. elegans screen identifies autophagy genes specific to multicellular organisms. Cell 141: 1042-1055.
113. Tsukada M, Ohsumi Y. 1993. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333: 169-174.
114. Vergne I, Roberts E, Elmaoued RA, Tosch V, Delgado MA, Proikas-Cezanne T, Laporte J, Deretic V. 2009. Control of autophagy initiation by phosphoinositide 3-phosphatase Jumpy. EMBO J 28: 2244-2258.
115. Wang Z, Wilson WA, Fujino MA, Roach PJ. 2001. Antagonistic controls of autophagy and glycogen accumulation by Snf1p, the yeast homolog of AMP-activated protein kinase, and the cyclin-dependent kinase Pho85p. Mol Cell Biol 21: 5742-5752.
116. Wei H, Wei S, Gan B, Peng X, Zou W, Guan JL. 2011. Suppression of autophagy by FIP200 deletion inhibits mammary tumorigenesis. Genes Dev 25: 1510-1527.
117. Weidberg H, Shvets E, Elazar Z. 2010. Biogenesis and cargo selectivity of autophagosomes. Annu Rev Biochem 80: 125-156.
118. Wullschleger S, Loewith R, Hall MN. 2006. TORsignaling in growth and metabolism. Cell 124: 471-484.
119. Yang S, Wang X, Contino G, Liesa M, Sahin E, Ying H, Bause A, Li Y, Stommel JM, Dell'antonio G, et al. 2011. Pancreatic cancers require autophagy for tumor growth. Genes Dev 25: 717-729.
120. You YJ, Kim J, Cobb M, Avery L. 2006. Starvation activates MAP kinase through themuscarinic acetylcholine pathway in Caenorhabditis elegans pharynx. CellMetab 3: 237-245.
121. Yu L, Alva A, Su H, Dutt P, Freundt E, Welsh S, Baehrecke EH, Lenardo MJ. 2004. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304: 1500-1502.
122. Yu L, Wan F, Dutta S, Welsh S, Liu Z, Freundt E, Baehrecke EH, Lenardo MJ. 2006. Autophagic programmed cell death by selective catalase degradation. Proc Natl Acad Sci 103: 4952-4957.
123. Yu L, McPhee CK, Zheng L, Mardones GA, Rong Y, Peng J, Mi N, Zhao Y, Liu Z, Wan F, et al. 2010. Autophagy termination and lysosome reformation regulated by mTOR. Nature 465: 942-946.
124. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. 2003. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci 100: 15077-15082.