Autophagy regulation and integration with cell signaling

Antioxidants and Redox Signaling

Volumn 17, Issue 5, 2012, Pages 756-765

  Hamacher Brady, Anne ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGOSOME; AUTOPHAGY; CELL ORGANELLE; CELL STRESS; HUMAN; LYSOSOME; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; AUTOPHAGY; HUMANS; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 84863428905     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.4410     Document Type: Review

References (75)

1. Abedin MJ, Wang D, McDonnell MA, Lehmann U, and Kelekar A. Autophagy delays apoptotic death in breast cancer cells following DNA damage. Cell Death Differ 14: 500-510, 2007.
2. Behrends C, Sowa ME, Gygi SP, and Harper JW. Network organization of the human autophagy system. Nature 466: 68-76, 2010.
3. Brady NR, Hamacher-Brady A, Yuan H, and Gottlieb RA. The autophagic response to nutrient deprivation in the hl-1 cardiac myocyte is modulated by Bcl-2 and sarco/endoplasmic reticulum calcium stores. FEBS J 274: 3184-3197, 2007. (Pubitemid 46849098)
4. Cardenas C, Miller RA, Smith I, Bui T, Molgo J, Muller M, Vais H, Cheung KH, Yang J, Parker I, Thompson CB, Birnbaum MJ, Hallows KR, and Foskett JK. Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2 + transfer to mitochondria. Cell 142: 270-283, 2010.
5. Cheong H, Lindsten T, Wu J, Lu C, and Thompson CB. Ammonia-induced autophagy is independent of ULK1/ULK2 kinases. Proc Natl Acad Sci USA 108: 11121-11126, 2011.
6. Cherra SJ, 3rd, Kulich SM, Uechi G, Balasubramani M, Mountzouris J, Day BW, and Chu CT. Regulation of the autophagy protein LC3 by phosphorylation. J Cell Biol 190: 533-539, 2010.
7. Copetti T, Bertoli C, Dalla E, Demarchi F, and Schneider C. p65/RelA modulates BECN1 transcription and autophagy. Mol Cell Biol 29: 2594-2608, 2009.
8. Criollo A, Maiuri MC, Tasdemir E, Vitale I, Fiebig AA, Andrews D, Molgo J, Diaz J, Lavandero S, Harper F, Pierron G, di Stefano D, Rizzuto R, Szabadkai G, and Kroemer G. Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Differ 14: 1029-1039, 2007. (Pubitemid 46629841)
9. Cuervo AM. Autophagy: Many paths to the same end. Mol Cell Biochem 263: 55-72, 2004. (Pubitemid 39256145)
10. Di Bartolomeo S, Corazzari M, Nazio F, Oliverio S, Lisi G, Antonioli M, Pagliarini V, Matteoni S, Fuoco C, Giunta L, D'Amelio M, Nardacci R, Romagnoli A, Piacentini M, Cecconi F, and Fimia GM. The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J Cell Biol 191: 155-168, 2010.
11. Duran A, Amanchy R, Linares JF, Joshi J, Abu-Baker S, Porollo A, Hansen M, Moscat J, and Diaz-Meco MT. p62 Iis a key regulator of nutrient sensing in the mTORC1 pathway. Mol Cell 44: 134-146, 2011.
12. Elgendy M, Sheridan C, Brumatti G, and Martin SJ. Oncogenic Ras-induced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival. Mol Cell 42: 23-35, 2011.
13. Filimonenko M, Stuffers S, Raiborg C, Yamamoto A, Malerod L, Fisher EM, Isaacs A, Brech A, Stenmark H, and Simonsen A. Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J Cell Biol 179: 485-500, 2007. (Pubitemid 350074792)
14. Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, Corazzari M, Fuoco C, Ucar A, Schwartz P, Gruss P, Piacentini M, Chowdhury K, and Cecconi F. Ambra1 regulates autophagy and development of the nervous system. Nature 447: 1121-125, 2007. (Pubitemid 47014434)
15. Ganley IG, Wong PM, Gammoh N, and Jiang X. Distinct autophagosomal- lysosomal fusion mechanism revealed by thapsigargin-induced autophagy arrest. Mol Cell 42: 731-743, 2011.
16. Geng J and Klionsky DJ. The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. 'Protein modifications: Beyond the usual suspects' review series. EMBO Rep 9: 859-864, 2008.
17. Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK, and Lippincott-Schwartz J. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141: 656-667, 2010.
18. Hamacher-Brady A, Brady NR, and Gottlieb RA. Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. J Biol Chem 281: 29776-29787, 2006. (Pubitemid 44536987)
19. Hamacher-Brady A, Brady NR, Logue SE, Sayen MR, Jinno M, Kirshenbaum LA, Gottlieb RA, and Gustafsson AB. Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ 14: 146-157, 2007. (Pubitemid 44911902)
20. Harr MW and Distelhorst CW. Apoptosis and autophagy: Decoding calcium signals that mediate life or death. Cold Spring Harb Perspect Biol 2: a005579, 2010.
21. He C and Levine B. The Beclin 1 interactome. Curr Opin Cell Biol 22: 140-149, 2010.
22. Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S, Natsume T, Takehana K, Yamada N, Guan JL, Oshiro N, and Mizushima N. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 20: 1981-1991, 2009.
23. Hoyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, Bianchi K, Fehrenbacher N, Elling F, Rizzuto R, Mathiasen IS, and Jaattela M. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol Cell 25: 193-205, 2007. (Pubitemid 46109606)
24. Hundeshagen P, Hamacher-Brady A, Eils R, and Brady NR. Concurrent detection of autolysosome formation and lysosomal degradation by flow cytometry in a high-content screen for inducers of autophagy. BMC Biol 9: 38, 2011.
25. Ichimura Y, Kumanomidou T, Sou YS, Mizushima T, Ezaki J, Ueno T, Kominami E, Yamane T, Tanaka K, and Komatsu M. Structural basis for sorting mechanism of p62 in selective autophagy. J Biol Chem 283: 22847-22857, 2008.
26. Itakura E, Kishi C, Inoue K, and Mizushima N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 19: 5360-5372, 2008.
27. Itakura E and Mizushima N. p62 Targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding. J Cell Biol 192: 17-27, 2011.
28. Iwata A, Riley BE, Johnston JA, and Kopito RR. HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 280: 40282-40292, 2005. (Pubitemid 41779165)
29. Jain A, Lamark T, Sjottem E, Larsen KB, Awuh JA, Overvatn A, McMahon M, Hayes JD, and Johansen T. p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J Biol Chem 285: 22576-22591, 2010.
30. Johansen T and Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 7: 279-296, 2011.
31. Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, Kundu M, and Kim DH. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 20: 1992-2003, 2009.
32. Kim J, Kundu M, Viollet B, and Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13: 132-141, 2011.
33. Klionsky DJ. Autophagy: From phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8: 931-937, 2007. (Pubitemid 47622558)
34. Korolchuk VI, Saiki S, Lichtenberg M, Siddiqi FH, Roberts EA, Imarisio S, Jahreiss L, Sarkar S, Futter M, Menzies FM, O'Kane CJ, Deretic V, and Rubinsztein DC. Lysosomal positioning coordinates cellular nutrient responses. Nat Cell Biol 13: 453-460, 2011.
35. Kouno T, Mizuguchi M, Tanida I, Ueno T, Kanematsu T, Mori Y, Shinoda H, Hirata M, Kominami E, and Kawano K. Solution structure of microtubule-associated protein light chain 3 and identification of its functional subdomains. J Biol Chem 280: 24610-24617, 2005. (Pubitemid 40934549)
36. Kristensen AR, Schandorff S, Hoyer-Hansen M, Nielsen MO, Jaattela M, Dengjel J, and Andersen JS. Ordered organelle degradation during starvation-induced autophagy. Mol Cell Proteom 7: 2419-2428, 2008.
37. Li H, Wang P, Sun Q, Ding WX, Yin XM, Sobol RW, Stolz DB, Yu J, and Zhang L. Following cytochrome c release, autophagy is inhibited during chemotherapy-induced apoptosis by caspase 8-mediated cleavage of Beclin 1. Cancer Res 71: 3625-3634, 2011.
38. Liang C, Lee JS, Inn KS, Gack MU, Li Q, Roberts EA, Vergne I, Deretic V, Feng P, Akazawa C, and Jung JU. Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 10: 776-787, 2008. (Pubitemid 351927707)
39. Luo S and Rubinsztein DC. Apoptosis blocks Beclin 1-dependent autophagosome synthesis: An effect rescued by Bcl-xL. Cell Death Differ 17: 268-277, 2010.
40. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, and Sandri M. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6: 458-471, 2007. (Pubitemid 350163055)
41. Mathew R, Karp CM, Beaudoin B, Vuong N, Chen G, Chen HY, Bray K, Reddy A, Bhanot G, Gelinas C, Dipaola RS, Karantza-Wadsworth V, and White E. Autophagy suppresses tumorigenesis through elimination of p62. Cell 137: 1062-1075, 2009.
42. Matsumoto G, Wada K, Okuno M, Kurosawa M, and Nukina N. Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Mol Cell 44: 279-289, 2011.
43. Matsunaga K, Saitoh T, Tabata K, Omori H, Satoh T, Kurotori N, Maejima I, Shirahama-Noda K, Ichimura T, Isobe T, Akira S, Noda T, and Yoshimori T. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 11: 385-396, 2009.
44. Mercer CA, Kaliappan A, and Dennis PB. A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 5: 649-662, 2009.
45. Nair U, Jotwani A, Geng J, Gammoh N, Richerson D, Yen WL, Griffith J, Nag S, Wang K, Moss T, Baba M, McNew JA, Jiang X, Reggiori F, Melia TJ, and Klionsky DJ. SNARE proteins are required for macroautophagy. Cell 146: 290-302, 2011.
46. Narita M, Young AR, Arakawa S, Samarajiwa SA, Nakashima T, Yoshida S, Hong S, Berry LS, Reichelt S, Ferreira M, Tavare S, Inoki K, and Shimizu S. Spatial coupling of mTOR and autophagy augments secretory phenotypes. Science 332: 966-970, 2011.
47. Noda T, Fujita N, and Yoshimori T. The late stages of autophagy: How does the end begin? Cell Death Differ 16: 984-990, 2009.
48. Novak I, Kirkin V, McEwan DG, Zhang J, Wild P, Rozenknop A, Rogov V, Lohr F, Popovic D, Occhipinti A, Reichert AS, Terzic J, Dotsch V, Ney PA, and Dikic I. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 11: 45-51, 2010.
49. Pankiv S, Alemu EA, Brech A, Bruun JA, Lamark T, Overvatn A, Bjorkoy G, and Johansen T. FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus enddirected vesicle transport. J Cell Biol 188: 253-269, 2010.
50. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, and Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282: 24131-24145, 2007. (Pubitemid 47328003)
51. Pena-Llopis S, Vega-Rubin-de-Celis S, Schwartz JC, Wolff NC, Tran TA, Zou L, Xie XJ, Corey DR, and Brugarolas J. Regulation of TFEB and V-ATPases by mTORC1. EMBO J 30: 3242-3258, 2011.
52. Proikas-Cezanne T, Ruckerbauer S, Stierhof YD, Berg C, and Nordheim A. Human WIPI-1 puncta-formation: A novel assay to assess mammalian autophagy. FEBS Lett 581: 3396-3404, 2007. (Pubitemid 47048184)
53. Ravikumar B, Moreau K, Jahreiss L, Puri C, and Rubinsztein DC. Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol 12: 747-757, 2010.
54. Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, Massey DC, Menzies FM, Moreau K, Narayanan U, Renna M, Siddiqi FH, Underwood BR, Winslow AR, and Rubinsztein DC. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 90: 1383-1435, 2010.
55. Razi M, Chan EY, and Tooze SA. Early endosomes and endosomal coatomer are required for autophagy. J Cell Biol 185: 305-321, 2009.
56. Renna M, Schaffner C, Winslow AR, Menzies FM, Peden AA, Floto RA, and Rubinsztein DC. Autophagic substrate clearance requires activity of the syntaxin-5 SNARE complex. J Cell Sci 124: 469-482, 2011.
57. Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, Cook LJ, and Rubinsztein DC. Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol 170: 1101-1111, 2005. (Pubitemid 41362642)
58. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, and Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26: 1749-1760, 2007. (Pubitemid 46624042)
59. Schweers RL, Zhang J, Randall MS, Loyd MR, Li W, Dorsey FC, Kundu M, Opferman JT, Cleveland JL, Miller JL, and Ney PA. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci USA 104: 19500-19505, 2007.
60. Sengupta A, Molkentin JD, and Yutzey KE. FoxO transcription factors promote autophagy in cardiomyocytes. J Biol Chem 284: 28319-28331, 2009.
61. Seo YK, Jeon TI, Chong HK, Biesinger J, Xie X, and Osborne TF. Genome-wide localization of SREBP-2 in hepatic chromatin predicts a role in autophagy. Cell Metab 13: 367-375, 2011.
62. Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, Sardiello M, Rubinsztein DC, and Ballabio A. TFEB links autophagy to lysosomal biogenesis. Science 332: 1429-1433, 2011.
63. Strappazzon F, Vietri-Rudan M, Campello S, Nazio F, Florenzano F, Fimia GM, Piacentini M, Levine B, and Cecconi F. Mitochondrial BCL-2 inhibits AMBRA1-induced autophagy. EMBO J 30: 1195-1208, 2011.
64. Stromhaug PE, Berg TO, Fengsrud M, and Seglen PO. Purification and characterization of autophagosomes from rat hepatocytes. Biochem J 335: 217-224, 1998. (Pubitemid 28491054)
65. Sun Q, Fan W, Chen K, Ding X, Chen S, and Zhong Q. Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA 105: 19211-19216, 2008.
66. Takahashi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y, Liang C, Jung JU, Cheng JQ, Mule JJ, Pledger WJ, and Wang HG. Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 9: 1142-1151, 2007. (Pubitemid 47500490)
67. Wei Y, Sinha S, and Levine B. Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 4: 949-951, 2008.
68. Weidberg H, Shpilka T, Shvets E, Abada A, Shimron F, and Elazar Z. LC3 and GATE-16 N termini mediate membrane fusion processes required for autophagosome biogenesis. Dev Cell 20: 444-454, 2011.
69. Weidberg H, Shvets E, Shpilka T, Shimron F, Shinder V, and Elazar Z. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J 29: 1792-1802, 2010.
70. Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR, Richter B, Korac J, Waidmann O, Choudhary C, Dotsch V, Bumann D, and Dikic I. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333: 228-233, 2011.
71. Williams A, Sarkar S, Cuddon P, Ttofi EK, Saiki S, Siddiqi FH, Jahreiss L, Fleming A, Pask D, Goldsmith P, O'Kane CJ, Floto RA, and Rubinsztein DC. Novel targets for Huntington's disease in an mTOR-independent autophagy pathway. Nat Chem Biol 4: 295-305, 2008. (Pubitemid 351550888)
72. Yu L, McPhee CK, Zheng L, Mardones GA, Rong Y, Peng J, Mi N, Zhao Y, Liu Z, Wan F, Hailey DW, Oorschot V, Klumperman J, Baehrecke EH, and Lenardo MJ. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 465: 942-946, 2010.
73. Zeng X and Kinsella TJ. Mammalian target of rapamycin and S6 kinase 1 positively regulate 6-thioguanine-induced autophagy. Cancer Res 68: 2384-2390, 2008. (Pubitemid 351521813)
74. Zeng X, Overmeyer JH, and Maltese WA. Functional specificity of the mammalian Beclin-Vps34 PI 3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J Cell Sci 119: 259-270, 2006. (Pubitemid 43210695)
75. Zhu Y, Zhao L, Liu L, Gao P, TianW,WangX, JinH,XuH, and Chen Q. Beclin 1 cleavage by caspase-3 inactivates autophagy and promotes apoptosis. Protein Cell 1: 468-477, 2010.