Autophagy in acute kidney injury

Kidney International

Volumn 89, Issue 4, 2016, Pages 779-791

  Kaushal, Gur P ^a,b   Shah, Sudhir V ^a,b  

^a CENTRAL ARKANSAS VETERANS HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

acute kidney injury; apoptosis; autophagy; cell death; cisplatin nephrotoxicity; ischemia reperfusion; mitophagy

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; BECLIN 1; CASPASE; CHLOROQUINE; CISPLATIN; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROTEIN BCL 2; PROTEIN P62; TAURINE; TEMSIROLIMUS; ANTINEOPLASTIC AGENT; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; TARGET OF RAPAMYCIN KINASE;

ACUTE KIDNEY FAILURE; APOPTOSIS; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CELL PROTECTION; CHAPERONE-MEDIATED AUTOPHAGY; ENDOPLASMIC RETICULUM STRESS; ENDOTOXEMIA; HUMAN; KIDNEY NECROSIS; LYSOSOME; MACROAUTOPHAGY; MICROAUTOPHAGY; MITOPHAGY; NECROPTOSIS; NEPHROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PEXOPHAGY; PRIORITY JOURNAL; RENAL PROTECTION; REPERFUSION INJURY; REVIEW; SEPSIS; ACUTE KIDNEY INJURY; ANIMAL; ANTAGONISTS AND INHIBITORS; COMPLICATION; METABOLISM;

ACUTE KIDNEY INJURY; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; CASPASES; CISPLATIN; HUMANS; LYSOSOMES; MULTIPROTEIN COMPLEXES; SEPSIS; TOR SERINE-THREONINE KINASES;

EID: 84964683444     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1016/j.kint.2015.11.021     Document Type: Review

References (188)

1. C. De Duve The lysosome Sci Am 208 1963 64 72
2. R.L. Deter, P. Baudhuin, and C. De Duve Participation of lysosomes in cellular autophagy induced in rat liver by glucagon J Cell Biol 35 1967 C11 C16
3. D.J. Klionsky Autophagy revisited: a conversation with Christian de Duve Autophagy 4 2008 740 743
4. Z. Yang, and D.J. Klionsky Mammalian autophagy: core molecular machinery and signaling regulation Curr Opin Cell Biol 22 2010 124 131
5. N. Mizushima, and M. Komatsu Autophagy: renovation of cells and tissues Cell 147 2011 728 741
6. Y. Feng, D. He, Z. Yao, and D.J. Klionsky The machinery of macroautophagy Cell Res 24 2014 24 41
7. G. Kroemer, G. Marino, and B. Levine Autophagy and the integrated stress response Mol Cell 40 2010 280 293
8. M. Kundu, and C.B. Thompson Autophagy: basic principles and relevance to disease Annu Rev Pathol 3 2008 427 455
9. D.C. Rubinsztein, P. Codogno, and B. Levine Autophagy modulation as a potential therapeutic target for diverse diseases Nat Rev Drug Discov 11 2012 709 730
10. R.C. Russell, H.X. Yuan, and K.L. Guan Autophagy regulation by nutrient signaling Cell Res 24 2014 42 45
11. R.A. Nixon The role of autophagy in neurodegenerative disease Nat Med 19 2013 983 997
12. M. Mari, J. Griffith, E. Rieter, and et al. An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis J Cell Biol 190 2010 1005 1022
13. W.L. Yen, T. Shintani, U. Nair, and et al. The conserved oligomeric Golgi complex is involved in double-membrane vesicle formation during autophagy J Cell Biol 188 2010 101 114
14. E.L. Axe, S.A. Walker, M. Manifava, and et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum J Cell Biol 182 2008 685 701
15. S.A. Tooze, H.B. Jefferies, E. Kalie, and et al. Trafficking and signaling in mammalian autophagy IUBMB Life 62 2010 503 508
16. L. Ge, and R. Schekman The ER-Golgi intermediate compartment feeds the phagophore membrane Autophagy 10 2014 170 172
17. S. Kaushik, and A.M. Cuervo Chaperone-mediated autophagy: a unique way to enter the lysosome world Trends Cell Biol 22 2012 407 417
18. S.A. Tooze, and T. Yoshimori The origin of the autophagosomal membrane Nat Cell Biol 12 2010 831 835
19. D.C. Rubinsztein, T. Shpilka, and Z. Elazar Mechanisms of autophagosome biogenesis Curr Biol 22 2012 R29 R34
20. C.A. Lamb, T. Yoshimori, and S.A. Tooze The autophagosome: origins unknown, biogenesis complex Nat Rev Mol Cell Biol 14 2013 759 774
21. N. Mizushima The role of the Atg1/ULK1 complex in autophagy regulation Curr Opin Cell Biol 22 2010 132 139
22. S. Wullschleger, R. Loewith, and M.N. Hall TOR signaling in growth and metabolism Cell 124 2006 471 484
23. C.H. Jung, C.B. Jun, S.H. Ro, and et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery Mol Biol Cell 20 2009 1992 2003
24. Y.C. Kim, and K.L. Guan mTOR: a pharmacologic target for autophagy regulation J Clin Invest 125 2015 25 32
25. S. Sengupta, T.R. Peterson, and D.M. Sabatini Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress Mol Cell 40 2010 310 322
26. J. Kim, M. Kundu, B. Viollet, and K.L. Guan AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1 Nat Cell Biol 13 2011 132 141
27. S. Alers, A.S. Löffler, S. Wesselborg, and B. Stork Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks Mol Cell Biol 32 2012 2 11
28. N. Hosokawa, T. Hara, T. Kaizuka, and et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy Mol Biol Cell 20 2009 1981 1991
29. T. Hara, A. Takamura, C. Kishi, and et al. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells J Cell Biol 181 2008 497 510
30. E.Y. Chan, A. Longatti, N.C. McKnight, and S.A. Tooze Kinase-inactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13-independent mechanism Mol Cell Biol 29 2009 157 171
31. E.A. Dunlop, and A.R. Tee mTOR and autophagy: a dynamic relationship governed by nutrients and energy Semin Cell Dev Biol 36 2014 121 129
32. R.C. Russell, Y. Tian, H. Yuan, and et al. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase Nat Cell Biol 15 2013 741 750
33. S. Di Bartolomeo, M. Corazzari, F. Nazio, and et al. The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy J Cell Biol 191 2010 155 168
34. I. Koyama-Honda, E. Itakura, T.K. Fujiwara, and N. Mizushima Temporal analysis of recruitment of mammalian ATG proteins to the autophagosome formation site Autophagy 9 2013 1491 1499
35. S.R. Carlsson, and A. Simonsen Membrane dynamics in autophagosome biogenesis J Cell Sci 128 2015 193 205
36. F. Reggiori, and S.A. Tooze Autophagy regulation through Atg9 traffic J Cell Biol 198 2012 151 153
37. C. Puri, M. Renna, C.F. Bento, and et al. ATG16L1 meets ATG9 in recycling endosomes: additional roles for the plasma membrane and endocytosis in autophagosome biogenesis Autophagy 10 2014 182 184
38. N. Mizushima, A. Kuma, Y. Kobayashi, and et al. Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate J Cell Sci 116 2003 1679 1688
39. J. Romanov, M. Walczak, I. Ibiricu, and et al. Mechanism and functions of membrane binding by the Atg5-Atg12/Atg16 complex during autophagosome formation EMBO J 31 2012 4304 4317
40. H.C. Dooley, M. Razi, H.E. Polson, and et al. WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1 Mol Cell 55 2014 238 252
41. H.C. Dooley, M.I. Wilson, and S.A. Tooze WIPI2B links PtdIns3P to LC3 lipidation through binding ATG16L1 Autophagy 11 2015 190 191
42. I. Vergne, and V. Deretic The role of PI3P phosphatases in the regulation of autophagy FEBS Lett 584 2010 1313 1318
43. M.G. Gutierrez, D.B. Munafó, W. Berón, and M.I. Colombo Rab7 is required for the normal progression of the autophagic pathway in mammalian cells J Cell Sci 117 2004 2687 2697
44. S. Jäger, C. Bucci, I. Tanida, and et al. Role for Rab7 in maturation of late autophagic vacuoles J Cell Sci 117 2004 4837 4848
45. B. Carroll, N. Mohd-Naim, F. Maximiano, and et al. The TBC/RabGAP Armus coordinates Rac1 and Rab7 functions during autophagy Dev Cell 25 2013 15 28
46. J. Diao, R. Liu, Y. Rong, and et al. ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes Nature 520 2015 563 566
47. S.R. Yoshii, and N. Mizushima Autophagy machinery in the context of mammalian mitophagy Biochim Biophys Acta 1853 2015 2797 2801
48. A. Stolz, A. Ernst, and I. Dikic Cargo recognition and trafficking in selective autophagy Nat Cell Biol 16 2014 495 501
49. K. Mizumura, A.M. Choi, and S.W. Ryter Emerging role of selective autophagy in human diseases Front Pharmacol 5 2014 1 8
50. A. Khaminets, T. Heinrich, M. Mari, and et al. Regulation of endoplasmic reticulum turnover by selective autophagy Nature 522 2015 354 358
51. G. Bjørkøy, T. Lamark, A. Brech, and et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death J Cell Biol 171 2005 603 614
52. S. Pankiv, T.H. Clausen, T. Lamark, and et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy J Biol Chem 282 2007 24131 24145
53. M. Komatsu, S. Waguri, M. Koike, and et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice Cell 131 2007 1149 1163
54. Y. Ichimura, T. Kumanomidou, Y.S. Sou, and et al. Structural basis for sorting mechanism of p62 in selective autophagy J Biol Chem 283 2008 22847 22857
55. Å.B. Birgisdottir, T. Lamark, and T. Johansen The LIR motif - crucial for selective autophagy J Cell Sci 126 2013 3237 3247
56. L.J. Stallons, J.A. Funk, and R.G. Schnellmann Mitochondrial homeostasis in acute organ failure Curr Pathobiol Rep 2013 2013 3
57. M. Zhan, C. Brooks, F. Liu, and et al. Mitochondrial dynamics: regulatory mechanisms and emerging role in renal pathophysiology Kidney Int 83 2013 568 581
58. S.M. Parikh, Y. Yang, L. He, and et al. Mitochondrial function and disturbances in the septic kidney Semin Nephrol 35 2015 108 119
59. D.R. Green, L. Galluzzi, and G. Kroemer Mitochondria and the autophagy-inflammation-cell death axis in organismal aging Science 333 2011 1109 1112
60. T. Kitada, S. Asakawa, N. Hattori, and et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism Nature 392 1998 605 608
61. E.M. Valente, P.M. Abou-Sleiman, V. Caputo, and et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1 Science 304 2004 1158 1160
62. A.M. Pickrell, and R.J. Youle The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson's disease Neuron 85 2015 257 273
63. R.J. Youle, and D.P. Narendra Mechanisms of mitophagy Nat Rev Mol Cell Biol 12 2011 9 14
64. F. Koyano, K. Okatsu, H. Kosako, and et al. Ubiquitin is phosphorylated by PINK1 to activate parkin Nature 510 2014 162 166
65. K. Okatsu, F. Koyano, M. Kimura, and et al. Phosphorylated ubiquitin chain is the genuine Parkin receptor J Cell Biol 209 2015 111 128
66. H. Wei, L. Liu, and Q. Chen Selective removal of mitochondria via mitophagy: distinct pathways for different mitochondrial stresses Biochim Biophys Acta S0167-4889 2015 00114 00117
67. Y.C. Wong, and E.L. Holzbaur Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation Proc Natl Acad Sci U S A 111 2014 E4439 E4448
68. I. Novak, V. Kirkin, D.G. McEwan, and et al. Nix is a selective autophagy receptor for mitochondrial clearance EMBO Rep 11 2010 45 51
69. H. Sandoval, P. Thiagarajan, S.K. Dasgupta, and et al. Essential role for Nix in autophagic maturation of erythroid cells Nature 454 2008 232 235
70. J. Zhang, and P.A. Ney Role of BNIP3 and NIX in cell death, autophagy, and mitophagy Cell Death Differ 16 2009 939 946
71. L. Liu, D. Feng, G. Chen, and et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells Nat Cell Biol 14 2012 177 185
72. M. Ishihara, M. Urushido, K. Hamada, and et al. Sestrin-2 and BNIP3 regulate autophagy and mitophagy in renal tubular cells in acute kidney injury Am J Physiol Renal Physiol 305 2013 F495 F509
73. Declèves AE, Sharma K, Satriano J. Beneficial effects of AMP-activated protein kinase agonists in kidney ischemia-reperfusion: autophagy and cellular stress markers [e-pub ahead of print]. Nephron Exp Nephrol. doi: 10.1159/000368932, accessed January 2, 2016.
74. J. Cui, S. Shi, X. Sun, and et al. Mitochondrial autophagy involving renal injury and aging is modulated by caloric intake in aged rat kidneys PLoS One 8 2013 e69720
75. R. Vasko, B.B. Ratliff, S. Bohr, and et al. Endothelial peroxisomal dysfunction and impaired pexophagy promotes oxidative damage in lipopolysaccharide-induced acute kidney injury Antioxid Redox Signal 19 2013 211 230
76. C.T. Chien, S.K. Shyue, and M.K. Lai Bcl-xL augmentation potentially reduces ischemia/reperfusion induced proximal and distal tubular apoptosis and autophagy Transplantation 84 2007 1183 1190
77. C. Suzuki, Y. Isaka, Y. Takabatake, and et al. Participation of autophagy in renal ischemia/reperfusion injury Biochem Biophys Res Commun 368 2008 100 106
78. Y. Isaka, C. Suzuki, T. Abe, and et al. Bcl-2 protects tubular epithelial cells from ischemia/reperfusion injury by dual mechanisms Transplant Proc 41 2009 52 54
79. M. Jiang, K. Liu, J. Luo, and Z. Dong Autophagy is a renoprotective mechanism during in vitro hypoxia and in vivo ischemia-reperfusion injury Am J Pathol 176 2010 1181 1192
80. K. Turkmen, J. Martin, A. Akcay, and et al. Apoptosis and autophagy in cold preservation ischemia Transplantation 91 2011 1192 1197
81. T. Kimura, Y. Takabatake, A. Takahashi, and et al. Autophagy protects the proximal tubule from degeneration and acute ischemic injury J Am Soc Nephrol 22 2011 902 913
82. Y.L. Zhang, J. Zhang, L.Y. Cui, and S. Yang Autophagy activation attenuates renal ischemia-reperfusion injury in rats Exp Biol Med (Maywood) 240 2015 1590 1598
83. N. Mizushima, T. Yoshimori, and B. Levine Methods in mammalian autophagy research Cell 140 2010 313 326
84. J. Lempiäinen, P. Finckenberg, E.E. Mervaala, and et al. Caloric restriction ameliorates kidney ischaemia/reperfusion injury through PGC-1α-eNOS pathway and enhanced autophagy Acta Physiol (Oxf) 208 2013 410 421
85. F. Grahammer, N. Haenisch, F. Steinhardt, and et al. mTORC1 maintains renal tubular homeostasis and is essential in response to ischemic stress Proc Natl Acad Sci U S A 111 2014 E2817 E2826
86. N. Wanner, B. Hartleben, N. Herbach, and et al. Unraveling the role of podocyte turnover in glomerular aging and injury J Am Soc Nephrol 25 2014 707 716
87. S. Nakagawa, K. Nishihara, K. Inui, and S. Masuda Involvement of autophagy in the pharmacological effects of the mTOR inhibitor everolimus in acute kidney injury Eur J Pharmacol 696 2012 143 154
88. W. Lieberthal, R. Fuhro, C.C. Andry, and et al. Rapamycin impairs recovery from acute renal failure: role of cell-cycle arrest and apoptosis of tubular cells Am J Physiol Renal Physiol 281 2001 F693 F706
89. W. Lieberthal, R. Fuhro, C.C. Andry, and et al. Rapamycin delays but does not prevent recovery from acute renal failure: role of acquired tubular resistance Transplantation 82 2006 17 22
90. C. Esposito, F. Grosjean, M. Torreggiani, and et al. Sirolimus prevents short-term renal changes induced by ischemia-reperfusion injury in rats Am J Nephrol 33 2011 239 249
91. L. Li, Z.V. Wang, J.A. Hill, and F. Lin New autophagy reporter mice reveal dynamics of proximal tubular autophagy J Am Soc Nephrol 25 2014 305 315
92. L.T. Wang, B.L. Chen, C.T. Wu, and et al. Protective role of AMP-activated protein kinase-evoked autophagy on an in vitro model of ischemia/reperfusion-induced renal tubular cell injury PLoS One 8 2013 e79814
93. B.L. Chen, L.T. Wang, K.H. Huang, and et al. Quercetin attenuates renal ischemia/reperfusion injury via an activation of AMP-activated protein kinase-regulated autophagy pathway J Nutr Biochem 25 2014 1226 1234
94. C. Yang, V. Kaushal, S.V. Shah, and G.P. Kaushal Autophagy is associated with apoptosis in cisplatin injury to renal tubular epithelial cells Am J Physiol Renal Physiol 294 2008 F777 F787
95. S. Periyasamy-Thandavan, M. Jiang, and et al. Autophagy is cytoprotective during cisplatin injury of renal proximal tubular cells Kidney Int 74 2008 631 640
96. K. Inoue, H. Kuwana, Y. Shimamura, and et al. Cisplatin-induced macroautophagy occurs prior to apoptosis in proximal tubules in vivo Clin Exp Nephrol 14 2010 112 122
97. S. Bolisetty, A.M. Traylor, J. Kim, and et al. Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury J Am Soc Nephrol 21 2010 1702 1712
98. C. Herzog, C. Yang, A. Holmes, and G.P. Kaushal z-VAD-fmk prevents cisplatin-induced cleavage of autophagy proteins but impairs autophagic flux and worsens renal function Am J Physiol Renal Physiol 303 2012 F1239 F1250
99. M. Jiang, Q. Wei, G. Dong, and et al. Autophagy in proximal tubules protects against acute kidney injury Kidney Int 82 2012 1271 1283
100. A. Takahashi, T. Kimura, Y. Takabatake, and et al. Autophagy guards against cisplatin-induced acute kidney injury Am J Pathol 180 2012 517 525
101. F. Rovetta, A. Stacchiotti, A. Consiglio, and et al. ER signaling regulation drives the switch between autophagy and apoptosis in NRK-52E cells exposed to cisplatin Exp Cell Res 318 2012 238 250
102. H.W. Hsiao, K. Tsai, L. Wang, and et al. The decline of autophagy contributes to proximal tubular dysfunction during sepsis Shock 37 2012 289 296
103. G.M. Howell, H. Gomez, R.D. Collage, and et al. Augmenting autophagy to treat acute kidney injury during endotoxemia in mice PLoS One 8 2013 e69520
104. D.A. Escobar, A.M. Botero-Quintero, B.C. Kautza, and et al. Adenosine monophosphate-activated protein kinase activation protects against sepsis-induced organ injury and inflammation J Surg Res 194 2015 262 272
105. X. Zhang, G.M. Howell, L. Guo, and et al. CaMKIV-dependent preservation of mTOR expression is required for autophagy during lipopolysaccharide-induced inflammation and acute kidney injury J Immunol 193 2014 2405 2415
106. Y. Chen, M.B. Azad, and S.B. Gibson Superoxide is the major reactive oxygen species regulating autophagy Cell Death Differ 16 2009 1040 1052
107. R. Scherz-Shouval, and Z. Elazar Regulation of autophagy by ROS: physiology and pathology Trends Biochem Sci 36 2011 30 38
108. Y. Wang, Y. Nartiss, B. Steipe, and et al. ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy Autophagy 8 2012 1462 1476
109. M. Peyrou, P.E. Hanna, and A.E. Cribb Cisplatin, gentamicin, and p-aminophenol induce markers of endoplasmic reticulum stress in the rat kidneys Toxicol Sci 99 2007 346 353
110. M. Kitamura Endoplasmic reticulum stress and unfolded protein response in renal pathophysiology: Janus faces Am J Physiol Renal Physiol 295 2008 F323 F334
111. T. Kawakami, R. Inagi, H. Takano, and et al. Endoplasmic reticulum stress induces autophagy in renal proximal tubular cells Nephrol Dial Transplant 24 2009 2665 2672
112. T. Yorimitsu, U. Nair, Z. Yang, and D.J. Klionsky Endoplasmic reticulum stress trigger autophagy J Biol Chem 281 2006 30299 30304
113. B.B. Chandrika, C. Yang, Y. Ou, and et al. Endoplasmic reticulum stress-induced autophagy provides cytoprotection from chemical hypoxia and oxidant injury and ameliorates renal ischemia-reperfusion injury PLoS One 10 2015 e0140025
114. W. Prachasilchai, H. Sonoda, N. Yokota-Ikeda, and et al. The protective effect of a newly developed molecular chaperone-inducer against mouse ischemic acute kidney injury J Pharmacol Sci 109 2009 311 314
115. W. Prachasilchai, H. Sonoda, N. Yokota-Ikeda, and et al. A protective role of unfolded protein response in mouse ischemic acute kidney injury Eur J Pharmacol 592 2008 138 145
116. M.J. Livingston, and Z. Dong Autophagy in acute kidney injury Semin Nephrol 34 2014 17 26
117. X.H. Liang, L.K. Kleeman, H.H. Jiang, and et al. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein J Virol 72 1998 8586 8596
118. S. Pattingre, A. Tassa, X. Qu, and et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy Cell 122 2005 927 939
119. S. Erlich, L. Mizrachy, O. Segev, and et al. Differential interactions between Beclin 1 and Bcl-2 family members Autophagy 3 2007 561 568
120. G. Robert, C. Gastaldi, A. Puissant, and et al. The anti-apoptotic Bcl-B protein inhibits BECN1-dependent autophagic cell death Autophagy 8 2012 637 649
121. I.A. Ciechomska, G.C. Goemans, J.N. Skepper, and A.M. Tolkovsky Bcl-2 complexed with Beclin-1 maintains full anti-apoptotic function Oncogene 28 2009 2128 2141
122. Y. Wei, S. Pattingre, S. Sinha, and et al. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy Mol Cell 30 2008 678 688
123. N.C. Chang, M. Nguyen, M. Germain, and G.C. Shore Antagonism of Beclin 1-dependent autophagy by BCL-2 at the endoplasmic reticulum requires NAF-1 EMBO J 29 2010 606 618
124. N.M. Mazure, and J. Pouysségur Atypical BH3-domains of BNIP3 and BNIP3L lead to autophagy in hypoxia Autophagy 5 2009 868 869
125. S. Malik, I. Orhon, E. Morselli, and et al. BH3 mimetics activate multiple pro-autophagic pathways Oncogene 30 2011 3918 3929
126. J.M. Pedro, Y. Wei, V. Sica, and et al. BAX and BAK1 are dispensable for ABT-737-induced dissociation of the BCL2-BECN1 complex and autophagy Autophagy 11 2015 452 459
127. J.O. Pyo, M.H. Jang, Y.K. Kwon, and et al. Essential roles of Atg5 and FADD in autophagic cell death: dissection of autophagic cell death into vacuole formation and cell death J Biol Chem 280 2005 20722 20729
128. B.D. Bell, S. Leverrier, B.M. Weist, and et al. FADD and caspase-8 control the outcome of autophagic signaling in proliferating T cells Proc Natl Acad Sci U S A 105 2008 16677 16682
129. M.A. Laussmann, E. Passante, H. Düssmann, and et al. Proteasome inhibition can induce an autophagy-dependent apical activation of caspase-8 Cell Death Differ 18 2011 1584 1597
130. M.M. Young, Y. Takahashi, O. Khan, and et al. Autophagosomal membrane serves as platform for intracellular death-inducing signaling complex (iDISC)-mediated caspase-8 activation and apoptosis J Biol Chem 287 2012 12455 12468
131. Z. Jin, Y. Li, R. Pitti, and et al. Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling Cell 137 2009 721 735
132. G.P. Kaushal, V. Kaushal, C. Herzog, and C.A. Yang Autophagy delays apoptosis in renal tubular epithelial cells in cisplatin cytotoxicity Autophagy 4 2008 710 712
133. D.H. Cho, Y.K. Jo, J.J. Hwang, and et al. Caspase-mediated cleavage of ATG6/Beclin-1 links apoptosis to autophagy in HeLa cells Cancer Lett 274 2009 95 100
134. S. Luo, and D.C. Rubinsztein Apoptosis blocks Beclin 1-dependent autophagosome synthesis: an effect rescued by Bcl-xL Cell Death Differ 17 2010 268 277
135. Y. Zhu, L. Zhao, L. Liu, and et al. Beclin 1 cleavage by caspase-3 inactivates autophagy and promotes apoptosis Protein Cell 1 2010 468 477
136. M. You, N. Savaraj, M.T. Kuo, and et al. TRAIL induces autophagic protein cleavage through caspase activation in melanoma cell lines under arginine deprivation Mol Cell Biochem 374 2012 181 190
137. E. Wirawan, L. Vande Walle, K. Kersse, and et al. Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria Cell Death Dis 1 2010 e18
138. O. Oral, D. Oz-Arslan, Z. Itah, and et al. Cleavage of Atg3 protein by caspase-8 regulates autophagy during receptor-activated cell death Apoptosis 17 2012 810 820
139. V.M. Betin, and J.D. Lane Caspase cleavage of Atg4D stimulates GABARAP-L1 processing and triggers mitochondrial targeting and apoptosis J Cell Sci 122 2009 2554 2566
140. K.G. Lassen, P. Kuballa, K.L. Conway, and et al. Atg16L1 T300A variant decreases selective autophagy resulting in altered cytokine signaling and decreased antibacterial defense Proc Natl Acad Sci U S A 111 2014 7741 7746
141. V. Pagliarini, E. Wirawan, A. Romagnoli, and et al. Proteolysis of Ambra1 during apoptosis has a role in the inhibition of the autophagic pro-survival response Cell Death Differ 19 2012 1495 1504
142. D. Vercammen, R. Beyaert, G. Denecker, and et al. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor J Exp Med 187 1998 1477 1485
143. N. Holler, R. Zaru, O. Micheau, and et al. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule Nat Immunol 1 2000 489 495
144. W.J. Kaiser, J.W. Upton, A.B. Long, and et al. RIP3 mediates the embryonic lethality of caspase-8-deficient mice Nature 471 2011 368 372
145. A. Oberst, C.P. Dillon, R. Weinlich, and et al. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis Nature 471 2011 363 367
146. C.A. Wilson, and J.L. Browning Death of HT29 adenocarcinoma cells induced by TNF family receptor activation is caspase-independent and displays features of both apoptosis and necrosis Cell Death Differ 9 2002 1321 1333
147. T. Tenev, K. Bianchi, M. Darding, and et al. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs Mol Cell 43 2011 432 448
148. M. Feoktistova, P. Geserick, B. Kellert, and et al. cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms Mol Cell 43 2011 449 463
149. W.J. Kaiser, H. Sridharan, C. Huang, and et al. Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL J Biol Chem 288 2013 31268 31279
150. S. He, Y. Liang, F. Shao, and X. Wang Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway Proc Natl Acad Sci U S A 108 2011 20054 20059
151. R.J. Thapa, S. Nogusa, P. Chen, and et al. Interferon-induced RIP1/RIP3-mediated necrosis requires PKR and is licensed by FADD and caspases Proc Natl Acad Sci U S A 110 2013 E3109 E3118
152. R. Shindo, H. Kakehashi, K. Okumura, and et al. Critical contribution of oxidative stress to TNFα-induced necroptosis downstream of RIPK1 activation Biochem Biophys Res Commun 436 2013 212 216
153. C.W. Davis, B.J. Hawkins, S. Ramasamy, and et al. Nitration of the mitochondrial complex I subunit NDUFB8 elicits RIP1- and RIP3-mediated necrosis Free Radic Biol Med 48 2010 306 317
154. H. Sridharan, and J.W. Upton Programmed necrosis in microbial pathogenesis Trends Microbiol 22 2014 199 207
155. O. Micheau, and J. Tschopp Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes Cell 114 2003 181 190
156. M.A. O'Donnell, D. Legarda-Addison, P. Skountzos, and et al. Ubiquitination of RIP1 regulates an NF-kappaB-independent cell-death switch in TNF signaling Curr Biol 17 2007 418 424
157. J.E. Vince, W.W. Wong, N. Khan, and et al. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis Cell 131 2007 682 693
158. S.C. Sun CYLD: a tumor suppressor deubiquitinase regulating NF-kappaB activation and diverse biological processes Cell Death Differ 17 2010 25 34
159. L. Wang, F. Du, and X. Wang TNF-alpha induces two distinct caspase-8 activation pathways Cell 133 2008 693 703
160. S. He, L. Wang, L. Miao, and et al. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha Cell 137 2009 1100 1111
161. Y.S. Cho, S. Challa, D. Moquin, and et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation Cell 137 2009 1112 1123
162. D.W. Zhang, J. Shao, J. Lin, and et al. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis Science 325 2009 332 336
163. Y. Lin, A. Devin, Y. Rodriguez, and Z.G. Liu Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis Genes Dev 13 1999 2514 2526
164. S. Feng, Y. Yang, Y. Mei, and et al. Cleavage of RIP3 inactivates its caspase-independent apoptosis pathway by removal of kinase domain Cell Signal 19 2007 2056 2067
165. M.A. O'Donnell, E. Perez-Jimenez, A. Oberst, and et al. Caspase 8 inhibits programmed necrosis by processing CYLD Nat Cell Biol 13 2011 1437 1442
166. L. Sun, H. Wang, Z. Wang, and et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase Cell 148 2012 213 227
167. Y. Dondelinger, W. Declercq, S. Montessuit, and et al. MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates Cell Rep 7 2014 971 981
168. H. Wang, L. Sun, L. Su, and et al. Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3 Mol Cell 54 2014 133 146
169. X. Chen, W. Li, J. Ren, and et al. Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death Cell Res 24 2014 105 121
170. Z. Cai, S. Jitkaew, J. Zhao, and et al. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis Nat Cell Biol 16 2014 55 65
171. A. Linkermann, J.H. Bräsen, N. Himmerkus, and et al. Rip1 (receptor-interacting protein kinase 1) mediates necroptosis and contributes to renal ischemia/reperfusion injury Kidney Int 81 2012 751 761
172. Y. Xu, H. Ma, J. Shao, and et al. A role for tubular necroptosis in cisplatin-induced AKI J Am Soc Nephrol 26 2015 2647 2658
173. A. Linkermann, J.O. Heller, A. Prókai, and et al. The RIP1-kinase inhibitor necrostatin-1 prevents osmotic nephrosis and contrast-induced AKI in mice J Am Soc Nephrol 24 2013 1545 1557
174. P. Sridevi, M.K. Nhiayi, and J.Y. Wang Genetic disruption of Abl nuclear import reduces renal apoptosis in a mouse model of cisplatin-induced nephrotoxicity Cell Death Differ 20 2013 953 962
175. L. Yu, A. Alva, H. Su, and et al. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8 Science 304 2004 1500 1502
176. L. Bonapace, B.C. Bornhauser, M. Schmitz, and et al. Induction of autophagy-dependent necroptosis is required for childhood acute lymphoblastic leukemia cells to overcome glucocorticoid resistance J Clin Invest 120 2010 1310 1323
177. Y.T. Wu, H.L. Tan, Q. Huang, and et al. Autophagy plays a protective role during zVAD-induced necrotic cell death Autophagy 4 2008 457 466
178. M. Khan, M. Rizwan Alam, M. Waldeck-Weiermair, and et al. Inhibition of autophagy rescues palmitic acid-induced necroptosis of endothelial cells J Biol Chem 287 2012 21110 21120
179. Y.Q. Wang, L. Wang, M.Y. Zhang, and et al. Necrostatin-1 suppresses autophagy and apoptosis in mice traumatic brain injury model Neurochem Res 37 2012 1849 1858
180. B. Loos, A.M. Engelbrecht, R.A. Lockshin, and et al. The variability of autophagy and cell death susceptibility: Unanswered questions Autophagy 9 2013 1270 1285
181. J.J. Lemasters The mitochondrial permeability transition: from biochemical curiosity to pathophysiological mechanism Gastroenterology 115 1998 783 786
182. S. Jin, R.S. DiPaola, R. Mathew, and E. White Metabolic catastrophe as a means to cancer cell death J Cell Sci 120 2007 379 383
183. X. Liang, Y. Chen, L. Zhang, and et al. Necroptosis, a novel form of caspase-independent cell death, contributes to renal epithelial cell damage in an ATP-depleted renal ischemia model Mol Med Rep 10 2014 719 724
184. R.K. Amaravadi, and C.B. Thompson The roles of therapy-induced autophagy and necrosis in cancer treatment Clin Cancer Res 13 2007 7271 7279
185. Y.T. Wu, H.L. Tan, Q. Huang, and et al. Activation of the PI3K-Akt-mTOR signaling pathway promotes necrotic cell death via suppression of autophagy Autophagy 5 2009 824 834
186. Y. Matsuzawa, S. Oshima, Y. Nibe, and et al. RIPK3 regulates p62-LC3 complex formation via the caspase-8-dependent cleavage of p62 Biochem Biophys Res Commun 456 2015 298 304
187. J.S. Lee, Q. Li, J.Y. Lee, and et al. FLIP-mediated autophagy regulation in cell death control Nat Cell Biol 11 2009 1355 1362
188. M.X. He, and Y.W. He CFLAR/c-FLIPL: a star in the autophagy, apoptosis and necroptosis alliance Autophagy 9 2013 791 793