Autophagy induced during apoptosis degrades mitochondria and inhibits type i interferon secretion

Cell Death and Differentiation

Volumn 25, Issue 4, 2018, Pages 782-794

  Lindqvist, Lisa M ^a,b   Frank, Daniel ^a,b   McArthur, Kate ^a,b,c   Dite, Toby A ^b   Lazarou, Michael ^c   Oakhill, Jonathan S ^b   Kile, Benjamin T ^a,b,c   Vaux, David L ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; APOPTOSOME; AUTOPHAGY RELATED PROTEIN 5; AUTOPHAGY RELATED PROTEIN 7; BETA INTERFERON; BH3 PROTEIN; CASPASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INTERFERON; INTERLEUKIN 6; PROTEIN BAK; PROTEIN BAX; SERINE THREONINE PROTEIN KINASE ULK1; APOPTOSIS REGULATORY PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DAMAGE; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EMBRYO; ENZYME ACTIVATION; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; INTERFERON TYPE I; MICE; MICE, KNOCKOUT; MITOCHONDRIA;

EID: 85037705823     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/s41418-017-0017-z     Document Type: Article

References (60)

1. Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition. Autophagy. 2016;12:1-222.
2. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, et al. Phosphorylation of ULK1 (hATG1) by AMPactivated protein kinase connects energy sensing to mitophagy. Science. 2011;331:456-61.
3. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13:132-41.
4. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell. 2008;30:214-26.
5. Nguyen TN, Padman BS, Usher J, Oorschot V, Ramm G, Lazarou M. Atg8 family LC3/GABARAP proteins are crucial for autophagosome-lysosome fusion but not autophagosome formation during PINK1/Parkin mitophagy and starvation. J Cell Biol. 2016;215:857-74.
6. Abeliovich H, Dunn WA Jr., Kim J, Klionsky DJ. Dissection of autophagosome biogenesis into distinct nucleation and expansion steps. J Cell Biol. 2000;151:1025-34.
7. Nakatogawa H, Ichimura Y, Ohsumi Y. Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell. 2007;130:165-78.
8. Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, et al. A protein conjugation system essential for autophagy. Nature. 1998;395:395-8.
9. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell. 2010;140:313-26.
10. Klionsky DJ, Elazar Z, Seglen PO, Rubinsztein DC. Does bafilomycin A1 block the fusion of autophagosomes with lysosomes Autophagy. 2008;4:849-50.
11. Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol. 2008;183:795-803.
12. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010;8:e1000298.
13. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, Kim J, et al. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci USA. 2010;107:378-83.
14. Lazarou M, Sliter DA, Kane LA, Sarraf SA, Wang C, Burman JL, et al. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature. 2015;524:309-14.
15. Lalaoui N, Lindqvist LM, Sandow JJ, Ekert PG. The molecular relationships between apoptosis, autophagy and necroptosis. Semin Cell Dev Biol. 2015;39:63-9.
16. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, et al. Proapoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science. 2001;292:727-30.
17. Kotschy A, Szlavik Z, Murray J, Davidson J, Maragno AL, Le Toumelin-Braizat G, et al. The MCL1 inhibitor S63845 is tolerable and effective in diverse cancer models. Nature. 2016;538:477-82.
18. van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, Czabotar PE, et al. The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell. 2006;10:389-99.
19. Lindqvist LM, Simon AK, Baehrecke EH. Current questions and possible controversies in autophagy. Cell Death Discov. 2015;1. 10.1038/cddiscovery.2015.36.
20. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005;122:927-39.
21. Pedro JM, Wei Y, Sica V, Maiuri MC, Zou Z, Kroemer G, et al. BAX and BAK1 are dispensable for ABT-737-induced dissociation of the BCL2-BECN1 complex and autophagy. Autophagy. 2015;11:452-9.
22. Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell. 2008;30:678-88.
23. Maiuri MC, Criollo A, Tasdemir E, Vicencio JM, Tajeddine N, Hickman JA, et al. BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X(L). Autophagy. 2007;3:374-6.
24. Liang XH, Kleeman LK, Jiang HH, Gordon G, Goldman JE, Berry G, et al. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J Virol. 1998;72:8586-96.
25. Lindqvist LM, Heinlein M, Huang DC, Vaux DL. Prosurvival Bcl-2 family members affect autophagy only indirectly, by inhibiting Bax and Bak. Proc Natl Acad Sci USA. 2014;111:8512-7.
26. Reljic B, Conos S, Lee EF, Garnier JM, Dong L, Lessene G, et al. BAX-BAK1-independent LC3B lipidation by BH3 mimetics is unrelated to BH3 mimetic activity and has only minimal effects on autophagic flux. Autophagy. 2016;12:1083-93.
27. Lindqvist LM, Vaux DL. BCL2 and related prosurvival proteins require BAK1 and BAX to affect autophagy. Autophagy. 2014;10:1474-5.
28. Yee KS, Wilkinson S, James J, Ryan KM, Vousden KH. PUMAand Bax-induced autophagy contributes to apoptosis. Cell Death Differ. 2009;16:1135-45.
29. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA, et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature. 2005;435:677-81.
30. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012;149:274-93.
31. Katayama H, Kogure T, Mizushima N, Yoshimori T, Miyawaki A. A sensitive and quantitative technique for detecting autophagic events based on lysosomal delivery. Chem Biol. 2011;18:1042-52.
32. White MJ, McArthur K, Metcalf D, Lane RM, Cambier JC, Herold MJ, et al. Apoptotic Caspases Suppress mtDNA-Induced STINGMediated Type I IFN Production. Cell. 2014;159:1549-62.
33. Rongvaux A, Jackson R, Harman CC, Li T, West AP, de Zoete MR, et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell. 2014;159:1563-77.
34. Cai X, Chiu YH, Chen ZJ. The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling. Mol Cell. 2014;54:289-96.
35. Saitoh T, Fujita N, Hayashi T, Takahara K, Satoh T, Lee H, et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc Natl Acad Sci USA. 2009;106:20842-6.
36. Jounai N, Takeshita F, Kobiyama K, Sawano A, Miyawaki A, Xin KQ, et al. The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc Natl Acad Sci USA. 2007;104:14050-5.
37. Tal MC, Sasai M, Lee HK, Yordy B, Shadel GS, Iwasaki A. Absence of autophagy results in reactive oxygen speciesdependent amplification of RLR signaling. Proc Natl Acad Sci USA. 2009;106:2770-5.
38. Ge L, Melville D, Zhang M, Schekman R. The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. Elife. 2013;2:e00947.
39. Bernardini JP, Lazarou M, Dewson G. Parkin and mitophagy in cancer. Oncogene. 2016;36:1315-27.
40. Rogov V, Dotsch V, Johansen T, Kirkin V. Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol Cell. 2014;53:167-78.
41. Colell A, Ricci JE, Tait S, Milasta S, Maurer U, Bouchier-Hayes L, et al. GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation. Cell. 2007;129:983-97.
42. Ichim G, Lopez J, Ahmed SU, Muthalagu N, Giampazolias E, Delgado ME, et al. Limited mitochondrial permeabilization causes DNA damage and genomic instability in the absence of cell death. Mol Cell. 2015;57:860-72.
43. Mortensen M, Ferguson DJ, Edelmann M, Kessler B, Morten KJ, Komatsu M, et al. Loss of autophagy in erythroid cells leads to defective removal of mitochondria and severe anemia in vivo. Proc Natl Acad Sci USA. 2010;107:832-7.
44. Pua HH, Guo J, Komatsu M, He YW. Autophagy is essential for mitochondrial clearance in mature T lymphocytes. J Immunol. 2009;182:4046-55.
45. Mortensen M, Soilleux EJ, Djordjevic G, Tripp R, Lutteropp M, Sadighi-Akha E, et al. The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance. J Exp Med. 2011;208:455-67.
46. Orelio C, Dzierzak E. Bcl-2 expression and apoptosis in the regulation of hematopoietic stem cells. Leuk Lymphoma. 2007;48:16-24.
47. Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity. 2006;25:373-81.
48. De Leo MG, Staiano L, Vicinanza M, Luciani A, Carissimo A, Mutarelli M, et al. Autophagosome-lysosome fusion triggers a lysosomal response mediated by TLR9 and controlled by OCRL. Nat Cell Biol. 2016;18:839-50.
49. Lindqvist LM. Can the cargo control the car Mitochondrial DNA as a stimulator of TLR9-mediated autophagosome-lysosome fusion. Cell Death Differ. 2016;23:1737-8.
50. Schulz O, Diebold SS, Chen M, Naslund TI, Nolte MA, Alexopoulou L, et al. Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature. 2005;433:887-92.
51. Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI, et al. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 2005;19:1294-305.
52. Marsden VS, O'Connor L, O'Reilly LA, Silke J, Metcalf D, Ekert PG, et al. Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome c/Apaf-1/caspase-9 apoptosome. Nature. 2002;419:634-7.
53. Dite TA, Ling NXY, Scott JW, Hoque A, Galic S, Parker BL, et al. The autophagy initiator ULK1 sensitizes AMPK to allosteric drugs. Nat Commun. 2017;8:571.
54. N'Diaye EN, Kajihara KK, Hsieh I, Morisaki H, Debnath J, Brown EJ. PLIC proteins or ubiquilins regulate autophagydependent cell survival during nutrient starvation. EMBO Rep. 2009;10:173-9.
55. Yamano K, Fogel AI, Wang C, van der Bliek AM, Youle RJ. Mitochondrial Rab GAPs govern autophagosome biogenesis during mitophagy. Elife. 2014;3:e01612.
56. Sanjana NE, Shalem O, Zhang F. Improved vectors and genomewide libraries for CRISPR screening. Nat Methods. 2014;11:783-4.
57. Aubrey BJ, Kelly GL, Kueh AJ, Brennan MS, O'Connor L, Milla L, et al. An inducible lentiviral guide RNA platform enables the identification of tumor-essential genes and tumor-promoting mutations in vivo. Cell Rep. 2015;10:1422-32.
58. Scott JW, Galic S, Graham KL, Foitzik R, Ling NX, Dite TA, et al. Inhibition of AMP-activated protein kinase at the allosteric drug-binding site promotes islet insulin release. Chem Biol. 2015;22:705-11.
59. Fung C, Lock R, Gao S, Salas E, Debnath J. Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol Biol Cell. 2008;19:797-806.
60. Iyer S, Bell F, Westphal D, Anwari K, Gulbis J, Smith BJ, et al. Bak apoptotic pores involve a flexible C-terminal region and juxtaposition of the C-terminal transmembrane domains. Cell Death Differ. 2015;22:1665-75.