TNF-induced necroptosis initiates early autophagy events via RIPK3-dependent AMPK activation, but inhibits late autophagy

References

• Mercer TJ, Gubas A, Tooze SA. A molecular perspective of mammalian autophagosome biogenesis. J Biol Chem. 2018 Apr 13;293(15):5386–5395.
   PubMed Web of Science ®Google Scholar
• Hawley SA, Boudeau J, Reid JL, et al. Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J Biol. 2003;2(4):28.
   PubMedGoogle Scholar
• Shaw RJ, Kosmatka M, Bardeesy N, et al. The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci U S A. 2004 Mar 9;101(10):3329–3335.
   PubMed Web of Science ®Google Scholar
• Woods A, Johnstone SR, Dickerson K, et al. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol. 2003 Nov 11;13(22):2004–2008.
   PubMed Web of Science ®Google Scholar
• Alers S, Löffler AS, Wesselborg S, et al. Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol. 2012 Jan;32(1):2–11.
   PubMed Web of Science ®Google Scholar
• Zhao M, Klionsky DJ. AMPK-dependent phosphorylation of ULK1 induces autophagy. Cell Metab. 2011 Feb 2;13(2):119–120.
   PubMed Web of Science ®Google Scholar
• Hindupur SK, Gonzalez A, Hall MN. The opposing actions of target of rapamycin and AMP-activated protein kinase in cell growth control. Cold Spring Harb Perspect Biol. 2015 Aug 3;7(8):a019141.
   PubMed Web of Science ®Google Scholar
• Kim J, Kundu M, Viollet B, et al. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011 Feb;13(2):132–141.
   PubMed Web of Science ®Google Scholar
• Bach M, Larance M, James DE, et al. The serine/threonine kinase ULK1 is a target of multiple phosphorylation events. Biochem J. 2011 Dec 1;440(2):283–291.
   PubMed Web of Science ®Google Scholar
• Egan DF, Shackelford DB, Mihaylova MM, et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science. 2011 Jan 28;331(6016):456–461.
   PubMed Web of Science ®Google Scholar
• Mack HI, Zheng B, Asara JM, et al. AMPK-dependent phosphorylation of ULK1 regulates ATG9 localization [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. Autophagy. 2012 Aug;8(8):1197–1214.
   PubMed Web of Science ®Google Scholar
• Shang L, Chen S, Du F, et al. Nutrient starvation elicits an acute autophagic response mediated by Ulk1 dephosphorylation and its subsequent dissociation from AMPK. Proc Natl Acad Sci U S A. 2011 Mar 22;108(12):4788–4793.
   PubMed Web of Science ®Google Scholar
• Mizushima N. A brief history of autophagy from cell biology to physiology and disease. Nat Cell Biol. 2018 May;20(5):521–527.
   PubMed Web of Science ®Google Scholar
• Hurley JH, Young LN. Mechanisms of autophagy initiation. Annu Rev Biochem. 2017 Jun 20;86(86):225–244.
   PubMedGoogle Scholar
• Egan DF, Chun MG, Vamos M, et al. Small molecule inhibition of the autophagy kinase ULK1 and identification of ULK1 substrates. Mol Cell. 2015 Jul 16;59(2):285–297.
   PubMed Web of Science ®Google Scholar
• Kim J, Kim YC, Fang C, et al. Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy [Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S. Research Support, U.S. Gov’t, P.H.S.]. Cell. 2013 Jan 17;152(1–2):290–303.
   PubMed Web of Science ®Google Scholar
• Ma X, Zhang S, He L, et al. MTORC1-mediated NRBF2 phosphorylation functions as a switch for the class III PtdIns3K and autophagy. Autophagy. 2017 Mar 4;13(3):592–607.
   PubMed Web of Science ®Google Scholar
• Park JM, Jung CH, Seo M, et al. The ULK1 complex mediates MTORC1 signaling to the autophagy initiation machinery via binding and phosphorylating ATG14. Autophagy. 2016 Mar 3;12(3):547–564.
   PubMed Web of Science ®Google Scholar
• Russell RC, Tian Y, Yuan H, et al. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase [Research Support, N.I.H., extramural research support, Non-U.S. Gov’t research support, U.S. Gov’t, Non-P.H.S.]. Nat Cell Biol. 2013 Jul;15(7):741–750.
   PubMed Web of Science ®Google Scholar
• Axe EL, Walker SA, Manifava M, et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol. 2008 Aug 25;182(4):685–701.
   PubMed Web of Science ®Google Scholar
• Hayashi-Nishino M, Fujita N, Noda T, et al. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol. 2009 Dec;11(12):1433–1437.
   PubMed Web of Science ®Google Scholar
• Uemura T, Yamamoto M, Kametaka A, et al. A cluster of thin tubular structures mediates transformation of the endoplasmic reticulum to autophagic isolation membrane. Mol Cell Biol. 2014 May;34(9):1695–1706.
   PubMed Web of Science ®Google Scholar
• Yla-Anttila P, Vihinen H, Jokitalo E, et al. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy. 2009 Nov;5(8):1180–1185.
   PubMed Web of Science ®Google Scholar
• Hawley SA, Pan DA, Mustard KJ, et al. Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab. 2005 Jul;2(1):9–19.
   PubMed Web of Science ®Google Scholar
• Hurley RL, Anderson KA, Franzone JM, et al. The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J Biol Chem. 2005 Aug 12;280(32):29060–29066.
   PubMed Web of Science ®Google Scholar
• Momcilovic M, Hong SP, Carlson M. Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro. J Biol Chem. 2006 Sep 1;281(35):25336–25343.
   PubMed Web of Science ®Google Scholar
• Woods A, Dickerson K, Heath R, et al. Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab. 2005 Jul;2(1):21–33.
   PubMed Web of Science ®Google Scholar
• Herzig S, Shaw RJ. AMPK: guardian of metabolism and mitochondrial homeostasis [Review]. Nat Rev Mol Cell Biol. 2018 Feb;19(2):121–135.
   PubMed Web of Science ®Google Scholar
• Dalle Pezze P, Ruf S, Sonntag AG, et al. A systems study reveals concurrent activation of AMPK and mTOR by amino acids. Nat Commun. 2016 Nov 21;7(7):13254.
   PubMedGoogle Scholar
• Galluzzi L, Vitale I, Aaronson SA, et al. Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018 [Review]. Cell Death Differ. 2018 Mar;25(3):486–541.
   PubMed Web of Science ®Google Scholar
• Annibaldi A, Meier P. Checkpoints in TNF-induced cell death: implications in inflammation and cancer [Review]. Trends Mol Med. 2018 Jan;24(1):49–65.
   PubMed Web of Science ®Google Scholar
• Grootjans S, Vanden Berghe T, Vandenabeele P. Initiation and execution mechanisms of necroptosis: an overview [Review]. Cell Death Differ. 2017 Jul;24(7):1184–1195.
   PubMed Web of Science ®Google Scholar
• Feng S, Yang Y, Mei Y, et al. Cleavage of RIP3 inactivates its caspase-independent apoptosis pathway by removal of kinase domain. Cell Signal. 2007 Oct;19(10):2056–2067.
   PubMed Web of Science ®Google Scholar
• Lin Y, Devin A, Rodriguez Y, et al. Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev. 1999 Oct 1;13(19):2514–2526.
   PubMed Web of Science ®Google Scholar
• Oberst A, Dillon CP, Weinlich R, et al. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature. 2011 Mar 17;471(7338):363–367.
   PubMed Web of Science ®Google Scholar
• Cho YS, Challa S, Moquin D, et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell. 2009 Jun 12;137(6):1112–1123.
   PubMed Web of Science ®Google Scholar
• He S, Wang L, Miao L, et al. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell. 2009 Jun 12;137(6):1100–1111.
   PubMed Web of Science ®Google Scholar
• Vandenabeele P, Vanden Berghe T, Festjens N. Caspase inhibitors promote alternative cell death pathways [Review]. Sci STKE. 2006 Oct 24;2006(358):pe44.
   Google Scholar
• Sun L, Wang H, Wang Z, et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell. 2012 Jan 20;148(1–2):213–227.
   PubMed Web of Science ®Google Scholar
• Mandal P, Berger SB, Pillay S, et al. RIP3 induces apoptosis independent of pronecrotic kinase activity [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. Mol Cell. 2014 Nov 20;56(4):481–495.
   PubMed Web of Science ®Google Scholar
• Chauhan S, Mandell MA, Deretic V. IRGM governs the core autophagy machinery to conduct antimicrobial defense. Mol Cell. 2015 May 7;58(3):507–521.
   PubMed Web of Science ®Google Scholar
• Tian W, Li W, Chen Y, et al. Phosphorylation of ULK1 by AMPK regulates translocation of ULK1 to mitochondria and mitophagy. FEBS Lett. 2015 Jul 8;589(15):1847–1854.
   PubMed Web of Science ®Google Scholar
• Le DT, Jung S, Quynh NTN, et al. Inhibitory role of AMPactivated protein kinase in necroptosis of HCT116 colon cancer cells with p53 null mutation under nutrient starvation. Int J Oncol. 2019 Feb;54(2):702–712.
   PubMed Web of Science ®Google Scholar
• Wang YS, Yu P, Wang Y, et al. AMP-activated protein kinase protects against necroptosis via regulation of Keap1-PGAM5 complex. Int J Cardiol. 2018 May 15;259:153–162.
   PubMed Web of Science ®Google Scholar
• Wu W, Wang X, Berleth N, et al. The Autophagy-Initiating Kinase ULK1 controls RIPK1-mediated cell death. Cell Rep. 2020 Apr 21;31(3):107547.
   PubMed Web of Science ®Google Scholar
• Hieke N, Löffler AS, Kaizuka T, et al. Expression of a ULK1/2 binding-deficient ATG13 variant can partially restore autophagic activity in ATG13-deficient cells. Autophagy. 2015;11(9):1471–1483.
   PubMed Web of Science ®Google Scholar
• Hosokawa N, Hara T, Kaizuka T, et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell. 2009 Apr;20(7):1981–1991.
   PubMed Web of Science ®Google Scholar
• Wallot-Hieke N, Verma N, Schlütermann D, et al. Systematic analysis of ATG13 domain requirements for autophagy induction. Autophagy. 2018;14(5):743–763.
   PubMed Web of Science ®Google Scholar
• Leist M, Single B, Castoldi AF, et al. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis [Research Support, Non-U.S. Gov’t]. J Exp Med. 1997 Apr 21;185(8):1481–1486.
   PubMed Web of Science ®Google Scholar
• Vandenabeele P, Galluzzi L, Vanden Berghe T, et al. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol. 2010 Oct;11(10):700–714.
   PubMed Web of Science ®Google Scholar
• Hawley SA, Fyffe FA, Russell FM, et al. Intact cell assays to monitor AMPK and determine the contribution of the AMP-binding or ADaM sites to activation. Methods Mol Biol. 2018;1732:239–253.
   PubMedGoogle Scholar
• Mejlvang J, Olsvik H, Svenning S, et al. Starvation induces rapid degradation of selective autophagy receptors by endosomal microautophagy [Research Support, Non-U.S. Gov’t]. J Cell Biol. 2018 Oct 1;217(10):3640–3655.
   PubMed Web of Science ®Google Scholar
• Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007 Sep-Oct;3(5):452–460.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition) [Guideline Research Support, N.I.H., Extramural]. Autophagy. 2016;12(1):1–222.
   PubMed Web of Science ®Google Scholar
• Itakura E, Kishi-Itakura C, Mizushima N. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell. 2012 Dec 7;151(6):1256–1269.
   PubMed Web of Science ®Google Scholar
• Matsui T, Jiang P, Nakano S, et al. Autophagosomal YKT6 is required for fusion with lysosomes independently of syntaxin 17. J Cell Biol. 2018 Aug 6;217(8):2633–2645.
   PubMed Web of Science ®Google Scholar
• Frank D, Vaux DL, Murphy JM, et al. Activated MLKL attenuates autophagy following its translocation to intracellular membranes [Research Support, Non-U.S. Gov’t]. J Cell Sci. 2019 Feb 28;132:5.
   Web of Science ®Google Scholar
• Goodall ML, Fitzwalter BE, Zahedi S, et al. The autophagy machinery controls cell death switching between apoptosis and necroptosis. Dev Cell. 2016 May 23;37(4):337–349.
   PubMed Web of Science ®Google Scholar
• Harris KG, Morosky SA, Drummond CG, et al. RIP3 regulates autophagy and promotes Coxsackievirus B3 infection of intestinal epithelial cells [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. Cell Host Microbe. 2015 Aug 12;18(2):221–232.
   PubMed Web of Science ®Google Scholar
• Yonekawa T, Gamez G, Kim J, et al. RIP1 negatively regulates basal autophagic flux through TFEB to control sensitivity to apoptosis [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. EMBO Rep. 2015 Jun;16(6):700–708.
   PubMed Web of Science ®Google Scholar
• Fuchslocher Chico J, Saggau C, Adam D. Proteolytic control of regulated necrosis [Research Support, Non-U.S. Gov’t Review]. Biochim Biophys Acta Mol Cell Res. 2017 Nov;1864(11 Pt B):2147–2161.
   PubMed Web of Science ®Google Scholar
• Corona AK, Saulsbery HM, Corona Velazquez AF, et al. Enteroviruses Remodel Autophagic Trafficking through Regulation of Host SNARE Proteins to Promote Virus Replication and Cell Exit. Cell Rep. 2018 Mar 20;22(12):3304–3314.
   PubMed Web of Science ®Google Scholar
• Mohamud Y, Shi J, Qu J, et al. Enteroviral infection inhibits Autophagic Flux via Disruption of the SNARE complex to enhance viral replication. Cell Rep. 2018 Mar 20;22(12):3292–3303.
   PubMed Web of Science ®Google Scholar
• Dupont N, Codogno P. Non-canonical autophagy: facts and prospects. Curr Pathobiol Rep. 2013;1(4):263–271. 2013/12/01
   Google Scholar
• Florey O, Overholtzer M. Autophagy proteins in macroendocytic engulfment. Trends Cell Biol. 2012 Jul;22(7):374–380.
   PubMed Web of Science ®Google Scholar
• Fletcher K, Ulferts R, Jacquin E, et al. The WD40 domain of ATG16L1 is required for its non-canonical role in lipidation of LC3 at single membranes [Research Support, Non-U.S. Gov’t]. Embo J. 2018 Feb 15;37:4.
   Web of Science ®Google Scholar
• Florey O, Gammoh N, Kim SE, et al. V-ATPase and osmotic imbalances activate endolysosomal LC3 lipidation [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. Autophagy. 2015;11(1):88–99.
   PubMed Web of Science ®Google Scholar
• Jacquin E, Leclerc-Mercier S, Judon C, et al. Pharmacological modulators of autophagy activate a parallel noncanonical pathway driving unconventional LC3 lipidation. Autophagy. 2017 May 4;13(5):854–867.
   PubMed Web of Science ®Google Scholar
• Gao Y, Liu Y, Hong L, et al. Golgi-associated LC3 lipidation requires V-ATPase in noncanonical autophagy. Cell Death Dis. 2016 Aug 11;7(8):e2330.
   PubMedGoogle Scholar
• Rubinstein AD, Kimchi A. Life in the balance - a mechanistic view of the crosstalk between autophagy and apoptosis [Research Support, Non-U.S. Gov’t Review]. J Cell Sci. 2012 Nov 15;125(Pt 22):5259–5268.
   PubMed Web of Science ®Google Scholar
• Matsuzawa Y, Oshima S, Nibe Y, et al. RIPK3 regulates p62-LC3 complex formation via the caspase-8-dependent cleavage of p62. Biochem Biophys Res Commun. 2015 Jan 2;456(1):298–304.
   PubMed Web of Science ®Google Scholar
• Goodall ML, Cramer SD, Thorburn A. Autophagy RIPs into cell death. Cell Cycle. 2016 Nov 16;15(22):3014–3015.
   PubMed Web of Science ®Google Scholar
• Chen W, Zhou Z, Li L, et al. Diverse sequence determinants control human and mouse receptor interacting protein 3 (RIP3) and mixed lineage kinase domain-like (MLKL) interaction in necroptotic signaling [Research Support, Non-U.S. Gov’t]. J Biol Chem. 2013 Jun 7;288(23):16247–16261.
   PubMed Web of Science ®Google Scholar
• Zhang DW, Shao J, Lin J, et al. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis [Research Support, U.S. Gov’t, Non-P.H.S.]. Science 2009 Jul 17;325(5938):332–336.
   PubMed Web of Science ®Google Scholar
• Cheong H, Lindsten T, Wu J, et al. Ammonia-induced autophagy is independent of ULK1/ULK2 kinases. Proc Natl Acad Sci U S A. 2011 Jul 5;108(27):11121–11126.
   PubMed Web of Science ®Google Scholar
• Laderoute KR, Amin K, Calaoagan JM, et al. 5ʹ-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments [Research Support, N.I.H., extramural research support, Non-U.S. Gov’t]. Mol Cell Biol. 2006 Jul;26(14):5336–5347.
   PubMed Web of Science ®Google Scholar