Autophagy mediates phosphatidylserine exposure and phagosome degradation during apoptosis through specific functions of GABARAP/LGG-1 and LC3/LGG-2

References

• Savill J, Gregory C, Haslett C. Cell biology. Eat Me Die Science. 2003;302:1516–1517.
   Google Scholar
• Florey O, Kim SE, Sandoval CP, et al. Autophagy machinery mediates macroendocytic processing and entotic cell death by targeting single membranes. Nat Cell Biol. 2011;13:1335–1343.
   PubMed Web of Science ®Google Scholar
• Martinez J, Almendinger J, Oberst A, et al. Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells. Proc Natl Acad Sci U S A. 2011;108:17396–17401.
   PubMed Web of Science ®Google Scholar
• Sanjuan MA, Dillon CP, Tait SWG, et al. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature. 2007;450:1253–1257.
   PubMed Web of Science ®Google Scholar
• Henault J, Martinez J, Riggs JM, et al. Noncanonical autophagy is required for type I interferon secretion in response to DNA-immune complexes. Immunity. 2012;37:986–997.
   PubMed Web of Science ®Google Scholar
• Kim J-Y, Zhao H, Martinez J, et al. Noncanonical autophagy promotes the visual cycle. Cell. 2013;154:365–376.
   PubMed Web of Science ®Google Scholar
• Martinez J, Malireddi RKS, Lu Q, et al. Molecular characterization of LC3-associated phagocytosis reveals distinct roles for Rubicon, NOX2 and autophagy proteins. Nat Cell Biol. 2015;17:893–906.
   PubMed Web of Science ®Google Scholar
• Lerena MC, Colombo MI. Mycobacterium marinum induces a marked LC3 recruitment to its containing phagosome that depends on a functional ESX-1 secretion system. Cell Microbiol. 2011;13:814–835.
   PubMed Web of Science ®Google Scholar
• Nicola AM, Albuquerque P, Martinez LR, et al. Macrophage autophagy in immunity to Cryptococcus neoformans and Candida albicans. Infect Immun. 2012;80:3065–3076.
   PubMed Web of Science ®Google Scholar
• Shpilka T, Weidberg H, Pietrokovski S, et al. Atg8: an autophagy-related ubiquitin-like protein family. Genome Biol. 2011;12:226.
   PubMed Web of Science ®Google Scholar
• Behrends C, Sowa ME, Gygi SP, et al. Network organization of the human autophagy system. Nature. 2010;466:68–76.
   PubMed Web of Science ®Google Scholar
• von Muhlinen N, Akutsu M, Ravenhill BJ, et al. LC3C, bound selectively by a noncanonical LIR motif in NDP52, is required for antibacterial autophagy. Mol Cell. 2012;48:329–342.
   PubMed Web of Science ®Google Scholar
• Manil-Ségalen M, Lefebvre C, Jenzer C, et al. The C. elegans LC3 acts downstream of GABARAP to degrade autophagosomes by interacting with the HOPS subunit VPS39. Dev Cell. 2014;28:43–55.
   PubMed Web of Science ®Google Scholar
• Cheng S, Wu Y, Lu Q, et al. Autophagy genes coordinate with the class II PI/PtdIns 3-kinase PIKI-1 to regulate apoptotic cell clearance in C. elegans. Autophagy. 2013;9:2022–2032.
   PubMed Web of Science ®Google Scholar
• Huang S, Jia K, Wang Y, et al. Autophagy genes function in apoptotic cell corpse clearance during C. elegans embryonic development. Autophagy. 2013;9:138–149.
   PubMed Web of Science ®Google Scholar
• Li W, Zou W, Yang Y, et al. Autophagy genes function sequentially to promote apoptotic cell corpse degradation in the engulfing cell. J Cell Biol. 2012;197:27–35.
   PubMed Web of Science ®Google Scholar
• Gumienny TL, Lambie E, Hartwieg E, et al. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development. 1999;126:1011–1022.
   PubMed Web of Science ®Google Scholar
• Sulston JE, Schierenberg E, White JG, et al. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol. 1983;100:64–119.
   PubMed Web of Science ®Google Scholar
• Denning DP, Hatch V, Horvitz HR. Programmed elimination of cells by caspase-independent cell extrusion in C. elegans. Nature. 2012;488:226–230.
   PubMed Web of Science ®Google Scholar
• Alberti A, Michelet X, Djeddi A, et al. The autophagosomal protein LGG-2 acts synergistically with LGG-1 in dauer formation and longevity in C. elegans. Autophagy. 2010;6:622–633.
   PubMed Web of Science ®Google Scholar
• Yu X, Odera S, Chuang C-H, et al. C. elegans dynamin mediates the signaling of phagocytic receptor CED-1 for the engulfment and degradation of apoptotic cells. Dev Cell. 2006;10:743–757.
   PubMed Web of Science ®Google Scholar
• Ellis RE, Jacobson DM, Horvitz HR. Genes required for the engulfment of cell corpses during programmed cell death in Caenorhabditis elegans. Genetics. 1991;129:79–94.
   PubMed Web of Science ®Google Scholar
• Lu N, Shen Q, Mahoney TR, et al. Three sorting nexins drive the degradation of apoptotic cells in response to PtdIns(3)P signaling. Mol Biol Cell. 2011;22:354–374.
   PubMed Web of Science ®Google Scholar
• Kinchen JM, Doukoumetzidis K, Almendinger J, et al. A pathway for phagosome maturation during engulfment of apoptotic cells. Nat Cell Biol. 2008;10:556–566.
   PubMed Web of Science ®Google Scholar
• Chen Y-Z, Mapes J, Lee E-S, et al. Caspase-mediated activation of Caenorhabditis elegans CED-8 promotes apoptosis and phosphatidylserine externalization. Nat Commun. 2013;4:2726.
   PubMed Web of Science ®Google Scholar
• Mapes J, Chen Y-Z, Kim A, et al. CED-1, CED-7, and TTR-52 regulate surface phosphatidylserine expression on apoptotic and phagocytic cells. Curr Biol. 2012;22:1267–1275.
   PubMed Web of Science ®Google Scholar
• Venegas V, Zhou Z. Two alternative mechanisms that regulate the presentation of apoptotic cell engulfment signal in Caenorhabditis elegans. Mol Biol Cell. 2007;18:3180–3192.
   PubMed Web of Science ®Google Scholar
• Stanfield GM, Horvitz HR. The ced-8 gene controls the timing of programmed cell deaths in C. elegans. Mol Cell. 2000;5:423–433.
   PubMed Web of Science ®Google Scholar
• Suzuki J, Denning DP, Imanishi E, et al. Xk-related protein 8 and CED-8 promote phosphatidylserine exposure in apoptotic cells. Science. 2013;341:403–406.
   PubMed Web of Science ®Google Scholar
• Mellén MA, de la Rosa EJ, Boya P. The autophagic machinery is necessary for removal of cell corpses from the developing retinal neuroepithelium. Cell Death Differ. 2008;15:1279–1290.
   PubMed Web of Science ®Google Scholar
• Qu X, Zou Z, Sun Q, et al. Autophagy gene-dependent clearance of apoptotic cells during embryonic development. Cell. 2007;128:931–946.
   PubMed Web of Science ®Google Scholar
• Muller C, Salvayre R, Nègre-Salvayre A, et al. HDLs inhibit endoplasmic reticulum stress and autophagic response induced by oxidized LDLs. Cell Death Differ. 2011;18:817–828.
   PubMed Web of Science ®Google Scholar
• Green DR, Oguin TH, Martinez J. The clearance of dying cells: table for two. Cell Death Differ. 2016;23:915–926.
   PubMed Web of Science ®Google Scholar
• Kageyama S, Omori H, Saitoh T, et al. The LC3 recruitment mechanism is separate from Atg9L1-dependent membrane formation in the autophagic response against Salmonella. Mol Biol Cell. 2011;22:2290–2300.
   PubMed Web of Science ®Google Scholar
• Brooks CR, Yeung MY, Brooks YS, et al. KIM-1-/TIM-1-mediated phagocytosis links ATG5-/ULK1-dependent clearance of apoptotic cells to antigen presentation. EMBO J. 2015;34:2441–2464.
   PubMed Web of Science ®Google Scholar
• Johnston AD, Ebert PR. The redox system in C. elegans, a phylogenetic approach. J Toxicol. 2012;2012:546915.
   PubMedGoogle Scholar
• Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974;77:71–94.
   PubMed Web of Science ®Google Scholar
• Paix A, Folkmann A, Rasoloson D, et al. High efficiency, homology-directed genome editing in caenorhabditis elegans using CRISPR-Cas9 ribonucleoprotein complexes. Genetics. 2015;201:47–54.
   PubMed Web of Science ®Google Scholar
• Kamath RS, Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods. 2003;30:313–321.
   PubMed Web of Science ®Google Scholar
• Timmons L, Fire A. Specific interference by ingested dsRNA. Nature. 1998;395:854.
   PubMed Web of Science ®Google Scholar
• Legouis R, Gansmuller A, Sookhareea S, et al. LET-413 is a basolateral protein required for the assembly of adherens junctions in Caenorhabditis elegans. Nat Cell Biol. 2000;2:415–422.
   PubMed Web of Science ®Google Scholar
• Al Rawi S, Louvet-Vallée S, Djeddi A, et al. Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science. 2011;334:1144–1147.
   PubMed Web of Science ®Google Scholar
• Bolte S, Cordelières F. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc. 2006;224:213–232.
   PubMed Web of Science ®Google Scholar
• Kolotuev I, Schwab Y, Labouesse M. A precise and rapid mapping protocol for correlative light and electron microscopy of small invertebrate organisms. Biol Cell. 2010;102:121–132.
   Web of Science ®Google Scholar
• Watanabe S, Richards J, Hollopeter G, et al. Nano-fEM: protein localization using photo-activated localization microscopy and electron microscopy. J Vis Exp JoVE. 2012;70:e3995.
   PubMed Web of Science ®Google Scholar