Redundancy of human ATG4 protease isoforms in autophagy and LC3/GABARAP processing revealed in cells

References

• Bento CF, Renna M, Ghislat G, et al. Mammalian autophagy: how does it work? Annu. Rev Biochem. 2016;85:685–713.
   PubMed Web of Science ®Google Scholar
• Galluzzi L, Baehrecke EH, Ballabio A, et al. Molecular definitions of autophagy and related processes. Embo J. 2017;36:1811–1836.
   PubMed Web of Science ®Google Scholar
• Harding TM, Morano KA, Scott SV, et al. Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J Cell Biol. 1995;131:591–602.
   PubMed Web of Science ®Google Scholar
• Tsukada M, Ohsumi Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 1993;333:169–174.
   PubMed Web of Science ®Google Scholar
• Ichimura Y, Kirisako T, Takao T, et al. A ubiquitin-like system mediates protein lipidation. Nature. 2000;408:488–492.
   PubMed Web of Science ®Google Scholar
• Hanada T, Noda NN, Satomi Y, et al. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem. 2007;282:37298–37302.
   PubMed Web of Science ®Google Scholar
• Xie Z, Nair U, Klionsky DJ. Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell. 2008;19:3290–3298.
   PubMed Web of Science ®Google Scholar
• Pankiv S, Clausen TH, Lamark T, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem. 2007;282:24131–24145.
   PubMed Web of Science ®Google Scholar
• Kirisako T, Ichimura Y, Okada H, et al. The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol. 2000;151:263–276.
   PubMed Web of Science ®Google Scholar
• Nair U, Yen W-L, Mari M, et al. A role for Atg8-PE deconjugation in autophagosome biogenesis. Autophagy. 2012;8:780–793.
   PubMed Web of Science ®Google Scholar
• Nakatogawa H, Ishii J, Asai E, et al. Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis. Autophagy. 2012;8:177–186.
   PubMed Web of Science ®Google Scholar
• Yu Z-Q, Ni T, Hong B, et al. Dual roles of Atg8-PE deconjugation by Atg4 in autophagy. Autophagy. 2012;8:883–892.
   PubMed Web of Science ®Google Scholar
• Tsuboyama K, Koyama-Honda I, Sakamaki Y, et al. The ATG conjugation systems are important for degradation of the inner autophagosomal membrane. Science. 2016;354:1036–1041.
   PubMed Web of Science ®Google Scholar
• Nguyen TN, Padman BS, Usher J, et al. 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;215:857–874.
   PubMed Web of Science ®Google Scholar
• Weidberg H, Shvets E, Shpilka T, et al. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. Embo J. 2010;29:1792–1802.
   PubMed Web of Science ®Google Scholar
• Li M, Hou Y, Wang J, et al. Kinetics comparisons of mammalian Atg4 homologues indicate selective preferences toward diverse Atg8 substrates. J Biol Chem. 2011;286:7327–7338.
   PubMed Web of Science ®Google Scholar
• Scherz-Shouval R, Sagiv Y, Shorer H, et al. The COOH terminus of GATE-16, an intra-Golgi transport modulator, is cleaved by the human cysteine protease HsApg4A. J Biol Chem. 2003;278:14053–14058.
   PubMed Web of Science ®Google Scholar
• Betin VMS, Lane JD. Caspase cleavage of Atg4D stimulates GABARAP-L1 processing and triggers mitochondrial targeting and apoptosis. J Cell Sci. 2009;122:2554–2566.
   PubMed Web of Science ®Google Scholar
• Mariño G, Fernández AF, Cabrera S, et al. Autophagy is essential for mouse sense of balance. J Clin Invest. 2010;120:2331–2344.
   PubMed Web of Science ®Google Scholar
• Sou Y, Waguri S, Iwata J, et al. The Atg8 conjugation system is indispensable for proper development of autophagic isolation membranes in mice. Mol Biol Cell. 2008;19:4762–4775.
   PubMed Web of Science ®Google Scholar
• Pengo N, Agrotis A, Prak K, et al. A reversible phospho-switch mediated by ULK1 regulates the activity of autophagy protease ATG4B. Nat Commun. 2017;8:294.
   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;13:132–141.
   PubMed Web of Science ®Google Scholar
• Wang W, Chen Z, Billiar TR, et al. The carboxyl-terminal amino acids render pro-human LC3B migration similar to lipidated LC3B in SDS-PAGE. PloS One. 2013;8:e74222.
   PubMed Web of Science ®Google Scholar
• Tanida I, Sou Y, Ezaki J, et al. HsAtg4B/HsApg4B/autophagin-1 cleaves the carboxyl termini of three human Atg8 homologues and delipidates microtubule-associated protein light chain 3- and GABAA receptor-associated protein-phospholipid conjugates. J Biol Chem. 2004;279:36268–36276.
   PubMed Web of Science ®Google Scholar
• Skytte Rasmussen M, Mouilleron S, Kumar Shrestha B, et al. ATG4B contains a C-terminal LIR motif important for binding and efficient cleavage of mammalian orthologs of yeast Atg8. Autophagy. 2017;13:834–853.
   PubMed Web of Science ®Google Scholar
• Le Grand JN, Chakrama FZ, Seguin-Py S, et al. GABARAPL1 antibodies: target one protein, get one free! Autophagy. 2011;7:1302–1307.
   PubMed Web of Science ®Google Scholar
• Ylä-Anttila P, Vihinen H, Jokitalo E, et al. Monitoring autophagy by electron microscopy in mammalian cells. Methods Enzymol. 2009;452:143–164.
   PubMed Web of Science ®Google Scholar
• Bjørkøy G, Lamark T, Brech A, et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol. 2005;171:603–614.
   PubMed Web of Science ®Google Scholar
• Kauffman KJ, Yu S, Jin J, et al. Delipidation of mammalian Atg8-family proteins by each of the four ATG4 proteases. Autophagy. 2018;1–56.
   Web of Science ®Google Scholar
• Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J. 2000;19:5720–5728.
   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;3:452–460.
   PubMed Web of Science ®Google Scholar
• Fujita N, Hayashi-Nishino M, Fukumoto H, et al. An Atg4B mutant hampers the lipidation of LC3 paralogues and causes defects in autophagosome closure. Mol Biol Cell. 2008;19:4651–4659.
   PubMed Web of Science ®Google Scholar
• Abreu S, Kriegenburg F, Gómez-Sánchez R, et al. Conserved Atg8 recognition sites mediate Atg4 association with autophagosomal membranes and Atg8 deconjugation. EMBO Rep. 2017;18:765–780.
   PubMed Web of Science ®Google Scholar
• Sánchez-Wandelmer J, Kriegenburg F, Rohringer S, et al. Atg4 proteolytic activity can be inhibited by Atg1 phosphorylation. Nat Commun. 2017;8:295.
   PubMed Web of Science ®Google Scholar
• Hodgkins A, Farne A, Perera S, et al. WGE: a CRISPR database for genome engineering. Bioinforma Oxf Engl. 2015;31:3078–3080.
   PubMed Web of Science ®Google Scholar
• Ran FA, Hsu PD, Wright J, et al. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013;8:2281–2308.
   PubMed Web of Science ®Google Scholar
• Sanjana NE, Shalem O, Zhang F. Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods. 2014;11:783–784.
   PubMed Web of Science ®Google Scholar
• Costa JR, Prak K, Aldous S, et al. Autophagy gene expression profiling identifies a defective microtubule-associated protein light chain 3A mutant in cancer. Oncotarget. 2016;7:41203–41216.
   PubMedGoogle Scholar
• Rual J-F, Hirozane-Kishikawa T, Hao T, et al. Human ORFeome version 1.1: a platform for reverse proteomics. Genome Res. 2004;14:2128–2135.
   PubMed Web of Science ®Google Scholar
• Petschnigg J, Groisman B, Kotlyar M, et al. The mammalian-membrane two-hybrid assay (MaMTH) for probing membrane-protein interactions in human cells. Nat Methods. 2014;11:585–592.
   PubMed Web of Science ®Google Scholar
• Campeau E, Ruhl VE, Rodier F, et al. A versatile viral system for expression and depletion of proteins in mammalian cells. PloS One. 2009;4:e6529.
   PubMed Web of Science ®Google Scholar
• Ye J, Coulouris G, Zaretskaya I, et al. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics. 2012;13:134.
   PubMed Web of Science ®Google Scholar
• Karolchik D, Hinrichs AS, Furey TS, et al. The UCSC table browser data retrieval tool. Nucleic Acids Res. 2004;32:D493–496.
   PubMed Web of Science ®Google Scholar
• Yang H, Roberts MF. Cloning, overexpression, and characterization of a bacterial Ca2+-dependent phospholipase D. Protein Sci Publ Protein Soc. 2002;11:2958–2968.
   PubMed Web of Science ®Google Scholar
• Diao J, Liu R, Rong Y, et al. ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature. 2015;520:563–566.
   PubMed Web of Science ®Google Scholar
• Velikkakath AKG, Nishimura T, Oita E, et al. Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Mol Biol Cell. 2012;23:896–909.
   PubMed Web of Science ®Google Scholar