3,370
Views
27
CrossRef citations to date
0
Altmetric
Research Paper - Basic Science

Delipidation of mammalian Atg8-family proteins by each of the four ATG4 proteases

, , , , , , , & show all
Pages 992-1010 | Received 24 Jul 2017, Accepted 22 Jan 2018, Published online: 10 Apr 2018

References

  • Klionsky DJ, Schulman BA. Dynamic regulation of macroautophagy by distinctive ubiquitin-like proteins. Nat Struct Mol Biol. 2014;21:336–45. doi:10.1038/nsmb.2787. PMID:24699082
  • Fujita N, Hayashi-Nishino M, Fukumoto H, Omori H, Yamamoto A, Noda T, Yoshimori T. An Atg4B mutant hampers the lipidation of LC3 paralogues and causes defects in autophagosome closure. Mol Biol Cell. 2008;19:4651–9. Epub 2008/09/05. doi:10.1091/mbc.E08-03-0312. PMID:18768752
  • Weidberg H, Shvets E, Shpilka T, Shimron F, Shinder V, Elazar Z. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. The EMBO journal. 2010;29:1792–802. Epub 2010/04/27. doi:10.1038/emboj.2010.74. PMID:20418806
  • Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, Yoshimori T, Ohsumi M, Takao T, Noda T, Ohsumi Y. 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;151:263–76. Epub 2000/10/19. doi:10.1083/jcb.151.2.263. PMID:11038174
  • 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. Epub 2000/11/22. doi:10.1083/jcb.151.5.1025. PMID:11086004
  • Yu S, Melia TJ. The coordination of membrane fission and fusion at the end of autophagosome maturation. Curr Opin Cell Biol. 2017;47:92–8. doi:10.1016/j.ceb.2017.03.010. PMID:28463755
  • 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. PMID:27864321
  • Tsuboyama K, Koyama-Honda I, Sakamaki Y, Koike M, Morishita H, Mizushima N. The ATG conjugation systems are important for degradation of the inner autophagosomal membrane. Science (New York, NY.) 2016;354:1036–41. doi:10.1126/science.aaf6136.
  • Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. The EMBO journal. 2007;26:1749–60. Epub 2007/03/10. doi:10.1038/sj.emboj.7601623. PMID:17347651
  • Scherz-Shouval R, Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci. 2011;36:30–8. Epub 2010/08/24. doi:10.1016/j.tibs.2010.07.007. PMID:20728362
  • Bortnik S, Choutka C, Horlings HM, Leung S, Baker JH, Lebovitz C, Dragowska WH, Go NE, Bally MB, Minchinton AI, et al. Identification of breast cancer cell subtypes sensitive to ATG4B inhibition. Oncotarget. 2016;7:66970–88. doi:10.18632/oncotarget.11408. PMID:27556700
  • Yoshimura K, Shibata M, Koike M, Gotoh K, Fukaya M, Watanabe M, Uchiyama Y. Effects of RNA interference of Atg4B on the limited proteolysis of LC3 in PC12 cells and expression of Atg4B in various rat tissues. Autophagy. 2006;2:200–8. doi:10.4161/auto.2744. PMID:16874114
  • Nakatogawa H, Ishii J, Asai E, Ohsumi Y. Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis. Autophagy. 2012;8:177–86. Epub 2012/01/14. doi:10.4161/auto.8.2.18373. PMID:22240591
  • Wang W, Chen Z, Billiar TR, Stang MT, Gao W. The carboxyl-terminal amino acids render pro-human LC3B migration similar to lipidated LC3B in SDS-PAGE. PLoS One. 2013;8:e74222. doi:10.1371/journal.pone.0074222. PMID:24040206
  • Akin D, Wang SK, Habibzadegah-Tari P, Law B, Ostrov D, Li M, Yin XM, Kim JS, Horenstein N, Dunn WA, Jr. A novel ATG4B antagonist inhibits autophagy and has a negative impact on osteosarcoma tumors. Autophagy. 2014;10:2021–35. doi:10.4161/auto.32229. PMID:25483883
  • Li M, Chen X, Ye QZ, Vogt A, Yin XM. A high-throughput FRET-based assay for determination of Atg4 activity. Autophagy. 2012;8:401–12. Epub 2012/02/04. doi:10.4161/auto.18777. PMID:22302004
  • Li M, Hou Y, Wang J, Chen X, Shao ZM, Yin XM. Kinetics comparisons of mammalian Atg4 homologues indicate selective preferences toward diverse Atg8 substrates. The J Biol Chem. 2011;286:7327–38. Epub 2010/12/24. doi:10.1074/jbc.M110.199059. PMID:21177865
  • Shu CW, Madiraju C, Zhai D, Welsh K, Diaz P, Sergienko E, Sano R, Reed JC. High-throughput fluorescence assay for small-molecule inhibitors of autophagins/Atg4. J Biomol Screen. 2011;16:174–82. Epub 2011/01/20. doi:10.1177/1087057110392996. PMID:21245471
  • Betin VM, Lane JD. Caspase cleavage of Atg4D stimulates GABARAP-L1 processing and triggers mitochondrial targeting and apoptosis. Journal of cell science. 2009;122:2554–66. Epub 2009/06/25. doi:10.1242/jcs.046250. PMID:19549685
  • Marino G, Uria JA, Puente XS, Quesada V, Bordallo J, Lopez-Otin C. Human autophagins, a family of cysteine proteinases potentially implicated in cell degradation by autophagy. J Biol Chem. 2003;278:3671–8. Epub 2002/11/26. doi:10.1074/jbc.M208247200. PMID:12446702
  • Scherz-Shouval R, Sagiv Y, Shorer H, Elazar Z. The COOH terminus of GATE-16, an intra-Golgi transport modulator, is cleaved by the human cysteine protease HsApg4A. J Biol Chem. 2003;278:14053–8. Epub 2002/12/11. doi:10.1074/jbc.M212108200. PMID:12473658
  • Yu ZQ, Ni T, Hong B, Wang HY, Jiang FJ, Zou S, Chen Y, Zheng XL, Klionsky DJ, Liang Y, et al. Dual roles of Atg8-PE deconjugation by Atg4 in autophagy. Autophagy. 2012;8:883–92. doi:10.4161/auto.19652. PMID:22652539
  • Nair U, Yen WL, Mari M, Cao Y, Xie Z, Baba M, Reggiori F, Klionsky DJ. A role for Atg8-PE deconjugation in autophagosome biogenesis. Autophagy. 2012;8:780–93. doi:10.4161/auto.19385. PMID:22622160
  • Xie Z, Nair U, Klionsky DJ. Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell. 2008;19:3290–8. Epub 2008/05/30. doi:10.1091/mbc.E07-12-1292. PMID:18508918
  • Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, Yoshimori T, Noda T, Ohsumi Y. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J Cell Biol. 1999;147:435–46. doi:10.1083/jcb.147.2.435. PMID:10525546
  • Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK, Lippincott-Schwartz J. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell. 2010;141:656–67. Epub 2010/05/19. doi:10.1016/j.cell.2010.04.009. PMID:20478256
  • Choy A, Dancourt J, Mugo B, O'Connor TJ, Isberg RR, Melia TJ, Roy CR. The Legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation. Science (New York, NY. 2012;338:1072–6. Epub 2012/11/01. doi:10.1126/science.1227026. PMID:23112293
  • Yang Z, Wilkie-Grantham RP, Yanagi T, Shu CW, Matsuzawa S, Reed JC. ATG4B (Autophagin-1) phosphorylation modulates autophagy. J Biol Chem. 2015;290:26549–61. doi:10.1074/jbc.M115.658088. PMID:26378241
  • Sanchez-Wandelmer J, Kriegenburg F, Rohringer S, Schuschnig M, Gomez-Sanchez R, Zens B, Abreu S, Hardenberg R, Hollenstein D, Gao J, et al. Atg4 proteolytic activity can be inhibited by Atg1 phosphorylation. Nat Commun. 2017;8:295. doi:10.1038/s41467-017-00302-3. PMID:28821724
  • Abreu S, Kriegenburg F, Gomez-Sanchez R, Mari M, Sanchez-Wandelmer J, Skytte Rasmussen M, Soares Guimaraes R, Zens B, Schuschnig M, Hardenberg R, et al. Conserved Atg8 recognition sites mediate Atg4 association with autophagosomal membranes and Atg8 deconjugation. EMBO Rep. 2017;18:765–80. doi:10.15252/embr.201643146. PMID:28330855
  • Skytte Rasmussen M, Mouilleron S, Kumar Shrestha B, Wirth M, Lee R, Bowitz Larsen K, Abudu Princely Y, O'Reilly N, Sjottem E, Tooze SA, et al. ATG4B contains a C-terminal LIR motif important for binding and efficient cleavage of mammalian orthologs of yeast Atg8. Autophagy. 2017;13:834–53. doi:10.1080/15548627.2017.1287651. PMID:28287329
  • Pankiv S, Alemu EA, Brech A, Bruun JA, Lamark T, Overvatn A, Bjorkoy G, Johansen T. FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J Cell Biol. 2010;188:253–69. Epub 2010/01/27. doi:10.1083/jcb.200907015. PMID:20100911
  • Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem. 2007;282:24131–45. doi:10.1074/jbc.M702824200. PMID:17580304
  • Lystad AH, Ichimura Y, Takagi K, Yang Y, Pankiv S, Kanegae Y, Kageyama S, Suzuki M, Saito I, Mizushima T, et al. Structural determinants in GABARAP required for the selective binding and recruitment of ALFY to LC3B-positive structures. EMBO Rep. 2014;15:557–65. doi:10.1002/embr.201338003. PMID:24668264
  • Abert C, Kontaxis G, Martens S. Accessory Interaction Motifs in the Atg19 Cargo Receptor Enable Strong Binding to the Clustered Ubiquitin-related Atg8 Protein. J Biol Chem. 2016;291:18799–808. doi:10.1074/jbc.M116.736892. PMID:27402840
  • Behrends C, Sowa ME, Gygi SP, Harper JW. Network organization of the human autophagy system. Nature. 2010;466:68–76. Epub 2010/06/22. doi:10.1038/nature09204. PMID:20562859
  • Horenkamp FA, Kauffman KJ, Kohler LJ, Sherwood RK, Krueger KP, Shteyn V, Roy CR, Melia TJ, Reinisch KM. The Legionella Anti-autophagy Effector RavZ Targets the Autophagosome via PI3P- and Curvature-Sensing Motifs. Developmental Cell. 2015;34:569–76. doi:10.1016/j.devcel.2015.08.010. PMID:26343456
  • Sou YS, Tanida I, Komatsu M, Ueno T, Kominami E. Phosphatidylserine in addition to phosphatidylethanolamine is an in vitro target of the mammalian Atg8 modifiers, LC3, GABARAP, and GATE-16. J Biol Chem. 2006;281:3017–24. doi:10.1074/jbc.M505888200. PMID:16303767
  • Nath S, Dancourt J, Shteyn V, Puente G, Fong WM, Nag S, Bewersdorf J, Yamamoto A, Antonny B, Melia TJ. Lipidation of the LC3/GABARAP family of autophagy proteins relies on a membrane-curvature-sensing domain in Atg3. Nat Cell Biol. 2014;16:415–24. Epub 2014/04/22. doi:10.1038/ncb2940. PMID:24747438
  • Tanida I, Sou YS, Ezaki J, Minematsu-Ikeguchi N, Ueno T, Kominami E. 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;279:36268–76. doi:10.1074/jbc.M401461200. PMID:15187094
  • van Tilbeurgh H, Egloff MP, Martinez C, Rugani N, Verger R, Cambillau C. Interfacial activation of the lipase-procolipase complex by mixed micelles revealed by X-ray crystallography. Nature. 1993;362:814–20. Epub 1993/04/29. doi:10.1038/362814a0. PMID:8479519
  • Hanada T, Noda NN, Satomi Y, Ichimura Y, Fujioka Y, Takao T, Inagaki F, Ohsumi Y. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem. 2007;282:37298–302. Epub 2007/11/08. doi:10.1074/jbc.C700195200. PMID:17986448
  • Oh-oka K, Nakatogawa H, Ohsumi Y. Physiological pH and acidic phospholipids contribute to substrate specificity in lipidation of Atg8. J Biol Chem. 2008;283:21847–52. Epub 2008/06/12. doi:10.1074/jbc.M801836200. PMID:18544538
  • Betin VM, MacVicar TD, Parsons SF, Anstee DJ, Lane JD. A cryptic mitochondrial targeting motif in Atg4D links caspase cleavage with mitochondrial import and oxidative stress. Autophagy. 2012;8:664–76. Epub 2012/03/24. doi:10.4161/auto.19227. PMID:22441018
  • Satoo K, Noda NN, Kumeta H, Fujioka Y, Mizushima N, Ohsumi Y, Inagaki F. The structure of Atg4B-LC3 complex reveals the mechanism of LC3 processing and delipidation during autophagy. The EMBO Journal. 2009;28:1341–50. Epub 2009/03/27. doi:10.1038/emboj.2009.80. PMID:19322194
  • Cabrera S, Maciel M, Herrera I, Nava T, Vergara F, Gaxiola M, Lopez-Otin C, Selman M, Pardo A. Essential role for the ATG4B protease and autophagy in bleomycin-induced pulmonary fibrosis. Autophagy. 2015;11:670–84. doi:10.1080/15548627.2015.1034409. PMID:25906080
  • Marino G, Fernandez AF, Cabrera S, Lundberg YW, Cabanillas R, Rodriguez F, Salvador-Montoliu N, Vega JA, Germana A, Fueyo A, et al. Autophagy is essential for mouse sense of balance. J Clin Invest. 2010;120:2331–44. Epub 2010/06/26. doi:10.1172/JCI42601. PMID:20577052
  • Nguyen N, Shteyn V, Melia TJ. Sensing Membrane Curvature in Macroautophagy. J Mol Biol. 2017;429:457–72. doi:10.1016/j.jmb.2017.01.006.
  • Rao Y, Matscheko N, Wollert T. Autophagy in the test tube: In vitro reconstitution of aspects of autophagosome biogenesis. The FEBS journal. 2016;283:2034–43. doi:10.1111/febs.13661. PMID:26797728
  • Zens B, Sawa-Makarska J, Martens S. In vitro systems for Atg8 lipidation. Methods. 2015;75:37–43. doi:10.1016/j.ymeth.2014.11.004. PMID:25461810
  • Knorr RL, Nakatogawa H, Ohsumi Y, Lipowsky R, Baumgart T, Dimova R. Membrane morphology is actively transformed by covalent binding of the protein Atg8 to PE-lipids. PLoS One. 2014;9:e115357. doi:10.1371/journal.pone.0115357. PMID:25522362
  • Kaufmann A, Beier V, Franquelim HG, Wollert T. Molecular mechanism of autophagic membrane-scaffold assembly and disassembly. Cell. 2014;156:469–81. Epub 2014/02/04. doi:10.1016/j.cell.2013.12.022. PMID:24485455
  • Walczak M, Martens S. Dissecting the role of the Atg12-Atg5-Atg16 complex during autophagosome formation. Autophagy. 2013;9:424–5. doi:10.4161/auto.22931. PMID:23321721
  • Fracchiolla D, Sawa-Makarska J, Zens B, Ruiter A, Zaffagnini G, Brezovich A, Romanov J, Runggatscher K, Kraft C, Zagrovic B, et al. Mechanism of cargo-directed Atg8 conjugation during selective autophagy. Elife. 2016;5:e18544.
  • Kwon DH, Kim S, Jung YO, Roh KH, Kim L, Kim BW, Hong SB, Lee IY, Song JH, Lee WC, et al. The 1:2 complex between RavZ and LC3 reveals a mechanism for deconjugation of LC3 on the phagophore membrane. Autophagy. 2017;13:70–81. doi:10.1080/15548627.2016.1243199. PMID:27791457
  • Yang A, Pantoom S, Wu YW. Elucidation of the anti-autophagy mechanism of the Legionella effector RavZ using semisynthetic LC3 proteins. Elife. 2017;6: e23905.
  • Sawa-Makarska J, Abert C, Romanov J, Zens B, Ibiricu I, Martens S. Cargo binding to Atg19 unmasks additional Atg8 binding sites to mediate membrane-cargo apposition during selective autophagy. Nat Cell Biol. 2014;16:425–33. Epub 2014/04/08. doi:10.1038/ncb2935. PMID:24705553
  • Ni Z, Gong Y, Dai X, Ding W, Wang B, Gong H, Qin L, Cheng P, Li S, Lian J, et al. AU4S: a novel synthetic peptide to measure the activity of ATG4 in living cells. Autophagy. 2015;11:403–15. Epub 2015/04/02. doi:10.1080/15548627.2015.1009773. PMID:25831015
  • Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. Journal of cell science. 2004;117:2805–12. Epub 2004/06/01. doi:10.1242/jcs.01131. PMID:15169837
  • Qiao S, Dennis M, Song X, Vadysirisack DD, Salunke D, Nash Z, Yang Z, Liesa M, Yoshioka J, Matsuzawa S, et al. A REDD1/TXNIP pro-oxidant complex regulates ATG4B activity to control stress-induced autophagy and sustain exercise capacity. Nat Commun. 2015;6:7014. doi:10.1038/ncomms8014. PMID:25916556
  • Kuang E, Okumura CY, Sheffy-Levin S, Varsano T, Shu VC, Qi J, Niesman IR, Yang HJ, Lopez-Otin C, Yang WY, et al. Regulation of ATG4B stability by RNF5 limits basal levels of autophagy and influences susceptibility to bacterial infection. PLoS genetics. 2012;8:e1003007. doi:10.1371/journal.pgen.1003007. PMID:23093945
  • Williams RA, Woods KL, Juliano L, Mottram JC, Coombs GH. Characterization of unusual families of ATG8-like proteins and ATG12 in the protozoan parasite Leishmania major. Autophagy. 2009;5:159–72. Epub 2008/12/11. doi:10.4161/auto.5.2.7328. PMID:19066473
  • Wu F, Li Y, Wang F, Noda NN, Zhang H. Differential function of the two Atg4 homologues in the aggrephagy pathway in Caenorhabditis elegans. J Biol Chem. 2012;287:29457–67. Epub 2012/07/07. doi:10.1074/jbc.M112.365676. PMID:22767594
  • Alvarez VE, Kosec G, Sant'Anna C, Turk V, Cazzulo JJ, Turk B. Autophagy is involved in nutritional stress response and differentiation in Trypanosoma cruzi. J Biol Chem. 2008;283:3454–64. doi:10.1074/jbc.M708474200. PMID:18039653
  • Jo YK, Park NY, Park SJ, Kim BG, Shin JH, Jo DS, Bae DJ, Suh YA, Chang JH, Lee EK, et al. O-GlcNAcylation of ATG4B positively regulates autophagy by increasing its hydroxylase activity. Oncotarget. 2016;7:57186–96. doi:10.18632/oncotarget.11083. PMID:27527864

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.