Structural insights into the ubiquitin recognition by OPTN (optineurin) and its regulation by TBK1-mediated phosphorylation

References

• Klionsky DJ, Emr SD. Cell biology - Autophagy as a regulated pathway of cellular degradation. Science. 2000;290:1717–1721. doi:10.1126/science.290.5497.1717. PMID:11099404
   PubMed Web of Science ®Google Scholar
• Mizushima N. Autophagy: process and function. Genes Dev. 2007;21:2861–2873. doi:10.1101/gad.1599207. PMID:18006683
   PubMed Web of Science ®Google Scholar
• Jiang P, Mizushima N. Autophagy and human diseases. Cell Res. 2014;24:69–79. doi:10.1038/cr.2013.161. PMID:24323045
   PubMed Web of Science ®Google Scholar
• Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol. 2009;10:458–467. doi:10.1038/nrm2708. PMID:19491929
   PubMed Web of Science ®Google Scholar
• Feng YC, He D, Yao ZY, Klionsky DJ. The machinery of macroautophagy. Cell Res. 2014;24:24–41. doi:10.1038/cr.2013.168. PMID:24366339
   PubMed Web of Science ®Google Scholar
• Randow F, Youle RJ. Self and nonself: how autophagy targets mitochondria and bacteria. Cell Host & Microbe. 2014;15:404–412. doi:10.1016/j.chom.2014.03.012.
   Web of Science ®Google Scholar
• Stolz A, Ernst A, Dikic I. Cargo recognition and trafficking in selective autophagy. Nat Cell Biol. 2014;16:495–501. doi:10.1038/ncb2979. PMID:24875736
   PubMed Web of Science ®Google Scholar
• Gomes LC, Dikic I. Autophagy in antimicrobial immunity. Mol Cell. 2014;54:224–233. doi:10.1016/j.molcel.2014.03.009. PMID:24766886
   PubMed Web of Science ®Google Scholar
• Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011;7: 279–296. doi:10.4161/auto.7.3.14487. PMID:21189453
   PubMed Web of Science ®Google Scholar
• 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;53:167–178. doi:10.1016/j.molcel.2013.12.014. PMID:24462201
   PubMed Web of Science ®Google Scholar
• Thurston TL, Ryzhakov G, Bloor S, von Muhlinen N, Randow F. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat Immunol. 2009;10:1215–1221. doi:10.1038/ni.1800. PMID:19820708
   PubMed Web of Science ®Google Scholar
• Jiang SX, Wells CD, Roach PJ. Starch-binding domain-containing protein 1 (Stbd1) and glycogen metabolism: identification of the Atg8 family interacting motif (AIM) in Stbd1 required for interaction with GABARAPL1. Biochem Biophys Res Commun. 2011;413:420–425. doi:10.1016/j.bbrc.2011.08.106. PMID:21893048
   PubMed Web of Science ®Google Scholar
• Liu L, Feng D, Chen G, Chen M, Zheng QX, Song PP, Ma Q, Zhu CZ, Wang R, Qi WJ et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat Cell Biol. 2012;14:177–185. doi:10.1038/ncb2422. PMID:22267086
   PubMed Web of Science ®Google Scholar
• Mancias JD, Wang XX, Gygi SP, Harper JW, Kimmelman AC. Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy. Nature. 2014;509:105–109. doi:10.1038/nature13148. PMID:24695223
   PubMed Web of Science ®Google Scholar
• Dou Z, Xu C, Donahue G, Shimi T, Pan JA, Zhu J, Ivanov A, Capell BC, Drake AM, Shah PP et al. Autophagy mediates degradation of nuclear lamina. Nature. 2015;527:105–109. doi:10.1038/nature15548. PMID:26524528
   PubMed Web of Science ®Google Scholar
• Khaminets A, Heinrich T, Mari M, Grumati P, Huebner AK, Akutsu M, Liebmann L, Stolz A, Nietzsche S, Koch N et al. Regulation of endoplasmic reticulum turnover by selective autophagy. Nature. 2015;522:354–358. doi:10.1038/nature14498. PMID:26040720
   PubMed Web of Science ®Google Scholar
• Mochida K, Oikawa Y, Kimura Y, Kirisako H, Hirano H, Ohsumi Y, Nakatogawa H. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature. 2015;522: 359–362. doi:10.1038/nature14506. PMID:26040717
   PubMed Web of Science ®Google Scholar
• Mandell MA, Jain A, Arko-Mensah J, Chauhan S, Kimura T, Dinkins C, Silvestri G, Munch J, Kirchhoff F, Simonsen A et al. TRIM proteins regulate autophagy and can target autophagic substrates by direct recognition. Dev Cell. 2014;30: 394–409. doi:10.1016/j.devcel.2014.06.013. PMID:25127057
   PubMed Web of Science ®Google Scholar
• Zaffagnini G, Martens S. Mechanisms of selective autophagy. J Mol Biol. 2016;428: 1714–1724. doi:10.1016/j.jmb.2016.02.004. PMID:26876603
   PubMed Web of Science ®Google Scholar
• Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR, Richter B, Korac J, Waidmann O, Choudhary C et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science. 2011;333:228–233. doi:10.1126/science.1205405. PMID:21617041
   PubMed Web of Science ®Google Scholar
• Heo JM, Ordureau A, Paulo JA, Rinehart J, Harper JW. The PINK1-PARKIN mitochondrial ubiquitylation pathway drives a program of OPTN/NDP52 recruitment and TBK1 activation to promote mitophagy. Mol Cell. 2015;60:7–20. doi:10.1016/j.molcel.2015.08.016. PMID:26365381
   PubMed Web of Science ®Google Scholar
• Richter B, Sliter DA, Herhaus L, Stolz A, Wang C, Beli P, Zaffagnini G, Wild P, Martens S, Wagner SA et al. Phosphorylation of OPTN by TBK1 enhances its binding to Ub chains and promotes selective autophagy of damaged mitochondria. Proc Natl Acad Sci U S A. 2016;113:4039–4044. doi:10.1073/pnas.1523926113. PMID:27035970
   PubMed Web of Science ®Google Scholar
• McEwan DG, Dikic I. The three musketeers of autophagy: phosphorylation, ubiquitylation and acetylation. Trends Cell Biol. 2011;21:195–201. doi:10.1016/j.tcb.2010.12.006. PMID:21277210
   PubMed Web of Science ®Google Scholar
• Matsumoto G, Wada K, Okuno M, Kurosawa M, Nukina N. Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Mol Cell. 2011;44:279–289. doi:10.1016/j.molcel.2011.07.039. PMID:22017874
   PubMed Web of Science ®Google Scholar
• Kraft C, Peter M, Hofmann K. Selective autophagy: ubiquitin-mediated recognition and beyond. Nat Cell Biol. 2010;12:836–841. doi:10.1038/ncb0910-836. PMID:20811356
   PubMed Web of Science ®Google Scholar
• Lamark T, Johansen T. Aggrephagy: selective disposal of protein aggregates by macroautophagy. Int J Cell Biol. 2012;2012: 736905. doi:10.1155/2012/736905. PMID:22518139
   PubMedGoogle Scholar
• Dikic I, Wakatsuki S, Walters KJ. Ubiquitin-binding domains - from structures to functions. Nat Rev Mol Cell Biol. 2009;10:659–671. doi:10.1038/nrm2767. PMID:19773779
   PubMed Web of Science ®Google Scholar
• Pickart CM, Eddins MJ. Ubiquitin: structures, functions, mechanisms. Biochim Biophys Acta. 2004;1695:55–72. doi:10.1016/j.bbamcr.2004.09.019. PMID:15571809
   PubMed Web of Science ®Google Scholar
• Hicke L, Schubert HL, Hill CP. Ubiquitin-binding domains. Nat Rev Mol Cell Biol. 2005;6:610–621. doi:10.1038/nrm1701. PMID:16064137
   PubMed Web of Science ®Google Scholar
• Kerscher O, Felberbaum R, Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol. 2006;22:159–180. doi:10.1146/annurev.cellbio.22.010605.093503. PMID:16753028
   PubMed Web of Science ®Google Scholar
• Shaid S, Brandts CH, Serve H, Dikic I. Ubiquitination and selective autophagy. Cell Death Differ. 2013;20:21–30. doi:10.1038/cdd.2012.72. PMID:22722335
   PubMed Web of Science ®Google Scholar
• van Wijk SJ, Fiskin E, Putyrski M, Pampaloni F, Hou J, Wild P, Kensche T, Grecco HE, Bastiaens P, Dikic I. Fluorescence-based sensors to monitor localization and functions of linear and K63-linked ubiquitin chains in cells. Mol Cell. 2012;47:797–809. doi:10.1016/j.molcel.2012.06.017. PMID:22819327
   PubMed Web of Science ®Google Scholar
• Fiskin E, Bionda T, Dikic I, Behrends C. Global analysis of host and bacterial ubiquitinome in response to Salmonella Typhimurium infection. Mol Cell. 2016;62:967–981. doi:10.1016/j.molcel.2016.04.015. PMID:27211868
   PubMed Web of Science ®Google Scholar
• Korac J, Schaeffer V, Kovacevic I, Clement AM, Jungblut B, Behl C, Terzic J, Dikic I. Ubiquitin-independent function of optineurin in autophagic clearance of protein aggregates. J Cell Sci. 2013;126:580–592. doi:10.1242/jcs.114926. PMID:23178947
   PubMed Web of Science ®Google Scholar
• Lazarou M, Sliter DA, Kane LA, Sarraf SA, Wang C, Burman JL, Sideris DP, Fogel AI, Youle RJ. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature. 2015;524:309–314. doi:10.1038/nature14893. PMID:26266977
   PubMed Web of Science ®Google Scholar
• Wong YC, Holzbaur ELF. Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc Natl Acad Sci U S A. 2014;111:E4439–E4448. doi:10.1073/pnas.1405752111. PMID:25294927
   PubMed Web of Science ®Google Scholar
• Ying HY, Yue BYJT. Cellular and molecular biology of optineurin. Int Rev Cell Mol Biol. 2012;294:223–258. doi:10.1016/B978-0-12-394305-7.00005-7. PMID:22364875
   PubMed Web of Science ®Google Scholar
• Rahighi S, Ikeda F, Kawasaki M, Akutsu M, Suzuki N, Kato R, Kensche T, Uejima T, Bloor S, Komander D et al. Specific recognition of linear ubiquitin chains by NEMO is important for NF-kappaB activation. Cell. 2009;136:1098–109. doi:10.1016/j.cell.2009.03.007. PMID:19303852
   PubMed Web of Science ®Google Scholar
• Lo YC, Lin SC, Rospigliosi CC, Conze DB, Wu CJ, Ashwell JD, Eliezer D, Wu H. Structural basis for recognition of diubiquitins by NEMO. Mol Cell. 2009;33: 602–615. doi:10.1016/j.molcel.2009.01.012. PMID:19185524
   PubMed Web of Science ®Google Scholar
• Clark K, Nanda S, Cohen P. Molecular control of the NEMO family of ubiquitin-binding proteins. Nat Rev Mol Cell Biol. 2013;14:673–685. doi:10.1038/nrm3644. PMID:23989959
   PubMed Web of Science ®Google Scholar
• Morton S, Hesson L, Peggie M, Cohen P. Enhanced binding of TBK1 by an optineurin mutant that causes a familial form of primary open angle glaucoma. FEBS Lett. 2008;582:997–1002. doi:10.1016/j.febslet.2008.02.047. PMID:18307994
   PubMed Web of Science ®Google Scholar
• Li FX, Xie XQ, Wang YL, Liu JP, Cheng XF, Guo YJ, Gong YK, Hu SC, Pan LF. Structural insights into the interaction and disease mechanism of neurodegenerative disease-associated optineurin and TBK1 proteins. Nat Commun. 2016;7. doi:10.1038/ncomms12708.
   Web of Science ®Google Scholar
• Osawa T, Mizuno Y, Fujita Y, Takatama M, Nakazato Y, Okamoto K. Optineurin in neurodegenerative diseases. Neuropathology. 2011;31:569–574. doi:10.1111/j.1440-1789.2011.01199.x. PMID:21284751
   PubMed Web of Science ®Google Scholar
• Sirohi K, Swarup G. Defects in autophagy caused by glaucoma-associated mutations in optineurin. Exp Eye Res. 2015;144:54–63. doi:10.1016/j.exer.2015.08.020. PMID:26302410
   PubMed Web of Science ®Google Scholar
• Kachaner D, Genin P, Laplantine E, Weil R. Toward an integrative view of Optineurin functions. Cell Cycle. 2012;11:2808–2818. doi:10.4161/cc.20946. PMID:22801549
   PubMed Web of Science ®Google Scholar
• Slowicka K, Vereecke L, van Loo G. Cellular functions of optineurin in health and disease. Trends Immunol. 2016;37:621–633. doi:10.1016/j.it.2016.07.002. PMID:27480243
   PubMed Web of Science ®Google Scholar
• Rezaie T, Child A, Hitchings R, Brice G, Miller L, Coca-Prados M, Heon E, Krupin T, Ritch R, Kreutzer D et al. Adult-onset primary open-angle glaucoma caused by mutations in optineurin. Science. 2002;295:1077–1079. doi:10.1126/science.1066901. PMID:11834836
   PubMed Web of Science ®Google Scholar
• Maruyama H, Morino H, Ito H, Izumi Y, Kato H, Watanabe Y, Kinoshita Y, Kamada M, Nodera H, Suzuki H et al. Mutations of optineurin in amyotrophic lateral sclerosis. Nature. 2010;465:223–U109. doi:10.1038/nature08971. PMID:20428114
   PubMed Web of Science ®Google Scholar
• Ito Y, Ofengeim D, Najafov A, Das S, Saberi S, Li Y, Hitomi J, Zhu H, Chen H, Mayo L et al. RIPK1 mediates axonal degeneration by promoting inflammation and necroptosis in ALS. Science. 2016;353:603–608. doi:10.1126/science.aaf6803. PMID:27493188
   PubMed Web of Science ®Google Scholar
• Cirulli ET, Lasseigne BN, Petrovski S, Sapp PC, Dion PA, Leblond CS, Couthouis J, Lu YF, Wang Q, Krueger BJ et al. Exome sequencing in amyotrophic lateral sclerosis identifies risk genes and pathways. Science. 2015;347:1436–1441. doi:10.1126/science.aaa3650. PMID:25700176
   PubMed Web of Science ®Google Scholar
• Willoughby CE, Chan LLY, Herd S, Billingsley G, Noordeh N, Levin AV, Buys Y, Trope G, Sarfarazi M, Heon E. Defining the pathogenicity of optineurin in juvenile open-angle glaucoma. Invest Ophthalmol Vis Sci. 2004;45:3122–3130. doi:10.1167/iovs.04-0107. PMID:15326130
   PubMed Web of Science ®Google Scholar
• Mankouri J, Fragkoudis R, Richards KH, Wetherill LF, Harris M, Kohl A, Elliott RM, Macdonald A. Optineurin negatively regulates the induction of IFNbeta in response to RNA virus infection. PLoS Pathog. 2010;6:e1000778. doi:10.1371/journal.ppat.1000778. PMID:20174559
   PubMed Web of Science ®Google Scholar
• Nagabhushana A, Chalasani ML, Jain N, Radha V, Rangaraj N, Balasubramanian D, Swarup G. Regulation of endocytic trafficking of transferrin receptor by optineurin and its impairment by a glaucoma-associated mutant. BMC Cell Biol. 2010;11:4. doi:10.1186/1471-2121-11-4. PMID:20085643
   PubMed Web of Science ®Google Scholar
• Schwab C, Yu S, McGeer EG, McGeer PL. Optineurin in Huntington's disease intranuclear inclusions. Neurosci Lett. 2012;506:149–154. doi:10.1016/j.neulet.2011.10.070. PMID:22085693
   PubMed Web of Science ®Google Scholar
• Wiener R, Zhang X, Wang T, Wolberger C. The mechanism of OTUB1-mediated inhibition of ubiquitination. Nature. 2012;483:618–22. doi:10.1038/nature10911. PMID:22367539
   PubMed Web of Science ®Google Scholar
• Sato Y, Yamagata A, Goto-Ito S, Kubota K, Miyamoto R, Nakada S, Fukai S. Molecular basis of Lys-63-linked polyubiquitination inhibition by the interaction between human deubiquitinating enzyme OTUB1 and ubiquitin-conjugating enzyme UBC13. J Biol Chem. 2012;287:25860–25868. doi:10.1074/jbc.M112.364752. PMID:22679021
   PubMed Web of Science ®Google Scholar
• Kensche T, Tokunaga F, Ikeda F, Goto E, Iwai K, Dikic I. Analysis of nuclear factor-kappa B (NF-kappa B) essential modulator (NEMO) binding to linear and lysine-linked ubiquitin chains and its role in the activation of NF-kappa B. J Biol Chem. 2012;287:23626–23634. doi:10.1074/jbc.M112.347195. PMID:22605335
   PubMed Web of Science ®Google Scholar
• Yoshikawa A, Sato Y, Yamashita M, Mimura H, Yamagata A, Fukai S. Crystal structure of the NEMO ubiquitin-binding domain in complex with Lys 63-linked di-ubiquitin. FEBS Lett. 2009;583:3317–3322. doi:10.1016/j.febslet.2009.09.028. PMID:19766637
   PubMed Web of Science ®Google Scholar
• Nakazawa S, Oikawa D, Ishii R, Ayaki T, Takahashi H, Takeda H, Ishitani R, Kamei K, Takeyoshi I, Kawakami H et al. Linear ubiquitination is involved in the pathogenesis of optineurin-associated amyotrophic lateral sclerosis. Nat Commun. 2016;7. doi:10.1038/ncomms12547.
   Web of Science ®Google Scholar
• Gleason CE, Ordureau A, Gourlay R, Arthur JSC, Cohen P. Polyubiquitin binding to optineurin is required for optimal activation of TANK-binding kinase 1 and production of interferon beta. J Biol Chem. 2011;286:35663–35674. doi:10.1074/jbc.M111.267567. PMID:21862579
   PubMed Web of Science ®Google Scholar
• Hofmann RM, Pickart CM. In vitro assembly and recognition of Lys-63 polyubiquitin chains. J Biol Chem. 2001;276:27936–27943. doi:10.1074/jbc.M103378200. PMID:11369780
   PubMed Web of Science ®Google Scholar
• Piotrowski J, Beal R, Hoffman L, Wilkinson KD, Cohen RE, Pickart CM. Inhibition of the 26 S proteasome by polyubiquitin chains synthesized to have defined lengths. J Biol Chem. 1997;272:23712–23721. doi:10.1074/jbc.272.38.23712. PMID:9295315
   PubMed Web of Science ®Google Scholar
• Bax A, Grzesiek S. Methodological Advances in Protein Nmr. Acc Chem Res. 1993;26:131–138. doi:10.1021/ar00028a001.
   Web of Science ®Google Scholar
• DeLucas LJ, Bray TL, Nagy L, McCombs D, Chernov N, Hamrick D, Cosenza L, Belgovskiy A, Stoops B, Chait A. Efficient protein crystallization. J Struct Biol. 2003;142:188–206. doi:10.1016/S1047-8477(03)00050-9. PMID:12718931
   PubMed Web of Science ®Google Scholar
• Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Macromol Crystallogr, Pt A. 1997;276:307–326. doi:10.1016/S0076-6879(97)76066-X.
   Web of Science ®Google Scholar
• Storoni LC, McCoy AJ, Read RJ. Likelihood-enhanced fast rotation functions. Acta Crystallog, Sect D-Biol Crystallogr. 2004;60:432–438. doi:10.1107/S0907444903028956.
   PubMedGoogle Scholar
• Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr, Sect D-Biol Crystallogr. 2004;60:2126–2132. doi:10.1107/S0907444904019158.
   PubMed Web of Science ®Google Scholar
• Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr Sect D-Biol Crystallogr. 1997;53:240–255. doi:10.1107/S0907444996012255.
   PubMed Web of Science ®Google Scholar
• Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB, Snoeyink J, Richardson JS et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007;35:W375–W383. doi:10.1093/nar/gkm216. PMID:17452350
   PubMed Web of Science ®Google Scholar
• Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr Sect D-Biol Crystallogr. 2002;58:1948–1954. doi:10.1107/S0907444902016657.
   PubMed Web of Science ®Google Scholar
• Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013;8:2281–2308. doi:10.1038/nprot.2013.143. PMID:24157548
   PubMed Web of Science ®Google Scholar