Substrate recognition in selective autophagy and the ubiquitin-proteasome system

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 1, 2014, Pages 163-181

  Schreiber, Anne ^a   Peter, Matthias ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Posttranslational modification; Protein degradation; Selective autophagy; Substrate recognition; Ubiquitin proteasome system; Ubiquitination

Indexed keywords

ADAPTOR PROTEIN; CELL PROTEIN; DNA 26S; PROTEASOME; UBIQUITIN;

AUTOPHAGY; BACTERIUM; BINDING KINETICS; CELL VACUOLE; CYTOPLASM; ENZYME SUBSTRATE; HUMAN; MITOPHAGY; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SELECTIVE AUTOPHAGY; TRANSCRIPTION REGULATION; VIRUS;

EUKARYOTA;

EID: 84890178991     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.03.019     Document Type: Review

References (187)

1. Rabinowitz J.D., White E. Autophagy and metabolism. Science 2010, 330:1344-1348.
2. Bochtler M., Ditzel L., Groll M., Hartmann C., Huber R. The proteasome. Annu. Rev. Biophys. Biomol. Struct. 1999, 28:295-317.
3. Chuang C.K., Rockel B., Seyit G., Walian P.J., Schönegge A.-M., Peters J., Zwart P.H., Baumeister W., Jap B.K. Hybrid molecular structure of the giant protease tripeptidyl peptidase II. Nat. Struct. Mol. Biol. 2010, 17:990-996.
4. Demirel O., Jan I., Wolters D., Blanz J., Saftig P., Tampé R., Abele R. The lysosomal polypeptide transporter TAPL is stabilized by the interaction with LAMP-1 and LAMP-2. J. Cell Sci. 2012, 125(Pt18):4230-4240.
5. Peng J., Schwartz D., Elias J.E., Thoreen C.C., Cheng D., Marsischky G., Roelofs J., Finley D., Gygi S.P. A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 2003, 21:921-926.
6. Xu P., Duong D.M., Seyfried N.T., Cheng D., Xie Y., Robert J., Rush J., Hochstrasser M., Finley D., Peng J. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 2009, 137:133-145.
7. Komander D., Rape M. The ubiquitin code. Annu. Rev. Biochem. 2012, 81:203-229.
8. Husnjak K., Dikic I. Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 2012, 81:291-322.
9. Chau V., Tobias J.W., Bachmair A., Marriott D., Ecker D.J., Gonda D.K., Varshavsky A. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 1989, 243:1576-1583.
10. Thrower J.S., Hoffman L., Rechsteiner M., Pickart C.M. Recognition of the polyubiquitin proteolytic signal. EMBO J. 2000, 19:94-102.
11. Kirkpatrick D.S., Hathaway N.A., Hanna J., Elsasser S., Rush J., Finley D., King R.W., Gygi S.P. Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology. Nat. Cell Biol. 2006, 8:700-710.
12. Jin L., Williamson A., Banerjee S., Philipp I., Rape M. Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell 2008, 133:653-665.
13. Groll M., Ditzel L., Löwe J., Stock D., Bochtler M., Bartunik H.D., Huber R. Structure of 20S proteasome from yeast at 24 A resolution. Nature 1997, 386:463-471.
14. Wilk S., Orlowski M. Evidence that pituitary cation-sensitive neutral endopeptidase is a multicatalytic protease complex. J. Neurochem. 1983, 40:842-849.
15. Groll M., Bajorek M., Köhler A., Moroder L., Rubin D.M., Huber R., Glickman M.H., Finley D. A gated channel into the proteasome core particle. Nat. Struct. Biol. 2000, 7:1062-1067.
16. Beck F., Unverdorben P., Bohn S., Schweitzer A., Pfeifer G., Sakata E., Nickell S., Plitzko J.M., Villa E., Baumeister W., Förster F. Near-atomic resolution structural model of the yeast 26S proteasome. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:14870-14875.
17. da Fonseca P.C.A., Morris E.P. Structure of the human 26S proteasome: subunit radial displacements open the gate into the proteolytic core. J. Biol. Chem. 2008, 283:23305-23314.
18. Lander G.C., Estrin E., Matyskiela M.E., Bashore C., Nogales E., Martin A. Complete subunit architecture of the proteasome regulatory particle. Nature 2012, 482:186-191.
19. Smith D.M., Chang S.-C., Park S., Finley D., Cheng Y., Goldberg A.L. Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's alpha ring opens the gate for substrate entry. Mol. Cell 2007, 27:731-744.
20. Gillette T.G., Kumar B., Thompson D., Slaughter C.A., DeMartino G.N. Differential roles of the COOH termini of AAA subunits of PA700 (19S regulator) in asymmetric assembly and activation of the 26S proteasome. J. Biol. Chem. 2008, 283:31813-31822.
21. Riedinger C., Boehringer J., Trempe J.-F., Lowe E.D., Brown N.R., Gehring K., Noble M.E.M., Gordon C., Endicott J.A. Structure of Rpn10 and its interactions with polyubiquitin chains and the proteasome subunit Rpn12. J. Biol. Chem. 2010, 285:33992-34003.
22. Lasker K., Förster F., Bohn S., Walzthoeni T., Villa E., Unverdorben P., Beck F., Aebersold R., Sali A., Baumeister W. Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:1380-1387.
23. da Fonseca P.C.A., He J., Morris E.P. Molecular model of the human 26S proteasome. Mol. Cell 2012, 46:54-66.
24. Chen X., Lee B.-H., Finley D., Walters K.J. Structure of proteasome ubiquitin receptor hRpn13 and its activation by the scaffolding protein hRpn2. Mol. Cell 2010, 38:404-415.
25. He J., Kulkarni K., da Fonseca P.C.A., Krutauz D., Glickman M.H., Barford D., Morris E.P. The structure of the 26S proteasome subunit Rpn2 reveals its PC repeat domain as a closed toroid of two concentric α-helical rings. Structure 2012, 20:513-521.
26. Tian G., Park S., Lee M.J., Huck B., McAllister F., Hill C.P., Gygi S.P., Finley D. An asymmetric interface between the regulatory and core particles of the proteasome. Nat. Struct. Mol. Biol. 2011, 18:1259-1267.
27. Lam Y.A., Lawson T.G., Velayutham M., Zweier J.L., Pickart C.M. A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature 2002, 416:763-767.
28. Elsasser S., Gali R.R., Schwickart M., Larsen C.N., Leggett D.S., Müller B., Feng M.T., Tübing F., Dittmar G.A.G., Finley D. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nat. Cell Biol. 2002, 4:725-730.
29. Rosenzweig R., Bronner V., Zhang D., Fushman D., Glickman M.H. Rpn1 and Rpn2 coordinate ubiquitin processing factors at proteasome. J. Biol. Chem. 2012, 287:14659-14671.
30. Kaplun L., Tzirkin R., Bakhrat A., Shabek N., Ivantsiv Y., Raveh D. The DNA damage-inducible UbL-UbA protein Ddi1 participates in Mec1-mediated degradation of Ho endonuclease. Mol. Cell. Biol. 2005, 25:5355-5362.
31. Gomez T.A., Kolawa N., Gee M., Sweredoski M.J., Deshaies R.J. Identification of a functional docking site in the Rpn1 LRR domain for the UBA-UBL domain protein Ddi1. BMC Biol. 2011, 9:33.
32. Hamazaki J., Iemura S.-I., Natsume T., Yashiroda H., Tanaka K., Murata S. A novel proteasome interacting protein recruits the deubiquitinating enzyme UCH37 to 26S proteasomes. EMBO J. 2006, 25:4524-4536.
33. Rott R., Szargel R., Haskin J., Bandopadhyay R., Lees A.J., Shani V., Engelender S. α-Synuclein fate is determined by USP9X-regulated monoubiquitination. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:18666-18671.
34. Shabek N., Herman-Bachinsky Y., Buchsbaum S., Lewinson O., Haj-Yahya M., Hejjaoui M., Lashuel H.A., Sommer T., Brik A., Ciechanover A. The size of the proteasomal substrate determines whether its degradation will be mediated by mono- or polyubiquitylation. Mol. Cell 2012, 48(1):87-97.
35. Boutet S.C., Disatnik M.-H., Chan L.S., Iori K., Rando T.A. Regulation of Pax3 by proteasomal degradation of monoubiquitinated protein in skeletal muscle progenitors. Cell 2007, 130:349-362.
36. Dimova N.V., Hathaway N.A., Lee B.-H., Kirkpatrick D.S., Berkowitz M.L., Gygi S.P., Finley D., King R.W. APC/C-mediated multiple monoubiquitylation provides an alternative degradation signal for cyclin B1. Nat. Cell Biol. 2012, 14:168-176.
37. Takeuchi J., Chen H., Coffino P. Proteasome substrate degradation requires association plus extended peptide. EMBO J. 2007, 26:123-131.
38. Prakash S., Tian L., Ratliff K.S., Lehotzky R.E., Matouschek A. An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol. 2004, 11:830-837.
39. Prakash S., Inobe T., Hatch A.J., Matouschek A. Substrate selection by the proteasome during degradation of protein complexes. Nat. Chem. Biol. 2009, 5:29-36.
40. Inobe T., Fishbain S., Prakash S., Matouschek A. Defining the geometry of the two-component proteasome degron. Nat. Chem. Biol. 2011, 7:161-167.
41. Thurston T.L.M., Wandel M.P., von Muhlinen N., Foeglein A., Randow F. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 2012, 482:414-418.
42. Thurston T.L.M., 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.
43. Watson R.O., Manzanillo P.S., Cox J.S. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 2012, 150:803-815.
44. Orvedahl A., Sumpter R., Xiao G., Ng A., Zou Z., Tang Y., Narimatsu M., Gilpin C., Sun Q., Roth M., Forst C.V., Wrana J.L., Zhang Y.E., Luby-Phelps K., Xavier R.J., Xie Y., Levine B. Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 2011, 480:113-117.
45. Wang K., Klionsky D.J. Mitochondria removal by autophagy. Autophagy 2011, 7:297-300.
46. Farré J.-C., Manjithaya R., Mathewson R.D., Subramani S. PpAtg30 tags peroxisomes for turnover by selective autophagy. Dev. Cell 2008, 14:365-376.
47. Motley A.M., Nuttall J.M., Hettema E.H. Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. EMBO J. 2012, 31(13):2852-2868.
48. Bernales S., Schuck S., Walter P. ER-phagy: selective autophagy of the endoplasmic reticulum. Autophagy 2007, 3:285-287.
49. Kraft C., Deplazes A., Sohrmann M., Peter M. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 2008, 10:602-610.
50. Gibbings D., Mostowy S., Jay F., Schwab Y., Cossart P., Voinnet O. Selective autophagy degrades DICER and AGO2 and regulates miRNA activity. Nat. Cell Biol. 2012, (12):1314-1321.
51. Sandilands E., Serrels B., McEwan D.G., Morton J.P., Macagno J.P., McLeod K., Stevens C., Brunton V.G., Langdon W.Y., Vidal M., Sansom O.J., Dikic I., Wilkinson S., Frame M.C. Autophagic targeting of Src promotes cancer cell survival following reduced FAK signalling. Nat. Cell Biol. 2012, 14:51-60.
52. Cecconi F. c-Cbl targets active Src for autophagy. Nat. Cell Biol. 2010, 14:48-49.
53. Shi C.-S., Shenderov K., Huang N.-N., Kabat J., Abu-Asab M., Fitzgerald K.A., Sher A., Kehrl J.H. Activation of autophagy by inflammatory signals limits IL-1β production by targeting ubiquitinated inflammasomes for destruction. Nat. Immunol. 2012, 13:255-263.
54. Pohl C., Jentsch S. Midbody ring disposal by autophagy is a post-abscission event of cytokinesis. Nat. Cell Biol. 2009, 11:65-70.
55. Kuo T.-C., Chen C.-T., Baron D., Onder T.T., Loewer S., Almeida S., Weismann C.M., Xu P., Houghton J.-M., Gao F.-B., Daley G.Q., Doxsey S. Midbody accumulation through evasion of autophagy contributes to cellular reprogramming and tumorigenicity. Nat. Cell Biol. 2011, 13:1214-1223.
56. Hutchins M.U., Klionsky D.J. Vacuolar localization of oligomeric alpha-mannosidase requires the cytoplasm to vacuole targeting and autophagy pathway components in Saccharomyces cerevisiae. J. Biol. Chem. 2001, 276:20491-20498.
57. Scott S.V., Baba M., Ohsumi Y., Klionsky D.J. Aminopeptidase I is targeted to the vacuole by a nonclassical vesicular mechanism. J. Cell Biol. 1997, 138:37-44.
58. Scott S.V., Hefner-Gravink A., Morano K.A., Noda T., Ohsumi Y., Klionsky D.J. Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:12304-12308.
59. Baba M., Osumi M., Scott S.V., Klionsky D.J., Ohsumi Y. Two distinct pathways for targeting proteins from the cytoplasm to the vacuole/lysosome. J. Cell Biol. 1997, 139:1687-1695.
60. Harding T.M., Hefner-Gravink A., Thumm M., Klionsky D.J. Genetic and phenotypic overlap between autophagy and the cytoplasm to vacuole protein targeting pathway. J. Biol. Chem. 1996, 271:17621-17624.
61. Kim J., Scott S.V., Oda M.N., Klionsky D.J. Transport of a large oligomeric protein by the cytoplasm to vacuole protein targeting pathway. J. Cell Biol. 1997, 137:609-618.
62. Yuga M., Gomi K., Klionsky D.J., Shintani T. Aspartyl aminopeptidase is imported from the cytoplasm to the vacuole by selective autophagy in Saccharomyces cerevisiae. J. Biol. Chem. 2011, 286:13704-13713.
63. Suzuki K., Morimoto M., Kondo C., Ohsumi Y. Selective autophagy regulates insertional mutagenesis by the Ty1 retrotransposon in Saccharomyces cerevisiae. Dev. Cell 2011, 21:358-365.
64. Mijaljica D., Prescott M., Devenish R.J. Microautophagy in mammalian cells: revisiting a 40-year-old conundrum. Autophagy 2011, 7:673-682.
65. Arias E., Cuervo A.M. Chaperone-mediated autophagy in protein quality control. Curr. Opin. Cell Biol. 2011, 23:184-189.
66. Sahu R., Kaushik S., Clement C.C., Cannizzo E.S., Scharf B., Follenzi A., Potolicchio I., Nieves E., Cuervo A.M., Santambrogio L. Microautophagy of cytosolic proteins by late endosomes. Dev. Cell 2011, 20:131-139.
67. Tuttle D.L., Dunn W.A. Divergent modes of autophagy in the methylotrophic yeast Pichia pastoris. J. Cell Sci. 1995, 108(Pt 1):25-35.
68. Roberts P., Moshitch-Moshkovitz S., Kvam E., O'Toole E., Winey M., Goldfarb D.S. Piecemeal microautophagy of nucleus in Saccharomyces cerevisiae. Mol. Biol. Cell 2002, 14:129-141.
69. Krick R., Muehe Y., Prick T., Bremer S., Schlotterhose P., Eskelinen E.-L., Millen J., Goldfarb D.S., Thumm M. Piecemeal microautophagy of the nucleus requires the core macroautophagy genes. Mol. Biol. Cell 2008, 19:4492-4505.
70. Sandoval H., Thiagarajan P., Dasgupta S.K., Schumacher A., Prchal J.T., Chen M., Wang J. Essential role for Nix in autophagic maturation of erythroid cells. Nature 2008, 454:232-235.
71. Schweers R.L., Zhang J., Randall M.S., Loyd M.R., Li W., Dorsey F.C., Kundu M., Opferman J.T., Cleveland J.L., Miller J.L., Ney P.A. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19500-19505.
72. Cecconi F., Levine B. The role of autophagy in mammalian development: cell makeover rather than cell death. Dev. Cell 2008, 15. (14-14).
73. Wild P., Farhan H., McEwan D.G., Wagner S., Rogov V.V., Brady N.R., Richter B., Korac J., Waidmann O., Choudhary C., Dötsch V., Bumann D., Dikic I. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 2011, 333:228-233.
74. Das G., Shravage B.V., Baehrecke E.H. Regulation and function of autophagy during cell survival and cell death. Cold Spring Harb. Perspect. Biol. 2012, 4.
75. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
76. Nair U., Klionsky D.J. Molecular mechanisms and regulation of specific and nonspecific autophagy pathways in yeast. J. Biol. Chem. 2005, 280:41785-41788.
77. Lynch-Day M.A., Klionsky D.J. The Cvt pathway as a model for selective autophagy. FEBS Lett. 2010, 584:1359-1366.
78. Taherbhoy A.M., Tait S.W., Kaiser S.E., Williams A.H., Deng A., Nourse A., Hammel M., Kurinov I., Rock C.O., Green D.R., Schulman B.A. Atg8 transfer from Atg7 to Atg3: a distinctive E1-E2 architecture and mechanism in the autophagy pathway. Mol. Cell 2011, 44:451-461.
79. Yamaguchi M., Matoba K., Sawada R., Fujioka Y., Nakatogawa H., Yamamoto H., Kobashigawa Y., Hoshida H., Akada R., Ohsumi Y., Noda N.N., Inagaki F. Noncanonical recognition and UBL loading of distinct E2s by autophagy-essential Atg7. Nat. Struct. Mol. Biol. 2012, 19:1250-1256.
80. Geng J., Klionsky D.J. The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy "protein modifications: beyond the usual suspects" review series. EMBO Rep. 2008, 9:859-864.
81. Kaiser S.E., Mao K., Taherbhoy A.M., Yu S., Olszewski J.L., Duda D.M., Kurinov I., Deng A., Fenn T.D., Klionsky D.J., Schulman B.A. Noncanonical E2 recruitment by the autophagy E1 revealed by Atg7-Atg3 and Atg7-Atg10 structures. Nat. Struct. Mol. Biol. 2012, 19:1242-1249.
82. Hong S.B., Kim B.-W., Lee K.-E., Kim S.W., Jeon H., Kim J., Song H.K. Insights into noncanonical E1 enzyme activation from the structure of autophagic E1 Atg7 with Atg8. Nat. Struct. Mol. Biol. 2011, 18:1323-1330.
83. Satoo K., Noda N.N., 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. EMBO J. 2009, 28:1341-1350.
84. Nakatogawa H., Ishii J., Asai E., Ohsumi Y. Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis. Autophagy 2012, 8:177-186.
85. Kraft C., Kijanska M., Kalie E., Siergiejuk E., Lee S.S., Semplicio G., Stoffel I., Brezovich A., Verma M., Hansmann I., Ammerer G., Hofmann K., Tooze S., Peter M. Binding of the Atg1/ULK1 kinase to the ubiquitin-like protein Atg8 regulates autophagy. EMBO J. 2012, 31(18):3691-3703.
86. Nakatogawa H., Ohbayashi S., Sakoh-Nakatogawa M., Kakuta S., Suzuki S.W., Kirisako H., Kondo-Kakuta C., Noda N.N., Yamamoto H., Ohsumi Y. The autophagy-related protein kinase Atg1 interacts with the ubiquitin-like protein Atg8 via the Atg8 family interacting motif to facilitate autophagosome formation. J. Biol. Chem. 2012, 287(34):28503-28507.
87. Alemu E.A., Lamark T., Torgersen K.M., Birgisdottir A.B., Bowitz Larsen K., Jain A., Olsvik H., Øvervatn A., Kirkin V., Johansen T. ATG8 family proteins act as scaffolds for assembly of the ULK complex: sequence requirements for LC3-interacting region (LIR) motifs. J. Biol. Chem. 2012, 287(47):39275-39290.
88. Kraft C., Peter M., Hofmann K. Selective autophagy: ubiquitin-mediated recognition and beyond. Nat. Cell Biol. 2010, 12:836-841.
89. Johansen T., Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011, 7:279-296.
90. Okamoto K., Kondo-Okamoto N., Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 2009, 17:87-97.
91. Kirkin V., Lamark T., Sou Y.-S., Bjørkøy G., Nunn J.L., Bruun J.-A., Shvets E., McEwan D.G., Clausen T.H., Wild P., Bilusic I., Theurillat J.-P., Øvervatn A., Ishii T., Elazar Z., Komatsu M., Dikic I., Johansen T. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 2009, 33:505-516.
92. Shintani T., Huang W.-P., Stromhaug P.E., Klionsky D.J. Mechanism of cargo selection in the cytoplasm to vacuole targeting pathway. Dev. Cell 2002, 3:825-837.
93. Kondo-Okamoto N., Noda N.N., Suzuki S.W., Nakatogawa H., Takahashi I., Matsunami M., Hashimoto A., Inagaki F., Ohsumi Y., Okamoto K. Autophagy-related protein 32 acts as autophagic degron and directly initiates mitophagy. J. Biol. Chem. 2012, 287:10631-10638.
94. He C., Song H., Yorimitsu T., Monastyrska I., Yen W.-L., Legakis J.E., Klionsky D.J. Recruitment of Atg9 to the preautophagosomal structure by Atg11 is essential for selective autophagy in budding yeast. J. Cell Biol. 2006, 175:925-935.
95. Yamamoto H., Kakuta S., Watanabe T.M., Kitamura A., Sekito T., Kondo-Kakuta C., Ichikawa R., Kinjo M., Ohsumi Y. Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J. Cell Biol. 2012, 198:219-233.
96. Filimonenko M., Isakson P., Finley K.D., Anderson M., Jeong H., Melia T.J., Bartlett B.J., Myers K.M., Birkeland H.C.G., Lamark T., Krainc D., Brech A., Stenmark H., Simonsen A., Yamamoto A. The selective macroautophagic degradation of aggregated proteins requires the PI3P-binding protein Alfy. Mol. Cell 2010, 38. (15-15).
97. Deretic V. A master conductor for aggregate clearance by autophagy. Dev. Cell 2010, 18:694-696.
98. Kijanska M., Peter M. Atg1 kinase regulates early and late steps during autophagy. Autophagy 2012, 9.
99. Yamaguchi M., Noda N.N., Nakatogawa H., Kumeta H., Ohsumi Y., Inagaki F. Autophagy-related protein 8 (Atg8) family interacting motif in Atg3 mediates the Atg3-Atg8 interaction and is crucial for the cytoplasm-to-vacuole targeting pathway. J. Biol. Chem. 2010, 285:29599-29607.
100. Noda N.N., Kumeta H., Nakatogawa H., Satoo K., Adachi W., Ishii J., Fujioka Y., Ohsumi Y., Inagaki F. Structural basis of target recognition by Atg8/LC3 during selective autophagy. Genes Cells 2008, 13:1211-1218.
101. Liu L., Feng D., Chen G., Chen M., Zheng Q., Song P., Ma Q., Zhu C., Wang R., Qi W., Huang L., Xue P., Li B., Wang X., Jin H., Wang J., Yang F., Liu P., Zhu Y., Sui S., et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat. Cell Biol. 2012, 14:177-185.
102. von Muhlinen N., Akutsu M., Ravenhill B.J., Foeglein A., Bloor S., Rutherford T.J., Freund S.M.V., Komander D., Randow F. LC3C, bound selectively by a noncanonical LIR motif in NDP52, is required for antibacterial autophagy. Mol. Cell 2012, 48(3):329-342.
103. Kim P.K., Hailey D.W., Mullen R.T., Lippincott-Schwartz J. Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20567-20574.
104. Ravikumar B.B., Vacher C.C., Berger Z.Z., Davies J.E.J., Luo S.S., Oroz L.G.L., Scaravilli F.F., Easton D.F.D., Duden R.R., O'Kane C.J.C., Rubinsztein D.C.D. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 2004, 36:585-595.
105. Kamimoto T., Shoji S., Hidvegi T., Mizushima N., Umebayashi K., Perlmutter D.H., Yoshimori T. Intracellular inclusions containing mutant alpha1-antitrypsin Z are propagated in the absence of autophagic activity. J. Biol. Chem. 2006, 281:4467-4476.
106. Fortun J., Dunn W.A., Joy S., Li J., Notterpek L. Emerging role for autophagy in the removal of aggresomes in Schwann cells. J. Neurosci. 2003, 23:10672-10680.
107. Hara T., Nakamura K., Matsui M., Yamamoto A., Nakahara Y., Suzuki-Migishima R., Yokoyama M., Mishima K., Saito I., Okano H., Mizushima N. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006, 441:885-889.
108. Komatsu M., Waguri S., Chiba T., Murata S., Iwata J.-I., Tanida I., Ueno T., Koike M., Uchiyama Y., Kominami E., Tanaka K. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006, 441:880-884.
109. Bjørkøy G., Lamark T., Brech A., Outzen H., Perander M., Øvervatn A., Stenmark H., Johansen T. 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.
110. Komatsu M., Waguri S., Koike M., Sou Y.-S., Ueno T., Hara T., Mizushima N., Iwata J.-I., Ezaki J., Murata S., Hamazaki J., Nishito Y., Iemura S.-I., Natsume T., Yanagawa T., Uwayama J., Warabi E., Yoshida H., Ishii T., Kobayashi A., et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007, 131. (15-15).
111. Pankiv S., Clausen T.H., Lamark T., Brech A., Bruun J.-A., Outzen H., Øvervatn A., Bjørkøy G., Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 2007, 282:24131-24145.
112. Isogai S., Morimoto D., Arita K., Unzai S., Tenno T., Hasegawa J., Sou Y.-S., Komatsu M., Tanaka K., Shirakawa M., Tochio H. Crystal structure of the ubiquitin-associated (UBA) domain of p62 and its interaction with ubiquitin. J. Biol. Chem. 2011, 286:31864-31874.
113. Geisler S., Holmström K.M., Skujat D., Fiesel F.C., Rothfuss O.C., Kahle P.J., Springer W. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 2010, 12:119-131.
114. 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.
115. Lamark T., Perander M., Outzen H., Kristiansen K., Øvervatn A., Michaelsen E., Bjørkøy G., Johansen T. Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins. J. Biol. Chem. 2003, 278:34568-34581.
116. Ichimura Y., Kumanomidou T., Sou Y.-S., Mizushima T., Ezaki J., Ueno T., Kominami E., Yamane T., Tanaka K., Komatsu M. Structural basis for sorting mechanism of p62 in selective autophagy. J. Biol. Chem. 2008, 283:22847-22857.
117. Rozenknop A., Rogov V.V., Rogova N.Y., Löhr F., Güntert P., Dikic I., Dötsch V. Characterization of the interaction of GABARAPL-1 with the LIR motif of NBR1. J. Mol. Biol. 2011, 410:477-487.
118. Perrin A.J., Jiang X., Birmingham C.L., So N.S.Y., Brumell J.H. Recognition of bacteria in the cytosol of mammalian cells by the ubiquitin system. Curr. Biol. 2004, 14:806-811.
119. Cemma M., Kim P.K., Brumell J.H. The ubiquitin-binding adaptor proteins p62/SQSTM1 and NDP52 are recruited independently to bacteria-associated microdomains to target Salmonella to the autophagy pathway. Autophagy 2011, 7:341-345.
120. Zheng Y.T., Shahnazari S., Brech A., Lamark T., Johansen T., Brumell J.H. The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. J. Immunol. 2009, 183:5909-5916.
121. Kensche T., Tokunaga F., Ikeda F., Goto E., Iwai K., Dikic I. Analysis of nuclear factor-κB (NF-κB) essential modulator (NEMO) binding to linear and lysine-linked ubiquitin chains and its role in the activation of NF-κB. J. Biol. Chem. 2012, 287:23626-23634.
122. Olsen J.V., Blagoev B., Gnad F., Macek B., Kumar C., Mortensen P., Mann M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127:635-648.
123. Huttlin E.L., Jedrychowski M.P., Elias J.E., Goswami T., Rad R., Beausoleil S.A., Villén J., Haas W., Sowa M.E., Gygi S.P. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 2010, 143:1174-1189.
124. Kachaner D., Filipe J., Laplantine E., Bauch A., Bennett K.L., Superti-Furga G., Israël A., Weil R. Plk1-dependent phosphorylation of optineurin provides a negative feedback mechanism for mitotic progression. Mol. Cell 2012, 45:553-566.
125. 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.
126. Gleason C.E., Ordureau A., Gourlay R., Arthur J.S.C., Cohen P. Polyubiquitin binding to optineurin is required for optimal activation of TANK-binding kinase 1 and production of interferon β. J. Biol. Chem. 2011, 286:35663-35674.
127. Ryzhakov G., Randow F. SINTBAD, a novel component of innate antiviral immunity, shares a TBK1-binding domain with NAP1 and TANK. EMBO J. 2007, 26:3180-3190.
128. van Wijk S.J.L., Fiskin E., Putyrski M., Pampaloni F., Hou J., Wild P., Kensche T., Grecco H.E., 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.
129. Orvedahl A., MacPherson S., Sumpter R., Tallóczy Z., Zou Z., Levine B. Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe 2010, 7:115-127.
130. Novak I., Kirkin V., McEwan D.G., Zhang J., Wild P., Rozenknop A., Rogov V., Löhr F., Popovic D., Occhipinti A., Reichert A.S., Terzic J., Dötsch V., Ney P.A., Dikic I. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010, 11:45-51.
131. Schwarten M., Mohrlüder J., Ma P., Stoldt M., Thielmann Y., Stangler T., Hersch N., Hoffmann B., Merkel R., Willbold D. Nix directly binds to GABARAP: a possible crosstalk between apoptosis and autophagy. Autophagy 2009, 5:690-698.
132. Ding W.-X., Ni H.-M., Li M., Liao Y., Chen X., Stolz D.B., Dorn G.W., Yin X.-M. Nix is critical to two distinct phases of mitophagy, reactive oxygen species-mediated autophagy induction and Parkin-ubiquitin-p62-mediated mitochondrial priming. J. Biol. Chem. 2010, 285:27879-27890.
133. Suen D.-F., Narendra D.P., Tanaka A., Manfredi G., Youle R.J. Parkin overexpression selects against a deleterious mtDNA mutation in heteroplasmic cybrid cells. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:11835-11840.
134. Narendra D., Tanaka A., Suen D.-F., Youle R.J. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 2008, 183:795-803.
135. Park J., Lee S.B., Lee S., Kim Y., Song S., Kim S., Bae E., Kim J., Shong M., Kim J.-M., Chung J. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 2006, 441:1157-1161.
136. Narendra D.P., Jin S.M., Tanaka A., Suen D.-F., Gautier C.A., Shen J., Cookson M.R., Youle R.J. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010, 8:e1000298.
137. Matsuda N., Sato S., Shiba K., Okatsu K., Saisho K., Gautier C.A., Sou Y.-S., Saiki S., Kawajiri S., Sato F., Kimura M., Komatsu M., Hattori N., Tanaka K. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J. Cell Biol. 2010, 189:211-221.
138. Tanaka A., Cleland M.M., Xu S., Narendra D.P., Suen D.-F., Karbowski M., Youle R.J. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell Biol. 2010, 191:1367-1380.
139. Kim Y., Park J., Kim S., Song S., Kwon S.-K., Lee S.-H., Kitada T., Kim J.-M., Chung J. PINK1 controls mitochondrial localization of Parkin through direct phosphorylation. Biochem. Biophys. Res. Commun. 2008, 377:975-980.
140. Sha D., Chin L.-S., Li L. Phosphorylation of parkin by Parkinson disease-linked kinase PINK1 activates parkin E3 ligase function and NF-kappaB signaling. Hum. Mol. Genet. 2010, 19:352-363.
141. Shiba K., Arai T., Sato S., Kubo S.-I., Ohba Y., Mizuno Y., Hattori N. Parkin stabilizes PINK1 through direct interaction. Biochem. Biophys. Res. Commun. 2009, 383:331-335.
142. Um J.W., Stichel-Gunkel C., Lübbert H., Lee G., Chung K.C. Molecular interaction between parkin and PINK1 in mammalian neuronal cells. Mol. Cell. Neurosci. 2009, 40:421-432.
143. Gegg M.E., Cooper J.M., Chau K.-Y., Rojo M., Schapira A.H.V., Taanman J.-W. Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum. Mol. Genet. 2010, 19:4861-4870.
144. Wagner S.A., Beli P., Weinert B.T., Nielsen M.L., Cox J., Mann M., Choudhary C. A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol. Cell Proteomics 2011, 10.
145. Hanna R.A., Quinsay M.N., Orogo A.M., Giang K., Rikka S., Gustafsson Å.B. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J. Biol. Chem. 2012, 287:19094-19104.
146. Zhu Y., Massen S., Terenzio M., Lang V., Chen-Lindner S., Eils R., Novak I., Dikic I., Hamacher-Brady A., Brady N.R. Modulation of serines 17 and 24 in the LC3-interacting region of Bnip3 determines pro-survival mitophagy versus apoptosis. J. Biol. Chem. 2013, 288:1099-1113.
147. Kanki T., Wang K., Cao Y., Baba M., Klionsky D.J. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 2009, 17:98-109.
148. Kanki T., Klionsky D.J. Mitophagy in yeast occurs through a selective mechanism. J. Biol. Chem. 2008, 283:32386-32393.
149. Aoki Y., Kanki T., Hirota Y., Kurihara Y., Saigusa T., Uchiumi T., Kang D. Phosphorylation of Serine 114 on Atg32 mediates mitophagy. Mol. Biol. Cell 2011, 22:3206-3217.
150. Smolka M.B., Albuquerque C.P., Chen S.-H., Zhou H. Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:10364-10369.
151. Albuquerque C.P., Smolka M.B., Payne S.H., Bafna V., Eng J., Zhou H. A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol. Cell Proteomics 2008, 7:1389-1396.
152. Kissová I., Deffieu M., Manon S., Camougrand N. Uth1p is involved in the autophagic degradation of mitochondria. J. Biol. Chem. 2004, 279:39068-39074.
153. Tal R., Winter G., Ecker N., Klionsky D.J., Abeliovich H. Aup1p, a yeast mitochondrial protein phosphatase homolog, is required for efficient stationary phase mitophagy and cell survival. J. Biol. Chem. 2007, 282:5617-5624.
154. Umekawa M., Klionsky D.J. The cytoplasm-to-vacuole targeting pathway: a historical perspective. Int. J. Cell Biol. 2012, 2012:142634.
155. Watanabe Y., Noda N.N., Kumeta H., Suzuki K., Ohsumi Y., Inagaki F. Selective transport of alpha-mannosidase by autophagic pathways: structural basis for cargo recognition by Atg19 and Atg34. J. Biol. Chem. 2010, 285:30026-30033.
156. Scott S.V., Guan J., Hutchins M.U.M., Kim J., Klionsky D.J. Cvt19 is a receptor for the cytoplasm-to-vacuole targeting pathway. Mol. Cell 2001, 7. (11-11).
157. Suzuki K., Kondo C., Morimoto M., Ohsumi Y. Selective transport of alpha-mannosidase by autophagic pathways: identification of a novel receptor, Atg34p. J. Biol. Chem. 2010, 285:30019-30025.
158. Yorimitsu T., Klionsky D.J. Atg11 links cargo to the vesicle-forming machinery in the cytoplasm to vacuole targeting pathway. Mol. Biol. Cell 2005, 16:1593-1605.
159. Kim J., Kamada Y., Strømhaug P.E., Guan J., Hefner-Gravink A., Baba M., Scott S.V., Ohsumi Y., Dunn W.A., Klionsky D.J. Cvt9/Gsa9 functions in sequestering selective cytosolic cargo destined for the vacuole. J. Cell Biol. 2001, 153:381-396.
160. Till A., Lakhani R., Burnett S.F., Subramani S. Pexophagy: the selective degradation of peroxisomes. Int. J. Cell Biol. 2012, 2012:512721.
161. Pieuchot L., Jedd G. Peroxisome assembly and functional diversity in eukaryotic microorganisms. Annu. Rev. Microbiol. 2012, 66:237-263.
162. Yokota S., Dariush Fahimi H. Degradation of excess peroxisomes in mammalian liver cells by autophagy and other mechanisms. Histochem. Cell Biol. 2009, 131:455-458.
163. Kiel J.A.K.W., Komduur J.A., van der Klei I.J., Veenhuis M. Macropexophagy in Hansenula polymorpha: facts and views. FEBS Lett. 2003, 549:1-6.
164. Hara-Kuge S., Fujiki Y. The peroxin Pex14p is involved in LC3-dependent degradation of mammalian peroxisomes. Exp. Cell Res. 2008, 314:3531-3541.
165. Bellu A.R., Kram A.M., Kiel J.A., Veenhuis M., van der Klei I.J. Glucose-induced and nitrogen-starvation-induced peroxisome degradation are distinct processes in Hansenula polymorpha that involve both common and unique genes. FEMS Yeast Res. 2001, 1:23-31.
166. Hutchins M.U., Veenhuis M., Klionsky D.J. Peroxisome degradation in Saccharomyces cerevisiae is dependent on machinery of macroautophagy and the Cvt pathway. J. Cell Sci. 1999, 112(Pt 22):4079-4087.
167. Bellu A.R., Komori M., van der Klei I.J., Kiel J.A., Veenhuis M. Peroxisome biogenesis and selective degradation converge at Pex14p. J. Biol. Chem. 2001, 276:44570-44574.
168. Bellu A.R. Removal of Pex3p is an important initial stage in selective peroxisome degradation in Hansenula polymorpha. J. Biol. Chem. 2002, 277:42875-42880.
169. Zutphen T.V., Veenhuis M., van der Klei I.J. Pex14 is the sole component of the peroxisomal translocon that is required for pexophagy. Autophagy 2008, 4:63-66.
170. Munck J.M., Motley A.M., Nuttall J.M., Hettema E.H. A dual function for Pex3p in peroxisome formation and inheritance. J. Cell Biol. 2009, 187:463-471.
171. Nazarko T.Y., Farré J.-C., Subramani S. Peroxisome size provides insights into the function of autophagy-related proteins. Mol. Biol. Cell 2009, 20:3828-3839.
172. Kim W., Bennett E.J., Huttlin E.L., Guo A., Li J., Possemato A., Sowa M.E., Rad R., Rush J., Comb M.J., Harper J.W., Gygi S.P. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 2011, 44:325-340.
173. Cherra S.J., Kulich S.M., Uechi G., Balasubramani M., Mountzouris J., Day B.W., Chu C.T. Regulation of the autophagy protein LC3 by phosphorylation. J. Cell Biol. 2010, 190:533-539.
174. Jiang H., Cheng D., Liu W., Peng J., Feng J. Protein kinase C inhibits autophagy and phosphorylates LC3. Biochem. Biophys. Res. Commun. 2010, 395:471-476.
175. Molina H., Horn D.M., Tang N., Mathivanan S., Pandey A. Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:2199-2204.
176. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., Olsen J.V., Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
177. 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, 151:263-276.
178. Ucar A., Gupta S.K., Fiedler J., Erikci E., Kardasinski M., Batkai S., Dangwal S., Kumarswamy R., Bang C., Holzmann A., Remke J., Caprio M., Jentzsch C., Engelhardt S., Geisendorf S., Glas C., Hofmann T.G., Nessling M., Richter K., Schiffer M., et al. The miRNA-212/132 family regulates both cardiac hypertrophy and cardiomyocyte autophagy. Nat. Commun. 2012, 3. (1078-1078).
179. Pandey U.B., Nie Z., Batlevi Y., McCray B.A., Ritson G.P., Nedelsky N.B., Schwartz S.L., DiProspero N.A., Knight M.A., Schuldiner O., Padmanabhan R., Hild M., Berry D.L., Garza D., Hubbert C.C., Yao T.-P., Baehrecke E.H., Taylor J.P. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 2007, 447:859-863.
180. Iwata A., Riley B.E., Johnston J.A., Kopito R.R. HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J. Biol. Chem. 2005, 280:40282-40292.
181. Rideout H.J., Lang-Rollin I., Stefanis L. Involvement of macroautophagy in the dissolution of neuronal inclusions. Int. J. Biochem. Cell Biol. 2004, 36:2551-2562.
182. Suraweera A., Münch C., Hanssum A., Bertolotti A. Failure of amino acid homeostasis causes cell death following proteasome inhibition. Mol. Cell 2012.
183. Palombella V.J., Rando O.J., Goldberg A.L., Maniatis T. The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell 1994, 78:773-785.
184. Kroemer G., Mariño G., Levine B. Autophagy and the integrated stress response. Mol. Cell 2010, 40:280-293.
185. Korolchuk V.I., Mansilla A., Menzies F.M., Rubinsztein D.C. Autophagy inhibition compromises degradation of ubiquitin-proteasome pathway substrates. Mol. Cell 2009, 33:517-527.
186. Zhao J., Brault J.J., Schild A., Cao P., Sandri M., Schiaffino S., Lecker S.H., Goldberg A.L. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 2007, 6. (12-12).
187. Thielmann Y., Weiergräber O.H., Mohrlüder J., Willbold D. Structural framework of the GABARAP-calreticulin interface-implications for substrate binding to endoplasmic reticulum chaperones. FEBS J. 2009, 276:1140-1152.