Autophagic clearance of PolyQ proteins mediated by ubiquitin-Atg8 adaptors of the conserved CUET protein family

Cell

Volumn 158, Issue 3, 2014, Pages 549-563

  Lu, Kefeng ^a   Psakhye, Ivan ^a   Jentsch, Stefan ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; AUTOPHAGY PROTEIN 8; CUE DOMAIN PROTEIN 5; CUET PROTEIN; HUNTINGTIN; POLYGLUTAMINE; PROTEIN RSP5; TOLL INTERACTING PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; ATG8 PROTEIN, S CEREVISIAE; CUE5 PROTEIN, S CECEVISIAE; MICROTUBULE ASSOCIATED PROTEIN; PEPTIDE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TOLLIP PROTEIN, HUMAN;

ARTICLE; CONJUGATE; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; SELECTIVE AUTOPHAGY; SEQUENCE HOMOLOGY; UBIQUITINATION; AUTOPHAGY; METABOLISM; PROTEINOSIS;

EUKARYOTA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AUTOPHAGY; HUMANS; HUNTINGTON DISEASE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; PEPTIDES; PROTEIN AGGREGATION, PATHOLOGICAL; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITINATION;

EID: 84905491871     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.05.048     Document Type: Article

References (53)

1. G. Ankem, S. Mitra, F.R. Sun, A.C. Moreno, B. Chutvirasakul, H.F. Azurmendi, L.W. Li, and D.G.S. Capelluto The C2 domain of Tollip, a Toll-like receptor signalling regulator, exhibits broad preference for phosphoinositides Biochem. J. 435 2011 597 608
2. A. Bachmair, D. Finley, and A. Varshavsky In vivo half-life of a protein is a function of its amino-terminal residue Science 234 1986 179 186
3. K. Bagola, M. von Delbrück, G. Dittmar, M. Scheffner, I. Ziv, M.H. Glickman, A. Ciechanover, and T. Sommer Ubiquitin binding by a CUE domain regulates ubiquitin chain formation by ERAD E3 ligases Mol. Cell 50 2013 528 539
4. N.F. Bence, R.M. Sampat, and R.R. Kopito Impairment of the ubiquitin-proteasome system by protein aggregation Science 292 2001 1552 1555
5. G.M. Boratyn, A.A. Schäffer, R. Agarwala, S.F. Altschul, D.J. Lipman, and T.L. Madden Domain enhanced lookup time accelerated BLAST Biol. Direct 7 2012 12
6. D.G.S. Capelluto Tollip: a multitasking protein in innate immunity and protein trafficking Microbes Infect. 14 2012 140 147
7. B. Chen, J. Mariano, Y.C. Tsai, A.H. Chan, M. Cohen, and A.M. Weissman The activity of a human endoplasmic reticulum-associated degradation E3, gp78, requires its Cue domain, RING finger, and an E2-binding site Proc. Natl. Acad. Sci. USA 103 2006 341 346
8. A.M.K. Choi, S.W. Ryter, and B. Levine Autophagy in human health and disease N. Engl. J. Med. 368 2013 651 662
9. D.H. Cribbs, N.C. Berchtold, V. Perreau, P.D. Coleman, J. Rogers, A.J. Tenner, and C.W. Cotman Extensive innate immune gene activation accompanies brain aging, increasing vulnerability to cognitive decline and neurodegeneration: a microarray study J. Neuroinflammation 9 2012 179
10. H. Doi, K. Mitsui, M. Kurosawa, Y. Machida, Y. Kuroiwa, and N. Nukina Identification of ubiquitin-interacting proteins in purified polyglutamine aggregates FEBS Lett. 571 2004 171 176
11. K.M. Donaldson, H.W. Yin, N. Gekakis, F. Supek, and C.A.P. Joazeiro Ubiquitin signals protein trafficking via interaction with a novel ubiquitin binding domain in the membrane fusion regulator, Vps9p Curr. Biol. 13 2003 258 262
12. N.N. Fang, A.H. Ng, V. Measday, and T. Mayor Hul5 HECT ubiquitin ligase plays a major role in the ubiquitylation and turnover of cytosolic misfolded proteins Nat. Cell Biol. 13 2011 1344 1352
13. Y. Feng, D. He, Z. Yao, and D.J. Klionsky The machinery of macroautophagy Cell Res. 24 2014 24 41
14. D. Finley Recognition and processing of ubiquitin-protein conjugates by the proteasome Annu. Rev. Biochem. 78 2009 477 513
15. T. Hara, K. Nakamura, M. Matsui, A. Yamamoto, Y. Nakahara, R. Suzuki-Migishima, M. Yokoyama, K. Mishima, I. Saito, H. Okano, and N. Mizushima Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice Nature 441 2006 885 889
16. T. Hoppe, K. Matuschewski, M. Rape, S. Schlenker, H.D. Ulrich, and S. Jentsch Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing Cell 102 2000 577 586
17. D. Kaganovich, R. Kopito, and J. Frydman Misfolded proteins partition between two distinct quality control compartments Nature 454 2008 1088 1095
18. R.S. Kang, C.M. Daniels, S.A. Francis, S.C. Shih, W.J. Salerno, L. Hicke, and I. Radhakrishnan Solution structure of a CUE-ubiquitin complex reveals a conserved mode of ubiquitin binding Cell 113 2003 621 630
19. Y. Katoh, H. Imakagura, M. Futatsumori, and K. Nakayama Recruitment of clathrin onto endosomes by the Tom1-Tollip complex Biochem. Biophys. Res. Commun. 341 2006 143 149
20. Y.E. Kim, M.S. Hipp, A. Bracher, M. Hayer-Hartl, and F.U. Hartl Molecular chaperone functions in protein folding and proteostasis Annu. Rev. Biochem. 82 2013 323 355
21. V. Kirkin, T. Lamark, Y.S. Sou, G. Bjørkøy, J.L. Nunn, J.A. Bruun, E. Shvets, D.G. McEwan, T.H. Clausen, and P. Wild et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates Mol. Cell 33 2009 505 516
22. V. Kirkin, D.G. McEwan, I. Novak, and I. Dikic A role for ubiquitin in selective autophagy Mol. Cell 34 2009 259 269
23. D.J. Klionsky Autophagy: from phenomenology to molecular understanding in less than a decade Nat. Rev. Mol. Cell Biol. 8 2007 931 937
24. D.J. Klionsky, F.C. Abdalla, H. Abeliovich, R.T. Abraham, A. Acevedo-Arozena, K. Adeli, L. Agholme, M. Agnello, P. Agostinis, and J.A. Aguirre-Ghiso et al. Guidelines for the use and interpretation of assays for monitoring autophagy Autophagy 8 2012 445 544
25. M. Komatsu, S. Waguri, M. Koike, Y.S. Sou, T. Ueno, T. Hara, N. Mizushima, J. Iwata, J. Ezaki, and S. Murata et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice Cell 131 2007 1149 1163
26. C. Kraft, M. Peter, and K. Hofmann Selective autophagy: ubiquitin-mediated recognition and beyond Nat. Cell Biol. 12 2010 836 841
27. B. Levine, and G. Kroemer Autophagy in the pathogenesis of disease Cell 132 2008 27 42
28. B. Levine, N. Mizushima, and H.W. Virgin Autophagy in immunity and inflammation Nature 469 2011 323 335
29. M. Mann Functional and quantitative proteomics using SILAC Nat. Rev. Mol. Cell Biol. 7 2006 952 958
30. S. Mitra, C.A. Traughber, M.K. Brannon, S. Gomez, and D.G. Capelluto Ubiquitin interacts with the Tollip C2 and CUE domains and inhibits binding of Tollip to phosphoinositides J. Biol. Chem. 288 2013 25780 25791
31. N. Mizushima, T. Yoshimori, and Y. Ohsumi The role of Atg proteins in autophagosome formation Annu. Rev. Cell Dev. Biol. 27 2011 107 132
32. A.C. Moreno-Borchart, K. Strasser, M.G. Finkbeiner, A. Shevchenko, A. Shevchenko, and M. Knop Prospore membrane formation linked to the leading edge protein (LEP) coat assembly EMBO J. 20 2001 6946 6957
33. T. Noda, and Y. Ohsumi Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast J. Biol. Chem. 273 1998 3963 3966
34. A. Oguro, H. Kubota, M. Shimizu, S. Ishiura, and Y. Atomi Protective role of the ubiquitin binding protein Tollip against the toxicity of polyglutamine-expansion proteins Neurosci. Lett. 503 2011 234 239
35. Y. Ohsumi Molecular dissection of autophagy: two ubiquitin-like systems Nat. Rev. Mol. Cell Biol. 2 2001 211 216
36. S. Pankiv, T.H. Clausen, T. Lamark, A. Brech, J.A. Bruun, H. Outzen, A. Overvatn, G. Bjørkøy, and T. Johansen p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy J. Biol. Chem. 282 2007 24131 24145
37. S.H. Park, Y. Kukushkin, R. Gupta, T. Chen, A. Konagai, M.S. Hipp, M. Hayer-Hartl, and F.U. Hartl PolyQ proteins interfere with nuclear degradation of cytosolic proteins by sequestering the Sis1p chaperone Cell 154 2013 134 145
38. W. Piwko, and S. Jentsch Proteasome-mediated protein processing by bidirectional degradation initiated from an internal site Nat. Struct. Mol. Biol. 13 2006 691 697
39. C. Pohl, and S. Jentsch Midbody ring disposal by autophagy is a post-abscission event of cytokinesis Nat. Cell Biol. 11 2009 65 70
40. G. Prag, S. Misra, E.A. Jones, R. Ghirlando, B.A. Davies, B.F. Horazdovsky, and J.H. Hurley Mechanism of ubiquitin recognition by the CUE domain of Vps9p Cell 113 2003 609 620
41. T. Ravid, and M. Hochstrasser Diversity of degradation signals in the ubiquitin-proteasome system Nat. Rev. Mol. Cell Biol. 9 2008 679 690
42. V. Rogov, V. Dötsch, T. Johansen, and V. Kirkin Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy Mol. Cell 53 2014 167 178
43. D. Rotin, and S. Kumar Physiological functions of the HECT family of ubiquitin ligases Nat. Rev. Mol. Cell Biol. 10 2009 398 409
44. W. Seufert, and S. Jentsch Ubiquitin-conjugating enzymes UBC4 and UBC5 mediate selective degradation of short-lived and abnormal proteins EMBO J. 9 1990 543 550
45. S.C. Shih, G. Prag, S.A. Francis, M.A. Sutanto, J.H. Hurley, and L. Hicke A ubiquitin-binding motif required for intramolecular monoubiquitylation, the CUE domain EMBO J. 22 2003 1273 1281
46. M. Stefani, and C.M. Dobson Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution J. Mol. Med. 81 2003 678 699
47. O. Visvikis, L. Boyer, S. Torrino, A. Doye, M. Lemonnier, P. Lorès, M. Rolando, G. Flatau, A. Mettouchi, and D. Bouvard et al. Escherichia coli producing CNF1 toxin hijacks Tollip to trigger Rac1-dependent cell invasion Traffic 12 2011 579 590
48. C. Hoege, B. Pfander, G.L. Moldovan, G. Pyrowolakis, and S. Jentsch RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO Nature 419 2002 135 141
49. C. Janke, M.M. Magiera, N. Rathfelder, C. Taxis, S. Reber, H. Maekawa, A. Moreno-Borchart, G. Doenges, E. Schwob, E. Schiebel, and M. Knop A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes Yeast 21 2004 947 962
50. M. Knop, K. Siegers, G. Pereira, W. Zachariae, B. Winsor, K. Nasmyth, and E. Schiebel Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines Yeast 15 10B 1999 963 972
51. M. Sacher, B. Pfander, and S. Jentsch Identification of SUMO-protein conjugates Methods Enzymol. 399 2005 392 404
52. F. Sherman Getting started with yeast Methods Enzymol. 194 1991 3 21
53. H.D. Ulrich, and S. Jentsch Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair EMBO J. 19 2000 3388 3397