Interferon-stimulated gene 15 (ISG15) and ISG15-linked proteins can associate with members of the selective autophagic process, histone deacetylase 6 (HDAC6) and SQSTM1/p62

Journal of Biological Chemistry

Volumn 290, Issue 3, 2015, Pages 1485-1495

  Nakashima, Hiroshi ^a   Nguyen, Tran ^a   Goins, William F ^b   Chiocca, Ennio Antonio ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BIOSYNTHESIS; GENES; GLYCOPROTEINS; INTERFERONS;

AUTOPHAGIC DEGRADATION; CONJUGATED PROTEINS; HISTONE DEACETYLASES; MOLECULAR EVENTS; PATHOGENIC PROTEINS; PROTEASOME INHIBITORS; SIGNALING EVENTS; SIGNALING TRANSDUCTION;

PROTEINS;

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CARRIER PROTEINS AND BINDING PROTEINS; HISTONE DEACETYLASE 6; INTERFERON STIMULATED GENE 15 PROTEIN; PROTEIN P62; PROTEOME; UNCLASSIFIED DRUG; BENZYLOXYCARBONYLLEUCYL-LEUCYL-LEUCINE ALDEHYDE; COMPLEMENTARY DNA; CYTOKINE; DOXYCYCLINE; HDAC6 PROTEIN, HUMAN; HISTONE DEACETYLASE; ISG15 PROTEIN, HUMAN; LEUPEPTIN; PROTEASOME INHIBITOR; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SQSTM1 PROTEIN, HUMAN; UBIQUITIN;

ARTICLE; AUTOPHAGY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOSOL; LYSOSOME; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; UBIQUITINATION; CHEMISTRY; FLUORESCENCE MICROSCOPY; HEK293 CELL LINE; HOMEOSTASIS; HUMAN; INNATE IMMUNITY; METABOLISM; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AUTOPHAGY; CYTOKINES; CYTOSOL; DNA, COMPLEMENTARY; DOXYCYCLINE; HEK293 CELLS; HISTONE DEACETYLASES; HOMEOSTASIS; HUMANS; IMMUNITY, INNATE; LEUPEPTINS; LYSOSOMES; MICROSCOPY, FLUORESCENCE; PROTEASOME INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEOME; SIGNAL TRANSDUCTION; UBIQUITINS;

EID: 84961288140     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.593871     Document Type: Article

References (42)

1. Sadler, A. J., and Williams, B. R. (2008) Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8, 559-568
2. Durfee, L. A., Lyon, N., Seo, K., and Huibregtse, J. M. (2010) The ISG15 conjugation system broadly targets newly synthesized proteins: implications for the antiviral function of ISG15. Mol. Cell 38, 722-732
3. Malakhov, M. P., Malakhova, O. A., Kim, K. I., Ritchie, K. J., and Zhang, D. E. (2002) UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J. Biol. Chem. 277, 9976-9981
4. Morales, D. J., and Lenschow, D. J. (2013) The antiviral activities of ISG15. J. Mol. Biol. 425, 4995-5008
5. Romijn, R. A., Westein, E., Bouma, B., Schiphorst, M. E., Sixma, J. J., Lenting, P. J., and Huizinga, E. G. (2003) Mapping the collagen-binding site in the von Willebrand factor-A3 domain. J. Biol. Chem. 278, 15035-15039
6. Liu, M., Li, X. L., and Hassel, B. A. (2003) Proteasomes modulate conjugation to the ubiquitin-like protein, ISG15. J. Biol. Chem. 278, 1594-1602
7. Schmeisser, H., Bekisz, J., and Zoon, K. C. (2014) New function of type I IFN: induction of autophagy. J. Interferon Cytokine Res. 34, 71-78
8. Johansen, T., and Lamark, T. (2011) Selective autophagy mediated by autophagic adapter proteins. Autophagy 7, 279-296
9. Shaid, S., Brandts, C. H., Serve, H., and Dikic, I. (2013) Ubiquitination and selective autophagy. Cell Death Differ. 20, 21-30
10. Lee, J. Y., Koga, H., Kawaguchi, Y., Tang, W., Wong, E., Gao, Y. S., Pandey, U. B., Kaushik, S., Tresse, E., Lu, J., Taylor, J. P., Cuervo, A. M., and Yao, T. P. (2010) HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J. 29, 969-980
11. Tan, J. M., Wong, E. S., Kirkpatrick, D. S., Pletnikova, O., Ko, H. S., Tay, S. P., Ho, M. W., Troncoso, J., Gygi, S. P., Lee, M. K., Dawson, V. L., Dawson, T. M., and Lim, K. L. (2008) Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum. Mol. Genet. 17, 431-439
12. Hao, R., Nanduri, P., Rao, Y., Panichelli, R. S., Ito, A., Yoshida, M., and Yao, T. P. (2013) Proteasomes activate aggresome disassembly and clearance by producing unanchored ubiquitin chains. Mol. Cell 51, 819-828
13. Pankiv, S., Clausen, T. H., Lamark, T., Brech, A., Bruun, J. A., Outzen, H., Øvervatn, A., Bjørkøy, G., and Johansen, T. (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24131-24145
14. Babu, J. R., Geetha, T., and Wooten, M. W. (2005) Sequestosome 1/p62 shuttles polyubiquitinated τ for proteasomal degradation. J. Neurochem. 94, 192-203
15. Long, J., Gallagher, T. R., Cavey, J. R., Sheppard, P. W., Ralston, S. H., Layfield, R., and Searle, M. S. (2008) Ubiquitin recognition by the ubiquitin-associated domain of p62 involves a novel conformational switch. J. Biol. Chem. 283, 5427-5440
16. Olzmann, J. A., Li, L., Chudaev, M. V., Chen, J., Perez, F. A., Palmiter, R. D., and Chin, L. S. (2007) Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6. J. Cell Biol. 178, 1025-1038
17. Kawaguchi, Y., Kovacs, J. J., McLaurin, A., Vance, J. M., Ito, A., and Yao, T. P. (2003) The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115, 727-738
18. Pai, M. T., Tzeng, S. R., Kovacs, J. J., Keaton, M. A., Li, S. S., Yao, T. P., and Zhou, P. (2007) Solution structure of the Ubp-M BUZ domain, a highly specific protein module that recognizes the C-terminal tail of free ubiquitin. J. Mol. Biol. 370, 290-302
19. Zuin, A., Carmona, M., Morales-Ivorra, I., Gabrielli, N., Vivancos, A. P., Ayté, J., and Hidalgo, E. (2010) Lifespan extension by calorie restriction relies on the Sty1 MAP kinase stress pathway. EMBO J. 29, 981-991
20. Haggarty, S. J., Koeller, K. M., Wong, J. C., Grozinger, C. M., and Schreiber, S. L. (2003) Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl. Acad. Sci. U.S.A. 100, 4389-4394
21. Szymczak, A. L., Workman, C. J., Wang, Y., Vignali, K. M., Dilioglou, S., Vanin, E. F., and Vignali, D. A. (2004) Correction of multi-gene deficiency in vivo using a single 'self-cleaving' 2A peptide-based retroviral vector. Nat. Biotechnol. 22, 589-594
22. Reyes-Turcu, F. E., Horton, J. R., Mullally, J. E., Heroux, A., Cheng, X., and Wilkinson, K. D. (2006) The ubiquitin binding domain ZnF UBP recognizes the C-terminal diglycine motif of unanchored ubiquitin. Cell 124, 1197-1208
23. Ouyang, H., Ali, Y. O., Ravichandran, M., Dong, A., Qiu, W., MacKenzie, F., Dhe-Paganon, S., Arrowsmith, C. H., and Zhai, R. G. (2012) Protein aggregates are recruited to aggresome by histone deacetylase 6 via unanchored ubiquitin C termini. J. Biol. Chem. 287, 2317-2327
24. Kirkin, V., McEwan, D. G., Novak, I., and Dikic, I. (2009) A role for ubiquitin in selective autophagy. Mol. Cell 34, 259-269
25. Seibenhener, M. L., Babu, J. R., Geetha, T., Wong, H. C., Krishna, N. R., and Wooten, M. W. (2004) Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol. Cell. Biol. 24, 8055-8068
26. Ye, Y., and Godzik, A. (2003) Flexible structure alignment by chaining aligned fragment pairs allowing twists. Bioinformatics 19, Suppl. 2, ii246-ii255
27. Narasimhan, J., Wang, M., Fu, Z., Klein, J. M., Haas, A. L., and Kim, J. J. (2005) Crystal structure of the interferon-induced ubiquitin-like protein ISG15. J. Biol. Chem. 280, 27356-27365
28. Komander, D., Reyes-Turcu, F., Licchesi, J. D., Odenwaelder, P., Wilkinson, K. D., and Barford, D. (2009) Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep. 10, 466-473
29. Trempe, J. F., Brown, N. R., Noble, M. E., and Endicott, J. A. (2010) A new crystal form of Lys48-linked diubiquitin. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66, 994-998
30. Potter, J. L., Narasimhan, J., Mende-Mueller, L., and Haas, A. L. (1999) Precursor processing of pro-ISG15/UCRP, an interferon-β-induced ubiquitin-like protein. J. Biol. Chem. 274, 25061-25068
31. Komatsu, M., Kurokawa, H., Waguri, S., Taguchi, K., Kobayashi, A., Ichimura, Y., Sou, Y. S., Ueno, I., Sakamoto, A., Tong, K. I., Kim, M., Nishito, Y., Iemura, S., Natsume, T., Ueno, T., Kominami, E., Motohashi, H., Tanaka, K., and Yamamoto, M. (2010) The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol. 12, 213-223
32. Itakura, E., and Mizushima, N. (2011) p62 Targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding. J. Cell Biol. 192, 17-27
33. Searle, M. S., Garner, T. P., Strachan, J., Long, J., Adlington, J., Cavey, J. R., Shaw, B., and Layfield, R. (2012) Structural insights into specificity and diversity in mechanisms of ubiquitin recognition by ubiquitin-binding domains. Biochem. Soc. Trans. 40, 404-408
34. Wooten, M. W., Geetha, T., Babu, J. R., Seibenhener, M. L., Peng, J., Cox, N., Diaz-Meco, M. T., and Moscat, J. (2008) Essential role of sequestosome 1/p62 in regulating accumulation of Lys63-ubiquitinated proteins. J. Biol. Chem. 283, 6783-6789
35. Lenschow, D. J., Giannakopoulos, N. V., Gunn, L. J., Johnston, C., O'Guin, A. K., Schmidt, R. E., Levine, B., and Virgin, H. W., 4th (2005) Identification of interferon-stimulated gene 15 as an antiviral molecule during Sindbis virus infection in vivo. J. Virol. 79, 13974-13983
36. Boyle, K. B., and Randow, F. (2013) The role of 'eat-me' signals and autophagy cargo receptors in innate immunity. Curr. Opin. Microbiol. 16, 339-348
37. Orvedahl, A., MacPherson, S., Sumpter, R., Jr., Tallóczy, Z., Zou, Z., and Levine, B. (2010) Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe 7, 115-127
38. Judith, D., Mostowy, S., Bourai, M., Gangneux, N., Lelek, M., Lucas-Hourani, M., Cayet, N., Jacob, Y., Prévost, M. C., Pierre, P., Tangy, F., Zimmer, C., Vidalain, P. O., Couderc, T., and Lecuit, M. (2013) Species-specific impact of the autophagy machinery on Chikungunya virus infection. EMBO Rep. 14, 534-544
39. Geeraert, C., Ratier, A., Pfisterer, S. G., Perdiz, D., Cantaloube, I., Rouault, A., Pattingre, S., Proikas-Cezanne, T., Codogno, P., and Poüs, C. (2010) Starvation-induced hyperacetylation of tubulin is required for the stimulation of autophagy by nutrient deprivation. J. Biol. Chem. 285, 24184-24194
40. Reed, N. A., Cai, D., Blasius, T. L., Jih, G. T., Meyhofer, E., Gaertig, J., and Verhey, K. J. (2006) Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 16, 2166-2172
41. Sanz, L., Diaz-Meco, M. T., Nakano, H., and Moscat, J. (2000) The atypical PKC-interacting protein p62 channels NF-κB activation by the IL-1-TRAF6 pathway. EMBO J. 19, 1576-1586
42. Shi, H. X., Yang, K., Liu, X., Liu, X. Y., Wei, B., Shan, Y. F., Zhu, L. H., and Wang, C. (2010) Positive regulation of interferon regulatory factor 3 activation by Herc5 via ISG15 modification. Mol. Cell. Biol. 30, 2424-2436