Two independent mechanisms promote expression of an N-terminal truncated USP18 isoform with higher deISGylation activity in the nucleus

Journal of Biological Chemistry

Volumn 287, Issue 7, 2012, Pages 4883-4893

  Burkart, Christoph ^a   Fan, Jun Bao ^a   Zhang, Dong Er ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CODING REGION; DOWN-REGULATION; ENZYMATIC ACTIVITIES; FULL-LENGTH PROTEINS; INITIATION EFFICIENCY; INITIATION SITES; INTERNAL RIBOSOME ENTRY SITE; ISOFORMS; N-TERMINALS; SUBCELLULAR DISTRIBUTION; TYPE I INTERFERONS;

BIOCHEMISTRY; BIOLOGY;

TISSUE;

MEMBRANE PROTEIN; PROTEIN USP18; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL FRACTIONATION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; START CODON; TRANSCRIPTION INITIATION SITE; TRANSLATION INITIATION;

CELL NUCLEUS; CODON, INITIATOR; ENDOPEPTIDASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEK293 CELLS; HELA CELLS; HUMANS; ISOENZYMES; JURKAT CELLS; PEPTIDE CHAIN INITIATION, TRANSLATIONAL;

EID: 84863127277     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.255570     Document Type: Article

References (62)

1. Pestka, S., Krause, C. D., and Walter, M. R. (2004) Interferons, interferon-like cytokines, and their receptors. Immunol. Rev. 202, 8-32 (Pubitemid 39576902)
2. Leaman, D. W., Chawla-Sarkar, M., Jacobs, B., Vyas, K., Sun, Y., Ozdemir, A., Yi, T., Williams, B. R., and Borden, E. C. (2003) Novel growth and death related interferon-stimulated genes (ISGs) in melanoma: greater potency of IFN-beta compared with IFN-α2. J. Interferon. Cytokine Res. 23, 745-756 (Pubitemid 38041446)
3. Borden, E. C., and Williams, B. R. (2011) Interferon-stimulated genes and their protein products: what and how? J. Interferon. Cytokine Res. 31, 1-4
4. Platanias, L. C., and Fish, E. N. (1999) Signaling pathways activated by interferons. Exp. Hematol. 27, 1583-1592 (Pubitemid 29526742)
5. Biron, C. A. (2001) Interferons α and β as immune regulators - a new look. Immunity 14, 661-664
6. Chawla-Sarkar, M., Lindner, D. J., Liu, Y. F., Williams, B. R., Sen, G. C., Silverman, R. H., and Borden, E. C. (2003) Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 8, 237-249 (Pubitemid 36749609)
7. Liu, L. Q., Ilaria, R., Jr., Kingsley, P. D., Iwama, A., van Etten, R. A., Palis, J., and Zhang, D. E. (1999) A novel ubiquitin-specific protease, UBP43, cloned from leukemia fusion protein AML1-ETO-expressing mice, functions in hematopoietic cell differentiation. Mol. Cell. Biol. 19, 3029-3038 (Pubitemid 29144548)
8. Schwer, H., Liu, L. Q., Zhou, L., Little, M. T., Pan, Z., Hetherington, C. J., and Zhang, D. E. (2000) Cloning and characterization of a novel human ubiquitin-specific protease, a homologue of murine UBP43 (Usp18). Genomics 65, 44-52 (Pubitemid 30249914)
9. 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 (Pubitemid 34968105)
10. Kim, K. I., and Zhang, D. E. (2005) UBP43, an ISG15-specific deconjugating enzyme: expression, purification, and enzymatic assays. Methods Enzymol. 398, 491-499
11. Ritchie, K. J., Hahn, C. S., Kim, K. I., Yan, M., Rosario, D., Li, L., de la Torre, J. C., and Zhang, D. E. (2004) Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat. Med. 10, 1374-1378 (Pubitemid 40022720)
12. Randall, G., Chen, L., Panis, M., Fischer, A. K., Lindenbach, B. D., Sun, J., Heathcote, J., Rice, C. M., Edwards, A. M., and McGilvray, I. D. (2006) Silencing of USP18 potentiates the antiviral activity of interferon against hepatitis C virus infection. Gastroenterology 131, 1584-1591 (Pubitemid 44708944)
13. Malakhova, O. A., Kim, K. I., Luo, J. K., Zou, W., Kumar, K. G., Fuchs, S. Y., Shuai, K., and Zhang, D. E. (2006) UBP43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. EMBO J. 25, 2358-2367 (Pubitemid 44012219)
14. Sarasin-Filipowicz, M., Wang, X., Yan, M., Duong, F. H., Poli, V., Hilton, D. J., Zhang, D. E., and Heim, M. H. (2009) α interferon induces long-lasting refractoriness of JAK-STAT signaling in the mouse liver through induction of USP18/UBP43. Mol. Cell. Biol. 29, 4841-4851
15. Kozak, M. (1999) Initiation of translation in prokaryotes and eukaryotes. Gene 234, 187-208
16. Kozak, M. (2002) Pushing the limits of the scanning mechanism for initiation of translation. Gene 299, 1-34
17. Harding, H. P., Novoa, I., Zhang, Y., Zeng, H., Wek, R., Schapira, M., and Ron, D. (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6, 1099-1108
18. Dever, T. E. (2002) Gene-specific regulation by general translation factors. Cell 108, 545-556
19. Sudhakar, A., Ramachandran, A., Ghosh, S., Hasnain, S. E., Kaufman, R. J., and Ramaiah, K. V. (2000) Phosphorylation of serine 51 in initiation factor 2 α (eIF2α) promotes complex formation between eIF2 α(P) and eIF2B and causes inhibition in the guanine nucleotide exchange activity of eIF2B. Biochemistry 39, 12929-12938
20. Roth, W., Wagenknecht, B., Dichgans, J., and Weller, M. (1998) Interferon- α enhances CD95L-induced apoptosis of human malignant glioma cells. J. Neuroimmunol. 87, 121-129 (Pubitemid 28319852)
21. Marissen, W. E., and Lloyd, R. E. (1998) Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells. Mol. Cell. Biol. 18, 7565-7574 (Pubitemid 28533075)
22. Dhar, D., Roy, S., and Das, S. (2007) Translational control of the interferon regulatory factor 2 mRNA by IRES element. Nucleic Acids Res. 35, 5409-5421 (Pubitemid 47423915)
23. Oumard, A., Hennecke, M., Hauser, H., and Nourbakhsh, M. (2000) Translation of NRF mRNA is mediated by highly efficient internal ribosome entry. Mol. Cell. Biol. 20, 2755-2759 (Pubitemid 30183494)
24. Kim, K. I., Giannakopoulos, N. V., Virgin, H. W., and Zhang, D. E. (2004) Interferon-inducible ubiquitin E2, Ubc8, is a conjugating enzyme for protein ISGylation. Mol. Cell. Biol. 24, 9592-9600 (Pubitemid 39391694)
25. Papa, F. R., and Hochstrasser, M. (1993) The yeast DOA4 gene encodes a deubiquitinating enzyme related to a product of the human tre-2 oncogene. Nature 366, 313-319 (Pubitemid 23349357)
26. Potu, H., Sgorbissa, A., and Brancolini, C. (2010) Identification of USP18 as an important regulator of the susceptibility to IFN-alpha and drug-induced apoptosis. Cancer Res. 70, 655-665
27. Wegrzyn, J. L., Drudge, T. M., Valafar, F., and Hook, V. (2008) Bioinformatic analyses of mammalian 5′-UTR sequence properties of mRNAs predicts alternative translation initiation sites. BMC Bioinformatics 9, 232
28. Schwab, S. R., Shugart, J. A., Horng, T., Malarkannan, S., and Shastri, N. (2004) Unanticipated antigens: translation initiation at CUG with leucine. PLoS Biol. 2, e366
29. Gerashchenko, M. V., Su, D., and Gladyshev, V. N. (2010) CUG start codon generates thioredoxin/glutathione reductase isoforms in mouse testes. J. Biol. Chem. 285, 4595-4602
30. Baird, S. D., Turcotte, M., Korneluk, R. G., and Holcik, M. (2006) Searching for IRES. RNA 12, 1755-1785 (Pubitemid 44484249)
31. Pelletier, J., and Sonenberg, N. (1985) Insertion mutagenesis to increase secondary structure within the 5′-noncoding region of a eukaryotic mRNA reduces translational efficiency. Cell 40, 515-526 (Pubitemid 15076569)
32. Kozak, M. (1986) Influences of mRNA secondary structure on initiation by eukaryotic ribosomes. Proc. Natl. Acad. Sci. U.S.A. 83, 2850-2854
33. Van Eden, M. E., Byrd, M. P., Sherrill, K. W., and Lloyd, R. E. (2004) Demonstrating internal ribosome entry sites in eukaryotic mRNAs using stringent RNA test procedures. RNA 10, 720-730 (Pubitemid 38405950)
34. Holcik, M., Graber, T., Lewis, S. M., Lefebvre, C. A., Lacasse, E., and Baird, S. (2005) Spurious splicing within the XIAP 5′ UTR occurs in the Rluc/ Fluc but not the betagal/CAT bicistronic reporter system. RNA 11, 1605-1609 (Pubitemid 41505533)
35. Spriggs, K. A., Bushell, M., Mitchell, S. A., and Willis, A. E. (2005) Internal ribosome entry segment-mediated translation during apoptosis: the role of IRES-trans-acting factors. Cell Death Differ 12, 585-591 (Pubitemid 40767161)
36. Lewis, S. M., and Holcik, M. (2008) For IRES trans-acting factors, it is all about location. Oncogene 27, 1033-1035 (Pubitemid 351253194)
37. Semler, B. L., and Waterman, M. L. (2008) IRES-mediated pathways to polysomes: nuclear versus cytoplasmic routes. Trends Microbiol. 16, 1-5
38. Rutkowski, D. T., and Kaufman, R. J. (2004) A trip to the ER: coping with stress. Trends Cell Biol. 14, 20-28 (Pubitemid 38076857)
39. Warnakulasuriyarachchi, D., Cerquozzi, S., Cheung, H. H., and Holcík, M. (2004) Translational induction of the inhibitor of apoptosis protein HIAP2 during endoplasmic reticulum stress attenuates cell death and is mediated via an inducible internal ribosome entry site element. J. Biol. Chem. 279, 17148-17157 (Pubitemid 38560471)
40. Gradi, A., Svitkin, Y. V., Imataka, H., and Sonenberg, N. (1998) Proteolysis of human eukaryotic translation initiation factor eIF4GII, but not eIF4GI, coincides with the shutoff of host protein synthesis after poliovirus infection. Proc. Natl. Acad. Sci. U.S.A. 95, 11089-11094 (Pubitemid 28450086)
41. Fernandez, J., Yaman, I., Sarnow, P., Snider, M. D., and Hatzoglou, M. (2002) Regulation of internal ribosomal entry site-mediated translation by phosphorylation of the translation initiation factor eIF2α. J. Biol. Chem. 277, 19198-19205 (Pubitemid 34952487)
42. Robert, F., Kapp, L. D., Khan, S. N., Acker, M. G., Kolitz, S., Kazemi, S., Kaufman, R. J., Merrick, W. C., Koromilas, A. E., Lorsch, J. R., and Pelletier, J. (2006) Initiation of protein synthesis by hepatitis C virus is refractory to reduced eIF2.GTP.Met-tRNA(i)(Met) ternary complex availability. Mol. Biol. Cell 17, 4632-4644 (Pubitemid 44665734)
43. Kim, J. H., Park, S. M., Park, J. H., Keum, S. J., and Jang, S. K. (2011) eIF2A mediates translation of hepatitis C viral mRNA under stress conditions. EMBO J. 30, 2454-2464
44. Zhu, Y., Lambert, K., Corless, C., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., and D'Andrea, A. D. (1997) DUB-2 is a member of a novel family of cytokine-inducible deubiquitinating enzymes. J. Biol. Chem. 272, 51-57 (Pubitemid 27021529)
45. Duex, J. E., and Sorkin, A. (2009)RNAinterference screen identifies Usp18 as a regulator of epidermal growth factor receptor synthesis. Mol. Biol. Cell 20, 1833-1844
46. Bonnet, M. E., Erbacher, P., and Bolcato-Bellemin, A. L. (2008) Systemic delivery of DNA or siRNA mediated by linear polyethylenimine (L-PEI) does not induce an inflammatory response. Pharm. Res. 25, 2972-2982
47. Kim, J. H., Luo, J. K., and Zhang, D. E. (2008) The level of hepatitis B virus replication is not affected by protein ISG15 modification but is reduced by inhibition of UBP43 (USP18) expression. J. Immunol. 181, 6467-6472
48. Fitzgerald, K. D., and Semler, B. L. (2009) Bridging IRES elements in mRNAs to the eukaryotic translation apparatus. Biochim. Biophys. Acta 1789, 518-528
49. Morris, D. R., and Geballe, A. P. (2000) Upstream open reading frames as regulators of mRNA translation. Mol. Cell. Biol. 20, 8635-8642 (Pubitemid 32245897)
50. Calkhoven, C. F., Müller, C., and Leutz, A. (2000) Translational control of C/EBPα and C/EBPβ isoform expression. Genes Dev. 14, 1920-1932 (Pubitemid 30639525)
51. Vattem, K. M., and Wek, R. C. (2004) Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 101, 11269-11274 (Pubitemid 39038336)
52. Peabody, D. S. (1989) Translation initiation at non-AUG triplets in mammalian cells. J. Biol. Chem. 264, 5031-5035
53. Hann, S. R., Dixit, M., Sears, R. C., and Sealy, L. (1994) The alternatively initiated c-Myc proteins differentially regulate transcription through a noncanonical DNA-binding site. Genes Dev. 8, 2441-2452 (Pubitemid 24323822)
54. Spotts, G. D., Patel, S. V., Xiao, Q., and Hann, S. R. (1997) Identification of downstream-initiated c-Myc proteins which are dominant-negative inhibitors of transactivation by full-length c-Myc proteins. Mol. Cell. Biol. 17, 1459-1468 (Pubitemid 27097375)
55. Jang, S. K., Kräusslich, H. G., Nicklin, M. J., Duke, G. M., Palmenberg, A. C., and Wimmer, E. (1988) A segment of the 5′ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol. 62, 2636-2643
56. Mokrejs, M., Vopálensky, V., Kolenaty, O., Masek, T., Feketová, Z., Sekyrová, P., Skaloudová, B., Kríz, V., and Pospísek, M. (2006) IRESite: the database of experimentally verified IRES structures (www.iresite.org). Nucleic Acids Res. 34, D125-D130
57. Stoneley, M., Subkhankulova, T., Le Quesne, J. P., Coldwell, M. J., Jopling, C. L., Belsham, G. J., and Willis, A. E. (2000) Analysis of the c-myc IRES; a potential role for cell-type specific trans-acting factors and the nuclear compartment. Nucleic Acids Res. 28, 687-694 (Pubitemid 30068251)
58. Komar, A. A., and Hatzoglou, M. (2011) Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle 10, 229-240
59. Palam, L. R., Baird, T. D., and Wek, R. C. (2011) Phosphorylation of eIF2 facilitates ribosomal bypass of an inhibitory upstream ORF to enhance CHOP translation. J. Biol. Chem. 286, 10939-10949
60. Sasaki, A., Inagaki-Ohara, K., Yoshida, T., Yamanaka, A., Sasaki, M., Yasukawa, H., Koromilas, A. E., and Yoshimura, A. (2003) The N-terminal truncated isoform of SOCS3 translated from an alternative initiation AUG codon under stress conditions is stable due to the lack of a major ubiquitination site, Lys-6. J. Biol. Chem. 278, 2432-2436 (Pubitemid 36801318)
61. 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
62. Lu, G., Reinert, J. T., Pitha-Rowe, I., Okumura, A., Kellum, M., Knobeloch, K. P., Hassel, B., and Pitha, P. M. (2006) ISG15 enhances the innate antiviral response by inhibition of IRF-3 degradation. Cell Mol. Biol. 52, 29-41 (Pubitemid 43925158)