Diversity of ubiquitin and ISG15 specificity among nairoviruses' viral ovarian tumor domain proteases

Journal of Virology

Volumn 87, Issue 7, 2013, Pages 3815-3827

  Capodagli, Glenn C ^a   Deaton, Michelle K ^a   Baker, Erica A ^a   Lumpkin, Ryan J ^a   Pegan, Scott D ^a,b  

^a UNIVERSITY OF DENVER   (United States)

^b UNIVERSITY OF DENVER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON STIMULATED GENE FACTOR 15 PROTEIN; PROTEIN; PROTEINASE; UBIQUITIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BUNYAVIRUS; CRYSTAL STRUCTURE; ENZYME SPECIFICITY; NAIRO VIRUS; NUCLEOTIDE SEQUENCE; OVARY TUMOR; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN DOMAIN; TYMOVIRUS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; CYTOKINES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NAIROVIRUS; PEPTIDE HYDROLASES; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; SUBSTRATE SPECIFICITY; UBIQUITIN; UBIQUITINS; VIRAL PROTEINS; VIRULENCE FACTORS;

ANIMALIA; BRASSICA RAPA SUBSP. RAPA; CRIMEAN-CONGO HEMORRHAGIC FEVER VIRUS; DUGBE VIRUS; NAIROVIRUS; TYMOVIRUS;

EID: 84875540102     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03252-12     Document Type: Article

References (59)

1. Karti SS, Odabasi Z, Korten V, Yilmaz M, Sonmez M, Caylan R, Akdogan E, Eren N, Koksal I, Ovali E, Erickson BR, Vincent MJ, Nichol ST, Comer JA, Rollin PE, Ksiazek TG. 2004. Crimean-Congo hemorrhagic fever in Turkey. Emerg. Infect. Dis. 10:1379-1384.
2. Mishra AC, Mehta M, Mourya DT, Gandhi S. 2011. Crimean-Congo haemorrhagic fever in India. Lancet 378:372.
3. Ozkaya E, Dincer E, Carhan A, Uyar Y, Ertek M, Whitehouse CA, Ozkul A. 2010. Molecular epidemiology of Crimean-Congo hemorrhagic fever virus in Turkey: occurrence of local topotype. Virus Res. 149:64-70.
4. World Health Organization. 2001. Crimean-Congo haemorrhagic fever: fact sheet. WHO Media Centre, World Health Organization, Geneva, Switzerland.
5. World Health Organization. 2003. Crimean-Congo haemorrhagic fever (CCHF) in Mauritania: update. World Health Organization, Geneva, Switzerland.
6. Nalca A, Whitehouse CA, Ergonul O, Whitehouse CA (ed). 2007. Crimean-Congo hemorrhagic fever. Springer, Dordrecht, Netherlands.
7. Burt FJ, Spencer DC, Leman PA, Patterson B, Swanepoel R. 1996. Investigation of tick-borne viruses as pathogens of humans in South Africa and evidence of Dugbe virus infection in a patient with prolonged thrombocytopenia. Epidemiol. Infect. 116:353-361.
8. Dandawate CN, Work TH, Webb JK, Shah KV. 1969. Isolation of Ganjam virus from a human case of febrile illness: a report of a laboratory infection and serological survey of human sera from three different states of India. Indian J. Med. Res. 57:975-982.
9. Marczinke BI, Nichol ST. 2002. Nairobi sheep disease virus, an important tick-borne pathogen of sheep and goats in Africa, is also present in Asia. Virology 303:146-151.
10. Sudeep AB, Jadi RS, Mishra AC. 2009. Ganjam virus. Indian J. Med. Res. 130:514-519.
11. Sang R, Onyango C, Gachoya J, Mabinda E, Konongoi S, Ofula V, Dunster L, Okoth F, Coldren R, Tesh R, da Rossa AT, Finkbeiner S, Wang D, Crabtree M, Miller B. 2006. Tickborne arbovirus surveillance in market livestock, Nairobi, Kenya. Emerg. Infect. Dis. 12:1074-1080.
12. Steele GM, Nuttall PA. 1989. Difference in vector competence of two species of sympatric ticks, Amblyomma variegatum and Rhipicephalus appendiculatus, for Dugbe virus (Nairovirus, Bunyaviridae). Virus Res. 14: 73-84.
13. Dilcher M, Koch A, Hasib L, Dobler G, Hufert F, Weidmann M. 2012. Genetic characterization of Erve virus, a European nairovirus distantly related to Crimean-Congo hemorrhagic fever virus. Virus Genes 45:426-432.
14. Frias-Staheli N, Giannakopoulos NV, Kikkert M, Taylor SL, Bridgen A, Paragas J, Richt JA, Rowland RR, Schmaljohn CS, Lenschow DJ, Snijder EJ, Garcia-Sastre A, Virgin HW. 2007. Ovarian tumor domaincontaining viral proteases evade ubiquitin-and ISG15-dependent innate immune responses. Cell Host Microbe 2:404-416.
15. Bergeron E, Albarino CG, Khristova ML, Nichol ST. 2010. Crimean-Congo hemorrhagic fever virus-encoded ovarian tumor protease activity is dispensable for virus RNA polymerase function. J. Virol. 84:216-226.
16. Akutsu M, Ye Y, Virdee S, Chin JW, Komander D. 2010. Molecular basis for ubiquitin and ISG15 cross-reactivity in viral ovarian tumor domains. Proc. Natl. Acad. Sci. U. S. A. 108:2228-2233.
17. Capodagli GC, McKercher MA, Baker EA, Masters EM, Brunzelle JS, Pegan SD. 2011. Structural analysis of a viral ovarian tumor domain protease from the Crimean-Congo hemorrhagic fever virus in complex with covalently bonded ubiquitin. J. Virol. 85:3621-3630.
18. Edelmann MJ, Kessler BM. 2008. Ubiquitin and ubiquitin-like specific proteases targeted by infectious pathogens: emerging patterns and molecular principles. Biochim. Biophys. Acta 1782:809-816.
19. Bridgen A, Weber F, Fazakerley JK, Elliott RM. 2001. Bunyamwera bunyavirus nonstructural protein NSs is a nonessential gene product that contributes to viral pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 98:664-669.
20. Giorgi C, Accardi L, Nicoletti L, Gro MC, Takehara K, Hilditch C, Morikawa S, Bishop DH. 1991. Sequences and coding strategies of the S RNAs of Toscana and Rift Valley fever viruses compared to those of Punta Toro, Sicilian sandfly fever, and Uukuniemi viruses. Virology 180:738-753.
21. Komander D, Rape M. 2012. The ubiquitin code. Annu. Rev. Biochem. 81:203-229.
22. Xu P, Duong DM, Seyfried NT, Cheng D, Xie Y, Robert J, Rush J, Hochstrasser M, Finley D, Peng J. 2009. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 137:133-145.
23. Matsumoto ML, Wickliffe KE, Dong KC, Yu C, Bosanac I, Bustos D, Phu L, Kirkpatrick DS, Hymowitz SG, Rape M, Kelley RF, Dixit VM. 2010. K11-linked polyubiquitination in cell cycle control revealed by a K11 linkage-specific antibody. Mol. Cell 39:477-484.
24. Arimoto K, Funami K, Saeki Y, Tanaka K, Okawa K, Takeuchi O, Akira S, Murakami Y, Shimotohno K. 2010. Polyubiquitin conjugation to NEMO by triparite motif protein 23 (TRIM23) is critical in antiviral defense. Proc. Natl. Acad. Sci. U. S. A. 107:15856-15861.
25. Huang H, Jeon MS, Liao L, Yang C, Elly C, Yates JR, III, Liu YC. 2010. K33-linked polyubiquitination of T cell receptor-zeta regulates proteolysis-independent T cell signaling. Immunity 33:60-70.
26. Shang F, Deng G, Liu Q, Guo W, Haas AL, Crosas B, Finley D, Taylor A. 2005. Lys6-modified ubiquitin inhibits ubiquitin-dependent protein degradation. J. Biol. Chem. 280:20365-20374.
27. Zucchelli S, Codrich M, Marcuzzi F, Pinto M, Vilotti S, Biagioli M, Ferrer I, Gustincich S. 2010. TRAF6 promotes atypical ubiquitination of mutant DJ-1 and alpha-synuclein and is localized to Lewy bodies in sporadic Parkinson's disease brains. Hum. Mol. Genet. 19:3759-3770.
28. Herrmann J, Lerman LO, Lerman A. 2007. Ubiquitin and ubiquitin-like proteins in protein regulation. Circ. Res. 100:1276-1291.
29. Pickart CM, Cohen RE. 2004. Proteasomes and their kin: proteases in the machine age. Nat. Rev. Mol. Cell. Biol. 5:177-187.
30. Versteeg GA, García-Sastre A. 2010. Viral tricks to grid-lock the type I interferon system. Curr. Opin. Microbiol. 13:508-516.
31. Weber F, Mirazimi A. 2008. Interferon and cytokine responses to Crimean Congo hemorrhagic fever virus; an emerging and neglected viral zoonosis. Cytokine Growth Factor Rev. 19:395-404.
32. Zhao C, Denison C, Huibregtse JM, Gygi S, Krug RM. 2005. Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc. Natl. Acad. Sci. U. S. A. 102:10200-10205.
33. Ha BH, Kim EE. 2008. Structures of proteases for ubiquitin and ubiquitin-like modifiers. BMB Rep. 41:435-443.
34. Peyrefitte CN, Perret M, Garcia S, Rodrigues R, Bagnaud A, Lacote S, Crance JM, Vernet G, Garin D, Bouloy M, Paranhos-Baccala G. 2010. Differential activation profiles of Crimean-Congo hemorrhagic fever virus-and Dugbe virus-infected antigen-presenting cells. J. Gen. Virol. 91: 189-198.
35. Rodrigues R, Paranhos-Baccala G, Vernet G, Peyrefitte CN. 2012. Crimean-Congo hemorrhagic fever virus-infected hepatocytes induce ER-stress and apoptosis crosstalk. PLoS One 7:e29712. doi:10.1371/journal.pone.0029712.
36. Holzer B, Bakshi S, Bridgen A, Baron MD. 2011. Inhibition of interferon induction and action by the nairovirus Nairobi sheep disease virus/Ganjam virus. PLoS One 6:e28594. doi:c1710.1371/journal.pone.0028594.
37. Bakshi S, Holzer B, Bridgen A, McMullan G, Quinn D, Baron MD. 2012. The Dugbe virus ovarian tumour (OTU) domain interferes with ubiquitin/ISG15-regulated innate immune cell signalling. J. Gen. Virol. 94:298-307.
38. Chenon M, Camborde L, Cheminant S, Jupin I. 2011. A viral deubiquitylating enzyme targets viral RNA-dependent RNA polymerase and affects viral infectivity. EMBO J. 31:741-753.
39. Zhang HM, Yang J, Sun HR, Xin X, Wang HD, Chen JP, Adams MJ. 2007. Genomic analysis of rice stripe virus Zhejiang isolate shows the presence of an OTU-like domain in the RNA1 protein and a novel sequence motif conserved within the intergenic regions of ambisense segments of tenuiviruses. Arch. Virol. 152:1917-1923.
40. Kim KI, Zhang DE. 2005. UBP43, an ISG15-specific deconjugating en-zyme: expression, purification, and enzymatic assays. Methods Enzymol. 398:491-499.
41. Messick TE, Russell NS, Iwata AJ, Sarachan KL, Shiekhattar R, Shanks JR, Reyes-Turcu FE, Wilkinson KD, Marmorstein R. 2008. Structural basis for ubiquitin recognition by the Otu1 ovarian tumor domain protein. J. Biol. Chem. 283:11038-11049.
42. Wilkinson KD, Gan-Erdene T, Kolli N. 2005. Derivitization of the C terminus of ubiquitin and ubiquitin-like proteins using intein chemistry: methods and uses. Methods Enzymol. 399:37-51.
43. Gill SC, von Hippel PH. 1989. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182:319-326.
44. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr. A 276:307-326.
45. Bailey S. 1994. The CCP4 Suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
46. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
47. James TW, Frias-Staheli N, Bacik JP, Levingston-Macleod JM, Khajehpour M, Garcia-Sastre A, Mark BL. 2011. Structural basis for the removal of ubiquitin and interferon-stimulated gene 15 by a viral ovarian tumor domain-containing protease. Proc. Natl. Acad. Sci. U. S. A. 108:2222-2227.
48. Deyde VM, Khristova ML, Rollin PE, Ksiazek TG, Nichol ST. 2006. Crimean-Congo hemorrhagic fever virus genomics and global diversity. J. Virol. 80:8834-8842.
49. Huang OW, Ma X, Yin J, Flinders J, Maurer T, Kayagaki N, Phung Q, Bosanac I, Arnott D, Dixit VM, Hymowitz SG, Starovasnik MA, Cochran AG. 2012. Phosphorylation-dependent activity of the deubiquitinase DUBA. Nat. Struct. Mol. Biol. 19:171-175.
50. van Kasteren PB, Beugeling C, Ninaber DK, Frias-Staheli N, van Boheemen S, Garcia-Sastre A, Snijder EJ, Kikkert M. 2012. Arterivirus and nairovirus ovarian tumor domain-containing deubiquitinases target activated RIG-I to control innate immune signaling. J. Virol. 86:773-785.
51. Treib J, Dobler G, Haass A, von Blohn W, Strittmatter M, Pindur G, Froesner G, Schimrigk K. 1998. Thunderclap headache caused by Erve virus? Neurology 50:509-511.
52. Sridharan H, Zhao C, Krug RM. 2010. Species specificity of the NS1 protein of influenza B virus: it binds only human and non-human primate ubiquitin-like ISG15 proteins. J. Biol. Chem. 258:7852-7856.
53. Versteeg GA, Hale BG, van Boheemen S, Wolff T, Lenschow DJ, García-Sastre A. 2010. Species-specific antagonism of host ISGylation by the influenza B virus NS1 protein. J. Virol. 84:5423-5430.
54. Bente D, Alimonti J, Shieh W, Camus G, Stroher U, Zaki S, Jones S. 2010. Pathogenesis and immune response of Crimean-Congo hemorrhagic fever virus in a STAT-1 knockout mouse model. J. Virol. 84:11089.
55. Woessner R, Grauer MT, Langenbach J, Dobler G, Kroeger J, Mielke HG, Mueller P, Haass A, Treib J. 2000. The Erve virus: possible mode of transmission and reservoir. Infection 28:164-166.
56. Barretto N, Jukneliene D, Ratia K, Chen Z, Mesecar AD, Baker SC. 2005. The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity. J. Virol. 79:15189-15198.
57. Ratia K. 2008. Structure, function, and inhibition of the papain-like protease from SARS coronavirus. Ph.D. thesis. University of Illinois, Chicago, IL.
58. Schlieker C, Weihofen WA, Frijns E, Kattenhorn LM, Gaudet R, Ploegh HL. 2007. Structure of a herpesvirus-encoded cysteine protease reveals a unique class of deubiquitinating enzymes. Mol. Cell 25:677-687.
59. Bogunovic D, Byun M, Durfee LA, Abhyankar A, Sanal O, Mansouri D, Salem S, Radovanovic I, Grant AV, Adimi P, Mansouri N, Okada S, Bryant VL, Kong XF, Kreins A, Velez MM, Boisson B, Khalilzadeh S, Ozcelik U, Darazam IA, Schoggins JW, Rice CM, Al-Muhsen S, Behr M, Vogt G, Puel A, Bustamante J, Gros P, Huibregtse JM, Abel L, Boisson-Dupuis S, Casanova JL. 2012. Mycobacterial disease and impaired IFNgamma immunity in humans with inherited ISG15 deficiency. Science 337:1684-1688.