Characterization of the polyproline region of the hepatitis E virus in immunocompromised patients

Journal of Virology

Volumn 88, Issue 20, 2014, Pages 12017-12025

  Lhomme, Sebastien ^a,b   Abravanel, Florence ^a,b   Dubois, Martine ^a,b   Sandres Saune, Karine ^a,b   Mansuy, Jean Michel ^b   Rostaing, Lionel ^a,c   Kamar, Nassim ^a,c   Izopet, Jacques ^a,b  

^a INSERM   (France)

^b CHU PURPAN   (France)

^c CHU RANGUEIL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

POLYPEPTIDE; POLYPROLINE; RNA DIRECTED RNA POLYMERASE; UNCLASSIFIED DRUG; PEPTIDE; PRIMER DNA;

ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; GENE; GENE INSERTION; GENE SEQUENCE; HEPATITIS E; HEPATITIS E VIRUS; HUMAN; IMMUNOCOMPROMISED PATIENT; IN VITRO STUDY; ITI GENE; MAJOR CLINICAL STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ACETYLATION; PROTEIN PHOSPHORYLATION; TAT GENE; UBIQUITINATION; VIROGENESIS; VIRUS GENOME; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS STRAIN; AMINO ACID SEQUENCE; CHEMISTRY; GENETICS; MOLECULAR GENETICS; ORGAN TRANSPLANTATION; PATHOGENICITY; POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BASE SEQUENCE; DNA PRIMERS; GENOME, VIRAL; HEPATITIS E VIRUS; HUMANS; IMMUNOCOMPROMISED HOST; MOLECULAR SEQUENCE DATA; ORGAN TRANSPLANTATION; PEPTIDES; POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84907438873     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01625-14     Document Type: Article

References (39)

1. Hoofnagle JH, Nelson KE, Purcell RH. 2012. Hepatitis E. N. Engl. J. Med. 367:1237-1244. http://dx.doi.org/10.1056/NEJMra1204512.
2. Kamar N, Bendall R, Legrand-Abravanel F, Xia NS, Ijaz S, Izopet J, Dalton HR. 2012. Hepatitis E. Lancet 379:2477-2488. http://dx.doi.org /10.1016/S0140-6736(11)61849-7.
3. Meng XJ, Anderson D, Arankalle A, Emerson S, Harrison TJ, Jameel S, Okamoto H. 2012. Hepeviridae, p 1021-1028. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (ed), Virus taxonomy: classification and nomenclature of viruses: ninth report of the International Committee of Taxonomy of Viruses. Elsevier, San Diego, CA.
4. Grandadam M, Tebbal S, Caron M, Siriwardana M, Larouze B, Koeck JL, Buisson Y, Enouf V, Nicand E. 2004. Evidence for hepatitis E virus quasispecies. J. Gen. Virol. 85:3189-3194. http://dx.doi.org/10.1099/vir.0.80248-0.
5. Holla RP, Ahmad I, Ahmad Z, Jameel S. 2013. Molecular virology of hepatitis E virus. Semin. Liver Dis. 33:3-14. http://dx.doi.org/10.1055/s-0033-1338110.
6. Kamar N, Selves J, Mansuy JM, Ouezzani L, Peron JM, Guitard J, Cointault O, Esposito L, Abravanel F, Danjoux M, Durand D, Vinel JP, Izopet J, Rostaing L. 2008. Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N. Engl. J. Med. 358:811-817. http://dx.doi.org/10.1056/NEJMoa0706992.
7. Lhomme S, Abravanel F, Dubois M, Sandres Saune K, Rostaing L, Kamar N, Izopet J. 2012. HEV quasispecies and the outcome of acute hepatitis E in solid-organ transplant patients. J. Virol. 86:10006-10014. http://dx.doi.org/10.1128/JVI.01003-12.
8. Lhomme S, Garrouste C, Kamar N, Sandres Saune K, Abravanel F, Mansuy JM, Dubois M, Rostaing L, Izopet J. 2014. Influence of polyproline region and macro domain genetic heterogeneity on HEV persistence in immunocompromised patients. J. Infect. Dis. 209:300-303.
9. Suneetha PV, Pischke S, Schlaphoff V, Grabowski J, Fytili P, Gronert A, Bremer B, Markova A, Jaroszewicz J, Bara C, Manns MP, Cornberg M, Wedemeyer H. 2012. Hepatitis E virus (HEV)-specific T-cell responses are associated with control of HEV infection. Hepatology 55:695-708.
10. Shukla P, Nguyen HT, Torian U, Engle RE, Faulk K, Dalton HR, Bendall RP, Keane FE, Purcell RH, Emerson SU. 2011. Cross-species infections of cultured cells by hepatitis E virus and discovery of an infectious virus-host recombinant. Proc. Natl. Acad. Sci. U. S. A. 108:2438-2443. http://dx.doi.org/10.1073/pnas.1018878108.
11. Shukla P, Nguyen HT, Faulk K, Mather K, Torian U, Engle RE, Emerson SU. 2012. Adaptation of a genotype 3 hepatitis E virus to efficient growth in cell culture depends on an inserted human gene segment acquired by recombination. J. Virol. 86:5697-5707. http://dx.doi.org/10.1128/JVI.00146-12.
12. Nguyen HT, Torian U, Faulk K, Mather K, Engle RE, Thompson E, Bonkovsky HL, Emerson SU. 2012. A naturally occurring human/hepatitis E recombinant virus predominates in serum but not in faeces of a chronic hepatitis E patient and has a growth advantage in cell culture. J. Gen. Virol. 93:526-530. http://dx.doi.org/10.1099/vir.0.037259-0.
13. Abravanel F, Sandres-Saune K, Lhomme S, Dubois M, Mansuy JM, Izopet J. 2012. Genotype 3 diversity and quantification of hepatitis E virus RNA. J. Clin. Microbiol. 50:897-902. http://dx.doi.org/10.1128/JCM.05942-11.
14. Legrand-Abravanel F, Mansuy JM, Dubois M, Kamar N, Peron JM, Rostaing L, Izopet J. 2009. Hepatitis E virus genotype 3 diversity, France. Emerg. Infect. Dis. 15:110-114. http://dx.doi.org/10.3201/eid 1501.080296.
15. Blom N, Gammeltoft S, Brunak S. 1999. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294: 1351-1362. http://dx.doi.org/10.1006/jmbi.1999.3310.
16. Shao J, Xu D, Tsai SN, Wang Y, Ngai SM. 2009. Computational identification of protein methylation sites through bi-profile Bayes feature extraction. PLoS One 4:e4920. http://dx.doi.org/10.1371/journal.pone.0004920.
17. Ward JJ, Sodhi JS, McGuffin LJ, Buxton BF, Jones DT. 2004. Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol. 337:635-645. http://dx.doi.org/10.1016/j.jmb.2004.02.002.
18. Izopet J, Dubois M, Bertagnoli S, Lhomme S, Marchandeau S, Boucher S, Kamar N, Abravanel F, Guérin JL. 2012. Hepatitis E virus strains in rabbits and evidence of a closely related strain in humans, France. Emerg. Infect. Dis. 18:1274-1281. http://dx.doi.org/10.3201/eid1808.120057.
19. Purdy MA, Lara J, Khudyakov YE. 2012. The hepatitis E virus polyproline region is involved in viral adaptation. PLoS One 7:e35974. http://dx.doi.org/10.1371/journal.pone.0035974.
20. Kamar N, Dalton HR, Abravanel F, Izopet J. 2014. Hepatitis E virus infection. Clin. Microbiol. Rev. 27:116-138. http://dx.doi.org/10.1128 /CMR.00057-13.
21. Pudupakam RS, Kenney SP, Cordoba L, Huang YW, Dryman BA, Leroith T, Pierson FW, Meng XJ. 2011. Mutational analysis of the hypervariable region of hepatitis E virus reveals its involvement in the efficiency of viral RNA replication. J. Virol. 85:10031-10040. http://dx.doi.org/10.1128/JVI.00763-11.
22. Pudupakam RS, Huang YW, Opriessnig T, Halbur PG, Pierson FW, Meng XJ. 2009. Deletions of the hypervariable region (HVR) in open reading frame 1 of hepatitis E virus do not abolish virus infectivity: evidence for attenuation of HVR deletion mutants in vivo. J. Virol. 83:384-395. http://dx.doi.org/10.1128/JVI.01854-08.
23. Koonin EV, Gorbalenya AE, Purdy MA, Rozanov MN, Reyes GR, Bradley DW. 1992. Computer-assisted assignment of functional domains in the nonstructural polyprotein of hepatitis E virus: delineation of an additional group of positive-strand RNA plant and animal viruses. Proc. Natl. Acad. Sci. U. S. A. 89:8259-8263. http://dx.doi.org/10.1073/pnas.89.17.8259.
24. Dyson HJ, Wright PE. 2005. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6:197-208. http://dx.doi.org/10.1038 /nrm1589.
25. Tompa P. 2003. Intrinsically unstructured proteins evolve by repeat expansion. Bioessays 25:847-855. http://dx.doi.org/10.1002/bies.10324.
26. Dietrich JB. 1992. Tyrosine aminotransferase: a transaminase among others? Cell. Mol. Biol. 38:95-114.
27. Bost F, Diarra-Mehrpour M, Martin JP. 1998. Inter-alpha-trypsin inhibitor proteoglycan family-a group of proteins binding and stabilizing the extracellular matrix. Eur. J. Biochem. 252:339-346. http://dx.doi.org /10.1046/j.1432-1327.1998.2520339.x.
28. Purdy MA. 18 July 2012. Evolution of the hepatitis E virus polyproline region: order from disorder. J. Virol. http://dx.doi.org/10.1128/JVI.01374-12.
29. López T, Silva-Ayala D, López S, Arias CF. 2011. Replication of the rotavirus genome requires an active ubiquitin-proteasome system. J. Virol. 85:11964-11971. http://dx.doi.org/10.1128/JVI.05286-11.
30. Si X, Gao G, Wong J, Wang Y, Zhang J, Luo H. 2008. Ubiquitination is required for effective replication of coxsackievirus B3. PLoS One 3:e2585. http://dx.doi.org/10.1371/journal.pone.0002585.
31. Karpe YA, Meng XJ. 2012. Hepatitis E virus replication requires an active ubiquitin-proteasome system. J. Virol. 86:5948-5952. http://dx.doi.org /10.1128/JVI.07039-11.
32. Wang X, Chuang HC, Li JP, Tan TH. 2012. Regulation of PKC-theta function by phosphorylation in T cell receptor signaling. Front. Immunol. 3:197. http://dx.doi.org/10.3389/fimmu.2012.00197.
33. Derouiche A, Cousin C, Mijakovic I. 2012. Protein phosphorylation from the perspective of systems biology. Curr. Opin. Biotechnol. 23:585-590. http://dx.doi.org/10.1016/j.copbio.2011.11.008.
34. Kim SJ, Kim JH, Kim YG, Lim HS, Oh JW. 2004. Protein kinase C-related kinase 2 regulates hepatitis C virus RNA polymerase function by phosphorylation. J. Biol. Chem. 279:50031-50041. http://dx.doi.org/10.1074/jbc.M408617200.
35. Glozak MA, Sengupta N, Zhang X, Seto E. 2005. Acetylation and deacetylation of non-histone proteins. Gene 363:15-23. http://dx.doi.org /10.1016/j.gene.2005.09.010.
36. Sterner DE, Berger SL. 2000. Acetylation of histones and transcriptionrelated factors. Microbiol. Mol. Biol. Rev. 64:435-459. http://dx.doi.org /10.1128/MMBR.64.2.435-459.2000.
37. Cereseto A, Manganaro L, Gutierrez MI, Terreni M, Fittipaldi A, Lusic M, Marcello A, Giacca M. 2005. Acetylation of HIV-1 integrase by p300 regulates viral integration. EMBO J. 24:3070-3081. http://dx.doi.org/10.1038/sj.emboj.7600770.
38. Lorenzo FR, Tanaka T, Takahashi H, Ichiyama K, Hoshino Y, Yamada K, Inoue J, Takahashi M, Okamoto H. 2008. Mutational events during the primary propagation and consecutive passages of hepatitis E virus strain JE03-1760F in cell culture. Virus Res. 137:86-96. http://dx.doi.org /10.1016/j.virusres.2008.06.005.
39. Bouquet J, Cheval J, Rogee S, Pavio N, Eloit M. 2012. Identical consensus sequence and conserved genomic polymorphism of hepatitis E virus during controlled interspecies transmission. J. Virol. 86:6238-6245. http: //dx.doi.org/10.1128/JVI.06843-11.