DnaJA1/Hsp40 is co-opted by influenza A virus to enhance its viral RNA polymerase activity

Journal of Virology

Volumn 88, Issue 24, 2014, Pages 14078-14089

  Cao, Mengmeng ^a   Wei, Candong ^a   Zhao, Lili ^a   Wang, Jingfeng ^a   Jia, Qiannan ^a   Wang, Xue ^a   Jin, Qi ^a   Deng, Tao ^a  

^a INSTITUTE OF PATHOGEN BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; POLYMERASE ACIDIC PROTEIN; POLYMERASE BASIC PROTEIN 1; POLYMERASE BASIC PROTEIN 2; PROTEIN DNAJ; PROTEIN DNAJA1; RIBONUCLEOPROTEIN; RNA POLYMERASE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA; DNAJA1 PROTEIN, HUMAN; RNA DIRECTED RNA POLYMERASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; EMBRYO; ENZYME ACTIVITY; ENZYME REGULATION; GENE TRANSLOCATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA VIRUS A; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA SYNTHESIS; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS REPLICATION; BIOSYNTHESIS; CELL LINE; ENZYMOLOGY; HOST PATHOGEN INTERACTION; INFLUENZA A VIRUS; METABOLISM; PHYSIOLOGY;

INFLUENZA A VIRUS;

CELL LINE; HOST-PATHOGEN INTERACTIONS; HSP40 HEAT-SHOCK PROTEINS; HUMANS; INFLUENZA A VIRUS; RNA REPLICASE; RNA, VIRAL; VIRUS REPLICATION;

EID: 84911478240     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02475-14     Document Type: Article

References (53)

1. Palese P, Shaw ML. 2013. Orthomyxoviridae: the viruses and their replication, p 1151-1185. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (ed), Fields virology, 6th ed, vol 1. Lippincott Williams and Wilkins, Philadelphia, PA.
2. Taubenberger JK, Reid AH, Lourens RM, Wang R, Jin G, Fanning TG. 2005. Characterization of the 1918 influenza virus polymerase genes. Nature 437:889-893. http://dx.doi.org/10.1038/nature04230.
3. Mänz B, Schwemmle M, Brunotte L. 2013. Adaptation of avian influenza A virus polymerase in mammals to overcome the host species barrier. J. Virol. 87:7200-7209. http://dx.doi.org/10.1128/JVI.00980-13.
4. Fodor E, Brownlee GG. 2002. Influenza virus replication, p 1-29. In Potter CW (ed), Influenza. Elsevier Science, New York, NY.
5. Biswas SK, Nayak DP. 1994. Mutational analysis of the conserved motifs of influenza A virus polymerase basic protein 1. J. Virol. 68:1819-1826.
6. Fechter P, Brownlee GG. 2005. Recognition of mRNA cap structures by viral and cellular proteins. J. Gen. Virol. 86:1239-1249. http://dx.doi.org/10.1099/vir.0.80755-0.
7. Guilligay D, Tarendeau F, Resa-Infante P, Coloma R, Crepin T, Sehr P, Lewis J, Ruigrok RW, Ortin J, Hart DJ, Cusack S. 2008. The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat. Struct. Mol. Biol. 15:500-506. http://dx.doi.org/10.1038/nsmb.1421.
8. Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, Baudin F, Cusack S, Ruigrok RW. 2009. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458:914-918. http://dx.doi.org/10.1038/nature07745.
9. Yuan P, Bartlam M, Lou Z, Chen S, Zhou J, He X, Lv Z, Ge R, Li X, Deng T, Fodor E, Rao Z, Liu Y. 2009. Crystal structure of an avian influenza polymerase PA (N) reveals an endonuclease active site. Nature 458:909-913. http://dx.doi.org/10.1038/nature07720.
10. Palese P, Shaw ML. 2013. Orthomyxoviridae, p 1151-1185. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (ed), Fields virology, 6th ed. Lippincott Williams and Wilkins, Philadelphia, PA.
11. Deng T, Sharps J, Fodor E, Brownlee GG. 2005. In vitro assembly of PB2 with a PB1-PA dimer supports a new model of assembly of influenza A virus polymerase subunits into a functional trimeric complex. J. Virol. 79:8669-8674. http://dx.doi.org/10.1128/JVI.79.13.8669-8674.2005.
12. Fodor E, Smith M. 2004. The PA subunit is required for efficient nuclear accumulation of the PB1 subunit of the influenza A virus RNA polymerase complex. J. Virol. 78:9144-9153. http://dx.doi.org/10.1128/JVI.78.17.9144-9153.2004.
13. Tafforeau L, Chantier T, Pradezynski F, Pellet J, Mangeot PE, Vidalain PO, Andre P, Rabourdin-Combe C, Lotteau V. 2011. Generation and comprehensive analysis of an influenza virus polymerase cellular interaction network. J. Virol. 85:13010-13018. http://dx.doi.org/10.1128/JVI.02651-10.
14. Jorba N, Juarez S, Torreira E, Gastaminza P, Zamarreno N, Albar JP, Ortin J. 2008. Analysis of the interaction of influenza virus polymerase complex with human cell factors. Proteomics 8:2077-2088. http://dx.doi.org/10.1002/pmic.200700508.
15. Bradel-Tretheway BG, Mattiacio JL, Krasnoselsky A, Stevenson C, Purdy D, Dewhurst S, Katze MG. 2011. Comprehensive proteomic analysis of influenza virus polymerase complex reveals a novel association with mitochondrial proteins and RNA polymerase accessory factors. J. Virol. 85:8569-8581. http://dx.doi.org/10.1128/JVI.00496-11.
16. Fodor E. 2013. The RNA polymerase of influenza A virus: mechanisms of viral transcription and replication. Acta Virol. 57:113-122. http://dx.doi.org/10.4149/av_2013_02_113.
17. Nagata K, Kawaguchi A, Naito T. 2008. Host factors for replication and transcription of the influenza virus genome. Rev. Med. Virol. 18:247-260. http://dx.doi.org/10.1002/rmv.575.
18. Gething MJ, Sambrook J. 1992. Protein folding in the cell. Nature 355: 33-45. http://dx.doi.org/10.1038/355033a0.
19. Young JC, Agashe VR, Siegers K, Hartl FU. 2004. Pathways of chaperone-mediated protein folding in the cytosol. Nat. Rev. Mol. Cell Biol. 5:781-791. http://dx.doi.org/10.1038/nrm1492.
20. Bukau B, Weissman J, Horwich A. 2006. Molecular chaperones and protein quality control. Cell 125:443-451. http://dx.doi.org/10.1016/j.cell.2006.04.014.
21. Hartl FU. 1996. Molecular chaperones in cellular protein folding. Nature 381:571-579. http://dx.doi.org/10.1038/381571a0.
22. Naito T, Momose F, Kawaguchi A, Nagata K. 2007. Involvement of Hsp90 in assembly and nuclear import of influenza virusRNApolymerase subunits. J. Virol. 81:1339-1349. http://dx.doi.org/10.1128/JVI.01917-06.
23. Momose F, Naito T, Yano K, Sugimoto S, Morikawa Y, Nagata K. 2002. Identification of Hsp90 as a stimulatory host factor involved in influenza virus RNA synthesis. J. Biol. Chem. 277:45306-45314. http://dx.doi.org/10.1074/jbc.M206822200.
24. Chase G, Deng T, Fodor E, Leung BW, Mayer D, Schwemmle M, Brownlee G. 2008. Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 377:431-439. http://dx.doi.org/10.1016/j.virol.2008.04.040.
25. Hirayama E, Atagi H, Hiraki A, Kim J. 2004. Heat shock protein 70 is related to thermal inhibition of nuclear export of the influenza virus ribonucleoprotein complex. J. Virol. 78:1263-1270. http://dx.doi.org/10.1128/JVI.78.3.1263-1270.2004.
26. Li G, Zhang J, Tong X, Liu W, Ye X. 2011. Heat shock protein 70 inhibits the activity of influenza A virus ribonucleoprotein and blocks the replication of virus in vitro and in vivo. PLoS One 6:e16546. http://dx.doi.org/10.1371/journal.pone.0016546.
27. Manzoor R, Kuroda K, Yoshida R, Tsuda Y, Fujikura D, Miyamoto H, Kajihara M, Kida H, Takada A. 2014. Heat shock protein 70 modulates influenza A virus polymerase activity. J. Biol. Chem. 289:7599-7614. http://dx.doi.org/10.1074/jbc.M113.507798.
28. Cheetham ME, Caplan AJ. 1998. Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones 3:28-36. http://dx.doi.org/10.1379/1466-1268(1998)003<0028:SFAEOD>2.3.CO;2.
29. Cyr DM, Langer T, Douglas MG. 1994. DnaJ-like proteins: molecular chaperones and specific regulators of Hsp70. Trends Biochem. Sci. 19: 176-181. http://dx.doi.org/10.1016/0968-0004(94)90281-X.
30. Qiu XB, Shao YM, Miao S, Wang L. 2006. The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell. Mol. Life Sci. 63:2560-2570. http://dx.doi.org/10.1007/s00018-006-6192-6.
31. Knox C, Luke GA, Blatch GL, Pesce ER. 2011. Heat shock protein 40 (Hsp40) plays a key role in the virus life cycle. Virus Res. 160:15-24. http://dx.doi.org/10.1016/j.virusres.2011.06.013.
32. Wang RY, Huang YR, Chong KM, Hung CY, Ke ZL, Chang RY. 2011. DnaJ homolog Hdj2 facilitates Japanese encephalitis virus replication. Virol. J. 8:471. http://dx.doi.org/10.1186/1743-422X-8-471.
33. Dziuba N, Ferguson MR, O'Brien WA, Sanchez A, Prussia AJ, Mc-Donald NJ, Friedrich BM, Li G, Shaw MW, Sheng J, Hodge TW, Rubin DH, Murray JL. 2012. Identification of cellular proteins required for replication of human immunodeficiency virus type 1. AIDS Res. Hum. Retroviruses 28:1329-1339. http://dx.doi.org/10.1089/aid.2011.0358.
34. Zhou Z, Cao M, Guo Y, Zhao L, Wang J, Jia X, Li J, Wang C, Gabriel G, Xue Q, Yi Y, Cui S, Jin Q, Deng T. 2014. Fragile X mental retardation protein stimulates ribonucleoprotein assembly of influenza A virus. Nat. Commun. 5:3259. http://dx.doi.org/10.1038/ncomms4259.
35. Wiśniewski JR, Zougman A, Nagaraj N, Mann M. 2009. Universal sample preparation method for proteome analysis. Nat. Methods 6:359-362. http://dx.doi.org/10.1038/nmeth.1322.
36. Fodor E, Crow M, Mingay LJ, Deng T, Sharps J, Fechter P, Brownlee GG. 2002. A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase inhibits endonucleolytic cleavage of capped RNAs. J. Virol. 76:8989-9001. http://dx.doi.org/10.1128/JVI.76.18.8989-9001.2002.
37. Vreede FT, Jung TE, Brownlee GG. 2004. Model suggesting that replication of influenza virus is regulated by stabilization of replicative intermediates. J. Virol. 78:9568-9572. http://dx.doi.org/10.1128/JVI.78.17.9568-9572.2004.
38. Deng T, Engelhardt OG, Thomas B, Akoulitchev AV, Brownlee GG, Fodor E. 2006. Role of Ran binding protein 5 in nuclear import and assembly of the influenza virus RNA polymerase complex. J. Virol. 80: 11911-11919. http://dx.doi.org/10.1128/JVI.01565-06.
39. Walker VE, Wong MJ, Atanasiu R, Hantouche C, Young JC, Shrier A. 2010. Hsp40 chaperones promote degradation of the HERG potassium channel. J. Biol. Chem. 285:3319-3329. http://dx.doi.org/10.1074/jbc.M109.024000.
40. Abisambra JF, Jinwal UK, Suntharalingam A, Arulselvam K, Brady S, Cockman M, Jin Y, Zhang B, Dickey CA. 2012. DnaJA1 antagonizes constitutive Hsp70-mediated stabilization of tau. J. Mol. Biol. 421:653-661. http://dx.doi.org/10.1016/j.jmb.2012.02.003.
41. Orthwein A, Zahn A, Methot SP, Godin D, Conticello SG, Terada K, Di Noia JM. 2012. Optimal functional levels of activation-induced deaminase specifically require the Hsp40 DnaJa1. EMBO J. 31:679-691.
42. Brownlee GG, Sharps JL. 2002. The RNA polymerase of influenza A virus is stabilized by interaction with its viral RNA promoter. J. Virol. 76:7103-7113. http://dx.doi.org/10.1128/JVI.76.14.7103-7113.2002.
43. Goodman AG, Smith JA, Balachandran S, Perwitasari O, Proll SC, Thomas MJ, Korth MJ, Barber GN, Schiff LA, Katze MG. 2007. The cellular protein P58IPK regulates influenza virus mRNA translation and replication through a PKR-mediated mechanism. J. Virol. 81:2221-2230. http://dx.doi.org/10.1128/JVI.02151-06.
44. Guan Z, Liu D, Mi S, Zhang J, Ye Q, Wang M, Gao GF, Yan J. 2010. Interaction of Hsp40 with influenza virus M2 protein: implications for PKR signaling pathway. Protein Cell 1:944-955.
45. Sharma K, Tripathi S, Ranjan P, Kumar P, Garten R, Deyde V, Katz JM, Cox NJ, Lal RB, Sambhara S, Lal SK. 2011. Influenza A virus nucleoprotein exploits Hsp40 to inhibit PKR activation. PLoS One 6:e20215. http://dx.doi.org/10.1371/journal.pone.0020215.
46. Li J, Qian X, Sha B. 2009. Heat shock protein 40: structural studies and their functional implications. Protein Pept. Lett. 16:606-612. http://dx.doi.org/10.2174/092986609788490159.
47. Li J, Qian X, Sha B. 2003. The crystal structure of the yeast Hsp40 Ydj1 complexed with its peptide substrate. Structure 11:1475-1483. http://dx.doi.org/10.1016/j.str.2003.10.012.
48. Hartl FU, Hayer-Hartl M. 2002. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852-1858. http://dx.doi.org/10.1126/science.1068408.
49. Hageman J, Rujano MA, van Waarde MA, Kakkar V, Dirks RP, Govorukhina N, Oosterveld-Hut HM, Lubsen NH, Kampinga HH. 2010. A DNAJB chaperone subfamily with HDAC-dependent activities suppresses toxic protein aggregation. Mol. Cell 37:355-369. http://dx.doi.org/10.1016/j.molcel.2010.01.001.
50. Lu Z, Cyr DM. 1998. The conserved carboxyl terminus and zinc fingerlike domain of the co-chaperone Ydj1 assist Hsp70 in protein folding. J. Biol. Chem. 273:5970-5978. http://dx.doi.org/10.1074/jbc.273.10.5970.
51. Jorba N, Area E, Ortin J. 2008. Oligomerization of the influenza virus polymerase complex in vivo. J. Gen. Virol. 89:520-524. http://dx.doi.org/10.1099/vir.0.83387-0.
52. Resa-Infante P, Recuero-Checa MA, Zamarreno N, Llorca O, Ortin J. 2010. Structural and functional characterization of an influenza virus RNA polymerase-genomic RNA complex. J. Virol. 84:10477-10487. http://dx.doi.org/10.1128/JVI.01115-10.
53. Honda A, Okamoto T, Ishihama A. 2007. Host factor Ebp1: selective inhibitor of influenza virus transcriptase. Genes Cells 12:133-142. http://dx.doi.org/10.1111/j.1365-2443.2007.01047.x.