The N-terminal domain of PA from bat-derived influenza-like virus H17N10 has endonuclease activity

Journal of Virology

Volumn 88, Issue 4, 2014, Pages 1935-1941

  Tefsen, Boris ^a   Lu, Guangwen ^a   Zhu, Yaohua ^a,b   Haywood, Joel ^a   Zhao, Lili ^c   Deng, Tao ^c   Qi, Jianxun ^a   Gao, George F ^a,d,e  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

^c INSTITUTE OF PATHOGEN BIOLOGY   (China)

^d INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^e CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BASE SEQUENCE; CHIROPTERA; CLONING, MOLECULAR; CLUSTER ANALYSIS; CRYSTALLOGRAPHY, X-RAY; DNA PRIMERS; ENDONUCLEASES; INFLUENZA A VIRUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN CONFORMATION; RNA REPLICASE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; VIRAL PROTEINS;

EID: 84893487875     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03270-13     Document Type: Article

References (31)

1. Taubenberger JK, Kash JC. 2010. Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 7:440-451. http://dx.doi.org/10.1016/j.chom.2010.05.009.
2. Runstadler J, Hill N, Hussein IT, Puryear W, Keogh M. 2013. Connecting the study of wild influenza with the potential for pandemic disease. Infect. Genet. Evol. 17:162-187. http://dx.doi.org/10.1016/j.meegid.2013.02.020.
3. Liu D, Shi W, Shi Y, Wang D, Xiao H, Li W, Bi Y, Wu Y, Li X, Yan J, Liu W, Zhao G, Yang W, Wang Y, Ma J, Shu Y, Lei F, Gao GF. 2013. Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet 381:1926-1932. http://dx.doi.org/10.1016/S0140-6736(13)60938-1.
4. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, Rimmelzwaan GF, Osterhaus AD, Fouchier RA. 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336:1534-1541. http://dx.doi.org/10.1126/science.1213362.
5. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, Shinya K, Zhong G, Hanson A, Katsura H, Watanabe S, Li C, Kawakami E, Yamada S, Kiso M, Suzuki Y, Maher EA, Neumann G, Kawaoka Y. 2012. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486:420-428. http://dx.doi.org/10.1038/nature10831.
6. Tong S, Li Y, Rivailler P, Conrardy C, Castillo DA, Chen LM, Recuenco S, Ellison JA, Davis CT, York IA, Turmelle AS, Moran D, Rogers S, Shi M, Tao Y, Weil MR, Tang K, Rowe LA, Sammons S, Xu X, Frace M, Lindblade KA, Cox NJ, Anderson LJ, Rupprecht CE, Donis RO. 2012. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. U.S.A. 109:4269-4274. http://dx.doi.org/10.1073/pnas.1116200109.
7. Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Carney PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO. 2013. New world bats harbor diverse influenza a viruses. PLoS Pathog. 9:e1003657. http://dx.doi.org/10.1371/journal.ppat.1003657.
8. Luis AD, Hayman DT, O'Shea TJ, Cryan PM, Gilbert AT, Pulliam JR, Mills JN, Timonin ME, Willis CK, Cunningham AA, Fooks AR, Rupprecht CE, Wood JL, Webb CT. 2013. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc. Biol. Sci. 280:20122753. http://dx.doi.org/10.1098/rspb.2012.2753.
9. Sun X, Shi Y, Lu X, He J, Gao F, Yan J, Qi J, Gao GF. 2013. Bat-derived influenza hemagglutinin H17 does not bind canonical avian or human receptors and most likely uses a unique entry mechanism. Cell Rep. 3:769-778. http://dx.doi.org/10.1016/j.celrep.2013.01.025.
10. Zhu X, Yu W, McBride R, Li Y, Chen LM, Donis RO, Tong S, Paulson JC, Wilson IA. 2013. Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc. Natl. Acad. Sci. U.S.A. 110:1458-1463. http://dx.doi.org/10.1073/pnas.1218509110.
11. Li Q, Sun X, Li Z, Liu Y, Vavricka CJ, Qi J, Gao GF. 2012. Structural and functional characterization of neuraminidase-like molecule N10 derived from bat influenza A virus. Proc. Natl. Acad. Sci. U.S.A. 109:18897-18902. http://dx.doi.org/10.1073/pnas.1211037109.
12. Zhu X, Yang H, Guo Z, Yu W, Carney PJ, Li Y, Chen LM, Paulson JC, Donis RO, Tong S, Stevens J, Wilson IA. 2012. Crystal structures of two subtype N10 neuraminidase-like proteins from bat influenza A viruses reveal a diverged putative active site. Proc. Natl. Acad. Sci. U.S.A. 109:18903-18908. http://dx.doi.org/10.1073/pnas.1212579109.
13. Sugiyama K, Obayashi E, Kawaguchi A, Suzuki Y, Tame JR, Nagata K, Park SY. 2009. Structural insight into the essential PB1-PB2 subunit contact of the influenza virus RNA polymerase. EMBO J. 28:1803-1811. http://dx.doi.org/10.1038/emboj.2009.138.
14. Obayashi E, Yoshida H, Kawai F, Shibayama N, Kawaguchi A, Nagata K, Tame JR, Park SY. 2008. The structural basis for an essential subunit interaction in influenza virus RNA polymerase. Nature 454:1127-1131. http://dx.doi.org/10.1038/nature07225.
15. He X, Zhou J, Bartlam M, Zhang R, Ma J, Lou Z, Li X, Li J, Joachimiak A, Zeng Z, Ge R, Rao Z, Liu Y. 2008. Crystal structure of the polymerase PA(C)-PB1(N) complex from an avian influenza H5N1 virus. Nature 454: 1123-1126. http://dx.doi.org/10.1038/nature07120.
16. 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.
17. 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.
18. Datta K, Wolkerstorfer A, Szolar OH, Cusack S, Klumpp K. 2013. Characterization of PA-N terminal domain of influenza A polymerase reveals sequence specificRNAcleavage. Nucleic Acids Res. 41:8289-8299. http://dx.doi.org/10.1093/nar/gkt603.
19. Noble E, Cox A, Deval J, Kim B. 2012. Endonuclease substrate selectivity characterized with full-length PA of influenza A virus polymerase. Virology 433:27-34. http://dx.doi.org/10.1016/j.virol.2012.07.008.
20. Kowalinski E, Zubieta C, Wolkerstorfer A, Szolar OH, Ruigrok RW, Cusack S. 2012. Structural analysis of specific metal chelating inhibitor binding to the endonuclease domain of influenza pH1N1 (2009) polymerase. PLoS Pathog. 8:e1002831. http://dx.doi.org/10.1371/journal.ppat.1002831.
21. Dubois RM, Slavish PJ, Baughman BM, Yun MK, Bao J, Webby RJ, Webb TR, White SW. 2012. Structural and biochemical basis for development of influenza virus inhibitors targeting the PA endonuclease. PLoS Pathog. 8:e1002830. http://dx.doi.org/10.1371/journal.ppat.1002830.
22. Puigbo P, Guzman E, Romeu A, Garcia-Vallve S. 2007. OPTIMIZER: a web server for optimizing the codon usage of DNA sequences. Nucleic Acids Res. 35:W126-131. http://dx.doi.org/10.1093/nar/gkm219.
23. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
24. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J. Appl. Crystallogr. 40: 658-674. http://dx.doi.org/10.1107/S0021889807021206.
25. Bailey S. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763. http://dx.doi.org/10.1107/S0907444994003112.
26. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132. http://dx.doi.org/10.1107/S0907444904019158.
27. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66: 213-221. http://dx.doi.org/10.1107/S0907444909052925.
28. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291. http://dx.doi.org/10.1107/S0021889892009944.
29. Gouet P, Courcelle E, Stuart DI, Metoz F. 1999. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15:305-308. http://dx.doi.org/10.1093/bioinformatics/15.4.305.
30. Zhao C, Lou Z, Guo Y, Ma M, Chen Y, Liang S, Zhang L, Chen S, Li X, Liu Y, Bartlam M, Rao Z. 2009. Nucleoside monophosphate complex structures of the endonuclease domain from the influenza virus polymerase PA subunit reveal the substrate binding site inside the catalytic center. J. Virol. 83:9024-9030. http://dx.doi.org/10.1128/JVI.00911-09.
31. Dlugolenski D, Jones L, Tompkins SM, Crameri G, Wang LF, Tripp RA. 2013. Bat cells from Pteropus alecto are susceptible to influenza A virus infection and reassortment. Influenza Other Respir. Viruses 7:900-903. http://dx.doi.org/10.1111/irv.12128.