Phosphorylation controls the nuclear-cytoplasmic shuttling of influenza A virus nucleoprotein

Journal of Virology

Volumn 89, Issue 11, 2015, Pages 5822-5834

  Zheng, Weinan ^a,b   Li, Jing ^a   Wang, Shanshan ^a,i   Cao, Shuaishuai ^a,c   Jiang, Jingwen ^a,d   Chen, Can ^a,b   Ding, Chan ^e   Qin, Chuan ^f   Ye, Xin ^a,g   Gao, George F ^a,b,g,h   Liu, Wenjun ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c ANHUI UNIVERSITY   (China)

^d UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^e INSTITUTE OF PLANT PROTECTION   (China)

^f INSTITUTE OF LABORATORY ANIMAL SCIENCE   (China)

^g INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

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

ⁱ UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXPORTIN 1; KARYOPHERIN ALPHA; RNA POLYMERASE; VIRUS NUCLEOPROTEIN; CORE PROTEIN; NP PROTEIN, INFLUENZA A VIRUS; PROTEIN BINDING; RNA BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL CULTURE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; FEMALE; HUMAN; HUMAN CELL; INFLUENZA A; INFLUENZA VIRUS A; MOUSE; MOUSE MODEL; NONHUMAN; NUCLEAR CYTOPLASMIC SHUTTLING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; VIROGENESIS; VIRUS REPLICATION; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; CELL NUCLEUS; CONSERVED SEQUENCE; CYTOPLASM; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING;

INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

ALPHA KARYOPHERINS; ANIMALS; CELL LINE; CELL NUCLEUS; CONSERVED SEQUENCE; CYTOPLASM; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RNA-BINDING PROTEINS; VIRAL CORE PROTEINS;

EID: 84929630621     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00015-15     Document Type: Article

References (37)

1. Samji T. 2009. Influenza A: understanding the viral life cycle. Yale J Biol Med 82:153-159.
2. Portela A, Digard P. 2002. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J Gen Virol 83:723-734.
3. Coloma R, Valpuesta JM, Arranz R, Carrascosa JL, Ortin J, Martin-Benito J. 2009. The structure of a biologically active influenza virus ribonucleoprotein complex. PLoS Pathog 5:e1000491. http://dx.doi.org/10.1371/journal.ppat.1000491.
4. Hutchinson EC, Fodor E. 2012. Nuclear import of the influenza A virus transcriptional machinery. Vaccine 30:7353-7358. http://dx.doi.org/10.1016/j.vaccine.2012.04.085.
5. Whittaker G, Bui M, Helenius A. 1996. Nuclear trafficking of influenza virus ribonucleoproteins in heterokaryons. J Virol 70:2743-2756.
6. Wang P, Palese P, O'Neill RE. 1997. The NPI-1/NPI-3 (karyopherin alpha) binding site on the influenza A virus nucleoprotein NP is a nonconventional nuclear localization signal. J Virol 71:1850-1856.
7. Neumann G, Castrucci MR, Kawaoka Y. 1997. Nuclear import and export of influenza virus nucleoprotein. J Virol 71:9690-9700.
8. Davey J, Dimmock NJ, Colman A. 1985. Identification of the sequence responsible for the nuclear accumulation of the influenza virus nucleoprotein in Xenopus oocytes. Cell 40:667-675. http://dx.doi.org/10.1016/0092-8674(85)90215-6.
9. Yu M, Liu X, Cao S, Zhao Z, Zhang K, Xie Q, Chen C, Gao S, Bi Y, Sun L, Ye X, Gao GF, Liu W. 2012. Identification and characterization of three novel nuclear export signals in the influenza A virus nucleoprotein. J Virol 86:4970-4980. http://dx.doi.org/10.1128/JVI.06159-11.
10. Digard P, Elton D, Bishop K, Medcalf E, Weeds A, Pope B. 1999. Modulation of nuclear localization of the influenza virus nucleoprotein through interaction with actin filaments. J Virol 73:2222-2231.
11. Weber F, Kochs G, Gruber S, Haller O. 1998. A classical bipartite nuclear localization signal on Thogoto and influenza A virus nucleoproteins. Virology 250:9-18. http://dx.doi.org/10.1006/viro.1998.9329.
12. O'Neill RE, Jaskunas R, Blobel G, Palese P, Moroianu J. 1995. Nuclear import of influenza virusRNAcan be mediated by viral nucleoprotein and transport factors required for protein import. J Biol Chem 270:22701-22704. http://dx.doi.org/10.1074/jbc.270.39.22701.
13. Elton D, Simpson-Holley M, Archer K, Medcalf L, Hallam R, McCauley J, Digard P. 2001. Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J Virol 75:408-419. http://dx.doi.org/10.1128/JVI.75.1.408-419.2001.
14. Hutchinson EC, Denham EM, Thomas B, Trudgian DC, Hester SS, Ridlova G, York A, Turrell L, Fodor E. 2012. Mapping the phosphoproteome of influenza A and B viruses by mass spectrometry. PLoS Pathog 8:e1002993. http://dx.doi.org/10.1371/journal.ppat.1002993.
15. Wang S, Zhao Z, Bi Y, Sun L, Liu X, Liu W. 2013. Tyrosine 132 phosphorylation of influenza A virus M1 protein is crucial for virus replication by controlling the nuclear import of M1. J Virol 87:6182-6191. http://dx.doi.org/10.1128/JVI.03024-12.
16. Hsiang TY, Zhou L, Krug RM. 2012. Roles of the phosphorylation of specific serines and threonines in the NS1 protein of human influenza A viruses. J Virol 86:10370-10376. http://dx.doi.org/10.1128/JVI.00732-12.
17. Arrese M, Portela A. 1996. Serine 3 is critical for phosphorylation at the N-terminal end of the nucleoprotein of influenza virus A/Victoria/3/75. J Virol 70:3385-3391.
18. Mitzner D, Dudek SE, Studtrucker N, Anhlan D, Mazur I, Wissing J, Jansch L, Wixler L, Bruns K, Sharma A, Wray V, Henklein P, Ludwig S, Schubert U. 2009. Phosphorylation of the influenza A virus protein PB1-F2 by PKC is crucial for apoptosis promoting functions in monocytes. Cell Microbiol 11:1502-1516. http://dx.doi.org/10.1111/j.1462-5822.2009.01343.x.
19. Bullido R, Gomez-Puertas P, Albo C, Portela A. 2000. Several protein regions contribute to determine the nuclear and cytoplasmic localization of the influenza A virus nucleoprotein. J Gen Virol 81:135-142.
20. Bui M, Myers JE, Whittaker GR. 2002. Nucleo-cytoplasmic localization of influenza virus nucleoprotein depends on cell density and phosphorylation. Virus Res 84:37-44.http://dx.doi.org/10.1016/S0168-1702(01)00413-0.
21. Kumar N, Liang Y, Parslow TG, Liang Y. 2011. Receptor tyrosine kinase inhibitors block multiple steps of influenza A virus replication. J Virol 85:2818-2827. http://dx.doi.org/10.1128/JVI.01969-10.
22. Pleschka S, Wolff T, Ehrhardt C, Hobom G, Planz O, Rapp UR, Ludwig S. 2001. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signalling cascade. Nat Cell Biol 3:301-305. http://dx.doi.org/10.1038/35060098.
23. Kurokawa M, Ochiai H, Nakajima K, Niwayama S. 1990. Inhibitory effect of protein kinase C inhibitor on the replication of influenza type A virus. J Gen Virol 71:2149-2155. http://dx.doi.org/10.1099/0022-1317-71-9-2149.
24. Root CN, Wills EG, McNair LL, Whittaker GR. 2000. Entry of influenza viruses into cells is inhibited by a highly specific protein kinaseCinhibitor. J Gen Virol 81:2697-2705.
25. Chenavas S, Estrozi LF, Slama-Schwok A, Delmas B, Di Primo C, Baudin F, Li X, Crepin T, Ruigrok RW. 2013. Monomeric nucleoprotein of influenza A virus. PLoS Pathog 9:e1003275. http://dx.doi.org/10.1371/journal.ppat.1003275.
26. Turrell L, Hutchinson EC, Vreede FT, Fodor E. 2015. Regulation of influenza A virus nucleoprotein oligomerization by phosphorylation. J Virol 89:1452-1455. http://dx.doi.org/10.1128/JVI.02332-14.
27. Liu X, Sun L, Yu M, Wang Z, Xu C, Xue Q, Zhang K, Ye X, Kitamura Y, Liu W. 2009. Cyclophilin A interacts with influenza A virus M1 protein and impairs the early stage of the viral replication. Cell Microbiol 11:730-741. http://dx.doi.org/10.1111/j.1462-5822.2009.01286.x.
28. Neumann G, Watanabe T, Ito H, Watanabe S, Goto H, Gao P, Hughes M, Perez DR, Donis R, Hoffmann E, Hobom G, Kawaoka Y. 1999. Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci U S A 96:9345-9350. http://dx.doi.org/10.1073/pnas.96.16.9345.
29. Li Z, Watanabe T, Hatta M, Watanabe S, Nanbo A, Ozawa M, Kakugawa S, Shimojima M, Yamada S, Neumann G, Kawaoka Y. 2009. Mutational analysis of conserved amino acids in the influenza A virus nucleoprotein. J Virol 83:4153-4162. http://dx.doi.org/10.1128/JVI.02642-08.
30. Wang Z, Liu X, Zhao Z, Xu C, Zhang K, Chen C, Sun L, Gao GF, Ye X, Liu W. 2011. Cyclophilin E functions as a negative regulator to influenza virus replication by impairing the formation of the viral ribonucleoprotein complex. PLoS One 6:e22625. http://dx.doi.org/10.1371/journal.pone.0022625.
31. Boulo S, Akarsu H, Ruigrok RW, Baudin F. 2007. Nuclear traffic of influenza virus proteins and ribonucleoprotein complexes. Virus Res 124: 12-21. http://dx.doi.org/10.1016/j.virusres.2006.09.013.
32. Sasaki Y, Hagiwara K, Kakisaka M, Yamada K, Murakami T, Aida Y. 2013. Importin alpha3/Qip1 is involved in multiplication of mutant influenza virus with alanine mutation at amino acid 9 independently of nuclear transport function. PLoS One 8:e55765. http://dx.doi.org/10.1371/journal.pone.0055765.
33. Ozawa M, Fujii K, Muramoto Y, Yamada S, Yamayoshi S, Takada A, Goto H, Horimoto T, Kawaoka Y. 2007. Contributions of two nuclear localization signals of influenza A virus nucleoprotein to viral replication. J Virol 81:30-41. http://dx.doi.org/10.1128/JVI.01434-06.
34. Han Q, Chang C, Li L, Klenk C, Cheng J, Chen Y, Xia N, Shu Y, Chen Z, Gabriel G, Sun B, Xu K. 2014. Sumoylation of influenza A virus nucleoprotein is essential for intracellular trafficking and virus growth. J Virol 88:9379-9390. http://dx.doi.org/10.1128/JVI.00509-14.
35. Chutiwitoonchai N, Kakisaka M, Yamada K, Aida Y. 2014. Comparative analysis of seven viral nuclear export signals (NESs) reveals the crucial role of nuclear export mediated by the third NES consensus sequence of nucleoprotein (NP) in influenza A virus replication. PLoS One 9:e105081. http://dx.doi.org/10.1371/journal.pone.0105081.
36. Ye Q, Krug RM, Tao YJ. 2006. The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 444:1078-1082. http://dx.doi.org/10.1038/nature05379.
37. Kistner O, Muller K, Scholtissek C. 1989. Differential phosphorylation of the nucleoprotein of influenza A viruses. J Gen Virol 70:2421-2431. http://dx.doi.org/10.1099/0022-1317-70-9-2421.