Importin-α7 is required for enhanced influenza A virus replication in the alveolar epithelium and severe lung damage in mice

Journal of Virology

Volumn 88, Issue 14, 2014, Pages 8166-8179

  Resa Infante, Patricia ^a   Thieme, René ^b,c   Ernst, Thomas ^b   Arck, Petra C ^b   Ittrich, Harald ^b   Reimer, Rudolph ^a   Gabriel, Gülsah ^a  

^a LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

IMPORTIN ALPHA7; NUCLEAR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHUS MUCOSA; CELL INFILTRATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RESPONSE; EX VIVO STUDY; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA A (H1N1); INFLUENZA VIRUS A H1N1; LUNG ALVEOLUS EPITHELIUM; LUNG INJURY; MACROPHAGE; MONONUCLEAR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; VIRAL CLEARANCE; VIRAL TROPISM; VIRUS IMMUNITY; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS VIRULENCE;

ALPHA KARYOPHERINS; ANIMALS; CYTOKINES; EPITHELIAL CELLS; HOST-PATHOGEN INTERACTIONS; INFLUENZA A VIRUS, H1N1 SUBTYPE; LUNG; MAGNETIC RESONANCE IMAGING; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; RESPIRATORY MUCOSA; SURVIVAL ANALYSIS; VIRAL TROPISM; VIRUS REPLICATION;

EID: 84904612730     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00270-14     Document Type: Article

References (29)

1. Klenk HD, Garten W, Matrosovich M. 2011. Molecular mechanisms of interspecies transmission and pathogenicity of influenza viruses: lessons from the 2009 pandemic. Bioessays 33:180-188. http://dx.doi.org/10.1002/bies.201000118.
2. Resa-Infante P, Gabriel G. 2013. The nuclear import machinery is a determinant of influenza virus host adaptation. Bioessays 35:23-27. http: //dx.doi.org/10.1002/bies.201200138.
3. Strambio-De-Castillia C, Niepel M, Rout MP. 2010. The nuclear pore complex: bridging nuclear transport and gene regulation. Nat. Rev. Mol. Cell Biol. 11:490-501. http://dx.doi.org/10.1038/nrm2928.
4. Gabriel G, Herwig A, Klenk HD. 2008. Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathog. 4:e11. http://dx.doi.org/10.1371/journal.ppat.0040011.
5. Hudjetz B, Gabriel G. 2012. Human-like PB2 627K influenza virus polymerase activity is regulated by importin-alpha1 and-alpha7. PLoS Pathog. 8:e1002488. http://dx.doi.org/10.1371/journal.ppat.1002488.
6. Gabriel G, Klingel K, Otte A, Thiele S, Hudjetz B, Arman-Kalcek G, Sauter M, Shmidt T, Rother F, Baumgarte S, Keiner B, Hartmann E, Bader M, Brownlee GG, Fodor E, Klenk HD. 2011. Differential use of importin-alpha isoforms governs cell tropism and host adaptation of influenza virus. Nat. Commun. 2:156. http://dx.doi.org/10.1038/ncomms1158.
7. Braciale TJ, Sun J, Kim TS. 2012. Regulating the adaptive immune response to respiratory virus infection. Nat. Rev. Immunol. 12:295-305. http://dx.doi.org/10.1038/nri3166.
8. Short KR, Kroeze EJ, Fouchier RA, Kuiken T. 2014. Pathogenesis of influenza-induced acute respiratory distress syndrome. Lancet Infect. Dis. 14:57-69. http://dx.doi.org/10.1016/S1473-3099(13)70286-X.
9. Manicassamy B, Manicassamy S, Belicha-Villanueva A, Pisanelli G, Pulendran B, García-Sastre A. 2010. Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus. Proc. Natl. Acad. Sci. U. S. A. 107:11531-11536. http://dx.doi.org/10.1073/pnas.0914994107.
10. Perez JT, García-Sastre A, Manicassamy B. 2013. Insertion of a GFP reporter gene in influenza virus. Curr. Protoc. Microbiol. Chapter 15:Unit 15G.4. http://dx.doi.org/10.1002/9780471729259.mc15g04s29.
11. Rother F, Shmidt T, Popova E, Krivokharchenko A, Hugel S, Vilianovich L, Ridders M, Tenner K, Alenina N, Kohler M, Hartmann E, Bader M. 2011. Importin alpha7 is essential for zygotic genome activation and early mouse development. PLoS One 6:e18310. http://dx.doi.org/10.1371 /journal.pone.0018310.
12. Gabriel G, Klingel K, Planz O, Bier K, Herwig A, Sauter M, Klenk HD. 2009. Spread of infection and lymphocyte depletion in mice depends on polymerase of influenza virus. Am. J. Pathol. 175:1178-1186. http://dx.doi.org/10.2353/ajpath.2009.090339.
13. Simionescu N, Simionescu M. 1976. Galloylglucoses of low molecular weight as mordant in electron microscopy. I. Procedure, and evidence for mordanting effect. J. Cell Biol. 70:608-621.
14. Zhang X, Goncalves R, Mosser DM. 2008. The isolation and characterization of murine macrophages. Curr. Protoc. Immunol. Chapter 14:Unit 14.1. http://dx.doi.org/10.1002/0471142735.im1401s83.
15. Fujisawa H. 2008. Neutrophils play an essential role in cooperation with antibody in both protection against and recovery from pulmonary infection with influenza virus in mice. J. Virol. 82:2772-2783. http://dx.doi.org /10.1128/JVI.01210-07.
16. Gonzalez-Juarrero M, Shim TS, Kipnis A, Junqueira-Kipnis AP, Orme IM. 2003. Dynamics of macrophage cell populations during murine pulmonary tuberculosis. J. Immunol. 171:3128-3135. http://dx.doi.org/10.4049/jimmunol.171.6.3128.
17. Cline TD, Karlsson EA, Seufzer BJ, Schultz-Cherry S. 2013. The hemagglutinin protein of highly pathogenic H5N1 influenza viruses overcomes an early block in the replication cycle to promote productive replication in macrophages. J. Virol. 87:1411-1419. http://dx.doi.org/10.1128 /JVI.02682-12.
18. Perrone LA, Plowden JK, García-Sastre A, Katz JM, Tumpey TM. 2008. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog. 4:e1000115. http://dx.doi.org/10.1371/journal.ppat.1000115.
19. van Riel D, Kuiken T. 2012. The role of cell tropism for the pathogenesis of influenza in humans. Future Virol. 7:295-307. http://dx.doi.org/10.2217/fvl.12.11.
20. van Riel D, Leijten LM, van der Eerden M, Hoogsteden HC, Boven LA, Lambrecht BN, Osterhaus AD, Kuiken T. 2011. Highly pathogenic avian influenza virus H5N1 infects alveolar macrophages without virus production or excessive TNF-alpha induction. PLoS Pathog. 7:e1002099. http: //dx.doi.org/10.1371/journal.ppat.1002099.
21. Sakabe S, Takano R, Nagamura-Inoue T, Yamashita N, Nidom CA, Quynh Le M, Iwatsuki-Horimoto K, Kawaoka Y. 2013. Differences in cytokine production in human macrophages and in virulence in mice are attributable to the acidic polymerase protein of highly pathogenic influenza A virus subtype H5N1. J. Infect. Dis. 207:262-271. http://dx.doi.org /10.1093/infdis/jis523.
22. Fulcher AJ, Ahmed CM, Noon-Song EN, Kwan RY, Subramaniam PS, Johnson HM, Jans DA. 2008. Interferon gamma is recognised by importin alpha/beta: enhanced nuclear localising and transactivation activities of an interferon gamma mimetic. FEBS Lett. 582:1569-1574. http://dx.doi.org/10.1016/j.febslet.2008.03.054.
23. Theiss AL, Jenkins AK, Okoro NI, Klapproth JM, Merlin D, Sitaraman SV. 2009. Prohibitin inhibits tumor necrosis factor alpha-induced nuclear factor-kappa B nuclear translocation via the novel mechanism of decreasing importin alpha3 expression. Mol. Biol. Cell 20:4412-4423. http://dx.doi.org/10.1091/mbc.E09-05-0361.
24. Xue H, Chen B, Fan Y, Palikhe M, Li Y. 2011. The inhibitory effect of polypeptide cSN50 on alcoholic hepatic injuries through blocking the binding of NF-kappaB to importin alpha. Scand. J. Gastroenterol. 46:931-940. http://dx.doi.org/10.3109/00365521.2011.568516.
25. Turner JE, Morrison PJ, Wilhelm C, Wilson M, Ahlfors H, Renauld JC, Panzer U, Helmby H, Stockinger B. 2013. IL-9-mediated survival of type 2 innate lymphoid cells promotes damage control in helminth-induced lung inflammation. J. Exp. Med. 210:2951-2965. http://dx.doi.org/10.1084/jem.20130071.
26. Monteiro JM, Harvey C, Trinchieri G. 1998. Role of interleukin-12 in primary influenza virus infection. J. Virol. 72:4825-4831.
27. Damjanovic D, Small CL, Jeyanathan M, McCormick S, Xing Z. 2012. Immunopathology in influenza virus infection: uncoupling the friend from foe. Clin. Immunol. 144:57-69. http://dx.doi.org/10.1016/j.clim.2012.05.005.
28. Yasuhara N, Shibazaki N, Tanaka S, Nagai M, Kamikawa Y, Oe S, Asally M, Kamachi Y, Kondoh H, Yoneda Y. 2007. Triggering neural differentiation of ES cells by subtype switching of importin-alpha. Nat. Cell Biol. 9:72-79. http://dx.doi.org/10.1038/ncb1521.
29. Reed L, Muench H. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.