Avian influenza viruses inhibit the major cellular signalling integrator c-Abl

Cellular Microbiology

Volumn 16, Issue 12, 2014, Pages 1854-1874

  Hrincius, Eike R ^a,b   Liedmann, Swantje ^a   Anhlan, Darisuren ^a   Wolff, Thorsten ^c   Ludwig, Stephan ^a   Ehrhardt, Christina ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c ROBERT KOCH INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; ADAPTOR PROTEIN; CRK PROTEIN; NONSTRUCTURAL PROTEIN 1; UNCLASSIFIED DRUG; INS1 PROTEIN, INFLUENZA VIRUS; PROTEIN BINDING; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; AVIAN INFLUENZA; AVIAN INFLUENZA VIRUS; CELL FATE; CONSENSUS SEQUENCE; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; ENZYME ACTIVITY; ENZYME INHIBITION; GENE MUTATION; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; VIROGENESIS; VIRUS VIRULENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIRD; CELL LINE; HOST PATHOGEN INTERACTION; INFLUENZA VIRUS A; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; VIROLOGY;

AVIAN INFLUENZA VIRUS;

ANIMALS; BIRDS; CELL LINE; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS; INFLUENZA IN BIRDS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-ABL; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84911498654     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12332     Document Type: Article

References (73)

1. Andreolotti, A.G., Bragado, M.J., Tapia, J.A., Jensen, R.T., and Garcia-Marin, L.J. (2006) Adapter protein CRKII signaling is involved in the rat pancreatic acini response to reactive oxygen species. J Cell Biochem 97: 359-367.
2. Appel, S., Balabanov, S., Brummendorf, T.H., and Brossart, P. (2005) Effects of imatinib on normal hematopoiesis and immune activation. Stem Cells 23: 1082-1088.
3. Ayllon, J., Hale, B.G., and Garcia-Sastre, A. (2012) Strain-specific contribution of NS1-activated phosphoinositide 3-kinase signaling to influenza A virus replication and virulence. J Virol 86: 5366-5370.
4. Backert, S., Feller, S.M., and Wessler, S. (2008) Emerging roles of Abl family tyrosine kinases in microbial pathogenesis. Trends Biochem Sci 33: 80-90.
5. Barila, D., and Superti-Furga, G. (1998) An intramolecular SH3-domain interaction regulates c-Abl activity. Nat Genet 18: 280-282.
6. Baskaran, R., Escobar, S.R., and Wang, J.Y. (1999) Nuclear c-Abl is a COOH-terminal repeated domain (CTD)-tyrosine (CTD)-tyrosine kinase-specific for the mammalian RNA polymerase II: possible role in transcription elongation. Cell Growth Differ 10: 387-396.
7. Basler, C.F., Wang, X., Muhlberger, E., Volchkov, V., Paragas, J., Klenk, H.D., etal. (2000) The Ebola virus VP35 protein functions as a type I IFN antagonist. Proc Natl Acad Sci USA 97: 12289-12294.
8. Bavagnoli, L., Dundon, W.G., Garbelli, A., Zecchin, B., Milani, A., Parakkal, G., etal. (2011) The PDZ-ligand and Src-homology type 3 domains of epidemic avian influenza virus NS1 protein modulate human Src kinase activity during viral infection. PLoS ONE 6: e27789.
9. Birge, R.B., Knudsen, B.S., Besser, D., and Hanafusa, H. (1996) SH2 and SH3-containing adaptor proteins: redundant or independent mediators of intracellular signal transduction. Genes Cells 1: 595-613.
10. Brightbill, H., and Schlissel, M.S. (2009) The effects of c-Abl mutation on developing B cell differentiation and survival. Int Immunol 21: 575-585.
11. Burgui, I., Aragon, T., Ortin, J., and Nieto, A. (2003) PABP1 and eIF4GI associate with influenza virus NS1 protein in viral mRNA translation initiation complexes. J Gen Virol 84: 3263-3274.
12. Chen, S., Brier, S., Smithgall, T.E., and Engen, J.R. (2007) The Abl SH2-kinase linker naturally adopts a conformation competent for SH3 domain binding. Protein Sci 16: 572-581.
13. Dubey, K.D., and Ojha, R.P. (2011) Conformational flexibility, binding energy, role of salt bridge and alanine-mutagenesis for c-Abl kinase complex. J Mol Model 18: 1679-1689.
14. Egorov, A., Brandt, S., Sereinig, S., Romanova, J., Ferko, B., Katinger, D., etal. (1998) Transfectant influenza A viruses with long deletions in the NS1 protein grow efficiently in Vero cells. J Virol 72: 6437-6441.
15. Ehrhardt, C. (2011) From virus entry to release: the diverse functions of PI3K during RNA virus infection. Future Virol 6: 1225-1239.
16. Ehrhardt, C., and Ludwig, S. (2009) A new player in a deadly game: influenza viruses and the PI3K/Akt signalling pathway. Cell Microbiol 11: 863-871.
17. Feller, S.M. (2001) Crk family adaptors-signalling complex formation and biological roles. Oncogene 20: 6348-6371.
18. Feller, S.M., Knudsen, B., and Hanafusa, H. (1994) c-Abl kinase regulates the protein binding activity of c-Crk. EMBO J 13: 2341-2351.
19. Fernandez-Sesma, A. (2007) The influenza virus NS1 protein: inhibitor of innate and adaptive immunity. Infect Disord Drug Targets 7: 336-343.
20. Gabriel, G., Dauber, B., Wolff, T., Planz, O., Klenk, H.D., and Stech, J. (2005) The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci USA 102: 18590-18595.
21. Gack, M.U., Albrecht, R.A., Urano, T., Inn, K.S., Huang, I.C., Carnero, E., etal. (2009) Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5: 439-449.
22. Garcia, M., Cooper, A., Shi, W., Bornmann, W., Carrion, R., Kalman, D., and Nabel, G.J. (2012) Productive replication of Ebola virus is regulated by the c-Abl1 tyrosine kinase. Sci Transl Med 4: 123ra124.
23. Garcia-Sastre, A., Egorov, A., Matassov, D., Brandt, S., Levy, D.E., Durbin, J.E., etal. (1998) Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252: 324-330.
24. Gu, J.J., Ryu, J.R., and Pendergast, A.M. (2009) Abl tyrosine kinases in T-cell signaling. Immunol Rev 228: 170-183.
25. Hale, B.G., Jackson, D., Chen, Y.H., Lamb, R.A., and Randall, R.E. (2006) Influenza A virus NS1 protein binds p85beta and activates phosphatidylinositol-3-kinase signaling. Proc Natl Acad Sci USA 103: 14194-14199.
26. Hale, B.G., Batty, I.H., Downes, C.P., and Randall, R.E. (2008a) Binding of influenza A virus NS1 protein to the inter-SH2 domain of p85 suggests a novel mechanism for phosphoinositide 3-kinase activation. J Biol Chem 283: 1372-1380.
27. Hale, B.G., Randall, R.E., Ortin, J., and Jackson, D. (2008b) The multifunctional NS1 protein of influenza A viruses. J Gen Virol 89: 2359-2376.
28. Hale, B.G., Kerry, P.S., Jackson, D., Precious, B.L., Gray, A., Killip, M.J., etal. (2010) Structural insights into phosphoinositide 3-kinase activation by the influenza A virus NS1 protein. Proc Natl Acad Sci USA 107: 1954-1959.
29. Hantschel, O., and Superti-Furga, G. (2004) Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat Rev Mol Cell Biol 5: 33-44.
30. Heikkinen, L.S., Kazlauskas, A., Melen, K., Wagner, R., Ziegler, T., Julkunen, I., and Saksela, K. (2008) Avian and 1918 Spanish influenza A virus NS1 proteins bind to Crk/CrkL Src homology 3 domains to activate host cell signaling. J Biol Chem 283: 5719-5727.
31. Hoffmann, E., Neumann, G., Kawaoka, Y., Hobom, G., and Webster, R.G. (2000) A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci USA 97: 6108-6113.
32. Hoffmann, E., Krauss, S., Perez, D., Webby, R., and Webster, R.G. (2002) Eight-plasmid system for rapid generation of influenza virus vaccines. Vaccine 20: 3165-3170.
33. Hrincius, E.R., Wixler, V., Wolff, T., Wagner, R., Ludwig, S., and Ehrhardt, C. (2010) CRK adaptor protein expression is required for efficient replication of avian influenza A viruses and controls JNK-mediated apoptotic responses. Cell Microbiol 12: 831-843.
34. Hrincius, E.R., Dierkes, R., Anhlan, D., Wixler, V., Ludwig, S., and Ehrhardt, C. (2011) Phosphatidylinositol-3-kinase (PI3K) is activated by influenza virus vRNA via the pathogen pattern receptor Rig-I to promote efficient type I interferon production. Cell Microbiol 13: 1907-1919.
35. Hrincius, E.R., Hennecke, A.K., Gensler, L., Nordhoff, C., Anhlan, D., Vogel, P., etal. (2012) A single point mutation (Y89F) within the non-structural protein 1 of influenza A viruses limits epithelial cell tropism and virulence in mice. Am J Pathol 180: 2361-2374.
36. Huang, Y., Comiskey, E.O., Dupree, R.S., Li, S., Koleske, A.J., and Burkhardt, J.K. (2008) The c-Abl tyrosine kinase regulates actin remodeling at the immune synapse. Blood 112: 111-119.
37. Jackson, D., Hossain, M.J., Hickman, D., Perez, D.R., and Lamb, R.A. (2008) A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Proc Natl Acad Sci USA 105: 4381-4386.
38. de Jong, R., ten Hoeve, J., Heisterkamp, N., and Groffen, J. (1997) Tyrosine 207 in CRKL is the BCR/ABL phosphorylation site. Oncogene 14: 507-513.
39. Katsoulidis, E., Sassano, A., Majchrzak-Kita, B., Carayol, N., Yoon, P., Jordan, A., etal. (2008) Suppression of interferon (IFN)-inducible genes and IFN-mediated functional responses in BCR-ABL-expressing cells. J Biol Chem 283: 10793-10803.
40. Koleske, A.J., Gifford, A.M., Scott, M.L., Nee, M., Bronson, R.T., Miczek, K.A., and Baltimore, D. (1998) Essential roles for the Abl and Arg tyrosine kinases in neurulation. Neuron 21: 1259-1272.
41. Lee, J.H., Kim, S.H., Pascua, P.N., Song, M.S., Baek, Y.H., Jin, X., etal. (2010) Direct interaction of cellular hnRNP-F and NS1 of influenza A virus accelerates viral replication by modulation of viral transcriptional activity and host gene expression. Virology 397: 89-99.
42. Li, S., Min, J.Y., Krug, R.M., and Sen, G.C. (2006) Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology 349: 13-21.
43. Li, Y., Anderson, D.H., Liu, Q., and Zhou, Y. (2008) Mechanism of influenza A virus NS1 protein interaction with the p85beta, but not the p85alpha, subunit of phosphatidylinositol 3-kinase (PI3K) and up-regulation of PI3K activity. J Biol Chem 283: 23397-23409.
44. Livak, K.J., and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
45. Lu, M., and Krauss, R.S. (2010) Abl promotes cadherin-dependent adhesion and signaling in myoblasts. Cell Cycle 9: 2737-2741.
46. Ludwig, S. (2011) Disruption of virus-host cell interactions and cell signaling pathways as an anti-viral approach against influenza virus infections. Biol Chem 392: 837-847.
47. Malik Peiris, J.S. (2009) Avian influenza viruses in humans. Rev Sci Tech 28: 161-173.
48. Pielage, J.F., Powell, K.R., Kalman, D., and Engel, J.N. (2008) RNAi screen reveals an Abl kinase-dependent host cell pathway involved in Pseudomonas aeruginosa internalization. PLoS Pathog 4: e1000031.
49. Puthavathana, P., Auewarakul, P., Charoenying, P.C., Sangsiriwut, K., Pooruk, P., Boonnak, K., etal. (2005) Molecular characterization of the complete genome of human influenza H5N1 virus isolates from Thailand. J Gen Virol 86: 423-433.
50. Reichman, C., Singh, K., Liu, Y., Singh, S., Li, H., Fajardo, J.E., etal. (2005) Transactivation of Abl by the Crk II adapter protein requires a PNAY sequence in the Crk C-terminal SH3 domain. Oncogene 24: 8187-8199.
51. Ren, R., Ye, Z.S., and Baltimore, D. (1994) Abl protein-tyrosine kinase selects the Crk adapter as a substrate using SH3-binding sites. Genes Dev 8: 783-795.
52. Senechal, K., Heaney, C., Druker, B., and Sawyers, C.L. (1998) Structural requirements for function of the Crkl adapter protein in fibroblasts and hematopoietic cells. Mol Cell Biol 18: 5082-5090.
53. Seyer, R., Hrincius, E.R., Ritzel, D., Abt, M., Mellmann, A., Marjuki, H., etal. (2011) Synergistic adaptive mutations in the hemagglutinin and polymerase acidic protein lead to increased virulence of pandemic 2009 H1N1 influenza A virus in mice. J Infect Dis 205: 262-271.
54. Shin, Y.K., Li, Y., Liu, Q., Anderson, D.H., Babiuk, L.A., and Zhou, Y. (2007) SH3 binding motif 1 in influenza A virus NS1 protein is essential for PI3K/Akt signaling pathway activation. J Virol 81: 12730-12739.
55. Silberman, I., Sionov, R.V., Zuckerman, V., Haupt, S., Goldberg, Z., Strasser, A., etal. (2008) T cell survival and function requires the c-Abl tyrosine kinase. Cell Cycle 7: 3847-3857.
56. Sirvent, A., Benistant, C., and Roche, S. (2008) Cytoplasmic signalling by the c-Abl tyrosine kinase in normal and cancer cells. Biol Cell 100: 617-631.
57. Song, T., Wei, C., Zheng, Z., Xu, Y., Cheng, X., Yuan, Y., etal. (2010) c-Abl tyrosine kinase interacts with MAVS and regulates innate immune response. FEBS Lett 584: 33-38.
58. Sossey-Alaoui, K., Li, X., and Cowell, J.K. (2007) c-Abl-mediated phosphorylation of WAVE3 is required for lamellipodia formation and cell migration. J Biol Chem 282: 26257-26265.
59. Soubies, S.M., Volmer, C., Croville, G., Loupias, J., Peralta, B., Costes, P., etal. (2010) Species-specific contribution of the four C-terminal amino acids of influenza A virus NS1 protein to virulence. J Virol 84: 6733-6747.
60. Sriram, G., and Birge, R.B. (2010) Emerging roles for crk in human cancer. Genes Cancer 1: 1132-1139.
61. Sriram, G., Reichman, C., Tunceroglu, A., Kaushal, N., Saleh, T., Machida, K., etal. (2011) Phosphorylation of Crk on tyrosine 251 in the RT loop of the SH3C domain promotes Abl kinase transactivation. Oncogene 30: 4645-4655.
62. Van Etten, R.A., Debnath, J., Zhou, H., and Casasnovas, J.M. (1995) Introduction of a loss-of-function point mutation from the SH3 region of the Caenorhabditis elegans sem-5 gene activates the transforming ability of c-abl in vivo and abolishes binding of proline-rich ligands in vitro. Oncogene 10: 1977-1988.
63. Wagner, R., Herwig, A., Azzouz, N., and Klenk, H.D. (2005) Acylation-mediated membrane anchoring of avian influenza virus hemagglutinin is essential for fusion pore formation and virus infectivity. J Virol 79: 6449-6458.
64. Wessler, S., and Backert, S. (2011) Abl family of tyrosine kinases and microbial pathogenesis. Int Rev Cell Mol Biol 286: 271-300.
65. Wolff, T., O'Neill, R.E., and Palese, P. (1998) NS1-binding protein (NS1-BP): a novel human protein that interacts with the influenza A virus nonstructural NS1 protein is relocalized in the nuclei of infected cells. J Virol 72: 7170-7180.
66. Woodring, P.J., Litwack, E.D., O'Leary, D.D., Lucero, G.R., Wang, J.Y., and Hunter, T. (2002) Modulation of the F-actin cytoskeleton by c-Abl tyrosine kinase in cell spreading and neurite extension. J Cell Biol 156: 879-892.
67. Woodring, P.J., Hunter, T., and Wang, J.Y. (2003) Regulation of F-actin-dependent processes by the Abl family of tyrosine kinases. J Cell Sci 116: 2613-2626.
68. Wu, W., and Berg, L.J. (2008) c-Abl, an additional tyrosine kinase required for T cell development and function. Cell Cycle 7: 3791.
69. Zandy, N.L., and Pendergast, A.M. (2008) Abl tyrosine kinases modulate cadherin-dependent adhesion upstream and downstream of Rho family GTPases. Cell Cycle 7: 444-448.
70. Zandy, N.L., Playford, M., and Pendergast, A.M. (2007) Abl tyrosine kinases regulate cell-cell adhesion through Rho GTPases. Proc Natl Acad Sci USA 104: 17686-17691.
71. Zhang, D.G., Li, W.Z., Wang, G.F., Su, Y., Zeng, J., Zhang, C., etal. (2010) Heterologous SH3-p85beta inhibits influenza A virus replication. Virol J 7: 170.
72. Zielecki, F., Semmler, I., Kalthoff, D., Voss, D., Mauel, S., Gruber, A.D., etal. (2010) Virulence determinants of avian H5N1 influenza A virus in mammalian and avian hosts: role of the C-terminal ESEV motif in the viral NS1 protein. J Virol 84: 10708-10718.
73. Zipfel, P.A., Zhang, W., Quiroz, M., and Pendergast, A.M. (2004) Requirement for Abl kinases in T cell receptor signaling. Curr Biol 14: 1222-1231.