Actin-myosin network is required for proper assembly of influenza virus particles

Virology

Volumn 476, Issue , 2015, Pages 141-150

  Kumakura, Michiko ^a   Kawaguchi, Atsushi ^a   Nagata, Kyosuke ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Blebbistatin; Influenza virus assembly; Non muscle myosin II

Indexed keywords

ACTIN; MYOSIN II; RIBONUCLEOPROTEIN; SMALL INTERFERING RNA; VIRUS RNA; MYOSIN;

ACTIN MYOSIN INTERACTION; ARTICLE; CELL MEMBRANE; CELL NUCLEUS; GENE SILENCING; IMMUNOFLUORESCENCE; INFLUENZA VIRUS; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; MDCK CELL LINE; NONHUMAN; POLYMERIZATION; PROTEIN SYNTHESIS; RNA SYNTHESIS; SCANNING ELECTRON MICROSCOPY; VIRUS GENOME; VIRUS PARTICLE; ANIMAL; CELL LINE; CYTOPLASM; GENETICS; HUMAN; INFLUENZA; METABOLISM; PHYSIOLOGY; VIROLOGY; VIRUS ASSEMBLY;

ORTHOMYXOVIRIDAE;

ACTINS; ANIMALS; CELL LINE; CELL NUCLEUS; CYTOPLASM; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA, HUMAN; MYOSINS; VIRUS ASSEMBLY;

EID: 84919709326     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.12.016     Document Type: Article

References (61)

1. Ali A., Avalos R.T., Ponimaskin E., Nayak D.P. Influenza virus assembly: effect of influenza virus glycoproteins on the membrane association of M1 protein. J. Virol. 2000, 74:8709-8719.
2. Amorim M.J., Bruce E.A., Read E.K., Foeglein A., Mahen R., Stuart A.D., Digard P. A Rab11- and microtubule-dependent mechanism for cytoplasmic transport of influenza A virus viral RNA. J. Virol. 2011, 85:4143-4156.
3. Aunis D., Bader M.F. The cytoskeleton as a barrier to exocytosis in secretory cells. J. Exp. Biol. 1988, 139:253-266.
4. Avalos R.T., Yu Z., Nayak D.P. Association of influenza virus NP and M1 proteins with cellular cytoskeletal elements in influenza virus-infected cells. J. Virol. 1997, 71:2947-2958.
5. Berberian K., Torres A.J., Fang Q., Kisler K., Lindau M. F-actin and myosin II accelerate catecholamine release from chromaffin granules. J. Neurosci. 2009, 29:863-870.
6. Berg J.S., Powell B.C., Cheney R.E. A millennial myosin census. Mol. Biol. Cell 2001, 12:780-794.
7. Bruce E.A., Digard P., Stuart A.D. The Rab11 pathway is required for influenza A virus budding and filament formation. J. Virol. 2010, 84:5848-5859.
8. Chichili G.R., Rodgers W. Cytoskeleton-membrane interactions in membrane raft structure. Cell. Mol. Life Sci. 2009, 66:2319-2328.
9. Conti M.A., Adelstein R.S. Nonmuscle myosin II moves in new directions. J. Cell Sci. 2008, 121:11-18.
10. Diz-Muñoz A., Fletcher D.A., Weiner O.D. Use the force: membrane tension as an organizer of cell shape and motility. Trends Cell Biol. 2013, 23:47-53.
11. Eisfeld A.J., Kawakami E., Watanabe T., Neumann G., Kawaoka Y. RAB11A is essential for transport of the influenza virus genome to the plasma membrane. J. Virol. 2011, 85:6117-6126.
12. Elleman C.J., Barclay W.S. The M1 matrix protein controls the filamentous phenotype of influenza A virus. Virology 2004, 321:144-153.
13. Elton D., Simpson-Holley M., Archer K., Medcalf L., Hallam R., McCauley J., Digard P. Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J. Virol. 2001, 75:408-419.
14. Giannone G., Dubin-Thaler B.J., Rossier O., Cai Y., Chaga O., Jiang G., Beaver W., Döbereiner H.G., Freund Y., Borisy G., Sheetz M.P. Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 2007, 128:561-575.
15. Goswami D., Gowrishankar K., Bilgrami S., Ghosh S., Raghupathy R., Chadda R., Vishwakarma R., Rao M., Mayor S. Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 2008, 135:1085-1097.
16. Gudheti M.V., Curthoys N.M., Gould T.J., Kim D., Gunewardene M.S., Gabor K.A., Gosse J.A., Kim C.H., Zimmerberg J., Hess S.T. Actin mediates the nanoscale membrane organization of the clustered membrane protein influenza hemagglutinin. Biophys. J. 2013, 104:2182-2192.
17. Gómez-Puertas P., Albo C., Pérez-Pastrana E., Vivo A., Portela A. Influenza virus matrix protein is the major driving force in virus budding. J. Virol. 2000, 74:11538-11547.
18. Haidari M., Zhang W., Ganjehei L., Ali M., Chen Z. Inhibition of MLC phosphorylation restricts replication of influenza virus-a mechanism of action for anti-influenza agents. PLoS One 2011, 6:e21444.
19. Heissler S.M., Manstein D.J. Nonmuscle myosin-2: mix and match. Cell. Mol. Life Sci. 2013, 70:1-21.
20. Jaqaman K., Kuwata H., Touret N., Collins R., Trimble W.S., Danuser G., Grinstein S. Cytoskeletal control of CD36 diffusion promotes its receptor and signaling function. Cell 2011, 146:593-606.
21. Jarvius M., Paulsson J., Weibrecht I., Leuchowius K.J., Andersson A.C., Wählby C., Gullberg M., Botling J., Sjöblom T., Markova B., Ostman A., Landegren U., Söderberg O. In situ detection of phosphorylated platelet-derived growth factor receptor beta using a generalized proximity ligation method. Mol. Cell. Proteomics 2007, 6:1500-1509.
22. Jo S., Kawaguchi A., Takizawa N., Morikawa Y., Momose F., Nagata K. Involvement of vesicular trafficking system in membrane targeting of the progeny influenza virus genome. Microbes Infect. 2010, 12:1079-1084.
23. Jolly C., Mitar I., Sattentau Q.J. Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1. J. Virol. 2007, 81:5547-5560.
24. Kawaguchi A., Momose F., Nagata K. Replication-coupled and host factor-mediated encapsidation of the influenza virus genome by viral nucleoprotein. J. Virol. 2011, 85:6197-6204.
25. Kenworthy A.K., Edidin M. Distribution of a glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of <100A using imaging fluorescence resonance energy transfer. J. Cell Biol. 1998, 142:69-84.
26. Kolega J. The role of myosin II motor activity in distributing myosin asymmetrically and coupling protrusive activity to cell translocation. Mol. Biol. Cell 2006, 17:4435-4445.
27. Kovács M., Tóth J., Hetényi C., Málnási-Csizmadia A., Sellers J.R. Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 2004, 279:35557-35563.
28. Lehmann M.J., Sherer N.M., Marks C.B., Pypaert M., Mothes W. Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell Biol. 2005, 170:317-325.
29. Lillemeier B.F., Pfeiffer J.R., Surviladze Z., Wilson B.S., Davis M.M. Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:18992-18997.
30. Ma K., Roy A.M., Whittaker G.R. Nuclear export of influenza virus ribonucleoproteins: identification of an export intermediate at the nuclear periphery. Virology 2001, 282:215-220.
31. Marjuki H., Alam M.I., Ehrhardt C., Wagner R., Planz O., Klenk H.D., Ludwig S., Pleschka S. Membrane accumulation of influenza A virus hemagglutinin triggers nuclear export of the viral genome via protein kinase Calpha-mediated activation of ERK signaling. J. Biol. Chem. 2006, 281:16707-16715.
32. Mercer J., Helenius A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 2008, 320:531-535.
33. Mishra M., Kashiwazaki J., Takagi T., Srinivasan R., Huang Y., Balasubramanian M.K., Mabuchi I. In vitro contraction of cytokinetic ring depends on myosin II but not on actin dynamics. Nat. Cell Biol. 2013, 15:853-859.
34. Momose F., Kikuchi Y., Komase K., Morikawa Y. Visualization of microtubule-mediated transport of influenza viral progeny ribonucleoprotein. Microbes Infect. 2007, 9:1422-1433.
35. Momose F., Sekimoto T., Ohkura T., Jo S., Kawaguchi A., Nagata K., Morikawa Y. Apical transport of influenza A virus ribonucleoprotein requires Rab11-positive recycling endosome. PLoS One 2011, 6:e21123.
36. Neumann G., Hughes M.T., Kawaoka Y. Influenza A virus NS2 protein mediates vRNP nuclear export through NES-independent interaction with hCRM1. EMBO J. 2000, 19:6751-6758.
37. Numajiri Haruki A., Naito T., Nishie T., Saito S., Nagata K. Interferon-inducible antiviral protein MxA enhances cell death triggered by endoplasmic reticulum stress. J. Interferon Cytokine Res. 2011, 31:847-856.
38. O'Neill R.E., Talon J., Palese P. The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins. EMBO J. 1998, 17:288-296.
39. Papadopulos A., Tomatis V.M., Kasula R., Meunier F.A. The cortical acto-myosin network: from diffusion barrier to functional gateway in the transport of neurosecretory vesicles to the plasma membrane. Front. Endocrinol. (Lausanne) 2013, 4:153.
40. Porat-Shliom N., Milberg O., Masedunskas A., Weigert R. Multiple roles for the actin cytoskeleton during regulated exocytosis. Cell. Mol. Life Sci. 2013, 70:2099-2121.
41. Roberts P.C., Compans R.W. Host cell dependence of viral morphology. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:5746-5751.
42. Rossman J.S., Jing X., Leser G.P., Lamb R.A. Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 2010, 142:902-913.
43. Ruigrok R., Baudin F., Petit I., Weissenhorn W. Role of influenza virus M1 protein in the viral budding process. Int. Congr. Ser. 2001, 1219:397-404.
44. Salles F.T., Merritt R.C., Manor U., Dougherty G.W., Sousa A.D., Moore J.E., Yengo C.M., Dosé A.C., Kachar B. Myosin IIIa boosts elongation of stereocilia by transporting espin 1 to the plus ends of actin filaments. Nat. Cell Biol. 2009, 11:443-450.
45. Scheiffele P., Roth M.G., Simons K. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 1997, 16:5501-5508.
46. Simpson-Holley M., Ellis D., Fisher D., Elton D., McCauley J., Digard P. A functional link between the actin cytoskeleton and lipid rafts during budding of filamentous influenza virions. Virology 2002, 301:212-225.
47. Straight A.F., Cheung A., Limouze J., Chen I., Westwood N.J., Sellers J.R., Mitchison T.J. Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 2003, 299:1743-1747.
48. Söderberg O., Gullberg M., Jarvius M., Ridderstråle K., Leuchowius K.J., Jarvius J., Wester K., Hydbring P., Bahram F., Larsson L.G., Landegren U. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 2006, 3:995-1000.
49. Takeda M., Leser G.P., Russell C.J., Lamb R.A. Influenza virus hemagglutinin concentrates in lipid raft microdomains for efficient viral fusion. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:14610-14617.
50. Takizawa N., Kumakura M., Takeuchi K., Kobayashi N., Nagata K. Sorting of influenza A virus RNA genome segments after nuclear export. Virology 2010, 401:248-256.
51. Takizawa N., Watanabe K., Nouno K., Kobayashi N., Nagata K. Association of functional influenza viral proteins and RNAs with nuclear chromatin and sub-chromatin structure. Microbes Infect. 2006, 8:823-833.
52. Tang Y., Winkler U., Freed E.O., Torrey T.A., Kim W., Li H., Goff S.P., Morse H.C. Cellular motor protein KIF-4 associates with retroviral Gag. J. Virol. 1999, 73:10508-10513.
53. Thaa B., Herrmann A., Veit M. Intrinsic cytoskeleton-dependent clustering of influenza virus M2 protein with hemagglutinin assessed by FLIM-FRET. J. Virol. 2010, 84:12445-12449.
54. Veit M., Thaa B. Association of influenza virus proteins with membrane rafts. Adv. Virol. 2011, 2011:370606.
55. Verkhovsky A.B., Svitkina T.M., Borisy G.G. Myosin II filament assemblies in the active lamella of fibroblasts: their morphogenesis and role in the formation of actin filament bundles. J. Cell Biol. 1995, 131:989-1002.
56. Vicente-Manzanares M., Ma X., Adelstein R.S., Horwitz A.R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 2009, 10:778-790.
57. Vicente-Manzanares M., Zareno J., Whitmore L., Choi C.K., Horwitz A.F. Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J. Cell Biol. 2007, 176:573-580.
58. Watanabe K., Takizawa N., Katoh M., Hoshida K., Kobayashi N., Nagata K. Inhibition of nuclear export of ribonucleoprotein complexes of influenza virus by leptomycin B. Virus Res. 2001, 77:31-42.
59. Wu X., Wang F., Rao K., Sellers J.R., Hammer J.A. Rab27a is an essential component of melanosome receptor for myosin Va. Mol. Biol. Cell 2002, 13:1735-1749.
60. Xue F., Janzen D.M., Knecht D.A. Contribution of filopodia to cell migration: a mechanical link between protrusion and contraction. Int. J. Cell Biol. 2010, 2010:507821.
61. Zhang J., Leser G.P., Pekosz A., Lamb R.A. The cytoplasmic tails of the influenza virus spike glycoproteins are required for normal genome packaging. Virology 2000, 269:325-334.