A Rab11- and microtubule-dependent mechanism for cytoplasmic transport of influenza a virus viral RNA

Journal of Virology

Volumn 85, Issue 9, 2011, Pages 4143-4156

  Amorim, Maria Joao ^a   Bruce, Emily A ^a   Read, Eliot K C ^a   Foeglein, Ágnes ^a   Mahen, Robert ^b   Stuart, Amanda D ^a   Digard, Paul ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b HUTCHISON MRC RESEARCH CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DEMECOLCINE; GAMMA TUBULIN; GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATE; NOCODAZOLE; PACLITAXEL; RAB PROTEIN; RAB11 PROTEIN; RIBONUCLEOPROTEIN; RNA POLYMERASE; SMALL INTERFERING RNA; VIRUS RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL TRANSPORT; CONTROLLED STUDY; CYTOPLASM; ENDOSOME; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; HUMAN CELL; INFLUENZA VIRUS A; MICROTUBULE; MICROTUBULE ORGANIZING CENTER; PRECIPITATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; VIRUS GENOME; VIRUS RELEASE; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE; HUMANS; INFLUENZA A VIRUS; MICROSCOPY, FLUORESCENCE; MICROTUBULES; RAB GTP-BINDING PROTEINS; RNA, VIRAL; VIRUS REPLICATION;

INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

EID: 79955415241     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02606-10     Document Type: Article

References (61)

1. Afonso, P. V., A. Zamborlini, A. Saib, and R. Mahieux. 2007. Centrosome and retroviruses: the dangerous liaisons. Retrovirology 4:27.
2. Amorim, M. J., E. K. Read, R. M. Dalton, L. Medcalf, and P. Digard. 2007. Nuclear export of influenza A virus mRNAs requires ongoing RNA polymerase II activity. Traffic 8:1-11.
3. Apodaca, G., L. A. Katz, and K. E. Mostov. 1994. Receptor-mediated trans-cytosis of IgA in MDCK cells is via apical recycling endosomes. J. Cell Biol. 125:67-86.
4. Arcangeletti, M. C., et al. 1997. Modification of cytoskeleton and prosome networks in relation to protein synthesis in influenza A virus-infected LLC-MK2 cells. Virus Res. 51:19-34.
5. Avalos, R. T., Z. Yu, and D. P. Nayak. 1997. Association of influenza virus NP and M1 proteins with cellular cytoskeletal elements in influenza virus-infected cells. J. Virol. 71:2947-2958.
6. Babcock, H. P., C. Chen, and X. Zhuang. 2004. Using single-particle tracking to study nuclear trafficking of viral genes. Biophys. J. 87:2749-2758.
7. Balasubramanian, N., D. W. Scott, J. D. Castle, J. E. Casanova, and M. A. Schwartz. 2007. Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts. Nat. Cell Biol. 9:1381-1391.
8. Boulo, S., H. Akarsu, R. W. Ruigrok, and F. Baudin. 2007. Nuclear traffic of influenza virus proteins and ribonucleoprotein complexes. Virus Res. 124: 12-21.
9. Breitenfeld, P. M., and W. Schafer. 1957. The formation of fowl plague virus antigens in infected cells, as studied with fluorescent antibodies. Virology 4:328-345.
10. Bruce, E. A., P. Digard, and A. D. Stuart. 2010. The Rab11 pathway is required for influenza A virus budding and filament formation. J. Virol. 84:5848-5859.
11. Bruce, E. A., et al. 2009. Budding of filamentous and non-filamentous influenza A virus occurs via a VPS4 and VPS28-independent pathway. Virology 390:268-278.
12. Carrasco, M., M. J. Amorim, and P. Digard. 2004. Lipid raft-dependent targeting of the influenza A virus nucleoprotein to the apical plasma membrane. Traffic 5:979-992.
13. Casanova, J. E., et al. 1999. Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells. Mol. Biol. Cell 10:47-61.
14. Chambers, R., and T. Takimoto. 2010. Trafficking of Sendai virus nucleo-capsids is mediated by intracellular vesicles. PLoS One 5:e10994.
15. Chen, B. J., G. P. Leser, E. Morita, and R. A. Lamb. 2007. Influenza virus hemagglutinin and neuraminidase, but not the matrix protein, are required for assembly and budding of plasmid-derived virus-like particles. J. Virol. 81:7111-7123.
16. Dale, L. B., J. L. Seachrist, A. V. Babwah, and S. S. Ferguson. 2004. Regulation of angiotensin II type 1A receptor intracellular retention, degradation, and recycling by Rab5, Rab7, and Rab11 GTPases. J. Biol. Chem. 279: 13110-13118.
17. de Wit, E., et al. 2004. Efficient generation and growth of influenza virus A/PR/8/34 from eight cDNA fragments. Virus Res. 103:155-161.
18. Digard, P., V. C. Blok, and S. C. Inglis. 1989. Complex formation between influenza virus polymerase proteins expressed in Xenopus oocytes. Virology 171:162-169.
19. Digard, P., et al. 1999. Modulation of nuclear localization of the influenza virus nucleoprotein through interaction with actin filaments. J. Virol. 73: 2222-2231.
20. Dunn, K. W., T. E. McGraw, and F. R. Maxfield. 1989. Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome. J. Cell Biol. 109:3303-3314.
21. Elton, D., et al. 2001. Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J. Virol. 75:408-419.
22. Griffin, J. A., and R. W. Compans. 1979. Effect of cytochalasin B on the maturation of enveloped viruses. J. Exp. Med. 150:379-391.
23. Harman, A., H. Browne, and T. Minson. 2002. The transmembrane domain and cytoplasmic tail of herpes simplex virus type 1 glycoprotein H play a role in membrane fusion. J. Virol. 76:10708-10716.
24. Hayman, A., et al. 2007. NS1 proteins of avian influenza A viruses can act as antagonists of the human alpha/beta interferon response. J. Virol. 81:2318- 2327.
25. Hopkins, C. R., A. Gibson, M. Shipman, D. K. Strickland, and I. S. Trow-bridge. 1994. In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella. J. Cell Biol. 125:1265-1274.
26. Hutchinson, E. C., M. D. Curran, E. K. Read, J. R. Gog, and P. Digard. 2008. Mutational analysis of cis-acting RNA signals in segment 7 of influenza A virus. J. Virol. 82:11869-11879.
27. Hutchinson, E. C., J. C. von Kirchbach, J. R. Gog, and P. Digard. 2010. Genome packaging in influenza A virus. J. Gen. Virol. 91:313-328.
28. Jo, S., et al. 2010. Involvement of vesicular trafficking system in membrane targeting of the progeny influenza virus genome. Microbes Infect. 12:1079- 1084.
29. Loucaides, E. M., et al. 2009. Nuclear dynamics of influenza A virus ribo-nucleoproteins revealed by live-cell imaging studies. Virology 394:154-163.
30. Martin, K., and A. Helenius. 1991. Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell 67:117-130.
31. Mayer, D., et al. 2007. Identification of cellular interaction partners of the influenza virus ribonucleoprotein complex and polymerase complex using proteomic-based approaches. J. Proteome Res. 6:672-682.
32. Meijering, E., et al. 2004. Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58:167-176.
33. Mollenhauer, H. H., D. J. Morre, and L. D. Rowe. 1990. Alteration of intracellular traffic by monensin; mechanism, specificity and relationship to toxicity. Biochim. Biophys. Acta 1031:225-246.
34. Momose, F., Y. Kikuchi, K. Komase, and Y. Morikawa. 2007. Visualization of microtubule-mediated transport of influenza viral progeny ribonucleopro-tein. Microbes Infect. 9:1422-1433.
35. Mullin, A. E., R. M. Dalton, M. J. Amorim, D. Elton, and P. Digard. 2004. Increased amounts of the influenza virus nucleoprotein do not promote higher levels of viral genome replication. J. Gen. Virol. 85:3689-3698.
36. Nayak, D. P., R. A. Balogun, H. Yamada, Z. H. Zhou, and S. Barman. 2009. Influenza virus morphogenesis and budding. Virus Res. 143:147-161.
37. Noton, S. L., et al. 2007. Identification of the domains of the influenza A virus M1 matrix protein required for NP binding, oligomerization and incorporation into virions. J. Gen. Virol. 88:2280-2290.
38. Pleschka, S., et al. 1996. A plasmid-based reverse genetics system for influenza A virus. J. Virol. 70:4188-4192.
39. Poole, E., D. Elton, L. Medcalf, and P. Digard. 2004. Functional domains of the influenza A virus PB2 protein: identification of NP- and PB1-binding sites. Virology 321:120-133.
40. Portela, A., and P. Digard. 2002. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J. Gen. Virol. 83:723-734.
41. Radtke, K., K. Dohner, and B. Sodeik. 2006. Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell Microbiol. 8:387-400.
42. Read, E. K., and P. Digard. 2010. Individual influenza A virus mRNAs show differential dependence on cellular NXF1/TAP for their nuclear export. J. Gen. Virol. 91:1290-1301.
43. Ren, M., et al. 1998. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc. Natl. Acad. Sci. U. S. A. 95:6187-6192.
44. Rietdorf, J., et al. 2001. Kinesin-dependent movement on microtubules precedes actin-based motility of vaccinia virus. Nat. Cell Biol. 3:992-1000.
45. Rindler, M. J., I. E. Ivanov, and D. D. Sabatini. 1987. Microtubule-acting drugs lead to the nonpolarized delivery of the influenza hemagglutinin to the cell surface of polarized Madin-Darby canine kidney cells. J. Cell Biol. 104:231-241.
46. Robb, N. C, M. Smith, F. T. Vreede, and E. Fodor. 2009. NS2/NEP protein regulates transcription and replication of the influenza virus RNA genome. J. Gen. Virol. 90:1398-1407.
47. Roberts, P. C, and R. W. Compans. 1998. Host cell dependence of viral morphology. Proc. Natl. Acad. Sci. U. S. A. 95:5746-5751.
48. Rossman, J. S., X. Jing, G. P. Leser, and R. A. Lamb. 2010. Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142: 902-913.
49. Sahlender, D. A., et al. 2005. Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J. Cell Biol. 169:285-295.
50. Salas, P. J., et al. 1986. Microtubules and actin filaments are not critically involved in the biogenesis of epithelial cell surface polarity. J. Cell Biol. 102:1853-1867.
51. Seachrist, J. L., P. H. Anborgh, and S. S. Ferguson. 2000. Beta 2-adrenergic receptor internalization, endosomal sorting, and plasma membrane recycling are regulated by rab GTPases. J. Biol. Chem. 275:27221-27228.
52. Shaw, M. L., K. L. Stone, C. M. Colangelo, E. E. Gulcicek, and P. Palese. 2008. Cellular proteins in influenza virus particles. PLoS Pathog. 4:e1000085.
53. Simpson-Holley, M., et al. 2002. A functional link between the actin cyto-skeleton and lipid rafts during budding of filamentous influenza virions. Virology 301:212-225.
54. Söderberg, O., et al. 2006. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3:995-1000.
55. Taubenberger, J. K., and J. C. Kash. 2010. Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 7:440-451.
56. Ullrich, O., S. Reinsch, S. Urbe, M. Zerial, and R. G. Parton. 1996. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135:913-924.
57. Ward, B. M., and B. Moss. 2001. Vaccinia virus intracellular movement is associated with microtubules and independent of actin tails. J. Virol. 75: 11651-11663.
58. Watanabe, R., and R. A. Lamb. 2010. Influenza virus budding does not require a functional AAA+ ATPase, VPS4. Virus Res. 153:58-63.
59. Weisz, O. A., and E. Rodriguez-Boulan. 2009. Apical trafficking in epithelial cells: signals, clusters and motors. J. Cell Sci. 122:4253-4266.
60. Wileman, T. 2007. Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design? Annu. Rev. Microbiol. 61:149-167.
61. Wise, H. M., et al. 2009. A complicated message: identification of a novel PB1-related protein translated from influenza A virus segment 2 mRNA J. Virol. 83:8021-8031.