Studies of an influenza A virus temperature-sensitive mutant identify a late role for NP in the formation of infectious virions

Journal of Virology

Volumn 83, Issue 2, 2009, Pages 562-571

  Noton, Sarah L ^a,c   Simpson Holley, Martha ^a,d   Medcalf, Elizabeth ^a,f   Wise, Helen M ^a   Hutchinson, Edward C ^a   McCauley, John W ^b,e   Digard, Paul ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^e NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^f ANIMAL HEALTH TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS NUCLEOPROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FOWL PLAGUE VIRUS; GENE MUTATION; GENE REPLICATION; GENE SEQUENCE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INFLUENZA VIRUS A; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; RNA SYNTHESIS; SEQUENCE ANALYSIS; TEMPERATURE SENSITIVE MUTANT; VIRION; VIRUS ASSEMBLY; VIRUS GENE; VIRUS LOAD; VIRUS PARTICLE; VIRUS STRAIN; WILD TYPE;

AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; CHICK EMBRYO; CHICKENS; DOGS; HOT TEMPERATURE; HUMANS; INFLUENZA A VIRUS; MUTANT PROTEINS; MUTATION, MISSENSE; PLAQUE ASSAY; RNA, VIRAL; RNA-BINDING PROTEINS; VIRAL CORE PROTEINS; VIRAL MATRIX PROTEINS; VIRAL PROTEINS; VIRION; VIRUS ASSEMBLY; VIRUS REPLICATION;

FOWL PLAGUE VIRUS; INFLUENZA A VIRUS;

EID: 58149526763     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01424-08     Document Type: Article

References (72)

1. Akarsu, H., W. P. Burmeister, C. Petosa, I. Petit, C. W. Muller, R. W. Ruigrok, and F. Baudin. 2003. Crystal structure of the M1 protein-binding domain of the influenza A virus nuclear export protein (NEP/NS2). EMBO J. 22:4646-4655.
2. Ali, A., R. T. Avalos, E. Ponimaskin, and D. P. Nayak. 2000. Influenza virus assembly: effect of influenza virus glycoproteins on the membrane association of M1 protein. J. Virol. 74:8709-8719.
3. Almond, J. W., D. McGeoch, and R. D. Barry. 1977. Method for assigning temperature-sensitive mutations of influenza viruses to individual segments of the genome. Virology 81:62-73.
4. Almond, J. W., D. McGeoch, and R. D. Barry. 1979. Temperature-sensitive mutants of fowl plague virus: isolation and genetic characterization. Virology 92:416-427.
5. 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.
6. 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.
7. Beaton, A. R., and R. M. Krug. 1986. Transcription antitermination during influenza viral template RNA synthesis requires the nucleocapsid protein and the absence of a 5′ capped end. Proc. Natl. Acad. Sci. USA 83:6282-6286.
8. Biswas, S. K., P. L. Boutz, and D. P. Nayak. 1998. Influenza virus nucleoprotein interacts with influenza virus polymerase proteins. J. Virol. 72:5493-5501.
9. 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.
10. Bourmakina, S. V., and A. Garcia-Sastre. 2003. Reverse genetics studies on the filamentous morphology of influenza A virus. J. Gen. Virol. 84:517-527.
11. Bron, R., A. P. Kendal, H. D. Klenk, and J. Wilschut. 1993. Role of the M2 protein in influenza virus membrane fusion: effects of amantadine and monensin on fusion kinetics. Virology 195:808-811.
12. Burleigh, L. M., L. J. Calder, J. J. Skehel, and D. A. Steinhauer. 2005. Influenza A viruses with mutations in the m1 helix six domain display a wide variety of morphological phenotypes. J. Virol. 79:1262-1270.
13. 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.
14. Chen, B. J., and R. A. Lamb. 2008. Mechanisms for enveloped virus budding: can some viruses do without an ESCRT? Virology 372:221-232.
15. Chen, B. J., G. P. Leser, D. Jackson, and R. A. Lamb. 2008. The influenza virus M2 protein cytoplasmic tail interacts with the M1 protein and influences virus assembly at the site of virus budding. J. Virol. 82:10059-10070.
16. 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.
17. Dalton, R. M., A. E. Mullin, M. J. Amorim, E. Medcalf, L. S. Tiley, and P. Digard. 2006. Temperature sensitive influenza A virus genome replication results from low thermal stability of polymerase-cRNA complexes. Virol. J. 3:58.
18. de Wit, E., M. I. Spronken, T. M. Bestebroer, G. F. Rimmelzwaan, A. D. Osterhaus, and R. A. Fouchier. 2004. Efficient generation and growth of influenza virus A/PR/8/34 from eight cDNA fragments. Virus Res. 103:155-161.
19. Digard, P., D. Elton, K. Bishop, E. Medcalf, A. Weeds, and B. Pope. 1999. Modulation of nuclear localization of the influenza virus nucleoprotein through interaction with actin filaments. J. Virol. 73:2222-2231.
20. Donald, H. B., and A. Isaacs. 1954. Counts of influenza virus particles. J. Gen. Microbiol. 10:457-464.
21. Elleman, C. J., and W. S. Barclay. 2004. The M1 matrix protein controls the filamentous phenotype of influenza A virus. Virology 321:144-153.
22. Elton, D., M. J. Amorim, L. Medcalf, and P. Digard. 2005. 'Genome gating'; polarized intranuclear trafficking of influenza virus RNPs. Biol. Lett. 1:113-117.
23. Elton, D., P. Digard, L. Tiley, and J. Ortin. 2006. Structure and function of the influenza virus RNP, p. 1-36. In E. Yawaoka (ed.), Influenza virology: current topics. Caister Academic Press, Wymondham, United Kingdom.
24. Elton, D., L. Medcalf, K. Bishop, D. Harrison, and P. Digard. 1999. Identification of amino acid residues of influenza virus nucleoprotein essential for RNA binding. J. Virol. 73:7357-7367.
25. Elton, D., M. Simpson-Holley, K. Archer, L. Medcalf, R. Hallam, J. McCauley, and P. Digard. 2001. Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J. Virol. 75:408-419.
26. Gog, J. R., S. Afonso Edos, R. M. Dalton, I. Leclercq, L. Tiley, D. Elton, J. C. von Kirchbach, N. Naffakh, N. Escriou, and P. Digard. 2007. Codon conservation in the influenza A virus genome defines RNA packaging signals. Nucleic Acids Res. 35:1897-1907.
27. Gomez-Puertas, P., C. Albo, E. Perez-Pastrana, A. Vivo, and A. Portela. 2000. Influenza virus matrix protein is the major driving force in virus budding. J. Virol. 74:11538-11547.
28. Harris, A., G. Cardone, D. C. Winkler, J. B. Heymann, M. Brecher, J. M. White, and A. C. Steven. 2006. Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc. Natl. Acad. Sci. USA 103:19123-19127.
29. Honda, A., K. Ueda, K. Nagata, and A. Ishihama. 1988. RNA polymerase of influenza virus: role of NP in RNA chain elongation. J. Biochem. 104:1021-1026.
30. Huang, T. S., P. Palese, and M. Krystal. 1990. Determination of influenza virus proteins required for genome replication. J. Virol. 64:5669-5673.
31. 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.
32. Imai, M., S. Watanabe, A. Ninomiya, M. Obuchi, and T. Odagiri. 2004. Influenza B virus BM2 protein is a crucial component for incorporation of viral ribonucleoprotein complex into virions during virus assembly. J. Virol. 78:11007-11015.
33. Iwatsuki-Horimoto, K., T. Horimoto, T. Noda, M. Kiso, J. Maeda, S. Watanabe, Y. Muramoto, K. Fujii, and Y. Kawaoka. 2006. The cytoplasmic tail of the influenza A virus M2 protein plays a role in viral assembly. J. Virol. 80:5233-5240.
34. Jin, H., G. P. Leser, J. Zhang, and R. A. Lamb. 1997. Influenza virus hemagglutinin and neuraminidase cytoplasmic tails control particle shape. EMBO J. 16:1236-1247.
35. Krug, R. M., M. Ueda, and P. Palese. 1975. Temperature-sensitive mutants of influenza WSN virus defective in virus-specific RNA synthesis. J. Virol. 16:790-796.
36. Latham, T., and J. M. Galarza. 2001. Formation of wild-type and chimeric influenza virus-like particles following simultaneous expression of only four structural proteins. J. Virol. 75:6154-6165.
37. Lee, M. T., K. Bishop, L. Medcalf, D. Elton, P. Digard, and L. Tiley. 2002. Definition of the minimal viral components required for the initiation of unprimed RNA synthesis by influenza virus RNA polymerase. Nucleic Acids Res. 30:429-438.
38. Liu, T., J. Muller, and Z. Ye. 2002. Association of influenza virus matrix protein with ribonucleoproteins may control viral growth and morphology. Virology 304:89-96.
39. Liu, T., and Z. Ye. 2004. Introduction of a temperature-sensitive phenotype into influenza A/WSN/33 virus by altering the basic amino acid domain of influenza virus matrix protein. J. Virol. 78:9585-9591.
40. Mahy, B. W. J. 1983. Mutants of influenza virus, p. 192-254. In P. Palese and D. W. Kingsbury (ed.), Genetics of influenza viruses. Springer-Verlag, Vienna, Austria.
41. Mahy, B. W. J., T. Barrett, S. T. Nichol, C. R. Penn, and A. J. Wolstenholme. 1981. Analysis of the functions of influenza virus genome RNA segments by use of temperature sensitive mutants of fowl plague virus, p. 379-387. In D. H. L. Bishop and R. W. Compans (ed.), The replication of negative stranded viruses. Elsevier North Holland, Inc., New York, NY.
42. Mandler, J., K. Muller, and C. Scholtissek. 1991. Mutants and revertants of an avian influenza A virus with temperature-sensitive defects in the nucleoprotein and PB2. Virology 181:512-519.
43. Mandler, J., and C. Scholtissek. 1989. Localisation of the temperaturesensitive defect in the nucleoprotein of an influenza A/FPV/Rostock/34 virus. Virus Res. 12:113-121.
44. 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.
45. Martin, K., and A. Helenius. 1991. Transport of incoming influenza virus nucleocapsids into the nucleus. J. Virol. 65:232-244.
46. McCown, M. F., and A. Pekosz. 2006. Distinct domains of the influenza a virus M2 protein cytoplasmic tail mediate binding to the M1 protein and facilitate infectious virus production. J. Virol. 80:8178-8189.
47. McCown, M. F., and A. Pekosz. 2005. The influenza A virus M2 cytoplasmic tail is required for infectious virus production and efficient genome packaging. J. Virol. 79:3595-3605.
48. Medcalf, L., E. Poole, D. Elton, and P. Digard. 1999. Temperature-sensitive lesions in two influenza A viruses defective for replicative transcription disrupt RNA binding by the nucleoprotein. J. Virol. 73:7349-7356.
49. Momose, F., Y. Kikuchi, K. Komase, and Y. Morikawa. 2007. Visualization of microtubule-mediated transport of influenza viral progeny ribonucleoprotein. Microbes Infect. 9:1422-1433.
50. 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.
51. Ng, A. K., H. Zhang, K. Tan, Z. Li, J. H. Liu, P. K. Chan, S. M. Li, W. Y. Chan, S. W. Au, A. Joachimiak, T. Walz, J. H. Wang, and P. C. Shaw. 2008. Structure of the influenza virus A H5N1 nucleoprotein: implications for RNA binding, oligomerization, and vaccine design. FASEB J. 22:3638-3647.
52. Noton, S. L., E. Medcalf, D. Fisher, A. E. Mullin, D. Elton, and P. Digard. 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.
53. O'Neill, R. E., R. Jaskunas, G. Blobel, P. Palese, and J. Moroianu. 1995. Nuclear import of influenza virus RNA can be mediated by viral nucleoprotein and transport factors required for protein import. J. Biol. Chem. 270: 22701-22704.
54. Overby, A. K., R. F. Pettersson, and E. P. Neve. 2007. The glycoprotein cytoplasmic tail of Uukuniemi virus (Bunyaviridae) interacts with ribonucleoproteins and is critical for genome packaging. J. Virol. 81:3198-3205.
55. 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.
56. 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.
57. Ruigrok, R. W., P. C. Krijgsman, F. M. de Ronde-Verloop, and J. C. de Jong. 1985. Natural heterogeneity of shape, infectivity and protein composition in an influenza A (H3N2) virus preparation. Virus Res. 3:69-76.
58. Scholtissek, C., and H. Becht. 1971. Binding of ribonucleic acids to the RNP-antigen protein of influenza viruses. J. Gen. Virol. 10:11-16.
59. Scholtissek, C., and A. L. Bowles. 1975. Isolation and characterization of temperature-sensitive mutants of fowl plague virus. Virology 67:576-587.
60. Schulze, I. T. 1972. The structure of influenza virus. II. A model based on the morphology and composition of subviral particles. Virology 47:181-196.
61. Shapiro, G. I., and R. M. Krug. 1988. Influenza virus RNA replication in vitro: synthesis of viral template RNAs and virion RNAs in the absence of an added primer. J. Virol. 62:2285-2290.
62. Simpson-Holley, M., D. Ellis, D. Fisher, D. Elton, J. McCauley, and P. Digard. 2002. A functional link between the actin cytoskeleton and lipid rafts during budding of filamentous influenza virions. Virology 301:212-225.
63. Thierry, F., and O. Danos. 1982. Use of specific single stranded DNA probes cloned in M13 to study the RNA synthesis of four temperature- sensitive mutants of HK/68 influenza virus. Nucleic Acids Res. 10:2925-2938.
64. Tomley, F. M., and I. J. Roditi. 1984. Nucleotide-sequence of RNA segment 5, encoding the nucleoprotein, of influenza A/FPV/Rostock/34. Virus Res. 1:625-630.
65. Vreede, F. T., T. E. Jung, and G. G. Brownlee. 2004. Model suggesting that replication of influenza virus is regulated by stabilization of replicative intermediates. J. Virol. 78:9568-9572.
66. Yamaguchi, M., R. Danev, K. Nishiyama, K. Sugawara, and K. Nagayama. 2008. Zernike phase contrast electron microscopy of ice-embedded influenza A virus. J. Struct. Biol. 162:271-276.
67. Yamanaka, K., A. Ishihama, and K. Nagata. 1990. Reconstitution of influenza virus RNA-nucleoprotein complexes structurally resembling native viral ribonucleoprotein cores. J. Biol. Chem. 265:11151-11155.
68. Ye, Q., R. M. Krug, and Y. J. Tao. 2006. The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 444:1078-1082.
69. Ye, Z., T. Liu, D. P. Offringa, J. McInnis, and R. A. Levandowski. 1999. Association of influenza virus matrix protein with ribonucleoproteins. J. Virol. 73:7467-7473.
70. Zhang, J., and R. A. Lamb. 1996. Characterization of the membrane association of the influenza virus matrix protein in living cells. Virology 225:255-266.
71. Zhang, J., G. P. Leser, A. Pekosz, and R. A. Lamb. 2000. The cytoplasmic tails of the influenza virus spike glycoproteins are required for normal genome packaging. Virology 269:325-334.
72. Zvonarjev, A. Y., and Y. Z. Ghendon. 1980. Influence of membrane (M) protein on influenza A virus virion transcriptase activity in vitro and its susceptibility to rimantadine. J. Virol. 33:583-586.