The compensatory G88R change is essential in restoring the normal functions of influenza A/WSN/33 virus matrix protein 1 with a disrupted nuclear localization signal

Journal of Virology

Volumn 87, Issue 1, 2013, Pages 345-353

  Xie, Hang ^a   Lin, Zhengshi ^a   Mosier, Philip D ^b   Desai, Umesh R ^b   Gao, Yamei ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; GUANINE; MATRIX PROTEIN; MATRIX PROTEIN 1; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FEMALE; GENE FUNCTION; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA A; INFLUENZA VIRUS A; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TRANSMISSION ELECTRON MICROSCOPY; VIRUS REPLICATION; WILD TYPE;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; DOGS; FEMALE; INFLUENZA A VIRUS; MICE; MICE, INBRED BALB C; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MUTATION, MISSENSE; NUCLEAR LOCALIZATION SIGNALS; PROTEIN CONFORMATION; SUPPRESSION, GENETIC; VIRAL MATRIX PROTEINS; VIRUS REPLICATION;

ORTHOMYXOVIRIDAE;

EID: 84871982938     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02024-12     Document Type: Article

References (33)

1. Arzt S, Baudin F, Barge A, Timmins P, Burmeister WP, Ruigrok RW. 2001. Combined results from solution studies on intact influenza virus M1 protein and from a new crystal form of its N-terminal domain show that M1 is an elongated monomer. Virology 279(2):439-446.
2. Baudin F, Bach C, Cusack S, Ruigrok RW. 1994. Structure of influenza virus RNP. I. Influenza virus nucleoprotein melts secondary structure in panhandle RNA and exposes the bases to the solvent. EMBO J. 13(13): 3158-3165.
3. Elster C, Larsen K, Gagnon J, Ruigrok RW, Baudin F. 1997. Influenza virus M1 protein binds to RNA through its nuclear localization signal. J. Gen. Virol. 78(Pt 7):1589-1596.
4. Rossman JS, Lamb RA. 2011. Influenza virus assembly and budding. Virology 411(2):229-236.
5. Das SC, Watanabe S, Hatta M, Noda T, Neumann G, Ozawa M,Kawaoka Y. 2012. The highly conserved arginine residues at positions 76 through 78 of influenza A virus matrix protein M1 play an important role in viral replication by affecting the intracellular localization of M1. J. Virol. 86(3):1522-1530.
6. Martin K, Helenius A. 1991. Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell 67(1):117-130.
7. Sakaguchi A, Hirayama E, Hiraki A, Ishida Y, Kim J. 2003. Nuclear export of influenza viral ribonucleoprotein is temperature-dependently inhibited by dissociation of viral matrix protein. Virology 306(2):244-253.
8. Ye Z, Robinson D, Wagner RR. 1995. Nucleus-targeting domain of the matrix protein (M1) of influenza virus. J. Virol. 69(3):1964-1970.
9. Liu T, Ye Z. 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(18):9585-9591.
10. Liu T, Ye Z. 2005. Attenuating mutations of the matrix gene of influenza A/WSN/33 virus. J. Virol. 79(3):1918-1923.
11. Xie H, Liu TM, Lu X, Wu Z, Belser JA, Katz JM, Tumpey TM, Ye Z. 2009.Alive attenuated H1N1M1mutant provides broad cross-protection against influenza A viruses, including highly pathogenic A/Vietnam/1203/ 2004, in mice. J. Infect. Dis. 200(12):1874-1883.
12. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc. Natl. Acad. Sci. U. S. A. 97(11):6108-61131.
13. Qi L, Carbone KM, Ye Z, Liu T, Ovanesov M, Pletnikov M, Sauder C, Rubin SA. 2008. Genetic contributions to influenza virus attenuation in the rat brain. J. Neurovirol. 14(2):136-142.
14. Xie H, Liu T, Chen H, Huang X, Ye Z. 2007. Evaluating the vaccine potential of an influenza A viral hemagglutinin and matrix double insertion DNA plasmid. Vaccine 25(44):7649-7655.
15. Thaa B, Herrmann A, Veit M. 2009. The polybasic region is not essential for membrane binding of the matrix protein M1 of influenza virus. Virology 383(1):150-155.
16. Adamo JE, Liu T, Schmeisser F, Ye Z. 2009. Optimizing viral protein yield of influenza virus strain A/Vietnam/1203/2004 by modification of the neuraminidase gene. J. Virol. 83(9):4023-4029.
17. Burleigh LM, Calder LJ, Skehel JJ, Steinhauer DA. 2005. Influenza a viruses with mutations in the m1 helix six domain display a wide variety of morphological phenotypes. J. Virol. 79(2):1262-1270.
18. Ruigrok RW, Calder LJ, Wharton SA. 1989. Electron microscopy of the influenza virus submembranal structure. Virology 173(1):311-316.
19. Zhang J, Lamb RA. 1996. Characterization of the membrane association of the influenza virus matrix protein in living cells. Virology 225(2):255-266.
20. Arzt S, Petit I, Burmeister WP, Ruigrok RW, Baudin F. 2004. Structure of a knockout mutant of influenza virus M1 protein that has altered activities in membrane binding, oligomerisation and binding to NEP (NS2). Virus Res. 99(2):115-119.
21. Harris A, Forouhar F, Qiu S, Sha B, Luo M. 2001. The crystal structure of the influenza matrix protein M1 at neutral pH: M1-M1 protein interfaces can rotate in the oligomeric structures of M1. Virology 289(1):34-44.
22. Ruigrok RW, Barge A, Durrer P, Brunner J, Ma K, Whittaker GR. 2000. Membrane interaction of influenza virus M1 protein. Virology 267(2): 289-298.
23. Noton SL, Medcalf E, Fisher D, Mullin AE, Elton D, Digard P. 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(Pt 8):2280-2290.
24. Boulo, S, Akarsu, H, Ruigrok, RW, Baudin, F. 2007. Nuclear traffic of influenza virus proteins and ribonucleoprotein complexes. Virus Res. 124(1-2):12-21.
25. Bui M, Wills EG, Helenius A, Whittaker GR. 2000. Role of the influenza virus M1 protein in nuclear export of viral ribonucleoproteins. J. Virol. 74(4):1781-1786.
26. Whittaker G, Bui M, Helenius A. 1996. The role of nuclear import and export in influenza virus infection. Trends Cell Biol. 6(2):67-71.
27. Baudin F, Petit I, Weissenhorn W, Ruigrok RW. 2001. In vitro dissection of the membrane and RNP binding activities of influenza virus M1 protein. Virology 281(1):102-108.
28. Kretzschmar E, Bui M, Rose JK. 1996. Membrane association of influenza virus matrix protein does not require specific hydrophobic domains or the viral glycoproteins. Virology 220(1):37-45.
29. Ali A, Avalos RT, Ponimaskin E, Nayak DP. 2000. Influenza virus assembly: effect of influenza virus glycoproteins on the membrane association of M1 protein. J. Virol. 74(18):8709-8719.
30. Calder LJ, Wasilewski S, Berriman JA, Rosenthal PB. 2010. Structural organization of a filamentous influenza A virus. Proc. Natl. Acad. Sci. U. S. A. 107(23):10685-10690.
31. Sha B, Luo M. 1997. Crystallization and preliminary X-ray crystallographic studies of type A influenza virus matrix protein M1. Acta Crystallogr. D Biol. Crystallogr. 53(Pt 4):458-460.
32. Sha B, Luo M. 1997. Structure of a bifunctional membrane-RNA binding protein, influenza virus matrix protein M1. Nat. Struct. Biol. 4(3):239-244.
33. Elena SF, Carrasco P, Daros JA, Sanjuan R. 2006. Mechanisms of genetic robustness in RNA viruses. EMBO. Rep. 7(2):168-173.