This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Enami, M. Articles by Enami, K. Search for Related Content PubMed PubMed Citation Articles by Enami, M. Articles by Enami, K.

 Previous Article  |  Next Article 

J. Virol., Oct 1996, 6653-6657, Vol 70, No. 10
Copyright © 1996, American Society for Microbiology

Influenza virus hemagglutinin and neuraminidase glycoproteins stimulate the membrane association of the matrix protein

M Enami and K Enami
Department of Biochemistry, Kanazawa University School of Medicine, Ishikawa, Japan.

We have analyzed the mechanism by which the matrix (M1) protein associates with cellular membranes during influenza A virus assembly. Interaction of the M1 protein with the viral hemagglutinin (HA) or neuraminidase (NA) glycoprotein was extensively analyzed by using wild- type and transfectant influenza viruses as well as recombinant vaccinia viruses expressing the M1 protein, HA, or NA. Membrane binding of the M1 protein was significantly stimulated at the late stage of virus infection. Using recombinant vaccinia viruses, we found that a relatively small fraction (20 to 40%) of the cytoplasmic M1 protein associated with cellular membranes in the absence of other viral proteins, while coexpression of the HA and the NA stimulated membrane binding of the M1 protein. The stimulatory effect of the NA (>90%) was significant and higher than that of the HA (>60%). Introduction of mutations into the cytoplasmic tail of the NA interfered with its stimulatory effect. Meanwhile, the HA may complement the defective NA and facilitate virus assembly in cells infected with the NA/TAIL(-) transfectant. In conclusion, the highly conserved cytoplasmic tails of the HA and NA play an important role in virus assembly.

This article has been cited by other articles:

• Swinteck, B. D., Lyles, D. S. (2008). Plasma Membrane Microdomains Containing Vesicular Stomatitis Virus M Protein Are Separate from Microdomains Containing G Protein and Nucleocapsids. J. Virol. 82: 5536-5547 [Abstract] [Full Text]  
• Imai, M., Kawasaki, K., Odagiri, T. (2008). Cytoplasmic Domain of Influenza B Virus BM2 Protein Plays Critical Roles in Production of Infectious Virus. J. Virol. 82: 728-739 [Abstract] [Full Text]  
• Muraki, Y., Murata, T., Takashita, E., Matsuzaki, Y., Sugawara, K., Hongo, S. (2007). A Mutation on Influenza C Virus M1 Protein Affects Virion Morphology by Altering the Membrane Affinity of the Protein. J. Virol. 81: 8766-8773 [Abstract] [Full Text]  
• Noton, S. L., Medcalf, E., Fisher, D., Mullin, A. E., 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: 2280-2290 [Abstract] [Full Text]  
• Chen, B. J., Leser, G. P., Morita, E., Lamb, R. A. (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 [Abstract] [Full Text]  
• McCown, M. F., Pekosz, A. (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 [Abstract] [Full Text]  
• Iwatsuki-Horimoto, K., Horimoto, T., Noda, T., Kiso, M., Maeda, J., Watanabe, S., Muramoto, Y., Fujii, K., Kawaoka, Y. (2006). The cytoplasmic tail of the influenza a virus m2 protein plays a role in viral assembly.. J. Virol. 80: 5233-5240 [Abstract] [Full Text]  
• Chen, B. J., Takeda, M., Lamb, R. A. (2005). Influenza Virus Hemagglutinin (H3 Subtype) Requires Palmitoylation of Its Cytoplasmic Tail for Assembly: M1 Proteins of Two Subtypes Differ in Their Ability To Support Assembly. J. Virol. 79: 13673-13684 [Abstract] [Full Text]  
• Bourmakina, S. V., Garcia-Sastre, A. (2005). The Morphology and Composition of Influenza A Virus Particles Are Not Affected by Low Levels of M1 and M2 Proteins in Infected Cells. J. Virol. 79: 7926-7932 [Abstract] [Full Text]  
• Liu, T., Ye, Z. (2005). Attenuating Mutations of the Matrix Gene of Influenza A/WSN/33 Virus. J. Virol. 79: 1918-1923 [Abstract] [Full Text]  
• Burleigh, L. M., Calder, L. J., Skehel, J. J., Steinhauer, D. A. (2005). Influenza A Viruses with Mutations in the M1 Helix Six Domain Display a Wide Variety of Morphological Phenotypes. J. Virol. 79: 1262-1270 [Abstract] [Full Text]  
• Imai, M., Watanabe, S., Ninomiya, A., Obuchi, M., Odagiri, T. (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 [Abstract] [Full Text]  
• 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: 9585-9591 [Abstract] [Full Text]  
• Watanabe, S., Imai, M., Ohara, Y., Odagiri, T. (2003). Influenza B Virus BM2 Protein Is Transported through the trans-Golgi Network as an Integral Membrane Protein. J. Virol. 77: 10630-10637 [Abstract] [Full Text]  
• Horimoto, T., Takada, A., Iwatsuki-Horimoto, K., Hatta, M., Goto, H., Kawaoka, Y. (2003). Generation of Influenza A Viruses with Chimeric (Type A/B) Hemagglutinins. J. Virol. 77: 8031-8038 [Abstract] [Full Text]  
• Bourmakina, S. V., Garcia-Sastre, A. (2003). Reverse genetics studies on the filamentous morphology of influenza A virus. J. Gen. Virol. 84: 517-527 [Abstract] [Full Text]  
• Liu, T., Ye, Z. (2002). Restriction of Viral Replication by Mutation of the Influenza Virus Matrix Protein. J. Virol. 76: 13055-13061 [Abstract] [Full Text]  
• Reid, A. H., Fanning, T. G., Janczewski, T. A., McCall, S., Taubenberger, J. K. (2002). Characterization of the 1918 "Spanish" Influenza Virus Matrix Gene Segment. J. Virol. 76: 10717-10723 [Abstract] [Full Text]  
• Luo, C., Nobusawa, E., Nakajima, K. (2002). Analysis of the desialidation process of the haemagglutinin protein of influenza B virus: the host-dependent desialidation step. J. Gen. Virol. 83: 1729-1734 [Abstract] [Full Text]  
• Mora, R., Rodriguez-Boulan, E., Palese, P., Garcia-Sastre, A. (2002). Apical Budding of a Recombinant Influenza A Virus Expressing a Hemagglutinin Protein with a Basolateral Localization Signal. J. Virol. 76: 3544-3553 [Abstract] [Full Text]  
• Pickl, W. F., Pimentel-Muinos, F. X., Seed, B. (2001). Lipid Rafts and Pseudotyping. J. Virol. 75: 7175-7183 [Abstract] [Full Text]  
• Gómez-Puertas, P., Albo, C., Pérez-Pastrana, E., Vivo, A., Portela, A. (2000). Influenza Virus Matrix Protein Is the Major Driving Force in Virus Budding. J. Virol. 74: 11538-11547 [Abstract] [Full Text]  
• Ali, A., Avalos, R. T., Ponimaskin, E., Nayak, D. P. (2000). Influenza Virus Assembly: Effect of Influenza Virus Glycoproteins on the Membrane Association of M1 Protein. J. Virol. 74: 8709-8719 [Abstract] [Full Text]  
• Zhang, J., Pekosz, A., Lamb, R. A. (2000). Influenza Virus Assembly and Lipid Raft Microdomains: a Role for the Cytoplasmic Tails of the Spike Glycoproteins. J. Virol. 74: 4634-4644 [Abstract] [Full Text]  
• Yao, Q., Compans, R. W. (2000). Filamentous particle formation by human parainfluenza virus type 2. J. Gen. Virol. 81: 1305-1312 [Abstract] [Full Text]  
• Godeke, G.-J., de Haan, C. A. M., Rossen, J. W. A., Vennema, H., Rottier, P. J. M. (2000). Assembly of Spikes into Coronavirus Particles Is Mediated by the Carboxy-Terminal Domain of the Spike Protein. J. Virol. 74: 1566-1571 [Abstract] [Full Text]  
• Luo, C., Nobusawa, E., Nakajima, K. (1999). An analysis of the role of neuraminidase in the receptor-binding activity of influenza B virus: the inhibitory effect of Zanamivir on haemadsorption. J. Gen. Virol. 80: 2969-2976 [Abstract] [Full Text]  
• Ye, Z., Liu, T., Offringa, D. P., McInnis, J., Levandowski, R. A. (1999). Association of Influenza Virus Matrix Protein with Ribonucleoproteins. J. Virol. 73: 7467-7473 [Abstract] [Full Text]  
• Plotch, S. J., O'Hara, B., Morin, J., Palant, O., LaRocque, J., Bloom, J. D., Lang, S. A. Jr., DiGrandi, M. J., Bradley, M., Nilakantan, R., Gluzman, Y. (1999). Inhibition of Influenza A Virus Replication by Compounds Interfering with the Fusogenic Function of the Viral Hemagglutinin. J. Virol. 73: 140-151 [Abstract] [Full Text]  
• Garoff, H., Hewson, R., Opstelten, D.-J. E. (1998). Virus Maturation by Budding. Microbiol. Mol. Biol. Rev. 62: 1171-1190 [Abstract] [Full Text]  
• Park, E. K., Castrucci, M. R., Portner, A., Kawaoka, Y. (1998). The M2 Ectodomain Is Important for Its Incorporation into Influenza A Virions. J. Virol. 72: 2449-2455 [Abstract] [Full Text]