Influenza Virus Assembly: Effect of Influenza Virus Glycoproteins on the Membrane Association of M1 Protein

doi:10.1128/JVI.74.18.8709-8719.2000

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Journal of Virology, September 2000, p. 8709-8719, Vol. 74, No. 18
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Influenza Virus Assembly: Effect of Influenza Virus Glycoproteins on the Membrane Association of M1 Protein

Ayub Ali,¹ Roy T. Avalos,¹ Evgeni Ponimaskin,² and Debi P. Nayak¹^,^*

Department of Microbiology, Immunology and Molecular Genetics, Molecular Biology Institute, Johnsson Comprehensive Cancer Center, UCLA School of Medicine, Los Angeles, California 90095-1747,¹ and Institut für Immunologie und Molekularbiologie, Fachbereich Veterinärmedizin der Freien Universität Berlin, D-10117 Berlin, Germany²

Received 22 February 2000/Accepted 8 June 2000

Influenza virus matrix protein (M1), a critical protein required for virus assembly and budding, is presumed to interact withviral glycoproteins on the outer side and viral ribonucleoproteinon the inner side. However, because of the inherent membrane-bindingability of M1 protein, it has been difficult to demonstrate thespecific interaction of M1 protein with hemagglutinin (HA) orneuraminidase (NA), the influenza virus envelope glycoproteins.Using Triton X-100 (TX-100) detergent treatment of membrane fractionsand floatation in sucrose gradients, we observed that the membrane-boundM1 protein expressed alone or coexpressed with heterologous Sendaivirus F was totally TX-100 soluble but the membrane-bound M1 proteinexpressed in the presence of HA and NA was predominantly detergentresistant and floated to the top of the density gradient. Furthermore,both the cytoplasmic tail and the transmembrane domain of HA facilitatedbinding of M1 to detergent-resistant membranes. Analysis of themembrane association of M1 in the early and late phases of theinfluenza virus infectious cycle revealed that the interactionof M1 with mature glycoproteins which associated with the detergent-resistantlipid rafts was responsible for the detergent resistance of membrane-boundM1. Immunofluorescence analysis by confocal microscopy also demonstratedthat, in influenza virus-infected cells, a fraction of M1 proteincolocalized with HA and associated with the HA in transit to theplasma membrane via the exocytic pathway. Similar results forcolocalization were obtained when M1 and HA were coexpressed andHA transport was blocked by monensin treatment. These studiesindicate that both HA and NA interact with influenza virus M1and that HA associates with M1 via its cytoplasmic tail and transmembranedomain.

^* Corresponding author. Mailing address: Department of Microbiology, Immunology and Molecular Genetics, Molecular Biology Institute,Johnsson Comprehensive Cancer Center, UCLA School of Medicine,Los Angeles, CA 90095-1747. Phone: (310) 825-8558. Fax: (310)206-3865. E-mail: dnayak{at}ucla.edu.

Journal of Virology, September 2000, p. 8709-8719, Vol. 74, No. 18
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

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