This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow An erratum has been published
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Manié, S. N.
Right arrow Articles by Gerlier, D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Manié, S. N.
Right arrow Articles by Gerlier, D.

 Previous Article  |  Next Article 

Journal of Virology, January 2000, p. 305-311, Vol. 74, No. 1
0022-538X/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Measles Virus Structural Components Are Enriched into Lipid Raft Microdomains: a Potential Cellular Location for Virus Assembly

Serge N. Manié,* Sylvain Debreyne, Séverine Vincent, and Denis Gerlier

Immunité et Infections Virales, IVMC, CNRS-UCBL UMR5537, 69372 Lyon Cedex 08, France

Received 13 May 1999/Accepted 21 September 1999

The process of measles virus (MV) assembly and subsequent budding is thought to occur in localized regions of the plasma membrane, to favor specific incorporation of viral components, and to facilitate the exclusion of host proteins. We demonstrate that during the course of virus replication, a significant proportion of MV structural proteins were selectively enriched in the detergent-resistant glycosphingolipids and cholesterol-rich membranes (rafts). Isolated rafts could infect the cell through a membrane fusion step and thus contained all of the components required to create a functional virion. However, they could be distinguished from the mature virions with regards to density and Triton X-100 resistance behavior. We further show that raft localization of the viral internal nucleoprotein and matrix protein was independent of the envelope glycoproteins, indicating that raft membranes could provide a platform for MV assembly. Finally, at least part of the raft MV components were included in the viral particle during the budding process. Taken together, these results strongly suggest a role for raft membranes in the processes of MV assembly and budding.


* Corresponding author. Mailing address: Immunite et Infections Virales, CNRS-UCBL UMR5537, Faculte de Medecine Lyon RTH Laennec, 69372 Lyon Cedex 08, France. Phone: 33 (0)4-78-77-87-53. Fax: 33 (0)4-78-77-87-54. E-mail: manie{at}laennec1.univ-lyon1.fr.


Journal of Virology, January 2000, p. 305-311, Vol. 74, No. 1
0022-538X/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Iwasaki, M., Takeda, M., Shirogane, Y., Nakatsu, Y., Nakamura, T., Yanagi, Y. (2009). The Matrix Protein of Measles Virus Regulates Viral RNA Synthesis and Assembly by Interacting with the Nucleocapsid Protein. J. Virol. 83: 10374-10383 [Abstract] [Full Text]  
  • Agnihothram, S. S., Dancho, B., Grant, K. W., Grimes, M. L., Lyles, D. S., Nunberg, J. H. (2009). Assembly of Arenavirus Envelope Glycoprotein GPC in Detergent-Soluble Membrane Microdomains. J. Virol. 83: 9890-9900 [Abstract] [Full Text]  
  • Robinzon, S., Dafa-Berger, A., Dyer, M. D., Paeper, B., Proll, S. C., Teal, T. H., Rom, S., Fishman, D., Rager-Zisman, B., Katze, M. G. (2009). Impaired Cholesterol Biosynthesis in a Neuronal Cell Line Persistently Infected with Measles Virus. J. Virol. 83: 5495-5504 [Abstract] [Full Text]  
  • Clemente, R., de Parseval, A., Perez, M., de la Torre, J. C. (2009). Borna Disease Virus Requires Cholesterol in both Cellular Membrane and Viral Envelope for Efficient Cell Entry. J. Virol. 83: 2655-2662 [Abstract] [Full Text]  
  • Bhattacharya, B., Roy, P. (2008). Bluetongue Virus Outer Capsid Protein VP5 Interacts with Membrane Lipid Rafts via a SNARE Domain. J. Virol. 82: 10600-10612 [Abstract] [Full Text]  
  • Noisakran, S., Dechtawewat, T., Avirutnan, P., Kinoshita, T., Siripanyaphinyo, U., Puttikhunt, C., Kasinrerk, W., Malasit, P., Sittisombut, N. (2008). Association of dengue virus NS1 protein with lipid rafts. J. Gen. Virol. 89: 2492-2500 [Abstract] [Full Text]  
  • Espenel, C., Margeat, E., Dosset, P., Arduise, C., Le Grimellec, C., Royer, C. A., Boucheix, C., Rubinstein, E., Milhiet, P.-E. (2008). Single-molecule analysis of CD9 dynamics and partitioning reveals multiple modes of interaction in the tetraspanin web. JCB 182: 765-776 [Abstract] [Full Text]  
  • 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]  
  • Runkler, N., Dietzel, E., Moll, M., Klenk, H.-D., Maisner, A. (2008). Glycoprotein targeting signals influence the distribution of measles virus envelope proteins and virus spread in lymphocytes. J. Gen. Virol. 89: 687-696 [Abstract] [Full Text]  
  • Capul, A. A., Perez, M., Burke, E., Kunz, S., Buchmeier, M. J., de la Torre, J. C. (2007). Arenavirus Z-Glycoprotein Association Requires Z Myristoylation but Not Functional RING or Late Domains. J. Virol. 81: 9451-9460 [Abstract] [Full Text]  
  • Kueng, H. J., Leb, V. M., Haiderer, D., Raposo, G., Thery, C., Derdak, S. V., Schmetterer, K. G., Neunkirchner, A., Sillaber, C., Seed, B., Pickl, W. F. (2007). General Strategy for Decoration of Enveloped Viruses with Functionally Active Lipid-Modified Cytokines. J. Virol. 81: 8666-8676 [Abstract] [Full Text]  
  • Imhoff, H., von Messling, V., Herrler, G., Haas, L. (2007). Canine Distemper Virus Infection Requires Cholesterol in the Viral Envelope. J. Virol. 81: 4158-4165 [Abstract] [Full Text]  
  • Pohl, C., Duprex, W. P., Krohne, G., Rima, B. K., Schneider-Schaulies, S. (2007). Measles virus M and F proteins associate with detergent-resistant membrane fractions and promote formation of virus-like particles. J. Gen. Virol. 88: 1243-1250 [Abstract] [Full Text]  
  • Fleming, E. H., Kolokoltsov, A. A., Davey, R. A., Nichols, J. E., Roberts, N. J. Jr. (2006). Respiratory Syncytial Virus F Envelope Protein Associates with Lipid Rafts without a Requirement for Other Virus Proteins. J. Virol. 80: 12160-12170 [Abstract] [Full Text]  
  • Bukrinsky, M., Sviridov, D. (2006). Human immunodeficiency virus infection and macrophage cholesterol metabolism.. J. Leukoc. Biol. 80: 1044-1051 [Abstract] [Full Text]  
  • Laliberte, J. P., McGinnes, L. W., Peeples, M. E., Morrison, T. G. (2006). Integrity of membrane lipid rafts is necessary for the ordered assembly and release of infectious newcastle disease virus particles.. J. Virol. 80: 10652-10662 [Abstract] [Full Text]  
  • Oomens, A. G. P., Bevis, K. P., Wertz, G. W. (2006). The Cytoplasmic Tail of the Human Respiratory Syncytial Virus F Protein Plays Critical Roles in Cellular Localization of the F Protein and Infectious Progeny Production. J. Virol. 80: 10465-10477 [Abstract] [Full Text]  
  • Bhattacharya, J., Repik, A., Clapham, P. R. (2006). Gag regulates association of human immunodeficiency virus type 1 envelope with detergent-resistant membranes.. J. Virol. 80: 5292-5300 [Abstract] [Full Text]  
  • Reuter, T., Weissbrich, B., Schneider-Schaulies, S., Schneider-Schaulies, J. (2006). RNA Interference with Measles Virus N, P, and L mRNAs Efficiently Prevents and with Matrix Protein mRNA Enhances Viral Transcription.. J. Virol. 80: 5951-5957 [Abstract] [Full Text]  
  • Parr, R. D., Storey, S. M., Mitchell, D. M., McIntosh, A. L., Zhou, M., Mir, K. D., Ball, J. M. (2006). The Rotavirus Enterotoxin NSP4 Directly Interacts with the Caveolar Structural Protein Caveolin-1. J. Virol. 80: 2842-2854 [Abstract] [Full Text]  
  • Goluszko, P., Nowicki, B. (2005). Membrane Cholesterol: a Crucial Molecule Affecting Interactions of Microbial Pathogens with Mammalian Cells. Infect. Immun. 73: 7791-7796 [Full Text]  
  • Murray, J. L., Mavrakis, M., McDonald, N. J., Yilla, M., Sheng, J., Bellini, W. J., Zhao, L., Le Doux, J. M., Shaw, M. W., Luo, C.-C., Lippincott-Schwartz, J., Sanchez, A., Rubin, D. H., Hodge, T. W. (2005). Rab9 GTPase Is Required for Replication of Human Immunodeficiency Virus Type 1, Filoviruses, and Measles Virus. J. Virol. 79: 11742-11751 [Abstract] [Full Text]  
  • Chan, W.-E., Lin, H.-H., Chen, S. S.-L. (2005). Wild-Type-Like Viral Replication Potential of Human Immunodeficiency Virus Type 1 Envelope Mutants Lacking Palmitoylation Signals. J. Virol. 79: 8374-8387 [Abstract] [Full Text]  
  • Cantin, R., Methot, S., Tremblay, M. J. (2005). Plunder and Stowaways: Incorporation of Cellular Proteins by Enveloped Viruses. J. Virol. 79: 6577-6587 [Full Text]  
  • Brown, E. L., Lyles, D. S. (2005). Pseudotypes of Vesicular Stomatitis Virus with CD4 Formed by Clustering of Membrane Microdomains during Budding. J. Virol. 79: 7077-7086 [Abstract] [Full Text]  
  • Wagner, R., Herwig, A., Azzouz, N., Klenk, H. D. (2005). Acylation-Mediated Membrane Anchoring of Avian Influenza Virus Hemagglutinin Is Essential for Fusion Pore Formation and Virus Infectivity. J. Virol. 79: 6449-6458 [Abstract] [Full Text]  
  • Kitagawa, Y., Tani, H., Limn, C. K., Matsunaga, T. M., Moriishi, K., Matsuura, Y. (2005). Ligand-Directed Gene Targeting to Mammalian Cells by Pseudotype Baculoviruses. J. Virol. 79: 3639-3652 [Abstract] [Full Text]  
  • Hoenen, T., Volchkov, V., Kolesnikova, L., Mittler, E., Timmins, J., Ottmann, M., Reynard, O., Becker, S., Weissenhorn, W. (2005). VP40 Octamers Are Essential for Ebola Virus Replication. J. Virol. 79: 1898-1905 [Abstract] [Full Text]  
  • Zhang, L., Bukreyev, A., Thompson, C. I., Watson, B., Peeples, M. E., Collins, P. L., Pickles, R. J. (2005). Infection of Ciliated Cells by Human Parainfluenza Virus Type 3 in an In Vitro Model of Human Airway Epithelium. J. Virol. 79: 1113-1124 [Abstract] [Full Text]  
  • Campbell, S., Gaus, K., Bittman, R., Jessup, W., Crowe, S., Mak, J. (2004). The Raft-Promoting Property of Virion-Associated Cholesterol, but Not the Presence of Virion-Associated Brij 98 Rafts, Is a Determinant of Human Immunodeficiency Virus Type 1 Infectivity. J. Virol. 78: 10556-10565 [Abstract] [Full Text]  
  • Avota, E., Muller, N., Klett, M., Schneider-Schaulies, S. (2004). Measles Virus Interacts with and Alters Signal Transduction in T-Cell Lipid Rafts. J. Virol. 78: 9552-9559 [Abstract] [Full Text]  
  • Devaux, P., Christiansen, D., Plumet, S., Gerlier, D. (2004). Cell surface activation of the alternative complement pathway by the fusion protein of measles virus. J. Gen. Virol. 85: 1665-1673 [Abstract] [Full Text]  
  • Favoreel, H. W., Mettenleiter, T. C., Nauwynck, H. J. (2004). Copatching and Lipid Raft Association of Different Viral Glycoproteins Expressed on the Surfaces of Pseudorabies Virus-Infected Cells. J. Virol. 78: 5279-5287 [Abstract] [Full Text]  
  • Gao, L., Aizaki, H., He, J.-W., Lai, M. M. C. (2004). Interactions between Viral Nonstructural Proteins and Host Protein hVAP-33 Mediate the Formation of Hepatitis C Virus RNA Replication Complex on Lipid Raft. J. Virol. 78: 3480-3488 [Abstract] [Full Text]  
  • Nguyen, D. G., Booth, A., Gould, S. J., Hildreth, J. E. K. (2003). Evidence That HIV Budding in Primary Macrophages Occurs through the Exosome Release Pathway. J. Biol. Chem. 278: 52347-52354 [Abstract] [Full Text]  
  • Dolganiuc, V., McGinnes, L., Luna, E. J., Morrison, T. G. (2003). Role of the Cytoplasmic Domain of the Newcastle Disease Virus Fusion Protein in Association with Lipid Rafts. J. Virol. 77: 12968-12979 [Abstract] [Full Text]  
  • Bender, F. C., Whitbeck, J. C., Ponce de Leon, M., Lou, H., Eisenberg, R. J., Cohen, G. H. (2003). Specific Association of Glycoprotein B with Lipid Rafts during Herpes Simplex Virus Entry. J. Virol. 77: 9542-9552 [Abstract] [Full Text]  
  • Chazal, N., Gerlier, D. (2003). Virus Entry, Assembly, Budding, and Membrane Rafts. Microbiol. Mol. Biol. Rev. 67: 226-237 [Abstract] [Full Text]  
  • Inoue, M., Tokusumi, Y., Ban, H., Kanaya, T., Shirakura, M., Tokusumi, T., Hirata, T., Nagai, Y., Iida, A., Hasegawa, M. (2003). A New Sendai Virus Vector Deficient in the Matrix Gene Does Not Form Virus Particles and Shows Extensive Cell-to-Cell Spreading. J. Virol. 77: 6419-6429 [Abstract] [Full Text]  
  • Browne, H., Bruun, B., Whiteley, A., Minson, T. (2003). Analysis of the role of the membrane-spanning and cytoplasmic tail domains of herpes simplex virus type 1 glycoprotein D in membrane fusion. J. Gen. Virol. 84: 1085-1089 [Abstract] [Full Text]  
  • Briggs, J. A. G., Wilk, T., Fuller, S. D. (2003). Do lipid rafts mediate virus assembly and pseudotyping?. J. Gen. Virol. 84: 757-768 [Abstract] [Full Text]  
  • Shi, S. T., Lee, K.-J., Aizaki, H., Hwang, S. B., Lai, M. M. C. (2003). Hepatitis C Virus RNA Replication Occurs on a Detergent-Resistant Membrane That Cofractionates with Caveolin-2. J. Virol. 77: 4160-4168 [Abstract] [Full Text]  
  • McCurdy, L. H., Graham, B. S. (2003). Role of Plasma Membrane Lipid Microdomains in Respiratory Syncytial Virus Filament Formation. J. Virol. 77: 1747-1756 [Abstract] [Full Text]  
  • Ding, L., Derdowski, A., Wang, J.-J., Spearman, P. (2003). Independent Segregation of Human Immunodeficiency Virus Type 1 Gag Protein Complexes and Lipid Rafts. J. Virol. 77: 1916-1926 [Abstract] [Full Text]  
  • Lee, G. E., Church, G. A., Wilson, D. W. (2003). A Subpopulation of Tegument Protein vhs Localizes to Detergent-Insoluble Lipid Rafts in Herpes Simplex Virus-Infected Cells. J. Virol. 77: 2038-2045 [Abstract] [Full Text]  
  • Li, M., Yang, C., Tong, S., Weidmann, A., Compans, R. W. (2002). Palmitoylation of the Murine Leukemia Virus Envelope Protein Is Critical for Lipid Raft Association and Surface Expression. J. Virol. 76: 11845-11852 [Abstract] [Full Text]  
  • Guyader, M., Kiyokawa, E., Abrami, L., Turelli, P., Trono, D. (2002). Role for Human Immunodeficiency Virus Type 1 Membrane Cholesterol in Viral Internalization. J. Virol. 76: 10356-10364 [Abstract] [Full Text]  
  • Llano, M., Kelly, T., Vanegas, M., Peretz, M., Peterson, T. E., Simari, R. D., Poeschla, E. M. (2002). Blockade of Human Immunodeficiency Virus Type 1 Expression by Caveolin-1. J. Virol. 76: 9152-9164 [Abstract] [Full Text]  
  • Stuart, A. D., Eustace, H. E., McKee, T. A., Brown, T. D. K. (2002). A Novel Cell Entry Pathway for a DAF-Using Human Enterovirus Is Dependent on Lipid Rafts. J. Virol. 76: 9307-9322 [Abstract] [Full Text]  
  • Brown, G., Rixon, H. W. McL., Sugrue, R. J. (2002). Respiratory syncytial virus assembly occurs in GM1-rich regions of the host-cell membrane and alters the cellular distribution of tyrosine phosphorylated caveolin-1. J. Gen. Virol. 83: 1841-1850 [Abstract] [Full Text]  
  • Lu, X., Xiong, Y., Silver, J. (2002). Asymmetric Requirement for Cholesterol in Receptor-Bearing but Not Envelope-Bearing Membranes for Fusion Mediated by Ecotropic Murine Leukemia Virus. J. Virol. 76: 6701-6709 [Abstract] [Full Text]  
  • Nguyen, D. H., Taub, D. (2002). Cholesterol is essential for macrophage inflammatory protein 1beta binding and conformational integrity of CC chemokine receptor 5. Blood 99: 4298-4306 [Abstract] [Full Text]  
  • Vincent, S., Tigaud, I., Schneider, H., Buchholz, C. J., Yanagi, Y., Gerlier, D. (2002). Restriction of Measles Virus RNA Synthesis by a Mouse Host Cell Line: trans-Complementation by Polymerase Components or a Human Cellular Factor(s). J. Virol. 76: 6121-6130 [Abstract] [Full Text]  
  • Christiansen, D., De Sousa, E. R., Loveland, B., Kyriakou, P., Lanteri, M., Wild, F. T., Gerlier, D. (2002). A CD46CD[55-46] chimeric receptor, eight short consensus repeats long, acts as an inhibitor of both CD46 (MCP)- and CD150 (SLAM)-mediated cell-cell fusion induced by CD46-using measles virus. J. Gen. Virol. 83: 1147-1155 [Abstract] [Full Text]  
  • Popik, W., Alce, T. M., Au, W.-C. (2002). Human Immunodeficiency Virus Type 1 Uses Lipid Raft-Colocalized CD4 and Chemokine Receptors for Productive Entry into CD4+ T Cells. J. Virol. 76: 4709-4722 [Abstract] [Full Text]  
  • Bavari, S., Bosio, C. M., Wiegand, E., Ruthel, G., Will, A. B., Geisbert, T. W., Hevey, M., Schmaljohn, C., Schmaljohn, A., Aman, M. J. (2002). Lipid Raft Microdomains: A Gateway for Compartmentalized Trafficking of Ebola and Marburg Viruses. JEM 195: 593-602 [Abstract] [Full Text]  
  • Brown, G., Aitken, J., Rixon, H. W. McL., Sugrue, R. J. (2002). Caveolin-1 is incorporated into mature respiratory syncytial virus particles during virus assembly on the surface of virus-infected cells. J. Gen. Virol. 83: 611-621 [Abstract] [Full Text]  
  • Kozak, S. L., Heard, J. M., Kabat, D. (2002). Segregation of CD4 and CXCR4 into Distinct Lipid Microdomains in T Lymphocytes Suggests a Mechanism for Membrane Destabilization by Human Immunodeficiency Virus. J. Virol. 76: 1802-1815 [Abstract] [Full Text]  
  • Cantin, R., Martin, G., Tremblay, M. J. (2001). A novel virus capture assay reveals a differential acquisition of host HLA-DR by clinical isolates of human immunodeficiency virus type 1 expanded in primary human cells depending on the nature of producing cells and the donor source. J. Gen. Virol. 82: 2979-2987 [Abstract] [Full Text]  
  • Lindwasser, O. W., Resh, M. D. (2001). Multimerization of Human Immunodeficiency Virus Type 1 Gag Promotes Its Localization to Barges, Raft-Like Membrane Microdomains. J. Virol. 75: 7913-7924 [Abstract] [Full Text]  
  • Niyogi, K., Hildreth, J. E. K. (2001). Characterization of New Syncytium-Inhibiting Monoclonal Antibodies Implicates Lipid Rafts in Human T-Cell Leukemia Virus Type 1 Syncytium Formation. J. Virol. 75: 7351-7361 [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]  
  • Esser, M. T., Graham, D. R., Coren, L. V., Trubey, C. M., Bess, J. W. Jr., Arthur, L. O., Ott, D. E., Lifson, J. D. (2001). Differential Incorporation of CD45, CD80 (B7-1), CD86 (B7-2), and Major Histocompatibility Complex Class I and II Molecules into Human Immunodeficiency Virus Type 1 Virions and Microvesicles: Implications for Viral Pathogenesis and Immune Regulation. J. Virol. 75: 6173-6182 [Abstract] [Full Text]  
  • Vincent, S., Gerlier, D., Manié, S. N. (2000). Measles Virus Assembly within Membrane Rafts. J. Virol. 74: 9911-9915 [Abstract] [Full Text]