Virus Entry, Assembly, Budding, and Membrane Rafts Nathalie Chazal, Denis Gerlier
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Virus Entry, Assembly, Budding, and Membrane Rafts Nathalie Chazal, Denis Gerlier To cite this version: Nathalie Chazal, Denis Gerlier. Virus Entry, Assembly, Budding, and Membrane Rafts. Microbi- ology and Molecular Biology Reviews, American Society for Microbiology, 2003, 67 (2), pp.226-237. 10.1128/MMBR.67.2.226-237.2003. hal-02147208 HAL Id: hal-02147208 https://hal.archives-ouvertes.fr/hal-02147208 Submitted on 7 Jun 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. MICROBIOLOGY AND MOLECULAR BIOLOGY REVIEWS, June 2003, p. 226–237 Vol. 67, No. 2 1092-2172/03/$08.00ϩ0 DOI: 10.1128/MMBR.67.2.226–237.2003 Copyright © 2003, American Society for Microbiology. All Rights Reserved. Virus Entry, Assembly, Budding, and Membrane Rafts Nathalie Chazal1* and Denis Gerlier2 Immunologie-Virologie, EA 3038, Universite´Paul Sabatier, 31062 Toulouse,1 and Immunite´& Infections Virales, CNRS-UCBL UMR 5537, IFR Laennec, 69372 Lyon Cedex 08,2 France INTRODUCTION .......................................................................................................................................................226 DEFINITION OF RAFTS..........................................................................................................................................226 Composition of Rafts..............................................................................................................................................226 Functions of Rafts...................................................................................................................................................227 RAFTS AS PLATFORMS FOR VIRUS ENTRY ....................................................................................................227 Nonenveloped Viruses ............................................................................................................................................227 Downloaded from Enveloped Viruses...................................................................................................................................................228 RAFTS AS PLATFORMS FOR VIRUS ASSEMBLY ............................................................................................229 Nonenveloped Viruses ............................................................................................................................................229 Enveloped Viruses...................................................................................................................................................229 RAFTS AS PLATFORMS FOR VIRUS BUDDING ..............................................................................................232 Gateway for Budding Viruses................................................................................................................................233 Recruitment of Cellular Machinery Needed for Virus Budding ......................................................................233 CONCLUDING REMARKS AND PROSPECTS ...................................................................................................233 ACKNOWLEDGMENTS ...........................................................................................................................................234 REFERENCES ............................................................................................................................................................234 http://mmbr.asm.org/ INTRODUCTION organized in microdomains or rafts in the ordered rigid liquid crystal state (L ), distinct from the disordered fluid liquid Specific microdomains of the plasma membrane called rafts o phase membranes (L ) of the surrounding phospholipids (16, appear to be involved in many biological events such as bio- c 62). The tight packing organization of lipid rafts confers their synthetic traffic, endocytic traffic, and the signal transduction resistance to some detergents, such as the nonionic detergent pathway. Among pathogens, viruses, which are obligate intra- Triton X-100 (TX-100) at low temperature, and allows their cellular parasites, are confronted with the plasma membrane purification from low-density fractions after flotation in a su- during their life cycle. They have to enter their host cells by crose gradient. In cell plasma membranes, a similar organiza- on June 4, 2019 by guest fusion, permeation, or endocytic vesicle discharge and to exit tion of lipids is likely to occur, and after solubilization in them by budding or membrane disruption. TX-100 at 4°C, membrane microdomains rich in cholesterol In this review, we focus on data supporting the involvement and sphingolipids can be similarly isolated by flotation. These of membrane rafts in the virus replication cycle, their role as a microdomains were given various names such as detergent- viral entry site, a platform for the assembly of viral compo- resistant membrane (17, 38), detergent insoluble glycolipid- nents, and a scaffold for the budding of virus from infected enriched complex (48), or Triton-insoluble floating fraction cells. The elucidation of these interactions requires a detailed (48) and are now called membrane rafts. The detergent resis- understanding of raft structures and dynamics. tance of rafts is critically dependent on the presence of cho- lesterol. DEFINITION OF RAFTS In addition to biochemical fractionation, several lines of Composition of Rafts evidence support the in vivo existence of rafts (30, 38, 55). Their in vivo size has been estimated to be between 25 and 700 Although their existence has been debated, the presence of nm by using fluorescence resonance energy transfer micros- specific microdomains into the biological membranes is now a copy and single-molecule-tracking microscopy (55, 94, 104, largely accepted concept (106). According to this concept, the 116). Many, but not all, proteins anchored to the membrane by microdomains have been named “rafts” because they can be a lipid moiety associate with membrane rafts. They include the seen as floating device within the “fluid mosaic” lipid sea of the glycosylphosphatidylinositol (GPI)-anchored proteins, which Singer and Nicholson model (108). In model membranes made are located on the extracellular leaflet, and palmitoylated or of a pure phospholipid-sphingolipid mixture, sphingolipids doubly acetylated proteins, which are enriched in the inner tend to pack together in microdomains separate from phos- cytoplasmic leaflet. However, geranylated proteins are ex- pholipids because the former have long, largely saturated acyl cluded from rafts (see references 48, 105, and 107 for reviews). chains. In the presence of cholesterol, the sphingolipids are Several data point to the existence of different subsets of rafts depending on the combinatorial association of different sphingolipid species with cholesterol and protein contents (72, * Corresponding author. Mailing address: Immuno-Virologie. EA 3038. Universite´Paul Sabatier, 118 Route de Narbonne, 31062 Tou- 104). One particular membrane raft subset is caveolae. Present louse, France. Phone: (33) 5 61 55 86 06. Fax: (33) 5 61 55 86 06. in many mammalian cells except lymphocytes and neurons, E-mail: [email protected]. caveolae are 50- to 70-nm plasma membrane invaginations 226 VOL. 67, 2003 VIRUS ENTRY, ASSEMBLY, BUDDING, AND RAFTS 227 which are surrounded by a striated coat made of the 22-kDa more than one way. Increasing evidence indicates that viruses, caveolins tightly bound to cholesterol (77). Likewise, some including nonenveloped viruses, can use specific membranes bona fide membrane rafts are soluble in 1% TX-100 yet insol- microdomains to penetrate the host cell. uble in a lower concentration of TX-100 or in other nonionic detergents, e.g., Brij or Lubrol (98). Several techniques to study and characterize membrane rafts Nonenveloped Viruses have been described in the literature. The simplest one is to collect the pellet from a cell extract solubilized with 1% TX- After attachment to cell surface receptors, the bound cap- 100 at 4°C and centrifuged at 10,000 ϫ g. This technique is not sids of nonenveloped viruses are internalized mostly if not reliable because only the “heaviest” raft structures, which are exclusively by invagination of the plasma membrane and intra- contaminated with unsoluble material such as protein aggre- cytoplasmic vesiculation. The involvement of membrane rafts gates, are collected. The classical biochemical experiment in- in mediating this process has been highlighted for several vi- volves flotation on a density (sucrose or iodixanol) gradient, ruses. The most convincing evidence has been provided for with the cell extract being loaded at the bottom of the gradient. simian virus 40 (SV40), a member of the Papovaviridae, and Downloaded from The quality of the separation should be checked using bona echovirus type 1 (EV1), a member of the Picornaviridae, which fide raft and nonraft markers. The alternative approach is to use caveolae for internalization and transport to the perinu- study the colocalization of