The Role of Lipid Microdomains in Virus Biology

  • Debi P. Nayak
  • Eric K.-W. Hui
Part of the Subcellular Biochemistry book series (SCBI, volume 37)


Many of the highly pathogenic viruses including influenza virus, HIV and others of world wide epidemiological importance are enveloped and possess a membrane around the nucleocapsid containing the viral genome. Viral membrane is required to protect the viral genome and provide important functions for attachment, morphogenesis and transmission. Viral membrane is essentially composed of lipids and proteins. While the proteins on the viral envelope are almost exclusively virally encoded, lipids, on the other hand, are all of host origin and recruited from host membrane. However, lipids on the viral membrane are not incorporated randomly and do not represent average lipid composition of the host membrane. Recent studies support that specific lipid microdomains such as lipid rafts play critical roles in many aspects of the virus infectious cycle including attachment, entry, uncoating, protein transport and sorting as well as viral morphogenesis and budding. Lipid microdomains aid in bringing and concentrating viral components to the budding site. Similarly, specific viral protein plays an important role in organizing lipid microdomains in and around the assembly and budding site of the virus. This review deals with the specific role of lipid microdomains in different aspects of the virus life cycle and the role of specific viral proteins in organizing the lipid microdomains.


Human Immunodeficiency Virus Type Influenza Virus Lipid Raft Measle Virus Semliki Forest Virus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



atomic force microscopy


acquired immune deficiency syndrome


nontransforming avian leukosis virus


avian sarcoma virus


B cell antigen receptor


cell, baby hamster kidney cell




chick embryo cells


Chilo Iridescent virus


confocal laser scanning microscopy






cytoplasmic tail


detergent insoluble GSL-enriched domain


detergent resistant membranes


equine arteritis virus


Ebola virus


Epstein-Barr virus


endoplasmic reticulum


Fisher rat thyroid cells


fowl plague virus


fluorescence energy transfer

Gal Cer

galactosyl ceramide


GSL-enriched membrane








hamster kidney cells


cytoplasmic tail minus HA


hepatitis B virus


hepatitis C virus


human immunodeficiency virus


herpes simplex virus


intermediate pre-Golgi compartment

I domain

interacting domain


liquid crystalline phase


liquid disordered phase


liquid ordered phase


lysobisphosphatidic acid

L domain

late domain


matrix protein of influenza virus


membrane attachment domain


Marburg virus

MDCK cell

MadinDarby canine kidney cell


major histocompatibility complex


mouse hepatitis virus


Mason-Pfizer monkey virus


Measles virus




Newcastle disease virus






phospholipase D2


respiratory syncytial virus


Semliki Forest virus


Sindbis virus


scanning near field optical microscopy


Sendai virus


Sendai virus


Simian virus 40


T cell antigen receptor


trans Golgi network


Triton-insoluble membrane




transmembrane domain


transfection receptor


Triton X-100


Venezuelan equine encephalitis virus


virus like particle


vesicular stomatitis virus


wild type.


  1. Alt Slimane, T. and Hoekstra, D. (2002) Sphingolipid trafficking and protein sorting in epithelial cells. FEBS Lett. 529: 54–59.CrossRefGoogle Scholar
  2. Alfsen, A., Iniguez, P., Bouguyon, E. and Bomsel, M. (2001) Secretory IgA specific for a conserved epitope on gp41 envelope glycoprotein inhibits epithelial transcytosis of HIV-1. J. Immunol. 166: 6257–6265.PubMedGoogle Scholar
  3. Ali, A., Avalos, R.T., Ponimaskin, E. and Nayak, D.P. (2000) Influenza virus assembly: effect of influenza virus glycoproteins on the membrane association of M1 protein. J. Virol. 74: 8709–8719.PubMedCrossRefGoogle Scholar
  4. Ali, A. and Nayak, D.P. (2000) Assembly of Sendai virus: M protein interacts with F and HN proteins and with the cytoplasmic tail and transmembrane domain of F protein. Virology 276: 289–303.Google Scholar
  5. Aloia, R.C., Tian, H. and Jensen, F.C. (1993) Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes. Proc. Natl. Acad. Sci. USA 90: 5181–5185.Google Scholar
  6. Alonso, M.A. and Milian, J. (2001) The role of lipid rafts in signalling and membrane trafficking in T lymphocytes. J. Cell Sci. 114: 3957–3965.PubMedGoogle Scholar
  7. Aman, M.J., Tosello-Trampont, A.-C. and Ravichandran, K. (2001) FcyRIIB1/SHIP-mediated inhibitory signaling in B cells involves lipid rafts. J. Biol. Chem. 276: 46371–46378.Google Scholar
  8. Balange-Orange, N. and Devauchelle, G. (1982) Lipid composition of an Iridescent virus type 6 (CIV). Arch. Virol. 73: 363–367.Google Scholar
  9. Barman, S. and Nayak, D.P. (2000) Analysis of the transmembrane domain of influenza virus neuraminidase, a type II transmembrane glycoprotein, for apical sorting and raft association. J. Virol. 74: 6538–6545.PubMedCrossRefGoogle Scholar
  10. Barman, S., Ali, A., Hui, E.K.-W, Adhikary, L. and Nayak, D.P. (2001) Transport of viral proteins to the apical membranes and interaction of matrix protein with glycoproteins in the assembly of influenza viruses. Virus. Res. 77: 61–69.Google Scholar
  11. Barman, S., Adhikary, L., Kawaoka, Y. and Nayak, D.P. (2003) Influenza A virus hemagglutinin containing basolateral localization signal does not alter the apical budding of a recombinant influenza A virus in polarized MDCK cells. Virology 305: 138–152.PubMedCrossRefGoogle Scholar
  12. Bastiani, L., Laal, S., Kim, M. and Zolla-Pazner, S. (1997) Host cell-dependent alterations in envelope components of human immunodeficiency virus type 1 virions. J. Virol. 71: 3444–3450.PubMedGoogle Scholar
  13. Bavari, S., Bosio, C.M., Wiegand, E., Ruthel, G., Will, A.B., Geisbert, T.W., Hevey, M., Schmaljohn, C., Schmaljohn, A. and Aman, M.J. (2002) Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses. J. Exp. Med. 195: 593–602.Google Scholar
  14. Blau, D.M. and Compans, R.W. (1995) Entry and release of measles virus are polarized in epithelial cells. Virology 210: 91–99.PubMedCrossRefGoogle Scholar
  15. Bourmakina, S.V. and Garcia-Sastre, A. (2003) Reverse genetics studies on the filamentous morphology of influenza A virus. J. Gen. Virol. 84: 517–527.Google Scholar
  16. Brewer, G.J. (1979) In vivo assembly of a biological membrane of defined size, shape, and lipid composition. J. Virol. 30: 875–882.PubMedGoogle Scholar
  17. Brewer, C.B. and Roth, M.G. (1991) A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J. Cell Biol. 114: 413–421.PubMedCrossRefGoogle Scholar
  18. Briggs, J.A.G., Wilk, T. and Fuller, S.D. (2003) Do lipid rafts mediate virus assembly and pseudotyping? J. Gen. Virol. 84: 757–768.Google Scholar
  19. Brown, D.A. and London, E. (1998a) Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14, 111–136.Google Scholar
  20. Brown, D.A. and London, E. (1998b) Structure and origin of ordered lipid domains in biological membranes. J. Membr. Biol. 164, 103–114.Google Scholar
  21. Brown, D.A., Crise, B. and Rose, J.K. (1989) Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science 245: 1499–1501.PubMedCrossRefGoogle Scholar
  22. Brown, G., Aitken, J., Rixon, H.W. and Sugrue, R.J. (2000a) 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.Google Scholar
  23. Brown, G., Rixon, H.W. and Sugrue, R.J. (2002b) Respiratory syncytial virus assembly occurs in GM 1-rich regions of the host-cell membrane and alters the cellular distribution of tyrosine phosphorylated caveolin-1. J. Gen. Virol. 83: 1841–1850.Google Scholar
  24. Cadd, T.L., Skoging, U., and Liljestrom, P. (1997) Budding of enveloped viruses from the plasma membrane. Bioessays 19: 993–1000.PubMedCrossRefGoogle Scholar
  25. Campbell, S.M., Crowe, S.M. and Mak, J. (2001) Lipid rafts and HIV-1: from viral entry to assembly of progeny virions. J. Clin. Virol. 22: 217–227.Google Scholar
  26. Chatterjee, P.K., Eng, C.H. and Kielian, M. (2002) Novel mutations that control the sphingolipid and cholesterol dependence of the Semliki Forest virus fusion protein. J. Virol. 76: 12712–12722.PubMedCrossRefGoogle Scholar
  27. Chazal, N. and Gerlier, D. (2003) Virus entry, assembly, budding, and membrane rafts. Microbiol. Mol. Biol. Rev. 67: 226–237.Google Scholar
  28. Cheng, H., Hoxie, J. and Parks, W.P. (1999) The conserved core of human immunodeficiency virus type 1 Nef is essential for association with Lck and for enhanced viral replication in T-lymphocytes. Virology 264: 5–15.PubMedCrossRefGoogle Scholar
  29. Cherukuri, A., Dykstra, M. and Pierce, S.K. (2001) Floating the raft hypothesis: lipid rafts play a role in immune cell activation. Immunity 14: 657–660.PubMedCrossRefGoogle Scholar
  30. Cimarelli, A. and Darlix, J.-L. (2002) Assembling the human immunodeficiency virus type 1. Cell. Mol. Life Sci. 59: 1166–1184.Google Scholar
  31. Collette, Y., Arold, S., Picard, C., Janvier, K., Benichou, S., Benarous, R., Olive, D. and Dumas, C. (2000) 11IV-2 and SW Nef proteins target different Src family SH3 domains than does HIV-1 Nef because of a triple amino acid substitution. J. Biol. Chem. 275: 4171–4176.Google Scholar
  32. Compans, R.W. (1995) Virus entry and release in polarized epithelial cells. Curr. Top. Microbio. Immunol. 202: 209–219.Google Scholar
  33. Czarny, M., Lavie, Y., Fiucci, G. and Liscovitch, M. (1999) Localization of phospholipase D in detergent-insoluble, caveolin-rich membrane domains: modulation by caveolin-1 expression and caveolin-182–101. J. Biol. Chem. 274: 2717–2724.Google Scholar
  34. Damjanovich, S., Matyus, L., Damjanovich, L., Bene, L., Jenei, A., Matkó, J., Gaspar, Jr., R. and Szöllösi, J. (2002) Does mosaicism of the plasma membrane at molecular and high hierarchical levels in human lymphocytes carry information on the immediate history of cells? Immunol. Lett. 82: 93–99.Google Scholar
  35. Danielsen, E.M. (1995) Involvement of detergent-insoluble complexes in the intracellular transport of intestinal brush border enzymes. Biochemistry 34: 1596–1605.PubMedCrossRefGoogle Scholar
  36. Danielsen, E.M. and van Deurs, B. (1995) A transferrin-like GPI-linked iron-binding protein in detergent-insoluble noncaveolar microdomains at the apical surface of fetal intestinal epithelial cells. J. Cell Biol. 131: 939–950.PubMedCrossRefGoogle Scholar
  37. David A.E. (1971) Lipid composition of Sindbis virus. Virology 46: 711–720.PubMedCrossRefGoogle Scholar
  38. Demirov, D.G., Ono, A., Orenstein, J.M. and Freed, E.O. (2002) Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc. Natl. Acad. Sci. USA 99: 955–960.Google Scholar
  39. Deschambeault, J., Lalonde, J.P., Cervantes-Acosta, G., Lodge, R., Cohen, E.A. and Lemay, G. (1999) Polarized human immunodeficiency virus budding in lymphocytes involves a tyrosine-based signal and favors cell-to-cell viral transmission. J. Virol. 73, 5010–5017.PubMedGoogle Scholar
  40. Dimitrov, D.S. (2000) Cell biology of virus entry. Cell 101: 697–702.PubMedCrossRefGoogle Scholar
  41. Drevot, P., Langlet, C., Guo, X.J., Bernard, A.M., Colard, O., Chauvin, J.P., Lasserre, R. and He, H.T. (2002) TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J. 21: 1899–1908.PubMedCrossRefGoogle Scholar
  42. Farsad, K. and De Camilli, P. (2003) Lipids in endocytic membrane transport and sorting. Curr. Opin. Cell Biol. 15: 372-Freed, E.O. (2002) Viral late domain. J. Virol. 76: 4679–4687.Google Scholar
  43. Galbiati, E, Razani, B. and Lisanti, M.P. (2001) Emerging themes in lipid rafts and caveolae. Cell 106: 403–411.PubMedCrossRefGoogle Scholar
  44. Garbutt, M., Chan, H. and Hobman, T.C. (1999) Secretion of rubella virions and virus-like particles in cultured epithelial cells. Virology 261: 340–346.PubMedCrossRefGoogle Scholar
  45. Garoff, H., Hewson, R. and Opstelten, D.-J.E. (1998) Virus maturation by budding. Microbiol. Mol. Biol. Rev. 62: 1171–1190.Google Scholar
  46. Gurus, J.E., von Schwedler, U.K., Pornillos, O.W., Morham, S.G., Zavitz, K.H., Wang, H.E., Wettstein, D.A., Stray, K.M., Côte, M., Rich, R.L., Mysxka, D.G. and Sundquist, W.I. (2001) Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107: 55–65.CrossRefGoogle Scholar
  47. Goila-Gaur, R., Demirov, D.G., Orenstein, J.M., Ono, A. and Freed, E.O. (2003) Defects in human immunodeficiency virus budding and endosomal sorting induced by TSG101 overexpression. J. Virol. 77: 6507–6519.PubMedCrossRefGoogle Scholar
  48. Graham, D.R.M., Chertova, E., Hilburn, J.M., Arthur, L.O. and Hildreth, J.E.K. (2003) Cholesterol depletion of human immunodeficiency virus type 1 and simian immunodeficiency virus with b-cyclodextrin inactivates and permeabilizes the virions: evidence for virion-associated lipid rafts. J. Virol. 77: 8237–8248.PubMedCrossRefGoogle Scholar
  49. Gujuluva, C.N., Kundu, A., Murti, K.G. and Nayak, D.P. (1994) Abortive replication of influenza virus A/WSN/33 in HeLa cells: defective viral entry and budding processes. Virology 204: 491–505.PubMedCrossRefGoogle Scholar
  50. Guo, B., Kato, R.M., Garcia-Lloret, M., Wahl, M.I. and Rawlings, D.J. (2000) Engagement of the human pre-B cell receptor generates a lipid raft-dependent calcium signaling cornplex. Immunity 13: 243–253.PubMedCrossRefGoogle Scholar
  51. Harder, T. (2003) Formation of functional cell membrane domains: the interplay of lipid-and protein-mediated interactions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358: 863–868.Google Scholar
  52. Harder, T. and Simons, K. (1999) Clusters of glycolipid and glycosylphosphatidylinositolanchored proteins in lymphoid cells: accumulation of actin regulated by local tyrosine phosphorylation. Eur. J. Immunol. 29: 556–562.Google Scholar
  53. Harder, T, Scheiffele, P., Verkade, P. and Simons, K. (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141: 929–942.PubMedCrossRefGoogle Scholar
  54. Hermida-Matsumoto, L. and Resh, M.D. (2000) Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging. J. Viral. 74, 8670–8679.CrossRefGoogle Scholar
  55. Heydrick, F.P., Corner, J.F. and Wachter, R.F. (1971) Phospholipid composition of Venezuelan equine encephalitis virus. J. Virol. 7: 642–645.PubMedGoogle Scholar
  56. Hiipakka, M. and Saksela, K. (2002) Capacity of simian immunodeficiency virus strain mac Nef for high-affinity Src homology 3 (SH3) binding revealed by ligand-tailored SH3 domains. J. Gen. Virol. 83: 3147–3152.Google Scholar
  57. Hobman, T.C. (1993) Targeting of viral glycoproteins to the Golgi complex. Trends Microbiol. 1: 124–130.PubMedCrossRefGoogle Scholar
  58. Hoessli, D.C., Ilangumaran, S, Soltermann, A., Robinson, P.J., Borisch, B. and Nasir-UdDin. (2001) Signaling through sphingolipid microdomains of the plasma membrane: the concept of signaling platform. Glycoconjugate J. 17: 191–197.CrossRefGoogle Scholar
  59. Holm, K., Weclewicz, K., Hewson, R. and Suomalainen, M. (2003) Human immunodeficiency virus type 1 assembly and lipid rafts: Pr55 associates with membrane domains that are largely resistant to Brij98 but sensitive to Triton X-100. J. Virol. 77: 4805–4817.PubMedCrossRefGoogle Scholar
  60. Holopainen, J.M., Angelora, M.I. and Kinnunen, P.K. (2000) Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys. J. 78: 830–838.Google Scholar
  61. Holowka, D., Sheets, E.D. and Baird, B. (2000) Interactions between and lipid raft components are regulated by the actin cytoskeleton. J. Cell Sci. 113: 1009–1019.PubMedGoogle Scholar
  62. Hug, P., Lin, H.-M.J., Korte, T., Xiaodong, X., Dimitrov, D.S., Wang, J.M., Puri, A. and Blumenthal, R. (2000) Glycosphingolipids promote entry of a broad range of human immunodeficiency virus type 1 isolates into cell lines expressing CD4, CXCR4, and/or CCR5. J. Virol. 74: 6377–6385.PubMedCrossRefGoogle Scholar
  63. Hughey, P.G., Compans, R.W., Zebedee, S.L. and Lamb, R.A. (1992) Expression of the influenza A virus M2 protein is restricted to apical surfaces of polarized epithelial cells. J. Virol. 66: 5542–5552.PubMedGoogle Scholar
  64. Hui, E.K.-W. and Nayak, D.P. (2001) Role of ATP in influenza virus budding. Virology 290: 329–341.PubMedCrossRefGoogle Scholar
  65. Hui, E.K.-W and Nayak, D.P. (2002) Role of G protein and protein kinase signalling in influenza virus budding in MDCK cells. J. Gen. Virol. 83: 3055–3066.Google Scholar
  66. Hui, E.K.-W., Barman, S., Yang, T.Y. and Nayak, D.P. (2003) Basic residues of the helix six domain of influenza virus M1 involved in nuclear translocation of Ml can be replaced by PTAP and YPDL late assembly domain motifs. J. Virol. 77: 7078–7092.PubMedCrossRefGoogle Scholar
  67. Ikonen, E. (2001) Roles of lipid rafts in membrane transport. Curr. Opin. Cell Biol. 13: 470–477.Google Scholar
  68. Janes, P.W., Ley, S.C. and Magee, A.I. (1999) Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147: 447–461.PubMedCrossRefGoogle Scholar
  69. Katagiri, Y.U., Liyokawa, N. and Fujimoto, J. (2001) A role for lipid rafts in immune cell signaling. Microbiol. Immunol. 45: 1–8.Google Scholar
  70. Kate, M., Allison, A.C., Tyrrell, D.A.J. and James, A.T. (1961) Lipids of influenza virus and their relation to those of the host cell. Biochim. Biophys. Acta 52: 455–466.Google Scholar
  71. Keller, P. and Simons, K. (1998) Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 140: 1357–1367.PubMedCrossRefGoogle Scholar
  72. Khanna, K.V., Whaley, K.J., Zeitlin, L., Moench, T.R., Mehrazar, K., Cone, R.A., Liao, Z., Hildreth, J.E.K., Hoen, T.E., Shultz, L. and Markham, R.B. (2002) Vaginal transmission of cell-associated HIV-1 in the mouse is blocked by a topical, membrane-modifying agent. J. Clin. Invest. 109: 205–211.Google Scholar
  73. Kielian, M.C. and Helenius, A. (1984) Role of cholesterol in fusion of Semliki Forest virus with membranes. J. Virol. 52: 281–283.PubMedGoogle Scholar
  74. Klenk, H.-D. and Choppin, P.W. (1970) Plasma membrane lipids and parainfluenza virus assembly. Virology 40: 939–947.PubMedCrossRefGoogle Scholar
  75. Kobayashi, T. and Hirabayashi, Y. (2001) Lipid membrane domains in cell surface and vacuolar systems. Glycoconjugate J. 17: 163–171.CrossRefGoogle Scholar
  76. Kundu, A., Avalos, R.T., Sanderson, C.M. and Nayak, D.P. (1996) Transmembrane domain of influenza virus neuraminidase, a type II protein, possesses an apical sorting signal in polarized MDCK cells. J. Virol. 70, 6508–6515.PubMedGoogle Scholar
  77. Kusumi, A. and Sako, Y. (1996) Cell surface organization by the membrane skeleton. Curr. Opin. Cell Biol. 8: 566–574.Google Scholar
  78. Lafont, E, Lecat, S., Verkade, P. and Simons, K. (1998) Annexin XIIb associates with lipid microdomains to function in apical delivery. J. Cell Biol. 142: 1413–1427.PubMedCrossRefGoogle Scholar
  79. Langlet, C., Bernard, A.M., Drevot, P. and He, H.T. (2000) Membrane rafts and signaling by the multichain immune recognition receptors. Curr. Opin. Immunol. 12: 250–255.Google Scholar
  80. Li, M., Yang, C., Tong, S., Weidmann, A. and 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.PubMedCrossRefGoogle Scholar
  81. Li, S., Okamoto, T., Chun, M., Sargiacomo, M., Casanova, J.E., Hansen, S.H., Nishimoto, I. And Lisanti, M.P. (1995) Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J. Biol. Chem. 270: 15693–15701.Google Scholar
  82. Lin, S., Naim, H.Y., Rodriguez, A.C. and Roth, M. G. (1998) Mutations in the middle of the transmembrane domain reverse the polarity of transport of the influenza virus hemagglutinin in MDCK epithelial cells. J. Cell Biol. 142: 51–57.PubMedCrossRefGoogle Scholar
  83. Lindwasser, O.W. and 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.PubMedCrossRefGoogle Scholar
  84. Lodge, R., Gottlinger, H., Gabuzda, D., Cohen, E.A. and Lemay, G. (1994). The intracytoplasmic domain of gp41 mediates polarized budding of human immunodeficiency virus type 1 in MDCK cells. J. Virol. 68: 4857–4861.PubMedGoogle Scholar
  85. Lodge, R., Lalonde, J.P., Lemay, G. and Cohen, E. A. (1997) The membrane-proximal intra-cytoplasmic tyrosine residue of HIV-1 envelope glycoprotein is critical for basolateral targeting of viral budding in MDCK cells. EMBO J. 16, 695–705.PubMedCrossRefGoogle Scholar
  86. Lu, Y.E., Cassese, T. and Kielian, M. (1999) The cholesterol requirement for Sindbis virus entry and exit and characterization of a spike protein region involved in cholesterol dependence. J. Virol. 73: 4272–4278.PubMedGoogle Scholar
  87. Luan, P., Yang, L. and Glaser, M. (1995) Formation of membrane domains created during the budding of vesicular stomatitis virus: a model for selective lipid and protein sorting in biological membranes. Biochemistry 34: 9874–9883.PubMedCrossRefGoogle Scholar
  88. Luban, J. (2001) HIV-1 and Ebola virus: the getaway driver nabbed. Nat. Med. 7: 1278–1280. Maisner, A., Klenk, H., and Herrler, G. (1998) Polarized budding of measles virus is not determined by viral surface glycoproteins. J. Virol. 72: 5276–5278.Google Scholar
  89. Malvoisin, E. and Wild, E (1990) Effect of drugs which inhibit cholesterol synthesis on syncytia formation in vero cells infected with measles virus. Biochim. Biophys. Acta 1042: 359–364.Google Scholar
  90. Manié, S.N., Debreyne, S., Vincent, S. and Gerlier, D. (2000) Measles virus structural components are enriched into lipid raft microdomains: a potential cellular location for virus assembly. J. Virol. 74: 305–311.PubMedCrossRefGoogle Scholar
  91. Martin-Belmonte, E, Puertollano, R., Milian, J. and Alonso, M.A. (2000) The MAL proteolipid is necessary for the overall apical delivery of membrane proteins in the polarized epithelial Madin-Darby canine kidney and fischer rat thyroid cell lines. Mol. Biol. Cell 11: 2033–2045.Google Scholar
  92. Miceli, M.C., Moran, M., Chung, C.D., Patel, VP., Low, T. and Zinnznti, W. (2001) Co-stimulation and counter-stimulation: lipid raft clustering controls TCR signaling and functional outcomes. Semin. Immunol. 13: 115–128.Google Scholar
  93. Mora, R., Rodriguez-Boulan, E., Palese, P. and 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.PubMedCrossRefGoogle Scholar
  94. Müller, G. (2002) Dynamics of plasma membrane microdomains and cross-talk to the insulin signalling cascade. FEBS Lett. 531: 81–87.PubMedCrossRefGoogle Scholar
  95. Nabi, I.R. and Le, P.U. (2003) Caveolae/raft-dependent endocytosis. J. Cell Biol. 161: 673–677.PubMedCrossRefGoogle Scholar
  96. Naim, H. Y, Ehler, E., and Billeter, M.A. (2000) Measles virus matrix protein specifies api- cal virus release and glycoprotein sorting in epithelial cells. EMBO J. 19, 3576–3585.PubMedCrossRefGoogle Scholar
  97. Narayan, S., Barnard, R.J.O. and Young, J.A.T. (2003) Two retroviral entry pathways distinguished by lipid raft association of the viral receptor and differences in viral infectivity. J. Virol. 77: 1977–1983.PubMedCrossRefGoogle Scholar
  98. Nayak, D.P. and Barman, S. (2002) Role of lipid rafts in virus assembly and budding. Adv. Virus Res. 58: 1–28.Google Scholar
  99. Nayak, D.P. and Hui, E.K.-W (2002) Assembly and morphogenesis of influenza virus. Recent Res. Dev. Virol. 4: 35–54.Google Scholar
  100. Nguyen, D.H. and Hildreth, J.E.K. (2000) Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J. Virol. 74: 3264–3272.PubMedCrossRefGoogle Scholar
  101. Nieva, J.L., Bron, R., Corver, J. and Wilschut, J. (1994) Membrane fusion of Semliki Forest virus requires sphingolipids in the target membrane. EMBO J. 13: 2797–2804.PubMedGoogle Scholar
  102. Ono, A. and Freed, E.O. (2001) Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. USA 98: 13925–13990.Google Scholar
  103. Owens, R.J., Dubay, J.W., Hunter, E. and Compans, R.W. (1991) Human immunodeficiency virus envelope protein determines the site of virus release in polarized epithelial cells. Proc. Natl. Acad. Sci. USA 88: 3987–3991.Google Scholar
  104. Pelkmans, L. and Helenius, A. (2003) Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15: 414–422.Google Scholar
  105. Perez, O.D. and Nolan, G.P. (2001) Resistance is futile: assimilation of cellular machinery by HIV-1. Immunity 15: 687–690.PubMedCrossRefGoogle Scholar
  106. Phalen, T. and Kielian, M. (1991) Cholesterol is required for infection by Semliki Forest virus. J. Cell Biol. 112: 615–623.PubMedCrossRefGoogle Scholar
  107. Pickl, W.F., Pimentel-Muiíïos, F.X. and Seed, B. (2001) Lipid rafts and pseudotyping. J. Virol. 75: 7175–7183.PubMedCrossRefGoogle Scholar
  108. Pralle, A., Keller, P., Florin, E.-L., Simons, K. and Hörber, J.K.H. (2000) Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148: 997–1008.PubMedCrossRefGoogle Scholar
  109. Puertollano, R., Martin-Belmonte, E, Milian, J., de Marco, M.C., Albar, J.P., Kremer, L. and Alonso, M.A. (1999) The MAL proteolipid is necessary for normal apical transport and accurate sorting of the influenza virus hemagglutinin in Madin-Darby canine kidney cells. J. Cell Biol. 145: 141–151.PubMedCrossRefGoogle Scholar
  110. Quigley, J.P., Rifkin, D.B. and Reich, E. (1971) Phospholipid composition of Rous sarcoma virus, host cell membranes and other enveloped RNA viruses. Virology 46: 106–116.PubMedCrossRefGoogle Scholar
  111. Renkonen, O., Kääräinen, L., Simons, K. and Gahmberg, C.G. (1971) The lipid class composition of Semliki Forest virus and of plasma membranes of the host cells. Virology 46: 318–326.PubMedCrossRefGoogle Scholar
  112. Roberts, P.C. and Compans, R.W. (1998) Host cell dependence of viral morphology. Proc. Natl. Acad. Sci. USA 95: 5746–5751.Google Scholar
  113. Roberts, P.C., Lamb, R.A. and Compans, R.W. (1998) The Ml and M2 proteins of influenza A virus are important determinants in filamentous particle formation. Virology 240: 127–137.PubMedCrossRefGoogle Scholar
  114. Roper, K., Corbeil, D. and Huttner, W.B. (2000) Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat. Cell Biol. 2: 582–592.Google Scholar
  115. Rousso, I., Mixon, M.B., Chen, B.K. and Kim, P.S. (2000) Palmitoylation of the HIV-1 envelope glycoprotein is critical for viral infectivity. Proc. Natl. Acad. Sci. USA 97: 13523–13525.Google Scholar
  116. Salzwedel, K., West Jr., J.T., Mulligan, M.J. and Hunter, E. (1998) Retention of the human immunodeficiency virus type 1 envelope glycoprotein in the endoplasmic reticulum does not redirect virus assembly from the plasma membrane. J. Virol. 72: 7523–7531.PubMedGoogle Scholar
  117. Samsonov, A.V., Chatterjee, P.K., Razinkov, V.I., Eng, C.H., Kielian, M. and Cohen, F.S. (2002) Effects of membrane potential and sphingolipid structures on fusion of Semliki Forest virus. J. Virol. 76: 12691–12702.PubMedCrossRefGoogle Scholar
  118. Sanchez, V, Greis, K.D., Sztul, E. and Britt, W.J. (2000) Accumulation of virion tegument and envelope proteins in a stable cytoplasmic compartment during human cytomegalovirus replication: characterization of a potential site of virus assembly. J. Virol. 74, 975–986.PubMedCrossRefGoogle Scholar
  119. Sandefur, S., Smith, R.M., Varthakavi, V. and Spearman, P. (2000) Mapping and characterization of the N-terminal I domain of human immunodeficiency virus type 1 Pr55Gag J. Virol. 74: 7238–7249.PubMedCrossRefGoogle Scholar
  120. Sanger, C., Muhlberger, E., Ryabchikova, E., Kolesnikova, L., Klenk, H.D. and Becker, S. (2001) Sorting of marburg virus surface protein and virus release take place at opposite surfaces of infected polarized epithelial cells. J. Virol. 75: 1274–1283.PubMedCrossRefGoogle Scholar
  121. Scheiffele, P., Roth, M.G. and Simon, K. (1997) Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 16: 5501–5508.PubMedCrossRefGoogle Scholar
  122. Scheiffele, P., Verkade, P., Fra, A.M., Virta, H., Simons, K. and Ikonen, E. (1998) Caveolin-1 and -2 in the exocytic pathway of MDCK cells. J. Cell Biol. 140: 795–806.PubMedCrossRefGoogle Scholar
  123. Scheiffele, P., Rietveld, A., Wilk, T. and Simons, K. (1999) Influenza viruses select ordered lipid domains during budding from the plasma membrane. J. Biol. Chem. 274: 2038–2044.Google Scholar
  124. Schnitzer, J.E., Oh, P., Pinney, E. and Allard, J. (1994) Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J. Cell Biol. 127: 1217–1232.PubMedCrossRefGoogle Scholar
  125. Schütz, G.J., Kada, G., Pastushenko, V.P. and Schindler, H. (2000) Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy. EMBO J. 19: 892–901.PubMedCrossRefGoogle Scholar
  126. Sharma, P., Sabharanjak, S. and Mayor, S. (2002) Endocytosis of lipid rafts: an identity crisis. Semin. Cell Dev. Biol. 13: 205–214.Google Scholar
  127. Sheets, E.D., Lee, G.M., Simson, R. and Jacobson, K. (1997) Transient confinement of a glycosylphosphatidylinositol-anchored protein in the plasma membrane. Biochemistry 36: 12449–12458.PubMedCrossRefGoogle Scholar
  128. Shi, S.T., Lee, K.J., Aizaki, H., Hwang, S.B. and Lai, M.M. (2003) Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionate with caveolin-2. J. Virol. 77: 4160–4168.PubMedCrossRefGoogle Scholar
  129. Simons, K. and Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387: 569–572.PubMedCrossRefGoogle Scholar
  130. Simons, K. and Toomre, D. (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1: 31–39Google Scholar
  131. Simpson-Holley, M., Ellis, D., Fisher, D., Elton, D., McCauley, J. and Digard, P. (2002) A functional link between the actin cytoskeleton and lipid rafts during budding of filamentous influenza virions. Virology 301: 212–225.PubMedCrossRefGoogle Scholar
  132. Skibbens, J.E., Roth, M.G. and Matlin, K.S. (1989) Differential extractability of influenza virus hemagglutinin during intracellular transport in polarized epithelial cells and non-polar fibroblasts. J. Cell Biol. 108: 821–832.PubMedCrossRefGoogle Scholar
  133. Slimane, T.A. and Hoekstra, D. (2002) Sphingolipid trafficking and protein sorting in epithelial cells. FEBS Lett. 529: 54–59.CrossRefGoogle Scholar
  134. Song, K.S., Shengwen, L., Okamoto, T., Quilliam, L.A., Sargiacomo, M. and Lisanti, M.P. (1996) Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains: detergent-free purification of caveolae microdomains. J. Biol. Chem. 271: 9690–9697.Google Scholar
  135. Stang, E., Kartenbeck, J. and Parton, R.G. (1997) Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol. Biol. Cell 8: 47–57.Google Scholar
  136. Suomalainen, M. (2002) Lipid rafts and assembly of enveloped viruses. Traffic 3: 705–709.PubMedCrossRefGoogle Scholar
  137. Tatulian, S.A. and Tamm, L.K. (2000) Secondary structure, orientation, o1igomerization, and lipid interactions of the transmembrane domain of influenza hemagglutinin. Biochemistry 39: 496–507.PubMedCrossRefGoogle Scholar
  138. van der Goot, F.G. and Harder, T. (2001) Raft membrane domains: from a liquid-ordered membrane phase to a site of pathogen attack. Seminars Immun1. 13: 89–97.CrossRefGoogle Scholar
  139. van Genderen, I.L., Godeke, G.-J., Rottier, P.J.M. and van Meer, G. (1995) The phospholipid composition of enveloped viruses depends on the intracellular membrane through which they bud. Biochem. Soc. Trans. 23: 523–526.Google Scholar
  140. van Meer, G. and Simons, K. (1986) The function of tight junctions in maintaining differences in lipid composition between the apical and the basolateral cell surface domains of MDCK cells. EMBO J. 5: 1455–1464.PubMedGoogle Scholar
  141. Veit, M., Herder, G., Schmidt, M.F., Rott, R. and Klenk, H.D. (1990) The hemagglutinating glycoproteins of influenza B and C viruses are acylated with different fatty acids. Virology 177: 807–811.PubMedCrossRefGoogle Scholar
  142. Veit, M., Klenk, H.D., Kendal, A. and Rott, R. (1991) The M2 protein of influenza A virus is acylated. J. Gen. Virol. 72: 1461–1465.Google Scholar
  143. Vincent, S., Gerlier, D. and Manié, S.N. (2000) Measles virus assembly within membrane rafts. J. Virol. 74: 9911–9915.PubMedCrossRefGoogle Scholar
  144. Vogt, A.B., Spindeldreher, S. and Kropshofer, H. (2002) Clustering of MHC-peptide complexes prior to their engagement in the immunological synapse: lipid raft and tetraspan microdomains. Immunol. Rev. 189: 136–151.Google Scholar
  145. Waarts, B.-L., Bittman, R. and Wilschut, J. (2002) Sphingolipid and cholesterol dependence of alphavirus membrane fusion. J. Biol. Chem. 277: 38141–38147.Google Scholar
  146. Wang, J.K., Kiyokawa, E., Verdin, E. and Trono, D. (2000) The Nef protein of HIV-1 associates with rafts and primes T cells for activation. Proc. Natl. Acad. Sci. USA 97: 394–399.Google Scholar
  147. Zhang, J., Pekosz, A. and 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.PubMedCrossRefGoogle Scholar
  148. Zheng, X., Lu, D. and Sadler, J.E. (1999) Apical sorting of bovine enteropeptidase does not involve detergent-resistant association with sphingolipid-cholesterol rafts. J. Biol. Chem. 274: 1596–1605.Google Scholar
  149. Zheng, Y.-H., Plemenitas, A., Linnemann, T., Fackler, O.T. and Peterlin, B.M. (2001) Nef increases infectivity of HIV via lipid rafts. Curr. Biol. 11: 875–879.Google Scholar
  150. Zimmer, G., Zimmer K.-P, Trotz, I. and Herrler, G. (2002) Vesicular somatitis virus glycoprotein does not determine the site of virus release in polarized epithelial cells. J. Virol. 76: 4103–4107.PubMedCrossRefGoogle Scholar
  151. Zurzolo, C., Polistina, C., Saini, M., Gentile, R., Aloj, L., Migliaccio, G., Bonatti, S. and Nitsch, L. (1992) Opposite polarity of virus budding and of viral envelope glycoprotein distribution in epithelial cells derived from different tissues. J. Cell Biol. 117: 551–564.PubMedCrossRefGoogle Scholar
  152. Zurzolo, C., van’t Hof, W, van Meer, G. and Rodriguez-Boulan, E. (1994) VIP21/caveolin, glycosphingolipid clusters and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells. EMBO J. 13: 42–53.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2004

Authors and Affiliations

  • Debi P. Nayak
    • 1
  • Eric K.-W. Hui
    • 1
  1. 1.Department of Microbiology, Immunology and Molecular GeneticsUCLA School of MedicineLos AngelesUSA

Personalised recommendations