1,323
Views
43
CrossRef citations to date
0
Altmetric
Review Article

Viral entry, lipid rafts and caveosomes

, , &
Pages 394-403 | Published online: 08 Jul 2009

References

  • Hyypiä T. Viral host cell receptors. Nature Publishing Group, London 2003
  • Fingeroth J. D., Weis J. J., Tedder T. F., Strominger J. L., Biro P. A., Fearon D. T. Epstein‐Barr virus receptor of human B lymphocytes is the C3d receptor CR2. Proc Natl Acad Sci U S A 1984; 81: 4510–4
  • Lentz T. L., Burrage T. G., Smith A. L., Crick J., Tignor G. H. Is the acetylcholine receptor a rabies virus receptor?. Science 1982; 215: 182–4
  • Smith A. E., Helenius A. How viruses enter animal cells. Science 2004; 304: 237–42
  • Singer S. J., Nicholson G. L. The fluid‐mosaic model of the structure of cell membranes. Science 1972; 175: 720–31
  • Simons K., Ikonen E. Functional rafts in cell membranes. Nature 1997; 387: 569–72
  • Parton R. G. Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. J Histochem Cytochem 1994; 42: 155–66
  • Anderson R. G., Jacobson K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 2002; 296: 1821–5
  • Varma R., Mayor S. GPI‐anchored proteins are organized in submicron domains at the cell surface. Nature 1998; 394: 798–801
  • Sharma P., Varma R., Sarasij R. C., Ira, Gousset K., Krishnamoorthy G. Nanoscale organization of multiple GPI‐anchored proteins in living cell membranes. Cell 2004; 116: 577–89
  • Friedrichson T., Kurzchalia T. V. Microdomains of GPI‐anchored proteins in living cells revealed by crosslinking. Nature 1998; 394: 802–5
  • Brown D. A., Rose J. K. Sorting of GPI‐anchored proteins to glycolipid‐enriched membrane subdomains during transport to the apical cell surface. Cell 1992; 68: 533–44
  • Foster L. J., De Hoog C. L., Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci U S A 2003; 100: 5813–8
  • Sargiacomo M., Sudol M., Tang Z., Lisanti M. P. Signal transducing molecules and glycosyl‐phosphatidylinositol‐linked proteins form a caveolin‐rich insoluble complex in MDCK cells. J Cell Biol 1993; 122: 789–807
  • Rothberg K. G., Heuser J. E., Donzell W. C., Ying Y. S., Glenney J. R., Anderson R. G. Caveolin, a protein component of caveolae membrane coats. Cell 1992; 68: 673–82
  • Mayor S., Rothberg K. G., Maxfield F. R. Sequestration of GPI‐anchored proteins in caveolae triggered by cross‐linking. Science 1994; 264: 1948–51
  • Simons K., Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 2000; 1: 31–9
  • Simons K., Ikonen E. How cells handle cholesterol. Science 2000; 290: 1721–6
  • Schnitzer J. E., Oh P., McIntosh D. P. Role of GTP hydrolysis in fission of caveolae directly from plasma membranes. Science 1996; 274: 239–42
  • Nichols B. J., Kenworthy A. K., Polishchuk R. S., Lodge R., Roberts T. H., Hirschberg K. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J Cell Biol 2001; 153: 529–41
  • Simons K., Ehehalt R. Cholesterol, lipid rafts, and disease. J Clin Invest 2002; 110: 597–603
  • Ehehalt R., Keller P., Haass C., Thiele C., Simons K. Amyloidogenic processing of the Alzheimer beta‐amyloid precursor protein depends on lipid rafts. J Cell Biol 2003; 160: 113–23
  • Ikonen E., Parton R. G. Caveolins and cellular cholesterol balance. Traffic 2000; 1: 212–7
  • Munro S. Lipid rafts: elusive or illusive?. Cell 2003; 115: 377–88
  • Schuck S., Honsho M., Ekroos K., Shevchenko A., Simons K. Resistance of cell membranes to different detergents. Proc Natl Acad Sci U S A 2003; 100: 5795–800
  • Zacharias D. A., Violin J. D., Newton A. C., Tsien R. Y. Partitioning of lipid‐modified monomeric GFPs into membrane microdomains of live cells. Science 2002; 296: 913–6
  • Palade G. Fine structure of blood capillaries. J Appl Physiol 1953; 24: 1424
  • Yamada E. The fine structure of the gall bladder epithelium of the mouse. J Biophys Biochem Cytol 1955; 1: 455–8
  • Kurzchalia T. V., Dupree P., Parton R. G., Kellner R., Virta H., Lehnert M. VIP21, a 21‐kD membrane protein is an integral component of trans‐Golgi‐network‐derived transport vesicles. J Cell Biol 1992; 118: 1003–14
  • Dietzen D. J., Hastings W. R., Lublin D. M. Caveolin is palmitoylated on multiple cysteine residues. Palmitoylation is not necessary for localization of caveolin to caveolae. J Biol Chem 1995; 270: 6838–42
  • Murata M., Peränen J., Schreiner R., Wieland F., Kurzchalia T. V., Simons K. VIP21/caveolin is a cholesterol‐binding protein. Proc Natl Acad Sci U S A 1995; 92: 10339–43
  • Scheiffele P., Verkade P., Fra A. M., Virta H., Simons K., Ikonen E. Caveolin‐1 and ‐2 in the exocytic pathway of MDCK cells. J Cell Biol 1998; 140: 795–806
  • Scherer P. E., Okamoto T., Chun M., Nishimoto I., Lodish H. F., Lisanti M. P. Identification, sequence, and expression of caveolin‐2 defines a caveolin gene family. Proc Natl Acad Sci U S A 1996; 93: 131–5
  • Parton R. G., Way M., Zorzi N., Stang E. Caveolin‐3 associates with developing T‐tubules during muscle differentiation. J Cell Biol 1997; 136: 137–54
  • Way M., Parton R. G. M‐caveolin, a muscle‐specific caveolin‐related protein. FEBS Lett 1995; 376: 108–12
  • Smart E. J., Ying Y., Donzell W. C., Anderson R. G. A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J Biol Chem 1996; 271: 29427–35
  • Hailstones D., Sleer L. S., Parton R. G., Stanley K. K. Regulation of caveolin and caveolae by cholesterol in MDCK cells. J Lipid Res 1998; 39: 369–79
  • Chang W. J., Rothberg K. G., Kamen B. A., Anderson R. G. Lowering the cholesterol content of MA104 cells inhibits receptor‐mediated transport of folate. J Cell Biol 1992; 118: 63–9
  • Monier S., Parton R. G., Vogel F., Behlke J., Henske A., Kurzchalia T. V. VIP21‐caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol Biol Cell 1995; 6: 911–27
  • Fernandez I., Ying Y., Albanesi J., Anderson R. G. Mechanism of caveolin filament assembly. Proc Natl Acad Sci U S A 2002; 99: 11193–8
  • Pelkmans L., Kartenbeck J., Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two‐step vesicular‐transport pathway to the ER. Nat Cell Biol 2001; 3: 473–83
  • Gagescu R., Demaurex N., Parton R. G., Hunziker W., Huber L. A., Gruenberg J. The recycling endosome of Madin‐Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol Biol Cell 2000; 11: 2775–91
  • Pelkmans L., Burli T., Zerial M., Helenius A. Caveolin‐stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 2004; 118: 767–80
  • Parton R. G., Joggerst B., Simons K. Regulated internalization of caveolae. J Cell Biol 1994; 127: 1199–215
  • Schnitzer J. E., McIntosh D. P., Dvorak A. M., Liu J., Oh P. Separation of caveolae from associated microdomains of GPI‐anchored proteins. Science 1995; 269: 1435–9
  • Mineo C., James G. L., Smart E. J., Anderson R. G. Localization of epidermal growth factor‐stimulated Ras/Raf‐1 interaction to caveolae membrane. J Biol Chem 1996; 271: 11930–5
  • Mineo C., Ying Y. S., Chapline C., Jaken S., Anderson R. G. Targeting of protein kinase Calpha to caveolae. J Cell Biol 1998; 141: 601–10
  • Garcia‐Cardena G., Oh P., Liu J., Schnitzer J. E., Sessa W. C. Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proc Natl Acad Sci U S A 1996; 93: 6448–53
  • Glenney J. R., J. r. Tyrosine phosphorylation of a 22‐kDa protein is correlated with transformation by Rous sarcoma virus. J Biol Chem 1989; 264: 20163–6
  • Cohen A. W., Hnasko R., Schubert W., Lisanti M. P. Role of caveolae and caveolins in health and disease. Physiol Rev 2004; 84: 1341–79
  • Woodman S. E., Sotgia F., Galbiati F., Minetti C., Lisanti M. P. Caveolinopathies: mutations in caveolin‐3 cause four distinct autosomal dominant muscle diseases. Neurology 2004; 62: 538–43
  • Nishiyama K., Trapp B. D., Ikezu T., Ransohoff R. M., Tomita T., Iwatsubo T. Caveolin‐3 upregulation activates beta‐secretase‐mediated cleavage of the amyloid precursor protein in Alzheimer's disease. J Neurosci 1999; 19: 6538–48
  • Drab M., Verkade P., Elger M., Kasper M., Lohn M., Lauterbach B. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin‐1 gene‐disrupted mice. Science 2001; 293: 2449–52
  • Park D. S., Cohen A. W., Frank P. G., Razani B., Lee H., Williams T. M. Caveolin‐1 null (‐/‐) mice show dramatic reductions in life span. Biochemistry 2003; 42: 15124–31
  • Mundy D. I., Machleidt T., Ying Y. S., Anderson R. G., Bloom G. S. Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. J Cell Sci 2002; 115: 4327–39
  • Henley J. R., Krueger E. W., Oswald B. J., McNiven M. A. Dynamin‐mediated internalization of caveolae. J Cell Biol 1998; 141: 85–99
  • Oh P., McIntosh D. P., Schnitzer J. E. Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP‐driven fission from the plasma membrane of endothelium. J Cell Biol 1998; 141: 101–14
  • Smart E. J., Foster D. C., Ying Y. S., Kamen B. A., Anderson R. G. Protein kinase C activators inhibit receptor‐mediated potocytosis by preventing internalization of caveolae. J Cell Biol 1994; 124: 307–13
  • Conrad P. A., Smart E. J., Ying Y. S., Anderson R. G., Bloom G. S. Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule‐dependent and microtubule‐independent steps. J Cell Biol 1995; 131: 1421–33
  • Damke H., Baba T., Warnock D. E., Schmid S. L. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 1994; 127: 915–34
  • Lamaze C., Dujeancourt A., Baba T., Lo C. G., Benmerah A., Dautry‐Varsat A. Interleukin 2 receptors and detergent‐resistant membrane domains define a clathrin‐independent endocytic pathway. Mol Cell 2001; 7: 661–71
  • Sharma D. K., Brown J. C., Choudhury A., Peterson T. E., Holicky E., Marks D. L. Selective stimulation of caveolar endocytosis by glycosphingolipids and cholesterol. Mol Biol Cell 2004; 15: 3114–22
  • Benlimame N., Le P. U., Nabi I. R. Localization of autocrine motility factor receptor to caveolae and clathrin‐independent internalization of its ligand to smooth endoplasmic reticulum. Mol Biol Cell 1998; 9: 1773–86
  • Montesano R., Roth J., Robert A., Orci L. Non‐coated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature 1982; 296: 651–3
  • Nichols B. J. A distinct class of endosome mediates clathrin‐independent endocytosis to the Golgi complex. Nat Cell Biol 2002; 4: 374–8
  • Shin J. S., Gao Z., Abraham S. N. Involvement of cellular caveolae in bacterial entry into mast cells. Science 2000; 289: 785–8
  • Pelkmans L., Helenius A. Endocytosis via caveolae. Traffic 2002; 3: 311–20
  • Peters P. J., Mironov A., Peretz D., Jr, van Donselaar E., Leclerc E., Erpel S. Trafficking of prion proteins through a caveolae‐mediated endosomal pathway. J Cell Biol 2003; 162: 703–17
  • Damm E. M., Pelkmans L., Kartenbeck J., Mezzacasa A., Kurzchalia T., Helenius A. Clathrin‐ and caveolin‐1‐independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 2005; 168: 477–88
  • Le P. U., Nabi I. R. Distinct caveolae‐mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. J Cell Sci 2003; 116: 1059–71
  • Anderson H. A., Chen Y., Norkin L. C. Bound simian virus 40 translocates to caveolin‐enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol Biol Cell 1996; 7: 1825–34
  • Pelkmans L., Puntener D., Helenius A. Local actin polymerization and dynamin recruitment in SV40‐induced internalization of caveolae. Science 2002; 296: 535–9
  • Marjomäki V., Pietiäinen V., Matilainen H., Upla P., Ivaska J., Nissinen L. Internalization of echovirus 1 in caveolae. J Virol 2002; 76: 1856–65
  • Pietiäinen V., Marjomäki V., Upla P., Pelkmans L., Helenius A., Hyypiä T. Echovirus 1 endocytosis into caveosomes requires lipid rafts, dynamin II, and signaling events. Mol Biol Cell 2004; 15: 4911–25
  • Richterova Z., Liebl D., Horak M., Palkova Z., Stokrova J., Hozak P. Caveolae are involved in the trafficking of mouse polyomavirus virions and artificial VP1 pseudocapsids toward cell nuclei. J Virol 2001; 75: 10880–91
  • Nunes‐Correia I., Eulalio A., Nir S., Pedroso de Lima M. C. Caveolae as an additional route for influenza virus endocytosis in MDCK cells. Cell Mol Biol Lett 2004; 9: 47–60
  • Nomura R., Kiyota A., Suzaki E., Kataoka K., Ohe Y., Miyamoto K. Human coronavirus 229E binds to CD13 in rafts and enters the cell through caveolae. J Virol 2004; 78: 8701–8
  • Bousarghin L., Touze A., Sizaret P. Y., Coursaget P. Human papillomavirus types 16, 31, and 58 use different endocytosis pathways to enter cells. J Virol 2003; 77: 3846–50
  • Brown G., Jeffree C. E., McDonald T., Rixon H. W., Aitken J. D., Sugrue R. J. Analysis of the interaction between respiratory syncytial virus and lipid‐rafts in Hep2 cells during infection. Virology 2004; 327: 175–85
  • Werling D., Hope J. C., Chaplin P., Collins R. A., Taylor G., Howard C. J. Involvement of caveolae in the uptake of respiratory syncytial virus antigen by dendritic cells. J Leukoc Biol 1999; 66: 50–8
  • Tsai B., Gilbert J. M., Stehle T., Lencer W., Benjamin T. L., Rapoport T. A. Gangliosides are receptors for murine polyoma virus and SV40. EMBO J 2003; 22: 4346–55
  • Bernacchi S., Mueller G., Langowski J., Waldeck W. Characterization of simian virus 40 on its infectious entry pathway in cells using fluorescence correlation spectroscopy. Biochem Soc Trans 2004; 32: 746–9
  • Anderson H. A., Chen Y., Norkin L. C. MHC class I molecules are enriched in caveolae but do not enter with simian virus 40. J Gen Virol 1998; 79: 1469–77
  • Stang E., Kartenbeck J., Parton R. G. Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol Biol Cell 1997; 8: 47–57
  • Pelkmans L., Helenius A. Insider information: what viruses tell us about endocytosis. Curr Opin Cell Biol 2003; 15: 414–22
  • Dangoria N. S., Breau W. C., Anderson H. A., Cishek D. M., Norkin L. C. Extracellular simian virus 40 induces an ERK/MAP kinase‐independent signalling pathway that activates primary response genes and promotes virus entry. J Gen Virol 1996; 77: 2173–82
  • Roy S., Luetterforst R., Harding A., Apolloni A., Etheridge M., Stang E. Dominant‐negative caveolin inhibits H‐Ras function by disrupting cholesterol‐rich plasma membrane domains. Nat Cell Biol 1999; 1: 98–105
  • Richards A. A., Stang E., Pepperkok R., Parton R. G. Inhibitors of COP‐mediated transport and cholera toxin action inhibit simian virus 40 infection. Mol Biol Cell 2002; 13: 1750–64
  • Kasamatsu H., Nakanishi A. How do animal DNA viruses get to the nucleus?. Annu Rev Microbiol 1998; 52: 627–86
  • Smith A. E., Lilie H., Helenius A. Ganglioside‐dependent cell attachment and endocytosis of murine polyomavirus‐like particles. FEBS Lett 2003; 555: 199–203
  • Gilbert J. M., Goldberg I. G., Benjamin T. L. Cell penetration and trafficking of polyomavirus. J Virol 2003; 77: 2615–22
  • Gilbert J. M., Benjamin T. L. Early steps of polyomavirus entry into cells. J Virol 2000; 74: 8582–8
  • Gilbert J., Benjamin T. Uptake pathway of polyomavirus via ganglioside GD1a. J Virol 2004; 78: 12259–67
  • Bergelson J. M., Shepley M. P., Chan B. M., Hemler M. E., Finberg R. W. Identification of the integrin VLA‐2 as a receptor for echovirus 1. Science 1992; 255: 1718–20
  • Bergelson J. M., St John N. F., Kawaguchi S., Pasqualini R., Berdichevsky F., Hemler M. E. The I domain is essential for echovirus 1 interaction with VLA‐2. Cell Adhes Commun 1994; 2: 455–64
  • Ward T., Powell R. M., Pipkin P. A., Evans D. J., Minor P. D., Almond J. W. Role for beta2‐microglobulin in echovirus infection of rhabdomyosarcoma cells. J Virol 1998; 72: 5360–5
  • Xing L., Huhtala M., Pietiäinen V., Käpyla J., Vuorinen K., Marjomäki V. Structural and functional analysis of integrin alpha2I domain interaction with echovirus 1. J Biol Chem 2004; 279: 11632–8
  • Upla P., Marjomäki V., Kankaanpää P., Ivaska J., Hyypiä T., Van Der Goot F. G. Clustering induces a lateral redistribution of alpha 2 beta 1 integrin from membrane rafts to caveolae and subsequent protein kinase C‐dependent internalization. Mol Biol Cell 2004; 15: 625–36
  • Pelkmans L., Fava E., Grabner H., Hannus M., Habermann B., Krausz E. Genome‐wide analysis of human kinases in clathrin‐ and caveolae/raft‐mediated endocytosis. Nature 2005
  • Narayan S., Barnard R. J., Young J. A. Two retroviral entry pathways distinguished by lipid raft association of the viral receptor and differences in viral infectivity. J Virol 2003; 77: 1977–83
  • Manes S., del Real G., Lacalle R. A., Lucas P., Gomez‐Mouton C., Sanchez‐Palomino S. Membrane raft microdomains mediate lateral assemblies required for HIV‐1 infection. EMBO Rep 2000; 1: 190–6
  • Avota E., Muller N., Klett M., Schneider‐Schaulies S. Measles virus interacts with and alters signal transduction in T‐cell lipid rafts. J Virol 2004; 78: 9552–9
  • Stuart A. D., Eustace H. E., McKee T. A., Brown T. D. A novel cell entry pathway for a DAF‐using human enterovirus is dependent on lipid rafts. J Virol 2002; 76: 9307–22
  • Triantafilou K., Triantafilou M. Lipid raft microdomains: key sites for Coxsackievirus A9 infectious cycle. Virology 2003; 317: 128–35
  • Triantafilou K., Triantafilou M. Lipid‐raft‐dependent Coxsackievirus B4 internalization and rapid targeting to the Golgi. Virology 2004; 326: 6–19
  • Sanchez‐San Martin C., Lopez T., Arias C. F., Lopez S. Characterization of rotavirus cell entry. J Virol 2004; 78: 2310–8
  • Ward T., Pipkin P. A., Clarkson N. A., Stone D. M., Minor P. D., Almond J. W. Decay‐accelerating factor CD55 is identified as the receptor for echovirus 7 using CELICS, a rapid immuno‐focal cloning method. EMBO J 1994; 13: 5070–4
  • Isa P., Realpe M., Romero P., Lopez S., Arias C. F. Rotavirus RRV associates with lipid membrane microdomains during cell entry. Virology 2004; 322: 370–81
  • Nisole S., Krust B., Hovanessian A. G. Anchorage of HIV on permissive cells leads to coaggregation of viral particles with surface nucleolin at membrane raft microdomains. Exp Cell Res 2002; 276: 155–73
  • Popik W., Alce T. M., Au W. C. Human immunodeficiency virus type 1 uses lipid raft‐colocalized CD4 and chemokine receptors for productive entry into CD4(+) T cells. J Virol 2002; 76: 4709–22
  • Del Real G., Jimenez‐Baranda S., Lacalle R. A., Mira E., Lucas P., Gomez‐Mouton C. Blocking of HIV‐1 infection by targeting CD4 to nonraft membrane domains. J Exp Med 2002; 196: 293–301
  • Liu N. Q., Lossinsky A. S., Popik W., Li X., Gujuluva C., Kriederman B. Human immunodeficiency virus type 1 enters brain microvascular endothelia by macropinocytosis dependent on lipid rafts and the mitogen‐activated protein kinase signaling pathway. J Virol 2002; 76: 6689–700
  • Percherancier Y., Lagane B., Planchenault T., Staropoli I., Altmeyer R., Virelizier J. L. HIV‐1 entry into T‐cells is not dependent on CD4 and CCR5 localization to sphingolipid‐enriched, detergent‐resistant, raft membrane domains. J Biol Chem 2003; 278: 3153–61
  • Popik W., Alce T. M. CD4 receptor localized to non‐raft membrane microdomains supports HIV‐1 entry. Identification of a novel raft localization marker in CD4. J Biol Chem 2004; 279: 704–12

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.