Pathogens: Raft hijackers

Nature Reviews Immunology

Volumn 3, Issue 7, 2003, Pages 557-568

  Mañes, Santos ^a   Del Real, Gustavo ^a   Martínez A, Carlos ^a  

^a CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; CELL MEMBRANE PROTEIN; CHOLESTEROL; GLYCOSPHINGOLIPID; MEMBRANE LIPID;

BACTERIAL INFECTION; CELL MEMBRANE; DRUG TARGETING; EBOLA VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; IMMUNE SYSTEM; LIPID RAFT; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SURVIVAL; VIRUS ASSEMBLY; VIRUS INFECTION;

ANIMALS; BACTERIA; BACTERIAL TOXINS; COMMUNICABLE DISEASES; HUMANS; IMMUNOLOGIC SURVEILLANCE; MEMBRANE MICRODOMAINS; PROTOZOA; SIGNAL TRANSDUCTION; VIRUSES;

EID: 0142197614     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri1129     Document Type: Review

References (114)

1. Brown, D. & London, E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221-17224 (2000).
2. Simons, K. & Toomre, D. Lipid rafts and signal transduction. Nature Rev. Mol. Cell Biol. 1, 31-39 (2000).
3. Pierce, S. Lipid rafts and B-cell activation. Nature Rev. Immunol. 2, 96-105 (2002).
4. Simons, K. & Ehehalt, R. Cholesterol, lipid rafts, and disease. J. Clin. Invest. 110, 597-603 (2002).
5. Pizzo, P. & Vola, A. Lymphocyte lipid rafts: structure and function. Curr. Opin. Immunol. 15, 255-260 (2003). References 1-5 are reviews that describe the importance of understanding what rafts are and how these microdomains modulate signalling through clonally distributed receptors in lymphocytes.
6. van der Goot, F. & Harder, T. Raft membrane domains: from a liquid-ordered membrane phase to a site of pathogen attack. Semin. Immunol. 13, 89-97 (2001).
7. Rosenberger, C., Brumell, J. & Finlay, B. Microbial pathogenesis: lipid rafts as pathogen portals. Curr. Biol. 10, R823-R825 (2000).
8. Harder, T., Scheiffele, P., Verkade, P. & Simons, K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141, 929-942 (1998). The first paper to show that clusters of rafts segregate from non-raft assemblies.
9. Miceli, M. et al. Co-stimulation and counter-stimulation: lipid raft clustering controls TCR signaling and functional outcomes. Semin. Immunol. 13, 115-128 (2001).
10. Drevot, P. et al. TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J. 21, 1899-1908 (2002).
11. Guo, B., Kato, R., Garcia-Lloret, M., Wahl, M. & Rawlings, D. Engagement of the human pre-B cell receptor generates a lipid raft-dependent calcium signaling complex. Immunity 13, 243-253 (2000).
12. Triantafilou, M., Miyake, K., Golenbock, D. & Triantafilou, K. Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J. Cell. Sci. 115, 2603-2611 (2002).
13. Beutler, B. & Rietschel, E. Innate immune sensing and its roots: the story of endotoxin. Nature Rev. Immunol. 3, 169-176 (2003).
14. Alfsen, A., Iniguez, P., Bouguyon, E. & Bomsel, M. Secretory IgA specific for a conserved epitope on gp41 envelope glycoprotein inhibits epithelial transcytosis of HIV-1. J. Immunol. 166, 6257-6265 (2001).
15. Mañes, S. et al. Membrane raft microdomains mediate lateral assemblies required for HIV-1 infection. EMBO Rep. 1, 190-196 (2000).
16. Peterlin, B. & Trono, D. Hide, shield and strike back: how HIV-infected cells avoid immune eradication. Nature Rev. Immunol. 3, 97-107 (2003).
17. Nguyen, D. & Hildreth, J. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipidenriched membrane lipid rafts. J. Virol. 74, 3264-3272 (2000).
18. Liu, N. et al. 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. 76, 6689-6700 (2002). References 14-18 describe the crucial role of rafts at distinct stages during the HIV-1 life cycle in immune and non-immune cells.
19. Selvarangan, R. et al. Role of decay-accelerating factor domains and anchorage in internalization of Dr-Fimbriated Escherichia coli. Infect. Immun. 68, 1391-1399 (2000).
20. Peiffer, I., Servin, A. & Bernet-Camard, M. Piracy of decay-accelerating factor (CD55) signal transduction by the diffusely adhering strain Escherichia coli C1845 promotes cytoskeletal F-actin rearrangements in cultured human intestinal INT407 cells. Infect. Immun. 66, 4036-4042 (1998).
21. Stuart, A., Eustace, H., McKee, T. & Brown, T. A novel cell entry pathway for a DAF-using human enterovirus is dependent on lipid rafts. J. Virol. 76, 9307-9322 (2002).
22. Oliferenko, S. et al. Analysis of CD44-containing lipid rafts: recruitment of annexin II and stabilization by the actin cytoskeleton. J. Cell Biol. 146, 843-854 (1999).
23. Desiardins, M. ER-mediated phagocytosis: a new membrane for new functions. Nature Rev. Immunol. 3, 280-291 (2003).
24. Gatfield, J. & Pieters, J. Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288, 1647-1650 (2000). This paper and reference 31 were the first to show the role of lipid rafts in promoting the intracellular survival of bacteria.
25. Peyron, P., Bordier, C., N'Diaye, E. & Maridonneau-Parini, I. Nonopsonic phagocytosis of Mycobacterium kansasii by human neutrophils depends on cholesterol and is mediated by CR3 associated with glycosylphosphatidylinositol-anchored proteins. J. Immunol. 165, 5186-5191 (2000).
26. Naroeni, A. & Porte, F. Role of cholesterol and the gangiloside GM1 in entry and short-term survival of Brucella suis in murine macrophages. Infect. Immun. 70, 640-1644 (2002).
27. Watarai, M. et al. Macrophage plasma membrane cholesterol contributes to Brucella abortus infection of mice. Infect. Immun. 70, 4818-4825 (2002).
28. Watarai, M. et al. Legionella pneumophila is internalized by a macropinocytotic uptake pathway controlled by the Dot/lcm system and the mouse Lgn1 locus. J. Exp. Med. 194, 1081-1096 (2001).
29. Kim, S., Watarai, M., Makino, S. & Shirahata, T. Membrane sorting during swimming internalization of Brucella is required for phagosome trafficking decisions. Microb. Pathog. 33, 225-237 (2002).
30. Ferrari, G., Langen, H., Naito, M. & Pieters, J. A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97, 435-447 (1999).
31. Shin, J., Gao, Z. & Abraham, S. Involvement of cellular caveolae in bacterial entry into mast cells. Science 289, 785-788 (2000).
32. Norkin, L., Wolfrom, S. & Stuart, E. Association of caveolin with Chlamydia trachomatis inclusions at early and late stages of infection. Exp. Cell Res. 288, 229-238 (2001).
33. Simons, K. & Gruenberg, J. Jamming the endosomal system: lipid rafts and lysosomal storage diseases. Trends Cell Biol. 10, 459-462 (2000).
34. Nichols, B. & Lippincott-Schwartz, J. Endocytosis without clathrin coats. Trends Cell Biol. 11, 406-412 (2001).
35. Mañes, S., Lacalle, R., Gómez-Moutón, C. & Martínez-A, C. From rafts to crafts: membrane assymetry in moving cells. Trends Immunol. 2003 24, 319-325 (2003).
36. Lafont, F., Tran Van Nhieu, G., Hanada, K., Sansonetti, P. & van der Goot, F. Initial steps of Shigella infection depend on the cholesterol/sphingolipid raft-mediated CD44-IpaB interaction. EMBO J. 21, 4449-4457 (2002). This study described how bacteria promote their macropinocytotic uptake by taking over host raft-associated signalling pathways that link these microdomains with the actin cytoskeleton.
37. Lacalle, R. et al. Specific SHP-2 partitioning in raft domains triggers integrin-mediated signaling via Rho activation. J. Cell Biol. 157, 277-289 (2002).
38. Coconnier, M., Lorrot, M., Barbat, A., Laboisse, C. & Servin, A. Listeriolysin O-induced stimulation of mucin exocytosis in polarized intestinal mucin-secreting cells: evidence for toxin recognition of membrane-associated lipids and subsequent toxin internalization through caveolae. Cell. Microbiol. 2, 487-504 (2000).
39. Kayal, S. et al. Listeriolysin O secreted by Listeria monocytogenes induces NF-κB signalling by activating the IκB kinase complex. Mol. Microbiol. 44, 1407-1419 (2002).
40. Grassmé, H. et al. Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nature Med. 9, 322-330 (2003).
41. Fivaz, M., Abrami, L. & van der Goot, F. Landing on lipid rafts. Trends Cell Biol. 9, 212-213 (1999).
42. Pfeiffer, A. et al. Lipopolysaccharide and ceramide docking to CD14 provokes ligand-specific receptor clustering in rafts. Eur. J. Immunol. 31, 3153-3164 (2001).
43. Norkin, L. Simian virus 40 infection via MHC class I molecules and caveolae. Immunol. Rev. 168, 13-22 (1999).
44. Parton, R. & Lindsay, M. Exploitation of major histocomplatibility complex class I molecules and caveolae by simian virus 40. Immunol. Rev. 168, 23-31 (1999).
45. Parton, R., Joggerst, B. & Simons, K. Regulated internalization of caveolae. J. Cell Biol. 127, 1199-1215 (1994).
46. Märjomaki, V. et al. Internalization of echovirus 1 in caveolae. J. Virol. 76, 1856-1865 (2002).
47. Ann, A., Gibbons, D. & Kielian, M. The fusion peptide of Semliki Forest virus associates with sterol-rich membrane domains. J. Virol. 76, 3267-3275 (2002).
48. Xu, X. & London, E. The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation Biochemistry 39, 843-849 (2000).
49. Waarts, B., Bittman, R. & Wilschut, J. Sphingolipid and cholesterol dependence of alphavirus membrane fusion. Lack of correlation with lipid raft formation in target liposomes. J. Biol. Chem. 277, 38141-38147 (2002).
50. Doms, R. & Trono, D. The plasma membrane as a combat zone in the HIV battlefield. Genes Dev. 14, 2677-2688 (2000).
51. Mellado, M., Rodríguez-Frade, J., Mañes, S. & Martínez-A, C. Chemokine signaling and functional responses: the role of receptor dimerization and TK pathway activation. Annu. Rev. Immunol. 19, 397-421 (2001).
52. Hammache, D., Yahi, N., Maresca, M., Pieroni, G. & Fantini, J. Human erythrocyte glycosphingolipids as alternative cofactors for human immunodeficiency virus type 1 (HIV-1) entry: evidence for CD4-induced interactions between HIV-1 gp120 and reconstituted membrane microdomains of glycosphingolipids (Gb3 and GM3). J. Virol. 73, 5244-5248 (1999).
53. Liao, Z., Cimakasky L., Hampton, R., Nguyen, D. & Hildreth, J. Lipid rafts and HIV pathogenesis: host membrane cholesterol is required for infection by HIV type 1. AIDS Res. Hum. Retroviruses 17, 1009-1019 (2001).
54. + T cells. J. Virol. 76, 4709-4722 (2002).
55. Khanna, K. et al. Vaginal transmission of cell-associated HIV-1 in the mouse is blocked by a topical, membrane-modifying agent. J. Clin. Invest. 109, 205-211 (2002). This article analyses the use of rafts as therapeutic targets to prevent infection with HIV-1 in vivo.
56. Nisole, S., Krust, B. & Hovanessian, A. Anchorage of HIV on permissive cells leads to coaggregation of viral particles with surface nucleolin at membrane raft microdomains. Exp. Cell Res. 216, 155-173 (2002).
57. del Real, G. et al. Blocking of HIV-1 infection by targeting CD4 to non-raft membrane domains. J. Exp. Med. 196, 293-301 (2002).
58. Gallo, S., Puri, A. & Blumenthal, R. HIV-1 gp41 six-helix bundle formation occurs rapidly after the engagement of gp120 by CXCR4 in the HIV-1 Env-mediated fusion process. Biochemistry 40, 12231-12236 (2001).
59. Viard, M. et al. Role of cholesterol in human immunodeficiency virus type 1 envelope protein-mediated fusion with host cells. J. Virol. 76, 11584-11595 (2002).
60. Nguyen, D. & Taub, D. Cholesterol is essential for macrophage inflammatory protein 1β binding and conformational integrity of CC chemokine receptor 5. Blood 99, 4296-4306 (2002).
61. Nguyen, D. & Taub, D. CXCR4 function requires membrane cholesterol: implications for HIV infection. J. Immunol. 168, 4121-4126 (2002).
62. Mañes, S. et al. Membrane raft microdomains mediate front-rear polarity in migrating cells. EMBO J. 18, 6211-6220 (1999).
63. Mañes, S. et al. Membrane raft microdomains in chemokine receptor function. Semin. Immunol. 13, 147-157 (2001).
64. Sorice, M. et al. Evidence for cell surface association between CXCR4 and ganglioside GM3 after gp120 binding in SupT1 lymphoblastoid cells. FEBS Letters 506, 55-60 (2001).
65. Hug, P. et al. 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 (2000).
66. Kozak, S., Heard, J. & Kabat, D. 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 (2002).
67. Percherancier, Y. et al. 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. 278, 3153-3161 (2003).
68. Scheiffele, P., Rietveld, A., Wilk, T. & Simons, K. Influenza viruses select ordered lipid domains during budding from the plasma membrane. J. Biol. Chem. 274, 2038-2044 (1999).
69. Manie, S., Debreyne, S., Vincent, S. & Gedier, D. Measles virus structural components are enriched into lipid raft microdomains: a potential cellular location for virus assembly. J. Virol. 74, 305-311 (2000).
70. Marquardt, M., Phalen, T. & Kielian, M. Cholesterol is required in the exit pathway of Semliki forest virus. J. Cell Biol. 123, 57-65 (1993).
71. Bavari, S. et al. Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg Viruses. J. Exp. Med. 195, 593-602 (2002).
72. Lee, G., Church, G. & Wilson, D. A subpopulation of tegument protein Vhs localizes to detergent-insoluble lipid rafts in herpes simplex virus-infected cells. J. Virol. 77, 2038-2045 (2003).
73. Campbell, S., Crowe, S. & Mak, J. Virion-associated cholesterol is critical for the maintenance of HIV-1 structure and infectivity. AIDS 16, 2253-2261 (2002).
74. Guyader, M., Kiyokawa, E., Abrami, L., Turelli, P. & Trono, D. Role for human immunodeficiency virus type 1 membrane cholesterol in viral internalization. J. Virol. 76, 10356-10364 (2002).
75. Vanderplasschen, A., Mathew, E., Hollinshead, M., Sim, R. & Smith, G. Extracellular enveloped vaccinia virus is resistant to complement because of incorporation of host complement control proteins into its envelope. Proc. Natl Acad. Sci. USA. 95, 7544-7549 (1998). The authors provide a clear example of how viruses bud from rafts to manipulate immune responses.
76. Knox, P. & Young, L. Epstein-Barr virus infection of CR2-transfected epithelial cells reveals the presence of MHC class II on the virion. Virology 213, 147-157 (1995).
77. Cantin, R., Fortin, J., Lamontagne, G. & Tremblay, M. The presence of host-derived HLA-DR1 on human immunodeficiency virus type 1 increases viral infectivity. J. Virol. 71, 1922-1930 (1997).
78. Hildreth, J. Syncytium-inhibiting monoclonal antibodies produced against human T-cell lymphotropic virus type 1-infected cells recognize class II major histocompatibility complex molecules and block by protein crowding. J. Virol. 12, 9544-9552 (1998).
79. Rossio, J., Bess, J., Henderson, L., Cresswell, P. & Arthur, L. HLA class II on HIV particles is functional in superantigen presentation to human T cells: implications for HIV pathogenesis. AIDS Res. Hum. Retroviruses 11, 1433-1439 (1995).
80. Aikawa, M., Miller, L., Johnson, J. & Rabbege, J. Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. J. Cell Biol. 77, 72-82 (1978).
81. Suss-Toby, E., Zimmerberg, J. & Ward, G. Toxoplasma invasion: the parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. Proc. Natl Acad. Sci. USA 93, 8413-8418 (1996).
82. Joiner, K., Fuhrman, S., Miettinen, H., Kasper, L. & Mellman, I. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249, 641-646 (1990).
83. Lauer, S. et al. Vacuolar uptake of host components, and a role for cholesterol and sphingomyelin in malarial infection. EMBO J. 19, 3556-3564 (2000). This paper and reference 114 show that raft-associated proteins can access the protozoa vacuole. In the absence of endocytosis, raft lipids such as sphingomyelin and cholesterol regulate the intracellular survival of the malaria protozoan.
84. Samuel, B. et al. The role of cholesterol and glycosylphosphatidylinositol-anchored proteins of erythrocyte rafts in regulating raft protein content and malarial infection. J. Biol. Chem. 276, 29319-29329 (2001).
85. Dobbelaere, D., Fernandez, P. & Heussler. V. Theileria parva: taking control of host cell proliferation and survival mechanisms. Cell. Microbiol. 2, 91-99 (2000).
86. Baumgartner, M. et al. Constitutive exclusion of Csk from Hck-positive membrane microdomains permits Src kinase-dependent proliferation of Theileria-transformed B lymphocytes. Blood 101, 1874-1881 (2003). The authors describe how protozoa hijack raft-associated signalling to manipulate proliferation and transformation of B cells.
87. Nolan, D. et al. Characterization of a novel alanine-rich protein located in surface microdomains in Trypanosoma brucei. J. Biol. Chem. 275, 4072-4080 (2000).
88. Denny, P., Field, M. & Smith, D. GPI-anchored proteins and glycoconjugates segregate into lipid rafts in Kinetoplastida. FEBS Lett. 491, 148-153 (2001).
89. Ostermeyer, A., Beckrich, B., Ivarson, K., Grove, K. & Brown, D. Glycosphingolipids are not essential for formation of detergent-resistant membrane rafts in melanoma cells. Methyl-β-cyclodextrin does not affect cell surface transport of a GPI-anchored protein. J. Biol. Chem. 274, 34459-34466 (1999).
90. De Angelis, D., Miesenbock, G., Zemelman, B. & Rothman, J. PRIM: proximity imaging of green fluorescent protein-tagged polypeptides. Proc. Natl Acad. Sci. USA 95, 12312-12316 (1998).
91. Varma, R. & Mayor, S. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394, 798-801 (1998).
92. Kenworthy, A., Petranova, N. & Edidin, M. High-resolution FRET microscopy of cholera toxin B-subunit and GPI-anchored protein in cell plasma membranes. Mol. Biol. Cell 11, 1645-1655 (2000).
93. Gómez-Moutón, C. et al. Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc. Natl Acad. Sci. USA 98, 9642-9647 (2001). The authors show the segregation of distinct raft domains in T cells, associating specific proteins and lipids.
94. Madore, N. et al. Functionally different GPI proteins are organized in different domains on the neuronal surface. EMBO J. 18, 6917-6926 (1999).
95. Parton, R. Caveolae - from ultrastructure to molecular mechanisms. Nature Rev. Mol. Cell Biol. 4, 162-167 (2003).
96. Wooldridge, K., Williams, P. & Ketley, J. Host signal transduction and endocytosis of Campylobacter jejuni. Microb. Pathog. 21, 299-305 (1996).
97. Baorto, D. et al. Survival of FimH-expressing enterobacteria in macrophages relies on glycolipid traffic. Nature 389, 636-639 (1997).
98. Garner, M., Hayward, R. & Koronakis, V. The Salmonella pathogenicity island 1 secretion system directs cellular cholesterol redistribution during mammalian cell entry and intracellular trafficking. Cell. Microbiol. 4, 153-165 (2002).
99. Catron, D. et al. The Salmonella-containing vacuole is a major site of intracellular cholesterol accumulation and recruits the GPI-anchored protein CD55. Cell. Microbiol. 4, 315-328 (2002).
100. Zitzer, A. et al. Coupling of cholesterol and cone-shaped lipids in bilayers augments membrane permeabilization by the cholesterol-specific toxins streptolysin O and Vibrio cholerae cytolysin. J. Biol. Chem. 276, 14628-14633 (2001).
101. Abrami, L. & van Der Goot, F. Plasma membrane microdomains act as concentration platforms to facilitate intoxication by aerolysin. J. Cell Biol. 147, 175-184 (1999). An elegant study showing that oligomerization efficiency of a toxin (and therefore toxicity) is markedly increased by its binding to and concentration in raft clusters.
102. Nishiki, T. et al. The high-affinity binding of Clostridium botulinum type B neurotoxin to synaptotagmin II associated with gangliosides GT1b/GD1a. FEBS Lett. 378, 253-257 (1996).
103. Herreros, J., Ng, T. & Schiavo, G. Lipid rafts act as specialized domains for tetanus toxin binding and internalization into neurons. Mol. Biol. Cell 12, 2947-2960 (2001).
104. Nusrat, A. et al. Clostridium difficile toxins disrupt epithelial barrier function by altering membrane microdomain localization of tight junction proteins. Infect. Immun. 69, 1329-1336 (2001).
105. Gordon, V. et al. Clostridium septicum α-toxin uses glycosylphosphatidylinositol-anchored protein receptors. J. Biol. Chem. 274, 27274-27280 (1999).
106. Miyata, S. et al. Clostridium perfringens ε-toxin forms a heptameric pore within the detergent-insoluble microdomains of Madin-Darby canine kidney cells and rat synaptosomes. J. Biol. Chem. 277, 39463-39468 (2002).
107. Waheed, A. et al. Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts). Proc. Natl Acad. Sci. USA 98, 4926-4931 (2001).
108. Abrami, L., Liu, S., Cosson, P., Leppla, S. & van der Goot, F. Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process. J. Cell Biol. 160, 321-328 (2003).
109. Zhuang, M. et al. Hellothis virescens and Manduca sexta lipid rafts are involved in Cry1A toxin binding to the midgut epithelium and subsequent pore formation. J. Biol. Chem. 277, 13863-13872 (2002).
110. Patel, H. et al. Plasma membrane cholesterol modulates cellular vacuolation induced by the Helicobacter pylori vacuolating cytotoxin. Infect. Immun. 70, 4112-4123 (2002).
111. Narayan, S., Barnard, R. & Young, J. Two retroviral entry pathways distinguished by lipid raft association of the viral receptor and differences in viral infectivity. J. Virol. 77, 1977-1983 (2003).
112. Lu, X., Xiong, Y. & Silver, J. 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 (2002).
113. Niyogi, K. & Hildreth, J. Charactenzation of new syncytium-inhibiting monoclonal antibodies implicates lipid rafts in human T-cell leukemia virus type 1 syncytium formation. J. Virol. 75, 7351-7361 (2001).
114. Mordue, D. Desai, N., Dustin, M. & Sibley, L. Invasion by Toxoplasma gondii establishes a moving junction that selectively excludes host cell plasma membrane proteins on the basis of their membrane anchoring. J. Exp. Med. 190, 1783-1792 (1999).