1887

Abstract

The immune system has a variety of tools at its disposal to combat virus infections. These can be subdivided roughly into two categories: ‘first line defence’, consisting of the non-specific, innate immune system, and ‘adaptive immune response’, acquired over time following virus infection or vaccination. During evolution, viruses have developed numerous, and often very ingenious, strategies to counteract efficient recognition of virions or virus-infected cells by both innate and adaptive immunity. This review will focus on the different strategies that viruses use to avoid recognition by one of the components of the immune system: the complement system. Complement evasion is of particular importance for viruses, since complement activation is a crucial component of innate immunity (alternative and mannan-binding lectin activation pathway) as well as of adaptive immunity (classical, antibody-dependent complement activation).

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.18709-0
2003-01-01
2020-01-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/1/vir840001.html?itemId=/content/journal/jgv/10.1099/vir.0.18709-0&mimeType=html&fmt=ahah

References

  1. Adler, R., Glorioso, J. C., Cossman, J. & Levine, M. ( 1978; ). Possible role of Fc receptors on cells infected and transformed by herpesvirus: escape from immune cytolysis. Infect Immun 21, 442–447.
    [Google Scholar]
  2. Afonso, C. L., Tulman, E. R., Lu, Z., Zsak, L., Osorio, F. A., Balinsky, C., Kutish, G. F. & Rock, D. L. ( 2002; ). The genome of swinepox virus. J Virol 76, 783–790.[CrossRef]
    [Google Scholar]
  3. Albrecht, J. C. & Fleckenstein, B. ( 1992; ). New member of the multigene family of complement control proteins in herpesvirus saimiri. J Virol 66, 3937–3940.
    [Google Scholar]
  4. Albrecht, J. C., Nicolas, J., Biller, D. & 7 other authors ( 1992a; ). Primary structure of the herpesvirus saimiri genome. J Virol 66, 5047–5058.
    [Google Scholar]
  5. Albrecht, J. C., Nicolas, J., Cameron, K. R., Newman, C., Fleckenstein, B. & Honess, R. W. ( 1992b; ). Herpesvirus saimiri has a gene specifying a homologue of the cellular membrane glycoprotein CD59. Virology 190, 527–530.[CrossRef]
    [Google Scholar]
  6. Appleyard, G., Hapel, A. J. & Boulter, E. A. ( 1971; ). An antigenic difference between intracellular and extracellular rabbitpox virus. J Gen Virol 13, 9–17.[CrossRef]
    [Google Scholar]
  7. Atalay, R., Zimmermann, A., Wagner, M., Borst, E., Benz, C., Messerle, M. & Hengel, H. ( 2002; ). Identification and expression of human cytomegalovirus transcription units coding for two distinct Fc gamma receptor homologs. J Virol 76, 8596–8608.[CrossRef]
    [Google Scholar]
  8. Barrett, J. W., Cao, J. X., Hota-Michell, S. & McFadden, G. ( 2001; ). Immunomodulatory proteins of myxoma virus. Semin Immunol 13, 73–84.[CrossRef]
    [Google Scholar]
  9. Bavari, S., Bosio, C. M., Wiegand, E. & 7 other authors ( 2002; ). Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses. J Exp Med 195, 593–602.[CrossRef]
    [Google Scholar]
  10. Benichou, G. & Voisin, G. A. ( 1987; ). Antibody bipolar bridging: isotype-dependent signals given to guinea pig alveolar macrophages by anti-MHC alloantibodies. Cell Immunol 106, 304–317.[CrossRef]
    [Google Scholar]
  11. Bergelson, J. M., Chan, M., Solomon, K. R., St John, N. F., Lin, H. & Finberg, R. W. ( 1994; ). Decay-accelerating factor (CD55), a glycosylphosphatidylinositol-anchored complement regulatory protein, is a receptor for several echoviruses. Proc Natl Acad Sci U S A 91, 6245–6249.[CrossRef]
    [Google Scholar]
  12. Betts, R. F. & Schmidt, S. G. ( 1981; ). Cytolytic IgM antibody to cytomegalovirus in primary cytomegalovirus infection in humans. J Infect Dis 143, 821–826.[CrossRef]
    [Google Scholar]
  13. Cooper, N. R., Jensen, F. C., Welsh, R. M., Jr & Oldstone, M. B. ( 1974; ). Lysis of RNA tumor viruses by human serum: direct antibody-independent triggering of the classical complement pathway. J Exp Med 144, 970–984.
    [Google Scholar]
  14. Crnkovic-Mertens, I., Messerle, M., Milotic, I., Szepan, U., Kucic, N., Krmpotic, A., Jonjic, S. & Koszinowski, U. H. ( 1998; ). Virus attenuation after deletion of the cytomegalovirus Fc receptor gene is not due to antibody control. J Virol 72, 1377–1382.
    [Google Scholar]
  15. Dorig, R. E., Marcil, A., Chopra, A. & Richardson, C. D. ( 1993; ). The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75, 295–305.[CrossRef]
    [Google Scholar]
  16. Dowler, K. W. & Veltri, R. W. ( 1984; ). In vitro neutralization of HSV-2: inhibition by binding of normal IgG and purified Fc to virion Fc receptor (FcR). J Med Virol 13, 251–259.[CrossRef]
    [Google Scholar]
  17. Dubin, G., Frank, I. & Friedman, H. M. ( 1990; ). Herpes simplex virustype 1 encodes two Fc receptors which have different binding characteristics for monomeric immunoglobulin G (IgG) and IgG complexes. J Virol 64, 2725–2731.
    [Google Scholar]
  18. Dubin, G., Socolof, E., Frank, I. & Friedman, H. M. ( 1991; ). Herpessimplex virus type 1 Fc receptor protects infected cells from antibody-dependent cellular cytotoxicity. J Virol 65, 7046–7050.
    [Google Scholar]
  19. Dubin, G., Basu, S., Mallory, D. L. P., Basu, M., Tal-Singer, R. & Friedman, H. M. ( 1994; ). Characterization of domains of herpes simplex virus type 1 glycoprotein E involved in Fc binding activity for immunoglobulin aggregates. J Virol 68, 2478–2486.
    [Google Scholar]
  20. Ebenbichler, C. F., Thielens, N. M., Vornhagen, R., Marschang, P., Arlaud, G. J. & Dierich, M. P. ( 1991; ). Human immunodeficiency virus type 1 activates the classical pathway of complement by direct C1 binding through specific sites in the transmembrane glycoprotein gp41. J Exp Med 174, 1417–1424.[CrossRef]
    [Google Scholar]
  21. Engelstad, M., Howard, S. T. & Smith, G. L. ( 1992; ). A constitutively expressed vaccinia gene encodes a 42-kDa glycoprotein related to complement control factors that forms part of the extracellular virus envelope. Virology 188, 801–810.[CrossRef]
    [Google Scholar]
  22. Favoreel, H. W., Nauwynck, H. J., Van Oostveldt, P., Mettenleiter, T. C. & Pensaert, M. B. ( 1997; ). Antibody-induced and cytoskeleton-mediated redistribution and shedding of viral glycoproteins, expressed on pseudorabies virus-infected cells. J Virol 71, 8254–8261.
    [Google Scholar]
  23. Favoreel, H. W., Nauwynck, H. J. & Pensaert, M. B. ( 1999a; ). Role of the cytoplasmic tail of gE in antibody-induced redistribution of viral glycoproteins expressed on pseudorabies virus-infected cells. Virology 259, 141–147.[CrossRef]
    [Google Scholar]
  24. Favoreel, H. W., Nauwynck, H. J., Halewyck, H. M., Van Oostveldt, P., Mettenleiter, T. C. & Pensaert, M. B. ( 1999b; ). Antibody-induced endocytosis of viral glycoproteins and major histocompatibility complex class I on pseudorabies virus-infected monocytes. J Gen Virol 80, 1283–1291.
    [Google Scholar]
  25. Favoreel, H. W., Van Minnebruggen, G., Nauwynck, H. J., Enquist, L. W. & Pensaert, M. B. ( 2002; ). A tyrosine-based motif in the cytoplasmic tail of pseudorabies virus glycoprotein B is important for both antibody-induced internalization of viral glycoproteins and efficient cell-to-cell spread. J Virol 76, 6845–6851.[CrossRef]
    [Google Scholar]
  26. Fingeroth, J. D., Weis, J. J., Tedder, T. F., Strominger, J. L., Biro, P. A. & Fearon, D. T. ( 1984; ). Epstein–Barr virus receptor of human B lymphocytes is the C3d receptor CR2. Proc Natl Acad Sci U S A 81, 4510–4514.[CrossRef]
    [Google Scholar]
  27. Fodor, W. L., Rollins, S. A., Bianco-Caron, S., Rother, R. P., Guilmette, E. R., Burton, W. V., Albrecht, J. C., Fleckenstein, B. & Squinto, S. P. ( 1995; ). The complement control protein homolog of herpesvirus saimiri regulates serum complement by inhibiting C3 convertase activity. J Virol 69, 3889–3892.
    [Google Scholar]
  28. Frank, I. & Friedman, H. M. ( 1989; ). A novel function of the herpes simplex virus type I Fc receptor: participation in bipolar bridging of antiviral immunoglobulin G. J Virol 63, 4479–4488.
    [Google Scholar]
  29. Friedman, H. M., Cohen, G. H., Eisenberg, R. J., Seidel, C. A. & Cines, D. B. ( 1984; ). Glycoprotein C of herpes simplex virus 1 acts as a receptor for the C3b complement component on infected cells. Nature 309, 633–634.[CrossRef]
    [Google Scholar]
  30. Fries, L. F., Friedman, H. M., Cohen, G. H., Eisenberg, R. J., Hammer, C. H. & Frank, M. M. ( 1986; ). Glycoprotein gC of herpes simplex virus 1 is an inhibitor of the complement cascade. J Immunol 137, 1636–1641.
    [Google Scholar]
  31. Hakozaki, Y., Yoshiba, M., Sekiyama, K. & 8 other authors ( 2002; ). Mannose-binding lectin and the prognosis of fulminant hepatic failure caused by HBV infection. Liver 22, 29–34.[CrossRef]
    [Google Scholar]
  32. Hannan, L. A. & Edidin, M. ( 1996; ). Traffic, polarity, and detergent solubility of a glycosylphosphatidylinositol-anchored protein after LDL-deprivation of MDCK cells. J Cell Biol 133, 1265–1276.[CrossRef]
    [Google Scholar]
  33. Harris, C. L., Spiller, O. B. & Morgan, B. P. ( 2000; ). Human and rodent decay-accelerating factors (CD55) are not species restricted intheir complement-inhibiting activities. Immunology 100, 462–470.[CrossRef]
    [Google Scholar]
  34. Haurum, J. S., Thiel, S., Jones, I. M., Fischer, P. B., Laursen, S. B. & Jensenius, J. C. ( 1993; ). Complement activation upon binding of mannan-binding protein to HIV envelope glycoproteins. AIDS 7, 1307–1313.[CrossRef]
    [Google Scholar]
  35. Herold, B. C., WuDunn, D., Soltys, N. & Spear, P. G. ( 1991; ). Glycoprotein C of herpes simplex virus type 1 plays a principal role in the adsorption of virus to the cells and in infectivity. J Virol 65, 1090–1098.
    [Google Scholar]
  36. Hirsch, R. L., Griffin, D. E. & Winkelstein, J. A. ( 1981; ). Host modification of Sindbis virus sialic acid content influences alternative complement pathway activation and virus clearance. J Immunol 127, 1740–1743.
    [Google Scholar]
  37. Hirsch, R. L., Griffin, D. E. & Winkelstein, J. A. ( 1983; ). Natural immunity to Sindbis virus is influenced by host tissue sialic acid content. Proc Natl Acad Sci U S A 80, 548–550.[CrossRef]
    [Google Scholar]
  38. Howard, J., Justus, D. E., Totmenin, A. V., Schelkunov, S. & Kotwal,G. J. ( 1998; ). Molecular mimicry of the inflammation modulatory proteins (IMPs) of poxviruses: evasion of the inflammatory response to preserve viral habitat. J Leukoc Biol 64, 68–71.
    [Google Scholar]
  39. Huemer, H. P., Larcher, C. & Coe, N. E. ( 1992; ). Pseudorabies virus glycoprotein III derived from virions and infected cells binds to the third component of complement. Virus Res 23, 271–280.[CrossRef]
    [Google Scholar]
  40. Huemer, H. P., Larcher, C., van Drunen Littel-van den Hurk, S. & Babiuk, L. A. ( 1993; ). Species selective interaction of Alphaherpesvirinae with the ‘unspecific’ immune system of the host. Arch Virol 130, 353–364.[CrossRef]
    [Google Scholar]
  41. Huemer, H. P., Nowotny, N., Crabb, B. S., Meyer, H. & Hubert, P. H. ( 1995; ). gp13 (EHV-gC): a complement receptor induced by equine herpesviruses. Virus Res 37, 113–126.[CrossRef]
    [Google Scholar]
  42. Hung, S. L., Srinivasan, S., Friedman, H. M., Eisenberg, R. J. & Cohen, G. H. ( 1992; ). Structural basis of C3b binding by glycoprotein C of herpes simplex virus. J Virol 66, 4013–4027.
    [Google Scholar]
  43. Hung, S. L., Peng, C., Kostavasili, I., Friedman, H. M., Lambris, J. D., Eisenberg, R. J. & Cohen, G. H. ( 1994; ). The interaction of glycoprotein C of herpes simplex virus types 1 and 2 with the alternative complement pathway. Virology 203, 299–312.[CrossRef]
    [Google Scholar]
  44. Ikeda, F., Haraguchi, Y., Jinno, A., Iino, Y., Morishita, Y., Shiraki, H. & Hoshino, H. ( 1998; ). Human complement component C1q inhibits the infectivity of cell-free HTLV-I. J Immunol 161, 5712–5719.
    [Google Scholar]
  45. Isaacs, S. N., Kotwal, G. J. & Moss, B. ( 1992; ). Vaccinia virus complement-control protein prevents antibody-dependent complement-enhanced neutralization of infectivity and contributes to virulence. Proc Natl Acad Sci U S A 89, 628–632.[CrossRef]
    [Google Scholar]
  46. Ishak, R., Andiman, W. A. & Tucker, G. ( 1984; ). Absence of IgG Fcreceptors on varicella-zoster virus-infected cells. J Med Virol 13, 261–267.[CrossRef]
    [Google Scholar]
  47. Janeway, C. A., Travers, P., Walport, M. & Shlomchik, M. ( 2001; ). Immunobiology – The Immune System in Health and Disease. NewYork: Garland Publishing.
  48. Johnson, D. C. & Feenstra, V. ( 1987; ). Identification of a novel herpesvirus simplex virus type 1-induced glycoprotein which complexes with gE and binds immunoglobulin. J Virol 61, 2208–2216.
    [Google Scholar]
  49. Johnson, D. C., Frame, M. C., Ligas, M. W., Cross, A. M. & Stow, N.D. ( 1988; ). Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI. J Virol 62, 1347–1354.
    [Google Scholar]
  50. Kapadia, S. B., Molina, H., van Berckel, V., Speck, S. H., & Virgin, H. W., IV ( 1999; ). Murine gammaherpesvirus 68 encodes a functional regulator of complement activation. J Virol 73, 7658–7670.
    [Google Scholar]
  51. Kase, T., Suzuki, Y., Kawai, T. & 7 other authors ( 1999; ). Human mannan-binding lectin inhibits the infection of influenza A virus without complement. Immunology 97, 385–392.[CrossRef]
    [Google Scholar]
  52. Kostavasili, J., Sahu, A., Friedman, H. M., Eisenberg, R. J., Cohen, G. H. & Lambris, J. D. ( 1997; ). Mechanism of complement inactivation byglycoprotein C of herpes simplex virus. J Immunol 158, 1763–1771.
    [Google Scholar]
  53. Kotwal, G. J., Isaacs, S. N., McKenzie, R., Frank, M. M. & Moss, B. ( 1990; ). Inhibition of the complement cascade by the major secretory protein of vaccinia virus. Science 250, 827–830.[CrossRef]
    [Google Scholar]
  54. Kotwal, G. J., Miller, C. G. & Justus, D. E. ( 1998; ). The inflammation protein (IMP) of cowpox virus drastically diminishes the tissue damage by down-regulating cellular infiltration resulting from complement activation. Mol Cell Biochem 185, 39–46.[CrossRef]
    [Google Scholar]
  55. Kubota, Y., Gaither, T. A., Cason, J., Oshea, J. J. & Lawley, T. J. ( 1987; ). Characterization of the C3 receptor induced by herpes simplex virus type 1 infection in human epidermal, endothelial, and A431 cells. J Immunol 138, 1137–1142.
    [Google Scholar]
  56. Lee, H. J., Essani, K. & Smith, G. L. ( 2001; ). The genome sequence of Yaba-like disease virus, a yatapoxvirus. Virology 281, 170–192.[CrossRef]
    [Google Scholar]
  57. Lilley, B. N., Ploegh, H. L. & Tirabassi, R. S. ( 2001; ). Human cytomegalovirus open reading frame TRL11/IRL11 encodes an immunoglobulin G Fc-binding protein. J Virol 75, 11218–11221.[CrossRef]
    [Google Scholar]
  58. Litwin, V. & Grose, C. ( 1992; ). Herpesviral Fc receptors and their relationship to the human Fc receptors. Immunol Res 11, 226–238.[CrossRef]
    [Google Scholar]
  59. Litwin, V., Sandor, M. & Grose, C. ( 1990; ). Cell surface expression ofthe varicella-zoster glycoproteins and Fc receptor. Virology 178, 263–272.[CrossRef]
    [Google Scholar]
  60. Litwin, V., Jackson, W. & Grose, C. ( 1992; ). Receptor properties of two varicella-zoster virus glycoproteins, gpI and gpIV, homologous to herpes simplex virus gE and gI. J Virol 66, 3643–3651.
    [Google Scholar]
  61. Lubinski, J. M., Wang, L., Soulika, A. M. & 7 other authors ( 1998; ). Herpes simplex virus type 1 glycoprotein gC mediates immune evasion in vivo. J Virol 72, 8257–8263.
    [Google Scholar]
  62. Lubinski, J. M., Wang, L., Mastellos, D., Sahu, A., Lambris, J. D. & Friedman, H. M. ( 1999; ). In vivo role of complement-interacting domains of herpes simplex virus type 1 glycoprotein gC. J Exp Med 190, 1637–1646.[CrossRef]
    [Google Scholar]
  63. Lubinski, J. M., Jiang, M., Hook, L. & 7 other authors ( 2002; ). Herpes simplex virus type 1 evades the effects of antibody and complement invivo. J Virol 76, 9232–9241.[CrossRef]
    [Google Scholar]
  64. MacCormac, L. P. & Grundy, J. P. ( 1996; ). Human cytomegalovirus induces an Fc gamma receptor (Fc gammaR) in endothelial cells and fibroblasts that is distinct from the human cellular Fc gammaRs. J Infect Dis 174, 1151–1161.[CrossRef]
    [Google Scholar]
  65. Mackowiak, P. A. & Marling-Cason, M. ( 1987; ). Immunoreactivity ofcytomegalovirus-induced Fc receptors. Microbiol Immunol 31, 427–434.[CrossRef]
    [Google Scholar]
  66. McKenzie, R., Kotwal, G. J., Moss, B., Hammer, C. H. & Frank, M. M. ( 1992; ). Regulation of complement activity by vaccinia virus complement-control protein. J Infect Dis 166, 1245–1250.[CrossRef]
    [Google Scholar]
  67. Maeda, K., Hayashi, S., Tanioka, Y., Matsumoto, Y. & Otsuka, H. ( 2002; ). Pseudorabies virus (PRV) is protected from complement attack by cellular factors and glycoprotein C (gC). Virus Res 84, 79–87.[CrossRef]
    [Google Scholar]
  68. Meri, S. & Pangburn, M. K. ( 1990; ). Discrimination between activators and nonactivators of the alternative pathway of complement: regulation via a sialic acid/polyanion binding site on factor H. Proc Natl Acad Sci U S A 87, 3982–3986.[CrossRef]
    [Google Scholar]
  69. Mettenleiter, T. C., Zsak, L., Zuckermann, F., Sugg, N., Kern, H. & Ben-Porat, T. ( 1990; ). Interaction of glycoprotein gIII with a cellular heparinlike substance mediates adsorption of pseudorabies virus. J Virol 64, 278–286.
    [Google Scholar]
  70. Middeldorp, J. M., Jongsma, J. & The, T. H. ( 1986; ). Killing of human cytomegalovirus-infected fibroblasts by antiviral antibody and complement. J Infect Dis 153, 48–55.[CrossRef]
    [Google Scholar]
  71. Mold, C., Bradt, B. M., Nemerow, G. R. & Cooper, N. R. ( 1988; ). Epstein–Barr virus regulates activation and processing of the third component of complement. J Exp Med 168, 949–969.[CrossRef]
    [Google Scholar]
  72. Nagashunmugam, T., Lubinski, J., Wang, L., Goldstein, L. T., Weeks, B. J., Sundaresan, P., Kang, E. H., Dubin, G. & Friedman, H. M. ( 1998; ). In vivo immune evasion mediated by the herpes simplex virus type 1 immunoglobulin G Fc receptor. J Virol 72, 5351–5359.
    [Google Scholar]
  73. Naniche, D., Varior-Krishnan, G., Cervoni, F., Wild, T. F., Rossi, B., Rabourdin-Combe, C. & Gerlier, D. ( 1993; ). Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J Virol 67, 6025–6032.
    [Google Scholar]
  74. Nauwynck, H. J. & Pensaert, M. B. ( 1992; ). Abortion induced by cell-associated pseudorabies virus in vaccinated sows. Am J Vet Res 53, 489–493.
    [Google Scholar]
  75. Nguyen, D. H. & Hildreth, J. E. ( 2000; ). Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J Virol 74, 3264–3272.[CrossRef]
    [Google Scholar]
  76. Ogata, M. & Shigeta, S. ( 1979; ). Appearance of immunoglobulin G Fc receptor in cultured human cells infected with varicella-zoster virus. Infect Immun 26, 770–774.
    [Google Scholar]
  77. Oleszak, E. L. ( 1994; ). Molecular mimicry between Fc receptors and viral antigens. Arch Immunol Ther Exp 42, 83–88.
    [Google Scholar]
  78. Oleszak, E. L., Perlman, S., Parr, R., Collisson, E. W. & Leibowitz, J. L. ( 1993; ). Molecular mimicry between S peplomer proteins of coronaviruses (MHV, BCV, TGEV and IBV) and Fc receptor. Adv Exp Med Biol 342, 183–188.
    [Google Scholar]
  79. Oleszak, E. L., Kuzmak, J., Hogue, B., Parr, R., Collisson, E. W., Rodkey, L. S. & Leibowitz, J. L. ( 1995; ). Molecular mimicry between Fc receptor and S peplomer protein of mouse hepatitis virus, bovine corona virus, and transmissible gastroenteritis virus. Hybridoma 14, 1–8.[CrossRef]
    [Google Scholar]
  80. Ono, A. & Freed, E. O. ( 2001; ). Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc Natl Acad Sci U S A 98, 13925–13930.[CrossRef]
    [Google Scholar]
  81. Pangburn, M. K. ( 1986; ). Immunobiology of the Complement System, pp. 45–62. Edited by G. D. Ross. New York: Academic Press.
  82. Para, M. F., Baucke, R. B. & Spear, P. G. ( 1982; ). Glycoprotein gE of herpes simplex virus type 1: effects of anti-gE on virion infectivity and on virus-induced Fc-binding receptors. J Virol 41, 129–136.
    [Google Scholar]
  83. Perez de la Lastra, J. M., Harris, C. L., Hinchliffe, S. J., Holt, D. S., Rushmere, N. K. & Morgan, B. P. ( 2000; ). Pigs express multiple forms of decay-accelerating factor (CD55), all of which contain only three short consensus repeats. J Immunol 165, 2563–2573.[CrossRef]
    [Google Scholar]
  84. Rahman, A. A., Teschner, M., Sethi, K. K. & Brandis, H. ( 1976; ). Appearance of IgG (Fc) receptor(s) on cultured human fibroblasts infected with human cytomegalovirus. J Immunol 117, 253–258.
    [Google Scholar]
  85. Reading, P. C., Morey, L. S., Crouch, E. C. & Anders, E. M. ( 1997; ). Collectin-mediated antiviral host defense of the lung: evidence from influenza virus infection of mice. J Virol 71, 8204–8212.
    [Google Scholar]
  86. Rosengard, A. M., Liu, Y., Nie, Z. & Jimenez, R. ( 2002; ). Variola virus immune evasion design: expression of a highly efficient inhibitor of human complement. Proc Natl Acad Sci U S A 99, 8808–8813.[CrossRef]
    [Google Scholar]
  87. Rother, R. P., Rollins, S. A., Fodor, W. F., Albrecht, J. C., Setter, E., Fleckenstein, B. & Squinto, S. P. ( 1994; ). Inhibition of complement-mediated cytolysis by the terminal complement inhibitor of herpesvirus saimiri. J Virol 68, 730–737.
    [Google Scholar]
  88. Rushmere, N. K., Tomlinson, S. & Morgan, B. P. ( 1997; ). Expression of rat CD59: functional analysis confirms lack of species selectivity and reveals that glycosylation is not required for function. Immunology 90, 640–646.[CrossRef]
    [Google Scholar]
  89. Rux, A. H., Lou, H., Lambris, J. D., Friedman, H. M., Eisenberg, R. J. & Cohen, G. H. ( 2002; ). Kinetic analysis of glycoprotein C of herpes simplex virus types 1 and 2 binding to heparin, heparan sulphate, and complement component C3b. Virology 294, 324–332.[CrossRef]
    [Google Scholar]
  90. Saifuddin, M., Parker, C. J., Peeples, M. E., Gorny, M. K., Zolla-Opazner, S., Ghassemi, M., Rooney, I. A., Atkinson, J. P. & Spear, G. T. ( 1995; ). Role of virion-associated glycosylphosphatidylinositol-linked proteins CD55 and CD59 in complement resistance of cell line-derived and primary isolates of HIV-1. J Exp Med 182, 501–509.[CrossRef]
    [Google Scholar]
  91. Saifuddin, M., Hedayati, T., Atkinson, J. P., Holgiun, M. H., Parker, C. J. & Spear, G. T. ( 1997; ). Human immunodeficiency virus type 1 incorporates both glycosyl phosphatidylinositol-anchored CD55 and CD59 and integral membrane CD64 at levels that protect from complement-mediated destruction. J Gen Virol 78, 1907–1911.
    [Google Scholar]
  92. Sasaki, K., Tsutsumi, A., Wakamiya, N., Ohtani, K., Suzuki, Y., Watanabe, Y., Nakayama, N. & Koike, T. ( 2000; ). Mannose-binding lectin polymorphisms in patients with hepatitis C virus infection. Scand J Gastroenterol 35, 960–965.[CrossRef]
    [Google Scholar]
  93. Scheiffele, P., Rietveld, A., Wilk, T. & Simons, K. ( 1999; ). Influenza viruses select ordered lipid domains during budding from the plasma membrane. J Biol Chem 274, 2038–2044.[CrossRef]
    [Google Scholar]
  94. Schmelz, M., Sodeik, B., Ericsson, M., Wolffe, E. J., Shida, H., Hiller, G. & Griffiths, G. ( 1994; ). Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans Golgi network. J Virol 68, 130–147.
    [Google Scholar]
  95. Schreurs, C., Mettenleiter, T. C., Zuckermann, F., Sugg, N. & Ben-Porat, T. ( 1988; ). Glycoprotein gIII of pseudorabies virus is multifunctional. J Virol 62, 2251–2257.
    [Google Scholar]
  96. Seidel-Dugan, C., Ponce de Leon, M., Friedman, H. M., Eisenberg,R. J. & Cohen, G. H. ( 1990; ). Identification of C3b-binding regions on herpes simplex virus type 2 glycoprotein C. J Virol 64, 1897–1906.
    [Google Scholar]
  97. Smiley, M. L., Hoxie, J. A. & Friedman, H. M. ( 1985; ). Herpes simplex virus type 1 infection of endothelial, epithelial and fibroblast cells induces a receptor for C3b. J Immunol 134, 2673–2678.
    [Google Scholar]
  98. Spear, G. T., Lurain, N. S., Parker, C. J., Ghassemi, M., Payne, G. H. & Saifuddin, M. ( 1995; ). Host cell-derived complement control proteins CD55 and CD59 are incorporated into the virions of twounrelated enveloped viruses. Human T cell leukemia/lymphoma virus type 1 (HTLV-1) and human cytomegalovirus (HCMV). J Immunol 155, 4376–4381.
    [Google Scholar]
  99. Spiller, O. B. & Morgan, B. P. ( 1998; ). Antibody-independent activation of the classical complement pathway by cytomegalovirus-infected fibroblasts. J Infect Dis 178, 1597–1603.[CrossRef]
    [Google Scholar]
  100. Spiller, O. B., Morgan, B. P., Tufaro, F. & Devine, D. V. ( 1996; ). Altered expression of host-encoded complement regulators on human cytomegalovirus-infected cells. Eur J Immunol 26, 1532–1538.[CrossRef]
    [Google Scholar]
  101. Stannard, L. M. & Hardie, D. R. ( 1991; ). An Fc receptor for human immunoglobulin G is located within the tegument of human cytomegalovirus. J Virol 65, 3411–3415.
    [Google Scholar]
  102. Stoiber, H., Kacani, L., Speth, C., Würzner, R. & Dierich, M. P. ( 2001; ). The supportive role of complement in HIV pathogenesis. Immunol Rev 180, 168–176.[CrossRef]
    [Google Scholar]
  103. Takahashi-Nishimaki, F., Funahashi, S., Miki, K., Hashizume, S. & Sugimoto, M. ( 1991; ). Regulation of plaque size and host range by a vaccinia virus gene related to complement system proteins. Virology 181, 158–164.[CrossRef]
    [Google Scholar]
  104. Thäle, R., Lucin, P., Schneider, K., Eggers, M. & Koszinowski, U. H. ( 1994; ). Identification and expression of a murine cytomegalovirus early gene coding for an Fc receptor. J Virol 68, 7757–7765.
    [Google Scholar]
  105. Tooze, J., Hollinshead, M., Reis, B., Radsak, K. & Kern, H. ( 1993; ). Progeny vaccinia and human cytomegalovirus particles utilize earlyendosomal cisternae for their envelopes. Eur J Cell Biol 60, 163–178.
    [Google Scholar]
  106. Van den Berg, C. W. & Morgan, B. P. ( 1994; ). Complement-inhibiting activities of human CD59 and analogues from rat, sheep, and pig are not homologously restricted. J Immunol 152, 4095–4101.
    [Google Scholar]
  107. Vanderplasschen, A., Mathew, E., Hollinshead, M., Sim, R. B. & Smith, G. L. ( 1998; ). Extracellular enveloped vaccinia virus is resistant to complement because of incorporation of host complement control proteins into its envelope. Proc Natl Acad Sci U S A 95, 7544–7549.[CrossRef]
    [Google Scholar]
  108. Van de Walle, G. R., Favoreel, H. W., Nauwynck, H. J., Van Oostveldt, P. & Pensaert, M. B. ( 2001; ). Involvement of cellular cytoskeleton components in antibody-induced internalization of viral glycoproteins in pseudorabies virus-infected monocytes. Virology 288, 129–138.[CrossRef]
    [Google Scholar]
  109. Vincent, S., Gerlier, D. & Manie, S. N. ( 2000; ). Measles virus assembly within membrane rafts. J Virol 74, 9911–9915.[CrossRef]
    [Google Scholar]
  110. Virgin, H. W., IV, Latreille, P., Wamsley, P., Hallsworth, K., Weck, K. E., Dal Canto, A. J. & Speck, S. H. ( 1997; ). Complete sequence andgenomic analysis of murine gammaherpesvirus 68. J Virol 71, 5894–5904.
    [Google Scholar]
  111. Watkins, J. F. ( 1964; ). Adsorption of sensitized sheep erythrocytes toHeLa cells infected with herpes simplex virus. Nature 202, 1364–1365.[CrossRef]
    [Google Scholar]
  112. Westmoreland, D. & Watkins, J. F. ( 1974; ). The IgG receptor induced by herpes simplex virus: studies using radioiodinated IgG. J Gen Virol 24, 167–178.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.18709-0
Loading
/content/journal/jgv/10.1099/vir.0.18709-0
Loading

Data & Media loading...

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error