Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-848d4c4894-cjp7w Total loading time: 0 Render date: 2024-07-06T21:34:16.023Z Has data issue: false hasContentIssue false

63 - Subversion of innate and adaptive immunity: immune evasion from antibody and complement

from Part V - Subversion of adaptive immunity

Published online by Cambridge University Press:  24 December 2009

By
Lauren M. Hook  and
Harvey M. Friedman
Edited by
Ann Arvin ,
Gabriella Campadelli-Fiume ,
Edward Mocarski ,
Patrick S. Moore ,
Bernard Roizman ,
Richard Whitley  and
Koichi Yamanishi
Lauren M. Hook
Affiliation:
Department of Medicine, University of Pennsylvania School of Medicine, PA, USA
Harvey M. Friedman
Affiliation:
Department of Medicine, University of Pennsylvania School of Medicine, PA, USA
Ann Arvin
Affiliation:
Stanford University, California
Gabriella Campadelli-Fiume
Affiliation:
Università degli Studi, Bologna, Italy
Edward Mocarski
Affiliation:
Emory University, Atlanta
Patrick S. Moore
Affiliation:
University of Pittsburgh
Bernard Roizman
Affiliation:
University of Chicago
Richard Whitley
Affiliation:
University of Alabama, Birmingham
Koichi Yamanishi
Affiliation:
University of Osaka, Japan
Get access

Summary

Many herpesviruses encode immune evasion molecules that interfere with activities mediated by antibody and complement, suggesting the importance of antibody and complement in host defense against herpes infections. How does this observation reconcile with the clinical findings that severe infections develop mostly in subjects with T-cell deficiencies, such as transplant recipients or those with advanced HIV infection? An explanation that we favor is that T-cells assume a pivotal role in host defense partly because herpesviruses are very effective at limiting the activities of antibody and complement. Support for this hypothesis comes from experimental studies using mutant HSV-1 strains defective in antibody and complement immune evasion that demonstrate a marked increased in effectiveness of antibody and complement in host defense against the mutant viruses (Lubinski et al., 2002).

Newborns lack mature T-cell repertoires and generally have low serum complement levels; therefore, observations in human newborns provide opportunities to assess the contributions of antibodies independent of T-cells and perhaps complement in host defense against herpesviruses. The severity of HSV and CMV infection in the fetus and newborn are greatly reduced when the infection in the mother is recurrent rather than primary. In recurrent infection, antibodies pass transplacentally to the fetus and protect against the infection. Passive transfer of VZV antibodies from mother to fetus protects the newborn from severe chickenpox when exposed days to weeks after delivery.

Type
Chapter
Information
Human Herpesviruses
Biology, Therapy, and Immunoprophylaxis
 , pp. 1137 - 1150
Publisher: Cambridge University Press
Print publication year: 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albrecht, J. C. and Fleckenstein, B. (1992). New member of the multigene family of complement control proteins in herpesvirus saimiri. J. Virol., 66(6), 3937–3940.Google ScholarPubMed
Albrecht, J. C., Nicholas, J., Biller, D.et al. (1992a). Primary structure of the herpesvirus saimiri genome. J. Virol., 66(8), 5047–5058.Google Scholar
Albrecht, J. C., Nicholas, J., Cameron, K. R., Newman, C., Fleckenstein, B., and Honess, R. W. (1992b). Herpesvirus saimiri has a gene specifying a homologue of the cellular membrane glycoprotein CD59. Virology, 190(1), 527–530.CrossRefGoogle Scholar
Antonsson, A. and Johansson, P. J. (2001). Binding of human and animal immunoglobulins to the IgG Fc receptor induced by human cytomegalovirus. J. Gen. Virol., 82(5), 1137–1145.CrossRefGoogle Scholar
Atalay, R., Zimmermann, A., Wagner, M.et al. (2002). Identification and expression of human cytomegalovirus transcription units coding for two distinct Fcgamma receptor homologs. J. Virol., 76(17), 8596–8608.CrossRefGoogle ScholarPubMed
Basu, S., Dubin, G., Basu, M., Nguyen, V., and Friedman, H. M. (1995). Characterization of regions of herpes simplex virus type 1 glycoprotein E involved in binding the Fc domain of monomeric IgG and in forming a complex with glycoprotein I. J. Immunol., 154(1), 260–267.Google ScholarPubMed
Bell, S., Cranage, M., Borysiewicz, L., and Minson, T. (1990). Induction of immunoglobulin G Fc receptors by recombinant vaccinia viruses expressing glycoproteins E and I of herpes simplex virus type 1. J. Virol., 64(5), 2181–2186.Google Scholar
Carroll, M. C. (2000). The role of complement in B cell activation and tolerance. Adv. Immunol., 74, 61–88.CrossRefGoogle Scholar
Chapman, T. L., You, I., Joseph, I. M., Bjorkman, P. J., Morrison, S. L., and Raghavan, M. (1999). Characterization of the interaction between the herpes simplex virus type I Fc receptor and immunoglobulin G. J. Biol. Chem., 274(11), 6911–6919.CrossRefGoogle ScholarPubMed
Crnkovic-Mertens, I., Messerle, M., Milotic, I.et al. (1998). Virus attenuation after deletion of the cytomegalovirus Fc receptor gene is not due to antibody control. J. Virol., 72(2), 1377–1382.Google Scholar
Da Costa, X. J., Brockman, M. A., Alicot, E.et al. (1999). Humoral response to herpes simplex virus is complement-dependent. Proc. Natl Acad. Sci. USA, 96(22), 12708–12712.CrossRefGoogle ScholarPubMed
Dubin, G., Frank, I., and Friedman, H. M. (1990). Herpes simplex virus type 1 encodes two Fc receptors which have different binding characteristics for monomeric immunoglobulin G (IgG) and IgG complexes. J. Virol., 64(6), 2725–2731.Google ScholarPubMed
Dubin, G., Socolof, E., Frank, I., and Friedman, H. M. (1991). Herpes simplex virus type 1 Fc receptor protects infected cells from antibody-dependent cellular cytotoxicity. J. Virol., 65(12), 7046–7050.Google ScholarPubMed
Dubin, G., Basu, S., Mallory, D. L., Basu, M., Tal-Singer, R., and Friedman, H. M. (1994). Characterization of domains of herpes simplex virus type 1 glycoprotein E involved in Fc binding activity for immunoglobulin G aggregates. J. Virol., 68(4), 2478–2485.Google ScholarPubMed
Edson, C. M., Hosler, B. A., and Waters, D. J. (1987). Varicella-zoster virus gpI and herpes simplex virus gE: phosphorylation and Fc binding. Virology, 161(2), 599–602.CrossRefGoogle ScholarPubMed
Eisenberg, R. J., Ponce de Leon, M., Friedman, H. M.et al. (1987). Complement component C3b binds directly to purified glycoprotein C of herpes simplex virus types 1 and 2. Microb. Path., 3(6), 423–435.CrossRefGoogle ScholarPubMed
Favoreel, H. W., Nauwynck, H. J., Oostveldt, P., Mettenleiter, T. C., and Pensaert, M. B. (1997). Antibody-induced and cytoskeleton-mediated redistribution and shedding of viral glycoproteins, expressed on pseudorabies virus-infected cells. J. Virol., 71(11), 8254–8261.Google ScholarPubMed
Favoreel, H. W., Nauwynck, H. J., and Pensaert, M. B. (1999). Role of the cytoplasmic tail of gE in antibody-induced redistribution of viral glycoproteins expressed on pseudorabies-virus-infected cells. Virology, 259(1), 141–147.CrossRefGoogle ScholarPubMed
Favoreel, H. W., Nauwynck, H. J., Halewyck, H. M., Oostveldt, P., Mettenleiter, T. C., and Pensaert, M. B. (2003). Antibody-induced endocytosis of viral glycoproteins and major histocompatibility complex class I on pseudorabies virus-infected monocytes. J. Gen. Virol., 80(5), 1283–1291.CrossRefGoogle Scholar
Fodor, W. L., Rollins, S. A., Bianco-Caron, S.et al. (1995). The complement control protein homolog of herpesvirus saimiri regulates serum complement by inhibiting C3 convertase activity. J. Virol., 69(6), 3889–3892.Google ScholarPubMed
Frank, I. and Friedman, H. M. (1989). A novel function of the herpes simplex virus type 1 Fc receptor: participation in bipolar bridging of antiviral immunoglobulin G. J. Virol., 63(11), 4479–4488.Google ScholarPubMed
Friedman, H. M. (1986). Laboratory diagnosis of herpes viruses in the immunocompromised host. Adv. Exp. Med. Biol., 202, 83–93.CrossRefGoogle ScholarPubMed
Friedman, H. M., Cohen, G. H., Eisenberg, R. J., Seidel, C. A., and 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(5969), 633–635.CrossRefGoogle ScholarPubMed
Friedman, H. M., Wang, L., Fishman, N. O.et al. (1996). Immune evasion properties of herpes simplex virus type 1 glycoprotein gC. J. Virol., 70(7), 4253–4260.Google ScholarPubMed
Friedman, H. M., Wang, L., Pangburn, M. K., Lambris, J. D., and Lubinski, J. (2000). Novel mechanism of antibody-independent complement neutralization of herpes simplex virus type 1. J. Immunol., 165(8), 4528–4536.CrossRefGoogle ScholarPubMed
Fries, L. F., Friedman, H. M., Cohen, G. H., Eisenberg, R. J., Hammer, C. H., and Frank, M. M. (1986). Glycoprotein C of herpes simplex virus 1 is an inhibitor of the complement cascade. J. Immunol., 137(5), 1636–1641.Google ScholarPubMed
Gerber, S. I., Belval, B. J., and Herold, B. C. (1995). Differences in the role of glycoprotein C of HSV-1 and HSV-2 in viral binding may contribute to serotype differences in cell tropism. Virology, 214(1), 29–39.CrossRefGoogle ScholarPubMed
Ghirlando, R., Keown, M. B., Mackay, G. A., Lewis, M. S., Unkeless, J. C., and Gould, H. J. (1995). Stoichiometry and thermodynamics of the interaction between the Fc fragment of human IgG1 and its low-affinity receptor Fc gamma RIII. Biochemistry, 34(41), 13320–13327.CrossRefGoogle ScholarPubMed
Harris, S. L., Frank, I., Yee, A., Cohen, G. H., Eisenberg, R. J., and Friedman, H. M. (1990). Glycoprotein C of herpes simplex virus type 1 prevents complement-mediated cell lysis and virus neutralization. J. Infect. Dis., 162(2), 331–337.CrossRefGoogle ScholarPubMed
Hung, S. L., Srinivasan, S., Friedman, H. M., Eisenberg, R. J., and Cohen, G. H. (1992). Structural basis of C3b binding by glycoprotein C of herpes simplex virus. J. Virol., 66(7), 4013–4027.Google ScholarPubMed
Hung, S. L., Peng, C., Kostavasili, I.et al. (1994). The interaction of glycoprotein C of herpes simplex virus types 1 and 2 with the alternative complement pathway. Virology, 203(2), 299–312.CrossRefGoogle ScholarPubMed
Johansson, P. J. and Blomberg, J. (1990). Characterization of herpes simplex virus type 1-induced Fc receptor in its interaction with rabbit immunoglobulin G (IgG). Apmis, 98(8), 685–694.CrossRefGoogle Scholar
Johansson, P. J., Hallberg, T., Oxelius, V. A., Grubb, A., and Blomberg, J. (1984). Human immunoglobulin class and subclass specificity of Fc receptors induced by herpes simplex virus type 1. J. Virol., 50(3), 796–804.Google ScholarPubMed
Johansson, P. J., Myhre, E. B., and Blomberg, J. (1985). Specificity of Fc receptors induced by herpes simplex virus type 1: comparison of immunoglobulin G from different animal species. J. Virol., 56(2), 489–494.Google ScholarPubMed
Johansson, P. J. H., Nardells, F. A., Sjoquist, J., Schroder, A. K., and Christensen, P. (1989). Herpes simplex type 1-induced Fc receptor binds to the Cgamma2-Cgamma3 interface region of IgG in the area that binds staphylococcal protein A. Immunology, 66, 8–13.Google ScholarPubMed
Johnson, D. C., Frame, M. C., Ligas, M. W., Cross, A. M., and 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(4), 1347–1354.Google ScholarPubMed
Kang, Y-S., Do, Y., Lee, H-K.et al. (2006). A dominant complement fixation pathway for pneumococcal polysaccharides initiated by SIGN-R1 interacting with C1q. Cell, 125(1); 46–58.CrossRefGoogle ScholarPubMed
Kapadia, S. B., Levine, B., Speck, S. H., and Virgin, H. W. T. (2002). Critical role of complement and viral evasion of complement in acute, persistent, and latent gamma-herpesvirus infection. Immunity, 17(2), 143–155.CrossRefGoogle ScholarPubMed
Kapadia, S. B., Molina, H., Berkel, V., Speck, S. H., and Virgin, H. W. T. (1999). Murine gammaherpesvirus 68 encodes a functional regulator of complement activation. J. Virol., 73(9), 7658–7670.Google ScholarPubMed
Klupp, B. G., Hengartner, C. J., Mettenleiter, T. C., and Enquist, L. W. (2004). Complete, annotated sequence of the pseudorabies virus genome.[erratum appears in J. Virol. 2004 Feb; 78(4):2166]. J. Virol., 78(1), 424–440.
Kostavasili, I., Sahu, A., Friedman, H. M., Eisenberg, R. J., Cohen, G. H., and Lambris, J. D. (1997). Mechanism of complement inactivation by glycoprotein C of herpes simplex virus. J. Immunol., 158(4), 1763–1771.Google ScholarPubMed
Lilley, B. N., Ploegh, H. L., and Tirabassi, R. S. (2001). Human cytomegalovirus open reading frame TRL11/IRL11 encodes an immunoglobulin G Fc-binding protein. J. Virol., 75(22), 11218–11221.CrossRefGoogle ScholarPubMed
Lin, X., Lubinski, J. M., and Friedman, H. M. (2004). Immunization strategies to block the herpes simplex virus type 1 immunoglobulin G Fc receptor. J. Virol., 78(5), 2562–2571.CrossRefGoogle ScholarPubMed
Litwin, V., Jackson, W., and 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(6), 3643–3651.Google ScholarPubMed
Lubinski, J., Wang, L., Mastellos, D., Sahu, A., Lambris, J. D., and Friedman, H. M. (1999). In vivo role of complement-interacting domains of herpes simplex virus type 1 glycoprotein gC. J. Exp. Med., 190(11), 1637–1646.CrossRefGoogle ScholarPubMed
Lubinski, J. M., Jiang, M., Hook, L.et al. (2002). Herpes simplex virus type 1 evades the effects of antibody and complement in vivo. J. Virol., 76(18), 9232–9241.CrossRefGoogle ScholarPubMed
Maeda, K., Hayashi, S., Tanioka, Y., Matsumoto, Y., and Otsuka, H. (2002). Pseudorabies virus (PRV) is protected from complement attack by cellular factors and glycoprotein C (gC). Virus Res., 84(1–2), 79–87.CrossRefGoogle Scholar
Miletic, V. D. and Frank, M. M. (1995). Complement-immunoglobulin interactions. Curr. Opin. Immunol., 7(1), 41–47.CrossRefGoogle ScholarPubMed
Mold, C., Bradt, B. M., Nemerow, G. R., and Cooper, N. R. (1988). Epstein-Barr virus regulates activation and processing of the third component of complement. J. Exp. Med., 168(3), 949–969.CrossRefGoogle Scholar
Mullick, J., Bernet, J., Singh, A. K., Lambris, J. D., and Sahu, A. (2003). Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) open reading frame 4 protein (kaposica) is a functional homolog of complement control proteins. J. Virol., 77(6), 3878–3881.CrossRefGoogle ScholarPubMed
Nagashunmugam, T., Lubinski, J., Wang, L.et al. (1998). In vivo immune evasion mediated by the herpes simplex virus type 1 immunoglobulin G Fc receptor. J. Virol., 72(7), 5351–5359.Google ScholarPubMed
Neipel, F., Albrecht, J. C., and Fleckenstein, B. (1997). Cell-homologous genes in the Kaposi's sarcoma-associated rhadinovirus human herpesvirus 8: determinants of its pathogenicity?J. Virol., 71(6), 4187–4192.Google ScholarPubMed
Olson, J. K. and Grose, C. (1997). Endocytosis and recycling of varicella-zoster virus Fc receptor glycoprotein gE: internalization mediated by a YXXL motif in the cytoplasmic tail. J. Virol., 71(5), 4042–4054.Google ScholarPubMed
Raghavan, M. and Bjorkman, P. J. (1996). Fc receptors and their interactions with immunoglobulins. Ann. Rev. Cell Dev. Biol., 12, 181–220.CrossRefGoogle ScholarPubMed
Ravetch, J. V. and Bolland, S. (2001). IgG Fc receptors. Ann. Rev. Immunol., 19, 275–290.CrossRefGoogle ScholarPubMed
Rizvi, S. M. and Raghavan, M. (2001). An N-terminal domain of herpes simplex virus type Ig E is capable of forming stable complexes with gI. J. Virol., 75(23), 11897–11901.CrossRefGoogle Scholar
Rizvi, S. M. and Raghavan, M. (2003). Responses of herpes simplex virus type 1-infected cells to the presence of extracellular antibodies: gE-dependent glycoprotein capping and enhancement in cell-to-cell spread. J. Virol., 77(1), 701–708.CrossRefGoogle ScholarPubMed
Rother, R. P., Rollins, S. A., Fodor, W. L.et al. (1994). Inhibition of complement-mediated cytolysis by the terminal complement inhibitor of herpesvirus saimiri. J. Virology, 68(2), 730–737.Google ScholarPubMed
Russo, J. J., Bohenzky, R. A., Chien, M. C.et al. (1996). Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc. Natl. Acad. Sci. USA, 93(25), 14862–14867.CrossRefGoogle Scholar
Rux, A. H., Moore, W. T., Lambris, J. D.et al. (1996). Disulfide bond structure determination and biochemical analysis of glycoprotein C from herpes simplex virus. J. Virol., 70(8), 5455–5465.Google ScholarPubMed
Rux, A. H., Lou, H., Lambris, J. D., Friedman, H. M., Eisenberg, R. J., and Cohen, G. H. (2002). Kinetic analysis of glycoprotein C of herpes simplex virus types 1 and 2 binding to heparin, heparan sulfate, and complement component C3b. Virology, 294(2), 324–332.CrossRefGoogle ScholarPubMed
Seidel-Dugan, C., Ponce de Leon, M., Friedman, H. M., Eisenberg, R. J., and Cohen, G. H. (1990). Identification of C3b-binding regions on herpes simplex virus type 2 glycoprotein C. J. Virol., 64(5), 1897–1906.Google ScholarPubMed
Smiley, M. L. and Friedman, H. M. (1985). Binding of complement component C3b to glycoprotein C is modulated by sialic acid on herpes simplex virus type 1-infected cells. J. Virol., 55(3), 857–861.Google ScholarPubMed
Sondermann, P., Huber, R., Oosthuizen, V., and Jacob, U. (2000). The 3.2-A crystal structure of the human IgG1 Fc fragment-Fc gammaRIII complex. Nature, 406(6793), 267–273.CrossRefGoogle ScholarPubMed
Spear, G. T., Lurain, N. S., Parker, C. J., Ghassemi, M., Payne, G. H., and Saifuddin, M. (1995). Host cell-derived complement control proteins CD55 and CD59 are incorporated into the virions of two unrelated enveloped viruses. Human T cell leukemia/lymphoma virus type I (HTLV-I) and human cytomegalovirus (HCMV). J. Immunol., 155(9), 4376–4381.Google Scholar
Spiller, O. B., Morgan, B. P., Tufaro, F., and Devine, D. V. (1996). Altered expression of host-encoded complement regulators on human cytomegalovirus-infected cells. Eur. J. Immunol., 26(7), 1532–1538.CrossRefGoogle ScholarPubMed
Spiller, O. B., Hanna, S. M., Devine, D. V., and Tufaro, F. (1997). Neutralization of cytomegalovirus virions: the role of complement. J. Infect. Dis., 176(2), 339–347.CrossRefGoogle Scholar
Spiller, O. B., Blackbourn, D. J., Mark, L., Proctor, D. G., and Blom, A. M. (2003a). Functional activity of the complement regulator encoded by Kaposi's sarcoma-associated herpesvirus. J. Biol. Chem., 278(11), 9283–9289.CrossRefGoogle Scholar
Spiller, O. B., Robinson, M., and O'Donnell, E. (2003b). Complement regulation by Kaposi's sarcoma-associated herpesvirus ORF4 protein. J. Virol., 77(1), 592–599.CrossRefGoogle Scholar
Sprague, E. R., Martin, W. L., and Bjorkman, P. J. (2004). pH dependence and stoichiometry of binding to the Fc region of IgG by the herpes simplex virus Fc receptor gE-gI. J. Biol. Chem., 279(14), 14184–14193.CrossRefGoogle ScholarPubMed
Sprague, E. R., Wang, C., Baker, D., and Bjorkman, P. J. (2006). Crystal structure of the HSV-1 Fc receptor bound to Fc reveals a mechanism for antibody bipolar bridging. PloS. Biol., 4(6); e148. DOI: 10.1371/journal. pbio.0040148.CrossRefGoogle ScholarPubMed
Tal-Singer, R., Seidel-Dugan, C., Fries, L.et al. (1991). Herpes simplex virus glycoprotein C is a receptor for complement component iC3b. J. Infect. Dis., 164(4), 750–753.CrossRefGoogle ScholarPubMed
Thale, R., Lucin, P., Schneider, K., Eggers, M., and Koszinowski, U. H. (1994). Identification and expression of a murine cytomegalovirus early gene coding for an Fc receptor. J. Virol., 68(12), 7757–7765.Google ScholarPubMed
Walle, G. R., Favoreel, H. W., Nauwynck, H. J., and Pensaert, M. B. (2003). Antibody-induced internalization of viral glycoproteins and gE-gI Fc receptor activity protect pseudorabies virus-infected monocytes from efficient complement-mediated lysis. J. Gen. Virol., 84(4), 939–947.CrossRefGoogle ScholarPubMed
Virgin, H. W. T., Latreille, P., Wamsley, P.et al. (1997). Complete sequence and genomic analysis of murine gammaherpesvirus 68. J. Virol., 71(8), 5894–5904.Google ScholarPubMed
Zheng, Y., Shopes, B., Holowka, D., and Baird, B. (1992). Dynamic conformations compared for IgE and IgG1 in solution and bound to receptors. Biochemistry, 31(33), 7446–7456.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×