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-77c89778f8-m42fx Total loading time: 0 Render date: 2024-07-18T19:30:53.900Z Has data issue: false hasContentIssue false

62 - Herpesvirus evasion of T-cell immunity

from Part V - Subversion of adaptive immunity

Published online by Cambridge University Press:  24 December 2009

By
Benjamin E. Gewurz ,
Jatin M. Vyas  and
Hidde L. Ploegh
Edited by
Ann Arvin ,
Gabriella Campadelli-Fiume ,
Edward Mocarski ,
Patrick S. Moore ,
Bernard Roizman ,
Richard Whitley  and
Koichi Yamanishi
Benjamin E. Gewurz
Affiliation:
Department of Pathology, Harvard Medical School, Boston, MA, USA
Jatin M. Vyas
Affiliation:
Division of Infectious Disease, Department of Medicine, Massachusetts General Hospital, Boston, MA, USA
Hidde L. Ploegh
Affiliation:
Department of Pathology, Harvard Medical School, Boston, MA, 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

The multiple layers of the human immune response present a challenge to viruses, which must survive and multiply within a host for a sufficient period of time to allow successful transmission to susceptible individuals. Given the large proteomes and comparatively low polymerase error rate of human herpesviruses, antiviral immunity at first glance appear to have the upper hand. Nonetheless, herpesviruses manage prolonged incubation periods following initial infection, with systemic dissemination and prolonged secretion, often from multiple sites. In contrast to the similarly large poxviruses, the ability to subsequently establish persistent infection is a hallmark of the human herpesviruses. To enable this lifestyle, the herpesviruses devote a significant proportion of their genome coding capacity to the expression of immuno-evasins, a collection of molecules that disrupt normal immune physiology. Each human herpesvirus studied has evolved elegant cell biological solutions to problems posed by the immune response.

Innate immunity, an evolutionarily conserved and relatively non-specific system of pattern recognition molecules hardwired in the genome, cytokines such as interferons, phagocytes and natural killer (NK) cells, represents the first line deployed against microbial invaders, including herpesviruses (Janeway and Medzhitov, 2002). The clonal expansion of B- and T- lymphocytes that bear antigen-specific receptors for viral epitopes underlies the adaptive antiviral immune response, laying the groundwork for a highly pathogen-specific defense. Such specificity comes at a price – lymphocyte proliferation requires time to unfold, and innate immunity, in particular NK-cell activity, limits the initial herpesvirus spread.

Type
Chapter
Information
Human Herpesviruses
Biology, Therapy, and Immunoprophylaxis
 , pp. 1117 - 1136
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

Abendroth, A. and Arvin, A. M. (2001). Immune evasion as a pathogenic mechanism of varicella zoster virus. Semin. Immunol., 13(1), 27–39.CrossRefGoogle ScholarPubMed
Abendroth, A., Lin, I., Slobedman, B.et al. (2001a). Varicella-zoster virus retains major histocompatibility complex class II proteins in the Golgi compartment of infected cells. J. Virol., 75(10), 4878–4888.CrossRefGoogle Scholar
Abendroth, A., Morrow, G., Cunningham, A. L.et al. (2001b). Varicella-zoster virus infection of human dendritic cells and transmission to T cells: implications for virus dissemination in the host. J. Virol., 75(13), 6183–6192.CrossRefGoogle Scholar
Abenes, G., Lee, M., Haghjoo, E.et al. (2001). Murine cytomegalovirus open reading frame M27 plays an important role in growth and virulence in mice. J. Virol., 75(4), 1697–1707.CrossRefGoogle ScholarPubMed
Ahn, K., Gruhler, A., Galocha, B.et al. (1997). The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity, 6(5), 613–621.CrossRefGoogle ScholarPubMed
Aisenbrey, C., Sizun, C., Koch, J.et al. (2006). Structure and dynamics of membrane-associated ICP47, a viral inhibitor of the MHC I antigen processing machinery. J. Biol. Chem. Epub.CrossRefGoogle ScholarPubMed
Andrews, D. M., Andoniou, C. E., Granucci, F.et al. (2001). Infection of dendritic cells by murine cytomegalovirus induces functional paralysis. Nat. Immunol., 2(11), 1077–1084.CrossRefGoogle ScholarPubMed
Arase, H., Mocarski, E. S., Campbell, A. E.et al. (2002). Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science, 296(5571), 1323–1326.CrossRefGoogle ScholarPubMed
Arrode, G., Boccaccio, C., Abasrado, J. P.et al. (2002). Cross-presentation of human cytomegalovirus pp65 (UL83) to CD8+ T cells is regulated by virus-induced, soluble-mediator-dependent maturation of dendritic cells. J. Virol., 76(1), 142–150.CrossRefGoogle ScholarPubMed
Barcy, S. and Corey, L. (2001). Herpes simplex inhibits the capacity of lymphoblastoid B cell lines to stimulate CD4+ T cells. J. Immunol., 166(10), 6242–6249.CrossRefGoogle ScholarPubMed
Barel, M. T., Ressing, M., Pizzato, N.et al. (2003). Human cytomegalovirus-encoded US2 differentially affects surface expression of class II MHC locus products and targets membrane-bound, but not soluble HLA-G1 for degradation. J. Immunol., 171(12), 6757–6765.CrossRefGoogle Scholar
Bartee, E., Mansouri, M., Nerenburg, Hovey B. T.et al. (2004). Downregulation of major histocompatibility complex class II by human ubiquitin ligases related to viral immune evasion proteins. J. Virol., 78(3), 1109–1120.CrossRefGoogle Scholar
Beck, S. and Barrell, B. (1991). An HCMV reading frame which has similarity with both the V and C regions of the TCR gamma chain. DNA Seq, 2(1), 33–38.CrossRefGoogle Scholar
Bennett, E. M., Bennink, J. R., Yewdell, J. W.et al. (1999). Cutting edge: adenovirus E19 has two mechanisms for affecting class II MHC expression. J. Immunol., 162(9), 5049–5052.Google Scholar
Berger, C., Xuereb, S., Johnson, D. C.et al. (2000). Expression of herpes simplex virus ICP47 and human cytomegalovirus US11 prevents recognition of transgene products by CD8(+) cytotoxic T lymphocytes. J. Virol., 74(10), 4465–4473.CrossRefGoogle ScholarPubMed
Biron, C. A., Byron, K. S., and Sullivan, J. L. (1989). Severe herpesvirus infections in an adolescent without natural killer cells. N. Engl. J. Med., 320(26), 1731–1735.CrossRefGoogle Scholar
Bjorkman, P. J., Saper, M. A., Samraoni, B.et al. (1987). Structure of the human class II histocompatibility antigen, HLA-A2. Nature, 329(6139), 506–512.CrossRefGoogle Scholar
Blake, N., Lee, S., Redchenko, I.et al. (1997). Human CD8+ T cell responses to EBV EBNA1: HLA class II presentation of the (Gly-Ala)-containing protein requires exogenous processing. Immunity, 7(6), 791–802.CrossRefGoogle Scholar
Blom, D., Hirsch, C., Stern, P.et al. (2004). A glycosylated type I membrane protein becomes cytosolic when peptide: N-glycanase is compromised. EMBO. J., 23(3), 650–658.CrossRefGoogle ScholarPubMed
Borriello, F., Sethna, M. P., Boyd, S. D.et al. (1997). B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity, 6(3), 303–313.CrossRefGoogle ScholarPubMed
Boss, J. M. (1997). Regulation of transcription of class II MHC genes. Curr. Opin. Immunol., 9(1), 107–113.CrossRefGoogle Scholar
Britt, W. J. and Mach, M. (1996). Human cytomegalovirus glycoproteins. Intervirology, 39(5–6), 401–412.CrossRefGoogle ScholarPubMed
Brown, M. G., Driscoll, J., and Monaco, J. J. (1991). Structural and serological similarity of MHC-linked LMP and proteasome (multicatalytic proteinase) complexes. Nature, 353(6342), 355–357.CrossRefGoogle ScholarPubMed
Bubic, I., Wagner, M., Krmpotic, A.et al. (2004). Gain of virulence caused by loss of a gene in murine cytomegalovirus. J. Virol., 78(14), 7536–7544.CrossRefGoogle ScholarPubMed
Cadwell, K. and Coscoy, L. (2005). Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science, 309(5731), 127–130.CrossRefGoogle ScholarPubMed
Cebulla, C. M., Miller, D. M., Zhang, Y.et al. (2002). Human cytomegalovirus disrupts constitutive class II MHC expression. J. Immunol., 169(1), 167–176.CrossRefGoogle Scholar
Chevalier, M. S. and Johnson, D. C. (2003). Human cytomegalovirus US3 chimeras containing US2 cytosolic residues acquire major histocompatibility class II and II protein degradation properties. J. Virol., 77(8), 4731–4738.CrossRefGoogle ScholarPubMed
Cho, N. H., Feng, P., Lee, S. H.et al. (2004a). Inhibition of T cell receptor signal transduction by tyrosine kinase-interacting protein of Herpesvirus saimiri. J. Exp. Med., 200(5), 681–687.CrossRefGoogle Scholar
Cho, N. H., Wingston, D., Chang, N.et al. (2004b). Association of herpesvirus Saimiri Tip is essential for downregulation of T-cell receptor and CD4 coreceptor. J. Urol., 80(1), 108–118.Google Scholar
Coscoy, L. and Ganem, D. (2003). PHD domains and E3 ubiquitin ligases: viruses make the connection. Trends Cell Biol., 13(1), 7–12.CrossRefGoogle ScholarPubMed
Coscoy, L., Sanchez, D. J., and Ganem, D. (2001). A novel class of herpesvirus-encoded membrane-bound E3 ubiquitin ligases regulates endocytosis of proteins involved in immune recognition. J. Cell. Biol., 155(7), 1265–1273.CrossRefGoogle ScholarPubMed
Cresswell, P. (2000). Intracellular surveillance: controlling the assembly of MHC class I-peptide complexes. Traffic, 1(4), 301–305.CrossRefGoogle ScholarPubMed
Crew, M. D. and Phanavanh, B. (2003). Exploiting virus stealth technology for xenotransplantation: reduced human T cell responses to porcine cells expressing herpes simplex virus ICP47. Xenotransplantation, 10(1), 50–59.CrossRefGoogle Scholar
Dantuma, N. P., Sharipo, A., and Masucci, M. G. (2002). Avoiding proteasomal processing: the case of EBNA1. Curr. Top. Microbiol. Immunol., 269, 23–36.Google ScholarPubMed
Campos-Lima, P. O., Gavioli, R., Zhang, Q. J.et al. (1993). HLA-A11 epitope loss isolates of Epstein–Barr virus from a highly A11+ population. Science, 260(5104), 98–100.CrossRefGoogle ScholarPubMed
Denzin, L. K. and Cresswell, P. (1995). HLA-DM induces CLIP dissociation from class II MHC alpha beta dimers and facilitates peptide loading. Cell, 82(1), 155–165.CrossRefGoogle ScholarPubMed
Dodd, R. B., Allen, M. D., Brown, S. E. et al. (2004). Solution structure of the kaposi's sarcoma-associated herpesvirus K3 N-terminal domain reveals a novel E2-binding C4HC3-type RING domain. J. Biol. Chem.CrossRef
Fiebiger, E., Story, C., Ploegh, H. L.et al. (2002). Visualization of the ER-to-cytosol dislocation reaction of a type I membrane protein. EMBO. J., 21(5), 1041–1053.CrossRefGoogle ScholarPubMed
Flierman, D., Ye, Y., Dai, M.et al. (2003). Polyubiquitin serves as a recognition signal, rather than a ratcheting molecule, during retrotranslocation of proteins across the endoplasmic reticulum membrane. J. Biol. Chem., 278(37), 34774–34782.CrossRefGoogle ScholarPubMed
Flierman, D., Coleman, C. S., Pickart, C. M.et al. (2006). E2-25K mediates US11-triggered retro-translocation of class II MHC heavy chains in a permeabilized cell system. Proc Natl Acad Sci, 103(31), 11589–11594.CrossRefGoogle Scholar
Freemont, P. S. (2000). RING for destruction?Curr. Biol., 10(2), R84–R87.CrossRefGoogle ScholarPubMed
Fruh, K., Bartee, E., Gouveia, K.et al. (2002). Immune evasion by a novel family of viral PHD/LAP-finger proteins of gamma-2 herpesviruses and poxviruses. Virus Res., 88(1–2), 55–69.CrossRefGoogle ScholarPubMed
Furman, M. H., Ploegh, H. L., and Schust, D. J. (2000). Can viruses help us to understand and classify the class II MHC molecules at the maternal-fetal interface?Hum. Immunol., 61(11), 1169–1176.CrossRefGoogle Scholar
Furman, M. H., Ploegh, H. L., and Tortorella, D. (2002). Membrane-specific, host-derived factors are required for US2- and US11-mediated degradation of major histocompatibility complex class II molecules. J. Biol. Chem., 277(5), 3258–3267.CrossRefGoogle Scholar
Furman, M. H., Loureiro, J., Ploegh, H. L.et al. (2003). Ubiquitinylation of the cytosolic domain of a type I membrane protein is not required to initiate its dislocation from the endoplasmic reticulum. J. Biol. Chem., 278(37), 34804–34811.CrossRefGoogle Scholar
Galocha, B., Hill, A., Barnett, B. C.et al. (1997). The active site of ICP47, a herpes simplex virus-encoded inhibitor of the major histocompatibility complex (MHC)-encoded peptide transporter associated with antigen processing (TAP), maps to the NH2-terminal 35 residues. J. Exp. Med., 185(9), 1565–1572.CrossRefGoogle Scholar
Gewurz, B. E., Gaudet, R., Tortorella, D.et al. (2001a). Antigen presentation subverted: Structure of the human cytomegalovirus protein US2 bound to the class II molecule HLA-A2. Proc. Natl Acad. Sci. USA, 98(12), 6794–6799.CrossRefGoogle Scholar
Gewurz, B. E., Wang, E. W., Tortorella, D.et al. (2001b). Human cytomegalovirus US2 endoplasmic reticulum-lumenal domain dictates association with major histocompatibility complex class II in a locus-specific manner. J. Virol., 75(11), 5197–5204.CrossRefGoogle Scholar
Gilbert, M. J., Riddell, S. R., Plachter, B.et al. (1996). Cytomegalovirus selectively blocks antigen processing and presentation of its immediate-early gene product. Nature, 383(6602), 720–722.CrossRefGoogle ScholarPubMed
Goldsmith, K., Chen, W., Johnson, D. C.et al. (1998). Infected cell protein (ICP)47 enhances herpes simplex virus neurovirulence by blocking the CD8+ T cell response. J. Exp. Med., 187(3), 341–348.CrossRefGoogle ScholarPubMed
Goto, E., Ishido, S., Ohgimoto, S.et al. (2003). c-MIR, a human E3 ubiquitin ligase, is a functional homolog of herpesvirus proteins MIR1 and MIR2 and has similar activity. J. Biol. Chem., 278(17), 14657–14668.CrossRefGoogle ScholarPubMed
Hamman, B. D., Chen, J. C., Johnson, E. E.et al. (1997). The aqueous pore through the translocon has a diameter of 40–60 A during cotranslational protein translocation at the ER membrane. Cell, 89(4), 535–544.CrossRefGoogle Scholar
Hassink, G. C., Barel, M. T., Van Voorden, S. B. et al. (2006). Ubiquitination of class II MHC heavy chains is essential for dislocation by human cytomegalovirus-encoded US2 but not US11. J. Biol Chem. July, 2006 (in press, epublication)
Heemels, M. T. and Ploegh, H. (1995). Generation, translocation, and presentation of MHC class I-restricted peptides. Annu. Rev. Biochem., 64, 463–491.CrossRefGoogle ScholarPubMed
Heise, M. T., Connick, M., and Virgin, H. W. 4th (1998). Murine cytomegalovirus inhibits interferon gamma-induced antigen presentation to CD4 T cells by macrophages via regulation of expression of major histocompatibility complex class II-associated genes. J. Exp. Med., 187(7), 1037–1046.CrossRefGoogle ScholarPubMed
Hengel, H., Reusch, U., Geginat, G.et al. (2000). Macrophages escape inhibition of major histocompatibility complex class I-dependent antigen presentation by cytomegalovirus. J. Virol., 74(17), 7861–7868.CrossRefGoogle ScholarPubMed
Hertel, L., Lacaille, V. G., Strobl, H.et al. (2003). Susceptibility of immature and mature Langerhans cell-type dendritic cells to infection and immunomodulation by human cytomegalovirus. J. Virol., 77(13), 7563–7574.CrossRefGoogle ScholarPubMed
Hewitt, E. W., Gupta, S. S., Mufti, D.et al. (2001). The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J., 20(3), 387–396.CrossRefGoogle ScholarPubMed
Hewitt, E. W., Duncan, L., Mufti, D.et al. (2002). Ubiquitylation of class II MHC by the K3 viral protein signals internalization and TSG101-dependent degradation. EMBO J., 21(10), 2418–2429.CrossRefGoogle Scholar
Hicke, L. (2001). A new ticket for entry into budding vesicles-ubiquitin. Cell, 106(5), 527–530.CrossRefGoogle ScholarPubMed
Hill, A., Jugovic, P.et al. (1995). Herpes simplex virus turns off the TAP to evade host immunity. Nature, 375(6530), 411–415.CrossRefGoogle ScholarPubMed
Holtappels, R., Podlech, J., York, I.et al. (2004). Cytomegalovirus misleads its host by priming of CD8 T cells specific for an epitope not presented in infected tissues. J. Exp. Med., 199(1), 131–136.CrossRefGoogle Scholar
Hudson, A. W., Howley, P. M., and Ploegh, H. L. (2001). A human herpesvirus 7 glycoprotein, U21, diverts major histocompatibility complex class II molecules to lysosomes. J. Virol., 75(24), 12347–12358.CrossRefGoogle Scholar
Hudson, A. W., Blom, D., Howley, P. M.et al. (2003). The ER-lumenal domain of the HHV-7 immunoevasin U21 directs class II MHC molecules to lysosomes. Traffic, 4(12), 824–837.CrossRefGoogle Scholar
Ishido, S., Choi, J. K., Lee, B. S.et al. (2000). Inhibition of natural killer cell-mediated cytotoxicity by Kaposi's sarcoma-associated herpesvirus K5 protein. Immunity, 13(3), 365–374.CrossRefGoogle ScholarPubMed
Janeway, C. A. Jr. and Medzhitov, R. (2002). Innate immune recognition. Annu. Rev. Immunol., 20, 197–216.CrossRefGoogle ScholarPubMed
Jenkins, C., Abendroth, A., and Slobedman, B. (2004). A novel viral transcript with homology to human interleukin-10 is expressed during latent human cytomegalovirus infection. J. Virol., 78(3), 1440–1447.CrossRefGoogle ScholarPubMed
Jones, T. R., Wiertz, E. J., Sun, L.et al. (1996). Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class II heavy chains. Proc. Natl Acad. Sci. USA, 93(21), 11327–11333.CrossRefGoogle Scholar
Kavanagh, D. G., Gold, M. C., Wagner, M.et al. (2001a). The multiple immune-evasion genes of murine cytomegalovirus are not redundant: m4 and m152 inhibit antigen presentation in a complementary and cooperative fashion. J. Exp. Med., 194(7), 967–978.CrossRefGoogle Scholar
Kavanagh, D. G., Koszinowski, U. H., and Hill, A. B. (2001b). The murine cytomegalovirus immune evasion protein m4/gp34 forms biochemically distinct complexes with class II MHC at the cell surface and in a pre-Golgi compartment. J. Immunol., 167(7), 3894–3902.CrossRefGoogle Scholar
Khan, S., Zimmermann, A., Bassler, M.et al. (2004). A cytomegalovirus inhibitor of gamma interferon signaling controls immunoproteasome induction. J. Virol., 78(4), 1831–1842.CrossRefGoogle ScholarPubMed
Khanna, R., Burrows, S. R., Steigerwald-Mullen, P. M.et al. (1995). Isolation of cytotoxic T lymphocytes from healthy seropositive individuals specific for peptide epitopes from Epstein–Barr virus nuclear antigen 1: implications for viral persistence and tumor surveillance. Virology, 214(2), 633–637.CrossRefGoogle ScholarPubMed
Kikkert, M., Hassink, G., Barel, M.et al. (2001). Ubiquitination is essential for human cytomegalovirus US11-mediated dislocation of class II MHC molecules from the endoplasmic reticulum to the cytosol. Biochem. J., 358(2), 369–377.CrossRefGoogle Scholar
Knop, M., Finger, A., Brawn, T.et al. (1996). Der1, a novel protein specifically required for endoplasmic reticulum degradation in yeast. EMBO. J., 15(4), 753–763.Google Scholar
Kobelt, D., Lechmann, M., and Steinkasserer, A. (2003). The interaction between dendritic cells and herpes simplex virus-1. Curr. Top. Microbiol. Immunol., 276, 145–161.Google ScholarPubMed
Koopers-Lalic, D., Reits, E. A., Ressing, M. E.et al. (2005). Varicelloviruses avoid T cell recognition by UL49.5-mediated inactivation of the transporter associated with antigen processing. Proc. Natl. Acad. Sci., 102(14): 5144–9.CrossRefGoogle Scholar
Kruse, M., Rosorius, O., Kratzer, F.et al. (2000). Mature dendritic cells infected with herpes simplex virus type 1 exhibit inhibited T-cell stimulatory capacity. J. Virol., 74(15), 7127–7136.CrossRefGoogle ScholarPubMed
Kyritsis, C., Gorbulev, S., Hutschenreiter, S.et al. (2001). Molecular mechanism and structural aspects of transporter associated with antigen processing inhibition by the cytomegalovirus protein US6. J. Biol. Chem., 276(51), 48031–48039.CrossRefGoogle ScholarPubMed
Lanier, L. L. (2003). Natural killer cell receptor signaling. Curr. Opin. Immunol., 15(3), 308–314.CrossRefGoogle ScholarPubMed
Lee, S., Park, B., and Ahn, K. (2003). Determinant for endoplasmic reticulum retention in the luminal domain of the human cytomegalovirus US3 glycoprotein. J. Virol., 77(3), 2147–2156.CrossRefGoogle ScholarPubMed
Lee, S., Yoon, J., Park, B.et al. (2000). Structural and functional dissection of human cytomegalovirus US3 in binding major histocompatibility complex class II molecules. J. Virol., 74(23), 11262–11269.CrossRefGoogle Scholar
Lee, S. P., Brooks, J. M., Al-Jarrah, H.et al. (2004). CD8 T cell recognition of endogenously expressed Epstein–Barr virus nuclear antigen 1. J. Exp. Med., 199(10), 1409–1420.CrossRefGoogle ScholarPubMed
Lewandowski, G. A., Lo, D., and Bloom, F. E.et al. (1993). Interference with major histocompatibility complex class II-restricted antigen presentation in the brain by herpes simplex virus type 1: a possible mechanism of evasion of the immune response. Proc. Natl Acad. Sci. USA, 90(5), 2005–2009.CrossRefGoogle ScholarPubMed
Li, L., Liu, D., Fletcher, L.et al. (2002). Epstein–Barr virus inhibits the development of dendritic cells by promoting apoptosis of their monocyte precursors in the presence of granulocyte macrophage-colony-stimulating factor and interleukin-4. Blood, 99(10), 3725–3734.CrossRefGoogle ScholarPubMed
Lilley, B. N. and Ploegh, H. L. (2004). A membrane protein required for dislocation of misfolded proteins from the ER. Nature, 429(6994), 834–840.CrossRefGoogle ScholarPubMed
Lilley, B. N. and Ploegh, H. L. (2005). Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proc. Natl Acad. Sci., 102(40), 14296–14301.CrossRefGoogle ScholarPubMed
Lilley, B. N., Tortorella, D., and Ploegh, H. L. (2003). Dislocation of a type I membrane protein requires interactions between membrane-spanning segments within the lipid bilayer. Mol. Biol. Cell., 14(9), 3690–3698.CrossRefGoogle ScholarPubMed
LoPiccolo, D. M., Gold, M. C., Kavanaugh, G. D.et al. (2003). Effective inhibition of K(b)- and D(b)-restricted antigen presentation in primary macrophages by murine cytomegalovirus. J. Virol., 77(1), 301–308.CrossRefGoogle Scholar
Lorenzo, M. E., Jung, J. U., and Ploegh, H. L. (2002). Kaposi's sarcoma-associated herpesvirus K3 utilizes the ubiquitin–proteasome system in routing class major histocompatibility complexes to late endocytic compartments. J. Virol., 76(11), 5522–5531.CrossRefGoogle ScholarPubMed
Loureiro, J., Lilley, B. N., Spooner, E.et al. (2006). Signal peptide peptidase is required for dislocation from the endoplasmic reticulum. Nature, 441(7095), 894–897.CrossRefGoogle ScholarPubMed
Lusso, P., Malnati, M., Maria, A.et al. (1991). Productive infection of CD4+ and CD8+ mature human T cell populations and clones by human herpesvirus 6. Transcriptional down-regulation of CD3. J. Immunol., 147(2), 685–691.Google Scholar
Lybarger, L., Wang, X., Harris, M. R.et al. (2003). Virus subversion of the class II MHC peptide-loading complex. Immunity, 18(1), 121–130.CrossRefGoogle Scholar
Machold, R. P., Wiertz, E. J., Jones, T. R.et al. (1997). The HCMV gene products US11 and US2 differ in their ability to attack allelic forms of murine major histocompatibility complex (MHC) class II heavy chains. J. Exp. Med., 185(2), 363–366.CrossRefGoogle Scholar
Mansouri, M., Douglas, J., and Rose, P. P. (2006). Kaposi's sarcoma herpesvirus K5 eliminates CD31/PECAM from endothelial cells. Blood in press e-publication.
McClain, K., Gehrz, R., Grierson, H.et al. (1988). Virus-associated histiocytic proliferations in children. Frequent association with Epstein–Barr virus and congenital or acquired immunodeficiencies. Am. J. Pediatr. Hematol. Oncol., 10(3), 196–205.Google Scholar
Means, R. E., Ishido, S., Alvarez, X.et al. (2002). Multiple endocytic trafficking pathways of class II MHC molecules induced by a Herpesvirus protein. EMBO J., 21(7), 1638–1649.CrossRefGoogle Scholar
Medzhitov, R. and Janeway, C. A. Jr. (1999). Innate immune induction of the adaptive immune response. Cold Spring Harb. Symp. Quant. Biol., 64, 429–435.CrossRefGoogle ScholarPubMed
Miller, D. M., Rahill, B. M., Boss, J. M.et al. (1998). Human cytomegalovirus inhibits major histocompatibility complex class II expression by disruption of the Jak/Stat pathway. J. Exp. Med., 187(5), 675–683.CrossRefGoogle ScholarPubMed
Misaghi, S., Sun, Z. Y., Stern, P.et al. (2004). Structural and functional analysis of human cytomegalovirus US3 protein. J. Virol., 78(1), 413–423.CrossRefGoogle ScholarPubMed
Momburg, F. and Tan, P. (2002). Tapasin-the keystone of the loading complex optimizing peptide binding by class II MHC molecules in the endoplasmic reticulum. Mol. Immunol., 39(3–4), 217–233.CrossRefGoogle Scholar
Morrow, G., Slobedman, B., Cunningham, A. L.et al. (2003). Varicella-zoster virus productively infects mature dendritic cells and alters their immune function. J. Virol., 77(8), 4950–4959.CrossRefGoogle ScholarPubMed
Moutaftsi, M., Brennan, P., Spector, S. A.et al. (2004). Impaired lymphoid chemokine-mediated migration due to a block on the chemokine receptor switch in human cytomegalovirus-infected dendritic cells. J. Virol., 78(6), 3046–3054.CrossRefGoogle ScholarPubMed
Mullen, M. M., Haan, K. M., Longnecker, R.et al. (2002). Structure of the Epstein–Barr virus gp42 protein bound to the class II MHC receptor HLA-DR1. Mol. Cell., 9(2), 375–385.CrossRefGoogle ScholarPubMed
Nazif, T. and Bogyo, M. (2001). Global analysis of proteasomal substrate specificity using positional-scanning libraries of covalent inhibitors. Proc. Natl Acad. Sci. USA, 98(6), 2967–3972.CrossRefGoogle ScholarPubMed
Neefjes, J. J., Momburg, F., and Hammerling, G. J. (1993). Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter. Science, 261(5122), 769–771.CrossRefGoogle ScholarPubMed
Neumann, L., Kraas, W., Uebel, S.et al. (1997). The active domain of the herpes simplex virus protein ICP47: a potent inhibitor of the transporter associated with antigen processing. J. Mol. Biol., 272(4), 484–492.CrossRefGoogle ScholarPubMed
Nikkels, A. F., Sadzot-Delvaux, C., and Pierard, G. E. (2004). Absence of intercellular adhesion molecule 1 expression in varicella zoster virus-infected keratinocytes during herpes zoster: another immune evasion strategy?Am. J. Dermatopathol., 26(1), 27–32.CrossRefGoogle ScholarPubMed
Orr, M. T., Edelmann, K. H., Vieira, J.et al. (2005). Inhibition of class II MHC Is a Virulence Factor in Herpes Simplex Virus Infection of Mice. PLOS Pathogens, 1(1), 62–71.Google Scholar
Owen, D. J. and Evans, P. R. (1998). A structural explanation for the recognition of tyrosine-based endocytotic signals. Science, 282(5392), 1327–1332.CrossRefGoogle ScholarPubMed
Park, B., Oh, H., Lee, S.et al. (2002). The class II MHC homolog of human cytomegalovirus is resistant to down-regulation mediated by the unique short region protein (US)2, US3, US6, and US11 gene products. J. Immunol., 168(7), 3464–3469.CrossRefGoogle Scholar
Park, B., Kim, Y., Shin, J.et al. (2004). Human cytomegalovirus inhibits tapasin-dependent peptide loading and optimization of the class II MHC peptide cargo for immune evasion. Immunity, 20(1), 71–85.CrossRefGoogle Scholar
Pfander, R., Neumann, L., Zweckstetter, M.et al. (1999). Structure of the active domain of the herpes simplex virus protein ICP47 in water/sodium dodecyl sulfate solution determined by nuclear magnetic resonance spectroscopy. Biochemistry, 38(41), 13692–13698.CrossRefGoogle ScholarPubMed
Piguet, V., Wan, L., Borel, C.et al. (2000). HIV-1 Nef protein binds to the cellular protein PACS-1 to downregulate class II major histocompatibility complexes. Nat. Cell. Biol., 2(3), 163–167.CrossRefGoogle Scholar
Prichard, M. N., Quenelle, D. C., Bidanset, D. J.et al. (2006). Human cytomegalovirus UL27 is not required for viral replication in human tissue implanted in SCID mice. Virology J, 3, 18–20.CrossRefGoogle Scholar
Radosevich, T. J., Seregina, T., Link, C. J.et al. (2003). Effective suppression of class II major histocompatibility complex expression by the US11 or ICP47 genes can be limited by cell type or interferon-gamma exposure. Hum. Gene. Ther., 14(18), 1765–1775.CrossRefGoogle ScholarPubMed
Rehm, A., Engelsberg, A., Tortorella, D.et al. (2002). Human cytomegalovirus gene products US2 and US11 differ in their ability to attack major histocompatibility class II heavy chains in dendritic cells. J. Virol., 76(10), 5043–5050.CrossRefGoogle ScholarPubMed
Ressing, M. E., Keating, S. E., Leeuwen, D.et al. (2005.) Impaired transporter associated with antigen processing-dependent peptide transport during productive EBV infection. J. Immunol., 174(11), 6829–6838.CrossRefGoogle ScholarPubMed
Ressing, M. E., van Leeuwen, D., Verreck, F. A. (2005). Epstein-Barr virus gp42 is posttranslationally modified to produce soluble gp42 that mediates HLA class II immune evasion. J. Virol., 79(2), 841–52.CrossRefGoogle ScholarPubMed
Reusch, U., Muranyi, W., Lucin, P.et al. (1999). A cytomegalovirus glycoprotein re-routes class II MHC complexes to lysosomes for degradation. EMBO J., 18(4), 1081–1091.CrossRefGoogle Scholar
Sanchez, D. J., Coscoy, L., and Ganem, D. (2002). Functional organization of MIR2, a novel viral regulator of selective endocytosis. J. Biol. Chem., 277(8), 6124–6130.CrossRefGoogle ScholarPubMed
Savard, M., Belanger, C., Tardif, M.et al. (2000). Infection of primary human monocytes by Epstein–Barr virus. J. Virol., 74(6), 2612–2619.CrossRefGoogle ScholarPubMed
Scheel, H. and Hofmann, K. (2003). No evidence for PHD fingers as ubiquitin ligases. Trends Cell. Biol., 13(6), 285–287; author reply 287–288.CrossRefGoogle ScholarPubMed
Schust, D. J., Tortorella, D., and Ploegh, H. L. (1998). Trophoblast class II major histocompatibility complex (MHC) products are resistant to rapid degradation imposed by the human cytomegalovirus (HCMV) gene products US2 and US11. J. Exp. Med., 188(3), 497–503.CrossRefGoogle Scholar
Shamu, C. E., Flierman, D., Ploegh, H. L.et al. (2001). Polyubiquitination is required for US11-dependent movement of class II MHC heavy chain from endoplasmic reticulum into cytosol. Mol. Biol. Cell., 12(8), 2546–2555.CrossRefGoogle Scholar
Shin, J., Park, B.Lee, S.et al. (2006). A short isoform of human cytomegalovirus US3 functions as a dominant negative inhibitor of the full-length form. J. Vir. 80(11), 5397–5404.CrossRefGoogle Scholar
Sloan, D. D., Zahariadis, G., Posavad, C. M.et al. (2003). CTL are inactivated by herpes simplex virus-infected cells expressing a viral protein kinase. J. Immunol., 171(12), 6733–6741.CrossRefGoogle ScholarPubMed
Sloan, D. D., Han, J. Y., Sandifer, T. K.et al. (2006). Inhibition of TCR signaling by herpes simplex virus. J. Immunol., 176(3), 1825–1833.CrossRefGoogle ScholarPubMed
Slobedman, B., Mocarski, E. S., Arvin, A.et al. (2002). Latent cytomegalovirus down-regulates major histocompatibility complex class II expression on myeloid progenitors. Blood, 100(8), 2867–2873.CrossRefGoogle ScholarPubMed
Spencer, J. V., Lockridge, K. M., Barry, P. A.et al. (2002). Potent immunosuppressive activities of cytomegalovirus-encoded interleukin-10. J. Virol., 76(3), 1285–1292.CrossRefGoogle ScholarPubMed
Spriggs, M. K., Armitage, R. J., Comeau, M. R.et al. (1996). The extracellular domain of the Epstein–Barr virus BZLF2 protein binds the HLA-DR beta chain and inhibits antigen presentation. J. Virol., 70(8), 5557–5563.Google ScholarPubMed
Sullivan, C. S., Grundhoff, A. T., Tevethia, S.et al. (2005). SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature, 432(7042), 682–686.CrossRefGoogle Scholar
Sutkowski, N., Conrad, B., Thorky-Lawson, D. A.et al. (2001). Epstein–Barr virus transactivates the human endogenous retrovirus HERV-K18 that encodes a superantigen. Immunity, 15(4), 579–589.CrossRefGoogle ScholarPubMed
Takatsu, H., Katoh, Y., Shiba, Y.et al. (2001). Golgi-localizing, gamma-adaptin ear homology domain, ADP-ribosylation factor-binding (GGA) proteins interact with acidic dileucine sequences within the cytoplasmic domains of sorting receptors through their Vps27p/Hrs/STAM (VHS) domains. J. Biol. Chem., 276(30), 28541–28545.CrossRefGoogle ScholarPubMed
Tellam, J., Connolly, G., Green, K. J.et al. (2004). Endogenous presentation of CD8+ T cell epitopes from Epstein–Barr virus-encoded nuclear antigen 1. J. Exp. Med., 199(10), 1421–1431.CrossRefGoogle ScholarPubMed
Tirabassi, R. S. and Ploegh, H. L. (2002). The human cytomegalovirus US8 glycoprotein binds to major histocompatibility complex class II products. J. Virol., 76(13), 6832–6835.CrossRefGoogle Scholar
Tirosh, B., M. Furman, H., Tortorella, D.et al. (2003). Protein unfolding is not a prerequisite for endoplasmic reticulum-to-cytosol dislocation. J. Biol. Chem., 278(9), 6664–6672.CrossRefGoogle Scholar
Tirosh, B., Iwakoshi, N. N., Lilley, B. N.et al. (2005). Human cytomegalovirus protein US11 provokes an unfolded protein response that may facilitate the degradation of class II major histocompatibility complex products. J. Virol., 79(5), 2768–2779.CrossRefGoogle Scholar
Tomasec, P., Braud, V. M., Rikards, C.et al. (2000). Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science, 287(5455), 1031.CrossRefGoogle ScholarPubMed
Tomazin, R., Schoot, N. E., Goldsmith, K.et al. (1998). Herpes simplex virus type 2 ICP47 inhibits human TAP but not mouse TAP. J. Virol., 72(3), 2560–2563.Google Scholar
Tomazin, R., Boname, J., Hegde, N. R.et al. (1999). Cytomegalovirus US2 destroys two components of the class II MHC pathway, preventing recognition by CD4+ T cells. Nat. Med., 5(9), 1039–1043.CrossRefGoogle ScholarPubMed
Tomescu, C., Law, W. K., and Keles, D. H. (2003). Surface downregulation of major histocompatibility complex class II, PE-CAM, and ICAM-1 following de novo infection of endothelial cells with Kaposi's sarcoma-associated herpesvirus. J. Virol., 77(17), 9669–9684.CrossRefGoogle Scholar
Tortorella, D., Gewurz, B. E., Furman, M. H.et al. (2000). Viral subversion of the immune system. Annu. Rev. Immunol., 18, 861–926.CrossRefGoogle ScholarPubMed
Van den Berg, B., Clemons, W. M. Jr., Collinson, I.et al. (2004). X-ray structure of a protein-conducting channel. Nature, 427(6969), 36–44.CrossRefGoogle ScholarPubMed
Varadan, R., Assfalg, M., Haririnia, A.et al. (2004). Solution conformation of Lys63-linked di-ubiquitin chain provides clues to functional diversity of polyubiquitin signaling. J. Biol. Chem., 279(8), 7055–7063.CrossRefGoogle ScholarPubMed
Voges, D., Zwickl, P., and Braumeister, W. (1999). The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem., 68, 1015–1068.CrossRefGoogle ScholarPubMed
Voo, K. S., Fu, T., Wang, H. Y.et al. (2004). Evidence for the presentation of major histocompatibility complex class I-restricted Epstein–Barr virus nuclear antigen 1 peptides to CD8+ T lymphocytes. J. Exp. Med., 199(4), 459–470.CrossRefGoogle ScholarPubMed
Wang, X., Lybarger, L., Connors, R.et al. (2004). Model for the interaction of gammaherpesvirus 68 RING-CH finger protein mK3 with major histocompatibility complex class II and the peptide-loading complex. J. Virol., 78(16), 8673–8686.CrossRefGoogle Scholar
Wang, X., Ye, Y., Lencer, W.et al. (2006). The viral E3 ubiquitin ligase mK3 uses the Derlin/p97 endoplasmic reticulum-associated degradation pathway to mediate down-regulation of major histocompatibility complex class II proteins. J. Biol. Chem., 281(13), 8636–8644.CrossRefGoogle Scholar
Wiertz, E. J., Jones, T. R., Sun, L.et al. (1996a). The human cytomegalovirus US11 gene product dislocates class II MHC heavy chains from the endoplasmic reticulum to the cytosol. Cell, 84(5), 769–779.CrossRefGoogle Scholar
Wiertz, E. J., Tortorella, D., Bogya, M.et al. (1996b). Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature, 384(6608), 432–438.CrossRefGoogle Scholar
Willcox, B. E., Thomas, L. M., and Bjorkman, P. J. (2003). Crystal structure of HLA-A2 bound to LIR-1, a host and viral major histocompatibility complex receptor. Nat. Immunol., 4(9), 913–919.CrossRefGoogle ScholarPubMed
Wubbolts, R. and Neefjes, J. (1999). Intracellular transport and peptide loading of class II MHC molecules: regulation by chaperones and motors. Immunol. Rev., 172, 189–208.CrossRefGoogle ScholarPubMed
Ye, Y., Meyer, H. H., and Rapoport, T. A. (2001). The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature, 414(6864), 652–656.CrossRefGoogle ScholarPubMed
Ye, Y., Shibata, Y., Yun, C.et al. (2004). A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature, 429(6994), 841–847.CrossRefGoogle ScholarPubMed
York, I. A., Roop, C., Andrew, D. W.et al. (1994). A cytosolic herpes simplex virus protein inhibits antigen presentation to CD8+ T lymphocytes. Cell, 77(4), 525–535.CrossRefGoogle ScholarPubMed
Zeidler, R., Eissner, G., Meissner, P.et al. (1997). Downregulation of TAP1 in B lymphocytes by cellular and Epstein–Barr virus-encoded interleukin-10. Blood, 90(6), 2390–2397.Google Scholar
Ziegler, H., Muranyi, W., Burgert, H. G.et al. (2000). The luminal part of the murine cytomegalovirus glycoprotein gp40 catalyzes the retention of class II MHC molecules. EMBO. J., 19(5), 870–881.CrossRefGoogle Scholar
Zimmermann, A., Trilling, M., Wagner, M.et al. (2005). A cytomegaloviral protein reveals a dual role for STAT2 in IFN-γ signaling and antiviral responses. J. Exp. Med., 201(10), 1543–1553.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
×