1,027
Views
20
CrossRef citations to date
0
Altmetric
Review

Dendritic cell biology in human cytomegalovirus infection and the clinical consequences for host immunity and pathology

&
Pages 621-634 | Received 27 Jul 2012, Accepted 14 Sep 2012, Published online: 17 Oct 2012

References

  • Britt WA, Alford CA. Cytomegalovirus. In: Fields BN, Roizman B, Knipe DM, Melnick JL, Howley PM, Chanock RM, et al., eds. Fields Virology. Philiadelphia: Lippincott-Raven Publishers, 1996:2493-523.
  • Pass RF. Cytomegalovirus. In: Knipe DM, Howley PM, eds. Fields Virology. Philadephia: Lippincott Williams & Wilkins, 2001:2675-706.
  • Söderberg-Nauclér C. Does cytomegalovirus play a causative role in the development of various inflammatory diseases and cancer?. J Intern Med 2006; 259:219 - 46; http://dx.doi.org/10.1111/j.1365-2796.2006.01618.x; PMID: 16476101
  • Tomazin R, Boname J, Hegde NR, Lewinsohn DM, Altschuler Y, Jones TR, et al. Cytomegalovirus US2 destroys two components of the MHC class II pathway, preventing recognition by CD4+ T cells. Nat Med 1999; 5:1039 - 43; http://dx.doi.org/10.1038/12478; PMID: 10470081
  • Odeberg J, Plachter B, Brandén L, Söderberg-Nauclér C. Human cytomegalovirus protein pp65 mediates accumulation of HLA-DR in lysosomes and destruction of the HLA-DR alpha-chain. Blood 2003; 101:4870 - 7; http://dx.doi.org/10.1182/blood-2002-05-1504; PMID: 12609847
  • Hegde NR, Tomazin RA, Wisner TW, Dunn C, Boname JM, Lewinsohn DM, et al. Inhibition of HLA-DR assembly, transport, and loading by human cytomegalovirus glycoprotein US3: a novel mechanism for evading major histocompatibility complex class II antigen presentation. J Virol 2002; 76:10929 - 41; http://dx.doi.org/10.1128/JVI.76.21.10929-10941.2002; PMID: 12368336
  • Loenen WA, Bruggeman CA, Wiertz EJ. Immune evasion by human cytomegalovirus: lessons in immunology and cell biology. Semin Immunol 2001; 13:41 - 9; http://dx.doi.org/10.1006/smim.2001.0294; PMID: 11289798
  • Noriega V, Redmann V, Gardner T, Tortorella D. Diverse immune evasion strategies by human cytomegalovirus. Immunol Res 2012; http://dx.doi.org/10.1007/s12026-012-8304-8; PMID: 22454101
  • Kim S, Lee S, Shin J, Kim Y, Evnouchidou I, Kim D, et al. Human cytomegalovirus microRNA miR-US4-1 inhibits CD8(+) T cell responses by targeting the aminopeptidase ERAP1. Nat Immunol 2011; 12:984 - 91; http://dx.doi.org/10.1038/ni.2097; PMID: 21892175
  • Hansen SG, Powers CJ, Richards R, Ventura AB, Ford JC, Siess D, et al. Evasion of CD8+ T cells is critical for superinfection by cytomegalovirus. Science 2010; 328:102 - 6; http://dx.doi.org/10.1126/science.1185350; PMID: 20360110
  • Wilkinson GW, Tomasec P, Stanton RJ, Armstrong M, Prod’homme V, Aicheler R, et al. Modulation of natural killer cells by human cytomegalovirus. J Clin Virol 2008; 41:206 - 12; http://dx.doi.org/10.1016/j.jcv.2007.10.027; PMID: 18069056
  • Beck S, Barrell BG. Human cytomegalovirus encodes a glycoprotein homologous to MHC class-I antigens. Nature 1988; 331:269 - 72; http://dx.doi.org/10.1038/331269a0; PMID: 2827039
  • Odeberg J, Cerboni C, Browne H, Kärre K, Möller E, Carbone E, et al. Human cytomegalovirus (HCMV)-infected endothelial cells and macrophages are less susceptible to natural killer lysis independent of the downregulation of classical HLA class I molecules or expression of the HCMV class I homologue, UL18. Scand J Immunol 2002; 55:149 - 61; http://dx.doi.org/10.1046/j.1365-3083.2002.01025.x; PMID: 11896931
  • Belz GT, Nutt SL. Transcriptional programming of the dendritic cell network. Nat Rev Immunol 2012; 12:101 - 13; http://dx.doi.org/10.1038/nri3149; PMID: 22273772
  • Liu K, Nussenzweig MC. Origin and development of dendritic cells. Immunol Rev 2010; 234:45 - 54; http://dx.doi.org/10.1111/j.0105-2896.2009.00879.x; PMID: 20193011
  • Sallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 1994; 179:1109 - 18; http://dx.doi.org/10.1084/jem.179.4.1109; PMID: 8145033
  • Ross MJ, Auger JA. The biology of the macrophage. In: Burke B, Lewis CE, eds. The Macrophage. Oxford: Oxford University Press, 2002:1-72.
  • Söderberg-Nauclér C, Streblow DN, Fish KN, Allan-Yorke J, Smith PP, Nelson JA. Reactivation of latent human cytomegalovirus in CD14(+) monocytes is differentiation dependent. J Virol 2001; 75:7543 - 54; http://dx.doi.org/10.1128/JVI.75.16.7543-7554.2001; PMID: 11462026
  • Verreck FA, de Boer T, Langenberg DM, Hoeve MA, Kramer M, Vaisberg E, et al. Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci USA 2004; 101:4560 - 5; http://dx.doi.org/10.1073/pnas.0400983101; PMID: 15070757
  • Swiecki M, Colonna M. Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunol Rev 2010; 234:142 - 62; http://dx.doi.org/10.1111/j.0105-2896.2009.00881.x; PMID: 20193017
  • Villadangos JA, Young L. Antigen-presentation properties of plasmacytoid dendritic cells. Immunity 2008; 29:352 - 61; http://dx.doi.org/10.1016/j.immuni.2008.09.002; PMID: 18799143
  • Gilliet M, Cao W, Liu YJ. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol 2008; 8:594 - 606; http://dx.doi.org/10.1038/nri2358; PMID: 18641647
  • Krug A, Luker GD, Barchet W, Leib DA, Akira S, Colonna M. Herpes simplex virus type 1 activates murine natural interferon-producing cells through toll-like receptor 9. Blood 2004; 103:1433 - 7; http://dx.doi.org/10.1182/blood-2003-08-2674; PMID: 14563635
  • Lund J, Sato A, Akira S, Medzhitov R, Iwasaki A. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J Exp Med 2003; 198:513 - 20; http://dx.doi.org/10.1084/jem.20030162; PMID: 12900525
  • Krug A, French AR, Barchet W, Fischer JA, Dzionek A, Pingel JT, et al. TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 2004; 21:107 - 19; http://dx.doi.org/10.1016/j.immuni.2004.06.007; PMID: 15345224
  • Varani S, Cederarv M, Feld S, Tammik C, Frascaroli G, Landini MP, et al. Human cytomegalovirus differentially controls B cell and T cell responses through effects on plasmacytoid dendritic cells. J Immunol 2007; 179:7767 - 76; PMID: 18025223
  • Gerna G, Zipeto D, Percivalle E, Parea M, Revello MG, Maccario R, et al. Human cytomegalovirus infection of the major leukocyte subpopulations and evidence for initial viral replication in polymorphonuclear leukocytes from viremic patients. J Infect Dis 1992; 166:1236 - 44; http://dx.doi.org/10.1093/infdis/166.6.1236; PMID: 1331248
  • Taylor-Wiedeman J, Sissons JG, Borysiewicz LK, Sinclair JH. Monocytes are a major site of persistence of human cytomegalovirus in peripheral blood mononuclear cells. J Gen Virol 1991; 72:2059 - 64; http://dx.doi.org/10.1099/0022-1317-72-9-2059; PMID: 1654370
  • Ibanez CE, Schrier R, Ghazal P, Wiley C, Nelson JA. Human cytomegalovirus productively infects primary differentiated macrophages. J Virol 1991; 65:6581 - 8; PMID: 1658363
  • Taylor-Wiedeman J, Sissons P, Sinclair J. Induction of endogenous human cytomegalovirus gene expression after differentiation of monocytes from healthy carriers. J Virol 1994; 68:1597 - 604; PMID: 8107221
  • Minton EJ, Tysoe C, Sinclair JH, Sissons JG. Human cytomegalovirus infection of the monocyte/macrophage lineage in bone marrow. J Virol 1994; 68:4017 - 21; PMID: 8189535
  • Einhorn L, Ost A. Cytomegalovirus infection of human blood cells. J Infect Dis 1984; 149:207 - 14; http://dx.doi.org/10.1093/infdis/149.2.207; PMID: 6321607
  • Gnann JW Jr., Ahlmén J, Svalander C, Olding L, Oldstone MB, Nelson JA. Inflammatory cells in transplanted kidneys are infected by human cytomegalovirus. Am J Pathol 1988; 132:239 - 48; PMID: 2840830
  • Fish KN, Depto AS, Moses AV, Britt W, Nelson JA. Growth kinetics of human cytomegalovirus are altered in monocyte-derived macrophages. J Virol 1995; 69:3737 - 43; PMID: 7745721
  • Söderberg-Nauclér C, Fish KN, Nelson JA. Growth of human cytomegalovirus in primary macrophages. Methods 1998; 16:126 - 38; http://dx.doi.org/10.1006/meth.1998.0650; PMID: 9774522
  • Sindre H, Tjøonnfjord GE, Rollag H, Ranneberg-Nilsen T, Veiby OP, Beck S, et al. Human cytomegalovirus suppression of and latency in early hematopoietic progenitor cells. Blood 1996; 88:4526 - 33; PMID: 8977244
  • Mendelson M, Monard S, Sissons P, Sinclair J. Detection of endogenous human cytomegalovirus in CD34+ bone marrow progenitors. J Gen Virol 1996; 77:3099 - 102; http://dx.doi.org/10.1099/0022-1317-77-12-3099; PMID: 9000102
  • Movassagh M, Gozlan J, Senechal B, Baillou C, Petit JC, Lemoine FM. Direct infection of CD34+ progenitor cells by human cytomegalovirus: evidence for inhibition of hematopoiesis and viral replication. Blood 1996; 88:1277 - 83; PMID: 8695845
  • Khaiboullina SF, Maciejewski JP, Crapnell K, Spallone PA, Dean Stock A, Pari GS, et al. Human cytomegalovirus persists in myeloid progenitors and is passed to the myeloid progeny in a latent form. Br J Haematol 2004; 126:410 - 7; http://dx.doi.org/10.1111/j.1365-2141.2004.05056.x; PMID: 15257715
  • Reeves MB, MacAry PA, Lehner PJ, Sissons JG, Sinclair JH. Latency, chromatin remodeling, and reactivation of human cytomegalovirus in the dendritic cells of healthy carriers. Proc Natl Acad Sci USA 2005; 102:4140 - 5; http://dx.doi.org/10.1073/pnas.0408994102; PMID: 15738399
  • Söderberg-Nauclér C, Fish KN, Nelson JA. Reactivation of latent human cytomegalovirus by allogeneic stimulation of blood cells from healthy donors. Cell 1997; 91:119 - 26; http://dx.doi.org/10.1016/S0092-8674(01)80014-3; PMID: 9335340
  • Söderberg-Nauclér C, Fish KN, Nelson JA. Interferon-gamma and tumor necrosis factor-alpha specifically induce formation of cytomegalovirus-permissive monocyte-derived macrophages that are refractory to the antiviral activity of these cytokines. J Clin Invest 1997; 100:3154 - 63; http://dx.doi.org/10.1172/JCI119871; PMID: 9399963
  • Reeves MB, Compton T. Inhibition of inflammatory interleukin-6 activity via extracellular signal-regulated kinase-mitogen-activated protein kinase signaling antagonizes human cytomegalovirus reactivation from dendritic cells. J Virol 2011; 85:12750 - 8; http://dx.doi.org/10.1128/JVI.05878-11; PMID: 21937636
  • Hargett D, Shenk TE. Experimental human cytomegalovirus latency in CD14+ monocytes. Proc Natl Acad Sci USA 2010; 107:20039 - 44; http://dx.doi.org/10.1073/pnas.1014509107; PMID: 21041645
  • Döcke WD, Prösch S, Fietze E, Kimel V, Zuckermann H, Klug C, et al. Cytomegalovirus reactivation and tumour necrosis factor. Lancet 1994; 343:268 - 9; http://dx.doi.org/10.1016/S0140-6736(94)91116-9; PMID: 7905100
  • Kutza AS, Muhl E, Hackstein H, Kirchner H, Bein G. High incidence of active cytomegalovirus infection among septic patients. Clin Infect Dis 1998; 26:1076 - 82; http://dx.doi.org/10.1086/520307; PMID: 9597229
  • Asadullah K, Prösch S, Audring H, Büttnerova I, Volk HD, Sterry W, et al. A high prevalence of cytomegalovirus antigenaemia in patients with moderate to severe chronic plaque psoriasis: an association with systemic tumour necrosis factor alpha overexpression. Br J Dermatol 1999; 141:94 - 102; http://dx.doi.org/10.1046/j.1365-2133.1999.02926.x; PMID: 10417521
  • Gredmark S, Söderberg-Nauclér C. Human cytomegalovirus inhibits differentiation of monocytes into dendritic cells with the consequence of depressed immunological functions. J Virol 2003; 77:10943 - 56; http://dx.doi.org/10.1128/JVI.77.20.10943-10956.2003; PMID: 14512544
  • Carlier J, Martin H, Mariamé B, Rauwel B, Mengelle C, Weclawiak H, et al. Paracrine inhibition of GM-CSF signaling by human cytomegalovirus in monocytes differentiating to dendritic cells. Blood 2011; 118:6783 - 92; http://dx.doi.org/10.1182/blood-2011-02-337956; PMID: 22031867
  • Gredmark S, Tilburgs T, Söderberg-Nauclér C. Human cytomegalovirus inhibits cytokine-induced macrophage differentiation. J Virol 2004; 78:10378 - 89; http://dx.doi.org/10.1128/JVI.78.19.10378-10389.2004; PMID: 15367604
  • Söderberg C, Giugni TD, Zaia JA, Larsson S, Wahlberg JM, Möller E. CD13 (human aminopeptidase N) mediates human cytomegalovirus infection. J Virol 1993; 67:6576 - 85; PMID: 8105105
  • Gredmark S, Britt WB, Xie X, Lindbom L, Söderberg-Nauclér C. Human cytomegalovirus induces inhibition of macrophage differentiation by binding to human aminopeptidase N/CD13. J Immunol 2004; 173:4897 - 907; PMID: 15470031
  • Mutimer D, Mirza D, Shaw J, O’Donnell K, Elias E. Enhanced (cytomegalovirus) viral replication associated with septic bacterial complications in liver transplant recipients. Transplantation 1997; 63:1411 - 5; http://dx.doi.org/10.1097/00007890-199705270-00007; PMID: 9175802
  • van den Berg AP, Klompmaker IJ, Haagsma EB, Peeters PM, Meerman L, Verwer R, et al. Evidence for an increased rate of bacterial infections in liver transplant patients with cytomegalovirus infection. Clin Transplant 1996; 10:224 - 31; PMID: 8664524
  • Paya CV, Wiesner RH, Hermans PE, Larson-Keller JJ, Ilstrup DM, Krom RA, et al. Risk factors for cytomegalovirus and severe bacterial infections following liver transplantation: a prospective multivariate time-dependent analysis. J Hepatol 1993; 18:185 - 95; http://dx.doi.org/10.1016/S0168-8278(05)80245-4; PMID: 8409334
  • Riegler S, Hebart H, Einsele H, Brossart P, Jahn G, Sinzger C. Monocyte-derived dendritic cells are permissive to the complete replicative cycle of human cytomegalovirus. J Gen Virol 2000; 81:393 - 9; PMID: 10644837
  • Sinzger C, Digel M, Jahn G. Cytomegalovirus cell tropism. Curr Top Microbiol Immunol 2008; 325:63 - 83; http://dx.doi.org/10.1007/978-3-540-77349-8_4; PMID: 18637500
  • Sinzger C, Hahn G, Digel M, Katona R, Sampaio KL, Messerle M, et al. Cloning and sequencing of a highly productive, endotheliotropic virus strain derived from human cytomegalovirus TB40/E. J Gen Virol 2008; 89:359 - 68; http://dx.doi.org/10.1099/vir.0.83286-0; PMID: 18198366
  • Gerna G, Percivalle E, Lilleri D, Lozza L, Fornara C, Hahn G, et al. Dendritic-cell infection by human cytomegalovirus is restricted to strains carrying functional UL131-128 genes and mediates efficient viral antigen presentation to CD8+ T cells. J Gen Virol 2005; 86:275 - 84; http://dx.doi.org/10.1099/vir.0.80474-0; PMID: 15659746
  • Hahn G, Revello MG, Patrone M, Percivalle E, Campanini G, Sarasini A, et al. Human cytomegalovirus UL131-128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J Virol 2004; 78:10023 - 33; http://dx.doi.org/10.1128/JVI.78.18.10023-10033.2004; PMID: 15331735
  • Halary F, Amara A, Lortat-Jacob H, Messerle M, Delaunay T, Houlès C, et al. Human cytomegalovirus binding to DC-SIGN is required for dendritic cell infection and target cell trans-infection. Immunity 2002; 17:653 - 64; http://dx.doi.org/10.1016/S1074-7613(02)00447-8; PMID: 12433371
  • Plazolles N, Humbert JM, Vachot L, Verrier B, Hocke C, Halary F. Pivotal advance: The promotion of soluble DC-SIGN release by inflammatory signals and its enhancement of cytomegalovirus-mediated cis-infection of myeloid dendritic cells. J Leukoc Biol 2011; 89:329 - 42; http://dx.doi.org/10.1189/jlb.0710386; PMID: 20940323
  • Haspot F, Lavault A, Sinzger C, Laib Sampaio K, Stierhof YD, Pilet P, et al. Human cytomegalovirus entry into dendritic cells occurs via a macropinocytosis-like pathway in a pH-independent and cholesterol-dependent manner. PLoS One 2012; 7:e34795; http://dx.doi.org/10.1371/journal.pone.0034795; PMID: 22496863
  • Raftery MJ, Schwab M, Eibert SM, Samstag Y, Walczak H, Schönrich G. Targeting the function of mature dendritic cells by human cytomegalovirus: a multilayered viral defense strategy. Immunity 2001; 15:997 - 1009; http://dx.doi.org/10.1016/S1074-7613(01)00239-4; PMID: 11754820
  • Beck K, Meyer-König U, Weidmann M, Nern C, Hufert FT. Human cytomegalovirus impairs dendritic cell function: a novel mechanism of human cytomegalovirus immune escape. Eur J Immunol 2003; 33:1528 - 38; http://dx.doi.org/10.1002/eji.200323612; PMID: 12778470
  • Moutaftsi M, Mehl AM, Borysiewicz LK, Tabi Z. Human cytomegalovirus inhibits maturation and impairs function of monocyte-derived dendritic cells. Blood 2002; 99:2913 - 21; http://dx.doi.org/10.1182/blood.V99.8.2913; PMID: 11929782
  • Mezger M, Bonin M, Kessler T, Gebhardt F, Einsele H, Loeffler J. Toll-like receptor 3 has no critical role during early immune response of human monocyte-derived dendritic cells after infection with the human cytomegalovirus strain TB40E. Viral Immunol 2009; 22:343 - 51; http://dx.doi.org/10.1089/vim.2009.0011; PMID: 19951172
  • Sénéchal B, Boruchov AM, Reagan JL, Hart DN, Young JW. Infection of mature monocyte-derived dendritic cells with human cytomegalovirus inhibits stimulation of T-cell proliferation via the release of soluble CD83. Blood 2004; 103:4207 - 15; http://dx.doi.org/10.1182/blood-2003-12-4350; PMID: 14962896
  • Wagner CS, Walther-Jallow L, Buentke E, Ljunggren HG, Achour A, Chambers BJ. Human cytomegalovirus-derived protein UL18 alters the phenotype and function of monocyte-derived dendritic cells. J Leukoc Biol 2008; 83:56 - 63; http://dx.doi.org/10.1189/jlb.0307181; PMID: 17898320
  • Moutaftsi M, Brennan P, Spector SA, Tabi Z. Impaired lymphoid chemokine-mediated migration due to a block on the chemokine receptor switch in human cytomegalovirus-infected dendritic cells. J Virol 2004; 78:3046 - 54; http://dx.doi.org/10.1128/JVI.78.6.3046-3054.2004; PMID: 14990723
  • Varani S, Frascaroli G, Homman-Loudiyi M, Feld S, Landini MP, Söderberg-Nauclér C. Human cytomegalovirus inhibits the migration of immature dendritic cells by down-regulating cell-surface CCR1 and CCR5. J Leukoc Biol 2005; 77:219 - 28; http://dx.doi.org/10.1189/jlb.0504301; PMID: 15522919
  • Kotenko SV, Saccani S, Izotova LS, Mirochnitchenko OV, Pestka S. Human cytomegalovirus harbors its own unique IL-10 homolog (cmvIL-10). Proc Natl Acad Sci USA 2000; 97:1695 - 700; http://dx.doi.org/10.1073/pnas.97.4.1695; PMID: 10677520
  • Jenkins C, Abendroth A, Slobedman B. A novel viral transcript with homology to human interleukin-10 is expressed during latent human cytomegalovirus infection. J Virol 2004; 78:1440 - 7; http://dx.doi.org/10.1128/JVI.78.3.1440-1447.2004; PMID: 14722299
  • Jenkins C, Garcia W, Godwin MJ, Spencer JV, Stern JL, Abendroth A, et al. Immunomodulatory properties of a viral homolog of human interleukin-10 expressed by human cytomegalovirus during the latent phase of infection. J Virol 2008; 82:3736 - 50; http://dx.doi.org/10.1128/JVI.02173-07; PMID: 18216121
  • Avdic S, Cao JZ, Cheung AK, Abendroth A, Slobedman B. Viral interleukin-10 expressed by human cytomegalovirus during the latent phase of infection modulates latently infected myeloid cell differentiation. J Virol 2011; 85:7465 - 71; http://dx.doi.org/10.1128/JVI.00088-11; PMID: 21593144
  • Chang WL, Baumgarth N, Yu D, Barry PA. Human cytomegalovirus-encoded interleukin-10 homolog inhibits maturation of dendritic cells and alters their functionality. J Virol 2004; 78:8720 - 31; http://dx.doi.org/10.1128/JVI.78.16.8720-8731.2004; PMID: 15280480
  • Raftery MJ, Wieland D, Gronewald S, Kraus AA, Giese T, Schönrich G. Shaping phenotype, function, and survival of dendritic cells by cytomegalovirus-encoded IL-10. J Immunol 2004; 173:3383 - 91; PMID: 15322202
  • Raftery MJ, Hitzler M, Winau F, Giese T, Plachter B, Kaufmann SH, et al. Inhibition of CD1 antigen presentation by human cytomegalovirus. J Virol 2008; 82:4308 - 19; http://dx.doi.org/10.1128/JVI.01447-07; PMID: 18287231
  • Hertel L, Lacaille VG, Strobl H, Mellins ED, Mocarski ES. Susceptibility of immature and mature Langerhans cell-type dendritic cells to infection and immunomodulation by human cytomegalovirus. J Virol 2003; 77:7563 - 74; http://dx.doi.org/10.1128/JVI.77.13.7563-7574.2003; PMID: 12805456
  • Lee AW, Hertel L, Louie RK, Burster T, Lacaille V, Pashine A, et al. Human cytomegalovirus alters localization of MHC class II and dendrite morphology in mature Langerhans cells. J Immunol 2006; 177:3960 - 71; PMID: 16951359
  • Lee AW, Wang N, Hornell TM, Harding JJ, Deshpande C, Hertel L, et al. Human cytomegalovirus decreases constitutive transcription of MHC class II genes in mature Langerhans cells by reducing CIITA transcript levels. Mol Immunol 2011; 48:1160 - 7; http://dx.doi.org/10.1016/j.molimm.2011.02.010; PMID: 21458073
  • Kvale EO, Dalgaard J, Lund-Johansen F, Rollag H, Farkas L, Midtvedt K, et al. CD11c+ dendritic cells and plasmacytoid DCs are activated by human cytomegalovirus and retain efficient T cell-stimulatory capability upon infection. Blood 2006; 107:2022 - 9; http://dx.doi.org/10.1182/blood-2005-05-2016; PMID: 16269620
  • Chang WL, Barry PA, Szubin R, Wang D, Baumgarth N. Human cytomegalovirus suppresses type I interferon secretion by plasmacytoid dendritic cells through its interleukin 10 homolog. Virology 2009; 390:330 - 7; http://dx.doi.org/10.1016/j.virol.2009.05.013; PMID: 19524994
  • Cederarv M, Söderberg-Nauclér C, Odeberg J. HCMV infection of PDCs deviates the NK cell response into cytokine-producing cells unable to perform cytotoxicity. Immunobiology 2009; 214:331 - 41; http://dx.doi.org/10.1016/j.imbio.2008.10.009; PMID: 19152985
  • Schneider K, Meyer-Koenig U, Hufert FT. Human cytomegalovirus impairs the function of plasmacytoid dendritic cells in lymphoid organs. PLoS One 2008; 3:e3482; http://dx.doi.org/10.1371/journal.pone.0003482; PMID: 18941519
  • Kurts C, Robinson BW, Knolle PA. Cross-priming in health and disease. Nat Rev Immunol 2010; 10:403 - 14; http://dx.doi.org/10.1038/nri2780; PMID: 20498667
  • Arrode G, Boccaccio C, Lulé J, Allart S, Moinard N, Abastado JP, et al. Incoming human cytomegalovirus pp65 (UL83) contained in apoptotic infected fibroblasts is cross-presented to CD8(+) T cells by dendritic cells. J Virol 2000; 74:10018 - 24; http://dx.doi.org/10.1128/JVI.74.21.10018-10024.2000; PMID: 11024130
  • Tabi Z, Moutaftsi M, Borysiewicz LK. Human cytomegalovirus pp65- and immediate early 1 antigen-specific HLA class I-restricted cytotoxic T cell responses induced by cross-presentation of viral antigens. J Immunol 2001; 166:5695 - 703; PMID: 11313411
  • Mandron M, Martin H, Bonjean B, Lulé J, Tartour E, Davrinche C. Dendritic cell-induced apoptosis of human cytomegalovirus-infected fibroblasts promotes cross-presentation of pp65 to CD8+ T cells. J Gen Virol 2008; 89:78 - 86; http://dx.doi.org/10.1099/vir.0.83278-0; PMID: 18089731
  • Magri G, Muntasell A, Romo N, Sáez-Borderías A, Pende D, Geraghty DE, et al. NKp46 and DNAM-1 NK-cell receptors drive the response to human cytomegalovirus-infected myeloid dendritic cells overcoming viral immune evasion strategies. Blood 2011; 117:848 - 56; http://dx.doi.org/10.1182/blood-2010-08-301374; PMID: 21030563
  • Romo N, Magri G, Muntasell A, Heredia G, Baía D, Angulo A, et al. Natural killer cell-mediated response to human cytomegalovirus-infected macrophages is modulated by their functional polarization. J Leukoc Biol 2011; 90:717 - 26; http://dx.doi.org/10.1189/jlb.0311171; PMID: 21742939
  • Zanghellini F, Boppana SB, Emery VC, Griffiths PD, Pass RF. Asymptomatic primary cytomegalovirus infection: virologic and immunologic features. J Infect Dis 1999; 180:702 - 7; http://dx.doi.org/10.1086/314939; PMID: 10438357
  • Naniche D, Oldstone MB. Generalized immunosuppression: how viruses undermine the immune response. Cell Mol Life Sci 2000; 57:1399 - 407; http://dx.doi.org/10.1007/PL00000625; PMID: 11078019
  • Carney WP, Rubin RH, Hoffman RA, Hansen WP, Healey K, Hirsch MS. Analysis of T lymphocyte subsets in cytomegalovirus mononucleosis. J Immunol 1981; 126:2114 - 6; PMID: 6262407
  • Carney WP, Hirsch MS. Mechanisms of immunosuppression in cytomegalovirus mononucleosis. II. Virus-monocyte interactions. J Infect Dis 1981; 144:47 - 54; http://dx.doi.org/10.1093/infdis/144.1.47; PMID: 6267142
  • Varani S, Rossini G, Mastroianni A, Tammik C, Frascaroli G, Landini MP, et al. High TNF-alpha and IL-8 levels predict low blood dendritic cell counts in primary cytomegalovirus infection. J Clin Virol 2012; 53:360 - 3; http://dx.doi.org/10.1016/j.jcv.2011.12.028; PMID: 22257833
  • Kunitani H, Shimizu Y, Murata H, Higuchi K, Watanabe A. Phenotypic analysis of circulating and intrahepatic dendritic cell subsets in patients with chronic liver diseases. J Hepatol 2002; 36:734 - 41; http://dx.doi.org/10.1016/S0168-8278(02)00062-4; PMID: 12044522
  • Dillon SM, Robertson KB, Pan SC, Mawhinney S, Meditz AL, Folkvord JM, et al. Plasmacytoid and myeloid dendritic cells with a partial activation phenotype accumulate in lymphoid tissue during asymptomatic chronic HIV-1 infection. J Acquir Immune Defic Syndr 2008; 48:1 - 12; http://dx.doi.org/10.1097/QAI.0b013e3181664b60; PMID: 18300699
  • Sallusto F, Schaerli P, Loetscher P, Schaniel C, Lenig D, Mackay CR, et al. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur J Immunol 1998; 28:2760 - 9; http://dx.doi.org/10.1002/(SICI)1521-4141(199809)28:09<2760::AID-IMMU2760>3.0.CO;2-N; PMID: 9754563
  • Duperray A, Mantovani A, Introna M, Dejana E. Endothelial cell regulation of leukocyte infiltration in inflammatory tissues. Mediators Inflamm 1995; 4:322 - 30; http://dx.doi.org/10.1155/S0962935195000524; PMID: 18475659
  • Frascaroli G, Varani S, Mastroianni A, Britton S, Gibellini D, Rossini G, et al. Dendritic cell function in cytomegalovirus-infected patients with mononucleosis. J Leukoc Biol 2006; 79:932 - 40; http://dx.doi.org/10.1189/jlb.0905499; PMID: 16501053
  • Toro AI, Ossa J. PCR activity of CMV in healthy CMV-seropositive individuals: does latency need redefinition?. Res Virol 1996; 147:233 - 8; http://dx.doi.org/10.1016/0923-2516(96)89654-3; PMID: 8837231
  • Heininger A, Jahn G, Engel C, Notheisen T, Unertl K, Hamprecht K. Human cytomegalovirus infections in nonimmunosuppressed critically ill patients. Crit Care Med 2001; 29:541 - 7; http://dx.doi.org/10.1097/00003246-200103000-00012; PMID: 11373417
  • Limaye AP, Kirby KA, Rubenfeld GD, Leisenring WM, Bulger EM, Neff MJ, et al. Cytomegalovirus reactivation in critically ill immunocompetent patients. JAMA 2008; 300:413 - 22; http://dx.doi.org/10.1001/jama.300.4.413; PMID: 18647984
  • Cook CH, Trgovcich J. Cytomegalovirus reactivation in critically ill immunocompetent hosts: a decade of progress and remaining challenges. Antiviral Res 2011; 90:151 - 9; http://dx.doi.org/10.1016/j.antiviral.2011.03.179; PMID: 21439328
  • Razonable RR. Cytomegalovirus infection after liver transplantation: current concepts and challenges. World J Gastroenterol 2008; 14:4849 - 60; http://dx.doi.org/10.3748/wjg.14.4849; PMID: 18756591
  • Nichols WG, Corey L, Gooley T, Davis C, Boeckh M. High risk of death due to bacterial and fungal infection among cytomegalovirus (CMV)-seronegative recipients of stem cell transplants from seropositive donors: evidence for indirect effects of primary CMV infection. J Infect Dis 2002; 185:273 - 82; http://dx.doi.org/10.1086/338624; PMID: 11807708
  • Fishman JA, Rubin RH. Infection in organ-transplant recipients. N Engl J Med 1998; 338:1741 - 51; http://dx.doi.org/10.1056/NEJM199806113382407; PMID: 9624195
  • Sun Q, Hall EC, Huang Y, Chen P, Dibadj K, Murawski M, et al. Pre-transplant myeloid dendritic cell deficiency associated with cytomegalovirus infection and death after kidney transplantation. Transpl Infect Dis 2012; http://dx.doi.org/10.1111/j.1399-3062.2012.00750.x; PMID: 22672201
  • Varani S, Frascaroli G, Gibellini D, Potena L, Lazzarotto T, Lemoli RM, et al. Impaired dendritic cell immunophenotype and function in heart transplant patients undergoing active cytomegalovirus infection. Transplantation 2005; 79:219 - 27; http://dx.doi.org/10.1097/01.TP.0000147359.63158.29; PMID: 15665771
  • Mezger M, Steffens M, Semmler C, Arlt EM, Zimmer M, Kristjanson GI, et al. Investigation of promoter variations in dendritic cell-specific ICAM3-grabbing non-integrin (DC-SIGN) (CD209) and their relevance for human cytomegalovirus reactivation and disease after allogeneic stem-cell transplantation. Clin Microbiol Infect 2008; 14:228 - 34; http://dx.doi.org/10.1111/j.1469-0691.2007.01902.x; PMID: 18076668
  • Fishman JA, Emery V, Freeman R, Pascual M, Rostaing L, Schlitt HJ, et al. Cytomegalovirus in transplantation - challenging the status quo. Clin Transplant 2007; 21:149 - 58; http://dx.doi.org/10.1111/j.1399-0012.2006.00618.x; PMID: 17425738
  • Dzabic M, Rahbar A, Yaiw KC, Naghibi M, Religa P, Fellström B, et al. Intragraft cytomegalovirus protein expression is associated with reduced renal allograft survival. Clin Infect Dis 2011; 53:969 - 76; http://dx.doi.org/10.1093/cid/cir619; PMID: 21960711
  • Varani S, Landini MP. Cytomegalovirus-induced immunopathology and its clinical consequences. Herpesviridae 2011; 2:6; http://dx.doi.org/10.1186/2042-4280-2-6; PMID: 21473750
  • Soderberg C, Sumitran-Karuppan S, Ljungman P, Moller E. CD13-specific autoimmunity in cytomegalovirus-infected immunocompromised patients. Transplantation 1996; 61:594 - 600; http://dx.doi.org/10.1097/00007890-199602270-00014; PMID: 8610387
  • Rahbar A, Boström L, Söderberg-Naucler C. Detection of cytotoxic CD13-specific autoantibodies in sera from patients with ulcerative colitis and Crohn’s disease. J Autoimmun 2006; 26:155 - 64; http://dx.doi.org/10.1016/j.jaut.2006.02.003; PMID: 16584867
  • Jego G, Palucka AK, Blanck JP, Chalouni C, Pascual V, Banchereau J. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 2003; 19:225 - 34; http://dx.doi.org/10.1016/S1074-7613(03)00208-5; PMID: 12932356
  • Carvalho A, Cunha C, Carotti A, Aloisi T, Guarrera O, Di Ianni M, et al. Polymorphisms in Toll-like receptor genes and susceptibility to infections in allogeneic stem cell transplantation. Exp Hematol 2009; 37:1022 - 9; http://dx.doi.org/10.1016/j.exphem.2009.06.004; PMID: 19539691
  • Nahum A, Dadi H, Bates A, Roifman CM. The L412F variant of Toll-like receptor 3 (TLR3) is associated with cutaneous candidiasis, increased susceptibility to cytomegalovirus, and autoimmunity. J Allergy Clin Immunol 2011; 127:528 - 31; http://dx.doi.org/10.1016/j.jaci.2010.09.031; PMID: 21093032
  • Varani S, Mastroianni A, Frascaroli G, Tammik C, Rahbar A, Christensson M, et al. Generalized Wegener’s granulomatosis in an immunocompetent adult after cytomegalovirus mononucleosis and bacterial urinary tract infection. Arthritis Rheum 2009; 60:1558 - 62; http://dx.doi.org/10.1002/art.24487; PMID: 19404959
  • Hsieh AH, Jhou YJ, Liang CT, Chang M, Wang SL. Fragment of tegument protein pp65 of human cytomegalovirus induces autoantibodies in BALB/c mice. Arthritis Res Ther 2011; 13:R162; http://dx.doi.org/10.1186/ar3481; PMID: 21989080
  • Chang M, Pan MR, Chen DY, Lan JL. Human cytomegalovirus pp65 lower matrix protein: a humoral immunogen for systemic lupus erythematosus patients and autoantibody accelerator for NZB/W F1 mice. Clin Exp Immunol 2006; 143:167 - 79; http://dx.doi.org/10.1111/j.1365-2249.2005.02974.x; PMID: 16367948
  • Baccala R, Hoebe K, Kono DH, Beutler B, Theofilopoulos AN. TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat Med 2007; 13:543 - 51; http://dx.doi.org/10.1038/nm1590; PMID: 17479100
  • Kono DH, Haraldsson MK, Lawson BR, Pollard KM, Koh YT, Du X, et al. Endosomal TLR signaling is required for anti-nucleic acid and rheumatoid factor autoantibodies in lupus. Proc Natl Acad Sci USA 2009; 106:12061 - 6; http://dx.doi.org/10.1073/pnas.0905441106; PMID: 19574451
  • Xu X, Bergman P, Willows T, Tammik C, Sund M, Hökfelt T, et al. CMV-associated encephalitis and antineuronal autoantibodies - a case report. BMC Neurol 2012; 12:87; http://dx.doi.org/10.1186/1471-2377-12-87; PMID: 22947340
  • Zucchini N, Bessou G, Traub S, Robbins SH, Uematsu S, Akira S, et al. Cutting edge: Overlapping functions of TLR7 and TLR9 for innate defense against a herpesvirus infection. J Immunol 2008; 180:5799 - 803; PMID: 18424698
  • Rahbar A, Boström L, Lagerstedt U, Magnusson I, Söderberg-Naucler C, Sundqvist VA. Evidence of active cytomegalovirus infection and increased production of IL-6 in tissue specimens obtained from patients with inflammatory bowel diseases. Inflamm Bowel Dis 2003; 9:154 - 61; http://dx.doi.org/10.1097/00054725-200305000-00002; PMID: 12792220
  • Baumgart DC, Metzke D, Schmitz J, Scheffold A, Sturm A, Wiedenmann B, et al. Patients with active inflammatory bowel disease lack immature peripheral blood plasmacytoid and myeloid dendritic cells. Gut 2005; 54:228 - 36; http://dx.doi.org/10.1136/gut.2004.040360; PMID: 15647187
  • Geist LJ, Monick MM, Stinski MF, Hunninghake GW. The immediate early genes of human cytomegalovirus upregulate tumor necrosis factor-alpha gene expression. J Clin Invest 1994; 93:474 - 8; http://dx.doi.org/10.1172/JCI116995; PMID: 8113386
  • Yamazaki S, Steinman RM. Dendritic cells as controllers of antigen-specific Foxp3+ regulatory T cells. J Dermatol Sci 2009; 54:69 - 75; http://dx.doi.org/10.1016/j.jdermsci.2009.02.001; PMID: 19286352
  • Ngoma AM, Ikeda K, Hashimoto Y, Mochizuki K, Takahashi H, Sano H, et al. Impaired regulatory T cell reconstitution in patients with acute graft-versus-host disease and cytomegalovirus infection after allogeneic bone marrow transplantation. Int J Hematol 2012; 95:86 - 94; http://dx.doi.org/10.1007/s12185-011-0976-7; PMID: 22160825
  • Pastore D, Delia M, Mestice A, Perrone T, Carluccio P, Gaudio F, et al. Recovery of CMV-specific CD8+ T cells and Tregs after allogeneic peripheral blood stem cell transplantation. Biol Blood Marrow Transplant 2011; 17:550 - 7; http://dx.doi.org/10.1016/j.bbmt.2010.04.011; PMID: 20457268
  • Nguyen VH, Shashidhar S, Chang DS, Ho L, Kambham N, Bachmann M, et al. The impact of regulatory T cells on T-cell immunity following hematopoietic cell transplantation. Blood 2008; 111:945 - 53; http://dx.doi.org/10.1182/blood-2007-07-103895; PMID: 17916743
  • Bruinsma M, Wils EJ, Löwenberg B, Cornelissen JJ, Braakman E. The impact of CD4+Foxp3+ Treg on immunity to murine cytomegalovirus after bone marrow transplantation depends on the peripheral or thymic source of T cell regeneration. Transpl Immunol 2010; 24:9 - 16; http://dx.doi.org/10.1016/j.trim.2010.08.003; PMID: 20801217
  • Li YN, Liu XL, Huang F, Zhou H, Huang YJ, Fang F. CD4+CD25+ regulatory T cells suppress the immune responses of mouse embryo fibroblasts to murine cytomegalovirus infection. Immunol Lett 2010; 131:131 - 8; http://dx.doi.org/10.1016/j.imlet.2010.03.011; PMID: 20381532
  • Streblow DN, Orloff SL, Nelson JA. Do pathogens accelerate atherosclerosis?. J Nutr 2001; 131:2798S - 804S; PMID: 11584110
  • Libby P. Inflammation in atherosclerosis. Nature 2002; 420:868 - 74; http://dx.doi.org/10.1038/nature01323; PMID: 12490960
  • Bobryshev YV, Lord RS, Pärsson H. Immunophenotypic analysis of the aortic aneurysm wall suggests that vascular dendritic cells are involved in immune responses. Cardiovasc Surg 1998; 6:240 - 9; http://dx.doi.org/10.1016/S0967-2109(97)00168-3; PMID: 9705095
  • Millonig G, Malcom GT, Wick G. Early inflammatory-immunological lesions in juvenile atherosclerosis from the Pathobiological Determinants of Atherosclerosis in Youth (PDAY)-study. Atherosclerosis 2002; 160:441 - 8; http://dx.doi.org/10.1016/S0021-9150(01)00596-2; PMID: 11849669
  • Yilmaz A, Lochno M, Traeg F, Cicha I, Reiss C, Stumpf C, et al. Emergence of dendritic cells in rupture-prone regions of vulnerable carotid plaques. Atherosclerosis 2004; 176:101 - 10; http://dx.doi.org/10.1016/j.atherosclerosis.2004.04.027; PMID: 15306181
  • Pryshchep O, Ma-Krupa W, Younge BR, Goronzy JJ, Weyand CM. Vessel-specific Toll-like receptor profiles in human medium and large arteries. Circulation 2008; 118:1276 - 84; http://dx.doi.org/10.1161/CIRCULATIONAHA.108.789172; PMID: 18765390
  • Niessner A, Sato K, Chaikof EL, Colmegna I, Goronzy JJ, Weyand CM. Pathogen-sensing plasmacytoid dendritic cells stimulate cytotoxic T-cell function in the atherosclerotic plaque through interferon-alpha. Circulation 2006; 114:2482 - 9; http://dx.doi.org/10.1161/CIRCULATIONAHA.106.642801; PMID: 17116765
  • Melnick JL, Hu C, Burek J, Adam E, DeBakey ME. Cytomegalovirus DNA in arterial walls of patients with atherosclerosis. J Med Virol 1994; 42:170 - 4; http://dx.doi.org/10.1002/jmv.1890420213; PMID: 8158112
  • Melnick JL, Petrie BL, Dreesman GR, Burek J, McCollum CH, DeBakey ME. Cytomegalovirus antigen within human arterial smooth muscle cells. Lancet 1983; 2:644 - 7; http://dx.doi.org/10.1016/S0140-6736(83)92529-1; PMID: 6136795
  • Gredmark S, Jonasson L, Van Gosliga D, Ernerudh J, Söderberg-Nauclér C. Active cytomegalovirus replication in patients with coronary disease. Scand Cardiovasc J 2007; 41:230 - 4; http://dx.doi.org/10.1080/14017430701383755; PMID: 17680510
  • Roberts ET, Haan MN, Dowd JB, Aiello AE. Cytomegalovirus antibody levels, inflammation, and mortality among elderly Latinos over 9 years of follow-up. Am J Epidemiol 2010; 172:363 - 71; http://dx.doi.org/10.1093/aje/kwq177; PMID: 20660122
  • Simanek AM, Dowd JB, Pawelec G, Melzer D, Dutta A, Aiello AE. Seropositivity to cytomegalovirus, inflammation, all-cause and cardiovascular disease-related mortality in the United States. PLoS One 2011; 6:e16103; http://dx.doi.org/10.1371/journal.pone.0016103; PMID: 21379581
  • Prösch S, Staak K, Stein J, Liebenthal C, Stamminger T, Volk HD, et al. Stimulation of the human cytomegalovirus IE enhancer/promoter in HL-60 cells by TNFalpha is mediated via induction of NF-kappaB. Virology 1995; 208:197 - 206; http://dx.doi.org/10.1006/viro.1995.1143; PMID: 11831701
  • van Leeuwen EM, Remmerswaal EB, Vossen MT, Rowshani AT, Wertheim-van Dillen PM, van Lier RA, et al. Emergence of a CD4+CD28- granzyme B+, cytomegalovirus-specific T cell subset after recovery of primary cytomegalovirus infection. J Immunol 2004; 173:1834 - 41; PMID: 15265915
  • Liuzzo G, Goronzy JJ, Yang H, Kopecky SL, Holmes DR, Frye RL, et al. Monoclonal T-cell proliferation and plaque instability in acute coronary syndromes. Circulation 2000; 101:2883 - 8; http://dx.doi.org/10.1161/01.CIR.101.25.2883; PMID: 10869258
  • Looney RJ, Falsey A, Campbell D, Torres A, Kolassa J, Brower C, et al. Role of cytomegalovirus in the T cell changes seen in elderly individuals. Clin Immunol 1999; 90:213 - 9; http://dx.doi.org/10.1006/clim.1998.4638; PMID: 10080833
  • Hazzan M, Labalette M, Noel C, Lelievre G, Dessaint JP. Recall response to cytomegalovirus in allograft recipients: mobilization of CD57+, CD28+ cells before expansion of CD57+, CD28- cells within the CD8+ T lymphocyte compartment. Transplantation 1997; 63:693 - 8; http://dx.doi.org/10.1097/00007890-199703150-00014; PMID: 9075840
  • Fasth AE, Dastmalchi M, Rahbar A, Salomonsson S, Pandya JM, Lindroos E, et al. T cell infiltrates in the muscles of patients with dermatomyositis and polymyositis are dominated by CD28null T cells. J Immunol 2009; 183:4792 - 9; http://dx.doi.org/10.4049/jimmunol.0803688; PMID: 19752224
  • Tovar-Salazar A, Patterson-Bartlett J, Jesser R, Weinberg A. Regulatory function of cytomegalovirus-specific CD4+CD27-CD28- T cells. Virology 2010; 398:158 - 67; http://dx.doi.org/10.1016/j.virol.2009.11.038; PMID: 20034645
  • Appay V, Dunbar PR, Callan M, Klenerman P, Gillespie GM, Papagno L, et al. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat Med 2002; 8:379 - 85; http://dx.doi.org/10.1038/nm0402-379; PMID: 11927944
  • Fletcher JM, Vukmanovic-Stejic M, Dunne PJ, Birch KE, Cook JE, Jackson SE, et al. Cytomegalovirus-specific CD4+ T cells in healthy carriers are continuously driven to replicative exhaustion. J Immunol 2005; 175:8218 - 25; PMID: 16339561