Circulating dendritic cells isolated from healthy seropositive donors are sites of human cytomegalovirus reactivation in vivo

Journal of Virology

Volumn 87, Issue 19, 2013, Pages 10660-10667

  Reeves, Matthew B ^a   Sinclair, John H ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BLOOD; BONE MARROW CELL; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CELL SURFACE; CONTROLLED STUDY; DENDRITIC CELL; DONOR; EX VIVO STUDY; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC SIMILARITY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; HUMAN TISSUE; IMMEDIATE EARLY GENE; IN VIVO STUDY; INFLAMMATION; MONOCYTE; MYELOID PROGENITOR CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PURIFICATION; VIRUS CARRIER; VIRUS GENOME; VIRUS LATENCY; VIRUS REACTIVATION;

CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DENDRITIC CELLS; DNA, VIRAL; FIBROBLASTS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; FORESKIN; HUMANS; MALE; POLYMERASE CHAIN REACTION; SEROEPIDEMIOLOGIC STUDIES; VIRUS ACTIVATION; VIRUS LATENCY;

EID: 84886041005     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01539-13     Document Type: Article

References (54)

1. Limaye AP, Kirby KA, Rubenfeld GD, Leisenring WM, Bulger EM, Neff MJ, Gibran NS, Huang ML, Santo Hayes TK, Corey L, Boeckh M. 2008. Cytomegalovirus reactivation in critically ill immunocompetent patients. JAMA 300:413-422.
2. Peggs KS, Mackinnon S. 2004. Cytomegalovirus: the role of CMV posthaematopoietic stem cell transplantation. Int. J. Biochem. Cell Biol. 36: 695-701.
3. Revello MG, Gerna G. 2004. Pathogenesis and prenatal diagnosis of human cytomegalovirus infection. J. Clin. Virol. 29:71-83.
4. Goodrum FD, Jordan CT, High K, Shenk T. 2002. Human cytomegalovirus gene expression during infection of primary hematopoietic progenitor cells: a model for latency. Proc. Natl. Acad. Sci. U.S.A. 99:16255-16260.
5. Hahn G, Jores R, Mocarski ES. 1998. Cytomegalovirus remains latent in a common precursor of dendritic and myeloid cells. Proc. Natl. Acad. Sci. U.S.A. 95:3937-3942.
6. + bone marrow progenitors. J. Gen. Virol. 77(Part 12):3099-3102.
7. Sindre H, Tjoonnfjord GE, Rollag H, Ranneberg-Nilsen T, Veiby OP, Beck S, Degre M, Hestdal K. 1996. Human cytomegalovirus suppression of and latency in early hematopoietic progenitor cells. Blood 88:4526-4533.
8. Zhuravskaya T, Maciejewski JP, Netski DM, Bruening E, Mackintosh FR, St Jeor S. 1997. Spread of human cytomegalovirus (HCMV) after infection of human hematopoietic progenitor cells: model of HCMV latency. Blood 90:2482-2491.
9. Bevan IS, Daw RA, Day PJ, Ala FA, Walker MR. 1991. Polymerase chain reaction for detection of human cytomegalovirus infection in a blood donor population. Br. J. Haematol. 78:94-99.
10. Kondo K, Kaneshima H, Mocarski ES. 1994. Human cytomegalovirus latent infection of granulocyte-macrophage progenitors. Proc. Natl. Acad. Sci. U.S.A. 91:11879-11883.
11. Prosch S, Docke WD, Reinke P, Volk HD, Kruger DH. 1999. Human cytomegalovirus reactivation in bone-marrow-derived granulocyte/ monocyte progenitor cells and mature monocytes. Intervirology 42:308-313.
12. Reeves MB, MacAry PA, Lehner PJ, Sissons JG, Sinclair JH. 2005. Latency, chromatin remodeling, and reactivation of human cytomegalovirus in the dendritic cells of healthy carriers. Proc. Natl. Acad. Sci. U.S.A. 102:4140-4145.
13. Slobedman B, Mocarski ES. 1999. Quantitative analysis of latent human cytomegalovirus. J. Virol. 73:4806-4812.
14. Taylor-Wiedeman J, Sissons JG, Borysiewicz LK, Sinclair JH. 1991. Monocytes are a major site of persistence of human cytomegalovirus in peripheral blood mononuclear cells. J. Gen. Virol. 72(Part 9):2059-2064.
15. Slobedman B, Cao JZ, Avdic S, Webster B, McAllery S, Cheung AK, Tan JC, Abendroth A. 2010. Human cytomegalovirus latent infection and associated viral gene expression. Future Microbiol. 5:883-900.
16. De Witte T, Schattenberg A, Van Dijk BA, Galama J, Olthuis H, Van der Meer JW, Kunst VA. 1990. Prevention of primary cytomegalovirus infection after allogeneic bone marrow transplantation by using leukocyte-poor random blood products from cytomegalovirus-unscreened blood-bank donors. Transplantation 50:964-968.
17. Gilbert GL, Hayes K, Hudson IL, James J. 1989. Prevention of transfusion-acquired cytomegalovirus infection in infants by blood filtration to remove leucocytes. Neonatal Cytomegalovirus Infection Study Group. Lancet i:1228-1231.
18. Jordan MC. 1983. Latent infection and the elusive cytomegalovirus. Rev. Infect. Dis. 5:205-215.
19. Bego MG, St Jeor S. 2006. Human cytomegalovirus infection of cells of hematopoietic origin: HCMV-induced immunosuppression, immune evasion, and latency. Exp. Hematol. 34:555-570.
20. + experimental latency model. J. Virol. 86:8507-8515.
21. Reeves MB, Compton T. 2011. 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. 85:12750-12758.
22. Reeves MB, Lehner PJ, Sissons JG, Sinclair JH. 2005. An in vitro model for the regulation of human cytomegalovirus latency and reactivation in dendritic cells by chromatin remodelling. J. Gen. Virol. 86:2949-2954.
23. Söderbérg-Naucler C, Fish KN, Nelson JA. 1997. Reactivation of latent human cytomegalovirus by allogeneic stimulation of blood cells from healthy donors. Cell 91:119-126.
24. Geissmann F, Prost C, Monnet JP, Dy M, Brousse N, Hermine O. 1998. Transforming growth factor beta1, in the presence of granulocyte/ macrophage colony-stimulating factor and interleukin 4, induces differentiation of human peripheral blood monocytes into dendritic Langerhans cells. J. Exp. Med. 187:961-966.
25. Grassi F, Dezutter-Dambuyant C, McIlroy D, Jacquet C, Yoneda K, Imamura S, Boumsell L, Schmitt D, Autran B, Debre P, Hosmalin A. 1998. Monocyte-derived dendritic cells have a phenotype comparable to that of dermal dendritic cells and display ultrastructural granules distinct from Birbeck granules. J. Leukoc. Biol. 64:484-493.
26. MacAry PA, Lindsay M, Scott MA, Craig JI, Luzio JP, Lehner PJ. 2001. Mobilization of MHC class I molecules from late endosomes to the cell surface following activation of CD34-derived human Langerhans cells. Proc. Natl. Acad. Sci. U.S.A. 98:3982-3987.
27. Merad M, Ginhoux F, Collin M. 2008. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat. Rev. Immunol. 8:935-947.
28. Peiser M, Wanner R, Kolde G. 2004. Human epidermal Langerhans cells differ from monocyte-derived Langerhans cells in CD80 expression and in secretion of IL-12 after CD40 cross-linking. J. Leukoc. Biol. 76:616-622.
29. Sallusto F, Lanzavecchia A. 1994. 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. 179:1109-1118.
30. Chang WL, Baumgarth N, Yu D, Barry PA. 2004. Human cytomegalovirus-encoded interleukin-10 homolog inhibits maturation of dendritic cells and alters their functionality. J. Virol. 78:8720-8731.
31. Grigoleit U, Riegler S, Einsele H, Laib Sampaio K, Jahn G, Hebart H, Brossart P, Frank F, Sinzger C. 2002. Human cytomegalovirus induces a direct inhibitory effect on antigen presentation by monocyte-derived immature dendritic cells. Br. J. Haematol. 119:189-198.
32. Hertel L, Lacaille VG, Strobl H, Mellins ED, Mocarski ES. 2003. Susceptibility of immature and mature Langerhans cell-type dendritic cells to infection and immunomodulation by human cytomegalovirus. J. Virol. 77:7563-7574.
33. Moutaftsi M, Brennan P, Spector SA, Tabi Z. 2004. Impaired lymphoid chemokine-mediated migration due to a block on the chemokine receptor switch in human cytomegalovirus-infected dendritic cells. J. Virol. 78: 3046-3054.
34. Moutaftsi M, Mehl AM, Borysiewicz LK, Tabi Z. 2002. Human cytomegalovirus inhibits maturation and impairs function of monocytederived dendritic cells. Blood 99:2913-2921.
35. Raftery MJ, Schwab M, Eibert SM, Samstag Y, Walczak H, Schonrich G. 2001. Targeting the function of mature dendritic cells by human cytomegalovirus: a multilayered viral defense strategy. Immunity 15:997-1009.
36. Sénéchal B, Boruchov AM, Reagan JL, Hart DN, Young JW. 2004. Infection of mature monocyte-derived dendritic cells with human cytomegalovirus inhibits stimulation of T-cell proliferation via the release of soluble CD83. Blood 103:4207-4215.
37. Varani S, Frascaroli G, Homman-Loudiyi M, Feld S, Landini MP, Soderberg-Naucler C. 2005. Human cytomegalovirus inhibits the migration of immature dendritic cells by down-regulating cell-surface CCR1 and CCR5. J. Leukoc. Biol. 77:219-228.
38. + dendritic cells and plasmacytoid DCs are activated by human cytomegalovirus and retain efficient T cell-stimulatory capability upon infection. Blood 107:2022-2029.
39. Prosch S, Wuttke R, Kruger DH, Volk HD. 2002. NF-kappaB-a potential therapeutic target for inhibition of human cytomegalovirus (re)activation? Biol. Chem. 383:1601-1609.
40. MacDonald KP, Munster DJ, Clark GJ, Dzionek A, Schmitz J, Hart DN. 2002. Characterization of human blood dendritic cell subsets. Blood 100: 4512-4520.
41. Robinson SP, Patterson S, English N, Davies D, Knight SC, Reid CD. 1999. Human peripheral blood contains two distinct lineages of dendritic cells. Eur. J. Immunol. 29:2769-2778.
42. Taylor-Wiedeman J, Sissons P, Sinclair J. 1994. Induction of endogenous human cytomegalovirus gene expression after differentiation of monocytes from healthy carriers. J. Virol. 68:1597-1604.
43. Weekes MP, Tan SY, Poole E, Talbot S, Antrobus R, Smith DL, Montag C, Gygi SP, Sinclair JH, Lehner PJ. 2013. Latency-associated degradation of the MRP1 drug transporter during latent human cytomegalovirus infection. Science 340:199-202.
44. Humar A, St Louis P, Mazzulli T, McGeer A, Lipton J, Messner H, MacDonald KS. 1999. Elevated serum cytokines are associated with cytomegalovirus infection and disease in bone marrow transplant recipients. J. Infect. Dis. 179:484-488.
45. Sinclair J, Sissons P. 2006. Latency and reactivation of human cytomegalovirus. J. Gen. Virol. 87:1763-1779.
46. Reinke P, Prosch S, Kern F, Volk HD. 1999. Mechanisms of human cytomegalovirus (HCMV) (re)activation and its impact on organ transplant patients. Transpl. Infect. Dis. 1:157-164.
47. + monocytes. Proc. Natl. Acad. Sci. U.S.A. 107:20039-20044.
48. Khaiboullina SF, Maciejewski JP, Crapnell K, Spallone PA, Dean Stock A, Pari GS, Zanjani ED, Jeor SS. 2004. Human cytomegalovirus persists in myeloid progenitors and is passed to the myeloid progeny in a latent form. Br. J. Haematol. 126:410-417.
49. Slobedman B, Mocarski ES, Arvin AM, Mellins ED, Abendroth A. 2002. Latent cytomegalovirus down-regulates major histocompatibility complex class II expression on myeloid progenitors. Blood 100:2867-2873.
50. Riegler S, Hebart H, Einsele H, Brossart P, Jahn G, Sinzger C. 2000. Monocyte-derived dendritic cells are permissive to the complete replicative cycle of human cytomegalovirus. J. Gen. Virol. 81:393-399.
51. Kondo K, Xu J, Mocarski ES. 1996. Human cytomegalovirus latent gene expression in granulocyte-macrophage progenitors in culture and in seropositive individuals. Proc. Natl. Acad. Sci. U.S.A. 93:11137-11142.
52. Taylor-Wiedeman J, Hayhurst GP, Sissons JG, Sinclair JH. 1993. Polymorphonuclear cells are not sites of persistence of human cytomegalovirus in healthy individuals. J. Gen. Virol. 74(Part 2):265-268.
53. Jackson SE, Mason GM, Wills MR. 2011. Human cytomegalovirus immunity and immune evasion. Virus Res. 157:151-160.
54. Minton EJ, Tysoe C, Sinclair JH, Sissons JG. 1994. Human cytomegalovirus infection of the monocyte/macrophage lineage in bone marrow. J. Virol. 68:4017-4021.