1887

Abstract

Human cytomegalovirus (HCMV) persists as a subclinical, lifelong infection in the normal human host, maintained at least in part by its carriage in the absence of detectable infectious virus – the hallmark of latent infection. Reactivation from latency in immunocompromised individuals, in contrast, often results in serious disease. Latency and reactivation are defining characteristics of the herpesviruses and key to understanding their biology. However, the precise cellular sites in which HCMV is carried and the mechanisms regulating its latency and reactivation during natural infection remain poorly understood. This review will detail our current knowledge of where HCMV is carried in healthy individuals, which viral genes are expressed upon carriage of the virus and what effect this has on cellular gene expression. It will also address the accumulating evidence suggesting that reactivation of HCMV from latency appears to be linked intrinsically to the differentiation status of the myeloid cell, and how the cellular mechanisms that normally control host gene expression play a critical role in the differential regulation of viral gene expression during latency and reactivation.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81891-0
2006-07-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/7/1763.html?itemId=/content/journal/jgv/10.1099/vir.0.81891-0&mimeType=html&fmt=ahah

References

  1. Adams, A. ( 1987; ). Replication of latent Epstein-Barr virus genomes in Raji cells. J Virol 61, 1743–1746.
    [Google Scholar]
  2. Adams, D. O. & Hamilton, T. A. ( 1987; ). Molecular transductional mechanisms by which IFN gamma and other signals regulate macrophage development. Immunol Rev 97, 5–27.[CrossRef]
    [Google Scholar]
  3. Adler, S. P. ( 1983; ). Transfusion-associated cytomegalovirus infections. Rev Infect Dis 5, 977–993.[CrossRef]
    [Google Scholar]
  4. Amon, W. & Farrell, P. J. ( 2005; ). Reactivation of Epstein-Barr virus from latency. Rev Med Virol 15, 149–156.[CrossRef]
    [Google Scholar]
  5. Apperley, J. F., Dowding, C., Hibbin, J., Buiter, J., Matutes, E., Sissons, P. J., Gordon, M. & Goldman, J. M. ( 1989; ). The effect of cytomegalovirus on hemopoiesis: in vitro evidence for selective infection of marrow stromal cells. Exp Hematol 17, 38–45.
    [Google Scholar]
  6. Arthur, J. L., Scarpini, C. G., Connor, V., Lachmann, R. H., Tolkovsky, A. M. & Efstathiou, S. ( 2001; ). Herpes simplex virus type 1 promoter activity during latency establishment, maintenance, and reactivation in primary dorsal root neurons in vitro. J Virol 75, 3885–3895.[CrossRef]
    [Google Scholar]
  7. Arvin, A. M., Fast, P., Myers, M., Plotkin, S. & Rabinovich, R. ( 2004; ). Vaccine development to prevent cytomegalovirus disease: report from the National Vaccine Advisory Committee. Clin Infect Dis 39, 233–239.[CrossRef]
    [Google Scholar]
  8. Bain, M. & Sinclair, J. ( 2005; ). Targeted inhibition of the transcription factor YY1 in an embryonal carcinoma cell line results in retarded cell growth, elevated levels of p53 but no increase in apoptotic cell death. Eur J Cell Biol 84, 543–553.[CrossRef]
    [Google Scholar]
  9. Bain, M., Mendelson, M. & Sinclair, J. ( 2003; ). Ets-2 Repressor Factor (ERF) mediates repression of the human cytomegalovirus major immediate-early promoter in undifferentiated non-permissive cells. J Gen Virol 84, 41–49.[CrossRef]
    [Google Scholar]
  10. Banchereau, J., Briere, F., Caux, C., Davoust, J., Lebecque, S., Liu, Y.-J., Pulendran, B. & Palucka, K. ( 2000; ). Immunobiology of dendritic cells. Annu Rev Immunol 18, 767–811.[CrossRef]
    [Google Scholar]
  11. Bannister, A. J., Zegerman, P., Partridge, J. F., Miska, E. A., Thomas, J. O., Allshire, R. C. & Kouzarides, T. ( 2001; ). Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120–124.[CrossRef]
    [Google Scholar]
  12. Bego, M., Maciejewski, J., Khaiboullina, S., Pari, G. & St Jeor, S. ( 2005; ). Characterization of an antisense transcript spanning the UL81-82 locus of human cytomegalovirus. J Virol 79, 11022–11034.[CrossRef]
    [Google Scholar]
  13. Beisser, P. S., Laurent, L., Virelizier, J.-L. & Michelson, S. ( 2001; ). Human cytomegalovirus chemokine receptor gene US28 is transcribed in latently infected THP-1 monocytes. J Virol 75, 5949–5957.[CrossRef]
    [Google Scholar]
  14. Bitsch, A., Kirchner, H., Dupke, R. & Bein, G. ( 1992; ). Failure to detect human cytomegalovirus DNA in peripheral blood leukocytes of healthy blood donors by the polymerase chain reaction. Transfusion 32, 612–617.[CrossRef]
    [Google Scholar]
  15. Bolovan-Fritts, C. A., Mocarski, E. S. & Wiedeman, J. A. ( 1999; ). Peripheral blood CD14+ cells from healthy subjects carry a circular conformation of latent cytomegalovirus genome. Blood 93, 394–398.
    [Google Scholar]
  16. Borysiewicz, L. K., Hickling, J. K., Graham, S., Sinclair, J., Cranage, M. P., Smith, G. L. & Sissons, J. G. P. ( 1988; ). Human cytomegalovirus-specific cytotoxic T cells. Relative frequency of stage-specific CTL recognizing the 72-kD immediate early protein and glycoprotein B expressed by recombinant vaccinia viruses. J Exp Med 168, 919–931.[CrossRef]
    [Google Scholar]
  17. Boshart, M., Weber, F., Jahn, G., Dorsch-Hasler, K., Fleckenstein, B. & Schaffner, W. ( 1985; ). A very strong enhancer is located upstream of an immediate early gene of human cytomegalovirus. Cell 41, 521–530.[CrossRef]
    [Google Scholar]
  18. Castillo, J. P. & Kowalik, T. F. ( 2002; ). Human cytomegalovirus immediate early proteins and cell growth control. Gene 290, 19–34.[CrossRef]
    [Google Scholar]
  19. Cha, T.-A., Tom, E., Kemble, G. W., Duke, G. M., Mocarski, E. S. & Spaete, R. R. ( 1996; ). Human cytomegalovirus clinical isolates carry at least 19 genes not found in laboratory strains. J Virol 70, 78–83.
    [Google Scholar]
  20. Challacombe, J. F., Rechtsteiner, A., Gottardo, R., Rocha, L. M., Browne, E. P., Shenk, T., Altherr, M. R. & Brettin, T. S. ( 2004; ). Evaluation of the host transcriptional response to human cytomegalovirus infection. Physiol Genomics 18, 51–62.[CrossRef]
    [Google Scholar]
  21. Colberg-Poley, A. M. ( 1996; ). Functional roles of immediate early proteins encoded by the human cytomegalovirus UL36-38, UL115-119, TRS1/IRS1 and US3 loci. Intervirology 39, 350–360.
    [Google Scholar]
  22. de Graan-Hentzen, Y. C., Gratama, J. W., Mudde, G. C. & 7 other authors ( 1989; ). Prevention of primary cytomegalovirus infection in patients with hematologic malignancies by intensive white cell depletion of blood products. Transfusion 29, 757–760.[CrossRef]
    [Google Scholar]
  23. Drew, W. L. ( 1988; ). Diagnosis of cytomegalovirus infection. Rev Infect Dis 10 (Suppl. 3), S468–S476.[CrossRef]
    [Google Scholar]
  24. Eberharter, A. & Becker, P. B. ( 2002; ). Histone acetylation: a switch between repressive and permissive chromatin. EMBO Rep 3, 224–229.[CrossRef]
    [Google Scholar]
  25. Einhorn, L., Einhorn, S. & Wahren, B. ( 1985; ). Interferon induction in human leukocytes after in vitro exposure to cytomegalovirus or Epstein-Barr virus. Intervirology 23, 140–149.[CrossRef]
    [Google Scholar]
  26. Epstein, S. E., Speir, E., Zhou, Y. F., Guetta, E., Leon, M. & Finkel, T. ( 1996; ). The role of infection in restenosis and atherosclerosis: focus on cytomegalovirus. Lancet 348 (Suppl. 1), S13–S17.
    [Google Scholar]
  27. Everett, R. D. ( 2000; ). ICP0, a regulator of herpes simplex virus during lytic and latent infection. Bioessays 22, 761–770.[CrossRef]
    [Google Scholar]
  28. Fish, K. N., Britt, W. & Nelson, J. A. ( 1996; ). A novel mechanism for persistence of human cytomegalovirus in macrophages. J Virol 70, 1855–1862.
    [Google Scholar]
  29. Fortunato, E. A., McElroy, A. K., Sanchez, I. & Spector, D. H. ( 2000; ). Exploitation of cellular signaling and regulatory pathways by human cytomegalovirus. Trends Microbiol 8, 111–119.[CrossRef]
    [Google Scholar]
  30. Gerna, G., Percivalle, E., Lilleri, D., Lozza, L., Fornara, C., Hahn, G., Baldanti, F. & Revello, M. G. ( 2005; ). 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 86, 275–284.[CrossRef]
    [Google Scholar]
  31. Ghazal, P., Lubon, H., Reynolds-Kohler, C., Hennighausen, L. & Nelson, J. A. ( 1990; ). Interactions between cellular regulatory proteins and a unique sequence region in the human cytomegalovirus major immediate-early promoter. Virology 174, 18–25.[CrossRef]
    [Google Scholar]
  32. Gnann, J. W., Jr, Ahlmen, J., Svalander, C., Olding, L., Oldstone, M. B. & Nelson, J. A. ( 1988; ). Inflammatory cells in transplanted kidneys are infected by human cytomegalovirus. Am J Pathol 132, 239–248.
    [Google Scholar]
  33. Goldmacher, V. S. ( 2004; ). Cell death suppressors encoded by cytomegalovirus. Prog Mol Subcell Biol 36, 1–18.
    [Google Scholar]
  34. Gonczol, E., Andrews, P. W. & Plotkin, S. A. ( 1984; ). Cytomegalovirus replicates in differentiated but not in undifferentiated human embryonal carcinoma cells. Science 224, 159–161.[CrossRef]
    [Google Scholar]
  35. Goodrum, F. D., Jordan, C. T., 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.[CrossRef]
    [Google Scholar]
  36. Goodrum, F., Jordan, C. T., Terhune, S. S., High, K. & Shenk, T. ( 2004; ). Differential outcomes of human cytomegalovirus infection in primitive hematopoietic cell subpopulations. Blood 104, 687–695.[CrossRef]
    [Google Scholar]
  37. Hahn, G., Jores, R. & Mocarski, E. S. ( 1998; ). Cytomegalovirus remains latent in a common precursor of dendritic and myeloid cells. Proc Natl Acad Sci U S A 95, 3937–3942.[CrossRef]
    [Google Scholar]
  38. Hahn, G., Revello, M. G., Patrone, M. & 9 other authors ( 2004; ). Human cytomegalovirus UL131-128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J Virol 78, 10023–10033.[CrossRef]
    [Google Scholar]
  39. Halford, W. P. & Schaffer, P. A. ( 2001; ). ICP0 is required for efficient reactivation of herpes simplex virus type 1 from neuronal latency. J Virol 75, 3240–3249.[CrossRef]
    [Google Scholar]
  40. Hendrix, R. M. G., Wagenaar, M., Slobbe, R. L. & Bruggeman, C. A. ( 1997; ). Widespread presence of cytomegalovirus DNA in tissues of healthy trauma victims. J Clin Pathol 50, 59–63.[CrossRef]
    [Google Scholar]
  41. Hertel, L., Lacaille, V. G., Strobl, H., Mellins, E. D. & Mocarski, E. S. ( 2003; ). Susceptibility of immature and mature Langerhans cell-type dendritic cells to infection and immunomodulation by human cytomegalovirus. J Virol 77, 7563–7574.[CrossRef]
    [Google Scholar]
  42. Huang, T. H., Oka, T., Asai, T., Okada, T., Merrills, B. W., Gertson, P. N., Whitson, R. H. & Itakura, K. ( 1996; ). Repression by a differentiation-specific factor of the human cytomegalovirus enhancer. Nucleic Acids Res 24, 1695–1701.[CrossRef]
    [Google Scholar]
  43. Hunninghake, G. W., Monick, M. M., Liu, B. & Stinski, M. F. ( 1989; ). The promoter-regulatory region of the major immediate-early gene of human cytomegalovirus responds to T-lymphocyte stimulation and contains functional cyclic AMP-response elements. J Virol 63, 3026–3033.
    [Google Scholar]
  44. Ibanez, C. E., Schrier, R., Ghazal, P., Wiley, C. & Nelson, J. A. ( 1991; ). Human cytomegalovirus productively infects primary differentiated macrophages. J Virol 65, 6581–6588.
    [Google Scholar]
  45. Jarvis, M. A. & Nelson, J. A. ( 2002; ). Mechanisms of human cytomegalovirus persistence and latency. Front Biosci 7, d1575–d1582.[CrossRef]
    [Google Scholar]
  46. Jenkins, P. J., Binné, U. K. & Farrell, P. J. ( 2000; ). Histone acetylation and reactivation of Epstein-Barr virus from latency. J Virol 74, 710–720.[CrossRef]
    [Google Scholar]
  47. Jenkins, C., Abendroth, A. & Slobedman, B. ( 2004; ). A novel viral transcript with homology to human interleukin-10 is expressed during latent human cytomegalovirus infection. J Virol 78, 1440–1447.[CrossRef]
    [Google Scholar]
  48. Jordan, M. C. ( 1983; ). Latent infection and the elusive cytomegalovirus. Rev Infect Dis 5, 205–215.[CrossRef]
    [Google Scholar]
  49. Kahl, M., Siegel-Axel, D., Stenglein, S., Jahn, G. & Sinzger, C. ( 2000; ). Efficient lytic infection of human arterial endothelial cells by human cytomegalovirus strains. J Virol 74, 7628–7635.[CrossRef]
    [Google Scholar]
  50. Katz, F. E., Tindle, R., Sutherland, D. R. & Greaves, M. F. ( 1985; ). Identification of a membrane glycoprotein associated with haemopoietic progenitor cells. Leuk Res 9, 191–198.[CrossRef]
    [Google Scholar]
  51. Kern, F., Bunde, T., Faulhaber, N. & 10 other authors ( 2002; ). Cytomegalovirus (CMV) phosphoprotein 65 makes a large contribution to shaping the T cell repertoire in CMV-exposed individuals. J Infect Dis 185, 1709–1716.[CrossRef]
    [Google Scholar]
  52. Khochbin, S., Verdel, A., Lemercier, C. & Seigneurin-Berny, D. ( 2001; ). Functional significance of histone deacetylase diversity. Curr Opin Genet Dev 11, 162–166.[CrossRef]
    [Google Scholar]
  53. Khorasanizadeh, S. ( 2004; ). The nucleosome: from genomic organization to genomic regulation. Cell 116, 259–272.[CrossRef]
    [Google Scholar]
  54. Kondo, K. & Mocarski, E. S. ( 1995; ). Cytomegalovirus latency and latency-specific transcription in hematopoietic progenitors. Scand J Infect Dis Suppl 99, 63–67.
    [Google Scholar]
  55. Kondo, K., Kaneshima, H. & Mocarski, E. S. ( 1994; ). Human cytomegalovirus latent infection of granulocyte–macrophage progenitors. Proc Natl Acad Sci U S A 91, 11879–11883.[CrossRef]
    [Google Scholar]
  56. Kondo, K., Xu, J. & Mocarski, E. S. ( 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.[CrossRef]
    [Google Scholar]
  57. Kothari, S., Baillie, J., Sissons, J. G. P. & Sinclair, J. H. ( 1991; ). The 21bp repeat element of the human cytomegalovirus major immediate early enhancer is a negative regulator of gene expression in undifferentiated cells. Nucleic Acids Res 19, 1767–1771.[CrossRef]
    [Google Scholar]
  58. Kubat, N. J., Tran, R. K., McAnany, P. & Bloom, D. C. ( 2004; ). Specific histone tail modification and not DNA methylation is a determinant of herpes simplex virus type 1 latent gene expression. J Virol 78, 1139–1149.[CrossRef]
    [Google Scholar]
  59. Kuo, M.-H. & Allis, C. D. ( 1998; ). Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays 20, 615–626.[CrossRef]
    [Google Scholar]
  60. LaFemina, R. & Hayward, G. S. ( 1986; ). Constitutive and retinoic acid-inducible expression of cytomegalovirus immediate-early genes in human teratocarcinoma cells. J Virol 58, 434–440.
    [Google Scholar]
  61. LaFemina, R. L. & Hayward, G. S. ( 1988; ). Differences in cell type-specific blocks to immediate early gene expression and DNA replication of human, simian and murine cytomegalovirus. J Gen Virol 69, 355–374.[CrossRef]
    [Google Scholar]
  62. Landini, M. P., Lazzarotto, T., Xu, J., Geballe, A. P. & Mocarski, E. S. ( 2000; ). Humoral immune response to proteins of human cytomegalovirus latency-associated transcripts. Biol Blood Marrow Transplant 6, 100–108.[CrossRef]
    [Google Scholar]
  63. Lang, D., Fickenscher, H. & Stamminger, T. ( 1992; ). Analysis of proteins binding to the proximal promoter region of the human cytomegalovirus IE-1/2 enhancer/promoter reveals both consensus and aberrant recognition sequences for transcription factors Sp1 and CREB. Nucleic Acids Res 20, 3287–3295.[CrossRef]
    [Google Scholar]
  64. Larsson, S., Söderberg-Nauclér, C., Wang, F. Z. & Moller, E. ( 1998; ). Cytomegalovirus DNA can be detected in peripheral blood mononuclear cells from all seropositive and most seronegative healthy blood donors over time. Transfusion 38, 271–278.[CrossRef]
    [Google Scholar]
  65. Lathey, J. L. & Spector, S. A. ( 1991; ). Unrestricted replication of human cytomegalovirus in hydrocortisone-treated macrophages. J Virol 65, 6371–6375.
    [Google Scholar]
  66. Leight, E. R. & Sugden, B. ( 2000; ). EBNA-1: a protein pivotal to latent infection by Epstein-Barr virus. Rev Med Virol 10, 83–100.[CrossRef]
    [Google Scholar]
  67. Liu, R., Baillie, J., Sissons, J. G. P. & Sinclair, J. H. ( 1994; ). The transcription factor YY1 binds to negative regulatory elements in the human cytomegalovirus major immediate early enhancer/promoter and mediates repression in non-permissive cells. Nucleic Acids Res 22, 2453–2459.[CrossRef]
    [Google Scholar]
  68. Lubon, H., Ghazal, P., Hennighausen, L., Reynolds-Kohler, C., Lockshin, C. & Nelson, J. ( 1989; ). Cell-specific activity of the modulator region in the human cytomegalovirus major immediate-early gene. Mol Cell Biol 9, 1342–1345.
    [Google Scholar]
  69. Lunetta, J. M. & Wiedeman, J. A. ( 2000; ). Latency-associated sense transcripts are expressed during in vitro human cytomegalovirus productive infection. Virology 278, 467–476.[CrossRef]
    [Google Scholar]
  70. Lusser, A. ( 2002; ). Acetylated, methylated, remodeled: chromatin states for gene regulation. Curr Opin Plant Biol 5, 437–443.[CrossRef]
    [Google Scholar]
  71. Maciejewski, J. P. & St Jeor, S. C. ( 1999; ). Human cytomegalovirus infection of human hematopoietic progenitor cells. Leuk Lymphoma 33, 1–13.
    [Google Scholar]
  72. McLaughlin-Taylor, E., Pande, H., Forman, S. J., Tanamachi, B., Li, C. R., Zaia, J. A., Greenberg, P. D. & Riddell, S. R. ( 1994; ). Identification of the major late human cytomegalovirus matrix protein pp65 as a target antigen for CD8+ virus-specific cytotoxic T lymphocytes. J Med Virol 43, 103–110.[CrossRef]
    [Google Scholar]
  73. Meier, J. L. ( 2001; ). Reactivation of the human cytomegalovirus major immediate-early regulatory region and viral replication in embryonal NTera2 cells: role of trichostatin A, retinoic acid, and deletion of the 21-base-pair repeats and modulator. J Virol 75, 1581–1593.[CrossRef]
    [Google Scholar]
  74. Meier, J. L. & Pruessner, J. A. ( 2000; ). The human cytomegalovirus major immediate-early distal enhancer region is required for efficient viral replication and immediate-early gene expression. J Virol 74, 1602–1613.[CrossRef]
    [Google Scholar]
  75. Meier, J. L. & Stinski, M. F. ( 1996; ). Regulation of human cytomegalovirus immediate-early gene expression. Intervirology 39, 331–342.
    [Google Scholar]
  76. Meier, J. L. & Stinski, M. F. ( 1997; ). Effect of a modulator deletion on transcription of the human cytomegalovirus major immediate-early genes in infected undifferentiated and differentiated cells. J Virol 71, 1246–1255.
    [Google Scholar]
  77. Meier, J. L. & Stinski, M. F. ( 2006; ). Major immediate-early enhancer and its gene products. In Cytomegaloviruses: Molecular Biology and Immunology, pp. 150–166. Edited by M. J. Reddehase. Wymondham, UK: Caister.
  78. Mendelson, M., Monard, S., Sissons, P. & Sinclair, J. ( 1996; ). Detection of endogenous human cytomegalovirus in CD34+ bone marrow progenitors. J Gen Virol 77, 3099–3102.[CrossRef]
    [Google Scholar]
  79. Metcalf, D. ( 1989; ). The molecular control of cell division, differentiation commitment and maturation in haemopoietic cells. Nature 339, 27–30.[CrossRef]
    [Google Scholar]
  80. Meyer-Konig, U., Hufert, F. T. & von Laer, D. M. ( 1997; ). Infection of blood and bone marrow cells with the human cytomegalovirus in vivo. Leuk Lymphoma 25, 445–454.
    [Google Scholar]
  81. Michelson, S., Rohrlich, P., Beisser, P. & 7 other authors ( 2001; ). Human cytomegalovirus infection of bone marrow myofibroblasts enhances myeloid progenitor adhesion and elicits viral transmission. Microbes Infect 3, 1005–1013.[CrossRef]
    [Google Scholar]
  82. Minton, E. J., Tysoe, C., Sinclair, J. H. & Sissons, J. G. P. ( 1994; ). Human cytomegalovirus infection of the monocyte/macrophage lineage in bone marrow. J Virol 68, 4017–4021.
    [Google Scholar]
  83. Mocarski, E. S., Jr, Hahn, G., White, K. L., Xu, J., Slobedman, B., Hertel, L., Aguirre, S. A. & Noda, S. ( 2006; ). Myeloid cell recruitment and function in pathogenesis and latency. In Cytomegaloviruses: Molecular Biology and Immunology, pp. 465–481. Edited by M. J. Reddehase. Wymondham, UK: Caister.
  84. Murphy, J. C., Fischle, W., Verdin, E. & Sinclair, J. H. ( 2002; ). Control of cytomegalovirus lytic gene expression by histone acetylation. EMBO J 21, 1112–1120.[CrossRef]
    [Google Scholar]
  85. Nelson, J. A. & Groudine, M. ( 1986; ). Transcriptional regulation of the human cytomegalovirus major immediate-early gene is associated with induction of DNase I-hypersensitive sites. Mol Cell Biol 6, 452–461.
    [Google Scholar]
  86. Nelson, J. A., Reynolds-Kohler, C. & Smith, B. A. ( 1987; ). Negative and positive regulation by a short segment in the 5′-flanking region of the human cytomegalovirus major immediate-early gene. Mol Cell Biol 7, 4125–4129.
    [Google Scholar]
  87. Nelson, J. A., Gnann, J. W., Jr & Ghazal, P. ( 1990; ). Regulation and tissue-specific expression of human cytomegalovirus. Curr Top Microbiol Immunol 154, 75–100.
    [Google Scholar]
  88. Pizzorno, M. C. ( 2001; ). Nuclear cathepsin B-like protease cleaves transcription factor YY1 in differentiated cells. Biochim Biophys Acta 1536, 31–42.[CrossRef]
    [Google Scholar]
  89. Quirici, N., Soligo, D., Caneva, L., Servida, F., Bossolasco, P. & Deliliers, G. L. ( 2001; ). Differentiation and expansion of endothelial cells from human bone marrow CD133+ cells. Br J Haematol 115, 186–194.[CrossRef]
    [Google Scholar]
  90. Reeves, M. B., Coleman, H., Chadderton, J., Goddard, M., Sissons, J. G. P. & Sinclair, J. H. ( 2004; ). Vascular endothelial and smooth muscle cells are unlikely to be major sites of latency of human cytomegalovirus in vivo. J Gen Virol 85, 3337–3341.[CrossRef]
    [Google Scholar]
  91. Reeves, M. B., Lehner, P. J., Sissons, J. G. P. & Sinclair, J. H. ( 2005a; ). 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.[CrossRef]
    [Google Scholar]
  92. Reeves, M. B., MacAry, P. A., Lehner, P. J., Sissons, J. G. P. & Sinclair, J. H. ( 2005b; ). 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.[CrossRef]
    [Google Scholar]
  93. Reeves, M., Sissons, P. & Sinclair, J. ( 2005c; ). Reactivation of human cytomegalovirus in dendritic cells. Discov Med 5, 170–174.
    [Google Scholar]
  94. Rice, G. P. A., Schrier, R. D. & Oldstone, M. B. A. ( 1984; ). Cytomegalovirus infects human lymphocytes and monocytes: virus expression is restricted to immediate-early gene products. Proc Natl Acad Sci U S A 81, 6134–6138.[CrossRef]
    [Google Scholar]
  95. Rice, J. C., Briggs, S. D., Ueberheide, B., Barber, C. M., Shabanowitz, J., Hunt, D. F., Shinkai, Y. & Allis, C. D. ( 2003; ). Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol Cell 12, 1591–1598.[CrossRef]
    [Google Scholar]
  96. Riddell, S. R., Rabin, M., Geballe, A. P., Britt, W. J. & Greenberg, P. D. ( 1991; ). Class I MHC-restricted cytotoxic T lymphocyte recognition of cells infected with human cytomegalovirus does not require endogenous viral gene expression. J Immunol 146, 2795–2804.
    [Google Scholar]
  97. 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.
    [Google Scholar]
  98. Rubin, R. H. ( 1990; ). Impact of cytomegalovirus infection on organ transplant recipients. Rev Infect Dis 12 (Suppl. 7), S754–S766.[CrossRef]
    [Google Scholar]
  99. Saccani, S. & Natoli, G. ( 2002; ). Dynamic changes in histone H3 Lys 9 methylation occurring at tightly regulated inducible inflammatory genes. Genes Dev 16, 2219–2224.[CrossRef]
    [Google Scholar]
  100. Saccani, S., Pantano, S. & Natoli, G. ( 2002; ). p38-dependent marking of inflammatory genes for increased NF-κB recruitment. Nat Immunol 3, 69–75.[CrossRef]
    [Google Scholar]
  101. Sambucetti, L. C., Cherrington, J. M., Wilkinson, G. W. G. & Mocarski, E. S. ( 1989; ). NF-κB activation of the cytomegalovirus enhancer is mediated by a viral transactivator and by T cell stimulation. EMBO J 8, 4251–4258.
    [Google Scholar]
  102. Sawtell, N. M. ( 1998; ). The probability of in vivo reactivation of herpes simplex virus type 1 increases with the number of latently infected neurons in the ganglia. J Virol 72, 6888–6892.
    [Google Scholar]
  103. Schotta, G., Ebert, A., Krauss, V., Fischer, A., Hoffmann, J., Rea, S., Jenuwein, T., Dorn, R. & Reuter, G. ( 2002; ). Central role of Drosophila SU(VAR)3–9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J 21, 1121–1131.[CrossRef]
    [Google Scholar]
  104. Schrier, R. D., Nelson, J. A. & Oldstone, M. B. ( 1985; ). Detection of human cytomegalovirus in peripheral blood lymphocytes in a natural infection. Science 230, 1048–1051.[CrossRef]
    [Google Scholar]
  105. Shelbourn, S. L., Kothari, S. K., Sissons, J. G. & Sinclair, J. H. ( 1989; ). Repression of human cytomegalovirus gene expression associated with a novel immediate early regulatory region binding factor. Nucleic Acids Res 17, 9165–9171.[CrossRef]
    [Google Scholar]
  106. Simon, C., Seckert, C., Grzimek, N. & Reddehase, M. ( 2006; ). Murine models of cytomegalovirus latency and reactivation. In Cytomegaloviruses: Molecular Biology and Immunology, pp. 483–500. Edited by M. J. Reddehase. Wymondham, UK: Caister.
  107. Sinclair, A. J. ( 2003; ). bZIP proteins of human gammaherpesviruses. J Gen Virol 84, 1941–1949.[CrossRef]
    [Google Scholar]
  108. Sinclair, J. & Sissons, P. ( 1996; ). Latent and persistent infections of monocytes and macrophages. Intervirology 39, 293–301.
    [Google Scholar]
  109. Sinclair, J. H., Baillie, J., Bryant, L. A., Taylor-Wiedeman, J. A. & Sissons, J. G. P. ( 1992; ). Repression of human cytomegalovirus major immediate early gene expression in a monocytic cell line. J Gen Virol 73, 433–435.[CrossRef]
    [Google Scholar]
  110. Sinzger, C., Grefte, A., Plachter, B., Gouw, A. S. H., The, T. H. & Jahn, G. ( 1995; ). Fibroblasts, epithelial cells, endothelial cells and smooth muscle cells are major targets of human cytomegalovirus infection in lung and gastrointestinal tissues. J Gen Virol 76, 741–750.[CrossRef]
    [Google Scholar]
  111. Slobedman, B. & Mocarski, E. S. ( 1999; ). Quantitative analysis of latent human cytomegalovirus. J Virol 73, 4806–4812.
    [Google Scholar]
  112. Slobedman, B., Mocarski, E. S., Arvin, A. M., Mellins, E. D. & Abendroth, A. ( 2002; ). Latent cytomegalovirus down-regulates major histocompatibility complex class II expression on myeloid progenitors. Blood 100, 2867–2873.[CrossRef]
    [Google Scholar]
  113. Slobedman, B., Stern, J. L., Cunningham, A. L., Abendroth, A., Abate, D. A. & Mocarski, E. S. ( 2004; ). Impact of human cytomegalovirus latent infection on myeloid progenitor cell gene expression. J Virol 78, 4054–4062.[CrossRef]
    [Google Scholar]
  114. Smyth, R. L., Sinclair, J., Scott, J. P., Gray, J. J., Higenbottam, T. W., Wreghitt, T. G., Wallwork, J. & Borysiewicz, L. K. ( 1991; ). Infection and reactivation with cytomegalovirus strains in lung transplant recipients. Transplantation 52, 480–482.[CrossRef]
    [Google Scholar]
  115. Söderberg-Nauclér, C., Fish, K. N. & Nelson, J. A. ( 1997; ). Reactivation of latent human cytomegalovirus by allogeneic stimulation of blood cells from healthy donors. Cell 91, 119–126.[CrossRef]
    [Google Scholar]
  116. Söderberg-Nauclér, C., Streblow, D. N., Fish, K. N., Allan-Yorke, J., Smith, P. P. & Nelson, J. A. ( 2001; ). Reactivation of latent human cytomegalovirus in CD14+ monocytes is differentiation dependent. J Virol 75, 7543–7554.[CrossRef]
    [Google Scholar]
  117. Speck, S. H., Chatila, T. & Flemington, E. ( 1997; ). Reactivation of Epstein-Barr virus: regulation and function of the BZLF1 gene. Trends Microbiol 5, 399–405.[CrossRef]
    [Google Scholar]
  118. Spector, D. H. ( 1996; ). Activation and regulation of human cytomegalovirus early genes. Intervirology 39, 361–377.
    [Google Scholar]
  119. Stagno, S., Reynolds, D. W., Pass, R. F. & Alford, C. A. ( 1980; ). Breast milk and the risk of cytomegalovirus infection. N Engl J Med 302, 1073–1076.[CrossRef]
    [Google Scholar]
  120. Stanier, P., Kitchen, A. D., Taylor, D. L. & Tyms, A. S. ( 1992; ). Detection of human cytomegalovirus in peripheral mononuclear cells and urine samples using PCR. Mol Cell Probes 6, 51–58.[CrossRef]
    [Google Scholar]
  121. Stenberg, R. M. ( 1996; ). The human cytomegalovirus major immediate-early gene. Intervirology 39, 343–349.
    [Google Scholar]
  122. Strahl, B. D. & Allis, C. D. ( 2000; ). The language of covalent histone modifications. Nature 403, 41–45.[CrossRef]
    [Google Scholar]
  123. Streblow, D. N. & Nelson, J. A. ( 2003; ). Models of HCMV latency and reactivation. Trends Microbiol 11, 293–295.[CrossRef]
    [Google Scholar]
  124. Strobl, H. ( 2003; ). Molecular mechanisms of dendritic cell sublineage development from human hematopoietic progenitor/stem cells. Int Arch Allergy Immunol 131, 73–79.[CrossRef]
    [Google Scholar]
  125. Sylwester, A. W., Mitchell, B. L., Edgar, J. B. & 9 other authors ( 2005; ). Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J Exp Med 202, 673–685.[CrossRef]
    [Google Scholar]
  126. Tang, Q. & Maul, G. G. ( 2006; ). Immediate early interactions and epigenetic defense mechanisms. In Cytomegaloviruses: Molecular Biology and Immunology, pp. 131–149. Edited by M. J. Reddehase. Wymondham, UK: Caister.
  127. Taylor-Wiedeman, J., Sissons, J. G. P., Borysiewicz, L. K. & Sinclair, J. H. ( 1991; ). Monocytes are a major site of persistence of human cytomegalovirus in peripheral blood mononuclear cells. J Gen Virol 72, 2059–2064.[CrossRef]
    [Google Scholar]
  128. Taylor-Wiedeman, J., Hayhurst, G. P., Sissons, J. G. P. & Sinclair, J. H. ( 1993; ). Polymorphonuclear cells are not sites of persistence of human cytomegalovirus in healthy individuals. J Gen Virol 74, 265–268.[CrossRef]
    [Google Scholar]
  129. 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.
    [Google Scholar]
  130. Thomas, M. J. & Seto, E. ( 1999; ). Unlocking the mechanisms of transcription factor YY1: are chromatin modifying enzymes the key? Gene 236, 197–208.[CrossRef]
    [Google Scholar]
  131. Tolpin, M. D., Stewart, J. A., Warren, D. & 7 other authors ( 1985; ). Transfusion transmission of cytomegalovirus confirmed by restriction endonuclease analysis. J Pediatr 107, 953–956.[CrossRef]
    [Google Scholar]
  132. Toorkey, C. B. & Carrigan, D. R. ( 1989; ). Immunohistochemical detection of an immediate early antigen of human cytomegalovirus in normal tissues. J Infect Dis 160, 741–751.[CrossRef]
    [Google Scholar]
  133. Wang, D. & Shenk, T. ( 2005; ). Human cytomegalovirus UL131 open reading frame is required for epithelial cell tropism. J Virol 79, 10330–10338.[CrossRef]
    [Google Scholar]
  134. Weinshenker, B. G., Wilton, S. & Rice, G. P. ( 1988; ). Phorbol ester-induced differentiation permits productive human cytomegalovirus infection in a monocytic cell line. J Immunol 140, 1625–1631.
    [Google Scholar]
  135. Weintraub, H. & Groudine, M. ( 1976; ). Chromosomal subunits in active genes have an altered conformation. Science 193, 848–856.[CrossRef]
    [Google Scholar]
  136. White, K. L., Slobedman, B. & Mocarski, E. S. ( 2000; ). Human cytomegalovirus latency-associated protein pORF94 is dispensable for productive and latent infection. J Virol 74, 9333–9337.[CrossRef]
    [Google Scholar]
  137. Wills, M. R., Carmichael, A. J., Mynard, K., Jin, X., Weekes, M. P., Plachter, B. & Sissons, J. G. P. ( 1996; ). The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J Virol 70, 7569–7579.
    [Google Scholar]
  138. Wills, M. R., Okecha, G., Weekes, M. P., Gandhi, M. K., Sissons, P. J. G. & Carmichael, A. J. ( 2002; ). Identification of naive or antigen-experienced human CD8+ T cells by expression of costimulation and chemokine receptors: analysis of the human cytomegalovirus-specific CD8+ T cell response. J Immunol 168, 5455–5464.[CrossRef]
    [Google Scholar]
  139. Wright, E., Bain, M., Teague, L., Murphy, J. & Sinclair, J. ( 2005; ). Ets-2 repressor factor recruits histone deacetylase to silence human cytomegalovirus immediate-early gene expression in non-permissive cells. J Gen Virol 86, 535–544.[CrossRef]
    [Google Scholar]
  140. Yeager, A. S., Grumet, F. C., Hafleigh, E. B., Arvin, A. M., Bradley, J. E. & Prober, C. G. ( 1981; ). Prevention of transfusion-acquired cytomegalovirus infections in newborn infants. J Pediatr 98, 281–287.[CrossRef]
    [Google Scholar]
  141. Zhang, X.-Y., Inamdar, N. M., Supakar, P. C., Wu, K., Ehrlich, K. C. & Ehrlich, M. ( 1991; ). Three MDBP sites in the immediate-early enhancer-promoter region of human cytomegalovirus. Virology 182, 865–869.[CrossRef]
    [Google Scholar]
  142. Zhu, H., Cong, J.-P., Mamtora, G., Gingeras, T. & Shenk, T. ( 1998; ). Cellular gene expression altered by human cytomegalovirus: global monitoring with oligonucleotide arrays. Proc Natl Acad Sci U S A 95, 14470–14475.[CrossRef]
    [Google Scholar]
  143. Zweidler-McKay, P. A., Grimes, H. L., Flubacher, M. M. & Tsichlis, P. N. ( 1996; ). Gfi-1 encodes a nuclear zinc finger protein that binds DNA and functions as a transcriptional repressor. Mol Cell Biol 16, 4024–4034.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81891-0
Loading
/content/journal/jgv/10.1099/vir.0.81891-0
Loading

Data & Media loading...

Most Cited This Month

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