Human herpesvirus 6A (HHV-6A) and HHV-6B alter E2F1/Rb pathways and E2F1 localization and cause cell cycle arrest in infected T cells

Journal of Virology

Volumn 81, Issue 24, 2007, Pages 13499-13508

  Mlechkovich, Guy ^a   Frenkel, Niza ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN E; MINICHROMOSOME MAINTENANCE PROTEIN 5; PROTEIN; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F1;

ARTICLE; CELL CYCLE ARREST; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 6; HUMAN HERPESVIRUS 6 A; HUMAN HERPESVIRUS 6 B; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE; TRANSCRIPTION REGULATION; UPREGULATION; VIRUS CULTURE; VIRUS INACTIVATION; VIRUS STRAIN;

CELL CYCLE; CELL LINE; CELL NUCLEUS; CYTOPLASM; E2F1 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; HERPESVIRUS 6, HUMAN; HUMANS; RETINOBLASTOMA PROTEIN; T-LYMPHOCYTES; ULTRAVIOLET RAYS;

HUMAN HERPESVIRUS 6; HUMAN HERPESVIRUS 6A;

EID: 37049010534     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01496-07     Document Type: Article

References (88)

1. Ablashi, A. H., Z. Berneman, et al. 1993. Human herpesvirus-6 strain groups: a nomenclature. Arch. Virol. 129:363-366.
2. Alvarez-Lafuente, R., V. De Las Heras, M. Bartolome, M. Garcia-Montojo, and R. Arroyo. 2006. Human herpesvirus 6 and multiple sclerosis: a one-year follow-up study. Brain Pathol. 16:20-27.
3. Alvarez-Lafuente, R., V. de Las Heras, M. Garcia-Montojo, M. Bartolome, and R. Arroyo. 2007. Human herpesvirus-6 and multiple sclerosis: relapsing-remitting versus secondary progressive. Mult. Scler. 13:578-583.
4. Alvarez-Lafuente, R., M. Garcia-Montojo, V. De las Heras, M. Bartolome, and R. Arroyo. 2006. Clinical parameters and HHV-6 active replication in relapsing-remitting multiple sclerosis patients. J. Clin. Virol. 37(Suppl. 1): S24-S26.
5. Apostolova, M. D., I. A. Ivanova, C. Dagnino, S. J. D'Souza, and L. Dagnino. 2002. Active nuclear import and export pathways regulate E2F-5 subcellular localization. J. Biol. Chem. 277:34471-34479.
6. Asano, Y., T. Yoshikawa, Y. Kajita, R. Ogura, S. Suga, T. Yazaki, T. Nakashima, A. Yamada, and T. Kurata. 1992. Fatal encephalitis/encephalopathy in primary human herpesvirus-6 infection. Arch. Dis. Child. 67:1484-1485.
7. Bagchi, S., R. Weinmann, and P. Raychaudhuri. 1991. The retinoblastoma protein copurifies with E2F-I, an E1A-regulated inhibitor of the transcription factor E2F. Cell 65:1063-1072.
8. Balachandran, N., S. Tirawatnapong, B. Pfeiffer, D. V. Ablashi, and S. Z. Salahuddin. 1991. Electrophoretic analysis of human herpesvirus 6 polypeptides immunoprecipitated from infected cells with human sera. J. Infect. Dis. 163:29-34.
9. Boeckh, M., V. Erard, D. Zerr, and J. Englund. 2005. Emerging viral infections after hematopoietic cell transplantation. Pediatr. Transplant 9(Suppl. 7):48-54.
10. Bosco, G., W. Du, and T. L. Orr-Weaver. 2001. DNA replication control through interaction of E2F-RB and the origin recognition complex. Nat. Cell Biol. 3:289-295.
11. Bracken, A. P., M. Ciro, A. Cocito, and K. Helin. 2004. E2F target genes: unraveling the biology. Trends Biochem. Sci. 29:409-417.
12. 1/S transition and DNA replication. Cancer Cell 3:311-316.
13. Chang, C. K., and N. Balachandran. 1991. Identification, characterization, and sequence analysis of a cDNA encoding a phosphoprotein of human herpesvirus 6. J. Virol. 65:2884-2894.
14. Chapenko, S., A. Millers, Z. Nora, I. Logina, R. Kukaine, and M. Murovska. 2003. Correlation between HHV-6 reactivation and multiple sclerosis disease activity. J. Med. Virol. 69:111-117.
15. Chau, B. N., C. W. Pan, and J. Y. Wang. 2006. Separation of anti-proliferation and anti-apoptotic functions of retinoblastoma protein through targeted mutations of its A/B domain. PLoS 1:e82.
16. Chellappan, S. P., S. Hiebert, M. Mudryj, J. M. Horowitz, and J. R. Nevins. 1991. The E2F transcription factor is a cellular target for the RB protein. Cell 65:1053-1061.
17. 2 phase of the cell cycle. FEBS Lett. 560:25-29.
18. DeGregori, J., and D. G. Johnson. 2006. Distinct and overlapping roles for E2F family members in transcription, proliferation and apoptosis. Curr. Mol. Med. 6:739-748.
19. Dick, F. A., E. Sailhamer, and N. J. Dyson. 2000. Mutagenesis of the pRb pocket reveals that cell cycle arrest functions are separable from binding to viral oncoproteins. Mol. Cell. Biol. 20:3715-3727.
20. Di Luca, D., G. Katsafanas, E. C. Schirmer, N. Balachandran, and N. Frenkel. 1990. The replication of viral and cellular DNA in human herpes-virus 6-infected cells. Virology 175:199-210.
21. 1 entry in quiescent cells. Virology 267:335-349.
22. Forsburg, S. L. 2004. Eukaryotic MCM proteins: beyond replication initiation. Microbiol. Mol. Biol. Rev. 68:109-131.
23. Fotheringham, J., and S. Jacobson. 2005. Human herpesvirus 6 and multiple sclerosis: potential mechanisms for virus-induced disease. Herpes 12:4-9.
24. Frenkel, N., and R. Borenstein. 2006. Characterization of the lymphotropic amplicons-6 and tamplicon-7 vectors derived from HHV-6 and HHV-7. Curr. Gene Ther. 6:399-420.
25. Frenkel, N., G. C. Katsafanas, L. S. Wyatt, T. Yoshikawa, and Y. Asano. 1994. Bone marrow transplant recipients harbor the B variant of human herpesvirus 6. Bone Marrow Transplant. 14:839-843.
26. Grand, R. J., A. P. Ibrahim, A. M. Taylor, A. E. Milner, C. D. Gregory, P. H. Gallimore, and A. S. Turnell. 1998. Human cells arrest in S phase in response to adenovirus 12 E1A. Virology 244:330-342.
27. Helin, K., J. A. Lees, M. Vidal, N. Dyson, E. Harlow, and A. Fattaey. 1992. A cDNA encoding a pRB-binding protein with properties of the transcription factor E2F. Cell 70:337-350.
28. Helin, K., C. L. Wu, A. R. Fattaey, J. A. Lees, B. D. Dynlacht, C. Ngwu, and E. Harlow. 1993. Heterodimerization of the transcription factors E2F-1 and DP-1 leads to cooperative trans-activation. Genes Dev. 7:1850-1861.
29. Hilton, M. J., D. Mounghane, T. McLean, N. V. Contractor, J. O'Neil, K. Carpenter, and S. L. Bachenheimer. 1995. Induction by herpes simplex virus of free and heteromeric forms of E2F transcription factor. Virology 213: 624-638.
30. Hwang, H. C., and B. E. Clurman. 2005. Cyclin E in normal and neoplastic cell cycles. Oncogene 24:2776-2786.
31. Jault, F. M., J. M. Jault, F. Ruchti, E. A. Fortunato, C. Clark, J. Corbeil, D. D. Richman, and D. H. Spector. 1995. Cytomegalovirus infection induces high levels of cyclins, phosphorylated Rb, and p53, leading to cell cycle arrest. J. Virol. 69:6697-6704.
32. Kaelin, W. G., Jr., W. Krek, W. R. Sellers, J. A. DeCaprio, F. Ajchenbaum, C. S. Fuchs, T. Chittenden, Y. Li, P. J. Farnham, M. A. Blanar, et al. 1992. Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell 70:351-364.
33. Kel, A. E., O. V. Kel-Margoulis, P. J. Farnham, S. M. Bartley, E. Wingender, and M. Q. Zhang. 2001. Computer-assisted identification of cell cycle-related genes: new targets for E2F transcription factors. J. Mol. Biol. 309:99-120.
34. Komaroff, A. L. 2006. Is human herpesvirus-6 a trigger for chronic fatigue syndrome? J. Clin. Virol. 37(Suppl. 1):S39-S46.
35. Koutsami, M. K., P. K. Tsantoulis, M. Kouloukoussa, K. Apostolopoulou, I. S. Pateras, Z. Spartinou, A. Drougou, K. Evangelou, C. Kittas, J. Bartkova, J. Bartek, and V. G. Gorgoulis. 2006. Centrosome abnormalities are frequently observed in non-small-cell lung cancer and are associated with aneuploidy and cyclin E overexpression. J. Pathol. 209:512-521.
36. Kovesdi, I., R. Reichel, and J. R. Nevins. 1986. Identification of a cellular transcription factor involved in E1A trans-activation. Cell 45:219-228.
37. Krueger, G., and D. V. Ablashi (ed.). 2006. Human herpesvirus-6, general virology, epidemiology and clinical pathology. Perspectives in medical virology, vol. 12. Elsevier Science B.V., Amsterdam, The Netherlands.
38. Lee, C., and Y. Cho. 2002. Interactions of SV40 large T antigen and other viral proteins with retinoblastoma tumour suppressor. Rev. Med. Virol. 12:81-92.
39. Lees, J. A., M. Saito, M. Vidal, M. Valentine, T. Look, E. Harlow, N. Dyson, and K. Helin. 1993. The retinoblastoma protein binds to a family of E2F transcription factors. Mol. Cell. Biol. 13:7813-7825.
40. Lindeman, G. J., S. Gaubatz, D. M. Livingston, and D. Ginsberg. 1997. The subcellular localization of E2F-4 is cell-cycle dependent. Proc. Natl. Acad. Sci. USA 94:5095-5100.
41. Ljungman, P., and N. Singh. 2006. Human herpesvirus-6 infection in solid organ and stem cell transplant recipients. J. Clin. Virol. 37(Suppl. 1):S87-S91.
42. Lopez, C., P. Pellett, J. Stewart, C. Goldsmith, K. Sanderlin, J. Black, D. Warfield, and P. Feorino. 1988. Characteristics of human herpesvirus-6. J. Infect. Dis. 157:1271-1273.
43. Magae, J., C. L. Wu, S. Illenye, E. Harlow, and N. H. Heintz. 1996. Nuclear localization of DP and E2F transcription factors by heterodimeric partners and retinoblastoma protein family members. J. Cell Sci. 109:1717-1726.
44. Mameli, G., V. Astone, G. Arru, S. Marconi, L. Lovato, C. Serra, S. Sotgiu, B. Bonetti, and A. Dolei. 2007. Brains and peripheral blood mononuclear cells of multiple sclerosis (MS) patients hyperexpress MS-associated retrovirus/HERV-W endogenous retrovirus, but not human herpesvirus 6. J. Gen. Virol. 88:264-274.
45. Mayne, M., C. Cheadle, S. S. Soldan, C. Cermelli, Y. Yamano, N. Akhyani, J. E. Nagel, D. D. Taub, K. G. Becker, and S. Jacobson. 2001. Gene expression profile of herpesvirus-infected T cells obtained using immunomicroarrays: induction of proinflammatory mechanisms. J. Virol. 75:11641-11650.
46. Müller, H., A. P. Bracken, R. Vernell, M. C. Moroni, F. Christians, E. Grassilli, E. Prosperini, E. Vigo, J. D. Oliner, and K. Helin. 2001. E2Fs regulate the expression of genes involved in differentiation, development, proliferation, and apoptosis. Genes Dev. 15:267-285.
47. Müller, H., M. C. Moroni, E. Vigo, B. O. Petersen, J. Bartek, and K. Helin. 1997. Induction of S-phase entry by E2F transcription factors depends on their nuclear localization. Mol. Cell. Biol. 17:5508-5520.
48. Mundle, S. D., and G. Saberwal. 2003. Evolving intricacies and implications of E2F1 regulation. FASEB J. 17:569-574.
49. Nagasawa, T., I. Kimura, Y. Abe, and A. Oka. 2007. HHV-6 encephalopathy with cluster of convulsions during eruptive stage. Pediatr. Neurol. 36:61-63.
50. Ohtani, K., J. DeGregori, and J. R. Nevins. 1995. Regulation of the cyclin E gene by transcription factor E2F1. Proc. Natl. Acad. Sci. USA 92:12146-12150.
51. Ohtani, K., R. Iwanaga, M. Nakamura, M. Ikeda, N. Yabuta, H. Tsuruga, and H. Nojima. 1999. Cell growth-regulated expression of mammalian MCM5 and MCM6 genes mediated by the transcription factor E2F. Oncogene 18:2299-2309.
52. Øster, B., B. Bundgaard, and P. Hollsberg. 2005. Human herpesvirus 6B induces cell cycle arrest concomitant with p53 phosphorylation and accumulation in T cells. J. Virol. 79:1961-1965.
53. Oster, B., M. D. Kaspersen, E. Kofod-Olsen, B. Bundgaard, and P. Hollsberg. 2006. Human herpesvirus 6B inhibits cell proliferation by a p53-independent pathway. J. Clin. Virol. 37(Suppl. 1):S63-S68.
54. Pellett, D. A. 2002. Human herpesviruses 6A, 6B, and 7 and their replication, p. 2769-2784. In B. N. Fields and D. M. Knipe (ed.), Fields virology, 4th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, PA.
55. Rapaport, D., D. Engelhard, G. Tagger, R. Or, and N. Frenkel. 2002. Antiviral prophylaxis may prevent human herpesvirus-6 reactivation in bone marrow transplant recipients. Transplant. Infect. Dis. 4:10-16.
56. Rotola, A., I. Merlotti, L. Caniatti, E. Caselli, E. Granieri, M. R. Tola, D. Di Luca, and E. Cassai. 2004. Human herpesvirus 6 infects the central nervous system of multiple sclerosis patients in the early stages of the disease. Mult. Scler. 10:348-354.
57. Ryu, S., J. Holzschuh, S. Erhardt, A. K. Ettl, and W. Driever. 2005. Depletion of minichromosome maintenance protein 5 in the zebrafish retina causes cell-cycle defect and apoptosis. Proc. Natl. Acad. Sci. USA 102:18467-18472.
58. Salahuddin, S. Z., D. V. Ablashi, P. D. Markham, S. F. Josephs, S. Sturzenegger, M. Kaplan, G. Halligan, P. Biberfeld, F. Wong-Staal, B. Kramarsky, et al. 1986. Isolation of a new virus, HBLV, in patients with lymphoproliferative disorders. Science 234:596-601.
59. Santoro, F., P. E. Kennedy, G. Locatelli, M. S. Malnati, E. A. Berger, and P. Lusso. 1999. CD46 is a cellular receptor for human herpesvirus 6. Cell 99:817-827.
60. Schirmer, E. C., L. S. Wyatt, K. Yamanishi, W. J. Rodriguez, and N. Frenkel. 1991. Differentiation between two distinct classes of viruses now classified as human herpesvirus 6. Proc. Natl. Acad. Sci. USA 88:5922-5926.
61. Schwed, G., N. May, Y. Pechersky, and B. R. Calvi. 2002. Drosophila minichromosome maintenance 6 is required for chorion gene amplification and genomic replication. Mol. Biol. Cell 13:607-620.
62. Shan, B., X. Zhu, P. L. Chen, T. Durfee, Y. Yang, D. Sharp, and W. H. Lee. 1992. Molecular cloning of cellular genes encoding retinoblastoma- associated proteins: identification of a gene with properties of the transcription factor E2F. Mol. Cell. Biol. 12:5620-5631.
63. Singer, J. D., M. Gurian-West, B. Clurman, and J. M. Roberts. 1999. Cullin-3 targets cyclin E for ubiquitination and controls S phase in mammalian cells. Genes Dev. 13:2375-2387.
64. Singer, O., and N. Frenkel. 1997. Human herpesvirus 7 (HHV-7) DNA: analyses of clones spanning the entire genome. Arch. Virol. 142:287-303.
65. Smith, J. M., and R. A. McDonald. 2006. Emerging viral infections in transplantation. Pediatr. Transplant. 10:838-843.
66. Soldan, S. S., A. D. Goodman, and S. Jacobson. 2006. HHV-6 and the central nervous system, p. 213-224. In G. Krueger and D. V. Ablashi (ed.), Human herpesvirus-6, general virology, epidemiology and clinical pathology. Perspectives in medical virology, vol. 12. Elsevier Science B.V., Amsterdam, The Netherlands.
67. Song, Y. J., and M. F. Stinski. 2002. Effect of the human cytomegalovirus IE86 protein on expression of E2F-responsive genes: a DNA microarray analysis. Proc. Natl. Acad. Sci. USA 99:2836-2841.
68. Stagljar, I., U. Hubscher, and A. Barberis. 1999. Activation of DNA replication in yeast by recruitment of the RNA polymerase II transcription complex. Biol. Chem. 380:525-530.
69. Stanelle, J., and B. M. Putzer. 2006. E2F1-induced apoptosis: turning killers into therapeutics. Trends Mol. Med. 12:177-185.
70. Suga, S., K. Suzuki, M. Ihira, T. Yoshikawa, Y. Kajita, T. Ozaki, K. Iida, Y. Saito, and Y. Asano. 2000. Clinical characteristics of febrile convulsions during primary HHV-6 infection. Arch. Dis. Child. 82:62-66.
71. Takaku, T., J. H. Ohyashiki, Y. Zhang, and K. Ohyashiki. 2005. Estimating immunoregulatory gene networks in human herpesvirus type 6-infected T cells. Biochem. Biophys. Res. Commun. 336:469-477.
72. Takemoto, M., M. Koike, Y. Mori, S. Yonemoto, Y. Sasamoto, K. Kondo, Y. Uchiyama, and K. Yamanishi. 2005. Human herpesvirus 6 open reading frame U14 protein and cellular p53 interact with each other and are contained in the virion. J. Virol. 79:13037-13046.
73. Takemoto, M., Y. Mori, K. Ueda, K. Kondo, and K. Yamanishi. 2004. Productive human herpesvirus 6 infection causes aberrant accumulation of p53 and prevents apoptosis. J. Gen. Virol. 85:869-879.
74. Tomonari, A., S. Takahashi, J. Ooi, T. Iseki, K. Takasugi, M. Uchiyama, T. Konuma, M. Futami, N. Ohno, K. Uchimaru, A. Tojo, and S. Asano. 2005. Human herpesvirus 6 variant B infection in adult patients after unrelated cord blood transplantation. Int. J. Hematol. 81:352-355.
75. Trimarchi, J. M., and J. A. Lees. 2002. Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell Biol. 3:11-20.
76. Tuke, P. W., S. Hawke, P. D. Griffiths, and D. A. Clark. 2004. Distribution and quantification of human herpesvirus 6 in multiple sclerosis and control brains. Mult. Scler. 10:355-359.
77. Ward, K. N., N. J. Andrews, C. M. Verity, E. Miller, and E. M. Ross. 2005. Human herpesviruses-6 and -7 each cause significant neurological morbidity in Britain and Ireland. Arch. Dis. Child 90:619-623.
78. Yamanishi, K. 2002. Human herpesvirus 6 and human herpesvirus 7, p. 2785-2801. In B. N. Fields and D. M. Knipe (ed.), Fields virology, 4th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, PA.
79. Yamanishi, K., T. Okuno, K. Shiraki, M. Takahashi, T. Kondo, Y. Asano, and T. Kurata. 1988. Identification of human herpesvirus-6 as a causal agent for exanthem subitum. Lancet i:1065-1067.
80. Yamashita, N., and T. Morishima. 2005. HHV-6 and seizures. Herpes 12: 46-49.
81. Yao, K., N. Akyani, D. Donati, N. Sengamalay, J. Fotheringham, E. Ghedin, M. Bishop, J. Barrett, F. Kashanchi, and S. Jacobson. 2006. Detection of HHV-6B in post-mortem central nervous system tissue of a post-bone marrow transplant recipient: a multi-virus array analysis. J. Clin. Virol. 37(Suppl. 1):S57-S62.
82. Yoshikawa, T., and Y. Asano. 2000. Central nervous system complications in human herpesvirus-6 infection. Brain Dev. 22:307-314.
83. Yoshikawa, T., Y. Asano, M. Ihira, K. Suzuki, M. Ohashi, S. Suga, K. Kudo, K. Horibe, S. Kojima, K. Kato, T. Matsuyama, and Y. Nishiyama. 2002. Human herpesvirus 6 viremia in bone marrow transplant recipients: clinical features and risk factors. J. Infect. Dis. 185:847-853.
84. Yoshikawa, T., T. Nakashima, S. Suga, Y. Asano, T. Yazaki, H. Kimura, T. Morishima, K. Kondo, and K. Yamanishi. 1992. Human herpesvirus-6 DNA in cerebrospinal fluid of a child with exanthem subitum and meningoencephalitis. Pediatrics 89:888-890.
85. Yoshikawa, T., S. Suga, Y. Asano, T. Nakashima, T. Yazaki, Y. Ono, T. Fujita, K. Tsuzuki, S. Sugiyama, and S. Oshima. 1992. A prospective study of human herpesvirus-6 infection in renal transplantation. Transplantation 54:879-883.
86. Yoshikawa, T., S. Suga, Y. Asano, T. Nakashima, T. Yazaki, R. Sobue, M. Hirano, M. Fukuda, S. Kojima, and T. Matsuyama. 1991. Human herpesvirus-6 infection in bone marrow transplantation. Blood 78:1381-1384.
87. Zerr, D. M. 2006. Human herpesvirus 6 and central nervous system disease in hematopoietic cell transplantation. J. Clin. Virol. 37(Suppl. 1):S52-S56.
88. Zerr, D. M. 2006. Human herpesvirus 6: a clinical update. Herpes 13:20-24.