Parvovirus nonstructural proteins induce an epigenetic modification through histone acetylation in host genes and revert tumor malignancy to benignancy

Journal of Virology

Volumn 79, Issue 14, 2005, Pages 8886-8893

  Iseki, Hiroyoshi ^a   Shimizukawa, Rie ^a   Sugiyama, Fumihiro ^a   Kunita, Satoshi ^a   Iwama, Atsushi ^b   Onodera, Masafumi ^a   Nakauchi, Hiromitsu ^b   Yagami, Ken Ichi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AZACITIDINE; BUTYRIC ACID; CILIARY NEUROTROPHIC FACTOR RECEPTOR; CILIARY NEUROTROPHIC FACTOR RECEPTOR ALPHA; COMPLEMENTARY DNA; DNA METHYLTRANSFERASE; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; RNA; TRICHOSTATIN A; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; DNA METHYLATION; DNA SYNTHESIS; EPIGENETICS; FEMALE; GENE EXPRESSION; GROWTH INHIBITION; LYMPHOMA CELL LINE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARVOVIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; THYMOCYTE; TUMOR CELL; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; VIRUS CELL INTERACTION; VIRUS VIRULENCE;

ACETYLATION; ANIMALS; CREB-BINDING PROTEIN; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION PROFILING; HISTONES; MICE; MICE, INBRED BALB C; NEOPLASMS, EXPERIMENTAL; NUCLEAR PROTEINS; PARVOVIRUS; PHENOTYPE; RATS; RECEPTOR, CILIARY NEUROTROPHIC FACTOR; TRANS-ACTIVATORS; VIRAL NONSTRUCTURAL PROTEINS;

PARVOVIRUS;

EID: 21644483935     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.14.8886-8893.2005     Document Type: Article

References (44)

1. Astell, C. R., Q. Liu, C. E. Harris, J. Brunstein, H. K. Jindal, and P. Tam. 1996. Minute virus of mice cis-acting sequences required for genome replication and the role of the trans-acting viral protein, NS-1. Prog. Nucleic Acids Res. Mol. Biol. 55:245-285.
2. Bodendorf, U. C., J. C. Cziepluch, J. Jauniaux, J. Rommelaere, and N. Salome. 1999. Nuclear export factor CRM1 interacts with nonstructural proteins NS2 from parvovirus minute virus of mice. J. Virol. 73:7769-7779.
3. Brandenburger, A., and T. Velu. 2004. Autonomous parvovirus vectors: preventing the generation of wild-type or replication-competent virus. J. Gene Med. 6:S203-211.
4. Brown, R., and G. Strathdee. 2002. Epigenomics and epigenetic therapy of cancer. Trends Mol. Med. 8:S43-8.
5. Cervoni, N., and M. Szyf. 2001. Demethylase activity is directed by histone acetylation. J. Biol. Chem. 276:40778-40787.
6. Chan, H. M., and N. B. La Thangue. 2001. p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J. Cell Sci. 114:2363-2373.
7. Cornelis, J. J., N. Salome, C. Dinsart, and J. Rommelaere. 2004. Vectors based on autonomous parvoviruses: novel tools to treat cancer? J. Gene Med. 6:S193-202.
8. Davis, S., T. H. Aldrich, D. M. Valenzuela, V. V. Wong, M. E. Furth, S. P. Squinto, and G. D. Yancopoulos. 1991. The receptor for ciliary neurotrophic factor. Science 253:59-63.
9. Detich, N., V. Bovenzi, and M. Szyf. 2003. Valproate induces replication-independent active DNA demethylation. J. Biol. Chem. 278:27586-27592.
10. Doerig, C., B. Hirt, P. Beard, and J. P. Antonietti. 1988. Minute virus of mice non-structural protein NS-1 is necessary and sufficient for trans-activation of the viral P39 promoter. J. Gen. Virol. 69:2563-2573.
11. Egger, G., G. Liang, A. Aparicio, and P. A. Jones. 2004. Epigenetics in human disease and prospects for epigenetic therapy. Nature 429:457-463.
12. Elson, G. C., E. Lelievre, C. Guillet, S. Chevalier, H. Plun-Favreau, J. Froger, I. Suard, A. B. de Coignac, Y. Delneste, J. Y. Bonnefoy, J. F. Gauchat, and H. Gascan. 2000. CLF associates with CLC to form a functional heteromeric ligand for the CNTF receptor complex. Nat. Neurosci. 3:867-872.
13. Hsu, T. C., W. J. Wu, M. C. Chen, and G. J. Tsay. 2004. Human parvovirus B19 non-structural protein (NS1) induces apoptosis through mitochondria cell death pathway in COS-7 cells. Scand. J. Infect. Dis. 36:570-577.
14. Iwama, A., P. Zhang, G. J. Darlington, S. R. McKercher, R. Maki, and D. G. Tenen. 1998. Use of RDA analysis of knockout mice to identify myeloid genes regulated in vivo by PU. 1 and C/EBPalpha. Nucleic Acids Res. 26:3034-3043.
15. Jaenisch, R., and A. Bird. 2003. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33:245-254.
16. Jindal, H. K., C. B. Yong, G. M. Wilson, P. Tam, and C. R. Astell. 1994. Mutations in the NTP-binding motif of minute virus of mice (MVM) NS-1 protein uncouple ATPase and DNA helicase functions. J. Biol. Chem. 269:3283-3289.
17. Jones, P. A., and S. B. Baylin. 2002. The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 3:415-428.
18. Kishikawa, S., H. Ugai, T. Murata, and K. K. Yokoyama. 2002. Roles of histone acetylation in the Dnmt1 gene expression. Nucleic Acid Res. Suppl.:209-210.
19. Kiss, C., J. Nishikawa, K. Takada, P. Trivedi, G. Klein, and L. Szekely. 2003. T cell leukemia I oncogene expression depends on the presence of Epstein-Barr virus in the virus-carrying Burkitt lymphoma lines. Proc. Natl. Acad. Sci. USA. 100:4813-4818.
20. Lelievre, E., H. Plun-Favreau, S. Chevalier, J. Froger, C. Guillet, GC. Elson, JF. Gauchat, and H. Gascan. 2001. Signaling pathways recruited by the cardiotrophin-like cytokine/cytokine-like factor-1 composite cytokine: specific requirement of the membrane-bound form of ciliary neurotrophic factor receptor alpha component. J. Biol. Chem. 276:22476-22484.
21. Li, M., B. Damania, X. Alvarez, V. Ogryzko, K. Ozato, and J. U. Jung. 2000. Inhibition of p300 histone acetyltransferase by viral interferon regulatory factor. Mol. Cell Biol. 20:8254-8263.
22. Lopez-Guerrero, J. A., B. Rayet, M. Tuynder, J. Rommelaere, and C. Dinsart. 1997. Constitutive activation of U937 promonocytic cell clones selected for their resistance to parvovirus H-1 infection. Blood 89:1642-1653.
23. Louis, J. C., E. Magal, S. Takayama, and S. Varon. 1993. CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science 259:689-692.
24. Lubyova, B., M. J. Kellum, A. J. Frisancho, and P. M. Pitha. 2004. Kaposi's sarcoma-associated herpesvirus-encoded vIRF-3 stimulates the transcriptional activity of cellular IRF-3 and IRF-7. J. Biol. Chem. 279:7643-7654.
25. Middleton, G., M. Hamanoue, Y. Enokido, S. Wyatt, D. Pennica, E. Jaffray, R. T. Hay, and A. M. Davies. 2000. Cytokine-induced nuclear factor kappa B activation promotes the survival of developing neurons. J. Cell Biol. 148:325-332.
26. Miller, C. L., and D. J. Pintel. 2002. Interaction between parvovirus NS2 protein and nuclear export factor Crm1 is important for viral egress from the nucleus of murine cells. J. Virol. 76:3257-3266.
27. Momparler, R. L. 2003. Cancer epigenetics. Oncogene 22:6479-6483.
28. Ohshima, T., M. Iwama, Y. Ueno, F. Sugiyama, T. Nakajima, A. Fukamizu, and K. Yagami. 1998. Induction of apoptosis in vitro and in vivo by H-1 parvovirus infection. J. Gen. Virol. 79:3067-3071.
29. Ohshima, T., T. Nakajima, T. Oishi, N. Imamoto, Y. Yoneda, A. Fukamizu, and K. Yagami. 1999. CRM1 mediates nuclear export of nonstructural protein 2 from parvovirus minute virus of mice. Biochem. Biophys. Res. Commun. 264:144-150.
30. Ohshima, T., E. Yoshida, T. Nakajima, K. Yagami, and A. Fukamizu. 2001. Effects of interaction between parvovirus minute virus of mice NS1 and coactivator CBP on NS1- and p53-transactivation. Int. J. Mol. Med. 7:49-54.
31. Op De Beeck, A., J. Sobczak-Thepot, H. Sirma, F. Bourgain, C. Brechot, and P. Caillet-Fauquet. 2001. NS1- and minute virus of mice-induced cell cycle arrest: involvement of p53 and p21(cip1). J. Virol. 75:11071-11078.
32. Plun-Favreau, H., G. Elson, M. Chabbert, J. Froger, O. deLapeyriere, E. Lelievre, C. Guillet, J. Hemann, J. F. Gauchat, H. Gascan, and S. Chevalier. 2001. The ciliary neurotrophic factor receptor alpha component induces the secretion of and is required for functional responses to cardiotrophin-like cytokine. EMBO J. 20:1692-1703.
33. Rhode, S. L., 3rd, and S. M. Richard. 1987. Characterization of the transactivation-responsive element of the parvovirus H-1 P38 promoter. J. Virol. 61:2807-2815.
34. Rommelaere, J., and J. J. Cornelis. 1991. Antineoplastic activity of parvoviruses. J. Virol. Methods. 33:233-251.
35. Sol, N., J. Le Junter, I. Vassias, J. M. Freyssinier, A. Thomas, A. F. Prigent, B. B. Rudkin, S. Fichelson, and F. Morinet. 1999. Possible interactions between the NS-1 protein and tumor necrosis factor alpha pathways in erythroid cell apoptosis induced by human parvovirus B19. J. Virol. 73:8762-8770.
36. Sterner, D. E., and S. L. Berger. 2000. Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64:435-459.
37. Suzuki, A., K. Obi, T. Urabe, H. Hayakawa, M. Yamada, S. Kaneko, M. Onodera, Y. Mizuno, and H. Mochizuki. 2002. Feasibility of ex vivo gene therapy for neurological disorders using the new retroviral vector GCDNsap packaged in the vesicular stomatitis virus G protein. J. Neurochem. 82:953-960.
38. Telerman, A., M. Tuynder, T. Dupressoir, R. B. Obaye, F. Sigaux, E. Shaulian, M. Oren, J. Rommelaere, and R. Amson. 1993. A model for tumor suppression using H-1 parvovirus. Proc. Natl. Acad. Sci. USA. 90:8702-8706.
39. Tolosano, E., M. A. Cutufia, E. Hirsch, G. Stefanuto, S. Voyron, A. Fasolo, L. Silengo, and F. Altruda. 1996. Ciliary neurotrophic factor constitutively expressed in the nervous system of transgenic mice protects embryonic dorsal root ganglion neurons from apoptosis. Eur. J. Neurosci. 8:521-529.
40. Ueno, Y., T. Harada, H. Iseki, T. Ohshima, F. Sugiyama, and K. Yagami. 2001. Propagation of rat parvovirus in thymic lymphoma cell line C58(NT)D and subsequent appearance of a resistant cell clone after lytic infection. J. Virol. 75:3965-3970.
41. Valls, E., X. de la Cruz, and M. A. Martinez-Balbas. 2003. The SV40 T antigen modulates CBP histone acetyltransferase activity. Nucleic Acids Res. 31:3114-3122.
42. Villar-Garea, A., and M. Esteller. 2004. Histone deacetylase inhibitors: Understanding a new wave of anticancer agents. Int. J. Cancer 112:171-178.
43. Wilson, G. M., H. K. Jindal, D. E. Yeung, W. Chen, and C. R. Astell. 1991. Expression of minute virus of mice major nonstructural protein in insect cells: purification and identification of ATPase and helicase activities. Virology 185:90-98.
44. Yaegashi, N., T. Niinuma, H. Chisaka, S. Uehara, S. Moffatt, K. Tada, M. Iwabuchi, Y. Matsunaga, M. Nakayama, C. Yutani, Y. Osamura, E. Hirayama, K. Okamura, K. Sugamura, and A. Yajima. 1999. Parvovirus B19 infection induces apoptosis of erythroid cells in vitro and in vivo. J. Infect. 39:68-76.