Dynamic DNA methylation and histone modifications contribute to lentiviral transgene silencing in murine embryonic carcinoma cells

Journal of Virology

Volumn 79, Issue 21, 2005, Pages 13497-13508

  He, Jin ^a   Yang, Qing ^a   Chang, Lung Ji ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; DNA; HISTONE H4;

ANIMAL CELL; ARTICLE; CARCINOMA CELL; CELL CLONE; CHROMATIN CONDENSATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DEACETYLATION; DNA METHYLATION; DNA MODIFICATION; EMBRYO; EMBRYONIC STEM CELL; GENE SEQUENCE; GENE SILENCING; IMMUNOPRECIPITATION; KINETICS; LENTIVIRINAE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROVIRUS; SAFETY; SEQUENCE ANALYSIS; TRANSGENE; VIRUS GENOME;

ANIMALS; AZACITIDINE; BETA-GALACTOSIDASE; CHROMATIN; CPG ISLANDS; DNA METHYLATION; GENE SILENCING; HISTONES; LENTIVIRUS; METHYLATION; MICE; PEPTIDE ELONGATION FACTOR 1; PROMOTER REGIONS (GENETICS); TRANSDUCTION, GENETIC; TUMOR STEM CELLS; VIRUS ACTIVATION;

MURINAE;

EID: 27144536258     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.21.13497-13508.2005     Document Type: Article

References (33)

1. Brooks, A. R., R. N. Harkins, P. Wang, H. S. Qian, P. Liu, and G. M. Rubanyi. 2004. Transcriptional silencing is associated with extensive methylation of the CMV promoter following adenoviral gene delivery to muscle. J. Gene Med. 6:395-404.
2. Challita, P. M., D. Skelton, A. El-Khouelry, X. J. Yu, K. Weinberg, and D. B. Kohn. 1995. Multiple modifications in cis elements of the long terminal repeat of retroviral vectors lead to increased expression and decreased DNA methylation in embryonic carcinoma cells. J. Virol. 69:748-755.
3. Cherry, S. R., D. Biniszkiewicz, L. van Parijs, D. Baltimore, and R. Jaenisch. 2000. Retroviral expression in embryonic stem cells and hematopoietic stem cells. Mol. Cell. Biol. 20:7419-7426.
4. Deng, G., A. Chen, E. Pong, and Y. S. Kim. 2001. Methylation in hMLH1 promoter interferes with its binding to transcription factor CBF and inhibits gene expression. Oncogene 20:7120-7127.
5. Fox, A. H., Y. W. Lam, A. K. Leung, C. E. Lyon, J. Andersen, M. Mann, and A. I. Lamond. 2002. Paraspeckles: a novel nuclear domain. Curr. Biol. 12:13-25.
6. Gautsch, J. W., and M. C. Wilson. 1983. Delayed de novo methylation in teratocarcinoma suggests additional tissue-specific mechanisms for controlling gene expression. Nature 301:32-37.
7. Gropp, M., P. Itsykson, O. Singer, T. Ben-Hur, E. Reinhartz, E. Galun, and B. E. Reubinoff. 2003. Stable genetic modification of human embryonic stem cells by lentiviral vectors. Mol. Ther. 7:281-287.
8. Hawley, R. G. 2001. Progress toward vector design for hematopoietic stem cell gene therapy. Curr. Gene Ther. 1:1-17.
9. Hino, S., J. Fan, S. Taguwa, K. Akasaka, and M. Matsuoka. 2004. Sea urchin insulator protects lentiviral vector from silencing by maintaining active chromatin structure. Gene Ther. 11:819-828.
10. Imren, S., E. Payen, K. A. Westerman, R. Pawliuk, M. E. Fabry, C. J. Eaves, B. Cavilla, L. D. Wadsworth, Y. Beuzard, E. E. Bouhassira, R. Russell, I. M. London, R. L. Nagel, P. Leboulch, and R. K. Humphries. 2002. Permanent and panerythroid correction of murine beta thalassemia by multiple lentiviral integration in hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 99:14380-14385.
11. Jahner, D., H. Stuhlmann, C. L. Stewart, K. Harbers, J. Lohler, I. Simon, and R. Jaenisch. 1982. De novo methylation and expression of retroviral genomes during mouse embryogenesis. Nature 298:623-628.
12. Krause, D. S., N. D. Theise, M. I. Collector, O. Henegariu, S. Hwang, R. Gardner, S. Neutzel, and S. J. Sharkis. 2001. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105:369-377.
13. Ku, J. L., S. B. Kang, Y. K. Shin, H. C. Kang, S. H. Hong, I. J. Kim, J. H. Shin, I. O. Han, and J. G. Park. 2004. Promoter hypermethylation down-regulates RUNX3 gene expression in colorectal cancer cell lines. Oncogene 23:6736-6742.
14. LaFace, D., P. Hermonat, E. Wakeland, and A. Peck. 1988. Gene transfer into hematopoietic progenitor cells mediated by an adeno-associated virus vector. Virology 162:483-486.
15. Lois, C., E. J. Hong, S. Pease, E. J. Brown, and D. Baltimore. 2002. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295:868-872.
16. Ma, Y., A. Ramezani, R. Lewis, R. G. Hawley, and J. A. Thomson. 2003. High-level sustained transgene expression in human embryonic stem cells using lentiviral vectors. Stem Cells 21:111-117.
17. May, C., S. Rivella, A. Chadburn, and M. Sadelain. 2002. Successful treatment of murine beta-thalassemia intermedia by transfer of the human beta-globin gene. Blood 99:1902-1908.
18. McBurney, M. W. 1993. P19 embryonal carcinoma cells. Int. J. Dev. Biol. 37:135-140.
19. McBurney, M. W., E. M. Jones-Villeneuve, M. K. Edwards, and P. J. Anderson. 1982. Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line. Nature 299:165-167.
20. Mummaneni, P., K. A. Walker, P. L. Bishop, and M. S. Turker. 1995. Epigenetic gene inactivation induced by a cis-acting methylation center. J. Biol. Chem. 270:788-792.
21. Mutskov, V., and G. Felsenfeld. 2004. Silencing of transgene transcription precedes methylation of promoter DNA and histone H3 lysine 9. EMBO J. 23:138-149.
22. Pannell, D., and J. Ellis. 2001. Silencing of gene expression: implications for design of retrovirus vectors. Rev. Med. Virol. 11:205-217.
23. Pawliuk, R., K. A. Westerman, M. E. Fabry, E. Payen, R. Tighe, E. E. Bouhassira, S. A. Acharya, J. Ellis, I. M. London, C. J. Eaves, R. K. Humphries, Y. Beuzard, R. L. Nagel, and P. Leboulch. 2001. Correction of sickle cell disease in transgenic mouse models by gene therapy. Science 294:2368-2371.
24. Pfeifer, A., M. Ikawa, Y. Dayn, and I. M. Verma. 2002. Transgenesis by lentiviral vectors: lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos. Proc. Natl. Acad. Sci. USA 99:2140-2145.
25. Ramezani, A., T. S. Hawley, and R. G. Hawley. 2003. Performance- and safety-enhanced lentiviral vectors containing the human interferon-beta scaffold attachment region and the chicken beta-globin insulator. Blood 101:4717-4724.
26. Schroder, A., P. Shinn, H. Chen, C. Berry, J. Ecker, and F. Bushman. 2002. HIV-1 Integration in the human genome favors active genes and local hotspots. Cell 110:521-529.
27. Stuhlmann, H., D. Jahner, and R. Jaenisch. 1981. Infectivity and methylation of retroviral genomes is correlated with expression in the animal. Cell 26:221-232.
28. Turker, M. S. 2002. Gene silencing in mammalian cells and the spread of DNA methylation. Oncogene 21:5388-5393.
29. Turner, B. M. 2002. Cellular memory and the histone code. Cell 111:285-291.
30. Uchida, N., R. E. Sutton, A. M. Friera, D. He, M. J. Reitsma, W. C. Chang, G. Veres, R. Scollay, and I. L. Weissman. 1998. HIV, but not murine leukemia virus, vectors mediate high efficiency gene transfer into freshly isolated G0/G1 human hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 95:11939-11944.
31. Wilson, J. M., O. Danos, M. Grossman, D. H. Raulet, and R. C. Mulligan. 1990. Expression of human adenosine deaminase in mice reconstituted with retrovirus-transduced hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 87:439-443.
32. Yao, S., T. Sukonnik, T. Kean, R. R. Bharadwaj, P. Pasceri, and J. Ellis. 2004. Retrovirus silencing, variegation, extinction, and memory are controlled by a dynamic interplay of multiple epigenetic modifications. Mol. Ther. 10:27-36.
33. Zaiss, A.-K., S. Son, and L.-J. Chang. 2002. RNA 3′-readthrough of oncoretrovirus and lentivirus: implications in vector safety and efficacy. J. Virol. 76:7209-7219.