Asynchronous transcriptional silencing of individual retroviral genomes in embryonic cells

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Schlesinger, Sharon ^a   Meshorer, Eran ^b   Goff, Stephen P ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Chromatin modifications; Embryonic stem cells; Transcriptional silencing

Indexed keywords

RETROVIRUS VECTOR; VIRUS DNA;

ARTICLE; CONTROLLED STUDY; EMBRYONAL CARCINOMA STEM CELL; EPIGENETICS; GENE EXPRESSION; GENE LOCUS; GENE SILENCING; GENETIC TRANSCRIPTION; GENETIC TRANSDUCTION; MOLONEY LEUKEMIA ONCOVIRUS; NONHUMAN; RETROVIRUS; VIRUS GENOME; 3T3 CELL LINE; ANIMAL; CELL LINE; EMBRYONIC STEM CELL; GENE VECTOR; GENETIC EPIGENESIS; GENETICS; MOLONEY MURINE LEUKEMIA VIRUS; MOUSE; PHYSIOLOGY; RETROVIRIDAE;

MOLONEY MURINE LEUKEMIA VIRUS;

ANIMALS; CELL LINE; DNA, VIRAL; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; GENE SILENCING; GENETIC VECTORS; GENOME, VIRAL; MICE; MOLONEY MURINE LEUKEMIA VIRUS; NIH 3T3 CELLS; RETROVIRIDAE; TRANSCRIPTION, GENETIC;

EID: 84899977580     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-11-31     Document Type: Article

References (33)

1. Balázsi G, van Oudenaarden A, Collins J. Cellular decision making and biological noise: from microbes to mammals. Cell 2011, 144:910-925.
2. Raser J, O'Shea E. Control of stochasticity in eukaryotic gene expression. Science (New York, NY) 2004, 304:1811-1814.
3. Martinez Arias A, Brickman J. Gene expression heterogeneities in embryonic stem cell populations: origin and function. Curr Opin Cell Biol 2011, 23:650-656.
4. Buchanan FQ, Rochette-Egly C, Asson-Batres MA. Detection of variable levels of RARalpha and RARgamma proteins in pluripotent and differentiating mouse embryonal carcinoma and mouse embryonic stem cells. Cell Tissue Res 2011, 346:43-51.
5. Hayashi K, Lopes S, Tang F, Surani M. Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 2008, 3:391-401.
6. Kobayashi T, Mizuno H, Imayoshi I, Furusawa C, Shirahige K, Kageyama R. The cyclic gene Hes1 contributes to diverse differentiation responses of embryonic stem cells. Gene Dev 2009, 23:1870-1875.
7. Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, Robertson M, Vrana J, Jones K, Grotewold L, Smith A. Nanog safeguards pluripotency and mediates germline development. Nature 2007, 450:1230-1234.
8. Franz K, Singh A, Weinberger LS. Lentiviral vectors to study stochastic noise in gene expression. "Synthetic Biology, Part A", Methods in Enzymology, Volume 497 2011, 603-622. Amsterdam NL/Academic Press, NY NY: Elsevier, Voight C.
9. Teich NM, Weiss RA, Martin GR, Lowy DR. Virus infection of murine teratocarcinoma stem cell lines. Cell 1977, 12:973-982.
10. Bogerd HP, Wiegand HL, Hulme AE, Garcia-Perez JL, O'Shea KS, Moran JV, Cullen BR. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci U S A 2006, 103:8780-8785.
11. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, Maillard PV, Layard-Liesching H, Verp S, Marquis J, Spitz F, Constam DB, Trono D. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 2010, 463:237-240.
12. Harada F, Peters GG, Dahlberg JE. The primer tRNA for Moloney murine leukemia virus DNA synthesis. Nucleotide sequence and aminoacylation of tRNAPro. J Biol Chem 1979, 254:10979-10985.
13. Petersen R, Kempler G, Barklis E. A stem cell-specific silencer in the primer-binding site of a retrovirus. Mol Cell Biol 1991, 11:1214-1221.
14. Wolf D, Goff SP. TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell 2007, 131:46-57.
15. Wolf D, Goff SP. Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 2009, 458:1201-1204.
16. Pannell D, Ellis J. Silencing of gene expression: implications for design of retrovirus vectors. Rev Med Virol 2001, 11:205-217.
17. Cherry SR, Biniszkiewicz D, van Parijs L, Baltimore D, Jaenisch R. Retroviral expression in embryonic stem cells and hematopoietic stem cells. Mol Cell Biol 2000, 20:7419-7426.
18. Lueders KK, Kuff EL. Sequences associated with intracisternal A particles are reiterated in the mouse genome. Cell 1977, 12:963-972.
19. Schlesinger S, Goff S. Silencing of proviruses in embryonic cells: efficiency, stability and chromatin modifications. EMBO Rep 2013, 14:73-79.
20. Santoni FA, Guerra J, Luban J. HERV-H RNA is abundant in human embryonic stem cells and a precise marker for pluripotency. Retrovirology 2012, 9:111.
21. Wong RC, Ibrahim A, Fong H, Thompson N, Lock LF, Donovan PJ. L1TD1 is a marker for undifferentiated human embryonic stem cells. PLoS One 2011, 6:e19355.
22. Berstine EG, Hooper ML, Grandchamp S, Ephrussi B. Alkaline phosphatase activity in mouse teratoma. Proc Natl Acad Sci U S A 1973, 70:3899-3903.
23. Artzt K, Dubois P, Bennett D, Condamine H, Babinet C, Jacob F. Surface antigens common to mouse cleavage embryos and primitive teratocarcinoma cells in culture. Proc Natl Acad Sci U S A 1973, 70:2988-2992.
24. Macfarlan T, Gifford W, Driscoll S, Lettieri K, Rowe H, Bonanomi D, Firth A, Singer O, Trono D, Pfaff S. Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 2012, 487:57-63.
25. Katz R, Jack-Scott E, Narezkina A, Palagin I, Boimel P, Kulkosky J, Nicolas E, Greger J, Skalka A. High-frequency epigenetic repression and silencing of retroviruses can be antagonized by histone deacetylase inhibitors and transcriptional activators, but uniform reactivation in cell clones is restricted by additional mechanisms. J Virol 2007, 81:2592-2604.
26. Taketo M, Gilboa E, Sherman MI. Isolation of embryonal carcinoma cell lines that express integrated recombinant genes flanked by the Moloney murine leukemia virus long terminal repeat. Proc Natl Acad Sci U S A 1985, 82:2422-2426.
27. Sorge J, Cutting AE, Erdman VD, Gautsch JW. Integration-specific retrovirus expression in embryonal carcinoma cells. Proc Natl Acad Sci U S A 1984, 81:6627-6631.
28. Swartzendruber DE, Lehman JM. Neoplastic differentiation: interaction of simian virus 40 and polyoma virus with murine teratocarcinoma cells in vitro. J Cell Physiol 1975, 85:179-187.
29. Venters BJ, Wachi S, Mavrich TN, Andersen BE, Jena P, Sinnamon AJ, Jain P, Rolleri NS, Jiang C, Hemeryck-Walsh C, Pugh BF. A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol Cell 2011, 41:480-492.
30. Maamar H, Raj A, Dubnau D. Noise in gene expression determines cell fate in Bacillus subtilis. Science 2007, 317:526-529.
31. Carey LB, van Dijk D, Sloot PM, Kaandorp JA, Segal E. Promoter sequence determines the relationship between expression level and noise. PLoS Biol 2013, 11:e1001528.
32. Barklis E, Mulligan RC, Jaenisch R. Chromosomal position or virus mutation permits retrovirus expression in embryonal carcinoma cells. Cell 1986, 47:391-399.
33. Ooi SK, Wolf D, Hartung O, Agarwal S, Daley GQ, Goff SP, Bestor TH. Dynamic instability of genomic methylation patterns in pluripotent stem cells. Epigenetics Chromatin 2010, 3:17.