Retrovirus Silencing, Variegation, Extinction, and Memory Are Controlled by a Dynamic Interplay of Multiple Epigenetic Modifications

Challita, 1994, Lack of expression from a retroviral vector after transduction of murine hematopoietic stem cells is associated with methylation in vivo, Proc. Natl. Acad. Sci. USA, 91, 2567, 10.1073/pnas.91.7.2567 Jahner, 1982, De novo methylation and expression of retroviral genomes during mouse embryogenesis, Nature, 298, 623, 10.1038/298623a0 Klug, 2000, Inactivation of a GFP retrovirus occurs at multiple levels in long-term repopulating stem cells and their differentiated progeny, Blood, 96, 894, 10.1182/blood.V96.3.894 Bird, 2002, DNA methylation patterns and epigenetic memory, Genes Dev, 16, 6, 10.1101/gad.947102 Jenuwein, 2001, Translating the histone code, Science, 293, 1074, 10.1126/science.1063127 Cherry, 2000, Retroviral expression in embryonic stem cells and hematopoietic stem cells, Mol. Cell. Biol, 20, 7419, 10.1128/MCB.20.20.7419-7426.2000 Lorincz, 2000, Dynamic analysis of proviral induction and de novo methylation: implications for a histone deacetylase-independent, methylation density-dependent mechanism of transcriptional repression, Mol. Cell. Biol, 20, 842, 10.1128/MCB.20.3.842-850.2000 Lorincz, 2002, DNA methylation density influences the stability of an epigenetic imprint and Dnmt3a/b-independent de novo methylation, Mol. Cell. Biol, 22, 7572, 10.1128/MCB.22.21.7572-7580.2002 Pannell, 2000, Retrovirus vector silencing is de novo methylase independent and marked by a repressive histone code, EMBO J, 19, 5884, 10.1093/emboj/19.21.5884 Lorincz, 2001, Methylation-mediated proviral silencing is associated with MeCP2 recruitment and localized histone H3 deacetylation, Mol. Cell. Biol, 21, 7913, 10.1128/MCB.21.23.7913-7922.2001 Swindle, 2004, Mutation of CpGs in the murine stem cell virus retroviral vector long terminal repeat represses silencing in embryonic stem cells, J. Biol. Chem, 279, 34, 10.1074/jbc.M309128200 Zentilin, 2000, Variegation of retroviral vector gene expression in myeloid cells, Gene Ther, 7, 153, 10.1038/sj.gt.3301057 Laker, 1998, Host cis-mediated extinction of a retrovirus permissive for expression in embryonal stem cells during differentiation, J. Virol, 72, 339, 10.1128/JVI.72.1.339-348.1998 Niwa, 1983, Independent mechanisms involved in suppression of the Moloney leukemia virus genome during differentiation of murine teratocarcinoma cells, Cell, 32, 1105, 10.1016/0092-8674(83)90294-5 Lois, 2002, Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors, Science, 295, 868, 10.1126/science.1067081 Pfeifer, 2002, Transgenesis by lentiviral vectors: lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos, Proc. Natl. Acad. Sci. USA, 99, 2140, 10.1073/pnas.251682798 Pawliuk, 2001, Correction of sickle cell disease in transgenic mouse models by gene therapy, Science, 294, 2368, 10.1126/science.1065806 Hawley, 1994, Versatile retroviral vectors for potential use in gene therapy, Gene Ther, 1, 136 Tate, 1996, The methyl-CpG binding protein MeCP2 is essential for embryonic development in the mouse, Nat. Genet, 12, 205, 10.1038/ng0296-205 Zufferey, 1998, Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery, J. Virol, 72, 9873, 10.1128/JVI.72.12.9873-9880.1998 Herrera, 2000, Histone H1 is a specific repressor of core histone acetylation in chromatin, Mol. Cell. Biol, 20, 523, 10.1128/MCB.20.2.523-529.2000 Lever, 2000, Rapid exchange of histone H1.1 on chromatin in living human cells, Nature, 408, 873, 10.1038/35048603 Misteli, 2000, Dynamic binding of histone H1 to chromatin in living cells, Nature, 408, 877, 10.1038/35048610 Nan, 1997, MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin, Cell, 88, 471, 10.1016/S0092-8674(00)81887-5 Yu, 2000, Histone deacetylase-independent transcriptional repression by methyl-CpG-binding protein 2, Nucleic Acids Res, 28, 2201, 10.1093/nar/28.10.2201 Georgel, 2003, Chromatin compaction by human MeCP2: assembly of novel secondary chromatin structures in the absence of DNA methylation, J. Biol. Chem, 278, 32181, 10.1074/jbc.M305308200 Schroder, 2002, HIV-1 integration in the human genome favors active genes and local hotspots, Cell, 110, 521, 10.1016/S0092-8674(02)00864-4 Wu, 2003, Transcription start regions in the human genome are favored targets for MLV integration, Science, 300, 1749, 10.1126/science.1083413 Rivella, 2000, The cHS4 insulator increases the probability of retroviral expression at random chromosomal integration sites, J. Virol, 74, 4679, 10.1128/JVI.74.10.4679-4687.2000 Yao, 2003, Retrovirus silencer blocking by the cHS4 insulator is CTCF independent, Nucleic Acids Res, 31, 5317, 10.1093/nar/gkg742 Challita, 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, 10.1128/JVI.69.2.748-755.1995 Osborne, 1999, Amelioration of retroviral vector silencing in locus control region beta-globin-transgenic mice and transduced F9 embryonic cells, J. Virol, 73, 5490, 10.1128/JVI.73.7.5490-5496.1999 Ramalho-Santos, 2002, “Stemness”: transcriptional profiling of embryonic and adult stem cells, Science, 298, 597, 10.1126/science.1072530 Dillon, 2002, Unravelling heterochromatin: competition between positive and negative factors regulates accessibility, Trends Genet, 18, 252, 10.1016/S0168-9525(02)02648-3 Hacein-Bey-Abina, 2003, LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1, Science, 302, 415, 10.1126/science.1088547 Li, 2002, Murine leukemia induced by retroviral gene marking, Science, 296, 497, 10.1126/science.1068893 Ramezani, 2003, Performance- and safety-enhanced lentiviral vectors containing the human interferon-beta scaffold attachment region and the chicken beta-globin insulator, Blood, 101, 4717, 10.1182/blood-2002-09-2991 Kinsella, 1996, Episomal vectors rapidly and stably produce high-titer recombinant retrovirus, Hum. Gene Ther, 7, 1405, 10.1089/hum.1996.7.12-1405