Silencing and variegation of gammaretrovirus and lentivirus vectors

Human Gene Therapy

Volumn 16, Issue 11, 2005, Pages 1241-1246

  Ellis, James ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLOBIN; DNA; GREEN FLUORESCENT PROTEIN; LENTIVIRUS VECTOR; METHYLTRANSFERASE; RETROVIRUS VECTOR;

BIOSAFETY; CARCINOMA CELL; CELL DIFFERENTIATION; CYTOMEGALOVIRUS; DNA METHYLATION; GENE EXPRESSION; GENE SILENCING; GENE TRANSFER; HEMATOPOIETIC STEM CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LONG INTERSPERSED REPEAT; LONG TERMINAL REPEAT; MATRIX ATTACHMENT REGION; MICROINJECTION; MURINE LEUKEMIA VIRUS; NEURAL STEM CELL; NONHUMAN; POSITION EFFECT VARIEGATION; PROMOTER REGION; REPORTER GENE; REVIEW; SCID MOUSE; SILENCER ELEMENT; TRANSGENIC MOUSE; VIRAL GENE THERAPY; VIRUS DNA CELL DNA INTERACTION; WILD TYPE;

ANIMALS; GAMMARETROVIRUS; GENE SILENCING; GENETIC VECTORS; LENTIVIRUS; MICE; MICE, TRANSGENIC; STEM CELLS; TRANSCRIPTION, GENETIC; VIRUS INTEGRATION;

CYTOMEGALOVIRUS; GAMMARETROVIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRUS; MURINE LEUKEMIA VIRUS; MUS MUSCULUS;

EID: 27744489220     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2005.16.1241     Document Type: Review

References (68)

1. AILLES, L., SCHMIDT, M., SANTONI DE SIO, F.R., GLIMM, H., CAVALIERI, S., BRUNO, S., PIACIBELLO, W., VON KALLE, C., and NALDINI, L. (2002). Molecular evidence of lentiviral vector-mediated gene transfer into human self-renewing, multi-potent, long-term NOD/SCID repopulating hematopoietic cells. Mol. Ther. 6, 615-626.
2. BARKLIS, E., MULLIGAN, R.C., and JAENISCH, R. (1986). Chromosomal position or virus mutation permits retrovirus expression in embryonal carcinoma cells. Cell 47, 391-399.
3. CHALLITA, P.M., and KOHN, D.B. (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. U.S.A. 91, 2567-2571.
4. CHALLITA, P.M., SKELTON, D., EL-KHOUEIRY, A., YU, X.J., WEINBERG, K., and KOHN, D.B. (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.
5. COLICELLI, J., and GOFF, S.P. (1986). Isolation of a recombinant murine leukemia virus utilizing a new primer tRNA. J. Virol. 57, 37-45.
6. CONSIGLIO, A., GRITTI, A., DOLCETTA, D., FOLLENZI, A., BORDIGNON, C., GAGE, F.H., VESCOVI, A.L., and NALDINI, L. (2004). Robust in vivo gene transfer into adult mammalian neural stem cells by lentiviral vectors. Proc. Natl. Acad. Sci. U.S.A. 101, 14835-14840.
7. DANG, Q., AUTEN, J., and PLAVEC, I. (2000). Human β interferon scaffold attachment region inhibits de novo methylation and confers long-term, copy number-dependent expression to a retroviral vector. J. Virol. 74, 2671-2678.
8. ELLIS, J., and YAO, S. (2005). Retrovirus silencing and vector design: Relevance to normal and cancer stem cells? Curr. Gene Ther. 5, 367-373.
9. EMERY, D.W., YANNAKI, E., TUBB, J., and STAMATOY-ANNOPOULOS, G. (2000). A chromatin insulator protects retrovirus vectors from chromosomal position effects. Proc. Natl. Acad. Sci. U.S.A. 97, 9150-9155.
10. GAUTSCH, J.W., and WILSON, M.C. (1983). Delayed de novo methylation in teratocarcinoma suggests additional tissue-specific mechanisms for controlling gene expression. Nature 301, 32-37.
11. GREZ, M., AKGUN, E., HILBERG, F., and OSTERTAG, W. (1990). Embryonic stem cell virus, a recombinant murine retrovirus with expression in embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 87, 9202-9206.
12. GROPP, M., ITSYKSON, P., SINGER, O., BEN-HUR, T., REINHARTZ, E., GALUN, E., and REUBINOFF, B.E. (2003). Stable genetic modification of human embryonic stem cells by lentiviral vectors. Mol. Ther. 7, 281-287.
13. HAAS, D.L., LUTZKO, C., LOGAN, A.C., CHO, G.J., SKELTON, D., JIN YU, X., PEPPER, K.A., and KOHN, D.B. (2003). The Moloney murine leukemia virus repressor binding site represses expression in murine and human hematopoietic stem cells. J. Virol. 77, 9439-9450.
14. HAMAGUCHI, I., WOODS, N.B., PANAGOPOULOS, I., ANDERSSON, E., MIKKOLA, H., FAHLMAN, C., ZUFFEREY, R., CARLSSON, L., TRONO, D., and KARLSSON, S. (2000). Lentivirus vector gene expression during ES cell-derived hematopoietic development in vitro. J. Virol. 74, 10778-10784.
15. HAMRA, F.K., GATLIN, J., CHAPMAN, K.M., GRELLHESL, D.M., GARCIA, J.V., HAMMER, R.E., and GARBERS, D.L. (2002). Production of transgenic rats by lentiviral transduction of male germ-line stem cells. Proc. Natl. Acad. Sci. U.S.A. 99, 14931-14936.
16. HAWLEY, R.G., LIEU, F.H., FONG, A.Z., and HAWLEY, T.S. (1994). Versatile retroviral vectors for potential use in gene therapy. Gene Ther. 1, 136-138.
17. HILBERG, F., STOCKING, C., OSTERTAG, W., and GREZ, M. (1987). Functional analysis of a retroviral host-range mutant: Altered long terminal repeat sequences allow expression in embryonal carcinoma cells. Proc. Natl. Acad. Sci. U.S.A. 84, 5232-5236.
18. HINO, S., FAN, J., TAGUWA, S., AKASAKA, K., and MATSUOKA, M. (2004). Sea urchin insulator protects lentiviral vector from silencing by maintaining active chromatin structure. Gene Ther. 11, 819-828.
19. HOFMANN, A., KESSLER, B., EWERLING, S., WEPPERT, M., VOGG, B., LUDWIG, H., STOJKOVIC, M., BOELHAUVE, M., BREM, G., WOLF, E., and PFEIFER, A. (2003). Efficient transgenesis in farm animals by lentiviral vectors. EMBO Rep. 4, 1054-1060.
20. IBA, H., MIZUTANI, T., and ITO, T. (2003). SWI/SNF chromatin remodelling complex and retroviral gene silencing. Rev. Med. Virol. 13, 99-110.
21. IKAWA, M., TANAKA, N., KAO, W.W., and VERMA, I.M. (2003). Generation of transgenic mice using lentiviral vectors: A novel preclinical assessment of lentiviral vectors for gene therapy. Mol. Ther. 8, 666-673.
22. IMREN, S., PAYEN, E., WESTERMAN, K.A., PAWLIUK, R., FABRY, M.E., EAVES, C.J., CAVILLA, B., WADSWORTH, L.D., BEUZARD, Y., BOUHASSIRA, E.E., RUSSELL, R., LONDON, I.M., NAGEL, R.L., LEBOULCH, P., and HUMPHRIES, R.K. (2002). Permanent and panerythroid correction of murine β thalassemia by multiple lentiviral integration in hematopoietic stem cells. Proc. Natl. Acad. Sci. U.S.A. 99, 14380-14385.
23. JAHNER, D., STUHLMANN, H., STEWART, C.L., HARBERS, K., LOHLER, J., SIMON, I., and JAENISCH, R. (1982). De novo methylation and expression of retroviral genomes during mouse embryogenesis. Nature 298, 623-628.
24. JAKOBSSON, J., ROSENQVIST, N., THOMPSON, L., BARRAUD, P., and LUNDBERG, C. (2004). Dynamics of transgene expression in a neural stem cell line transduced with lentiviral vectors incorporating the cHS4 insulator. Exp. Cell Res. 298, 611-623.
25. KALBERER, C.P., PAWLIUK, R., IMREN, S., BACHELOT, T., TAKEKOSHI, K.J., FABRY, M., EAVES, C.J., LONDON, I.M., HUMPHRIES, R.K., and LEBOULCH, P. (2000). Preselection of retrovirally transduced bone marrow avoids subsequent stem cell gene silencing and age-dependent extinction of expression of human β-globin in engrafted mice. Proc. Natl. Acad. Sci. U.S.A. 97, 5411-5415.
26. + baboon repopulating cells. Blood 102, 3117-3119.
27. KUSTIKOVA, O., FEHSE, B., MODLICH, U., YANG, M., DULLMANN, J., KAMINO, K., VON NEUHOFF, N., SCHLEGELBERGER, B., LI, Z., and BAUM, C. (2005). Clonal dominance of hematopoietic stem cells triggered by retroviral gene marking. Science 308, 1171-1174.
28. KUSTIKOVA, O.S., WAHLERS, A., KUHLCKE, K., STAHLE, B., ZANDER, A.R., BAUM, C., and FEHSE, B. (2003). Dose finding with retroviral vectors: Correlation of retroviral vector copy numbers in single cells with gene transfer efficiency in a cell population. Blood 102, 3934-3937.
29. LAKER, C., MEYER, J., SCHOPEN, A., FRIEL, J., HEBERLEIN, C., OSTERTAG, W., and STOCKING, C. (1998). Host cis-mediated extinction of a retrovirus permissive for expression in embryonal stem cells during differentiation. J. Virol. 72, 339-348.
30. LEWINSKI, M.K., BISGROVE, D., SHINN, P., CHEN, H., HOFFMANN, C., HANNENHALLI, S., VERDIN, E., BERRY, C.C., ECKER, J.R., and BUSHMAN, F.D. (2005). Genome-wide analysis of chromosomal features repressing human immunodeficiency virus transcription. J. Virol. 79, 6610-6619.
31. LOIS, C., HONG, E.J., PEASE, S., BROWN, E.J., and BALTIMORE, D. (2002). Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295, 868-872.
32. MA, Y., RAMEZANI, A., LEWIS, R., HAWLEY, R.G., and THOMSON, J.A. (2003). High-level sustained transgene expression in human embryonic stem cells using lentiviral vectors. Stem Cells 21, 111-117.
33. MAY, C., RIVELLA, S., CALLEGARI, J., HELLER, G., GAENSLER, K.M., LUZZATTO, L., and SADELAIN, M. (2000). Therapeutic haemoglobin synthesis in β-thalassaemic mice expressing lentivirus-encoded human β-globin. Nature 406, 82-86.
34. McCUNE, S.L., and TOWNES, T.M. (1994). Retroviral vector sequences inhibit human β-globin gene expression in transgenic mice. Nucleic Acids Res. 22, 4477-4481.
35. MIKKOLA, H., WOODS, N.B., SJOGREN, M., HELGADOTTIR, H., HAMAGUCHI, I., JACOBSEN, S.E., TRONO, D., and KARLSSON, S. (2000). Lentivirus gene transfer in murine hematopoietic progenitor cells is compromised by a delay in proviral integration and results in transduction mosaicism and heterogeneous gene expression in progeny cells. J. Virol. 74, 11911-11918.
36. MITCHELL, R.S., BEITZEL, B.F., SCHRODER, A.R., SHINN, P., CHEN, H., BERRY, C.C., ECKER, J.R., and BUSHMAN, F.D. (2004). Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol. 2, E234.
37. + cells that mediate long-term engraftment of NOD/SCID mice by HIV vectors. Science 283, 682-686.
38. MODIN, C., PEDERSEN, F.S., and DUCH, M. (2000). Lack of shielding of primer binding site silencer-mediated repression of an internal promoter in a retrovirus vector by the putative insulators scs, BEAD-1, and HS4. J. Virol. 74, 11697-11707.
39. MOHAMEDALI, A., MOREAU-GAUDRY, F., RICHARD, E., XIA, P., NOLTA, J., and MALIK, P. (2004). Self-inactivating lentiviral vectors resist proviral methylation but do not confer position-independent expression in hematopoietic stem cells. Mol. Ther. 10, 249-259.
40. NALDINI, L., BLOMER, U., GALLAY, P., ORY, D., MULLIGAN, R., GAGE, F.H., VERMA, I.M., and TRONO, D. (1996). In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272, 263-267.
41. NIWA, O., YOKOTA, Y., ISHIDA, H., and SUGAHARA, T. (1983). Independent mechanisms involved in suppression of the Moloney leukemia virus genome during differentiation of murine teratocarcinoma cells. Cell 32, 1105-1113.
42. OSBORNE, C.S., PASCERI, P., SINGAL, R., SUKONNIK, T., GINDER, G.D., and ELLIS, J. (1999). Amelioration of retroviral vector silencing in locus control region β-globin transgenic mice and transduced F9 embryonic cells. J. Virol. 73, 5490-5496.
43. PANNELL, D., and ELLIS, J. (2001). Silencing of gene expression: Implications for design of retrovirus vectors. Rev. Med. Virol. 11, 205-217.
44. PANNELL, D., OSBORNE, C.S., YAO, S., SUKONNIK, T., PASCERI, P., KARAISKAKIS, A., OKANO, M., LI, E., LIPSHITZ, H.D., and ELLIS, J. (2000). Retrovirus vector silencing is de novo methylase independent and marked by a repressive histone code. EMBO J. 19, 5884-5894.
45. PAWLIUK, R., WESTERMAN, K.A., FABRY, M.E., PAYEN, E., TIGHE, R., BOUHASSIRA, E.E., ACHARYA, S.A., ELLIS, J., LONDON, I.M., EAVES, C.J., HUMPHRIES, R.K., BEUZARD, Y., NAGEL, R.L., and LEBOULCH, P. (2001). Correction of sickle cell disease in transgenic mouse models by gene therapy. Science 294, 2368-2371.
46. PERSONS, D.A., HARGROVE, P.W., ALLAY, E.R., HANAWA, H., and NIENHUIS, A.W. (2003). The degree of phenotypic correction of murine β-thalassemia intermedia following lentiviral-mediated transfer of a human gamma-globin gene is influenced by chromosomal position effects and vector copy number. Blood 101, 2175-2183.
47. PFEIFER, A., IKAWA, M., DAYN, Y., and VERMA, I.M. (2002). Transgenesis by lentiviral vectors: Lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos. Proc. Natl. Acad. Sci. U.S.A. 99, 2140-2145.
48. RAMEZANI, A., HAWLEY, T.S., and HAWLEY, R.G. (2003). Performance- and safety-enhanced lentiviral vectors containing the human interferon-β scaffold attachment region and the chicken β-globin insulator. Blood 101, 4717-4724.
49. RECILLAS-TARGA, F., PIKAART, M.J., BURGESS-BEUSSE, B., BELL, A.C., LITT, M.D., WEST, A.G., GASZNER, M., and FELSENFELD, G. (2002). Position-effect protection and enhancer blocking by the chicken β-globin insulator are separable activities. Proc. Natl. Acad. Sci. U.S.A. 99, 6883-6888.
50. RIVELLA, S., CALLEGARI, J.A., MAY, C., TAN, C.W., and SADELAIN, M. (2000). The cHS4 insulator increases the probability of retroviral expression at random chromosomal integration sites. J. Virol. 74, 4679-4687.
51. ROBBINS, P.B., YU, X.J., SKELTON, D.M., PEPPER, K.A., WASSERMAN, R.M., ZHU, L., and KOHN, D.B. (1997). Increased probability of expression from modified retroviral vectors in embryonal stem cells and embryonal carcinoma cells. J. Virol. 71, 9466-9474.
52. ROBBINS, P.B., SKELTON, D.C., YU, X.J., HALENE, S., LEONARD, E.H., and KOHN, D.B. (1998). Consistent, persistent expression from modified retroviral vectors in murine hematopoietic stem cells. Proc. Natl. Acad. Sci. U.S.A. 95, 10182-10187.
53. SCHRODER, A., SHINN, P., CHEN, H., BERRY, C., ECKER, J., and BUSHMAN, F. (2002). HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110, 521.
54. SIMON, D., STUHLMANN, H., JAHNER, D., WAGNER, H., WERNER, E., and JAENISCH, R. (1983). Retrovirus genomes methylated by mammalian but not bacterial methylase are non-infectious. Nature 304, 275-277.
55. SPEERS, W.C., GAUTSCH, J.W., and DIXON, F.J. (1980). Silent infection of murine embryonal carcinoma cells by Moloney murine leukemia virus. Virology 105, 241-244.
56. STEWART, C.L., STUHLMANN, H., JAHNER, D., and JAENISCH, R. (1982). De novo methylation, expression, and infectivity of retroviral genomes introduced into embryonal carcinoma cells. Proc. Natl. Acad. Sci. U.S.A. 79, 4098-4102.
57. SWINDLE, C.S., and KLUG, C.A. (2002). Mechanisms that regulate silencing of gene expression from retroviral vectors. J. Hematother. Stem Cell Res. 11, 449-456.
58. SWINDLE, C.S., KIM, H.G., and KLUG, C.A. (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, 34-41.
59. TEICH, N.M., WEISS, R.A., MARTIN, G.R., and LOWY, D.R. (1977). Virus infection of murine teratocarcinoma stem cell lines. Cell 12, 973-982.
60. VROEMEN, M., WEIDNER, N., and BLESCH, A. (2005). Loss of gene expression in lentivirus- and retrovirus-transduced neural progenitor cells is correlated to migration and differentiation in the adult spinal cord. Exp. Neurol. 195, 127-139.
61. WEIHER, H., BARKLIS, E., OSTERTAG, W., and JAENISCH, R. (1987). Two distinct sequence elements mediate retroviral gene expression in embryonal carcinoma cells. J. Virol. 61, 2742-2746.
62. WOODS, N.B., MUESSIG, A., SCHMIDT, M., FLYGARE, J., OLSSON, K., SALMON, P., TRONO, D., VON KALLE, C., and KARLSSON, S. (2003). Lentiviral vector transduction of NOD/SCID repopulating cells results in multiple vector integrations per transduced cell: Risk of insertional mutagenesis. Blood 101, 1284-1289.
63. WU, X., LI, Y., CRISE, B., and BURGESS, S.M. (2003). Transcription start regions in the human genome are favored targets for MLV integration. Science 300, 1749-1751.
64. YAO, S., OSBORNE, C.S., BHARADWAJ, R.R., PASCERI, P., SUKONNIK, T., PANNELL, D., RECILLAS-TARGA, F., WEST, A.G., and ELLIS, J. (2003). Retrovirus silencer blocking by the cHS4 insulator is CTCF independent. Nucleic Acids Res. 31, 5317-5323.
65. YAO, S., SUKONNIK, T., KEAN, T., BHARADWAJ, R.R., PASCERI, P., and ELLIS, J. (2004). Retrovirus silencing, variegation, extinction, and memory are controlled by a dynamic interplay of multiple epigenetic modifications. Mol. Ther. 10, 27-36.
66. YU, S.F., VON RUDEN, T., KANTOFF, P.W., GARBER, C., SEIBERG, M., RUTHER, U., ANDERSON, W.F., WAGNER, E.F., and GILBOA, E. (1986). Self-inactivating retroviral vectors designed for transfer of whole genes into mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 83, 3194-3198.
67. ZENTILIN, L., QIN, G., TAFURO, S., DINAUER, M.C., BAUM, C., and GIACCA, M. (2000). Variegation of retroviral vector gene expression in myeloid cells. Gene Ther. 7, 153-166.
68. ZUFFEREY, R., DULL, T., MANDEL, R.J., BUKOVSKY, A., QUIROZ, D., NALDINI, L., and TRONO, D. (1998). Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J. Virol. 72, 9873-9880.