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. 1986 Dec 9;14(23):9381–9396. doi: 10.1093/nar/14.23.9381

Comparison of promoter suppression in avian and murine retrovirus vectors.

M Emerman, H M Temin
PMCID: PMC311965  PMID: 3025812

Abstract

Previously, we described "promoter suppression" in infectious retrovirus vectors with two genes and an internal promoter. Here, we examined several parameters of promoter suppression and found that the amount of suppression in an integrated retrovirus vector was dependent both on whether the vector was derived from spleen necrosis virus or murine leukemia virus and on which internal promoter was present in the vector. Murine leukemia virus vectors showed less suppression than analogous spleen necrosis virus vectors. Furthermore, the amount of suppression was not dependent on either the relative strengths of the promoters nor the distance between the promoters. Moreover, we found that in vectors in which one promoter was suppressed, there was an inverse correlation between the DNaseI sensitivity of the chromatin surrounding a promoter and the suppression of its expression.

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Selected References

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  1. Adhya S., Gottesman M. Promoter occlusion: transcription through a promoter may inhibit its activity. Cell. 1982 Jul;29(3):939–944. doi: 10.1016/0092-8674(82)90456-1. [DOI] [PubMed] [Google Scholar]
  2. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  3. Breindl M., Harbers K., Jaenisch R. Retrovirus-induced lethal mutation in collagen I gene of mice is associated with an altered chromatin structure. Cell. 1984 Aug;38(1):9–16. doi: 10.1016/0092-8674(84)90521-x. [DOI] [PubMed] [Google Scholar]
  4. Cullen B. R., Lomedico P. T., Ju G. Transcriptional interference in avian retroviruses--implications for the promoter insertion model of leukaemogenesis. Nature. 1984 Jan 19;307(5948):241–245. doi: 10.1038/307241a0. [DOI] [PubMed] [Google Scholar]
  5. Donoghue D. J., Anderson C., Hunter T., Kaplan P. L. Transmission of the polyoma virus middle T gene as the oncogene of a murine retrovirus. Nature. 1984 Apr 19;308(5961):748–750. doi: 10.1038/308748a0. [DOI] [PubMed] [Google Scholar]
  6. Embretson J. E., Temin H. M. Pseudotyped retroviral vectors reveal restrictions to reticuloendotheliosis virus replication in rat cells. J Virol. 1986 Nov;60(2):662–668. doi: 10.1128/jvi.60.2.662-668.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Emerman M., Temin H. M. Genes with promoters in retrovirus vectors can be independently suppressed by an epigenetic mechanism. Cell. 1984 Dec;39(3 Pt 2):449–467. [PubMed] [Google Scholar]
  8. Emerman M., Temin H. M. Quantitative analysis of gene suppression in integrated retrovirus vectors. Mol Cell Biol. 1986 Mar;6(3):792–800. doi: 10.1128/mcb.6.3.792. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Episkopou V., Murphy A. J., Efstratiadis A. Cell-specified expression of a selectable hybrid gene. Proc Natl Acad Sci U S A. 1984 Aug;81(15):4657–4661. doi: 10.1073/pnas.81.15.4657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  11. Hartung S., Jaenisch R., Breindl M. Retrovirus insertion inactivates mouse alpha 1(I) collagen gene by blocking initiation of transcription. 1986 Mar 27-Apr 2Nature. 320(6060):365–367. doi: 10.1038/320365a0. [DOI] [PubMed] [Google Scholar]
  12. Hausler B., Somerville R. L. Interaction in vivo between strong closely spaced constitutive promoters. J Mol Biol. 1979 Jan 25;127(3):353–356. doi: 10.1016/0022-2836(79)90335-8. [DOI] [PubMed] [Google Scholar]
  13. Hwang L. S., Park J., Gilboa E. Role of intron-contained sequences in formation of moloney murine leukemia virus env mRNA. Mol Cell Biol. 1984 Nov;4(11):2289–2297. doi: 10.1128/mcb.4.11.2289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jamieson A. T., Subak-Sharpe J. H. Biochemical studies on the herpes simplex virus-specified deoxypyrimidine kinase activity. J Gen Virol. 1974 Sep;24(3):481–492. doi: 10.1099/0022-1317-24-3-481. [DOI] [PubMed] [Google Scholar]
  15. Jongstra J., Reudelhuber T. L., Oudet P., Benoist C., Chae C. B., Jeltsch J. M., Mathis D. J., Chambon P. Induction of altered chromatin structures by simian virus 40 enhancer and promoter elements. Nature. 1984 Feb 23;307(5953):708–714. doi: 10.1038/307708a0. [DOI] [PubMed] [Google Scholar]
  16. Joyner A. L., Bernstein A. Retrovirus transduction: segregation of the viral transforming function and the herpes simplex virus tk gene in infectious Friend spleen focus-forming virus thymidine kinase vectors. Mol Cell Biol. 1983 Dec;3(12):2191–2202. doi: 10.1128/mcb.3.12.2191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kawai S., Nishizawa M. New procedure for DNA transfection with polycation and dimethyl sulfoxide. Mol Cell Biol. 1984 Jun;4(6):1172–1174. doi: 10.1128/mcb.4.6.1172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Keshet E., Temin H. M. Cell killing by spleen necrosis virus is correlated with a transient accumulation of spleen necrosis virus DNA. J Virol. 1979 Aug;31(2):376–388. doi: 10.1128/jvi.31.2.376-388.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kriegler M., Perez C. F., Hardy C., Botchan M. Transformation mediated by the SV40 T antigens: separation of the overlapping SV40 early genes with a retroviral vector. Cell. 1984 Sep;38(2):483–491. doi: 10.1016/0092-8674(84)90503-8. [DOI] [PubMed] [Google Scholar]
  20. Laimins L., Holmgren-König M., Khoury G. Transcriptional "silencer" element in rat repetitive sequences associated with the rat insulin 1 gene locus. Proc Natl Acad Sci U S A. 1986 May;83(10):3151–3155. doi: 10.1073/pnas.83.10.3151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Miller A. D., Ong E. S., Rosenfeld M. G., Verma I. M., Evans R. M. Infectious and selectable retrovirus containing an inducible rat growth hormone minigene. Science. 1984 Sep 7;225(4666):993–998. doi: 10.1126/science.6089340. [DOI] [PubMed] [Google Scholar]
  22. Miller C. K., Temin H. M. Insertion of several different DNAs in reticuloendotheliosis virus strain T suppresses transformation by reducing the amount of subgenomic mRNA. J Virol. 1986 Apr;58(1):75–80. doi: 10.1128/jvi.58.1.75-80.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Miller T. J., Mertz J. E. Template structural requirements for transcription in vivo by RNA polymerase II. Mol Cell Biol. 1982 Dec;2(12):1595–1607. doi: 10.1128/mcb.2.12.1595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rubenstein J. L., Nicolas J. F., Jacob F. Construction of a retrovirus capable of transducing and expressing genes in multipotential embryonic cells. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7137–7140. doi: 10.1073/pnas.81.22.7137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sorge J., Cutting A. E., Erdman V. D., Gautsch J. W. Integration-specific retrovirus expression in embryonal carcinoma cells. Proc Natl Acad Sci U S A. 1984 Nov;81(21):6627–6631. doi: 10.1073/pnas.81.21.6627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sorge J., Wright D., Erdman V. D., Cutting A. E. Amphotropic retrovirus vector system for human cell gene transfer. Mol Cell Biol. 1984 Sep;4(9):1730–1737. doi: 10.1128/mcb.4.9.1730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Southern P. J., Berg P. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter. J Mol Appl Genet. 1982;1(4):327–341. [PubMed] [Google Scholar]
  28. Stalder J., Groudine M., Dodgson J. B., Engel J. D., Weintraub H. Hb switching in chickens. Cell. 1980 Apr;19(4):973–980. doi: 10.1016/0092-8674(80)90088-4. [DOI] [PubMed] [Google Scholar]
  29. Tabin C. J., Hoffmann J. W., Goff S. P., Weinberg R. A. Adaptation of a retrovirus as a eucaryotic vector transmitting the herpes simplex virus thymidine kinase gene. Mol Cell Biol. 1982 Apr;2(4):426–436. doi: 10.1128/mcb.2.4.426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Taketo M., Gilboa E., Sherman M. I. 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 Apr;82(8):2422–2426. doi: 10.1073/pnas.82.8.2422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Van Beveren C., Rands E., Chattopadhyay S. K., Lowy D. R., Verma I. M. Long terminal repeat of murine retroviral DNAs: sequence analysis, host-proviral junctions, and preintegration site. J Virol. 1982 Feb;41(2):542–556. doi: 10.1128/jvi.41.2.542-556.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wagner E. F., Vanek M., Vennström B. Transfer of genes into embryonal carcinoma cells by retrovirus infection: efficient expression from an internal promoter. EMBO J. 1985 Mar;4(3):663–666. doi: 10.1002/j.1460-2075.1985.tb03680.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wagner M. J., Sharp J. A., Summers W. C. Nucleotide sequence of the thymidine kinase gene of herpes simplex virus type 1. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1441–1445. doi: 10.1073/pnas.78.3.1441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Watanabe S., Temin H. M. Construction of a helper cell line for avian reticuloendotheliosis virus cloning vectors. Mol Cell Biol. 1983 Dec;3(12):2241–2249. doi: 10.1128/mcb.3.12.2241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Weintraub H. Assembly and propagation of repressed and depressed chromosomal states. Cell. 1985 Oct;42(3):705–711. doi: 10.1016/0092-8674(85)90267-3. [DOI] [PubMed] [Google Scholar]
  36. Weintraub H., Cheng P. F., Conrad K. Expression of transfected DNA depends on DNA topology. Cell. 1986 Jul 4;46(1):115–122. doi: 10.1016/0092-8674(86)90865-2. [DOI] [PubMed] [Google Scholar]
  37. Weintraub H., Groudine M. Chromosomal subunits in active genes have an altered conformation. Science. 1976 Sep 3;193(4256):848–856. doi: 10.1126/science.948749. [DOI] [PubMed] [Google Scholar]
  38. Wilkie N. M., Clements J. B., Boll W., Mantei N., Lonsdale D., Weissmann C. Hybrid plasmids containing an active thymidine kinase gene of Herpes simplex virus 1. Nucleic Acids Res. 1979 Oct 25;7(4):859–877. doi: 10.1093/nar/7.4.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Williams D. A., Orkin S. H., Mulligan R. C. Retrovirus-mediated transfer of human adenosine deaminase gene sequences into cells in culture and into murine hematopoietic cells in vivo. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2566–2570. doi: 10.1073/pnas.83.8.2566. [DOI] [PMC free article] [PubMed] [Google Scholar]

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