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. 1985 Nov;5(11):2924–2935. doi: 10.1128/mcb.5.11.2924

Sequence-dependent DNA replication in preimplantation mouse embryos.

D O Wirak, L E Chalifour, P M Wassarman, W J Muller, J A Hassell, M L DePamphilis
PMCID: PMC369103  PMID: 3018487

Abstract

Circular, double-stranded DNA molecules were injected into nuclei of mouse oocytes and one- or two-cell embryos to determine whether specific sequences were required to replicate DNA during mouse development. Although all of the injected DNAs were stable, replication of plasmid pML-1 DNA was not detected unless it contained either polyomavirus (PyV) or simian virus 40 (SV40) DNA sequences. Replication occurred in embryos, but not in oocytes. PyV DNA, either alone or recombined with pML-1, underwent multiple rounds of replication to produce superhelical and relaxed circular monomers after injection into one- or two-cell embryos. SV40 DNA also replicated, but only 3% as well as PyV DNA. Coinjection of PyV DNA with either pML-1 or SV40 had no effect on the replicating properties of the three DNAs. These results are consistent with a requirement for specific cis-acting sequences to replicate DNA in mammalian embryos, in contrast to sequence-independent replication of DNA injected into Xenopus eggs. Furthermore, PyV DNA replication in mouse embryos required PyV large T-antigen and either the alpha-beta-core or beta-core configuration of the PyV origin of replication. Although the alpha-core configuration replicated in differentiated mouse cells, it failed to replicate in mouse embryos, demonstrating cell-specific activation of an origin of replication. Replication or expression of PyV DNA interfered with normal embryonic development. These results reveal that mouse embryos are permissive for PyV DNA replication, in contrast to the absence of PyV DNA replication and gene expression in mouse embryonal carcinoma cells.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abramczuk J., Solter D., Koprowski H. The beneficial effect EDTA on development of mouse one-cell embryos in chemically defined medium. Dev Biol. 1977 Dec;61(2):378–383. doi: 10.1016/0012-1606(77)90308-6. [DOI] [PubMed] [Google Scholar]
  2. Anderson S., Kaufman G., DePamphilis M. L. RNA primers in SV40 DNA replication: identification of transient RNA-DNA covalent linkages in replicating DNA. Biochemistry. 1977 Nov 15;16(23):4990–4998. doi: 10.1021/bi00642a009. [DOI] [PubMed] [Google Scholar]
  3. Ariga H., Tsuchihashi Z., Naruto M., Yamada M. Cloned mouse DNA fragments can replicate in a simian virus 40 T antigen-dependent system in vivo and in vitro. Mol Cell Biol. 1985 Mar;5(3):563–568. doi: 10.1128/mcb.5.3.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bensaude O., Babinet C., Morange M., Jacob F. Heat shock proteins, first major products of zygotic gene activity in mouse embryo. Nature. 1983 Sep 22;305(5932):331–333. doi: 10.1038/305331a0. [DOI] [PubMed] [Google Scholar]
  5. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blumenthal A. B., Kriegstein H. J., Hogness D. S. The units of DNA replication in Drosophila melanogaster chromosomes. Cold Spring Harb Symp Quant Biol. 1974;38:205–223. doi: 10.1101/sqb.1974.038.01.024. [DOI] [PubMed] [Google Scholar]
  7. Boccara M., Kelly F. Etude de la sensibilité au virus du polyome et à SV40 de plusieurs lignées cellulaires de tératocarcinome. Ann Microbiol (Paris) 1978 Feb-Mar;129(2):227–238. [PubMed] [Google Scholar]
  8. Brinster R. L., Chen H. Y., Warren R., Sarthy A., Palmiter R. D. Regulation of metallothionein--thymidine kinase fusion plasmids injected into mouse eggs. Nature. 1982 Mar 4;296(5852):39–42. doi: 10.1038/296039a0. [DOI] [PubMed] [Google Scholar]
  9. Brinster R. L. Lactate dehydrogenase activity in the preimplanted mouse embryo. Biochim Biophys Acta. 1965 Nov 22;110(2):439–441. doi: 10.1016/s0926-6593(65)80056-x. [DOI] [PubMed] [Google Scholar]
  10. Calza R. E., Eckhardt L. A., DelGiudice T., Schildkraut C. L. Changes in gene position are accompanied by a change in time of replication. Cell. 1984 Mar;36(3):689–696. doi: 10.1016/0092-8674(84)90349-0. [DOI] [PubMed] [Google Scholar]
  11. Campbell B. A., Villarreal L. P. Host species specificity of polyomavirus DNA replication is not altered by simian virus 40 72-base-pair repeats. Mol Cell Biol. 1985 Jun;5(6):1534–1537. doi: 10.1128/mcb.5.6.1534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chambers J. C., Watanabe S., Taylor J. H. Dissection of a replication origin of Xenopus DNA. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5572–5576. doi: 10.1073/pnas.79.18.5572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chia W., Rigby P. W. Fate of viral DNA in nonpermissive cells infected with simian virus 40. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6638–6642. doi: 10.1073/pnas.78.11.6638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Clegg K. B., Pikó L. Poly(A) length, cytoplasmic adenylation and synthesis of poly(A)+ RNA in early mouse embryos. Dev Biol. 1983 Feb;95(2):331–341. doi: 10.1016/0012-1606(83)90034-9. [DOI] [PubMed] [Google Scholar]
  15. Cowie A., Kamen R. Multiple binding sites for polyomavirus large T antigen within regulatory sequences of polyomavirus DNA. J Virol. 1984 Dec;52(3):750–760. doi: 10.1128/jvi.52.3.750-760.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Cowie A., Tyndall C., Kamen R. Sequences at the capped 5'-ends of polyoma virus late region mRNAs: an example of extreme terminal heterogeneity. Nucleic Acids Res. 1981 Dec 11;9(23):6305–6322. doi: 10.1093/nar/9.23.6305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dandolo L., Blangy D., Kamen R. Regulation of polyoma virus transcription in murine embryonal carcinoma cells. J Virol. 1983 Jul;47(1):55–64. doi: 10.1128/jvi.47.1.55-64.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dilworth S. M., Cowie A., Kamen R. I., Griffin B. E. DNA binding activity of polyoma virus large tumor antigen. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1941–1945. doi: 10.1073/pnas.81.7.1941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dubensky T. W., Murphy F. A., Villarreal L. P. Detection of DNA and RNA virus genomes in organ systems of whole mice: patterns of mouse organ infection by polyomavirus. J Virol. 1984 Jun;50(3):779–783. doi: 10.1128/jvi.50.3.779-783.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fangman W. L., Hice R. H., Chlebowicz-Sledziewska E. ARS replication during the yeast S phase. Cell. 1983 Mar;32(3):831–838. doi: 10.1016/0092-8674(83)90069-7. [DOI] [PubMed] [Google Scholar]
  21. Flach G., Johnson M. H., Braude P. R., Taylor R. A., Bolton V. N. The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J. 1982;1(6):681–686. doi: 10.1002/j.1460-2075.1982.tb01230.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Forbes D. J., Kirschner M. W., Newport J. W. Spontaneous formation of nucleus-like structures around bacteriophage DNA microinjected into Xenopus eggs. Cell. 1983 Aug;34(1):13–23. doi: 10.1016/0092-8674(83)90132-0. [DOI] [PubMed] [Google Scholar]
  23. Fujimura F. K., Deininger P. L., Friedmann T., Linney E. Mutation near the polyoma DNA replication origin permits productive infection of F9 embryonal carcinoma cells. Cell. 1981 Mar;23(3):809–814. doi: 10.1016/0092-8674(81)90445-1. [DOI] [PubMed] [Google Scholar]
  24. Fujimura F. K., Linney E. Polyoma mutants that productively infect F9 embryonal carcinoma cells do not rescue wild-type polyoma in F9 cells. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1479–1483. doi: 10.1073/pnas.79.5.1479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Fujimura F. K., Silbert P. E., Eckhart W., Linney E. Polyoma virus infection of retinoic acid-induced differentiated teratocarcinoma cells. J Virol. 1981 Jul;39(1):306–312. doi: 10.1128/jvi.39.1.306-312.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gargiulo G., Razvi F., Worcel A. Assembly of transcriptionally active chromatin in Xenopus oocytes requires specific DNA binding factors. Cell. 1984 Sep;38(2):511–521. doi: 10.1016/0092-8674(84)90506-3. [DOI] [PubMed] [Google Scholar]
  27. Graessmann M., Graessman A. "Early" simian-virus-40-specific RNA contains information for tumor antigen formation and chromatin replication. Proc Natl Acad Sci U S A. 1976 Feb;73(2):366–370. doi: 10.1073/pnas.73.2.366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Harland R. M., Laskey R. A. Regulated replication of DNA microinjected into eggs of Xenopus laevis. Cell. 1980 Oct;21(3):761–771. doi: 10.1016/0092-8674(80)90439-0. [DOI] [PubMed] [Google Scholar]
  29. Hay R. T., Hendrickson E. A., DePamphilis M. L. Sequence specificity for the initiation of RNA-primed simian virus 40 DNA synthesis in vivo. J Mol Biol. 1984 May 15;175(2):131–157. doi: 10.1016/0022-2836(84)90471-6. [DOI] [PubMed] [Google Scholar]
  30. Heintz N. H., Milbrandt J. D., Greisen K. S., Hamlin J. L. Cloning of the initiation region of a mammalian chromosomal replicon. 1983 Mar 31-Apr 6Nature. 302(5907):439–441. doi: 10.1038/302439a0. [DOI] [PubMed] [Google Scholar]
  31. Herbomel P., Bourachot B., Yaniv M. Two distinct enhancers with different cell specificities coexist in the regulatory region of polyoma. Cell. 1984 Dec;39(3 Pt 2):653–662. doi: 10.1016/0092-8674(84)90472-0. [DOI] [PubMed] [Google Scholar]
  32. Herbomel P., Saragosti S., Blangy D., Yaniv M. Fine structure of the origin-proximal DNAase I-hypersensitive region in wild-type and EC mutant polyoma. Cell. 1981 Sep;25(3):651–658. doi: 10.1016/0092-8674(81)90172-0. [DOI] [PubMed] [Google Scholar]
  33. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. doi: 10.1016/0022-2836(67)90307-5. [DOI] [PubMed] [Google Scholar]
  34. Jat P., Novak U., Cowie A., Tyndall C., Kamen R. DNA sequences required for specific and efficient initiation of transcription at the polyoma virus early promoter. Mol Cell Biol. 1982 Jul;2(7):737–751. doi: 10.1128/mcb.2.7.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Johnson M. H. The molecular and cellular basis of preimplantation mouse development. Biol Rev Camb Philos Soc. 1981 Aug;56(3):463–498. doi: 10.1111/j.1469-185x.1981.tb00356.x. [DOI] [PubMed] [Google Scholar]
  36. Katinka M., Yaniv M. DNA replication origin of polyoma virus: early proximal boundary. J Virol. 1983 Jul;47(1):244–248. doi: 10.1128/jvi.47.1.244-248.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kelly F., Condamine H. Tumor viruses and early mouse embryos. Biochim Biophys Acta. 1982 Apr 29;651(2-3):105–141. doi: 10.1016/0304-419X(82)90009-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Lacks S., Greenberg B. Complementary specificity of restriction endonucleases of Diplococcus pneumoniae with respect to DNA methylation. J Mol Biol. 1977 Jul;114(1):153–168. doi: 10.1016/0022-2836(77)90289-3. [DOI] [PubMed] [Google Scholar]
  39. Laskey R. A., Mills A. D., Morris N. R. Assembly of SV40 chromatin in a cell-free system from Xenopus eggs. Cell. 1977 Feb;10(2):237–243. doi: 10.1016/0092-8674(77)90217-3. [DOI] [PubMed] [Google Scholar]
  40. Laskey R. A. The use of intensifying screens or organic scintillators for visualizing radioactive molecules resolved by gel electrophoresis. Methods Enzymol. 1980;65(1):363–371. doi: 10.1016/s0076-6879(80)65047-2. [DOI] [PubMed] [Google Scholar]
  41. Linney E., Donerly S. DNA fragments from F9 PyEC mutants increase expression of heterologous genes in transfected F9 cells. Cell. 1983 Dec;35(3 Pt 2):693–699. doi: 10.1016/0092-8674(83)90102-2. [DOI] [PubMed] [Google Scholar]
  42. Lusky M., Botchan M. Inhibition of SV40 replication in simian cells by specific pBR322 DNA sequences. Nature. 1981 Sep 3;293(5827):79–81. doi: 10.1038/293079a0. [DOI] [PubMed] [Google Scholar]
  43. Luthardt F. W., Donahue R. P. Pronuclear DNA synthesis in mouse eggs. An autoradiographic study. Exp Cell Res. 1973 Nov;82(1):143–151. doi: 10.1016/0014-4827(73)90256-5. [DOI] [PubMed] [Google Scholar]
  44. Luthman H., Nilsson M. G., Magnusson G. Non-contiguous segments of the polyoma genome required in cis for DNA replication. J Mol Biol. 1982 Nov 15;161(4):533–550. doi: 10.1016/0022-2836(82)90406-5. [DOI] [PubMed] [Google Scholar]
  45. Mariani B. D., Schimke R. T. Gene amplification in a single cell cycle in Chinese hamster ovary cells. J Biol Chem. 1984 Feb 10;259(3):1901–1910. [PubMed] [Google Scholar]
  46. Martin G. R. Teratocarcinomas and mammalian embryogenesis. Science. 1980 Aug 15;209(4458):768–776. doi: 10.1126/science.6250214. [DOI] [PubMed] [Google Scholar]
  47. McCutchan J. H., Pagano J. S. Enchancement of the infectivity of simian virus 40 deoxyribonucleic acid with diethylaminoethyl-dextran. J Natl Cancer Inst. 1968 Aug;41(2):351–357. [PubMed] [Google Scholar]
  48. McKnight S. L., Miller O. L., Jr Electron microscopic analysis of chromatin replication in the cellular blastoderm Drosophila melanogaster embryo. Cell. 1977 Nov;12(3):795–804. doi: 10.1016/0092-8674(77)90278-1. [DOI] [PubMed] [Google Scholar]
  49. McTiernan C. F., Stambrook P. J. Initiation of SV40 DNA replication after microinjection into Xenopus eggs. Biochim Biophys Acta. 1984 Jul 18;782(3):295–303. doi: 10.1016/0167-4781(84)90065-4. [DOI] [PubMed] [Google Scholar]
  50. 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]
  51. Mueller C. R., Mes-Masson A. M., Bouvier M., Hassell J. A. Location of sequences in polyomavirus DNA that are required for early gene expression in vivo and in vitro. Mol Cell Biol. 1984 Dec;4(12):2594–2609. doi: 10.1128/mcb.4.12.2594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Muggleton-Harris A., Whittingham D. G., Wilson L. Cytoplasmic control of preimplantation development in vitro in the mouse. Nature. 1982 Sep 30;299(5882):460–462. doi: 10.1038/299460a0. [DOI] [PubMed] [Google Scholar]
  53. Muller W. J., Mueller C. R., Mes A. M., Hassell J. A. Polyomavirus origin for DNA replication comprises multiple genetic elements. J Virol. 1983 Sep;47(3):586–599. doi: 10.1128/jvi.47.3.586-599.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Méchali M., Kearsey S. Lack of specific sequence requirement for DNA replication in Xenopus eggs compared with high sequence specificity in yeast. Cell. 1984 Aug;38(1):55–64. doi: 10.1016/0092-8674(84)90526-9. [DOI] [PubMed] [Google Scholar]
  55. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell. 1982 Oct;30(3):675–686. doi: 10.1016/0092-8674(82)90272-0. [DOI] [PubMed] [Google Scholar]
  56. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell. 1982 Oct;30(3):687–696. doi: 10.1016/0092-8674(82)90273-2. [DOI] [PubMed] [Google Scholar]
  57. Osheim Y. N., Miller O. L., Jr Novel amplification and transcriptional activity of chorion genes in Drosophila melanogaster follicle cells. Cell. 1983 Jun;33(2):543–553. doi: 10.1016/0092-8674(83)90435-x. [DOI] [PubMed] [Google Scholar]
  58. Pomerantz B. J., Mueller C. R., Hassell J. A. Polyomavirus large T antigen binds independently to multiple, unique regions on the viral genome. J Virol. 1983 Sep;47(3):600–610. doi: 10.1128/jvi.47.3.600-610.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  60. Rothwell V. M., Folk W. R. Comparison of the DNA sequence of the Crawford small-plaque variant of polyomavirus with those of polyomaviruses A2 and strain 3. J Virol. 1983 Nov;48(2):472–480. doi: 10.1128/jvi.48.2.472-480.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sawicki W., Abramczuk J., Blaton O. DNA synthesis in the second and third cell cycles of mouse preimplantation development. A cytophotometric study. Exp Cell Res. 1978 Mar 1;112(1):199–205. doi: 10.1016/0014-4827(78)90540-2. [DOI] [PubMed] [Google Scholar]
  62. Segal S., Levine A. J., Khoury G. Evidence for non-spliced SV40 RNA in undifferentiated murine teratocarcinoma stem cells. Nature. 1979 Jul 26;280(5720):335–338. doi: 10.1038/280335a0. [DOI] [PubMed] [Google Scholar]
  63. Sekikawa K., Levine A. J. Isolation and characterization of polyoma host range mutants that replicate in nullipotential embryonal carcinoma cells. Proc Natl Acad Sci U S A. 1981 Feb;78(2):1100–1104. doi: 10.1073/pnas.78.2.1100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  65. Stark G. R., Wahl G. M. Gene amplification. Annu Rev Biochem. 1984;53:447–491. doi: 10.1146/annurev.bi.53.070184.002311. [DOI] [PubMed] [Google Scholar]
  66. Stern S., Wassarman P. M. Meiotic maturation of the mammalian oocyte in vitro: effect of dibutyryl cyclic AMP on protein synthesis. J Exp Zool. 1974 Aug;189(2):275–281. doi: 10.1002/jez.1401890217. [DOI] [PubMed] [Google Scholar]
  67. Struhl K. The new yeast genetics. 1983 Sep 29-Oct 5Nature. 305(5933):391–397. doi: 10.1038/305391a0. [DOI] [PubMed] [Google Scholar]
  68. Swartzendruber D. E., Lehman J. M. Neoplastic differentiation: interaction of simian virus 40 and polyoma virus with murine teratocarcinoma cells in vitro. J Cell Physiol. 1975 Apr;85(2 Pt 1):179–187. doi: 10.1002/jcp.1040850204. [DOI] [PubMed] [Google Scholar]
  69. Tapper D. P., DePamphilis M. L. Discontinuous DNA replication: accumulation of Simian virus 40 DNA at specific stages in its replication. J Mol Biol. 1978 Apr 15;120(3):401–422. doi: 10.1016/0022-2836(78)90427-8. [DOI] [PubMed] [Google Scholar]
  70. Tyndall C., La Mantia G., Thacker C. M., Favaloro J., Kamen R. A region of the polyoma virus genome between the replication origin and late protein coding sequences is required in cis for both early gene expression and viral DNA replication. Nucleic Acids Res. 1981 Dec 11;9(23):6231–6250. doi: 10.1093/nar/9.23.6231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Vasseur M., Katinka M., Herbomel P., Yaniv M., Blangy D. Physical and biological features of polyoma virus mutants able to infect embryonal carcinoma cell lines. J Virol. 1982 Sep;43(3):800–808. doi: 10.1128/jvi.43.3.800-808.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Wahl G. M., Stern M., Stark G. R. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. doi: 10.1073/pnas.76.8.3683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Wassarman P. M., Josefowicz W. J. Oocyte development in the mouse: an ultrastructural comparison of oocytes isolated at various stages of growth and meiotic competence. J Morphol. 1978 May;156(2):209–235. doi: 10.1002/jmor.1051560206. [DOI] [PubMed] [Google Scholar]
  74. Whitten W. K., Biggers J. D. Complete development in vitro of the pre-implantation stages of the mouse in a simple chemically defined medium. J Reprod Fertil. 1968 Nov;17(2):399–401. doi: 10.1530/jrf.0.0170399. [DOI] [PubMed] [Google Scholar]
  75. Wyllie A. H., Laskey R. A., Finch J., Gurdon J. B. Selective DNA conservation and chromatin assembly after injection of SV40 DNA into Xenopus oocytes. Dev Biol. 1978 May;64(1):178–188. doi: 10.1016/0012-1606(78)90069-6. [DOI] [PubMed] [Google Scholar]
  76. Zakian V. A. Electron microscopic analysis of DNA replication in main band and satellite DNAs of Drosophila virilis. J Mol Biol. 1976 Dec;108(2):305–331. doi: 10.1016/s0022-2836(76)80123-4. [DOI] [PubMed] [Google Scholar]
  77. de Villiers J., Olson L., Tyndall C., Schaffner W. Transcriptional 'enhancers' from SV40 and polyoma virus show a cell type preference. Nucleic Acids Res. 1982 Dec 20;10(24):7965–7976. doi: 10.1093/nar/10.24.7965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. de Villiers J., Schaffner W. A small segment of polyoma virus DNA enhances the expression of a cloned beta-globin gene over a distance of 1400 base pairs. Nucleic Acids Res. 1981 Dec 11;9(23):6251–6264. doi: 10.1093/nar/9.23.6251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. de Villiers J., Schaffner W., Tyndall C., Lupton S., Kamen R. Polyoma virus DNA replication requires an enhancer. Nature. 1984 Nov 15;312(5991):242–246. doi: 10.1038/312242a0. [DOI] [PubMed] [Google Scholar]

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