Abstract
We have studied the effects of sodium butyrate on DNA-mediated gene transfer in an effort to investigate interrelationships between chromatin structure and expression of recombinant plasmids. Our results demonstrate that butyrate affects the early stages of gene activity following DNA uptake at least two levels. First, the number of cells able to express foreign DNA increases from 10% to up to 40%. Second, there is an increase in enhancer-dependent transcription, approximately 30 fold in HeLa cells, involving the SV40 early promoter. Stable transformation efficiencies increase to 4% and 10% in HeLa S3 and monkey kidney CV-1 cells, respectively. Finally, expression of integrated recombinant plasmid genes is reinducible by a second treatment five weeks after initial exposure to this agent.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Benoist C., Chambon P. In vivo sequence requirements of the SV40 early promotor region. Nature. 1981 Mar 26;290(5804):304–310. doi: 10.1038/290304a0. [DOI] [PubMed] [Google Scholar]
- Candido E. P., Reeves R., Davie J. R. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell. 1978 May;14(1):105–113. doi: 10.1016/0092-8674(78)90305-7. [DOI] [PubMed] [Google Scholar]
- Cousens L. S., Alberts B. M. Accessibility of newly synthesized chromatin to histone acetylase. J Biol Chem. 1982 Apr 10;257(7):3945–3949. [PubMed] [Google Scholar]
- D'Anna J. A., Tobey R. A., Gurley L. R. Concentration-dependent effects of sodium butyrate in Chinese hamster cells: cell-cycle progression, inner-histone acetylation, histone H1 dephosphorylation, and induction of an H1-like protein. Biochemistry. 1980 Jun 10;19(12):2656–2671. doi: 10.1021/bi00553a019. [DOI] [PubMed] [Google Scholar]
- Davie J. R., Candido E. P. Acetylated histone H4 is preferentially associated with template-active chromatin. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3574–3577. doi: 10.1073/pnas.75.8.3574. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Feinstein S. C., Ross S. R., Yamamoto K. R. Chromosomal position effects determine transcriptional potential of integrated mammary tumor virus DNA. J Mol Biol. 1982 Apr 15;156(3):549–565. doi: 10.1016/0022-2836(82)90266-2. [DOI] [PubMed] [Google Scholar]
- Frost E., Williams J. Mapping temperature-sensitive and host-range mutations of adenovirus type 5 by marker rescue. Virology. 1978 Nov;91(1):39–50. doi: 10.1016/0042-6822(78)90353-7. [DOI] [PubMed] [Google Scholar]
- Ghosh M. K., Cox R. P. Production of human chorionic gonadotropin in HeLa cell cultures. Nature. 1976 Feb 5;259(5542):416–417. doi: 10.1038/259416a0. [DOI] [PubMed] [Google Scholar]
- Ghosh N. K., Deutsch S. I., Griffin M. J., Cox R. P. Regulation of growth and morphological modulation of HeLa65 cells in monolayer culture by dibutyryl cyclic AMP, butyrate and their analogs. J Cell Physiol. 1975 Dec;86 (Suppl 2)(3 Pt 2):663–672. doi: 10.1002/jcp.1040860511. [DOI] [PubMed] [Google Scholar]
- Ginsburg E., Salomon D., Sreevalsan T., Freese E. Growth inhibition and morphological changes caused by lipophilic acids in mammalian cells. Proc Natl Acad Sci U S A. 1973 Aug;70(8):2457–2461. doi: 10.1073/pnas.70.8.2457. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorman C. M., Merlino G. T., Willingham M. C., Pastan I., Howard B. H. The Rous sarcoma virus long terminal repeat is a strong promoter when introduced into a variety of eukaryotic cells by DNA-mediated transfection. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6777–6781. doi: 10.1073/pnas.79.22.6777. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorman C., Padmanabhan R., Howard B. H. High efficiency DNA-mediated transformation of primate cells. Science. 1983 Aug 5;221(4610):551–553. doi: 10.1126/science.6306768. [DOI] [PubMed] [Google Scholar]
- Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
- Gruss P., Dhar R., Khoury G. Simian virus 40 tandem repeated sequences as an element of the early promoter. Proc Natl Acad Sci U S A. 1981 Feb;78(2):943–947. doi: 10.1073/pnas.78.2.943. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hagopian H. K., Riggs M. G., Swartz L. A., Ingram V. M. Effect of n-butyrate on DNA synthesis in chick fibroblasts and HeLa cells. Cell. 1977 Nov;12(3):855–860. doi: 10.1016/0092-8674(77)90284-7. [DOI] [PubMed] [Google Scholar]
- Harland R. M., Weintraub H., McKnight S. L. Transcription of DNA injected into Xenopus oocytes is influenced by template topology. Nature. 1983 Mar 3;302(5903):38–43. doi: 10.1038/302038a0. [DOI] [PubMed] [Google Scholar]
- Harris M. Induction of thymidine kinase in enzyme-deficient Chinese hamster cells. Cell. 1982 Jun;29(2):483–492. doi: 10.1016/0092-8674(82)90165-9. [DOI] [PubMed] [Google Scholar]
- Jakobovits E. B., Bratosin S., Aloni Y. A nucleosome-free region in SV40 minichromosomes. Nature. 1980 May 22;285(5762):263–265. doi: 10.1038/285263a0. [DOI] [PubMed] [Google Scholar]
- Kriegler M., Botchan M. Enhanced transformation by a simian virus 40 recombinant virus containing a Harvey murine sarcoma virus long terminal repeat. Mol Cell Biol. 1983 Mar;3(3):325–339. doi: 10.1128/mcb.3.3.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
- La Bella F., Vidali G., Vesco C. Histone acetylation in CV-1 cells infected with simian virus 40. Virology. 1979 Jul 30;96(2):564–575. doi: 10.1016/0042-6822(79)90112-0. [DOI] [PubMed] [Google Scholar]
- Laimins L. A., Khoury G., Gorman C., Howard B., Gruss P. Host-specific activation of transcription by tandem repeats from simian virus 40 and Moloney murine sarcoma virus. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6453–6457. doi: 10.1073/pnas.79.21.6453. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leder A., Leder P. Butyric acid, a potent inducer of erythroid differentiation in cultured erythroleukemic cells. Cell. 1975 Jul;5(3):319–322. doi: 10.1016/0092-8674(75)90107-5. [DOI] [PubMed] [Google Scholar]
- Levinson B., Khoury G., Vande Woude G., Gruss P. Activation of SV40 genome by 72-base pair tandem repeats of Moloney sarcoma virus. Nature. 1982 Feb 18;295(5850):568–572. doi: 10.1038/295568a0. [DOI] [PubMed] [Google Scholar]
- Levy-Wilson B., Watson D. C., Dixon G. H. Multiacetylated forms of H4 are found in a putative transcriptionally competent chromatin fraction from trout testis. Nucleic Acids Res. 1979 Jan;6(1):259–274. doi: 10.1093/nar/6.1.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Louie A. J., Candido E. P., Dixon G. H. Enzymatic modifications and their possible roles in regulating the binding of basic proteins to DNA and in controlling chromosomal structure. Cold Spring Harb Symp Quant Biol. 1974;38:803–819. doi: 10.1101/sqb.1974.038.01.084. [DOI] [PubMed] [Google Scholar]
- Loyter A., Scangos G. A., Ruddle F. H. Mechanisms of DNA uptake by mammalian cells: fate of exogenously added DNA monitored by the use of fluorescent dyes. Proc Natl Acad Sci U S A. 1982 Jan;79(2):422–426. doi: 10.1073/pnas.79.2.422. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Loyter A., Scangos G., Juricek D., Keene D., Ruddle F. H. Mechanisms of DNA entry into mammalian cells. II. Phagocytosis of calcium phosphate DNA co-precipitate visualized by electron microscopy. Exp Cell Res. 1982 May;139(1):223–234. doi: 10.1016/0014-4827(82)90336-6. [DOI] [PubMed] [Google Scholar]
- Mertz J. E. Linear DNA does not form chromatin containing regularly spaced nucleosomes. Mol Cell Biol. 1982 Dec;2(12):1608–1618. doi: 10.1128/mcb.2.12.1608. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Mottus R., Reeves R., Grigliatti T. A. Butyrate suppression of position-effect variegation in Drosophila melanogaster. Mol Gen Genet. 1980;178(2):465–469. doi: 10.1007/BF00270501. [DOI] [PubMed] [Google Scholar]
- Mulligan R. C., Berg P. Expression of a bacterial gene in mammalian cells. Science. 1980 Sep 19;209(4463):1422–1427. doi: 10.1126/science.6251549. [DOI] [PubMed] [Google Scholar]
- Mulligan R. C., Berg P. Selection for animal cells that express the Escherichia coli gene coding for xanthine-guanine phosphoribosyltransferase. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2072–2076. doi: 10.1073/pnas.78.4.2072. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pellicer A., Wigler M., Axel R., Silverstein S. The transfer and stable integration of the HSV thymidine kinase gene into mouse cells. Cell. 1978 May;14(1):133–141. doi: 10.1016/0092-8674(78)90308-2. [DOI] [PubMed] [Google Scholar]
- Perry M., Chalkley R. Histone acetylation increases the solubility of chromatin and occurs sequentially over most of the chromatin. A novel model for the biological role of histone acetylation. J Biol Chem. 1982 Jul 10;257(13):7336–7347. [PubMed] [Google Scholar]
- Perry M., Chalkley R. The effect of histone hyperacetylation on the nuclease sensitivity and the solubility of chromatin. J Biol Chem. 1981 Apr 10;256(7):3313–3318. [PubMed] [Google Scholar]
- Perucho M., Hanahan D., Wigler M. Genetic and physical linkage of exogenous sequences in transformed cells. Cell. 1980 Nov;22(1 Pt 1):309–317. doi: 10.1016/0092-8674(80)90178-6. [DOI] [PubMed] [Google Scholar]
- Radloff R., Bauer W., Vinograd J. A dye-buoyant-density method for the detection and isolation of closed circular duplex DNA: the closed circular DNA in HeLa cells. Proc Natl Acad Sci U S A. 1967 May;57(5):1514–1521. doi: 10.1073/pnas.57.5.1514. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reeves R., Cserjesi P. Sodium butyrate induces new gene expression in Friend erythroleukemic cells. J Biol Chem. 1979 May 25;254(10):4283–4290. [PubMed] [Google Scholar]
- 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]
- Roman A. Alteration in the simian virus 40 maturation pathway after butyrate-induced hyperacetylation of histones. J Virol. 1982 Dec;44(3):958–962. doi: 10.1128/jvi.44.3.958-962.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saragosti S., Moyne G., Yaniv M. Absence of nucleosomes in a fraction of SV40 chromatin between the origin of replication and the region coding for the late leader RNA. Cell. 1980 May;20(1):65–73. doi: 10.1016/0092-8674(80)90235-4. [DOI] [PubMed] [Google Scholar]
- Schaffhausen B. S., Benjamin T. L. Deficiency in histone acetylation in nontransforming host range mutants of polyoma virus. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1092–1096. doi: 10.1073/pnas.73.4.1092. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scott W. A., Wigmore D. J. Sites in simian virus 40 chromatin which are preferentially cleaved by endonucleases. Cell. 1978 Dec;15(4):1511–1518. doi: 10.1016/0092-8674(78)90073-9. [DOI] [PubMed] [Google Scholar]
- Simpson R. T. Structure of chromatin containing extensively acetylated H3 and H4. Cell. 1978 Apr;13(4):691–699. doi: 10.1016/0092-8674(78)90219-2. [DOI] [PubMed] [Google Scholar]
- 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]
- Ucker D. S., Firestone G. L., Yamamoto K. R. Glucocorticoids and chromosomal position modulate murine mammary tumor virus transcription by affecting efficiency of promoter utilization. Mol Cell Biol. 1983 Apr;3(4):551–561. doi: 10.1128/mcb.3.4.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Varshavsky A. J., Sundin O., Bohn M. A stretch of "late" SV40 viral DNA about 400 bp long which includes the origin of replication is specifically exposed in SV40 minichromosomes. Cell. 1979 Feb;16(2):453–466. doi: 10.1016/0092-8674(79)90021-7. [DOI] [PubMed] [Google Scholar]
- Vidali G., Boffa L. C., Bradbury E. M., Allfrey V. G. Butyrate suppression of histone deacetylation leads to accumulation of multiacetylated forms of histones H3 and H4 and increased DNase I sensitivity of the associated DNA sequences. Proc Natl Acad Sci U S A. 1978 May;75(5):2239–2243. doi: 10.1073/pnas.75.5.2239. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Wright J. A. Morphology and growth rate changes in Chinese hamster cells cultured in presence of sodium butyrate. Exp Cell Res. 1973 Apr;78(2):456–460. doi: 10.1016/0014-4827(73)90091-8. [DOI] [PubMed] [Google Scholar]
- Yamamoto K. R., Alberts B. M. Steroid receptors: elements for modulation of eukaryotic transcription. Annu Rev Biochem. 1976;45:721–746. doi: 10.1146/annurev.bi.45.070176.003445. [DOI] [PubMed] [Google Scholar]
- Zlatanova J., Swetly P. Uncoupled synthesis of histones and DNA during Friend cell differentiation. Nature. 1978 Nov 16;276(5685):276–277. doi: 10.1038/276276a0. [DOI] [PubMed] [Google Scholar]
- 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]