Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1990 Mar;10(3):1126–1133. doi: 10.1128/mcb.10.3.1126

Serum stimulation of the c-fos enhancer induces reversible changes in c-fos chromatin structure.

J L Feng 1, B Villeponteau 1
PMCID: PMC360979  PMID: 2106068

Abstract

Transcription of the proto-oncogene c-fos is known to be activated by growth factors in serum and subsequently repressed by the Fos protein. We show that generalized DNase I sensitivity of c-fos chromatin correlates closely with enhancer activity during induction, repression, and superinduction of the c-fos gene. Within 90 s of serum stimulation, proximal DNA sequences on both sides of the enhancer exhibit increased DNase I sensitivity. Within 5 min, elevated DNase I sensitivity spreads to chromatin at the distal 3' end of the c-fos gene. These results suggest that an open state of chromatin is propagated in both directions from the enhancer. The induced alterations in chromatin structure precede the increased transcriptional activity of the c-fos gene, suggesting that these changes in chromatin structure potentiate transcription.

Full text

PDF
1126

Images in this article

1127Image
on p.1127
1128Image
on p.1128

Selected References

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

  1. Alevy M. C., Tsai M. J., O'Malley B. W. DNase I sensitive domain of the gene coding for the glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase. Biochemistry. 1984 May 8;23(10):2309–2314. doi: 10.1021/bi00305a034. [DOI] [PubMed] [Google Scholar]
  2. Beaudet A. L., O'Brien W. E., Bock H. G., Freytag S. O., Su T. S. The human argininosuccinate synthetase locus and citrullinemia. Adv Hum Genet. 1986;15:161-96, 291-2. doi: 10.1007/978-1-4615-8356-1_3. [DOI] [PubMed] [Google Scholar]
  3. Brinster R. L., Ritchie K. A., Hammer R. E., O'Brien R. L., Arp B., Storb U. Expression of a microinjected immunoglobulin gene in the spleen of transgenic mice. Nature. 1983 Nov 24;306(5941):332–336. doi: 10.1038/306332a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burch J. B., Evans M. I. Chromatin structural transitions and the phenomenon of vitellogenin gene memory in chickens. Mol Cell Biol. 1986 Jun;6(6):1886–1893. doi: 10.1128/mcb.6.6.1886. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  6. Courey A. J., Plon S. E., Wang J. C. The use of psoralen-modified DNA to probe the mechanism of enhancer action. Cell. 1986 May 23;45(4):567–574. doi: 10.1016/0092-8674(86)90288-6. [DOI] [PubMed] [Google Scholar]
  7. Curran T., Peters G., Van Beveren C., Teich N. M., Verma I. M. FBJ murine osteosarcoma virus: identification and molecular cloning of biologically active proviral DNA. J Virol. 1982 Nov;44(2):674–682. doi: 10.1128/jvi.44.2.674-682.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Deschamps J., Meijlink F., Verma I. M. Identification of a transcriptional enhancer element upstream from the proto-oncogene fos. Science. 1985 Dec 6;230(4730):1174–1177. doi: 10.1126/science.3865371. [DOI] [PubMed] [Google Scholar]
  9. Folger K., Anderson J. N., Hayward M. A., Shapiro D. J. Nuclease sensitivity and DNA methylation in estrogen regulation of Xenopus laevis vitellogenin gene expression. J Biol Chem. 1983 Jul 25;258(14):8908–8914. [PubMed] [Google Scholar]
  10. Greenberg M. E., Hermanowski A. L., Ziff E. B. Effect of protein synthesis inhibitors on growth factor activation of c-fos, c-myc, and actin gene transcription. Mol Cell Biol. 1986 Apr;6(4):1050–1057. doi: 10.1128/mcb.6.4.1050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Greenberg M. E., Ziff E. B. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature. 1984 Oct 4;311(5985):433–438. doi: 10.1038/311433a0. [DOI] [PubMed] [Google Scholar]
  12. Gross D. S., Garrard W. T. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem. 1988;57:159–197. doi: 10.1146/annurev.bi.57.070188.001111. [DOI] [PubMed] [Google Scholar]
  13. Hogan B. Molecular biology. Enhancers, chromosome position effects, and transgenic mice. Nature. 1983 Nov 24;306(5941):313–314. doi: 10.1038/306313a0. [DOI] [PubMed] [Google Scholar]
  14. Jantzen K., Fritton H. P., Igo-Kemenes T. The DNase I sensitive domain of the chicken lysozyme gene spans 24 kb. Nucleic Acids Res. 1986 Aug 11;14(15):6085–6099. doi: 10.1093/nar/14.15.6085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lawson G. M., Knoll B. J., March C. J., Woo S. L., Tsai M. J., O'Malley B. W. Definition of 5' and 3' structural boundaries of the chromatin domain containing the ovalbumin multigene family. J Biol Chem. 1982 Feb 10;257(3):1501–1507. [PubMed] [Google Scholar]
  16. McMaster G. K., Carmichael G. G. Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4835–4838. doi: 10.1073/pnas.74.11.4835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Müller R., Bravo R., Burckhardt J., Curran T. Induction of c-fos gene and protein by growth factors precedes activation of c-myc. Nature. 1984 Dec 20;312(5996):716–720. doi: 10.1038/312716a0. [DOI] [PubMed] [Google Scholar]
  18. Sassone-Corsi P., Sisson J. C., Verma I. M. Transcriptional autoregulation of the proto-oncogene fos. Nature. 1988 Jul 28;334(6180):314–319. doi: 10.1038/334314a0. [DOI] [PubMed] [Google Scholar]
  19. Schönthal A., Herrlich P., Rahmsdorf H. J., Ponta H. Requirement for fos gene expression in the transcriptional activation of collagenase by other oncogenes and phorbol esters. Cell. 1988 Jul 29;54(3):325–334. doi: 10.1016/0092-8674(88)90195-x. [DOI] [PubMed] [Google Scholar]
  20. Shepherd J. H., Mulvihill E. R., Thomas P. S., Palmiter R. D. Commitment of chick oviduct tubular gland cells to produce ovalbumin mRNA during hormonal withdrawal and restimulation. J Cell Biol. 1980 Oct;87(1):142–151. doi: 10.1083/jcb.87.1.142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Treisman R. Transient accumulation of c-fos RNA following serum stimulation requires a conserved 5' element and c-fos 3' sequences. Cell. 1985 Oct;42(3):889–902. doi: 10.1016/0092-8674(85)90285-5. [DOI] [PubMed] [Google Scholar]
  24. Villeponteau B., Lundell M., Martinson H. Torsional stress promotes the DNAase I sensitivity of active genes. Cell. 1984 Dec;39(3 Pt 2):469–478. doi: 10.1016/0092-8674(84)90454-9. [DOI] [PubMed] [Google Scholar]
  25. Villeponteau B., Martinson H. G. Gamma rays and bleomycin nick DNA and reverse the DNase I sensitivity of beta-globin gene chromatin in vivo. Mol Cell Biol. 1987 May;7(5):1917–1924. doi: 10.1128/mcb.7.5.1917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Villeponteau B., Martinson H. Isolation and characterization of the complete chicken beta-globin gene region: frequent deletion of the adult beta-globin genes in lambda. Nucleic Acids Res. 1981 Aug 11;9(15):3731–3746. doi: 10.1093/nar/9.15.3731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Williams J. L., Tata J. R. Simultaneous analysis of conformation and transcription of A and B groups of vitellogenin genes in male and female Xenopus during primary and secondary activation by estrogen. Nucleic Acids Res. 1983 Feb 25;11(4):1151–1166. doi: 10.1093/nar/11.4.1151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wood W. I., Felsenfeld G. Chromatin structure of the chicken beta-globin gene region. Sensitivity to DNase I, micrococcal nuclease, and DNase II. J Biol Chem. 1982 Jul 10;257(13):7730–7736. [PubMed] [Google Scholar]
  31. 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]
  32. Zaret K. S., Yamamoto K. R. Reversible and persistent changes in chromatin structure accompany activation of a glucocorticoid-dependent enhancer element. Cell. 1984 Aug;38(1):29–38. doi: 10.1016/0092-8674(84)90523-3. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES