Skip to main content
PMC home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1992 Oct;12(10):4400–4411. doi: 10.1128/mcb.12.10.4400

Histone H2B gene transcription during Xenopus early development requires functional cooperation between proteins bound to the CCAAT and octamer motifs.

C Hinkley 1, M Perry 1
PMCID: PMC360364  PMID: 1406629

Abstract

The ubiquitously expressed transcription factor Oct-1 and several other members of the POU domain protein family bind to a site, termed the octamer motif, that functions in the promoter and enhancer regions of a variety of genes expressed under diverse conditions. An octamer motif present in a conserved histone H2B-specific promoter element is required for S-phase-specific transcription of mammalian histone H2B genes in cultured cells. We have previously shown that the octamer motif in a Xenopus histone H2B gene promoter was inactive in nondividing frog oocytes. Here we show that the octamer motif, in addition to regulatory elements (TATAA, CCAAT, and ATF motifs) that are active in oocytes, is required for maximal H2B gene transcription in developing frog embryos. Factors binding to each of the H2B upstream promoter elements are present in oocytes and increase slightly in abundance during early development. The activity of the H2B octamer motif in embryos is not specifically associated with increased binding by Oct-1 or the appearance of novel octamer-binding proteins but requires the presence of an intact CCAAT motif. Our results indicate that synergistic interactions among promoter-bound factors are important for octamer-dependent H2B transcription. We suggest that the activity of the H2B promoter is regulated primarily by changes in the interactions between proteins already bound to the promoter rather than by alterations in their intrinsic abilities to bind DNA.

Full text

PDF
4403

Images in this article

4402Image
on p.4402
4403Image
on p.4403
4403Image
on p.4403
4404Image
on p.4404
4405Image
on p.4405
4406Image
on p.4406
4408Image
on p.4408

Selected References

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

  1. Ach R. A., Weiner A. M. Cooperation between CCAAT and octamer motifs in the distal sequence element of the rat U3 small nucleolar RNA promoter. Nucleic Acids Res. 1991 Aug 11;19(15):4209–4218. doi: 10.1093/nar/19.15.4209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Artishevsky A., Wooden S., Sharma A., Resendez E., Jr, Lee A. S. Cell-cycle regulatory sequences in a hamster histone promoter and their interactions with cellular factors. 1987 Aug 27-Sep 2Nature. 328(6133):823–827. doi: 10.1038/328823a0. [DOI] [PubMed] [Google Scholar]
  3. Bell J., Char B. R., Maxson R. An octamer element is required for the expression of the alpha H2B histone gene during the early development of the sea urchin. Dev Biol. 1992 Apr;150(2):363–371. doi: 10.1016/0012-1606(92)90248-f. [DOI] [PubMed] [Google Scholar]
  4. Brüggemeier U., Kalff M., Franke S., Scheidereit C., Beato M. Ubiquitous transcription factor OTF-1 mediates induction of the MMTV promoter through synergistic interaction with hormone receptors. Cell. 1991 Feb 8;64(3):565–572. doi: 10.1016/0092-8674(91)90240-y. [DOI] [PubMed] [Google Scholar]
  5. Chodosh L. A., Baldwin A. S., Carthew R. W., Sharp P. A. Human CCAAT-binding proteins have heterologous subunits. Cell. 1988 Apr 8;53(1):11–24. doi: 10.1016/0092-8674(88)90483-7. [DOI] [PubMed] [Google Scholar]
  6. Dalton S., Wells J. R. Maximal binding levels of an H1 histone gene-specific factor in S-phase correlate with maximal H1 gene transcription. Mol Cell Biol. 1988 Oct;8(10):4576–4578. doi: 10.1128/mcb.8.10.4576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davidson I., Xiao J. H., Rosales R., Staub A., Chambon P. The HeLa cell protein TEF-1 binds specifically and cooperatively to two SV40 enhancer motifs of unrelated sequence. Cell. 1988 Sep 23;54(7):931–942. doi: 10.1016/0092-8674(88)90108-0. [DOI] [PubMed] [Google Scholar]
  8. DeLisle A. J., Graves R. A., Marzluff W. F., Johnson L. F. Regulation of histone mRNA production and stability in serum-stimulated mouse 3T6 fibroblasts. Mol Cell Biol. 1983 Nov;3(11):1920–1929. doi: 10.1128/mcb.3.11.1920. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dorn A., Bollekens J., Staub A., Benoist C., Mathis D. A multiplicity of CCAAT box-binding proteins. Cell. 1987 Sep 11;50(6):863–872. doi: 10.1016/0092-8674(87)90513-7. [DOI] [PubMed] [Google Scholar]
  10. Fletcher C., Heintz N., Roeder R. G. Purification and characterization of OTF-1, a transcription factor regulating cell cycle expression of a human histone H2b gene. Cell. 1987 Dec 4;51(5):773–781. doi: 10.1016/0092-8674(87)90100-0. [DOI] [PubMed] [Google Scholar]
  11. Gerster T., Roeder R. G. A herpesvirus trans-activating protein interacts with transcription factor OTF-1 and other cellular proteins. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6347–6351. doi: 10.1073/pnas.85.17.6347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gonzalez G. A., Yamamoto K. K., Fischer W. H., Karr D., Menzel P., Biggs W., 3rd, Vale W. W., Montminy M. R. A cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence. Nature. 1989 Feb 23;337(6209):749–752. doi: 10.1038/337749a0. [DOI] [PubMed] [Google Scholar]
  13. Hai T. W., Liu F., Coukos W. J., Green M. R. Transcription factor ATF cDNA clones: an extensive family of leucine zipper proteins able to selectively form DNA-binding heterodimers. Genes Dev. 1989 Dec;3(12B):2083–2090. doi: 10.1101/gad.3.12b.2083. [DOI] [PubMed] [Google Scholar]
  14. Harris M. E., Böhni R., Schneiderman M. H., Ramamurthy L., Schümperli D., Marzluff W. F. Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two posttranscriptional steps. Mol Cell Biol. 1991 May;11(5):2416–2424. doi: 10.1128/mcb.11.5.2416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Harvey R. P., Robins A. J., Wells J. R. Independently evolving chicken histone H2B genes: identification of a ubiquitous H2B-specific 5' element. Nucleic Acids Res. 1982 Dec 11;10(23):7851–7863. doi: 10.1093/nar/10.23.7851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Heindl L. M., Weil T. S., Perry M. Promoter sequences required for transcription of Xenopus laevis histone genes in injected frog oocyte nuclei. Mol Cell Biol. 1988 Sep;8(9):3676–3682. doi: 10.1128/mcb.8.9.3676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Heintz N., Sive H. L., Roeder R. G. Regulation of human histone gene expression: kinetics of accumulation and changes in the rate of synthesis and in the half-lives of individual histone mRNAs during the HeLa cell cycle. Mol Cell Biol. 1983 Apr;3(4):539–550. doi: 10.1128/mcb.3.4.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Herr W., Sturm R. A., Clerc R. G., Corcoran L. M., Baltimore D., Sharp P. A., Ingraham H. A., Rosenfeld M. G., Finney M., Ruvkun G. The POU domain: a large conserved region in the mammalian pit-1, oct-1, oct-2, and Caenorhabditis elegans unc-86 gene products. Genes Dev. 1988 Dec;2(12A):1513–1516. doi: 10.1101/gad.2.12a.1513. [DOI] [PubMed] [Google Scholar]
  19. Hinkley C. S., Martin J. F., Leibham D., Perry M. Sequential expression of multiple POU proteins during amphibian early development. Mol Cell Biol. 1992 Feb;12(2):638–649. doi: 10.1128/mcb.12.2.638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hinkley C., Perry M. A variant octamer motif in a Xenopus H2B histone gene promoter is not required for transcription in frog oocytes. Mol Cell Biol. 1991 Feb;11(2):641–654. doi: 10.1128/mcb.11.2.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hoeffler J. P., Meyer T. E., Yun Y., Jameson J. L., Habener J. F. Cyclic AMP-responsive DNA-binding protein: structure based on a cloned placental cDNA. Science. 1988 Dec 9;242(4884):1430–1433. doi: 10.1126/science.2974179. [DOI] [PubMed] [Google Scholar]
  22. Hwang I., Chae C. B. S-phase-specific transcription regulatory elements are present in a replication-independent testis-specific H2B histone gene. Mol Cell Biol. 1989 Mar;9(3):1005–1013. doi: 10.1128/mcb.9.3.1005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ingraham H. A., Flynn S. E., Voss J. W., Albert V. R., Kapiloff M. S., Wilson L., Rosenfeld M. G. The POU-specific domain of Pit-1 is essential for sequence-specific, high affinity DNA binding and DNA-dependent Pit-1-Pit-1 interactions. Cell. 1990 Jun 15;61(6):1021–1033. doi: 10.1016/0092-8674(90)90067-o. [DOI] [PubMed] [Google Scholar]
  24. Ito M., Sharma A., Lee A. S., Maxson R. Cell cycle regulation of H2b histone octamer DNA-binding activity in Chinese hamster lung fibroblasts. Mol Cell Biol. 1989 Feb;9(2):869–873. doi: 10.1128/mcb.9.2.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Janson L., Pettersson U. Cooperative interactions between transcription factors Sp1 and OTF-1. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4732–4736. doi: 10.1073/pnas.87.12.4732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kemler I., Bucher E., Seipel K., Müller-Immerglück M. M., Schaffner W. Promoters with the octamer DNA motif (ATGCAAAT) can be ubiquitous or cell type-specific depending on binding affinity of the octamer site and Oct-factor concentration. Nucleic Acids Res. 1991 Jan 25;19(2):237–242. doi: 10.1093/nar/19.2.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kemler I., Schaffner W. Octamer transcription factors and the cell type-specificity of immunoglobulin gene expression. FASEB J. 1990 Mar;4(5):1444–1449. doi: 10.1096/fasebj.4.5.2407588. [DOI] [PubMed] [Google Scholar]
  28. Kristie T. M., Sharp P. A. Interactions of the Oct-1 POU subdomains with specific DNA sequences and with the HSV alpha-trans-activator protein. Genes Dev. 1990 Dec;4(12B):2383–2396. doi: 10.1101/gad.4.12b.2383. [DOI] [PubMed] [Google Scholar]
  29. La Bella F., Gallinari P., McKinney J., Heintz N. Histone H1 subtype-specific consensus elements mediate cell cycle-regulated transcription in vitro. Genes Dev. 1989 Dec;3(12A):1982–1990. doi: 10.1101/gad.3.12a.1982. [DOI] [PubMed] [Google Scholar]
  30. LaBella F., Sive H. L., Roeder R. G., Heintz N. Cell-cycle regulation of a human histone H2b gene is mediated by the H2b subtype-specific consensus element. Genes Dev. 1988 Jan;2(1):32–39. doi: 10.1101/gad.2.1.32. [DOI] [PubMed] [Google Scholar]
  31. Mattaj I. W., Lienhard S., Jiricny J., De Robertis E. M. An enhancer-like sequence within the Xenopus U2 gene promoter facilitates the formation of stable transcription complexes. Nature. 1985 Jul 11;316(6024):163–167. doi: 10.1038/316163a0. [DOI] [PubMed] [Google Scholar]
  32. Mitchell P. J., Tjian R. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science. 1989 Jul 28;245(4916):371–378. doi: 10.1126/science.2667136. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Old R. W., Sheikh S. A., Chambers A., Newton C. A., Mohammed A., Aldridge T. C. Individual Xenopus histone genes are replication-independent in oocytes and replication-dependent in Xenopus or mouse somatic cells. Nucleic Acids Res. 1985 Oct 25;13(20):7341–7358. doi: 10.1093/nar/13.20.7341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Plumb M., Stein J., Stein G. Coordinate regulation of multiple histone mRNAs during the cell cycle in HeLa cells. Nucleic Acids Res. 1983 Apr 25;11(8):2391–2410. doi: 10.1093/nar/11.8.2391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ptashne M. How eukaryotic transcriptional activators work. Nature. 1988 Oct 20;335(6192):683–689. doi: 10.1038/335683a0. [DOI] [PubMed] [Google Scholar]
  37. Roberts S. B., Segil N., Heintz N. Differential phosphorylation of the transcription factor Oct1 during the cell cycle. Science. 1991 Aug 30;253(5023):1022–1026. doi: 10.1126/science.1887216. [DOI] [PubMed] [Google Scholar]
  38. Roebuck K. A., Szeto D. P., Green K. P., Fan Q. N., Stumph W. E. Octamer and SPH motifs in the U1 enhancer cooperate to activate U1 RNA gene expression. Mol Cell Biol. 1990 Jan;10(1):341–352. doi: 10.1128/mcb.10.1.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Rollins M. B., Andrews M. T. Morphogenesis and regulated gene activity are independent of DNA replication in Xenopus embryos. Development. 1991 Jun;112(2):559–569. doi: 10.1242/dev.112.2.559. [DOI] [PubMed] [Google Scholar]
  40. Santoro C., Mermod N., Andrews P. C., Tjian R. A family of human CCAAT-box-binding proteins active in transcription and DNA replication: cloning and expression of multiple cDNAs. Nature. 1988 Jul 21;334(6179):218–224. doi: 10.1038/334218a0. [DOI] [PubMed] [Google Scholar]
  41. Sive H. L., Heintz N., Roeder R. G. Multiple sequence elements are required for maximal in vitro transcription of a human histone H2B gene. Mol Cell Biol. 1986 Oct;6(10):3329–3340. doi: 10.1128/mcb.6.10.3329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Stern S., Tanaka M., Herr W. The Oct-1 homoeodomain directs formation of a multiprotein-DNA complex with the HSV transactivator VP16. Nature. 1989 Oct 19;341(6243):624–630. doi: 10.1038/341624a0. [DOI] [PubMed] [Google Scholar]
  43. Tanaka M., Grossniklaus U., Herr W., Hernandez N. Activation of the U2 snRNA promoter by the octamer motif defines a new class of RNA polymerase II enhancer elements. Genes Dev. 1988 Dec;2(12B):1764–1778. doi: 10.1101/gad.2.12b.1764. [DOI] [PubMed] [Google Scholar]
  44. Tanaka M., Herr W. Differential transcriptional activation by Oct-1 and Oct-2: interdependent activation domains induce Oct-2 phosphorylation. Cell. 1990 Feb 9;60(3):375–386. doi: 10.1016/0092-8674(90)90589-7. [DOI] [PubMed] [Google Scholar]
  45. Tanaka M., Lai J. S., Herr W. Promoter-selective activation domains in Oct-1 and Oct-2 direct differential activation of an snRNA and mRNA promoter. Cell. 1992 Feb 21;68(4):755–767. doi: 10.1016/0092-8674(92)90150-b. [DOI] [PubMed] [Google Scholar]
  46. Treacy M. N., He X., Rosenfeld M. G. I-POU: a POU-domain protein that inhibits neuron-specific gene activation. Nature. 1991 Apr 18;350(6319):577–584. doi: 10.1038/350577a0. [DOI] [PubMed] [Google Scholar]
  47. Wu R. S., Bonner W. M. Separation of basal histone synthesis from S-phase histone synthesis in dividing cells. Cell. 1981 Dec;27(2 Pt 1):321–330. doi: 10.1016/0092-8674(81)90415-3. [DOI] [PubMed] [Google Scholar]
  48. Xiao J. H., Davidson I., Matthes H., Garnier J. M., Chambon P. Cloning, expression, and transcriptional properties of the human enhancer factor TEF-1. Cell. 1991 May 17;65(4):551–568. doi: 10.1016/0092-8674(91)90088-g. [DOI] [PubMed] [Google Scholar]

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

RESOURCES