Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1997 Aug;17(8):4363–4371. doi: 10.1128/mcb.17.8.4363

Nucleosomal structures of c-myc promoters with transcriptionally engaged RNA polymerase II.

T Albert 1, J Mautner 1, J O Funk 1, K Hörtnagel 1, A Pullner 1, D Eick 1
PMCID: PMC232290  PMID: 9234694

Abstract

Organization of DNA into chromatin has been shown to contribute to a repressed state of gene transcription. Disruption of nucleosomal structure is observed in response to gene induction, suggesting a model in which RNA polymerase II (pol II) is recruited to the promoter upon reorganization of nucleosomes. Here we show that induction of c-myc transcription correlates with the disruption of two nucleosomes in the upstream promoter region. This nucleosomal disruption, however, is not necessary for the binding of pol II to the promoter. Transcriptionally engaged pol II complexes can be detected when the upstream chromatin is in a more closed configuration. Thus, upstream chromatin opening is suggested to affect activation of promoter-bound pol II rather than entry of polymerases into the promoter. Interestingly, pol II complexes are detectable in both sense and antisense transcriptional directions, but only complexes in the sense direction respond to activation signals resulting in processive transcription.

Full Text

The Full Text of this article is available as a PDF (1.8 MB).

Selected References

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

  1. Adams C. C., Workman J. L. Nucleosome displacement in transcription. Cell. 1993 Feb 12;72(3):305–308. doi: 10.1016/0092-8674(93)90109-4. [DOI] [PubMed] [Google Scholar]
  2. Archer T. K., Cordingley M. G., Wolford R. G., Hager G. L. Transcription factor access is mediated by accurately positioned nucleosomes on the mouse mammary tumor virus promoter. Mol Cell Biol. 1991 Feb;11(2):688–698. doi: 10.1128/mcb.11.2.688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Archer T. K., Lefebvre P., Wolford R. G., Hager G. L. Transcription factor loading on the MMTV promoter: a bimodal mechanism for promoter activation. Science. 1992 Mar 20;255(5051):1573–1576. doi: 10.1126/science.1347958. [DOI] [PubMed] [Google Scholar]
  4. Asselin C., Nepveu A., Marcu K. B. Molecular requirements for transcriptional initiation of the murine c-myc gene. Oncogene. 1989 May;4(5):549–558. [PubMed] [Google Scholar]
  5. Axelrod J. D., Reagan M. S., Majors J. GAL4 disrupts a repressing nucleosome during activation of GAL1 transcription in vivo. Genes Dev. 1993 May;7(5):857–869. doi: 10.1101/gad.7.5.857. [DOI] [PubMed] [Google Scholar]
  6. Becker P. B. The establishment of active promoters in chromatin. Bioessays. 1994 Aug;16(8):541–547. doi: 10.1002/bies.950160807. [DOI] [PubMed] [Google Scholar]
  7. Bentley D. L., Groudine M. A block to elongation is largely responsible for decreased transcription of c-myc in differentiated HL60 cells. Nature. 1986 Jun 12;321(6071):702–706. doi: 10.1038/321702a0. [DOI] [PubMed] [Google Scholar]
  8. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  9. Cesarman E., Dalla-Favera R., Bentley D., Groudine M. Mutations in the first exon are associated with altered transcription of c-myc in Burkitt lymphoma. Science. 1987 Nov 27;238(4831):1272–1275. doi: 10.1126/science.3685977. [DOI] [PubMed] [Google Scholar]
  10. Collins S., Groudine M. Amplification of endogenous myc-related DNA sequences in a human myeloid leukaemia cell line. Nature. 1982 Aug 12;298(5875):679–681. doi: 10.1038/298679a0. [DOI] [PubMed] [Google Scholar]
  11. Dalla-Favera R., Wong-Staal F., Gallo R. C. Onc gene amplification in promyelocytic leukaemia cell line HL-60 and primary leukaemic cells of the same patient. Nature. 1982 Sep 2;299(5878):61–63. doi: 10.1038/299061a0. [DOI] [PubMed] [Google Scholar]
  12. Dyson P. J., Littlewood T. D., Forster A., Rabbitts T. H. Chromatin structure of transcriptionally active and inactive human c-myc alleles. EMBO J. 1985 Nov;4(11):2885–2891. doi: 10.1002/j.1460-2075.1985.tb04018.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eick D., Bornkamm G. W. Transcriptional arrest within the first exon is a fast control mechanism in c-myc gene expression. Nucleic Acids Res. 1986 Nov 11;14(21):8331–8346. doi: 10.1093/nar/14.21.8331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eick D., Polack A., Kofler E., Bornkamm G. W. The block of elongation in c-myc exon 1 is abolished in Burkitt's lymphoma cell lines with variant translocation. Oncogene. 1988 Oct;3(4):397–403. [PubMed] [Google Scholar]
  15. Fahrlander P. D., Piechaczyk M., Marcu K. B. Chromatin structure of the murine c-myc locus: implications for the regulation of normal and chromosomally translocated genes. EMBO J. 1985 Dec 1;4(12):3195–3202. doi: 10.1002/j.1460-2075.1985.tb04065.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Felsenfeld G. Chromatin as an essential part of the transcriptional mechanism. Nature. 1992 Jan 16;355(6357):219–224. doi: 10.1038/355219a0. [DOI] [PubMed] [Google Scholar]
  17. Garrity P. A., Wold B. J. Effects of different DNA polymerases in ligation-mediated PCR: enhanced genomic sequencing and in vivo footprinting. Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):1021–1025. doi: 10.1073/pnas.89.3.1021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gazin C., Dupont de Dinechin S., Hampe A., Masson J. M., Martin P., Stehelin D., Galibert F. Nucleotide sequence of the human c-myc locus: provocative open reading frame within the first exon. EMBO J. 1984 Feb;3(2):383–387. doi: 10.1002/j.1460-2075.1984.tb01816.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Grunstein M. Histone function in transcription. Annu Rev Cell Biol. 1990;6:643–678. doi: 10.1146/annurev.cb.06.110190.003235. [DOI] [PubMed] [Google Scholar]
  20. Hall D. J. Regulation of c-myc transcription in vitro: dependence on the guanine-rich promoter element ME1a1. Oncogene. 1990 Jan;5(1):47–54. [PubMed] [Google Scholar]
  21. Han M., Grunstein M. Nucleosome loss activates yeast downstream promoters in vivo. Cell. 1988 Dec 23;55(6):1137–1145. doi: 10.1016/0092-8674(88)90258-9. [DOI] [PubMed] [Google Scholar]
  22. Hörtnagel K., Mautner J., Strobl L. J., Wolf D. A., Christoph B., Geltinger C., Polack A. The role of immunoglobulin kappa elements in c-myc activation. Oncogene. 1995 Apr 6;10(7):1393–1401. [PubMed] [Google Scholar]
  23. Jücker M., Roebroek A. J., Mautner J., Koch K., Eick D., Diehl V., Van de Ven W. J., Tesch H. Expression of truncated transcripts of the proto-oncogene c-fps/fes in human lymphoma and lymphoid leukemia cell lines. Oncogene. 1992 May;7(5):943–952. [PubMed] [Google Scholar]
  24. Kavathas P., Bach F. H., DeMars R. Gamma ray-induced loss of expression of HLA and glyoxalase I alleles in lymphoblastoid cells. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4251–4255. doi: 10.1073/pnas.77.7.4251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kohlhuber F., Strobl L. J., Eick D. Early down-regulation of c-myc in dimethylsulfoxide-induced mouse erythroleukemia (MEL) cells is mediated at the P1/P2 promoters. Oncogene. 1993 Apr;8(4):1099–1102. [PubMed] [Google Scholar]
  26. Kornberg R. D., Lorch Y. Chromatin structure and transcription. Annu Rev Cell Biol. 1992;8:563–587. doi: 10.1146/annurev.cb.08.110192.003023. [DOI] [PubMed] [Google Scholar]
  27. Krumm A., Hickey L. B., Groudine M. Promoter-proximal pausing of RNA polymerase II defines a general rate-limiting step after transcription initiation. Genes Dev. 1995 Mar 1;9(5):559–572. doi: 10.1101/gad.9.5.559. [DOI] [PubMed] [Google Scholar]
  28. Krumm A., Meulia T., Brunvand M., Groudine M. The block to transcriptional elongation within the human c-myc gene is determined in the promoter-proximal region. Genes Dev. 1992 Nov;6(11):2201–2213. doi: 10.1101/gad.6.11.2201. [DOI] [PubMed] [Google Scholar]
  29. Lavenu A., Pournin S., Babinet C., Morello D. The cis-acting elements known to regulate c-myc expression ex vivo are not sufficient for correct transcription in vivo. Oncogene. 1994 Feb;9(2):527–536. [PubMed] [Google Scholar]
  30. Lee H. L., Archer T. K. Nucleosome-mediated disruption of transcription factor-chromatin initiation complexes at the mouse mammary tumor virus long terminal repeat in vivo. Mol Cell Biol. 1994 Jan;14(1):32–41. doi: 10.1128/mcb.14.1.32. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lis J., Wu C. Protein traffic on the heat shock promoter: parking, stalling, and trucking along. Cell. 1993 Jul 16;74(1):1–4. doi: 10.1016/0092-8674(93)90286-y. [DOI] [PubMed] [Google Scholar]
  32. Lyons R. M., Moses H. L. Transforming growth factors and the regulation of cell proliferation. Eur J Biochem. 1990 Feb 14;187(3):467–473. doi: 10.1111/j.1432-1033.1990.tb15327.x. [DOI] [PubMed] [Google Scholar]
  33. Madisen L., Groudine M. Identification of a locus control region in the immunoglobulin heavy-chain locus that deregulates c-myc expression in plasmacytoma and Burkitt's lymphoma cells. Genes Dev. 1994 Sep 15;8(18):2212–2226. doi: 10.1101/gad.8.18.2212. [DOI] [PubMed] [Google Scholar]
  34. Marcu K. B., Bossone S. A., Patel A. J. myc function and regulation. Annu Rev Biochem. 1992;61:809–860. doi: 10.1146/annurev.bi.61.070192.004113. [DOI] [PubMed] [Google Scholar]
  35. Mautner J., Joos S., Werner T., Eick D., Bornkamm G. W., Polack A. Identification of two enhancer elements downstream of the human c-myc gene. Nucleic Acids Res. 1995 Jan 11;23(1):72–80. doi: 10.1093/nar/23.1.72. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. McCracken S., Fong N., Yankulov K., Ballantyne S., Pan G., Greenblatt J., Patterson S. D., Wickens M., Bentley D. L. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature. 1997 Jan 23;385(6614):357–361. doi: 10.1038/385357a0. [DOI] [PubMed] [Google Scholar]
  37. Miller H., Asselin C., Dufort D., Yang J. Q., Gupta K., Marcu K. B., Nepveu A. A cis-acting element in the promoter region of the murine c-myc gene is necessary for transcriptional block. Mol Cell Biol. 1989 Dec;9(12):5340–5349. doi: 10.1128/mcb.9.12.5340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Mizzen C. A., Yang X. J., Kokubo T., Brownell J. E., Bannister A. J., Owen-Hughes T., Workman J., Wang L., Berger S. L., Kouzarides T. The TAF(II)250 subunit of TFIID has histone acetyltransferase activity. Cell. 1996 Dec 27;87(7):1261–1270. doi: 10.1016/s0092-8674(00)81821-8. [DOI] [PubMed] [Google Scholar]
  39. Mueller P. R., Wold B. In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science. 1989 Nov 10;246(4931):780–786. doi: 10.1126/science.2814500. [DOI] [PubMed] [Google Scholar]
  40. Mymryk J. S., Archer T. K. Dissection of progesterone receptor-mediated chromatin remodeling and transcriptional activation in vivo. Genes Dev. 1995 Jun 1;9(11):1366–1376. doi: 10.1101/gad.9.11.1366. [DOI] [PubMed] [Google Scholar]
  41. Mymryk J. S., Berard D., Hager G. L., Archer T. K. Mouse mammary tumor virus chromatin in human breast cancer cells is constitutively hypersensitive and exhibits steroid hormone-independent loading of transcription factors in vivo. Mol Cell Biol. 1995 Jan;15(1):26–34. doi: 10.1128/mcb.15.1.26. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Nepveu A., Marcu K. B. Intragenic pausing and anti-sense transcription within the murine c-myc locus. EMBO J. 1986 Nov;5(11):2859–2865. doi: 10.1002/j.1460-2075.1986.tb04580.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Nishikura K. Sequences involved in accurate and efficient transcription of human c-myc genes microinjected into frog oocytes. Mol Cell Biol. 1986 Nov;6(11):4093–4098. doi: 10.1128/mcb.6.11.4093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. O'Brien T., Lis J. T. Rapid changes in Drosophila transcription after an instantaneous heat shock. Mol Cell Biol. 1993 Jun;13(6):3456–3463. doi: 10.1128/mcb.13.6.3456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Ogryzko V. V., Schiltz R. L., Russanova V., Howard B. H., Nakatani Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell. 1996 Nov 29;87(5):953–959. doi: 10.1016/s0092-8674(00)82001-2. [DOI] [PubMed] [Google Scholar]
  46. PULVERTAFT J. V. CYTOLOGY OF BURKITT'S TUMOUR (AFRICAN LYMPHOMA). Lancet. 1964 Feb 1;1(7327):238–240. doi: 10.1016/s0140-6736(64)92345-1. [DOI] [PubMed] [Google Scholar]
  47. Paranjape S. M., Kamakaka R. T., Kadonaga J. T. Role of chromatin structure in the regulation of transcription by RNA polymerase II. Annu Rev Biochem. 1994;63:265–297. doi: 10.1146/annurev.bi.63.070194.001405. [DOI] [PubMed] [Google Scholar]
  48. Pazin M. J., Sheridan P. L., Cannon K., Cao Z., Keck J. G., Kadonaga J. T., Jones K. A. NF-kappa B-mediated chromatin reconfiguration and transcriptional activation of the HIV-1 enhancer in vitro. Genes Dev. 1996 Jan 1;10(1):37–49. doi: 10.1101/gad.10.1.37. [DOI] [PubMed] [Google Scholar]
  49. Piña B., Brüggemeier U., Beato M. Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter. Cell. 1990 Mar 9;60(5):719–731. doi: 10.1016/0092-8674(90)90087-u. [DOI] [PubMed] [Google Scholar]
  50. Plet A., Eick D., Blanchard J. M. Elongation and premature termination of transcripts initiated from c-fos and c-myc promoters show dissimilar patterns. Oncogene. 1995 Jan 19;10(2):319–328. [PubMed] [Google Scholar]
  51. Polack A., Eick D., Koch E., Bornkamm G. W. Truncation does not abrogate transcriptional downregulation of the c-myc gene by sodium butyrate in Burkitt's lymphoma cells. EMBO J. 1987 Oct;6(10):2959–2964. doi: 10.1002/j.1460-2075.1987.tb02601.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Polack A., Feederle R., Klobeck G., Hörtnagel K. Regulatory elements in the immunoglobulin kappa locus induce c-myc activation and the promoter shift in Burkitt's lymphoma cells. EMBO J. 1993 Oct;12(10):3913–3920. doi: 10.1002/j.1460-2075.1993.tb06069.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Polack A., Strobl L., Feederle R., Schweizer M., Koch E., Eick D., Wiegand H., Bornkamm G. W. The intron enhancer of the immunoglobulin kappa gene activates c-myc but does not induce the Burkitt-specific promoter shift. Oncogene. 1991 Nov;6(11):2033–2040. [PubMed] [Google Scholar]
  54. Pullner A., Mautner J., Albert T., Eick D. Nucleosomal structure of active and inactive c-myc genes. J Biol Chem. 1996 Dec 6;271(49):31452–31457. doi: 10.1074/jbc.271.49.31452. [DOI] [PubMed] [Google Scholar]
  55. Rasmussen E. B., Lis J. T. Short transcripts of the ternary complex provide insight into RNA polymerase II elongational pausing. J Mol Biol. 1995 Oct 6;252(5):522–535. doi: 10.1006/jmbi.1995.0517. [DOI] [PubMed] [Google Scholar]
  56. Richard-Foy H., Hager G. L. Sequence-specific positioning of nucleosomes over the steroid-inducible MMTV promoter. EMBO J. 1987 Aug;6(8):2321–2328. doi: 10.1002/j.1460-2075.1987.tb02507.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Riggs M. G., Whittaker R. G., Neumann J. R., Ingram V. M. n-Butyrate causes histone modification in HeLa and Friend erythroleukaemia cells. Nature. 1977 Aug 4;268(5619):462–464. doi: 10.1038/268462a0. [DOI] [PubMed] [Google Scholar]
  58. Rougvie A. E., Lis J. T. Postinitiation transcriptional control in Drosophila melanogaster. Mol Cell Biol. 1990 Nov;10(11):6041–6045. doi: 10.1128/mcb.10.11.6041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Rougvie A. E., Lis J. T. The RNA polymerase II molecule at the 5' end of the uninduced hsp70 gene of D. melanogaster is transcriptionally engaged. Cell. 1988 Sep 9;54(6):795–804. doi: 10.1016/s0092-8674(88)91087-2. [DOI] [PubMed] [Google Scholar]
  60. Schmid A., Fascher K. D., Hörz W. Nucleosome disruption at the yeast PHO5 promoter upon PHO5 induction occurs in the absence of DNA replication. Cell. 1992 Nov 27;71(5):853–864. doi: 10.1016/0092-8674(92)90560-y. [DOI] [PubMed] [Google Scholar]
  61. Shopland L. S., Hirayoshi K., Fernandes M., Lis J. T. HSF access to heat shock elements in vivo depends critically on promoter architecture defined by GAGA factor, TFIID, and RNA polymerase II binding sites. Genes Dev. 1995 Nov 15;9(22):2756–2769. doi: 10.1101/gad.9.22.2756. [DOI] [PubMed] [Google Scholar]
  62. Siebenlist U., Bressler P., Kelly K. Two distinct mechanisms of transcriptional control operate on c-myc during differentiation of HL60 cells. Mol Cell Biol. 1988 Feb;8(2):867–874. doi: 10.1128/mcb.8.2.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Siebenlist U., Hennighausen L., Battey J., Leder P. Chromatin structure and protein binding in the putative regulatory region of the c-myc gene in Burkitt lymphoma. Cell. 1984 Jun;37(2):381–391. doi: 10.1016/0092-8674(84)90368-4. [DOI] [PubMed] [Google Scholar]
  64. Spencer C. A., Groudine M. Transcription elongation and eukaryotic gene regulation. Oncogene. 1990 Jun;5(6):777–785. [PubMed] [Google Scholar]
  65. Strobl L. J., Eick D. Hold back of RNA polymerase II at the transcription start site mediates down-regulation of c-myc in vivo. EMBO J. 1992 Sep;11(9):3307–3314. doi: 10.1002/j.1460-2075.1992.tb05409.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Strobl L. J., Kohlhuber F., Mautner J., Polack A., Eick D. Absence of a paused transcription complex from the c-myc P2 promoter of the translocation chromosome in Burkitt's lymphoma cells: implication for the c-myc P1/P2 promoter shift. Oncogene. 1993 Jun;8(6):1437–1447. [PubMed] [Google Scholar]
  67. Sugden B., Marsh K., Yates J. A vector that replicates as a plasmid and can be efficiently selected in B-lymphoblasts transformed by Epstein-Barr virus. Mol Cell Biol. 1985 Feb;5(2):410–413. doi: 10.1128/mcb.5.2.410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Svaren J., Hörz W. Regulation of gene expression by nucleosomes. Curr Opin Genet Dev. 1996 Apr;6(2):164–170. doi: 10.1016/s0959-437x(96)80046-3. [DOI] [PubMed] [Google Scholar]
  69. Taylor I. C., Workman J. L., Schuetz T. J., Kingston R. E. Facilitated binding of GAL4 and heat shock factor to nucleosomal templates: differential function of DNA-binding domains. Genes Dev. 1991 Jul;5(7):1285–1298. doi: 10.1101/gad.5.7.1285. [DOI] [PubMed] [Google Scholar]
  70. Thalmeier K., Synovzik H., Mertz R., Winnacker E. L., Lipp M. Nuclear factor E2F mediates basic transcription and trans-activation by E1a of the human MYC promoter. Genes Dev. 1989 Apr;3(4):527–536. doi: 10.1101/gad.3.4.527. [DOI] [PubMed] [Google Scholar]
  71. Truss M., Bartsch J., Schelbert A., Haché R. J., Beato M. Hormone induces binding of receptors and transcription factors to a rearranged nucleosome on the MMTV promoter in vivo. EMBO J. 1995 Apr 18;14(8):1737–1751. doi: 10.1002/j.1460-2075.1995.tb07163.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Van Lint C., Emiliani S., Ott M., Verdin E. Transcriptional activation and chromatin remodeling of the HIV-1 promoter in response to histone acetylation. EMBO J. 1996 Mar 1;15(5):1112–1120. [PMC free article] [PubMed] [Google Scholar]
  73. Venter U., Svaren J., Schmitz J., Schmid A., Hörz W. A nucleosome precludes binding of the transcription factor Pho4 in vivo to a critical target site in the PHO5 promoter. EMBO J. 1994 Oct 17;13(20):4848–4855. doi: 10.1002/j.1460-2075.1994.tb06811.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Verdin E., Paras P., Jr, Van Lint C. Chromatin disruption in the promoter of human immunodeficiency virus type 1 during transcriptional activation. EMBO J. 1993 Aug;12(8):3249–3259. doi: 10.1002/j.1460-2075.1993.tb05994.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Verdone L., Camilloni G., Di Mauro E., Caserta M. Chromatin remodeling during Saccharomyces cerevisiae ADH2 gene activation. Mol Cell Biol. 1996 May;16(5):1978–1988. doi: 10.1128/mcb.16.5.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Wang W., Carey M., Gralla J. D. Polymerase II promoter activation: closed complex formation and ATP-driven start site opening. Science. 1992 Jan 24;255(5043):450–453. doi: 10.1126/science.1310361. [DOI] [PubMed] [Google Scholar]
  77. Wolf D. A., Strobl L. J., Pullner A., Eick D. Variable pause positions of RNA polymerase II lie proximal to the c-myc promoter irrespective of transcriptional activity. Nucleic Acids Res. 1995 Sep 11;23(17):3373–3379. doi: 10.1093/nar/23.17.3373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Wolffe A. P. Transcription: in tune with the histones. Cell. 1994 Apr 8;77(1):13–16. doi: 10.1016/0092-8674(94)90229-1. [DOI] [PubMed] [Google Scholar]
  79. Yankulov K., Blau J., Purton T., Roberts S., Bentley D. L. Transcriptional elongation by RNA polymerase II is stimulated by transactivators. Cell. 1994 Jun 3;77(5):749–759. doi: 10.1016/0092-8674(94)90058-2. [DOI] [PubMed] [Google Scholar]

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

RESOURCES