Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1997 Jun;17(6):3284–3294. doi: 10.1128/mcb.17.6.3284

The ts13 mutation in the TAF(II)250 subunit (CCG1) of TFIID directly affects transcription of D-type cyclin genes in cells arrested in G1 at the nonpermissive temperature.

Y Suzuki-Yagawa 1, M Guermah 1, R G Roeder 1
PMCID: PMC232181  PMID: 9154827

Abstract

The general transcription initiation factor TFIID contains the TATA-binding protein (TBP) and TBP-associated factors (TAFs) implicated in the function of gene-specific activators. Previous studies have indicated that a hamster cell line (ts13) with a point mutation in the TAF(II)250/CCG1 (TAF(II)250) gene shows temperature-sensitive expression of a subset of genes and arrests in late G1 at 39.5 degrees C. Here, we report the identification of cell cycle-specific (G1-specific) genes that appear to be regulated directly through TAF(II)250 both in vivo and in vitro. Transcription rates of several cell cycle-regulatory genes were determined by run-on assays in nuclei from ts13 cells grown at permissive (33 degrees C) and nonpermissive (39.5 degrees C) temperatures. Temperature-dependent differences in transcription rates were observed for cyclin A, D1, and D3 genes. In transient-transfection assays, the human cyclin D1 promoter fused to a luciferase reporter showed a temperature-dependent reduction in activity in ts13 cells but not in parental BHK cells. In in vitro assays, upstream sequence-dependent transcription from the human cyclin D1 promoter was significantly reduced in ts13 nuclear extracts preincubated at 30 degrees C but not in similarly treated BHK nuclear extracts, and transcription in the ts13 extract was restored by addition of an affinity-purified human TFIID. Preincubation of the ts13 nuclear extracts did not affect the function of several GAL4-activation domain fusion proteins (GAL4-VP16, GAL4-p65, and GAL4-p53) on either the adenovirus major late or cyclin D1 core promoter bearing GAL4 sites, further indicating that the effect of the TAF(II)250 mutation is both core promoter and activator specific.

Full Text

The Full Text of this article is available as a PDF (901.1 KB).

Selected References

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

  1. Abmayr S. M., Workman J. L., Roeder R. G. The pseudorabies immediate early protein stimulates in vitro transcription by facilitating TFIID: promoter interactions. Genes Dev. 1988 May;2(5):542–553. doi: 10.1101/gad.2.5.542. [DOI] [PubMed] [Google Scholar]
  2. Albanese C., Johnson J., Watanabe G., Eklund N., Vu D., Arnold A., Pestell R. G. Transforming p21ras mutants and c-Ets-2 activate the cyclin D1 promoter through distinguishable regions. J Biol Chem. 1995 Oct 6;270(40):23589–23597. doi: 10.1074/jbc.270.40.23589. [DOI] [PubMed] [Google Scholar]
  3. Arias J., Alberts A. S., Brindle P., Claret F. X., Smeal T., Karin M., Feramisco J., Montminy M. Activation of cAMP and mitogen responsive genes relies on a common nuclear factor. Nature. 1994 Jul 21;370(6486):226–229. doi: 10.1038/370226a0. [DOI] [PubMed] [Google Scholar]
  4. Blair W. S., Bogerd H. P., Madore S. J., Cullen B. R. Mutational analysis of the transcription activation domain of RelA: identification of a highly synergistic minimal acidic activation module. Mol Cell Biol. 1994 Nov;14(11):7226–7234. doi: 10.1128/mcb.14.11.7226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brooks A. R., Shiffman D., Chan C. S., Brooks E. E., Milner P. G. Functional analysis of the human cyclin D2 and cyclin D3 promoters. J Biol Chem. 1996 Apr 12;271(15):9090–9099. doi: 10.1074/jbc.271.15.9090. [DOI] [PubMed] [Google Scholar]
  6. Burley S. K., Roeder R. G. Biochemistry and structural biology of transcription factor IID (TFIID). Annu Rev Biochem. 1996;65:769–799. doi: 10.1146/annurev.bi.65.070196.004005. [DOI] [PubMed] [Google Scholar]
  7. Carrozza M. J., DeLuca N. A. Interaction of the viral activator protein ICP4 with TFIID through TAF250. Mol Cell Biol. 1996 Jun;16(6):3085–3093. doi: 10.1128/mcb.16.6.3085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chen J. L., Attardi L. D., Verrijzer C. P., Yokomori K., Tjian R. Assembly of recombinant TFIID reveals differential coactivator requirements for distinct transcriptional activators. Cell. 1994 Oct 7;79(1):93–105. doi: 10.1016/0092-8674(94)90403-0. [DOI] [PubMed] [Google Scholar]
  10. Chiang C. M., Roeder R. G. Expression and purification of general transcription factors by FLAG epitope-tagging and peptide elution. Pept Res. 1993 Mar-Apr;6(2):62–64. [PubMed] [Google Scholar]
  11. Chrivia J. C., Kwok R. P., Lamb N., Hagiwara M., Montminy M. R., Goodman R. H. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature. 1993 Oct 28;365(6449):855–859. doi: 10.1038/365855a0. [DOI] [PubMed] [Google Scholar]
  12. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Erlanson D. A., Verdine G. L. Falling out of the fold: tumorigenic mutations and p53. Chem Biol. 1994 Oct;1(2):79–84. doi: 10.1016/1074-5521(94)90044-2. [DOI] [PubMed] [Google Scholar]
  14. Fisch T. M., Prywes R., Simon M. C., Roeder R. G. Multiple sequence elements in the c-fos promoter mediate induction by cAMP. Genes Dev. 1989 Feb;3(2):198–211. doi: 10.1101/gad.3.2.198. [DOI] [PubMed] [Google Scholar]
  15. Floros J., Ashihara T., Baserga R. Characterization of ts13 cells a temperature-sensitive mutant of the G1 phase of the cell cycle. Cell Biol Int Rep. 1978 May;2(3):259–269. doi: 10.1016/0309-1651(78)90006-1. [DOI] [PubMed] [Google Scholar]
  16. Geisberg J. V., Chen J. L., Ricciardi R. P. Subregions of the adenovirus E1A transactivation domain target multiple components of the TFIID complex. Mol Cell Biol. 1995 Nov;15(11):6283–6290. doi: 10.1128/mcb.15.11.6283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gill G., Pascal E., Tseng Z. H., Tjian R. A glutamine-rich hydrophobic patch in transcription factor Sp1 contacts the dTAFII110 component of the Drosophila TFIID complex and mediates transcriptional activation. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):192–196. doi: 10.1073/pnas.91.1.192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hai T., Curran T. Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3720–3724. doi: 10.1073/pnas.88.9.3720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hayashida T., Sekiguchi T., Noguchi E., Sunamoto H., Ohba T., Nishimoto T. The CCG1/TAFII250 gene is mutated in thermosensitive G1 mutants of the BHK21 cell line derived from golden hamster. Gene. 1994 Apr 20;141(2):267–270. doi: 10.1016/0378-1119(94)90583-5. [DOI] [PubMed] [Google Scholar]
  20. Helin K., Lees J. A., Vidal M., Dyson N., Harlow E., Fattaey A. A cDNA encoding a pRB-binding protein with properties of the transcription factor E2F. Cell. 1992 Jul 24;70(2):337–350. doi: 10.1016/0092-8674(92)90107-n. [DOI] [PubMed] [Google Scholar]
  21. Herber B., Truss M., Beato M., Müller R. Inducible regulatory elements in the human cyclin D1 promoter. Oncogene. 1994 Apr;9(4):1295–1304. [PubMed] [Google Scholar]
  22. Hisatake K., Hasegawa S., Takada R., Nakatani Y., Horikoshi M., Roeder R. G. The p250 subunit of native TATA box-binding factor TFIID is the cell-cycle regulatory protein CCG1. Nature. 1993 Mar 11;362(6416):179–181. doi: 10.1038/362179a0. [DOI] [PubMed] [Google Scholar]
  23. Horikoshi M., Hai T., Lin Y. S., Green M. R., Roeder R. G. Transcription factor ATF interacts with the TATA factor to facilitate establishment of a preinitiation complex. Cell. 1988 Sep 23;54(7):1033–1042. doi: 10.1016/0092-8674(88)90118-3. [DOI] [PubMed] [Google Scholar]
  24. Horowitz J. M., Park S. H., Bogenmann E., Cheng J. C., Yandell D. W., Kaye F. J., Minna J. D., Dryja T. P., Weinberg R. A. Frequent inactivation of the retinoblastoma anti-oncogene is restricted to a subset of human tumor cells. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2775–2779. doi: 10.1073/pnas.87.7.2775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kaelin W. G., Jr, Krek W., Sellers W. R., DeCaprio J. A., Ajchenbaum F., Fuchs C. S., Chittenden T., Li Y., Farnham P. J., Blanar M. A. Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell. 1992 Jul 24;70(2):351–364. doi: 10.1016/0092-8674(92)90108-o. [DOI] [PubMed] [Google Scholar]
  26. Kim T. K., Hashimoto S., Kelleher R. J., 3rd, Flanagan P. M., Kornberg R. D., Horikoshi M., Roeder R. G. Effects of activation-defective TBP mutations on transcription initiation in yeast. Nature. 1994 May 19;369(6477):252–255. doi: 10.1038/369252a0. [DOI] [PubMed] [Google Scholar]
  27. Kim Y. K., Lee A. S. Identification of a 70-base-pair cell cycle regulatory unit within the promoter of the human thymidine kinase gene and its interaction with cellular factors. Mol Cell Biol. 1991 Apr;11(4):2296–2302. doi: 10.1128/mcb.11.4.2296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Klemm R. D., Goodrich J. A., Zhou S., Tjian R. Molecular cloning and expression of the 32-kDa subunit of human TFIID reveals interactions with VP16 and TFIIB that mediate transcriptional activation. Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5788–5792. doi: 10.1073/pnas.92.13.5788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Koniecki J., Nugent P., Kordowska J., Baserga R. Effect of the SV40 T antigen on the posttranscriptional regulation of the proliferating cell nuclear antigen and DNA polymerase-alpha genes. Cancer Res. 1991 Mar 1;51(5):1465–1471. [PubMed] [Google Scholar]
  30. Kovelman R., Roeder R. G. Sarkosyl defines three intermediate steps in transcription initiation by RNA polymerase III: application to stimulation of transcription by E1A. Genes Dev. 1990 Apr;4(4):646–658. doi: 10.1101/gad.4.4.646. [DOI] [PubMed] [Google Scholar]
  31. Kwok R. P., Lundblad J. R., Chrivia J. C., Richards J. P., Bächinger H. P., Brennan R. G., Roberts S. G., Green M. R., Goodman R. H. Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature. 1994 Jul 21;370(6486):223–226. doi: 10.1038/370223a0. [DOI] [PubMed] [Google Scholar]
  32. Larner A. C., Jonak G., Cheng Y. S., Korant B., Knight E., Darnell J. E., Jr Transcriptional induction of two genes in human cells by beta interferon. Proc Natl Acad Sci U S A. 1984 Nov;81(21):6733–6737. doi: 10.1073/pnas.81.21.6733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lew D. J., Dulić V., Reed S. I. Isolation of three novel human cyclins by rescue of G1 cyclin (Cln) function in yeast. Cell. 1991 Sep 20;66(6):1197–1206. doi: 10.1016/0092-8674(91)90042-w. [DOI] [PubMed] [Google Scholar]
  34. Lieberman P. M., Berk A. J. A mechanism for TAFs in transcriptional activation: activation domain enhancement of TFIID-TFIIA--promoter DNA complex formation. Genes Dev. 1994 May 1;8(9):995–1006. doi: 10.1101/gad.8.9.995. [DOI] [PubMed] [Google Scholar]
  35. Lin Y. S., Carey M. F., Ptashne M., Green M. R. GAL4 derivatives function alone and synergistically with mammalian activators in vitro. Cell. 1988 Aug 26;54(5):659–664. doi: 10.1016/s0092-8674(88)80010-2. [DOI] [PubMed] [Google Scholar]
  36. Liu H. T., Gibson C. W., Hirschhorn R. R., Rittling S., Baserga R., Mercer W. E. Expression of thymidine kinase and dihydrofolate reductase genes in mammalian ts mutants of the cell cycle. J Biol Chem. 1985 Mar 25;260(6):3269–3274. [PubMed] [Google Scholar]
  37. Liu X., Miller C. W., Koeffler P. H., Berk A. J. The p53 activation domain binds the TATA box-binding polypeptide in Holo-TFIID, and a neighboring p53 domain inhibits transcription. Mol Cell Biol. 1993 Jun;13(6):3291–3300. doi: 10.1128/mcb.13.6.3291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Lu H., Levine A. J. Human TAFII31 protein is a transcriptional coactivator of the p53 protein. Proc Natl Acad Sci U S A. 1995 May 23;92(11):5154–5158. doi: 10.1073/pnas.92.11.5154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Lucibello F. C., Truss M., Zwicker J., Ehlert F., Beato M., Müller R. Periodic cdc25C transcription is mediated by a novel cell cycle-regulated repressor element (CDE). EMBO J. 1995 Jan 3;14(1):132–142. doi: 10.1002/j.1460-2075.1995.tb06983.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Martinez E., Chiang C. M., Ge H., Roeder R. G. TATA-binding protein-associated factor(s) in TFIID function through the initiator to direct basal transcription from a TATA-less class II promoter. EMBO J. 1994 Jul 1;13(13):3115–3126. doi: 10.1002/j.1460-2075.1994.tb06610.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Matsushime H., Roussel M. F., Ashmun R. A., Sherr C. J. Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell. 1991 May 17;65(4):701–713. doi: 10.1016/0092-8674(91)90101-4. [DOI] [PubMed] [Google Scholar]
  42. McKinney J. D., Heintz N. Transcriptional regulation in the eukaryotic cell cycle. Trends Biochem Sci. 1991 Nov;16(11):430–435. doi: 10.1016/0968-0004(91)90170-z. [DOI] [PubMed] [Google Scholar]
  43. Meyerson M., Enders G. H., Wu C. L., Su L. K., Gorka C., Nelson C., Harlow E., Tsai L. H. A family of human cdc2-related protein kinases. EMBO J. 1992 Aug;11(8):2909–2917. doi: 10.1002/j.1460-2075.1992.tb05360.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Motokura T., Arnold A. PRAD1/cyclin D1 proto-oncogene: genomic organization, 5' DNA sequence, and sequence of a tumor-specific rearrangement breakpoint. Genes Chromosomes Cancer. 1993 Jun;7(2):89–95. doi: 10.1002/gcc.2870070205. [DOI] [PubMed] [Google Scholar]
  45. Nakajima N., Horikoshi M., Roeder R. G. Factors involved in specific transcription by mammalian RNA polymerase II: purification, genetic specificity, and TATA box-promoter interactions of TFIID. Mol Cell Biol. 1988 Oct;8(10):4028–4040. doi: 10.1128/mcb.8.10.4028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Noguchi E., Sekiguchi T., Nohiro Y., Hayashida T., Hirose E., Hayashi N., Nishimoto T. Minimum essential region of CCG1/TAFII250 required for complementing the temperature-sensitive cell cycle mutants, tsBN462 and ts13 cells, of hamster BHK21 cells. Somat Cell Mol Genet. 1994 Nov;20(6):505–513. doi: 10.1007/BF02255841. [DOI] [PubMed] [Google Scholar]
  47. Oelgeschläger T., Chiang C. M., Roeder R. G. Topology and reorganization of a human TFIID-promoter complex. Nature. 1996 Aug 22;382(6593):735–738. doi: 10.1038/382735a0. [DOI] [PubMed] [Google Scholar]
  48. Pearson B. E., Nasheuer H. P., Wang T. S. Human DNA polymerase alpha gene: sequences controlling expression in cycling and serum-stimulated cells. Mol Cell Biol. 1991 Apr;11(4):2081–2095. doi: 10.1128/mcb.11.4.2081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Philipp A., Schneider A., Väsrik I., Finke K., Xiong Y., Beach D., Alitalo K., Eilers M. Repression of cyclin D1: a novel function of MYC. Mol Cell Biol. 1994 Jun;14(6):4032–4043. doi: 10.1128/mcb.14.6.4032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Pine R. Constitutive expression of an ISGF2/IRF1 transgene leads to interferon-independent activation of interferon-inducible genes and resistance to virus infection. J Virol. 1992 Jul;66(7):4470–4478. doi: 10.1128/jvi.66.7.4470-4478.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Pines J., Hunter T. Human cyclin A is adenovirus E1A-associated protein p60 and behaves differently from cyclin B. Nature. 1990 Aug 23;346(6286):760–763. doi: 10.1038/346760a0. [DOI] [PubMed] [Google Scholar]
  52. Pines J., Hunter T. Isolation of a human cyclin cDNA: evidence for cyclin mRNA and protein regulation in the cell cycle and for interaction with p34cdc2. Cell. 1989 Sep 8;58(5):833–846. doi: 10.1016/0092-8674(89)90936-7. [DOI] [PubMed] [Google Scholar]
  53. Roeder R. G. The role of general initiation factors in transcription by RNA polymerase II. Trends Biochem Sci. 1996 Sep;21(9):327–335. [PubMed] [Google Scholar]
  54. Ruppert S., Tjian R. Human TAFII250 interacts with RAP74: implications for RNA polymerase II initiation. Genes Dev. 1995 Nov 15;9(22):2747–2755. doi: 10.1101/gad.9.22.2747. [DOI] [PubMed] [Google Scholar]
  55. Ruppert S., Wang E. H., Tjian R. Cloning and expression of human TAFII250: a TBP-associated factor implicated in cell-cycle regulation. Nature. 1993 Mar 11;362(6416):175–179. doi: 10.1038/362175a0. [DOI] [PubMed] [Google Scholar]
  56. Sauer F., Hansen S. K., Tjian R. Multiple TAFIIs directing synergistic activation of transcription. Science. 1995 Dec 15;270(5243):1783–1788. doi: 10.1126/science.270.5243.1783. [DOI] [PubMed] [Google Scholar]
  57. Sekiguchi T., Miyata T., Nishimoto T. Molecular cloning of the cDNA of human X chromosomal gene (CCG1) which complements the temperature-sensitive G1 mutants, tsBN462 and ts13, of the BHK cell line. EMBO J. 1988 Jun;7(6):1683–1687. doi: 10.1002/j.1460-2075.1988.tb02996.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Sekiguchi T., Noguchi E., Hayashida T., Nakashima T., Toyoshima H., Nishimoto T., Hunter T. D-type cyclin expression is decreased and p21 and p27 CDK inhibitor expression is increased when tsBN462 CCG1/TAFII250 mutant cells arrest in G1 at the restrictive temperature. Genes Cells. 1996 Jul;1(7):687–705. doi: 10.1046/j.1365-2443.1996.00259.x. [DOI] [PubMed] [Google Scholar]
  59. Sekiguchi T., Nohiro Y., Nakamura Y., Hisamoto N., Nishimoto T. The human CCG1 gene, essential for progression of the G1 phase, encodes a 210-kilodalton nuclear DNA-binding protein. Mol Cell Biol. 1991 Jun;11(6):3317–3325. doi: 10.1128/mcb.11.6.3317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Shao Z., Ruppert S., Robbins P. D. The retinoblastoma-susceptibility gene product binds directly to the human TATA-binding protein-associated factor TAFII250. Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3115–3119. doi: 10.1073/pnas.92.8.3115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sherr C. J. Mammalian G1 cyclins. Cell. 1993 Jun 18;73(6):1059–1065. doi: 10.1016/0092-8674(93)90636-5. [DOI] [PubMed] [Google Scholar]
  62. Sherr C. J., Roberts J. M. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 1995 May 15;9(10):1149–1163. doi: 10.1101/gad.9.10.1149. [DOI] [PubMed] [Google Scholar]
  63. Smale S. T., Baltimore D. The "initiator" as a transcription control element. Cell. 1989 Apr 7;57(1):103–113. doi: 10.1016/0092-8674(89)90176-1. [DOI] [PubMed] [Google Scholar]
  64. Smale S. T., Schmidt M. C., Berk A. J., Baltimore D. Transcriptional activation by Sp1 as directed through TATA or initiator: specific requirement for mammalian transcription factor IID. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4509–4513. doi: 10.1073/pnas.87.12.4509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Talavera A., Basilico C. Temperature sensitive mutants of BHK cells affected in cell cycle progression. J Cell Physiol. 1977 Sep;92(3):425–436. doi: 10.1002/jcp.1040920310. [DOI] [PubMed] [Google Scholar]
  66. Tanese N., Pugh B. F., Tjian R. Coactivators for a proline-rich activator purified from the multisubunit human TFIID complex. Genes Dev. 1991 Dec;5(12A):2212–2224. doi: 10.1101/gad.5.12a.2212. [DOI] [PubMed] [Google Scholar]
  67. Verrijzer C. P., Tjian R. TAFs mediate transcriptional activation and promoter selectivity. Trends Biochem Sci. 1996 Sep;21(9):338–342. [PubMed] [Google Scholar]
  68. Wade M., Kowalik T. F., Mudryj M., Huang E. S., Azizkhan J. C. E2F mediates dihydrofolate reductase promoter activation and multiprotein complex formation in human cytomegalovirus infection. Mol Cell Biol. 1992 Oct;12(10):4364–4374. doi: 10.1128/mcb.12.10.4364. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Wang E. H., Tjian R. Promoter-selective transcriptional defect in cell cycle mutant ts13 rescued by hTAFII250. Science. 1994 Feb 11;263(5148):811–814. doi: 10.1126/science.8303298. [DOI] [PubMed] [Google Scholar]
  70. Workman J. L., Abmayr S. M., Cromlish W. A., Roeder R. G. Transcriptional regulation by the immediate early protein of pseudorabies virus during in vitro nucleosome assembly. Cell. 1988 Oct 21;55(2):211–219. doi: 10.1016/0092-8674(88)90044-x. [DOI] [PubMed] [Google Scholar]
  71. Xiong Y., Connolly T., Futcher B., Beach D. Human D-type cyclin. Cell. 1991 May 17;65(4):691–699. doi: 10.1016/0092-8674(91)90100-d. [DOI] [PubMed] [Google Scholar]
  72. de Wet J. R., Wood K. V., DeLuca M., Helinski D. R., Subramani S. Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol. 1987 Feb;7(2):725–737. doi: 10.1128/mcb.7.2.725. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES