Abstract
To study the influence of various transactivators and the role of nucleosomal structure in gene regulation by steroid hormones, we have introduced mouse mammary tumor virus (MMTV) promoter sequences along with expression vectors for the glucocorticoid receptor (GR) and nuclear factor I (NFI) in Saccharomyces cerevisiae, an organism amenable to genetic manipulation. Both in the context of an episomal multicopy vector and in a centromeric single-copy plasmid, the MMTV promoter was virtually silent in the absence of inducer, even in yeast strains expressing GR and NFI. Induction was optimal with deacylcortivazol and required both GR and NFI. The transactivation function AF1 in the N-terminal half of GR is required for ligand-dependent induction and acts constitutively in truncated GR lacking the ligand binding domain. A piece of the MMTV long terminal repeat extending from -236 to +111 is sufficient to position a nucleosome, B, over the regulatory region of the promoter from -45 to -190 and another nucleosome over the transcription start region. The rotational orientation of the DNA on the surface of nucleosome B is the same as that previously found in animal cells and in reconstitution experiments. This orientation is compatible with binding of GR to two sites, while it should preclude binding of NFI and hence be responsible for constitutive repression. Upon ligand induction, there is no major chromatin rearrangement, but the proximal linker DNA, including the TATA box, becomes hypersensitive to nucleases. The transcriptional behavior of the MMTV promoter was unaffected by deletions of the genes for zuotin or SIN1/SPT2, two proteins which have been claimed to assume some of the functions of linker histones. Thus, despite the lack of histone H1, yeast cells could be a suitable system to study the contribution of nucleosomal organization to the regulated expression of the MMTV promoter.
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- Alani E., Cao L., Kleckner N. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics. 1987 Aug;116(4):541–545. doi: 10.1534/genetics.112.541.test. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Almer A., Hörz W. Nuclease hypersensitive regions with adjacent positioned nucleosomes mark the gene boundaries of the PHO5/PHO3 locus in yeast. EMBO J. 1986 Oct;5(10):2681–2687. doi: 10.1002/j.1460-2075.1986.tb04551.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Altmann H., Wendler W., Winnacker E. L. Transcriptional activation by CTF proteins is mediated by a bipartite low-proline domain. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3901–3905. doi: 10.1073/pnas.91.9.3901. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ammerer G. Expression of genes in yeast using the ADCI promoter. Methods Enzymol. 1983;101:192–201. doi: 10.1016/0076-6879(83)01014-9. [DOI] [PubMed] [Google Scholar]
- 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]
- Beato M. Transcriptional regulation of mouse mammary tumor virus by steroid hormones. Crit Rev Oncog. 1991;2(3):195–210. [PubMed] [Google Scholar]
- Bresnick E. H., Bustin M., Marsaud V., Richard-Foy H., Hager G. L. The transcriptionally-active MMTV promoter is depleted of histone H1. Nucleic Acids Res. 1992 Jan 25;20(2):273–278. doi: 10.1093/nar/20.2.273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Brüggemeier U., Rogge L., Winnacker E. L., Beato M. Nuclear factor I acts as a transcription factor on the MMTV promoter but competes with steroid hormone receptors for DNA binding. EMBO J. 1990 Jul;9(7):2233–2239. doi: 10.1002/j.1460-2075.1990.tb07393.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buetti E., Kühnel B. Distinct sequence elements involved in the glucocorticoid regulation of the mouse mammary tumor virus promoter identified by linker scanning mutagenesis. J Mol Biol. 1986 Aug 5;190(3):379–389. doi: 10.1016/0022-2836(86)90009-4. [DOI] [PubMed] [Google Scholar]
- Cato A. C., Miksicek R., Schütz G., Arnemann J., Beato M. The hormone regulatory element of mouse mammary tumour virus mediates progesterone induction. EMBO J. 1986 Sep;5(9):2237–2240. doi: 10.1002/j.1460-2075.1986.tb04490.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Certa U., Colavito-Shepanski M., Grunstein M. Yeast may not contain histone H1: the only known 'histone H1-like' protein in Saccharomyces cerevisiae is a mitochondrial protein. Nucleic Acids Res. 1984 Nov 12;12(21):7975–7985. doi: 10.1093/nar/12.21.7975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chalepakis G., Arnemann J., Slater E., Brüller H. J., Gross B., Beato M. Differential gene activation by glucocorticoids and progestins through the hormone regulatory element of mouse mammary tumor virus. Cell. 1988 May 6;53(3):371–382. doi: 10.1016/0092-8674(88)90157-2. [DOI] [PubMed] [Google Scholar]
- Chiang C. M., Roeder R. G. Cloning of an intrinsic human TFIID subunit that interacts with multiple transcriptional activators. Science. 1995 Jan 27;267(5197):531–536. doi: 10.1126/science.7824954. [DOI] [PubMed] [Google Scholar]
- Chodosh L. A., Olesen J., Hahn S., Baldwin A. S., Guarente L., Sharp P. A. A yeast and a human CCAAT-binding protein have heterologous subunits that are functionally interchangeable. Cell. 1988 Apr 8;53(1):25–35. doi: 10.1016/0092-8674(88)90484-9. [DOI] [PubMed] [Google Scholar]
- 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]
- Fedor M. J., Kornberg R. D. Upstream activation sequence-dependent alteration of chromatin structure and transcription activation of the yeast GAL1-GAL10 genes. Mol Cell Biol. 1989 Apr;9(4):1721–1732. doi: 10.1128/mcb.9.4.1721. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Garabedian M. J., Yamamoto K. R. Genetic dissection of the signaling domain of a mammalian steroid receptor in yeast. Mol Biol Cell. 1992 Nov;3(11):1245–1257. doi: 10.1091/mbc.3.11.1245. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Godowski P. J., Rusconi S., Miesfeld R., Yamamoto K. R. Glucocorticoid receptor mutants that are constitutive activators of transcriptional enhancement. Nature. 1987 Jan 22;325(6102):365–368. doi: 10.1038/325365a0. [DOI] [PubMed] [Google Scholar]
- Guarente L., Bermingham-McDonogh O. Conservation and evolution of transcriptional mechanisms in eukaryotes. Trends Genet. 1992 Jan;8(1):27–32. doi: 10.1016/0168-9525(92)90021-u. [DOI] [PubMed] [Google Scholar]
- Guarente L. Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol. 1983;101:181–191. doi: 10.1016/0076-6879(83)01013-7. [DOI] [PubMed] [Google Scholar]
- Hahn S., Hoar E. T., Guarente L. Each of three "TATA elements" specifies a subset of the transcription initiation sites at the CYC-1 promoter of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8562–8566. doi: 10.1073/pnas.82.24.8562. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hollenberg S. M., Evans R. M. Multiple and cooperative trans-activation domains of the human glucocorticoid receptor. Cell. 1988 Dec 2;55(5):899–906. doi: 10.1016/0092-8674(88)90145-6. [DOI] [PubMed] [Google Scholar]
- Kalff M., Gross B., Beato M. Progesterone receptor stimulates transcription of mouse mammary tumour virus in a cell-free system. Nature. 1990 Mar 22;344(6264):360–362. doi: 10.1038/344360a0. [DOI] [PubMed] [Google Scholar]
- Kim T. K., Roeder R. G. CTD-like sequences are important for transcriptional activation by the proline-rich activation domain of CTF1. Nucleic Acids Res. 1994 Jan 25;22(2):251–251. doi: 10.1093/nar/22.2.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kim T. K., Roeder R. G. Proline-rich activator CTF1 targets the TFIIB assembly step during transcriptional activation. Proc Natl Acad Sci U S A. 1994 May 10;91(10):4170–4174. doi: 10.1073/pnas.91.10.4170. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kralli A., Bohen S. P., Yamamoto K. R. LEM1, an ATP-binding-cassette transporter, selectively modulates the biological potency of steroid hormones. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4701–4705. doi: 10.1073/pnas.92.10.4701. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kruger W., Herskowitz I. A negative regulator of HO transcription, SIN1 (SPT2), is a nonspecific DNA-binding protein related to HMG1. Mol Cell Biol. 1991 Aug;11(8):4135–4146. doi: 10.1128/mcb.11.8.4135. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kruse U., Sippel A. E. Transcription factor nuclear factor I proteins form stable homo- and heterodimers. FEBS Lett. 1994 Jul 4;348(1):46–50. doi: 10.1016/0014-5793(94)00585-0. [DOI] [PubMed] [Google Scholar]
- Köhrer K., Domdey H. Preparation of high molecular weight RNA. Methods Enzymol. 1991;194:398–405. doi: 10.1016/0076-6879(91)94030-g. [DOI] [PubMed] [Google Scholar]
- 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]
- Lefebvre L., Smith M. Mutational and functional analysis of dominant SPT2 (SIN1) suppressor alleles in Saccharomyces cerevisiae. Mol Cell Biol. 1993 Sep;13(9):5393–5407. doi: 10.1128/mcb.13.9.5393. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Linder C., Thoma F. Histone H1 expressed in Saccharomyces cerevisiae binds to chromatin and affects survival, growth, transcription, and plasmid stability but does not change nucleosomal spacing. Mol Cell Biol. 1994 Apr;14(4):2822–2835. doi: 10.1128/mcb.14.4.2822. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marsolier M. C., Tanaka S., Livingstone-Zatchej M., Grunstein M., Thoma F., Sentenac A. Reciprocal interferences between nucleosomal organization and transcriptional activity of the yeast SNR6 gene. Genes Dev. 1995 Feb 15;9(4):410–422. doi: 10.1101/gad.9.4.410. [DOI] [PubMed] [Google Scholar]
- McEwan I. J., Wright A. P., Dahlman-Wright K., Carlstedt-Duke J., Gustafsson J. A. Direct interaction of the tau 1 transactivation domain of the human glucocorticoid receptor with the basal transcriptional machinery. Mol Cell Biol. 1993 Jan;13(1):399–407. doi: 10.1128/mcb.13.1.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McPherson C. E., Shim E. Y., Friedman D. S., Zaret K. S. An active tissue-specific enhancer and bound transcription factors existing in a precisely positioned nucleosomal array. Cell. 1993 Oct 22;75(2):387–398. doi: 10.1016/0092-8674(93)80079-t. [DOI] [PubMed] [Google Scholar]
- Miksicek R., Borgmeyer U., Nowock J. Interaction of the TGGCA-binding protein with upstream sequences is required for efficient transcription of mouse mammary tumor virus. EMBO J. 1987 May;6(5):1355–1360. doi: 10.1002/j.1460-2075.1987.tb02375.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miloshev G., Venkov P., van Holde K., Zlatanova J. Low levels of exogenous histone H1 in yeast cause cell death. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11567–11570. doi: 10.1073/pnas.91.24.11567. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Möws C. C., Preiss T., Slater E. P., Cao X., Verrijzer C. P., van Der Vliet P. C., Beato M. Two independent pathways for transcription from the MMTV promoter. J Steroid Biochem Mol Biol. 1994 Oct;51(1-2):21–32. doi: 10.1016/0960-0760(94)90111-2. [DOI] [PubMed] [Google Scholar]
- Nowock J., Borgmeyer U., Püschel A. W., Rupp R. A., Sippel A. E. The TGGCA protein binds to the MMTV-LTR, the adenovirus origin of replication, and the BK virus enhancer. Nucleic Acids Res. 1985 Mar 25;13(6):2045–2061. doi: 10.1093/nar/13.6.2045. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olesen J. T., Guarente L. The HAP2 subunit of yeast CCAAT transcriptional activator contains adjacent domains for subunit association and DNA recognition: model for the HAP2/3/4 complex. Genes Dev. 1990 Oct;4(10):1714–1729. doi: 10.1101/gad.4.10.1714. [DOI] [PubMed] [Google Scholar]
- Olesen J., Hahn S., Guarente L. Yeast HAP2 and HAP3 activators both bind to the CYC1 upstream activation site, UAS2, in an interdependent manner. Cell. 1987 Dec 24;51(6):953–961. doi: 10.1016/0092-8674(87)90582-4. [DOI] [PubMed] [Google Scholar]
- Oñate S. A., Prendergast P., Wagner J. P., Nissen M., Reeves R., Pettijohn D. E., Edwards D. P. The DNA-bending protein HMG-1 enhances progesterone receptor binding to its target DNA sequences. Mol Cell Biol. 1994 May;14(5):3376–3391. doi: 10.1128/mcb.14.5.3376. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Perlmann T. Glucocorticoid receptor DNA-binding specificity is increased by the organization of DNA in nucleosomes. Proc Natl Acad Sci U S A. 1992 May 1;89(9):3884–3888. doi: 10.1073/pnas.89.9.3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Perlmann T., Wrange O. Specific glucocorticoid receptor binding to DNA reconstituted in a nucleosome. EMBO J. 1988 Oct;7(10):3073–3079. doi: 10.1002/j.1460-2075.1988.tb03172.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peterson C. L., Kruger W., Herskowitz I. A functional interaction between the C-terminal domain of RNA polymerase II and the negative regulator SIN1. Cell. 1991 Mar 22;64(6):1135–1143. doi: 10.1016/0092-8674(91)90268-4. [DOI] [PubMed] [Google Scholar]
- Pfeifer G. P., Steigerwald S. D., Mueller P. R., Wold B., Riggs A. D. Genomic sequencing and methylation analysis by ligation mediated PCR. Science. 1989 Nov 10;246(4931):810–813. doi: 10.1126/science.2814502. [DOI] [PubMed] [Google Scholar]
- Pfeifer K., Prezant T., Guarente L. Yeast HAP1 activator binds to two upstream activation sites of different sequence. Cell. 1987 Apr 10;49(1):19–27. doi: 10.1016/0092-8674(87)90751-3. [DOI] [PubMed] [Google Scholar]
- Philippsen P., Stotz A., Scherf C. DNA of Saccharomyces cerevisiae. Methods Enzymol. 1991;194:169–182. doi: 10.1016/0076-6879(91)94014-4. [DOI] [PubMed] [Google Scholar]
- Pierce J., Fee B. E., Toohey M. G., Peterson D. O. A mouse mammary tumor virus promoter element near the transcription initiation site. J Virol. 1993 Jan;67(1):415–424. doi: 10.1128/jvi.67.1.415-424.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Piña B., Barettino D., Beato M. Nucleosome positioning and regulated gene expression. Oxf Surv Eukaryot Genes. 1991;7:83–117. [PubMed] [Google Scholar]
- 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]
- 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]
- Ristiniemi J., Oikarinen J. Histone H1 binds to the putative nuclear factor I recognition sequence in the mouse alpha 2(I) collagen promoter. J Biol Chem. 1989 Feb 5;264(4):2164–2174. [PubMed] [Google Scholar]
- Rothstein R., Helms C., Rosenberg N. Concerted deletions and inversions are caused by mitotic recombination between delta sequences in Saccharomyces cerevisiae. Mol Cell Biol. 1987 Mar;7(3):1198–1207. doi: 10.1128/mcb.7.3.1198. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rupp R. A., Kruse U., Multhaup G., Göbel U., Beyreuther K., Sippel A. E. Chicken NFI/TGGCA proteins are encoded by at least three independent genes: NFI-A, NFI-B and NFI-C with homologues in mammalian genomes. Nucleic Acids Res. 1990 May 11;18(9):2607–2616. doi: 10.1093/nar/18.9.2607. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scheidereit C., Beato M. Contacts between hormone receptor and DNA double helix within a glucocorticoid regulatory element of mouse mammary tumor virus. Proc Natl Acad Sci U S A. 1984 May;81(10):3029–3033. doi: 10.1073/pnas.81.10.3029. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scheidereit C., Geisse S., Westphal H. M., Beato M. The glucocorticoid receptor binds to defined nucleotide sequences near the promoter of mouse mammary tumour virus. Nature. 1983 Aug 25;304(5928):749–752. doi: 10.1038/304749a0. [DOI] [PubMed] [Google Scholar]
- Schena M., Picard D., Yamamoto K. R. Vectors for constitutive and inducible gene expression in yeast. Methods Enzymol. 1991;194:389–398. doi: 10.1016/0076-6879(91)94029-c. [DOI] [PubMed] [Google Scholar]
- Schena M., Yamamoto K. R. Mammalian glucocorticoid receptor derivatives enhance transcription in yeast. Science. 1988 Aug 19;241(4868):965–967. doi: 10.1126/science.3043665. [DOI] [PubMed] [Google Scholar]
- Sikorski R. S., Boeke J. D. In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast. Methods Enzymol. 1991;194:302–318. doi: 10.1016/0076-6879(91)94023-6. [DOI] [PubMed] [Google Scholar]
- Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Strubin M., Newell J. W., Matthias P. OBF-1, a novel B cell-specific coactivator that stimulates immunoglobulin promoter activity through association with octamer-binding proteins. Cell. 1995 Feb 10;80(3):497–506. doi: 10.1016/0092-8674(95)90500-6. [DOI] [PubMed] [Google Scholar]
- Thomas G. H., Elgin S. C. Protein/DNA architecture of the DNase I hypersensitive region of the Drosophila hsp26 promoter. EMBO J. 1988 Jul;7(7):2191–2201. doi: 10.1002/j.1460-2075.1988.tb03058.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Toohey M. G., Lee J. W., Huang M., Peterson D. O. Functional elements of the steroid hormone-responsive promoter of mouse mammary tumor virus. J Virol. 1990 Sep;64(9):4477–4488. doi: 10.1128/jvi.64.9.4477-4488.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Truss M., Beato M. Steroid hormone receptors: interaction with deoxyribonucleic acid and transcription factors. Endocr Rev. 1993 Aug;14(4):459–479. doi: 10.1210/edrv-14-4-459. [DOI] [PubMed] [Google Scholar]
- Wendler W., Altmann H., Ludwig-Winnacker E. Transcriptional activation of NFI/CTF1 depends on a sequence motif strongly related to the carboxyterminal domain of RNA polymerase II. Nucleic Acids Res. 1994 Jul 11;22(13):2601–2603. doi: 10.1093/nar/22.13.2601. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wieland S., Döbbeling U., Rusconi S. Interference and synergism of glucocorticoid receptor and octamer factors. EMBO J. 1991 Sep;10(9):2513–2521. doi: 10.1002/j.1460-2075.1991.tb07791.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wright A. P., Carlstedt-Duke J., Gustafsson J. A. Ligand-specific transactivation of gene expression by a derivative of the human glucocorticoid receptor expressed in yeast. J Biol Chem. 1990 Sep 5;265(25):14763–14769. [PubMed] [Google Scholar]
- Wright A. P., Gustafsson J. A. Glucocorticoid-specific gene activation by the intact human glucocorticoid receptor expressed in yeast. Glucocorticoid specificity depends on low level receptor expression. J Biol Chem. 1992 Jun 5;267(16):11191–11195. [PubMed] [Google Scholar]
- Wright A. P., McEwan I. J., Dahlman-Wright K., Gustafsson J. A. High level expression of the major transactivation domain of the human glucocorticoid receptor in yeast cells inhibits endogenous gene expression and cell growth. Mol Endocrinol. 1991 Oct;5(10):1366–1372. doi: 10.1210/mend-5-10-1366. [DOI] [PubMed] [Google Scholar]
- Yaneva J. N., Zlatanova J. S. Does histone H1 bind specifically to the nuclear factor I recognition sequence? Biochimie. 1993;75(6):497–500. doi: 10.1016/0300-9084(93)90116-a. [DOI] [PubMed] [Google Scholar]
- Yoshinaga S. K., Peterson C. L., Herskowitz I., Yamamoto K. R. Roles of SWI1, SWI2, and SWI3 proteins for transcriptional enhancement by steroid receptors. Science. 1992 Dec 4;258(5088):1598–1604. doi: 10.1126/science.1360703. [DOI] [PubMed] [Google Scholar]
- Zhang S., Lockshin C., Herbert A., Winter E., Rich A. Zuotin, a putative Z-DNA binding protein in Saccharomyces cerevisiae. EMBO J. 1992 Oct;11(10):3787–3796. doi: 10.1002/j.1460-2075.1992.tb05464.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zinn K., DiMaio D., Maniatis T. Identification of two distinct regulatory regions adjacent to the human beta-interferon gene. Cell. 1983 Oct;34(3):865–879. doi: 10.1016/0092-8674(83)90544-5. [DOI] [PubMed] [Google Scholar]