Abstract
During lytic infection, herpes simplex virus subverts the host cell RNA polymerase II transcription machinery to efficiently express its own genome while repressing the expression of most cellular genes. The mechanism by which RNA polymerase II is directed to the viral delayed-early and late genes is still unresolved. We report here that RNA polymerase II is preferentially localized to viral replication compartments early after infection with herpes simplex virus type 1. Concurrent with recruitment of RNA polymerase II into viral compartments is a rapid and aberrant phosphorylation of the large subunit carboxy-terminal domain (CTD). Aberrant phosphorylation of the CTD requires early viral gene expression but is not dependent on viral DNA replication or on the formation of viral replication compartments. Localization of RNA polymerase II and modifications to the CTD may be instrumental in favoring transcription of viral genes and repressing specific transcription of cellular genes.
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- Allison L. A., Ingles C. J. Mutations in RNA polymerase II enhance or suppress mutations in GAL4. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2794–2798. doi: 10.1073/pnas.86.8.2794. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Allison L. A., Wong J. K., Fitzpatrick V. D., Moyle M., Ingles C. J. The C-terminal domain of the largest subunit of RNA polymerase II of Saccharomyces cerevisiae, Drosophila melanogaster, and mammals: a conserved structure with an essential function. Mol Cell Biol. 1988 Jan;8(1):321–329. doi: 10.1128/mcb.8.1.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bartholomew B., Dahmus M. E., Meares C. F. RNA contacts subunits IIo and IIc in HeLa RNA polymerase II transcription complexes. J Biol Chem. 1986 Oct 25;261(30):14226–14231. [PubMed] [Google Scholar]
- Buermeyer A. B., Thompson N. E., Strasheim L. A., Burgess R. R., Farnham P. J. The HIP1 initiator element plays a role in determining the in vitro requirement of the dihydrofolate reductase gene promoter for the C-terminal domain of RNA polymerase II. Mol Cell Biol. 1992 May;12(5):2250–2259. doi: 10.1128/mcb.12.5.2250. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buratowski S., Sharp P. A. Transcription initiation complexes and upstream activation with RNA polymerase II lacking the C-terminal domain of the largest subunit. Mol Cell Biol. 1990 Oct;10(10):5562–5564. doi: 10.1128/mcb.10.10.5562. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cadena D. L., Dahmus M. E. Messenger RNA synthesis in mammalian cells is catalyzed by the phosphorylated form of RNA polymerase II. J Biol Chem. 1987 Sep 15;262(26):12468–12474. [PubMed] [Google Scholar]
- Chesnut J. D., Stephens J. H., Dahmus M. E. The interaction of RNA polymerase II with the adenovirus-2 major late promoter is precluded by phosphorylation of the C-terminal domain of subunit IIa. J Biol Chem. 1992 May 25;267(15):10500–10506. [PubMed] [Google Scholar]
- Cisek L. J., Corden J. L. Phosphorylation of RNA polymerase by the murine homologue of the cell-cycle control protein cdc2. Nature. 1989 Jun 29;339(6227):679–684. doi: 10.1038/339679a0. [DOI] [PubMed] [Google Scholar]
- Coen D. M., Weinheimer S. P., McKnight S. L. A genetic approach to promoter recognition during trans induction of viral gene expression. Science. 1986 Oct 3;234(4772):53–59. doi: 10.1126/science.3018926. [DOI] [PubMed] [Google Scholar]
- Conaway R. C., Bradsher J. N., Conaway J. W. Mechanism of assembly of the RNA polymerase II preinitiation complex. Evidence for a functional interaction between the carboxyl-terminal domain of the largest subunit of RNA polymerase II and a high molecular mass form of the TATA factor. J Biol Chem. 1992 Apr 25;267(12):8464–8467. [PubMed] [Google Scholar]
- Corden J. L., Cadena D. L., Ahearn J. M., Jr, Dahmus M. E. A unique structure at the carboxyl terminus of the largest subunit of eukaryotic RNA polymerase II. Proc Natl Acad Sci U S A. 1985 Dec;82(23):7934–7938. doi: 10.1073/pnas.82.23.7934. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Corden J. L. RNA polymerase II transcription cycles. Curr Opin Genet Dev. 1993 Apr;3(2):213–218. doi: 10.1016/0959-437x(93)90025-k. [DOI] [PubMed] [Google Scholar]
- Corden J. L. Tails of RNA polymerase II. Trends Biochem Sci. 1990 Oct;15(10):383–387. doi: 10.1016/0968-0004(90)90236-5. [DOI] [PubMed] [Google Scholar]
- DeLuca N. A., Courtney M. A., Schaffer P. A. Temperature-sensitive mutants in herpes simplex virus type 1 ICP4 permissive for early gene expression. J Virol. 1984 Dec;52(3):767–776. doi: 10.1128/jvi.52.3.767-776.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeLuca N. A., McCarthy A. M., Schaffer P. A. Isolation and characterization of deletion mutants of herpes simplex virus type 1 in the gene encoding immediate-early regulatory protein ICP4. J Virol. 1985 Nov;56(2):558–570. doi: 10.1128/jvi.56.2.558-570.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeLuca N. A., Schaffer P. A. Activation of immediate-early, early, and late promoters by temperature-sensitive and wild-type forms of herpes simplex virus type 1 protein ICP4. Mol Cell Biol. 1985 Aug;5(8):1997–2008. doi: 10.1128/mcb.5.8.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deshmane S. L., Fraser N. W. During latency, herpes simplex virus type 1 DNA is associated with nucleosomes in a chromatin structure. J Virol. 1989 Feb;63(2):943–947. doi: 10.1128/jvi.63.2.943-947.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dvir A., Peterson S. R., Knuth M. W., Lu H., Dynan W. S. Ku autoantigen is the regulatory component of a template-associated protein kinase that phosphorylates RNA polymerase II. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11920–11924. doi: 10.1073/pnas.89.24.11920. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Everett R. D. Activation of cellular promoters during herpes virus infection of biochemically transformed cells. EMBO J. 1985 Aug;4(8):1973–1980. doi: 10.1002/j.1460-2075.1985.tb03880.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fenwick M. L., Clark J. Early and delayed shut-off of host protein synthesis in cells infected with herpes simplex virus. J Gen Virol. 1982 Jul;61(Pt 50):121–125. doi: 10.1099/0022-1317-61-1-121. [DOI] [PubMed] [Google Scholar]
- Fenwick M. L., Owen S. A. On the control of immediate early (alpha) mRNA survival in cells infected with herpes simplex virus. J Gen Virol. 1988 Nov;69(Pt 11):2869–2877. doi: 10.1099/0022-1317-69-11-2869. [DOI] [PubMed] [Google Scholar]
- Gao M., Knipe D. M. Genetic evidence for multiple nuclear functions of the herpes simplex virus ICP8 DNA-binding protein. J Virol. 1989 Dec;63(12):5258–5267. doi: 10.1128/jvi.63.12.5258-5267.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Godowski P. J., Knipe D. M. Transcriptional control of herpesvirus gene expression: gene functions required for positive and negative regulation. Proc Natl Acad Sci U S A. 1986 Jan;83(2):256–260. doi: 10.1073/pnas.83.2.256. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
- Greenleaf A. L. Positive patches and negative noodles: linking RNA processing to transcription? Trends Biochem Sci. 1993 Apr;18(4):117–119. doi: 10.1016/0968-0004(93)90016-g. [DOI] [PubMed] [Google Scholar]
- Hill T. M., Sadler J. R., Betz J. L. Virion component of herpes simplex virus type 1 KOS interferes with early shutoff of host protein synthesis induced by herpes simplex virus type 2 186. J Virol. 1985 Oct;56(1):312–316. doi: 10.1128/jvi.56.1.312-316.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill T. M., Sinden R. R., Sadler J. R. Herpes simplex virus types 1 and 2 induce shutoff of host protein synthesis by different mechanisms in Friend erythroleukemia cells. J Virol. 1983 Jan;45(1):241–250. doi: 10.1128/jvi.45.1.241-250.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoffman M. The cell's nucleus shapes up. Science. 1993 Feb 26;259(5099):1257–1259. doi: 10.1126/science.8446894. [DOI] [PubMed] [Google Scholar]
- Homa F. L., Glorioso J. C., Levine M. A specific 15-bp TATA box promoter element is required for expression of a herpes simplex virus type 1 late gene. Genes Dev. 1988 Jan;2(1):40–53. doi: 10.1101/gad.2.1.40. [DOI] [PubMed] [Google Scholar]
- Honess R. W., Roizman B. Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins. J Virol. 1974 Jul;14(1):8–19. doi: 10.1128/jvi.14.1.8-19.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hozák P., Hassan A. B., Jackson D. A., Cook P. R. Visualization of replication factories attached to nucleoskeleton. Cell. 1993 Apr 23;73(2):361–373. doi: 10.1016/0092-8674(93)90235-i. [DOI] [PubMed] [Google Scholar]
- Jiménez-García L. F., Spector D. L. In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism. Cell. 1993 Apr 9;73(1):47–59. doi: 10.1016/0092-8674(93)90159-n. [DOI] [PubMed] [Google Scholar]
- Johnson D. C., Frame M. C., Ligas M. W., Cross A. M., Stow N. D. Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI. J Virol. 1988 Apr;62(4):1347–1354. doi: 10.1128/jvi.62.4.1347-1354.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson P. A., Everett R. D. The control of herpes simplex virus type-1 late gene transcription: a 'TATA-box'/cap site region is sufficient for fully efficient regulated activity. Nucleic Acids Res. 1986 Nov 11;14(21):8247–8264. doi: 10.1093/nar/14.21.8247. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kim W. Y., Dahmus M. E. Immunochemical analysis of mammalian RNA polymerase II subspecies. Stability and relative in vivo concentration. J Biol Chem. 1986 Oct 25;261(30):14219–14225. [PubMed] [Google Scholar]
- Kim W. Y., Dahmus M. E. Purification of RNA polymerase IIO from calf thymus. J Biol Chem. 1988 Dec 15;263(35):18880–18885. [PubMed] [Google Scholar]
- Kim W. Y., Dahmus M. E. The major late promoter of adenovirus-2 is accurately transcribed by RNA polymerases IIO, IIA, and IIB. J Biol Chem. 1989 Feb 25;264(6):3169–3176. [PubMed] [Google Scholar]
- Knipe D. M., Senechek D., Rice S. A., Smith J. L. Stages in the nuclear association of the herpes simplex virus transcriptional activator protein ICP4. J Virol. 1987 Feb;61(2):276–284. doi: 10.1128/jvi.61.2.276-284.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knipe D. M., Spang A. E. Definition of a series of stages in the association of two herpesviral proteins with the cell nucleus. J Virol. 1982 Jul;43(1):314–324. doi: 10.1128/jvi.43.1.314-324.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koleske A. J., Buratowski S., Nonet M., Young R. A. A novel transcription factor reveals a functional link between the RNA polymerase II CTD and TFIID. Cell. 1992 May 29;69(5):883–894. doi: 10.1016/0092-8674(92)90298-q. [DOI] [PubMed] [Google Scholar]
- Kolodziej P. A., Woychik N., Liao S. M., Young R. A. RNA polymerase II subunit composition, stoichiometry, and phosphorylation. Mol Cell Biol. 1990 May;10(5):1915–1920. doi: 10.1128/mcb.10.5.1915. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krämer A., Bautz E. K. Immunological relatedness of subunits of RNA polymerase II from insects and mammals. Eur J Biochem. 1981 Jul;117(3):449–455. doi: 10.1111/j.1432-1033.1981.tb06359.x. [DOI] [PubMed] [Google Scholar]
- Krämer A., Haars R., Kabisch R., Will H., Bautz F. A., Bautz E. K. Monoclonal antibody directed against RNA polymerase II of Drosophila melanogaster. Mol Gen Genet. 1980;180(1):193–199. doi: 10.1007/BF00267369. [DOI] [PubMed] [Google Scholar]
- Kwong A. D., Frenkel N. Herpes simplex virus-infected cells contain a function(s) that destabilizes both host and viral mRNAs. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1926–1930. doi: 10.1073/pnas.84.7.1926. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Laybourn P. J., Dahmus M. E. Phosphorylation of RNA polymerase IIA occurs subsequent to interaction with the promoter and before the initiation of transcription. J Biol Chem. 1990 Aug 5;265(22):13165–13173. [PubMed] [Google Scholar]
- Lee J. M., Greenleaf A. L. A protein kinase that phosphorylates the C-terminal repeat domain of the largest subunit of RNA polymerase II. Proc Natl Acad Sci U S A. 1989 May;86(10):3624–3628. doi: 10.1073/pnas.86.10.3624. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leinbach S. S., Summers W. C. The structure of herpes simplex virus type 1 DNA as probed by micrococcal nuclease digestion. J Gen Virol. 1980 Nov;51(Pt 1):45–59. doi: 10.1099/0022-1317-51-1-45. [DOI] [PubMed] [Google Scholar]
- Liao S. M., Taylor I. C., Kingston R. E., Young R. A. RNA polymerase II carboxy-terminal domain contributes to the response to multiple acidic activators in vitro. Genes Dev. 1991 Dec;5(12B):2431–2440. doi: 10.1101/gad.5.12b.2431. [DOI] [PubMed] [Google Scholar]
- Lu H., Flores O., Weinmann R., Reinberg D. The nonphosphorylated form of RNA polymerase II preferentially associates with the preinitiation complex. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10004–10008. doi: 10.1073/pnas.88.22.10004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lu H., Zawel L., Fisher L., Egly J. M., Reinberg D. Human general transcription factor IIH phosphorylates the C-terminal domain of RNA polymerase II. Nature. 1992 Aug 20;358(6388):641–645. doi: 10.1038/358641a0. [DOI] [PubMed] [Google Scholar]
- Mackem S., Roizman B. Regulation of herpesvirus macromolecular synthesis: temporal order of transcription of alpha genes is not dependent on the stringency of inhibition of protein synthesis. J Virol. 1981 Oct;40(1):319–322. doi: 10.1128/jvi.40.1.319-322.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayman B. A., Nishioka Y. Differential stability of host mRNAs in Friend erythroleukemia cells infected with herpes simplex virus type 1. J Virol. 1985 Jan;53(1):1–6. doi: 10.1128/jvi.53.1.1-6.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McKnight S., Tjian R. Transcriptional selectivity of viral genes in mammalian cells. Cell. 1986 Sep 12;46(6):795–805. doi: 10.1016/0092-8674(86)90061-9. [DOI] [PubMed] [Google Scholar]
- Muggeridge M. I., Fraser N. W. Chromosomal organization of the herpes simplex virus genome during acute infection of the mouse central nervous system. J Virol. 1986 Sep;59(3):764–767. doi: 10.1128/jvi.59.3.764-767.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nishioka Y., Silverstein S. Requirement of protein synthesis for the degradation of host mRNA in Friend erythroleukemia cells infected wtih herpes simplex virus type 1. J Virol. 1978 Sep;27(3):619–627. doi: 10.1128/jvi.27.3.619-627.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nonet M. L., Young R. A. Intragenic and extragenic suppressors of mutations in the heptapeptide repeat domain of Saccharomyces cerevisiae RNA polymerase II. Genetics. 1989 Dec;123(4):715–724. doi: 10.1093/genetics/123.4.715. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Paterson T., Everett R. D. The regions of the herpes simplex virus type 1 immediate early protein Vmw175 required for site specific DNA binding closely correspond to those involved in transcriptional regulation. Nucleic Acids Res. 1988 Dec 9;16(23):11005–11025. doi: 10.1093/nar/16.23.11005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Payne J. M., Dahmus M. E. Partial purification and characterization of two distinct protein kinases that differentially phosphorylate the carboxyl-terminal domain of RNA polymerase subunit IIa. J Biol Chem. 1993 Jan 5;268(1):80–87. [PubMed] [Google Scholar]
- Payne J. M., Laybourn P. J., Dahmus M. E. The transition of RNA polymerase II from initiation to elongation is associated with phosphorylation of the carboxyl-terminal domain of subunit IIa. J Biol Chem. 1989 Nov 25;264(33):19621–19629. [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]
- Peterson S. R., Dvir A., Anderson C. W., Dynan W. S. DNA binding provides a signal for phosphorylation of the RNA polymerase II heptapeptide repeats. Genes Dev. 1992 Mar;6(3):426–438. doi: 10.1101/gad.6.3.426. [DOI] [PubMed] [Google Scholar]
- Preston C. M. Control of herpes simplex virus type 1 mRNA synthesis in cells infected with wild-type virus or the temperature-sensitive mutant tsK. J Virol. 1979 Jan;29(1):275–284. doi: 10.1128/jvi.29.1.275-284.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quinlan M. P., Chen L. B., Knipe D. M. The intranuclear location of a herpes simplex virus DNA-binding protein is determined by the status of viral DNA replication. Cell. 1984 Apr;36(4):857–868. doi: 10.1016/0092-8674(84)90035-7. [DOI] [PubMed] [Google Scholar]
- Randall R. E., Dinwoodie N. Intranuclear localization of herpes simplex virus immediate-early and delayed-early proteins: evidence that ICP 4 is associated with progeny virus DNA. J Gen Virol. 1986 Oct;67(Pt 10):2163–2177. doi: 10.1099/0022-1317-67-10-2163. [DOI] [PubMed] [Google Scholar]
- Rice S. A., Knipe D. M. Gene-specific transactivation by herpes simplex virus type 1 alpha protein ICP27. J Virol. 1988 Oct;62(10):3814–3823. doi: 10.1128/jvi.62.10.3814-3823.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sacks W. R., Greene C. C., Aschman D. P., Schaffer P. A. Herpes simplex virus type 1 ICP27 is an essential regulatory protein. J Virol. 1985 Sep;55(3):796–805. doi: 10.1128/jvi.55.3.796-805.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sawadogo M., Sentenac A. RNA polymerase B (II) and general transcription factors. Annu Rev Biochem. 1990;59:711–754. doi: 10.1146/annurev.bi.59.070190.003431. [DOI] [PubMed] [Google Scholar]
- Scafe C., Chao D., Lopes J., Hirsch J. P., Henry S., Young R. A. RNA polymerase II C-terminal repeat influences response to transcriptional enhancer signals. Nature. 1990 Oct 4;347(6292):491–494. doi: 10.1038/347491a0. [DOI] [PubMed] [Google Scholar]
- Schek N., Bachenheimer S. L. Degradation of cellular mRNAs induced by a virion-associated factor during herpes simplex virus infection of Vero cells. J Virol. 1985 Sep;55(3):601–610. doi: 10.1128/jvi.55.3.601-610.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Serizawa H., Conaway J. W., Conaway R. C. Phosphorylation of C-terminal domain of RNA polymerase II is not required in basal transcription. Nature. 1993 May 27;363(6427):371–374. doi: 10.1038/363371a0. [DOI] [PubMed] [Google Scholar]
- Serizawa H., Conaway R. C., Conaway J. W. A carboxyl-terminal-domain kinase associated with RNA polymerase II transcription factor delta from rat liver. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7476–7480. doi: 10.1073/pnas.89.16.7476. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shepard A. A., Imbalzano A. N., DeLuca N. A. Separation of primary structural components conferring autoregulation, transactivation, and DNA-binding properties to the herpes simplex virus transcriptional regulatory protein ICP4. J Virol. 1989 Sep;63(9):3714–3728. doi: 10.1128/jvi.63.9.3714-3728.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sigler P. B. Transcriptional activation. Acid blobs and negative noodles. Nature. 1988 May 19;333(6170):210–212. doi: 10.1038/333210a0. [DOI] [PubMed] [Google Scholar]
- Smibert C. A., Smiley J. R. Differential regulation of endogenous and transduced beta-globin genes during infection of erythroid cells with a herpes simplex virus type 1 recombinant. J Virol. 1990 Aug;64(8):3882–3894. doi: 10.1128/jvi.64.8.3882-3894.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smiley J. R., Johnson D. C., Pizer L. I., Everett R. D. The ICP4 binding sites in the herpes simplex virus type 1 glycoprotein D (gD) promoter are not essential for efficient gD transcription during virus infection. J Virol. 1992 Feb;66(2):623–631. doi: 10.1128/jvi.66.2.623-631.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smiley J. R., Smibert C., Everett R. D. Expression of a cellular gene cloned in herpes simplex virus: rabbit beta-globin is regulated as an early viral gene in infected fibroblasts. J Virol. 1987 Aug;61(8):2368–2377. doi: 10.1128/jvi.61.8.2368-2377.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Su L., Knipe D. M. Herpes simplex virus alpha protein ICP27 can inhibit or augment viral gene transactivation. Virology. 1989 Jun;170(2):496–504. doi: 10.1016/0042-6822(89)90441-8. [DOI] [PubMed] [Google Scholar]
- Swedlow J. R., Sedat J. W., Agard D. A. Multiple chromosomal populations of topoisomerase II detected in vivo by time-lapse, three-dimensional wide-field microscopy. Cell. 1993 Apr 9;73(1):97–108. doi: 10.1016/0092-8674(93)90163-k. [DOI] [PubMed] [Google Scholar]
- Sydiskis R. J., Roizman B. Polysomes and protein synthesis in cells infected with a DNA virus. Science. 1966 Jul 1;153(3731):76–78. doi: 10.1126/science.153.3731.76. [DOI] [PubMed] [Google Scholar]
- Thompson N. E., Aronson D. B., Burgess R. R. Purification of eukaryotic RNA polymerase II by immunoaffinity chromatography. Elution of active enzyme with protein stabilizing agents from a polyol-responsive monoclonal antibody. J Biol Chem. 1990 Apr 25;265(12):7069–7077. [PubMed] [Google Scholar]
- Thompson N. E., Steinberg T. H., Aronson D. B., Burgess R. R. Inhibition of in vivo and in vitro transcription by monoclonal antibodies prepared against wheat germ RNA polymerase II that react with the heptapeptide repeat of eukaryotic RNA polymerase II. J Biol Chem. 1989 Jul 5;264(19):11511–11520. [PubMed] [Google Scholar]
- Usheva A., Maldonado E., Goldring A., Lu H., Houbavi C., Reinberg D., Aloni Y. Specific interaction between the nonphosphorylated form of RNA polymerase II and the TATA-binding protein. Cell. 1992 May 29;69(5):871–881. doi: 10.1016/0092-8674(92)90297-p. [DOI] [PubMed] [Google Scholar]
- Watson R. J., Clements J. B. A herpes simplex virus type 1 function continuously required for early and late virus RNA synthesis. Nature. 1980 May 29;285(5763):329–330. doi: 10.1038/285329a0. [DOI] [PubMed] [Google Scholar]
- Weinheimer S. P., McKnight S. L. Transcriptional and post-transcriptional controls establish the cascade of herpes simplex virus protein synthesis. J Mol Biol. 1987 Jun 20;195(4):819–833. doi: 10.1016/0022-2836(87)90487-6. [DOI] [PubMed] [Google Scholar]
- Wilcock D., Lane D. P. Localization of p53, retinoblastoma and host replication proteins at sites of viral replication in herpes-infected cells. Nature. 1991 Jan 31;349(6308):429–431. doi: 10.1038/349429a0. [DOI] [PubMed] [Google Scholar]
- Woychik N. A., Young R. A. RNA polymerase II: subunit structure and function. Trends Biochem Sci. 1990 Sep;15(9):347–351. doi: 10.1016/0968-0004(90)90074-l. [DOI] [PubMed] [Google Scholar]
- Xing Y., Johnson C. V., Dobner P. R., Lawrence J. B. Higher level organization of individual gene transcription and RNA splicing. Science. 1993 Feb 26;259(5099):1326–1330. doi: 10.1126/science.8446901. [DOI] [PubMed] [Google Scholar]
- Young R. A. RNA polymerase II. Annu Rev Biochem. 1991;60:689–715. doi: 10.1146/annurev.bi.60.070191.003353. [DOI] [PubMed] [Google Scholar]
- Zehring W. A., Greenleaf A. L. The carboxyl-terminal repeat domain of RNA polymerase II is not required for transcription factor Sp1 to function in vitro. J Biol Chem. 1990 May 25;265(15):8351–8353. [PubMed] [Google Scholar]
- Zehring W. A., Lee J. M., Weeks J. R., Jokerst R. S., Greenleaf A. L. The C-terminal repeat domain of RNA polymerase II largest subunit is essential in vivo but is not required for accurate transcription initiation in vitro. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3698–3702. doi: 10.1073/pnas.85.11.3698. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang J., Corden J. L. Identification of phosphorylation sites in the repetitive carboxyl-terminal domain of the mouse RNA polymerase II largest subunit. J Biol Chem. 1991 Feb 5;266(4):2290–2296. [PubMed] [Google Scholar]
- Zhang J., Corden J. L. Phosphorylation causes a conformational change in the carboxyl-terminal domain of the mouse RNA polymerase II largest subunit. J Biol Chem. 1991 Feb 5;266(4):2297–2302. [PubMed] [Google Scholar]
- de Bruyn Kops A., Knipe D. M. Formation of DNA replication structures in herpes virus-infected cells requires a viral DNA binding protein. Cell. 1988 Dec 2;55(5):857–868. doi: 10.1016/0092-8674(88)90141-9. [DOI] [PubMed] [Google Scholar]








