Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1997 Oct 15;16(20):6250–6262. doi: 10.1093/emboj/16.20.6250

Nuclear translocation and carboxyl-terminal domain phosphorylation of RNA polymerase II delineate the two phases of zygotic gene activation in mammalian embryos.

S Bellier 1, S Chastant 1, P Adenot 1, M Vincent 1, J P Renard 1, O Bensaude 1
PMCID: PMC1326309  PMID: 9321404

Abstract

In mammalian embryos, zygotic gene transcription initiates after a limited number of cell divisions through a two-step process termed the zygotic gene activation (ZGA). Here we report that RNA polymerase II undergoes major changes in mouse and rabbit preimplantation embryos during the ZGA. In transcriptionally inactive unfertilized oocytes, the RNA polymerase II largest subunit is predominantly hyperphosphorylated on its carboxy-terminal domain (CTD). The CTD is markedly dephosphorylated several hours after fertilization, before the onset of a period characterized by a weak transcriptional activity. The largest subunit of RNA polymerase II then lacks immunological and drug-sensitivity characteristics related to its phosphorylation by the TFIIH-associated kinase and gradually translocates into the nuclei independently of DNA replication and mitosis. A phosphorylation pattern of the largest subunit, close to that observed in somatic cells, is established in both mouse and rabbit embryos at the stage when transcription becomes a requirement for further development (respectively at the 2- and 8/16-cell stage). As these events occurred in the presence of actinomycin D, the nuclear translocation of RNA polymerase II and the phosphorylation of the CTD might be major determinants of ZGA.

Full Text

The Full Text of this article is available as a PDF (600.9 KB).

Selected References

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

  1. Adenot P. G., Szöllösi M. S., Geze M., Renard J. P., Debey P. Dynamics of paternal chromatin changes in live one-cell mouse embryo after natural fertilization. Mol Reprod Dev. 1991 Jan;28(1):23–34. doi: 10.1002/mrd.1080280105. [DOI] [PubMed] [Google Scholar]
  2. Akhtar A., Faye G., Bentley D. L. Distinct activated and non-activated RNA polymerase II complexes in yeast. EMBO J. 1996 Sep 2;15(17):4654–4664. [PMC free article] [PubMed] [Google Scholar]
  3. Almouzni G., Wolffe A. P. Constraints on transcriptional activator function contribute to transcriptional quiescence during early Xenopus embryogenesis. EMBO J. 1995 Apr 18;14(8):1752–1765. doi: 10.1002/j.1460-2075.1995.tb07164.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Aoki F., Worrad D. M., Schultz R. M. Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev Biol. 1997 Jan 15;181(2):296–307. doi: 10.1006/dbio.1996.8466. [DOI] [PubMed] [Google Scholar]
  5. Baskaran R., Chiang G. G., Wang J. Y. Identification of a binding site in c-Ab1 tyrosine kinase for the C-terminal repeated domain of RNA polymerase II. Mol Cell Biol. 1996 Jul;16(7):3361–3369. doi: 10.1128/mcb.16.7.3361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bellier S., Dubois M. F., Nishida E., Almouzni G., Bensaude O. Phosphorylation of the RNA polymerase II largest subunit during Xenopus laevis oocyte maturation. Mol Cell Biol. 1997 Mar;17(3):1434–1440. doi: 10.1128/mcb.17.3.1434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bensaude O., Babinet C., Morange M., Jacob F. Heat shock proteins, first major products of zygotic gene activity in mouse embryo. Nature. 1983 Sep 22;305(5932):331–333. doi: 10.1038/305331a0. [DOI] [PubMed] [Google Scholar]
  8. Bisotto S., Lauriault P., Duval M., Vincent M. Colocalization of a high molecular mass phosphoprotein of the nuclear matrix (p255) with spliceosomes. J Cell Sci. 1995 May;108(Pt 5):1873–1882. doi: 10.1242/jcs.108.5.1873. [DOI] [PubMed] [Google Scholar]
  9. Björklund S., Kim Y. J. Mediator of transcriptional regulation. Trends Biochem Sci. 1996 Sep;21(9):335–337. doi: 10.1016/s0968-0004(96)10051-7. [DOI] [PubMed] [Google Scholar]
  10. Bouniol C., Nguyen E., Debey P. Endogenous transcription occurs at the 1-cell stage in the mouse embryo. Exp Cell Res. 1995 May;218(1):57–62. doi: 10.1006/excr.1995.1130. [DOI] [PubMed] [Google Scholar]
  11. Bregman D. B., Du L., van der Zee S., Warren S. L. Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J Cell Biol. 1995 Apr;129(2):287–298. doi: 10.1083/jcb.129.2.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chabot B., Bisotto S., Vincent M. The nuclear matrix phosphoprotein p255 associates with splicing complexes as part of the [U4/U6.U5] tri-snRNP particle. Nucleic Acids Res. 1995 Aug 25;23(16):3206–3213. doi: 10.1093/nar/23.16.3206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Christians E., Campion E., Thompson E. M., Renard J. P. Expression of the HSP 70.1 gene, a landmark of early zygotic activity in the mouse embryo, is restricted to the first burst of transcription. Development. 1995 Jan;121(1):113–122. doi: 10.1242/dev.121.1.113. [DOI] [PubMed] [Google Scholar]
  14. Christians E., Rao V. H., Renard J. P. Sequential acquisition of transcriptional control during early embryonic development in the rabbit. Dev Biol. 1994 Jul;164(1):160–172. doi: 10.1006/dbio.1994.1188. [DOI] [PubMed] [Google Scholar]
  15. Cismowski M. J., Laff G. M., Solomon M. J., Reed S. I. KIN28 encodes a C-terminal domain kinase that controls mRNA transcription in Saccharomyces cerevisiae but lacks cyclin-dependent kinase-activating kinase (CAK) activity. Mol Cell Biol. 1995 Jun;15(6):2983–2992. doi: 10.1128/mcb.15.6.2983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Clarke H. J., Oblin C., Bustin M. Developmental regulation of chromatin composition during mouse embryogenesis: somatic histone H1 is first detectable at the 4-cell stage. Development. 1992 Jul;115(3):791–799. doi: 10.1242/dev.115.3.791. [DOI] [PubMed] [Google Scholar]
  17. Conover J. C., Temeles G. L., Zimmermann J. W., Burke B., Schultz R. M. Stage-specific expression of a family of proteins that are major products of zygotic gene activation in the mouse embryo. Dev Biol. 1991 Apr;144(2):392–404. doi: 10.1016/0012-1606(91)90431-2. [DOI] [PubMed] [Google Scholar]
  18. Cotton R. W., Manes C., Hamkalo B. A. Electron microscopic analysis of RNA transcription in preimplantation rabbit embryos. Chromosoma. 1980;79(2):169–178. doi: 10.1007/BF01175183. [DOI] [PubMed] [Google Scholar]
  19. Dahmus M. E. Phosphorylation of the C-terminal domain of RNA polymerase II. Biochim Biophys Acta. 1995 Apr 4;1261(2):171–182. doi: 10.1016/0167-4781(94)00233-s. [DOI] [PubMed] [Google Scholar]
  20. Dahmus M. E. Reversible phosphorylation of the C-terminal domain of RNA polymerase II. J Biol Chem. 1996 Aug 9;271(32):19009–19012. doi: 10.1074/jbc.271.32.19009. [DOI] [PubMed] [Google Scholar]
  21. Davis W., Jr, De Sousa P. A., Schultz R. M. Transient expression of translation initiation factor eIF-4C during the 2-cell stage of the preimplantation mouse embryo: identification by mRNA differential display and the role of DNA replication in zygotic gene activation. Dev Biol. 1996 Mar 15;174(2):190–201. doi: 10.1006/dbio.1996.0065. [DOI] [PubMed] [Google Scholar]
  22. Debey P., Renard J. P., Coppey-Moisan M., Monnot I., Geze M. Dynamics of chromatin changes in live one-cell mouse embryos: a continuous follow-up by fluorescence microscopy. Exp Cell Res. 1989 Aug;183(2):413–433. doi: 10.1016/0014-4827(89)90401-1. [DOI] [PubMed] [Google Scholar]
  23. Delouis C., Bonnerot C., Vernet M., Nicolas J. F. Expression of microinjected DNA and RNA in early rabbit embryos: changes in permissiveness for expression and transcriptional selectivity. Exp Cell Res. 1992 Aug;201(2):284–291. doi: 10.1016/0014-4827(92)90275-d. [DOI] [PubMed] [Google Scholar]
  24. Du L., Warren S. L. A functional interaction between the carboxy-terminal domain of RNA polymerase II and pre-mRNA splicing. J Cell Biol. 1997 Jan 13;136(1):5–18. doi: 10.1083/jcb.136.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Dubois M. F., Bellier S., Seo S. J., Bensaude O. Phosphorylation of the RNA polymerase II largest subunit during heat shock and inhibition of transcription in HeLa cells. J Cell Physiol. 1994 Mar;158(3):417–426. doi: 10.1002/jcp.1041580305. [DOI] [PubMed] [Google Scholar]
  26. Dubois M. F., Nguyen V. T., Bellier S., Bensaude O. Inhibitors of transcription such as 5,6-dichloro-1-beta-D-ribofuranosylbenzimidazole and isoquinoline sulfonamide derivatives (H-8 and H-7) promote dephosphorylation of the carboxyl-terminal domain of RNA polymerase II largest subunit. J Biol Chem. 1994 May 6;269(18):13331–13336. [PubMed] [Google Scholar]
  27. Dubois M. F., Nguyen V. T., Dahmus M. E., Pagès G., Pouysségur J., Bensaude O. Enhanced phosphorylation of the C-terminal domain of RNA polymerase II upon serum stimulation of quiescent cells: possible involvement of MAP kinases. EMBO J. 1994 Oct 17;13(20):4787–4797. doi: 10.1002/j.1460-2075.1994.tb06804.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Dubois M. F., Vincent M., Vigneron M., Adamczewski J., Egly J. M., Bensaude O. Heat-shock inactivation of the TFIIH-associated kinase and change in the phosphorylation sites on the C-terminal domain of RNA polymerase II. Nucleic Acids Res. 1997 Feb 15;25(4):694–700. doi: 10.1093/nar/25.4.694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Emili A., Ingles C. J. The RNA polymerase II carboxy-terminal domain: links to a bigger and better 'holoenzyme'? Curr Opin Genet Dev. 1995 Apr;5(2):204–209. doi: 10.1016/0959-437x(95)80009-3. [DOI] [PubMed] [Google Scholar]
  30. Flach G., Johnson M. H., Braude P. R., Taylor R. A., Bolton V. N. The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J. 1982;1(6):681–686. doi: 10.1002/j.1460-2075.1982.tb01230.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Gerber H. P., Hagmann M., Seipel K., Georgiev O., West M. A., Litingtung Y., Schaffner W., Corden J. L. RNA polymerase II C-terminal domain required for enhancer-driven transcription. Nature. 1995 Apr 13;374(6523):660–662. doi: 10.1038/374660a0. [DOI] [PubMed] [Google Scholar]
  32. Greenleaf A. L. A positive addition to a negative tail's tale. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):10896–10897. doi: 10.1073/pnas.90.23.10896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Henery C. C., Miranda M., Wiekowski M., Wilmut I., DePamphilis M. L. Repression of gene expression at the beginning of mouse development. Dev Biol. 1995 Jun;169(2):448–460. doi: 10.1006/dbio.1995.1160. [DOI] [PubMed] [Google Scholar]
  34. Herrmann C. H., Gold M. O., Rice A. P. Viral transactivators specifically target distinct cellular protein kinases that phosphorylate the RNA polymerase II C-terminal domain. Nucleic Acids Res. 1996 Feb 1;24(3):501–508. doi: 10.1093/nar/24.3.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Hoeijmakers J. H., Egly J. M., Vermeulen W. TFIIH: a key component in multiple DNA transactions. Curr Opin Genet Dev. 1996 Feb;6(1):26–33. doi: 10.1016/s0959-437x(96)90006-4. [DOI] [PubMed] [Google Scholar]
  36. Howlett S. K., Bolton V. N. Sequence and regulation of morphological and molecular events during the first cell cycle of mouse embryogenesis. J Embryol Exp Morphol. 1985 Jun;87:175–206. [PubMed] [Google Scholar]
  37. Jackson D. A., Cook P. R. Transcription occurs at a nucleoskeleton. EMBO J. 1985 Apr;4(4):919–925. doi: 10.1002/j.1460-2075.1985.tb03719.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kalab P., Kubiak J. Z., Verlhac M. H., Colledge W. H., Maro B. Activation of p90rsk during meiotic maturation and first mitosis in mouse oocytes and eggs: MAP kinase-independent and -dependent activation. Development. 1996 Jun;122(6):1957–1964. doi: 10.1242/dev.122.6.1957. [DOI] [PubMed] [Google Scholar]
  39. Kanka J., Fléchon J. E., Sutovský P. Onset of RNA synthesis and poly (A) content of early rabbit embryos. Comparison with sheep. Reprod Nutr Dev. 1993;33(5):465–474. doi: 10.1051/rnd:19930507. [DOI] [PubMed] [Google Scholar]
  40. Kim E., Du L., Bregman D. B., Warren S. L. Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of pre-mRNA. J Cell Biol. 1997 Jan 13;136(1):19–28. doi: 10.1083/jcb.136.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Koleske A. J., Young R. A. The RNA polymerase II holoenzyme and its implications for gene regulation. Trends Biochem Sci. 1995 Mar;20(3):113–116. doi: 10.1016/s0968-0004(00)88977-x. [DOI] [PubMed] [Google Scholar]
  42. Krek W., Maridor G., Nigg E. A. Casein kinase II is a predominantly nuclear enzyme. J Cell Biol. 1992 Jan;116(1):43–55. doi: 10.1083/jcb.116.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. Latham K. E., Garrels J. I., Chang C., Solter D. Quantitative analysis of protein synthesis in mouse embryos. I. Extensive reprogramming at the one- and two-cell stages. Development. 1991 Aug;112(4):921–932. doi: 10.1242/dev.112.4.921. [DOI] [PubMed] [Google Scholar]
  45. Latham K. E., Rambhatla L., Hayashizaki Y., Chapman V. M. Stage-specific induction and regulation by genomic imprinting of the mouse U2afbp-rs gene during preimplantation development. Dev Biol. 1995 Apr;168(2):670–676. doi: 10.1006/dbio.1995.1111. [DOI] [PubMed] [Google Scholar]
  46. Latham K. E., Solter D., Schultz R. M. Acquisition of a transcriptionally permissive state during the 1-cell stage of mouse embryogenesis. Dev Biol. 1992 Feb;149(2):457–462. doi: 10.1016/0012-1606(92)90300-6. [DOI] [PubMed] [Google Scholar]
  47. Linial M., Gunderson N., Groudine M. Enhanced transcription of c-myc in bursal lymphoma cells requires continuous protein synthesis. Science. 1985 Dec 6;230(4730):1126–1132. doi: 10.1126/science.2999973. [DOI] [PubMed] [Google Scholar]
  48. Majumder S., DePamphilis M. L. A unique role for enhancers is revealed during early mouse development. Bioessays. 1995 Oct;17(10):879–889. doi: 10.1002/bies.950171010. [DOI] [PubMed] [Google Scholar]
  49. Manes C. Nucleic acid synthesis in preimplantation rabbit embryos. III. A "dark period" immediately following fertilization, and the early predominance low molecular weight RNA synthesis. J Exp Zool. 1977 Aug;201(2):247–257. doi: 10.1002/jez.1402010209. [DOI] [PubMed] [Google Scholar]
  50. Marshall N. F., Peng J., Xie Z., Price D. H. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J Biol Chem. 1996 Oct 25;271(43):27176–27183. doi: 10.1074/jbc.271.43.27176. [DOI] [PubMed] [Google Scholar]
  51. Matsumoto K., Anzai M., Nakagata N., Takahashi A., Takahashi Y., Miyata K. Onset of paternal gene activation in early mouse embryos fertilized with transgenic mouse sperm. Mol Reprod Dev. 1994 Oct;39(2):136–140. doi: 10.1002/mrd.1080390203. [DOI] [PubMed] [Google Scholar]
  52. Maxon M. E., Goodrich J. A., Tjian R. Transcription factor IIE binds preferentially to RNA polymerase IIa and recruits TFIIH: a model for promoter clearance. Genes Dev. 1994 Mar 1;8(5):515–524. doi: 10.1101/gad.8.5.515. [DOI] [PubMed] [Google Scholar]
  53. 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]
  54. Michels A. A., Nguyen V. T., Konings A. W., Kampinga H. H., Bensaude O. Thermostability of a nuclear-targeted luciferase expressed in mammalian cells. Destabilizing influence of the intranuclear microenvironment. Eur J Biochem. 1995 Dec 1;234(2):382–389. doi: 10.1111/j.1432-1033.1995.382_b.x. [DOI] [PubMed] [Google Scholar]
  55. Moos J., Xu Z., Schultz R. M., Kopf G. S. Regulation of nuclear envelope assembly/disassembly by MAP kinase. Dev Biol. 1996 May 1;175(2):358–361. doi: 10.1006/dbio.1996.0121. [DOI] [PubMed] [Google Scholar]
  56. Mortillaro M. J., Blencowe B. J., Wei X., Nakayasu H., Du L., Warren S. L., Sharp P. A., Berezney R. A hyperphosphorylated form of the large subunit of RNA polymerase II is associated with splicing complexes and the nuclear matrix. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8253–8257. doi: 10.1073/pnas.93.16.8253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Nguyen V. T., Giannoni F., Dubois M. F., Seo S. J., Vigneron M., Kédinger C., Bensaude O. In vivo degradation of RNA polymerase II largest subunit triggered by alpha-amanitin. Nucleic Acids Res. 1996 Aug 1;24(15):2924–2929. doi: 10.1093/nar/24.15.2924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Nothias J. Y., Majumder S., Kaneko K. J., DePamphilis M. L. Regulation of gene expression at the beginning of mammalian development. J Biol Chem. 1995 Sep 22;270(38):22077–22080. doi: 10.1074/jbc.270.38.22077. [DOI] [PubMed] [Google Scholar]
  59. Nothias J. Y., Miranda M., DePamphilis M. L. Uncoupling of transcription and translation during zygotic gene activation in the mouse. EMBO J. 1996 Oct 15;15(20):5715–5725. [PMC free article] [PubMed] [Google Scholar]
  60. Patterton D., Wolffe A. P. Developmental roles for chromatin and chromosomal structure. Dev Biol. 1996 Jan 10;173(1):2–13. doi: 10.1006/dbio.1996.0002. [DOI] [PubMed] [Google Scholar]
  61. Prather R. S., Schatten G. Construction of the nuclear matrix at the transition from maternal to zygotic control of development in the mouse: an immunocytochemical study. Mol Reprod Dev. 1992 Jul;32(3):203–208. doi: 10.1002/mrd.1080320304. [DOI] [PubMed] [Google Scholar]
  62. Prioleau M. N., Buckle R. S., Méchali M. Programming of a repressed but committed chromatin structure during early development. EMBO J. 1995 Oct 16;14(20):5073–5084. doi: 10.1002/j.1460-2075.1995.tb00189.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Ram P. T., Schultz R. M. Reporter gene expression in G2 of the 1-cell mouse embryo. Dev Biol. 1993 Apr;156(2):552–556. doi: 10.1006/dbio.1993.1101. [DOI] [PubMed] [Google Scholar]
  64. Rangel L. M., Fernandez-Tomas C., Dahmus M. E., Gariglio P. Modification of RNA polymerase IIO subspecies after poliovirus infection. J Virol. 1987 Apr;61(4):1002–1006. doi: 10.1128/jvi.61.4.1002-1006.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Razin S. V., Yarovaya O. V., Georgiev G. P. Low ionic strength extraction of nuclease-treated nuclei destroys the attachment of transcriptionally active DNA to the nuclear skeleton. Nucleic Acids Res. 1985 Oct 25;13(20):7427–7444. doi: 10.1093/nar/13.20.7427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Rice S. A., Long M. C., Lam V., Spencer C. A. RNA polymerase II is aberrantly phosphorylated and localized to viral replication compartments following herpes simplex virus infection. J Virol. 1994 Feb;68(2):988–1001. doi: 10.1128/jvi.68.2.988-1001.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Roeder R. G. Multiple forms of deoxyribonucleic acid-dependent ribonucleic acid polymerase in Xenopus laevis. Levels of activity during oocyte and embryonic development. J Biol Chem. 1974 Jan 10;249(1):249–256. [PubMed] [Google Scholar]
  68. 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]
  69. Schultz R. M. Regulation of zygotic gene activation in the mouse. Bioessays. 1993 Aug;15(8):531–538. doi: 10.1002/bies.950150806. [DOI] [PubMed] [Google Scholar]
  70. Seydoux G., Dunn M. A. Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster. Development. 1997 Jun;124(11):2191–2201. doi: 10.1242/dev.124.11.2191. [DOI] [PubMed] [Google Scholar]
  71. Shpakovski G. V., Acker J., Wintzerith M., Lacroix J. F., Thuriaux P., Vigneron M. Four subunits that are shared by the three classes of RNA polymerase are functionally interchangeable between Homo sapiens and Saccharomyces cerevisiae. Mol Cell Biol. 1995 Sep;15(9):4702–4710. doi: 10.1128/mcb.15.9.4702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Svejstrup J. Q., Vichi P., Egly J. M. The multiple roles of transcription/repair factor TFIIH. Trends Biochem Sci. 1996 Sep;21(9):346–350. [PubMed] [Google Scholar]
  73. Taylor K. D., Pikó L. Patterns of mRNA prevalence and expression of B1 and B2 transcripts in early mouse embryos. Development. 1987 Dec;101(4):877–892. doi: 10.1242/dev.101.4.877. [DOI] [PubMed] [Google Scholar]
  74. Telford N. A., Watson A. J., Schultz G. A. Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev. 1990 May;26(1):90–100. doi: 10.1002/mrd.1080260113. [DOI] [PubMed] [Google Scholar]
  75. Temeles G. L., Ram P. T., Rothstein J. L., Schultz R. M. Expression patterns of novel genes during mouse preimplantation embryogenesis. Mol Reprod Dev. 1994 Feb;37(2):121–129. doi: 10.1002/mrd.1080370202. [DOI] [PubMed] [Google Scholar]
  76. Thompson E. M., Legouy E., Christians E., Renard J. P. Progressive maturation of chromatin structure regulates HSP70.1 gene expression in the preimplantation mouse embryo. Development. 1995 Oct;121(10):3425–3437. doi: 10.1242/dev.121.10.3425. [DOI] [PubMed] [Google Scholar]
  77. 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]
  78. Toyoda T., Wolffe A. P. Characterization of RNA polymerase II-dependent transcription in Xenopus extracts. Dev Biol. 1992 Sep;153(1):150–157. doi: 10.1016/0012-1606(92)90099-3. [DOI] [PubMed] [Google Scholar]
  79. 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]
  80. Valay J. G., Dubois M. F., Bensaude O., Faye G. Ccl1, a cyclin associated with protein kinase Kin28, controls the phosphorylation of RNA polymerase II largest subunit and mRNA transcription. C R Acad Sci III. 1996 Mar;319(3):183–189. [PubMed] [Google Scholar]
  81. Valay J. G., Simon M., Dubois M. F., Bensaude O., Facca C., Faye G. The KIN28 gene is required both for RNA polymerase II mediated transcription and phosphorylation of the Rpb1p CTD. J Mol Biol. 1995 Jun 9;249(3):535–544. doi: 10.1006/jmbi.1995.0316. [DOI] [PubMed] [Google Scholar]
  82. Vautier D., Besombes D., Chassoux D., Aubry F., Debey P. Redistribution of nuclear antigens linked to cell proliferation and RNA processing in mouse oocytes and early embryos. Mol Reprod Dev. 1994 Jun;38(2):119–130. doi: 10.1002/mrd.1080380202. [DOI] [PubMed] [Google Scholar]
  83. Venetianer A., Dubois M. F., Nguyen V. T., Bellier S., Seo S. J., Bensaude O. Phosphorylation state of the RNA polymerase II C-terminal domain (CTD) in heat-shocked cells. Possible involvement of the stress-activated mitogen-activated protein (MAP) kinases. Eur J Biochem. 1995 Oct 1;233(1):83–92. doi: 10.1111/j.1432-1033.1995.083_1.x. [DOI] [PubMed] [Google Scholar]
  84. Vincent M., Lauriault P., Dubois M. F., Lavoie S., Bensaude O., Chabot B. The nuclear matrix protein p255 is a highly phosphorylated form of RNA polymerase II largest subunit which associates with spliceosomes. Nucleic Acids Res. 1996 Dec 1;24(23):4649–4652. doi: 10.1093/nar/24.23.4649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Warren S. L., Landolfi A. S., Curtis C., Morrow J. S. Cytostellin: a novel, highly conserved protein that undergoes continuous redistribution during the cell cycle. J Cell Sci. 1992 Oct;103(Pt 2):381–388. doi: 10.1242/jcs.103.2.381. [DOI] [PubMed] [Google Scholar]
  86. Worrad D. M., Ram P. T., Schultz R. M. Regulation of gene expression in the mouse oocyte and early preimplantation embryo: developmental changes in Sp1 and TATA box-binding protein, TBP. Development. 1994 Aug;120(8):2347–2357. doi: 10.1242/dev.120.8.2347. [DOI] [PubMed] [Google Scholar]
  87. Worrad D. M., Turner B. M., Schultz R. M. Temporally restricted spatial localization of acetylated isoforms of histone H4 and RNA polymerase II in the 2-cell mouse embryo. Development. 1995 Sep;121(9):2949–2959. doi: 10.1242/dev.121.9.2949. [DOI] [PubMed] [Google Scholar]
  88. Yankulov K., Yamashita K., Roy R., Egly J. M., Bentley D. L. The transcriptional elongation inhibitor 5,6-dichloro-1-beta-D-ribofuranosylbenzimidazole inhibits transcription factor IIH-associated protein kinase. J Biol Chem. 1995 Oct 13;270(41):23922–23925. doi: 10.1074/jbc.270.41.23922. [DOI] [PubMed] [Google Scholar]
  89. Yasuda G. K., Schubiger G. Temporal regulation in the early embryo: is MBT too good to be true? Trends Genet. 1992 Apr;8(4):124–127. doi: 10.1016/0168-9525(92)90369-F. [DOI] [PubMed] [Google Scholar]
  90. 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]
  91. Yuryev A., Patturajan M., Litingtung Y., Joshi R. V., Gentile C., Gebara M., Corden J. L. The C-terminal domain of the largest subunit of RNA polymerase II interacts with a novel set of serine/arginine-rich proteins. Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):6975–6980. doi: 10.1073/pnas.93.14.6975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Zeng C., Kim E., Warren S. L., Berget S. M. Dynamic relocation of transcription and splicing factors dependent upon transcriptional activity. EMBO J. 1997 Mar 17;16(6):1401–1412. doi: 10.1093/emboj/16.6.1401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. van Blerkom J., Brockway G. O. Qualitative patterns of protein synthesis in the preimplantation mouse embryo. I. Normal pregnancy. Dev Biol. 1975 May;44(1):148–157. doi: 10.1016/0012-1606(75)90382-6. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES