Reproductive and Developmental Biology

The Korean Society of Animal Reproduction (한국동물번식학회)
권호 표지
DOI QR코드

DOI QR Code

General Transcription Factors and Embryonic Genome Activation

  • Oqani, Reza K. (Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University) ;
  • Kang, Jung Won (Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University) ;
  • Lin, Tao (Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University) ;
  • Lee, Jae Eun (Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University) ;
  • Jin, Dong-Il (Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University)
  • Received : 2014.03.17
  • Accepted : 2014.03.24
  • Published : 2014.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Embryonic genome activation (EGA) is a highly complex phenomenon that is controlled at various levels. New studies have ascertained some molecular mechanisms that control EGA in several species; it is apparent that these same mechanisms regulate EGA in all species. Protein phosphorylation, DNA methylation and histone modification regulate transcriptional activities, and mechanisms such as ubiquitination, SUMOylation and microRNAs post-transcriptionally regulate development. Each of these regulations is highly dynamic in the early embryo. A better understanding of these regulatory strategies can provide the possibility to improve the reproductive properties in mammals such as pigs, to develop methods of generating high-quality embryos in vitro, and to find markers for selecting developmentally competent embryos.

Keywords

References

  1. Aguilar-Fuentes J, Valadez-Graham V, Reynaud E, and Zurita M (2006): TFIIH trafficking and its nuclear assembly during early Drosophila embryo development. J Cell Sci 119: 3866-3875. https://doi.org/10.1242/jcs.03150
  2. Ahn SH, Kim M, Buratowski S (2004): Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3' end processing. Mol Cell 13:67-76. https://doi.org/10.1016/S1097-2765(03)00492-1
  3. Aoki E, Schultz RM (1999): DNA replication in the 1-cell mouse embryo: stimulatory effect of histone acetylation. Zygote 7:165-172. https://doi.org/10.1017/S0967199499000532
  4. Aoki F, Worrad DM, Schultz RM (1997): Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev Biol 181:296-307. https://doi.org/10.1006/dbio.1996.8466
  5. Aoki F, Worrad DM, Schultz RM (1997): Regulationof transcriptional activity during the first and second cell cyclesin the pre implantation mouse embryo. Dev Biol 181: 296-307. https://doi.org/10.1006/dbio.1996.8466
  6. Bacharova R (1985): Gene expression during oogenesis and oocyte development in mammals. Dev Biol 1:453-524.
  7. Bashirullah A, Halsell SR, Cooperstock RL, Kloc M, Karaiskakis A, Fisher WW, Fu W, Hamilton JK, Etkin LD, Lipshitz HD (1999): Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO J 18:2610-2620. https://doi.org/10.1093/emboj/18.9.2610
  8. Bellier S, Chastant S, Adenot P, Vincent M, Renard JP, Bensaude O (1997a): Nuclear translocation and carboxyl-terminal domain phosphorylation of RNA polymerase II delineate the two phases of zygotic gene activation in mammalian embryos. EMBO J 16:6250-6262. https://doi.org/10.1093/emboj/16.20.6250
  9. Bellier S, Dubois MF, Nishida E, Almouzni G, Bensaude O (1997b): Phosphorylation of the RNA polymerase II largest subunit during Xenopus laevis oocyte maturation. Mol Cell Biol 17:1434-1440. https://doi.org/10.1128/MCB.17.3.1434
  10. Bensaude O (2011): Inhibiting eukaryotic transcription: Which compound to choose? How to evaluate its activity? Transcription 2:103-108. https://doi.org/10.4161/trns.2.3.16172
  11. Biggiogera M, Fakan S, Kaufmann SH, Black A, Shaper JH, Busch H (1989): Simultaneous immunoelectron microscopic visualization of protein B23 and C23 distribution in the HeLa cell nucleolus. J Histochem Cytochem 37:1371-1374. https://doi.org/10.1177/37.9.2768807
  12. Bjerregaard B, Wrenzycki C, Philimonenko VV, Hozak P, Laurincik J, Niemann H, Motlik J, Maddox- Hyttel P (2004): Regulation of ribosomal RNA synthesis during the final phases of porcine oocyte growth. Biol Reprod 70:925-935.
  13. Bloom AM, Mukherjee BB (1972): RNA synthesis in maturing mouse oocytes. Exp Cell Res 74:577-582. https://doi.org/10.1016/0014-4827(72)90421-1
  14. Boisvert FM, Hendzel MJ, Bazett-Jones D (2000 Promyelocytic leukemia (PML) nuclear bodies are protein structures that do not accumulate RNA. J Cell Biol 148:283-292. https://doi.org/10.1083/jcb.148.2.283
  15. Boisvert FM, van Koningsbruggen S, Navascués J, Lamond AI (2007): The multifunctional nucleolus. Nat Rev Mol Cell Biol 8:574-585. https://doi.org/10.1038/nrm2184
  16. Bouniol C, Nguyen E, Debey P. 1995 Endogenous transcription occurs at the 1-cell stage in the mouse embryo. Exp Cell Res 218:57-62. https://doi.org/10.1006/excr.1995.1130
  17. Bouniol-Baly C, Hamraoui L, Guibert J, Beaujean N, Szöllösi MS, Debey P (1999): Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes. Biol Reprod 60:580-587. https://doi.org/10.1095/biolreprod60.3.580
  18. Bregman DB, L Du, S van der Zee, Warren SL (1995): Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J Cell Biol 129:287-298. https://doi.org/10.1083/jcb.129.2.287
  19. Bres V, Yoh SM, Jones KA (2008): The multi-tasking P-TEFb complex. Curr Opin Cell Biol 20:334-340. https://doi.org/10.1016/j.ceb.2008.04.008
  20. Buratowski S, Hahn S, Guarente L, Sharp PA (1989): Five intermediate complexes in transcription initiation by RNA polymerase II. Cell 56, 549-561. https://doi.org/10.1016/0092-8674(89)90578-3
  21. Byers SA, Price JP, Cooper JJ, Li Q, Price DH (2005): HEXIM2, a HEXIM1-related protein, regulates positive transcription elongation factor b through association with 7SK. J Biol Chem 280:16360-16367. https://doi.org/10.1074/jbc.M500424200
  22. Chambers RS, Dahmus ME (1994 Purification and characterization of a phosphatase from HeLa cells which dephosphorylates the C-terminal domain of RNA polymerase II. J Biol Chem 269:26243-26248.
  23. Chao SH, Price DH (2001 Flavopiridol inactivates P-TEFb and blocks most RNA polymerase II transcription in vivo. J Biol Chem 276:31793-31799. https://doi.org/10.1074/jbc.M102306200
  24. Chao SH, Fujinaga K, Marion JE, Taube R, Sausville EA, Senderowicz AM, Peterlin BM, Price DH (2000 Flavopiridol inhibits P-TEFb and blocks HIV- 1 replication. J Biol Chem 275:28345-28348. https://doi.org/10.1074/jbc.C000446200
  25. Chapman RD, Heidemann M, Hintermair C, Eick D (2008): Molecular evolution of the RNA polymerase II CTD. Trends Genet 24:289-296. https://doi.org/10.1016/j.tig.2008.03.010
  26. Cmarko D, Verschure PJ, Rothblum LI, Hernandez- Verdun D, Amalric F, van Driel R, Fakan S (2000): Ultrastructural analysis of nucleolar transcription in cells microinjected with 5-bromo-UTP. Histochem Cell Biol 113:181-187. https://doi.org/10.1007/s004180050437
  27. Crozet N, Motlik J, Szöllösi D. 1981 Nucleolar fine structure and RNA synthesis in porcine oocytes during the early stages of antrum formation. Biol Cell 41:35-42.
  28. De La Fuente R, Viveiros MM, Burns KH, Adashi EY, Matzuk MM, Eppig JJ (2004): Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function. Dev Biol 275:447-458. https://doi.org/10.1016/j.ydbio.2004.08.028
  29. De Renzis S, Elemento O, Tavazoie S, Wieschaus EF (2007): Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol 5(5):e117. https://doi.org/10.1371/journal.pbio.0050117
  30. Debey P, Szöllösi MS, Szöllösi D, Vautier D, Girousse A, Besombes D (1993): Competent mouse oocytes isolated from antral follicles exhibit different chromatin organization and follow different maturation dynamics. Mol Reprod Dev 36:59-74. https://doi.org/10.1002/mrd.1080360110
  31. Dey A, Nishiyama A, Karpova T, McNally J, Ozato K (2009): Brd4 marks select genes on mitotic chromatin and directs postmitotic transcription. Mol Biol Cell 20:4899-4909. https://doi.org/10.1091/mbc.E09-05-0380
  32. Drygin D, Rice WG, Grummt I (2010): The RNA polymerase I transcription machinery: an emerging target for the treatment of cancer. Annu Rev Pharmacol Toxicol 50:131-156. https://doi.org/10.1146/annurev.pharmtox.010909.105844
  33. Dundr M, Raska I (1993): Nonisotopic ultrastructural mapping of transcription sites within the nucleolus. Exp Cell Res 208:275-281. https://doi.org/10.1006/excr.1993.1247
  34. Eissenberg JC, Shilatifard A, Dorokhov N, Michener DE (2007): Cdk9 is an essential kinase in Drosophila that is required for heat shock gene expression, histone methylation and elongation factor recruitment. Mol Genet Genomics 277:101-114. https://doi.org/10.1007/s00438-006-0164-2
  35. Evsikov AV, Graber JH, Brockman JM, Hampl A, Holbrook AE, Singh P, Eppig JJ, Solter D, Knowles BB (2006): Cracking the egg: molecular dynamics and evolutionary aspects of the transition from the fully grown oocyte to embryo. Genes Dev 20:2713-2727. https://doi.org/10.1101/gad.1471006
  36. Fair T, Hyttel P, Greve T (1995): Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol Reprod Dev 42:437-442. https://doi.org/10.1002/mrd.1080420410
  37. Fong YW, Zhou Q (2000): Relief of two built-in autoinhibitory mechanisms in P-TEFb is required for assembly of a multicomponent transcription elongation complex at the human immunodeficiency virus type 1 promoter. Mol Cell Biol 20:5897-5907. https://doi.org/10.1128/MCB.20.16.5897-5907.2000
  38. Forlani S, Bonnerot C, Capgras S, Nicolas JF (1998): Relief of a repressed gene expression state in the mouse 1-cell embryo requires DNA replication. Development 125:3153-3166.
  39. Fraschini A, Bottone MG, Scovassi AI, Denegri M, Risueno MC, Testillano PS, Martin TE, Biggiogera M, Pellicciari C (2005): Changes in extranucleolar transcription during actinomycin D-induced apoptosis. Histol Histopathol 20:107-117.
  40. Fu TJ, Peng J, Lee G, Price DH, Flores O (1999): Cyclin K functions as a CDK9 regulatory subunit and participates in RNA polymerase II transcription. J Biol Chem 274:34527-34530. https://doi.org/10.1074/jbc.274.49.34527
  41. Ganuza M, Saiz-Ladera C, Canamero M, Gomez G, Schneider R, Blasco MA, Pisano D, Paramio JM, Santamaria D, Barbacid M (2012): Genetic inactivation of Cdk7 leads to cell cycle arrest and induces premature aging due to adult stem cell exhaustion. EMBO J 31:2498-2510. https://doi.org/10.1038/emboj.2012.94
  42. Garber ME, Mayall TP, Suess EM, Meisenhelder J, Thompson NE, Jones KA (2000): CDK9 autophosphorylation regulates high-affinity binding of the human immunodeficiency virus type 1 tat-P-TEFb complex to TAR RNA. Mol Cell Biol 20:6958-6969. https://doi.org/10.1128/MCB.20.18.6958-6969.2000
  43. Ghazy MA, Brodie SA, Ammerman ML, Ziegler L M, Ponticelli AS (2004): Aminoacid substitutions in yeast TFIIF confer upstream shifts in transcription initiation and altered interactions with RNA polymerase II. Mol Cell Biol 24:10975-10985. https://doi.org/10.1128/MCB.24.24.10975-10985.2004
  44. Ginisty H, Amalric F, Bouvet P (1998): Nucleolin functions in the first step of ribosomal RNA processing. EMBO J 17:1476-1486. https://doi.org/10.1093/emboj/17.5.1476
  45. Goodrich JA, Tijian R (1994): Transcription factors IIE and IIH and ATP hydrolysis direct promoter clearance by RNA polymerase II. Cell 77:145-156. https://doi.org/10.1016/0092-8674(94)90242-9
  46. Guthrie HD, Garrett WM (2000): Changes in porcine oocyte germinal vesicle development as follicles approach preovulatory maturity. Theriogenology 54:389-399. https://doi.org/10.1016/S0093-691X(00)00356-3
  47. Hahn S (2004): Structure and mechanism of the RNA polymerase II transcription machinery. Nat Struct Mol Biol 11:394-403. https://doi.org/10.1038/nsmb763
  48. Hamatani T, Carter MG, Sharov AA, Ko MS (2004): Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 6:117-131. https://doi.org/10.1016/S1534-5807(03)00373-3
  49. Hamatani T, Ko MSh, Yamada M, Kuji N, Mizusawa Y, Shoji M, Hada T, Asada H, Maruyama T, Yoshimura Y (2006): Global gene expression profiling of preimplantation embryos. Hum Cell 193: 98-117.
  50. Hiller MA, Lin TY, Wood C, Fuller MT (2001): Developmental regulation of transcription by tissuespecific TAF homolog. Genes Dev 15: 1021-1030. https://doi.org/10.1101/gad.869101
  51. Hozák P, Cook PR, Schöfer C, Mosgöller W, Wachtler F (1994): Site of transcription of ribosomal RNA and intranucleolar structure in HeLa cells. J Cell Sci 107:639-648.
  52. Iborra FJ, Pombo A, Jackson DA, Cook PR (1996): Active RNA polymerases are localized within discrete transcription "factories' in human nuclei. J Cell Sci 109:1427-1436.
  53. Inoue K, Ogonuki N, Miki M, Noda S, Kim JM, Aoki F, Miyoshi H, Ogura A (2006): Inefficient reprogramming of the hematopoietic stem cell genome following nuclear transfer. J Cell Sci 119:1985-1991. https://doi.org/10.1242/jcs.02913
  54. Jackson DA, Hassan AB, Errington RJ, Cook PR (1993): Visualization of focal sites of transcription within human nuclei. EMBO J 12:1059-1065.
  55. Jao CY, Salic A (2008): Exploring RNA transcription and turnover in vivo by using click chemistry. Proc Natl Acad Sci USA 105:15779-15784. https://doi.org/10.1073/pnas.0808480105
  56. Kedinger C, Nuret P, Chambon P (1971): Structural evidence for two alpha-amanitin sensitive RNA polymerases in calf thymus. FEBS Lett 15:169-174. https://doi.org/10.1016/0014-5793(71)80305-8
  57. Kelland LR (2000): Flavopiridol, the first cyclin-dependent kinase inhibitor to enter the clinic: current status. Expert Opin Investig Drugs 9:2903-2911. https://doi.org/10.1517/13543784.9.12.2903
  58. Kelly WG, Dahmus ME, Hart GW (1993): RNA polymerase II is a glycoprotein. Modification of the COOH-terminal domain by O-GlcNAc. J Biol Chem 268:10416-10424.
  59. Kopecny V, Landa V, Pavlok A (1995): Localization of nucleic acids in the nucleoli of oocytes and early embryos of mouse and hamster: an autoradiographic study. Mol Reprod Dev 41:449-458. https://doi.org/10.1002/mrd.1080410407
  60. Kuhn CD, Geiger SR, Baumli S, Gartmann M, Gerber J, Jennebach S, Mielke T, Tschochner H, Beckmann R, Cramer P (2007): Functional architecture of RNA polymerase I. Cell 131:1260-1272. https://doi.org/10.1016/j.cell.2007.10.051
  61. Lanclos KD, Hamilton TH (1975): Translation ofhormone- induced messenger RNA in amphibian oocytes. I.Induction by estrogen of messenger RNA encoded forvitellogenic protein in the liver of the male African clawedtoad (Xenopus laevis). Proc Natl Acad Sci USA 72: 3934-3938. https://doi.org/10.1073/pnas.72.10.3934
  62. Larochelle S, Chen J, Knights R, Pandur J, Morcillo P, Erdiument-Bromage H, Tempst P, Suter B, Fisher RP (2001): T-loop phosphorylation stabilizes the CDK7-cyclin HMAT1 complex in vivo and regulates its CTD kinase activity. EMBO J 20:3749-3759. https://doi.org/10.1093/emboj/20.14.3749
  63. Leclerc V, Raisin S, Leopold P (2000): Dominantnegative mutants reveal a role for the Cdk7 kinase at the mid-blastula transition in Drosophila embryos. EMBO J 19:1567-1575. https://doi.org/10.1093/emboj/19.7.1567
  64. Liu P, Greenleaf AL, Stiller JW (2008): The essential sequence elements required for RNAP II carboxylterminal domain function in yeast and their evolutionary conservation. Mol Biol Evol 25:719-727. https://doi.org/10.1093/molbev/msn017
  65. Liu P, Kenney JM, Stiller JW, Greenleaf AL (2010): Genetic organization, length conservation, and evolution of RNA polymerase II carboxyl-terminal domain. Mol Biol Evol 27:2628-2641. https://doi.org/10.1093/molbev/msq151
  66. Maller JL, Gross SD, Schwab MS, Finkielstein CV, Taieb FE, Oian YW (2001): Cell cycle transitions in early Xenopus development. Novartis Found Symp 237:58-73.
  67. Maxon ME, Goodrich JA, Tjian R (1994): Transcription factor IIE binds preferentially to RNA polymerase IIa and recruits TFIIH: a model for promoter clearance. Genes Dev 8:515-524. https://doi.org/10.1101/gad.8.5.515
  68. Mayer C, Grummt I (2006): Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene 25:6384-6391. https://doi.org/10.1038/sj.onc.1209883
  69. McStay B, Grummt I (2008): The epigenetics of r- RNA genes: from molecular to chromosome biology. Annu Rev Cell Dev Biol 24:131-157. https://doi.org/10.1146/annurev.cellbio.24.110707.175259
  70. Meininghaus M, Chapman RD, Horndasch M, Eick D (2000): Conditional expression of RNA polymerase II in mammalian cells. Deletion of the carboxyl- terminal domain of the large subunit affects early steps in transcription. J Biol Chem 275:24375-24382. https://doi.org/10.1074/jbc.M001883200
  71. Michels AA, Nguyen VT, Fraldi A, Labas V, Edwards M, Bonnet F, Lania L, Bensaude O (2003): MAQ1 and 7SK RNA interact with CDK9/cyclin T complexes in a transcription-dependent manner. Mol Cell Biol 23:4859-4869. https://doi.org/10.1128/MCB.23.14.4859-4869.2003
  72. Miyara F, Migne C, Dumont-Hassan M, Meur AL, Cohen-Bacrie P, Aubriot FX, Glissant A, Nathan C, Douard S, Stanovici A (2003): Chromatin configuration and transcriptional control in human and mouse oocytes. Mol Reprod Dev 64:458-470. https://doi.org/10.1002/mrd.10233
  73. Moore GPM, Lintern-Moore S, Peters H, Faber M (1974): RNA synthesis in the mouse oocyte. J Cell Biol 60:416-422. https://doi.org/10.1083/jcb.60.2.416
  74. Motlik J, Fulka J. 1976 Breakdown of the germinal vesicle in pig oocytes in vivo and in vitro. J Exp Zool 198:155-162. https://doi.org/10.1002/jez.1401980205
  75. Napolitano G, Licciardo P, Carbone R, Majello B, Lania L (2002): CDK9 has the intrinsic property to shuttle between nucleus and cytoplasm, and enhanced expression of cyclin T1 promotes its nuclear localization. J Cell Physiol 192:209-215. https://doi.org/10.1002/jcp.10130
  76. Napolitano G, Majello B, Lania L (2003): Catalytic activity of Cdk9 is required for nuclear co-localization of the Cdk9/cyclin T1 (P-TEFb) complex. J Cell Physiol 197:1-7. https://doi.org/10.1002/jcp.10376
  77. Nguyen VT, Giannoni F, Dubois MF, Seo SJ, Vigneron M, Kédinger C, Bensaude O (1996): In vivo degradation of RNA polymerase II largest subunit triggered by alpha-amanitin. Nucleic Acids Res 24: 2924-2929. https://doi.org/10.1093/nar/24.15.2924
  78. Nguyen VT, Kiss T, Michels AA, Bensaude O (2001): 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature 414: 322-325. https://doi.org/10.1038/35104581
  79. Ni Z, Schwartz BE, Werner J, Suarez JR, Lis JT (2004): Coordination of transcription, RNA processing, and surveillance by P-TEFb kinase on heat shock genes. Mol Cell 13:55-65. https://doi.org/10.1016/S1097-2765(03)00526-4
  80. Ochs RL (1998): Methods used to study structure and function of the nucleolus. Methods Cell Biol 53:303-321.
  81. Orphanides G, Reinberg D (2002): A unified theory of gene expression. Cell 108:439-451. https://doi.org/10.1016/S0092-8674(02)00655-4
  82. Orphanides G, Lagrange T, Reinberg D (1996): The general transcription factors of RNA polymerase II. Genes Dev 10:2657-2683. https://doi.org/10.1101/gad.10.21.2657
  83. Palancade B, Bellier S, Almounzi G, Bensaude O (2001b): Incomplete RNA polymerase II phosphorylation in Xenopus laevis early embryos J Cell Sci 114:2483-2489.
  84. Palancade B, Dubois MF, Dahmusd, Bensaude O (2001a): Transcription-independent RNA polymerase II dephosphorylation by the FCP1 carboxy-terminal domain phosphatase in Xenopus laevis early embryos. Mol Cell Biol 21:6359-6368. https://doi.org/10.1128/MCB.21.19.6359-6368.2001
  85. Peng J, Zhu Y, Milton JT, Price DH (1998): Identification of multiple cyclin subunits of human PTEFb. Genes Dev 12:755-762. https://doi.org/10.1101/gad.12.5.755
  86. Phatnani HP, Greenleaf AL (2006): Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev 20:2922-2936. https://doi.org/10.1101/gad.1477006
  87. Pirngruber J, Shchebet A, Johnsen SA (2009): Insights into the function of the human P-TEFb component CDK9 in the regulation of chromatin modifications and co-transcriptional mRNA processing. Cell Cycle 8:3636-3642. https://doi.org/10.4161/cc.8.22.9890
  88. Prasanth KV, Sacco-Bubulya PA, Prasanth SG, Spector DL (2003): Sequential entry of components of the gene expression machinery into daughter nuclei. Mol Biol Cell 14:1043-1057. https://doi.org/10.1091/mbc.E02-10-0669
  89. Prather RS, Ross JW, Isom SC, Green JA (2009): Transcriptional, post-transcriptional and epigenetic control of porcine oocyte maturation and embryogenesis. Soc Reprod Fertil 66:165-176.
  90. Price DH (2000): P-TEFb, a cyclin-dependent kinase controlling elongation by RNA polymerase II. Mol Cell Biol 20:2629-2634. https://doi.org/10.1128/MCB.20.8.2629-2634.2000
  91. Puvion-Dutilleul F, Puvion E, Bachellerie JP (1997): Early stages of pre-rRNA formation within the nucleolar ultrastructure of mouse cells studied by in situ hybridization with a 5'ETS leader probe. Chromosoma 105:496-505. https://doi.org/10.1007/BF02510486
  92. Ranish JA, Yudkosvsky N, Hahn S (1999): Intermediates in formation and activity of the RNA polymerase II preinitiation complex holoenzyme recruitment and a postrecruitment role for the TATA box and TFIIB. Genes Dev 13:49-63. https://doi.org/10.1101/gad.13.1.49
  93. Razin SV, Gavrilov AA, Pichugin A, Lipinski M, Iarovaia OV, Vassetzky YS (2011): Transcription factories in the context of the nuclear and genome organization. Nucleic Acids Res 39:9085-9092. https://doi.org/10.1093/nar/gkr683
  94. Reese JC (2003): Basal transcription factors. Curr Opin Genet Dev 13:114-118. https://doi.org/10.1016/S0959-437X(03)00013-3
  95. Rodman TC, Bachvarova R (1976): RNA synthesis in preovulatory mouse oocytes. J Cell Biol 70:251-257. https://doi.org/10.1083/jcb.70.1.251
  96. Schmerwitz UK, Sass G, Khandoga AG, Joore J, Mayer BA, Berberich N, Totzke F, Krombach F, Tiegs G, Zahler S, Vollmar AM, Fürst R (2011): Flavopiridol protects against inflammation by attenuating leukocyte-endothelial interaction via inhibition of cyclin-dependent kinase 9. Arterioscler Thromb Vasc Biol 2:280-288.
  97. Schneider DA (2012): RNA polymerase I activity is regulated at multiple steps in the transcription cycle: recent insights into factors that influence transcription elongation. Gene 493:176-184. https://doi.org/10.1016/j.gene.2011.08.006
  98. Schoenbeck RA, Peters MS, Rickords LF, Stumpf TT, Prather RS 1992 Characterization of deoxyribonucleic acid synthesis and the transition from maternal to embryonic control in the 4-cell porcine embryo. Biol Reprod 47:1118-1125. https://doi.org/10.1095/biolreprod47.6.1118
  99. Schultz RM (2002): The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum Reprod Update 8:323-331. https://doi.org/10.1093/humupd/8.4.323
  100. Senderowicz AM, Sausville EA (2000): Preclinical and clinical development of cyclin-dependent kinase modulators. J Natl Cancer Inst 92:376-387. https://doi.org/10.1093/jnci/92.5.376
  101. Serizawa H, Conaway JW, Conaway RC (1993): Phosphorylation of C-terminal domain of RNA polymerase II is not required in basal transcription. Nature 363:371-374. https://doi.org/10.1038/363371a0
  102. Seydoux G, Dunn MA (1997): Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster Development 124:2191-2201.
  103. Shilatifard A, Conoway RC, Conoway JW (2003): The RNA polymerase II elongation complex. Annu Rev Biochem 72:693-715. https://doi.org/10.1146/annurev.biochem.72.121801.161551
  104. Shim EY, Walker AK, Shi Y, Blackwell TK (2002): CDK-9/cyclin T (P-TEFb) is required in two postinitiation pathways for transcription in the C. elegans embryo. Genes Dev 16:2135-2146. https://doi.org/10.1101/gad.999002
  105. Sikorski TW, Buratowski S (2009): The basal initiation machinery: beyond the general transcription factors. Curr Opin Cell Biol 21:344-351. https://doi.org/10.1016/j.ceb.2009.03.006
  106. Sims RJ 3rd, Mandal SS, Reinberg D (2004): Recent highlights of RNA-polymerase-II-mediated transcription. Curr Opin Cell Biol 16:263-271. https://doi.org/10.1016/j.ceb.2004.04.004
  107. Solow S, Salunek M, Ryan R, Liberman PM (2001): TAF250 phosphorylates human transcription factor IIA on serine residues important for TBP binding and transcription activity. J Biol Chem 276l:15886-15892. https://doi.org/10.1074/jbc.M009385200
  108. Stiller JW, Cook MS (2004): Functional unit of the RNA polymerase II C-terminal domain lies within heptapeptide pairs. Eukaryot Cell 3:735-740. https://doi.org/10.1128/EC.3.3.735-740.2004
  109. Sun XS, Liu Y, Yue KZ, Ma SF, Tan JH (2004): Changes in germinal vesicle (GV) chromatin configurations during growth and maturation of porcine oocytes. Mol Reprod Dev 69:228-234. https://doi.org/10.1002/mrd.20123
  110. Tadros W, Goldman AL, Babak T, Menzies F, Vardy L, Orr-Weaver T, Hughes TR, Westwood JT, Smibert CA, Lipshitz H (2007): SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev Cell 12:143-154. https://doi.org/10.1016/j.devcel.2006.10.005
  111. Tan JH, Wang HL, Sun XS, Liu Y, Sui HS, Zhang J (2009): Chromatin configurations in the germinal vesicle of mammalian oocytes. Mol Hum Reprod 15:1-9. https://doi.org/10.1093/molehr/gan069
  112. Thomas MC, Chiang CM (2006) The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol 41:105-178. https://doi.org/10.1080/10409230600648736
  113. Tombácz I, Schauer T, Juhász I, Komonyi O, Boros I (2009): The RNA Pol II CTD phosphatase Fcp1 is essential for normal development in Drosophila melanogaster. Gene 446:58-67. https://doi.org/10.1016/j.gene.2009.07.012
  114. Walker AK, Boag PR, Blackwell TK (2007): Transcription reactivation steps stimulated by oocyte maturation in C. elegans. Dev Biol 304: 382-393. https://doi.org/10.1016/j.ydbio.2006.12.039
  115. Wang Z, Lindquist S (1998): Developmentally regulated nuclear transport of transcription factors in Drosophila embryos enable the heat shock response Development 125:4841-4850.
  116. Wang, QT, Piotrowska K, Ciemerych MA, Milenkovic L, Scott M, Davis RW, Zernicka-Goetz M (2004): A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev Cell 6:133-144. https://doi.org/10.1016/S1534-5807(03)00404-0
  117. Wang K, Sun F, Sheng HZ (2006): Regulated expression of TAF-1 in cell mouse embryos. Zygote 14:209-215. https://doi.org/10.1017/S0967199406003704
  118. Wansink DG, Schul W, van der Kraan I, van Steensel B, van Driel R, de Jong L (1993): Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus. J Cell Biol 122: 283-293. https://doi.org/10.1083/jcb.122.2.283
  119. Warner JR (1999): The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24:437-440. https://doi.org/10.1016/S0968-0004(99)01460-7
  120. Wassarman PM, Letourneau GE (1976): RNA synthesis in fully-grown mouse oocytes. Nature 261:73-74. https://doi.org/10.1038/261073a0
  121. Weinmann R, Raskas HJ, Roeder RG (1974): Role of DNA-dependent RNA polymerases II and III in transcription of the adenovirus genome late in productive infection. Proc Natl Acad Sci USA 71: 3426-3439. https://doi.org/10.1073/pnas.71.9.3426
  122. Werner M, Thuriaux P, Soutourina J (2009): Structure- function analysis of RNA polymerases I and III. Curr Opin Struct Biol 19:740-745. https://doi.org/10.1016/j.sbi.2009.10.005
  123. Worrad DM, Ram PT, Schultz RM (1994): Regulation of gene expressionin the mouse oocyte and early preimplantation embryo: developmental changes in Sp1 and TATA boxbinding protein, TBP. Development 120:2347-2357.
  124. Yamaguchi Y, Inukai N, Narita T, Wada T, Handa H (2002): Evidence that negative elongation factor represses transcription elongation through binding to a DRB sensitivity-inducing factor/RNA polymerase II complex and RNA. Mol Cell Biol 22: 2918-2927. https://doi.org/10.1128/MCB.22.9.2918-2927.2002
  125. Yamaguchi Y, Takagi T, Wada T, Yano K, Furuya A, Sugimoto S, Hasegawa J, Handa H (1999): NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 97:41-51. https://doi.org/10.1016/S0092-8674(00)80713-8
  126. Yang Z, He N, Zhou Q (2008): Brd4 recruits PTEFb to chromosomes at late mitosis to promote G1 gene expression and cell cycle progression. Mol Cell Biol 28:967-976. https://doi.org/10.1128/MCB.01020-07
  127. Yang Z, Zhu Q, Luo K, Zhou Q (2001): The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 414:317-322. https://doi.org/10.1038/35104575
  128. Yik JH, Chen R, Nishimura R, Jennings JL, Link AJ, Zhou Q (2003): Inhibition of P-TEFb (CDK9/ Cyclin T) kinase and RNA polymerase II transcription by the coordinated actions of HEXIM1 and 7SK snRNA. Mol Cell 12:971-982. https://doi.org/10.1016/S1097-2765(03)00388-5
  129. Zeng C, Kim E, Warren SL, Berget SM (1997): Dynamic relocation of transcription and splicing factors dependent upon transcriptional activity. EMBO J 16:1401-1412. https://doi.org/10.1093/emboj/16.6.1401
  130. Zeng F, Schultz RM (2005): RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. Dev Biol 283:40-57. https://doi.org/10.1016/j.ydbio.2005.03.038
  131. Zhou Q, Yik JH (2006): The Yin and Yang of PTEFb regulation: implications for human immunodeficiency virus gene expression and global control of cell growth and differentiation. Microbiol Mol Biol Rev 70:646-659. https://doi.org/10.1128/MMBR.00011-06
  132. Zuccotti M, Merico V, Cecconi S, Redi CA, Garagna S (2011): What does it take to make a developmentally competent mammalian egg? Hum Reprod Update 17:525-540. https://doi.org/10.1093/humupd/dmr009
  133. Zuccotti M, Piccinelli A, Rossi PG, Garagna S, Redi CA (1995): Chromatin organization during mouse oocyte growth. Mol Reprod Dev 41:479-485. https://doi.org/10.1002/mrd.1080410410
  134. Zurita M, Reynaud E, Aguilar-Fuentes J (2008): From the beginning: the basal transcription machinery and onset of transcription in the early animal embryo. Cell Mol Life Sci 65:212-227. https://doi.org/10.1007/s00018-007-7295-4
  135. Zurita M, Merino C (2003): The transcriptional complexity of the TFIIH complex. Trends Genet 19: 578-584. (Received: 17 March 2014/ Accepted: 24 March 2014) https://doi.org/10.1016/j.tig.2003.08.005