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. 1991 Dec;19(25):7251–7257. doi: 10.1093/nar/19.25.7251

Transcriptional selectivity in early mouse embryos: a qualitative study.

C Bonnerot 1, M Vernet 1, G Grimber 1, P Briand 1, J F Nicolas 1
PMCID: PMC332593  PMID: 1662816

Abstract

The mouse zygotic genome is activated at the 2-cell stage. At this stage, microinjected DNA can be expressed and its transcription, analysed qualitatively with LacZ reporter genes, has the following characteristics (i) Sp1-sensitive promoters are active; (ii) the SV40 early promoter does not require upstream enhancers; (iii) genes driven by the -447, +563 region of murine leukemia virus (M-MuLV) are repressed and; (iv) activation of promoters is possible as shown for the promoter of acetylcholine receptor alpha-subunit by MyoD. This transactivation can occur before the formation of the zygotic genome. The transcriptional selectivity of 2-cell embryos also characterizes oocytes and 4-cell embryos. Therefore the elements involved are present in the oocytes and they persist after fertilization. This transcriptional selectivity has numerous common characteristics with that in EC cells, and may be indicative of a genetic control program specific for multipotential cells.

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Selected References

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  1. Ambros V. A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell. 1989 Apr 7;57(1):49–57. doi: 10.1016/0092-8674(89)90171-2. [DOI] [PubMed] [Google Scholar]
  2. Bachvarova R., Cohen E. M., De Leon V., Tokunaga K., Sakiyama S., Paynton B. V. Amounts and modulation of actin mRNAs in mouse oocytes and embryos. Development. 1989 Jul;106(3):561–565. doi: 10.1242/dev.106.3.561. [DOI] [PubMed] [Google Scholar]
  3. Bachvarova R., De Leon V., Johnson A., Kaplan G., Paynton B. V. Changes in total RNA, polyadenylated RNA, and actin mRNA during meiotic maturation of mouse oocytes. Dev Biol. 1985 Apr;108(2):325–331. doi: 10.1016/0012-1606(85)90036-3. [DOI] [PubMed] [Google Scholar]
  4. Barklis E., Mulligan R. C., Jaenisch R. Chromosomal position or virus mutation permits retrovirus expression in embryonal carcinoma cells. Cell. 1986 Nov 7;47(3):391–399. doi: 10.1016/0092-8674(86)90596-9. [DOI] [PubMed] [Google Scholar]
  5. Barrera-Saldana H., Takahashi K., Vigneron M., Wildeman A., Davidson I., Chambon P. All six GC-motifs of the SV40 early upstream element contribute to promoter activity in vivo and in vitro. EMBO J. 1985 Dec 30;4(13B):3839–3849. doi: 10.1002/j.1460-2075.1985.tb04156.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bolton V. N., Oades P. J., Johnson M. H. The relationship between cleavage, DNA replication, and gene expression in the mouse 2-cell embryo. J Embryol Exp Morphol. 1984 Feb;79:139–163. [PubMed] [Google Scholar]
  7. Bonnerot C., Grimber G., Briand P., Nicolas J. F. Patterns of expression of position-dependent integrated transgenes in mouse embryo. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6331–6335. doi: 10.1073/pnas.87.16.6331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bonnerot C., Rocancourt D., Briand P., Grimber G., Nicolas J. F. A beta-galactosidase hybrid protein targeted to nuclei as a marker for developmental studies. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6795–6799. doi: 10.1073/pnas.84.19.6795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chalifour L. E., Wirak D. O., Hansen U., Wassarman P. M., DePamphilis M. L. cis- and trans-acting sequences required for expression of simian virus 40 genes in mouse oocytes. Genes Dev. 1987 Dec;1(10):1096–1106. doi: 10.1101/gad.1.10.1096. [DOI] [PubMed] [Google Scholar]
  10. Chalifour L. E., Wirak D. O., Wassarman P. M., DePamphilis M. L. Expression of simian virus 40 early and late genes in mouse oocytes and embryos. J Virol. 1986 Sep;59(3):619–627. doi: 10.1128/jvi.59.3.619-627.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. David-Watine B., Israël A., Kourilsky P. The regulation and expression of MHC class I genes. Immunol Today. 1990 Aug;11(8):286–292. doi: 10.1016/0167-5699(90)90114-o. [DOI] [PubMed] [Google Scholar]
  12. Dooley T. P., Miranda M., Jones N. C., DePamphilis M. L. Transactivation of the adenovirus EIIa promoter in the absence of adenovirus E1A protein is restricted to mouse oocytes and preimplantation embryos. Development. 1989 Dec;107(4):945–956. doi: 10.1242/dev.107.4.945. [DOI] [PubMed] [Google Scholar]
  13. Durand D. B., Shaw J. P., Bush M. R., Replogle R. E., Belagaje R., Crabtree G. R. Characterization of antigen receptor response elements within the interleukin-2 enhancer. Mol Cell Biol. 1988 Apr;8(4):1715–1724. doi: 10.1128/mcb.8.4.1715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Edwards A., Voss H., Rice P., Civitello A., Stegemann J., Schwager C., Zimmermann J., Erfle H., Caskey C. T., Ansorge W. Automated DNA sequencing of the human HPRT locus. Genomics. 1990 Apr;6(4):593–608. doi: 10.1016/0888-7543(90)90493-e. [DOI] [PubMed] [Google Scholar]
  15. Emilie D., Peuchmaur M., Barad M., Jouin H., Maillot M. C., Couez D., Nicolas J. F., Malissen B. Visualizing interleukin 2 gene expression at the single cell level. Eur J Immunol. 1989 Sep;19(9):1619–1624. doi: 10.1002/eji.1830190915. [DOI] [PubMed] [Google Scholar]
  16. Evans M. J., Kaufman M. H. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981 Jul 9;292(5819):154–156. doi: 10.1038/292154a0. [DOI] [PubMed] [Google Scholar]
  17. Feuer G., Taketo M., Hanecak R. C., Fan H. Two blocks in Moloney murine leukemia virus expression in undifferentiated F9 embryonal carcinoma cells as determined by transient expression assays. J Virol. 1989 May;63(5):2317–2324. doi: 10.1128/jvi.63.5.2317-2324.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fujimura F. K., Deininger P. L., Friedmann T., Linney E. Mutation near the polyoma DNA replication origin permits productive infection of F9 embryonal carcinoma cells. Cell. 1981 Mar;23(3):809–814. doi: 10.1016/0092-8674(81)90445-1. [DOI] [PubMed] [Google Scholar]
  19. Fuse A., Fujita T., Yasumitsu H., Kashima N., Hasegawa K., Taniguchi T. Organization and structure of the mouse interleukin-2 gene. Nucleic Acids Res. 1984 Dec 21;12(24):9323–9331. doi: 10.1093/nar/12.24.9323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Giebelhaus D. H., Weitlauf H. M., Schultz G. A. Actin mRNA content in normal and delayed implanting mouse embryos. Dev Biol. 1985 Feb;107(2):407–413. doi: 10.1016/0012-1606(85)90322-7. [DOI] [PubMed] [Google Scholar]
  21. Gordon J. W., Ruddle F. H. Gene transfer into mouse embryos: production of transgenic mice by pronuclear injection. Methods Enzymol. 1983;101:411–433. doi: 10.1016/0076-6879(83)01031-9. [DOI] [PubMed] [Google Scholar]
  22. Gorman C. M., Rigby P. W., Lane D. P. Negative regulation of viral enhancers in undifferentiated embryonic stem cells. Cell. 1985 Sep;42(2):519–526. doi: 10.1016/0092-8674(85)90109-6. [DOI] [PubMed] [Google Scholar]
  23. Gossler A., Joyner A. L., Rossant J., Skarnes W. C. Mouse embryonic stem cells and reporter constructs to detect developmentally regulated genes. Science. 1989 Apr 28;244(4903):463–465. doi: 10.1126/science.2497519. [DOI] [PubMed] [Google Scholar]
  24. Harding K., Wedeen C., McGinnis W., Levine M. Spatially regulated expression of homeotic genes in Drosophila. Science. 1985 Sep 20;229(4719):1236–1242. doi: 10.1126/science.3898362. [DOI] [PubMed] [Google Scholar]
  25. Harper M. I., Monk M. Evidence for translation of HPRT enzyme on maternal mRNA in early mouse embryos. J Embryol Exp Morphol. 1983 Apr;74:15–28. [PubMed] [Google Scholar]
  26. Imperiale M. J., Kao H. T., Feldman L. T., Nevins J. R., Strickland S. Common control of the heat shock gene and early adenovirus genes: evidence for a cellular E1A-like activity. Mol Cell Biol. 1984 May;4(5):867–874. doi: 10.1128/mcb.4.5.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Israel A., Yano O., Logeat F., Kieran M., Kourilsky P. Two purified factors bind to the same sequence in the enhancer of mouse MHC class I genes: one of them is a positive regulator induced upon differentiation of teratocarcinoma cells. Nucleic Acids Res. 1989 Jul 11;17(13):5245–5257. doi: 10.1093/nar/17.13.5245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Jakob H., Nicolas J. F. Mouse teratocarcinoma cells. Methods Enzymol. 1987;151:66–81. doi: 10.1016/s0076-6879(87)51009-6. [DOI] [PubMed] [Google Scholar]
  29. Jones N. C., Rigby P. W., Ziff E. B. Trans-acting protein factors and the regulation of eukaryotic transcription: lessons from studies on DNA tumor viruses. Genes Dev. 1988 Mar;2(3):267–281. doi: 10.1101/gad.2.3.267. [DOI] [PubMed] [Google Scholar]
  30. Kalderon D., Roberts B. L., Richardson W. D., Smith A. E. A short amino acid sequence able to specify nuclear location. Cell. 1984 Dec;39(3 Pt 2):499–509. doi: 10.1016/0092-8674(84)90457-4. [DOI] [PubMed] [Google Scholar]
  31. Katinka M., Vasseur M., Montreau N., Yaniv M., Blangy D. Polyoma DNA sequences involved in control of viral gene expression in murine embryonal carcinoma cells. Nature. 1981 Apr 23;290(5808):720–722. doi: 10.1038/290720a0. [DOI] [PubMed] [Google Scholar]
  32. Kim S. H., Moores J. C., David D., Respess J. G., Jolly D. J., Friedmann T. The organization of the human HPRT gene. Nucleic Acids Res. 1986 Apr 11;14(7):3103–3118. doi: 10.1093/nar/14.7.3103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kimura A., Israël A., Le Bail O., Kourilsky P. Detailed analysis of the mouse H-2Kb promoter: enhancer-like sequences and their role in the regulation of class I gene expression. Cell. 1986 Jan 31;44(2):261–272. doi: 10.1016/0092-8674(86)90760-9. [DOI] [PubMed] [Google Scholar]
  34. Klarsfeld A., Daubas P., Bourachot B., Changeux J. P. A 5'-flanking region of the chicken acetylcholine receptor alpha-subunit gene confers tissue specificity and developmental control of expression in transfected cells. Mol Cell Biol. 1987 Feb;7(2):951–955. doi: 10.1128/mcb.7.2.951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lin D., Chinault A. C. Comparative study of DNase I sensitivity at the X-linked human HPRT locus. Somat Cell Mol Genet. 1988 May;14(3):261–272. doi: 10.1007/BF01534587. [DOI] [PubMed] [Google Scholar]
  36. Linney E., Davis B., Overhauser J., Chao E., Fan H. Non-function of a Moloney murine leukaemia virus regulatory sequence in F9 embryonal carcinoma cells. 1984 Mar 29-Apr 4Nature. 308(5958):470–472. doi: 10.1038/308470a0. [DOI] [PubMed] [Google Scholar]
  37. Linney E., Donerly S. DNA fragments from F9 PyEC mutants increase expression of heterologous genes in transfected F9 cells. Cell. 1983 Dec;35(3 Pt 2):693–699. doi: 10.1016/0092-8674(83)90102-2. [DOI] [PubMed] [Google Scholar]
  38. Loh T. P., Sievert L. L., Scott R. W. Evidence for a stem cell-specific repressor of Moloney murine leukemia virus expression in embryonal carcinoma cells. Mol Cell Biol. 1990 Aug;10(8):4045–4057. doi: 10.1128/mcb.10.8.4045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Martínez-Salas E., Linney E., Hassell J., DePamphilis M. L. The need for enhancers in gene expression first appears during mouse development with formation of the zygotic nucleus. Genes Dev. 1989 Oct;3(10):1493–1506. doi: 10.1101/gad.3.10.1493. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Melton D. W., McEwan C., McKie A. B., Reid A. M. Expression of the mouse HPRT gene: deletional analysis of the promoter region of an X-chromosome linked housekeeping gene. Cell. 1986 Jan 31;44(2):319–328. doi: 10.1016/0092-8674(86)90766-x. [DOI] [PubMed] [Google Scholar]
  42. Miyazaki J., Appella E., Ozato K. Negative regulation of the major histocompatibility class I gene in undifferentiated embryonal carcinoma cells. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9537–9541. doi: 10.1073/pnas.83.24.9537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Modlinski J. A., Gerhäuser D., Lioi B., Winking H., Illmensee K. Nuclear transfer from teratocarcinoma cells into mouse oocytes and eggs. Development. 1990 Feb;108(2):337–348. doi: 10.1242/dev.108.2.337. [DOI] [PubMed] [Google Scholar]
  44. Nudel U., Zakut R., Shani M., Neuman S., Levy Z., Yaffe D. The nucleotide sequence of the rat cytoplasmic beta-actin gene. Nucleic Acids Res. 1983 Mar 25;11(6):1759–1771. doi: 10.1093/nar/11.6.1759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Ozato K., Wan Y. J., Orrison B. M. Mouse major histocompatibility class I gene expression begins at midsomite stage and is inducible in earlier-stage embryos by interferon. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2427–2431. doi: 10.1073/pnas.82.8.2427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Pankratz M. J., Jäckle H. Making stripes in the Drosophila embryo. Trends Genet. 1990 Sep;6(9):287–292. doi: 10.1016/0168-9525(90)90234-w. [DOI] [PubMed] [Google Scholar]
  47. Petersen R., Kempler G., Barklis E. A stem cell-specific silencer in the primer-binding site of a retrovirus. Mol Cell Biol. 1991 Mar;11(3):1214–1221. doi: 10.1128/mcb.11.3.1214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Piette J., Bessereau J. L., Huchet M., Changeux J. P. Two adjacent MyoD1-binding sites regulate expression of the acetylcholine receptor alpha-subunit gene. Nature. 1990 May 24;345(6273):353–355. doi: 10.1038/345353a0. [DOI] [PubMed] [Google Scholar]
  49. Reith A. D., Bernstein A. Molecular basis of mouse developmental mutants. Genes Dev. 1991 Jul;5(7):1115–1123. doi: 10.1101/gad.5.7.1115. [DOI] [PubMed] [Google Scholar]
  50. Sanes J. R., Rubenstein J. L., Nicolas J. F. Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J. 1986 Dec 1;5(12):3133–3142. doi: 10.1002/j.1460-2075.1986.tb04620.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Sassone-Corsi P., Duboule D., Chambon P. Viral enhancer activity in teratocarcinoma cells. Cold Spring Harb Symp Quant Biol. 1985;50:747–752. doi: 10.1101/sqb.1985.050.01.092. [DOI] [PubMed] [Google Scholar]
  52. Schirm S., Jiricny J., Schaffner W. The SV40 enhancer can be dissected into multiple segments, each with a different cell type specificity. Genes Dev. 1987 Mar;1(1):65–74. doi: 10.1101/gad.1.1.65. [DOI] [PubMed] [Google Scholar]
  53. Schultz R. M., Wassarman P. M. Biochemical studies of mammalian oogenesis: Protein synthesis during oocyte growth and meiotic maturation in the mouse. J Cell Sci. 1977 Apr;24:167–194. doi: 10.1242/jcs.24.1.167. [DOI] [PubMed] [Google Scholar]
  54. Schöler H. R., Hatzopoulos A. K., Balling R., Suzuki N., Gruss P. A family of octamer-specific proteins present during mouse embryogenesis: evidence for germline-specific expression of an Oct factor. EMBO J. 1989 Sep;8(9):2543–2550. doi: 10.1002/j.1460-2075.1989.tb08392.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Scott M. P., Carroll S. B. The segmentation and homeotic gene network in early Drosophila development. Cell. 1987 Dec 4;51(5):689–698. doi: 10.1016/0092-8674(87)90092-4. [DOI] [PubMed] [Google Scholar]
  56. Sekikawa K., Levine A. J. Isolation and characterization of polyoma host range mutants that replicate in nullipotential embryonal carcinoma cells. Proc Natl Acad Sci U S A. 1981 Feb;78(2):1100–1104. doi: 10.1073/pnas.78.2.1100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Sleigh M. J., Lockett T. J. SV40 enhancer activation during retinoic acid-induced differentiation of F9 embryonal carcinoma cells. EMBO J. 1985 Dec 30;4(13B):3831–3837. doi: 10.1002/j.1460-2075.1985.tb04155.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Stevens M. E., Meneses J. J., Pedersen R. A. Expression of a mouse metallothionein-Escherichia coli beta-galactosidase fusion gene (MT-beta gal) in early mouse embryos. Exp Cell Res. 1989 Aug;183(2):319–325. doi: 10.1016/0014-4827(89)90392-3. [DOI] [PubMed] [Google Scholar]
  59. Stuart G. W., Searle P. F., Chen H. Y., Brinster R. L., Palmiter R. D. A 12-base-pair DNA motif that is repeated several times in metallothionein gene promoters confers metal regulation to a heterologous gene. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7318–7322. doi: 10.1073/pnas.81.23.7318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Tsukiyama T., Niwa O., Yokoro K. Analysis of the binding proteins and activity of the long terminal repeat of Moloney murine leukemia virus during differentiation of mouse embryonal carcinoma cells. J Virol. 1991 Jun;65(6):2979–2986. doi: 10.1128/jvi.65.6.2979-2986.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Ullman K. S., Northrop J. P., Verweij C. L., Crabtree G. R. Transmission of signals from the T lymphocyte antigen receptor to the genes responsible for cell proliferation and immune function: the missing link. Annu Rev Immunol. 1990;8:421–452. doi: 10.1146/annurev.iy.08.040190.002225. [DOI] [PubMed] [Google Scholar]
  62. Wasylyk B., Wasylyk C., Augereau P., Chambon P. The SV40 72 bp repeat preferentially potentiates transcription starting from proximal natural or substitute promoter elements. Cell. 1983 Feb;32(2):503–514. doi: 10.1016/0092-8674(83)90470-1. [DOI] [PubMed] [Google Scholar]
  63. Wirak D. O., Chalifour L. E., Wassarman P. M., Muller W. J., Hassell J. A., DePamphilis M. L. Sequence-dependent DNA replication in preimplantation mouse embryos. Mol Cell Biol. 1985 Nov;5(11):2924–2935. doi: 10.1128/mcb.5.11.2924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Xiao J. H., Davidson I., Macchi M., Rosales R., Vigneron M., Staub A., Chambon P. In vitro binding of several cell-specific and ubiquitous nuclear proteins to the GT-I motif of the SV40 enhancer. Genes Dev. 1987 Oct;1(8):794–807. doi: 10.1101/gad.1.8.794. [DOI] [PubMed] [Google Scholar]
  65. Yang T. P., Caskey C. T. Nuclease sensitivity of the mouse HPRT gene promoter region: differential sensitivity on the active and inactive X chromosomes. Mol Cell Biol. 1987 Aug;7(8):2994–2998. doi: 10.1128/mcb.7.8.2994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Zenke M., Grundström T., Matthes H., Wintzerith M., Schatz C., Wildeman A., Chambon P. Multiple sequence motifs are involved in SV40 enhancer function. EMBO J. 1986 Feb;5(2):387–397. doi: 10.1002/j.1460-2075.1986.tb04224.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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