Abstract
The early development of the zebra fish (Danio rerio) embryo is characterized by a series of rapid and synchronous cell cycles with no detectable transcription. This period is followed by the midblastula transition (MBT), during which the cell cycle gradually lengthens, cell synchrony is lost, and zygotic transcription is initially detected. In this work, we examined the changes in the pattern of the cell cycle during MBT in zebra fish and whether these changes are dependent on the initiation of zygotic transcription. To characterize the pattern of the early zebra fish cell cycles, the embryonic DNA content was determined by flow cytometric analysis. We found that G1 phase is below detection levels during the first 10 cleavages and can be initially detected at the onset of MBT. Inhibition of zygotic transcription, by microinjection of actinomycin D, abolished the appearance of G1 phase at MBT. Premature activation of zygotic transcription, by microinjection of nonspecific DNA, induced G1 phase before the onset of MBT, while coinjection of actinomycin D and nonspecific DNA abolished this early appearance of G1 phase. We therefore suggest that during the early development of the zebra fish embryo, G1 phase appears at the onset of MBT and that the activation of transcription at MBT is essential and sufficient for the G1-phase induction.
Full Text
The Full Text of this article is available as a PDF (433.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- Bitzur S., Kam Z., Geiger B. Structure and distribution of N-cadherin in developing zebrafish embryos: morphogenetic effects of ectopic over-expression. Dev Dyn. 1994 Oct;201(2):121–136. doi: 10.1002/aja.1002010204. [DOI] [PubMed] [Google Scholar]
- Edgar B. A., Kiehle C. P., Schubiger G. Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development. Cell. 1986 Jan 31;44(2):365–372. doi: 10.1016/0092-8674(86)90771-3. [DOI] [PubMed] [Google Scholar]
- Edgar B. A., O'Farrell P. H. The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2 by string. Cell. 1990 Aug 10;62(3):469–480. doi: 10.1016/0092-8674(90)90012-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edgar B. A., Schubiger G. Parameters controlling transcriptional activation during early Drosophila development. Cell. 1986 Mar 28;44(6):871–877. doi: 10.1016/0092-8674(86)90009-7. [DOI] [PubMed] [Google Scholar]
- Foe V. E., Alberts B. M. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci. 1983 May;61:31–70. doi: 10.1242/jcs.61.1.31. [DOI] [PubMed] [Google Scholar]
- Frederick D. L., Andrews M. T. Cell cycle remodeling requires cell-cell interactions in developing Xenopus embryos. J Exp Zool. 1994 Nov 15;270(4):410–416. doi: 10.1002/jez.1402700411. [DOI] [PubMed] [Google Scholar]
- Graves B. J., Schubiger G. Cell cycle changes during growth and differentiation of imaginal leg discs in Drosophila melanogaster. Dev Biol. 1982 Sep;93(1):104–110. doi: 10.1016/0012-1606(82)90243-3. [DOI] [PubMed] [Google Scholar]
- Halevy O., Novitch B. G., Spicer D. B., Skapek S. X., Rhee J., Hannon G. J., Beach D., Lassar A. B. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science. 1995 Feb 17;267(5200):1018–1021. doi: 10.1126/science.7863327. [DOI] [PubMed] [Google Scholar]
- Harper J. W., Elledge S. J. Cdk inhibitors in development and cancer. Curr Opin Genet Dev. 1996 Feb;6(1):56–64. doi: 10.1016/s0959-437x(96)90011-8. [DOI] [PubMed] [Google Scholar]
- Kane D. A., Kimmel C. B. The zebrafish midblastula transition. Development. 1993 Oct;119(2):447–456. doi: 10.1242/dev.119.2.447. [DOI] [PubMed] [Google Scholar]
- Kane D. A., Warga R. M., Kimmel C. B. Mitotic domains in the early embryo of the zebrafish. Nature. 1992 Dec 24;360(6406):735–737. doi: 10.1038/360735a0. [DOI] [PubMed] [Google Scholar]
- Kimmel C. B., Ballard W. W., Kimmel S. R., Ullmann B., Schilling T. F. Stages of embryonic development of the zebrafish. Dev Dyn. 1995 Jul;203(3):253–310. doi: 10.1002/aja.1002030302. [DOI] [PubMed] [Google Scholar]
- Kimmel C. B., Law R. D. Cell lineage of zebrafish blastomeres. I. Cleavage pattern and cytoplasmic bridges between cells. Dev Biol. 1985 Mar;108(1):78–85. doi: 10.1016/0012-1606(85)90010-7. [DOI] [PubMed] [Google Scholar]
- Kornberg R. D., Lorch Y. Irresistible force meets immovable object: transcription and the nucleosome. Cell. 1991 Nov 29;67(5):833–836. doi: 10.1016/0092-8674(91)90354-2. [DOI] [PubMed] [Google Scholar]
- Lukas J., Bartkova J., Rohde M., Strauss M., Bartek J. Cyclin D1 is dispensable for G1 control in retinoblastoma gene-deficient cells independently of cdk4 activity. Mol Cell Biol. 1995 May;15(5):2600–2611. doi: 10.1128/mcb.15.5.2600. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marrable A. W. Cell numbers during cleavage of the zebra fish egg. J Embryol Exp Morphol. 1965 Aug;14(1):15–24. [PubMed] [Google Scholar]
- McKnight S. L., Miller O. L., Jr Electron microscopic analysis of chromatin replication in the cellular blastoderm Drosophila melanogaster embryo. Cell. 1977 Nov;12(3):795–804. doi: 10.1016/0092-8674(77)90278-1. [DOI] [PubMed] [Google Scholar]
- Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell. 1982 Oct;30(3):675–686. doi: 10.1016/0092-8674(82)90272-0. [DOI] [PubMed] [Google Scholar]
- Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell. 1982 Oct;30(3):687–696. doi: 10.1016/0092-8674(82)90273-2. [DOI] [PubMed] [Google Scholar]
- 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]
- Prioleau M. N., Huet J., Sentenac A., Méchali M. Competition between chromatin and transcription complex assembly regulates gene expression during early development. Cell. 1994 May 6;77(3):439–449. doi: 10.1016/0092-8674(94)90158-9. [DOI] [PubMed] [Google Scholar]
- Resnitzky D., Reed S. I. Different roles for cyclins D1 and E in regulation of the G1-to-S transition. Mol Cell Biol. 1995 Jul;15(7):3463–3469. doi: 10.1128/mcb.15.7.3463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rupp R. A., Weintraub H. Ubiquitous MyoD transcription at the midblastula transition precedes induction-dependent MyoD expression in presumptive mesoderm of X. laevis. Cell. 1991 Jun 14;65(6):927–937. doi: 10.1016/0092-8674(91)90545-a. [DOI] [PubMed] [Google Scholar]
- Sherr C. J. D-type cyclins. Trends Biochem Sci. 1995 May;20(5):187–190. doi: 10.1016/s0968-0004(00)89005-2. [DOI] [PubMed] [Google Scholar]
- Sherr C. J., Roberts J. M. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 1995 May 15;9(10):1149–1163. doi: 10.1101/gad.9.10.1149. [DOI] [PubMed] [Google Scholar]
- Sánchez I., Dynlacht B. D. Transcriptional control of the cell cycle. Curr Opin Cell Biol. 1996 Jun;8(3):318–324. doi: 10.1016/s0955-0674(96)80004-4. [DOI] [PubMed] [Google Scholar]
- Vasiliev J. M., Gelfand I. M., Domnina L. V., Rappoport R. I. Wound healing processes in cell cultures. Exp Cell Res. 1969 Jan;54(1):83–93. doi: 10.1016/0014-4827(69)90296-1. [DOI] [PubMed] [Google Scholar]
- Weinberg R. A. The retinoblastoma protein and cell cycle control. Cell. 1995 May 5;81(3):323–330. doi: 10.1016/0092-8674(95)90385-2. [DOI] [PubMed] [Google Scholar]
- Yarden A., Salomon D., Geiger B. Zebrafish cyclin D1 is differentially expressed during early embryogenesis. Biochim Biophys Acta. 1995 Dec 27;1264(3):257–260. doi: 10.1016/0167-4781(95)00175-1. [DOI] [PubMed] [Google Scholar]