Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-27T08:07:37.011Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of inhibitors of DNA replication on early zebrafish embryos: evidence for coordinate activation of multiple intrinsic cell-cycle checkpoints at the mid-blastula transition

Published online by Cambridge University Press:  26 September 2008

Richard Ikegami ,
Alma K. Rivera-Bennetts ,
Deborah L. Brooker  and
Thomas D. Yager
Richard Ikegami
Affiliation:
Division of Developmental Biology and Research Institute, Hospital for Sick Children, Toronto, Graduate Department of Molecular and Medical Genetics, University of Toronto, and Naiad Systems, Toronto, Ontario, Canada
Alma K. Rivera-Bennetts
Affiliation:
Division of Developmental Biology and Research Institute, Hospital for Sick Children, Toronto, Graduate Department of Molecular and Medical Genetics, University of Toronto, and Naiad Systems, Toronto, Ontario, Canada
Deborah L. Brooker
Affiliation:
Division of Developmental Biology and Research Institute, Hospital for Sick Children, Toronto, Graduate Department of Molecular and Medical Genetics, University of Toronto, and Naiad Systems, Toronto, Ontario, Canada
Thomas D. Yager*
Affiliation:
Division of Developmental Biology and Research Institute, Hospital for Sick Children, Toronto, Graduate Department of Molecular and Medical Genetics, University of Toronto, and Naiad Systems, Toronto, Ontario, Canada
*
T.D. Yager, Division of Developmental Biology and Research Institute, Hospital for Sick Children, Toronto, Ontario, Canada M59 1X8.
Get access Rights & Permissions [Opens in a new window]

Summary

We address the developmental activation, in the zebrafish embryo, of intrinsic cell-cycle checkpoints which monitor the DNA replication process and progression through the cell cycle. Eukaryotic DNA replication is probably carried out by a multiprotein complex containing numerous enzymes and accessory factors that act in concert to effect processive DNA synthesis (Applegren, N. et al. (1995) J. Cell. Biochem. 59, 91–107). We have exposed early zebrafish embryos to three chemical agents which are predicted to specifically inhibit the DNA polymerase α, topoisomerase I and topoisomerase II components of the DNA replication complex. We present four findings: (1) Before mid-blastula transition (MBT) an inhibition of DNA synthesis does not block cells from attempting to proceed through mitosis, implying the lack of functional checkpoints. (2) After MBT, the embryo displays two distinct modes of intrinsic checkpoint operation. One mode is a rapid and complete stop of cell division, and the other is an ‘adaptive’ response in which the cell cycle continues to operate, perhaps in a ‘repair’ mode, to generate daughter nuclei with few visible defects. (3) The embryo does not display a maximal capability for the ‘adaptive’ response until several hours after MBT, which is consistent with a slow rranscriptional control mechanism for checkpoint activation. (4) The slow activation of checkpoints at MBT provides a window of time during which inhibitors of DNA synthesis will induce cytogenetic lesions without killing the embryo. This could be useful in the design of a deletion-mutagenesis strategy.

Keywords

Cell-cycle checkpointsDeletion-mutagenesisDNA replicationMid-blastula transitionZebrafish
Type
Article
Information
Zygote , Volume 5 , Issue 2 , May 1997 , pp. 153 - 175
Copyright
Copyright © Cambridge University Press 1997

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adachi, Y. & Laemmli, U.K. (1992). Identification of nuclear pre-replication centers poised for DNA synthesis in Xenopus egg extracts: immunolocalization study of replication protein. A. J. Cell Biol. 119, 1–15.Google Scholar
Alexander, S.P. & Rieder, C.L. (1991). Chromosome motion during attachment to the vertebrate spindle: initial salta-tory-like behavior of chromosomes and quantitative analysis of force production by nascent kinetochore fibers. J. Cell Biol. 113, 805–15.Google Scholar
Applegren, N., Hickey, R.J., Kleinschmidt, A.M., Zhou, Q., Coll, J., Wills, P., Swaby, R., Wei, Y., Quan, J.Y. & Lee, M.Y. (1995). Further characterization of the human cell multi-protein DNA replication complex. J. Cell Biochem. 59, 91–107.Google Scholar
Araki, H., Leem, S.-H., Phongdara, A. & Sugino, A. (1995). Dpb11, which interacts with DNA polymerase II (e) in Saccharomyces cerevisiae, has a dual role in S-phase progression and at a cell cycle checkpoint. Proc. Natl. Acad. Sci. USA 92, 11791–5.CrossRefGoogle Scholar
Blaustein, A.R., Hoffman, P.D., Hokit, D.G., Kiesecher, J.M., Walls, S.C. & Hays, J.B. (1994). UV repair and resistance to solar UV-B in amphibian eggs: a link to population declines? Proc. Natl. Acad. Sci. USA 91, 1791–5.Google Scholar
Bryant, P.J., Watson, K.J., Justice, R.W. & Woods, D.F. (1993). Tumor suppressor genes encoding proteins required for cell interactions and signal transduction in Drosophila. Development (Suppl)., 239–49.Google Scholar
Buschman, E., Lepage, P. & Gros, P. (1994). P-glycoprotein homologues. Cancer Treat. Res. 73, 17–39.CrossRefGoogle ScholarPubMed
Chaudhary, N. & Courvalin, J.C. (1993). Stepwise reassembly of the nuclear envelope at the end of mitosis. J. Cell Biol. 122, 295–306.CrossRefGoogle ScholarPubMed
Chong, J.P.J., Thommes, P. & Blow, J.J. (1996). The role of MCM/P1 proteins in the licensing of DNA replication. Trends Biochem. Sci. 21, 102–6.CrossRefGoogle ScholarPubMed
Cochet-Meilhac, M. & Chambon, P. (1974). Animal DNA-dependent RNA polymerases. II. Mechanism of the inhibition of RNA polymerases B by amatoxins. Biochim. Biophys. Acta 353, 160–84.Google Scholar
Collodi, P., Miranda, C, Zhao, X., Buhler, D.R. & Barnes, D.W. (1994). Induction of zebrafish hepatic cytochrome P450 in vivo and in cell culture. Xenobiotica 24, 487–93.CrossRefGoogle ScholarPubMed
Daga, R.R., Thode, G. & Amores, A. (1996). Chromosome complement, C-banding, Ag-NOR and replication banding in the zebrafish Danio rerio. Chromosome Res. 4, 29–32.Google Scholar
Darzynkiewicz, Z. (1995). Apoptosis in anti-tumor strategies: modulation of cell cycle or differentiation. J. Cell. Biochem. 58, 151–9.Google Scholar
Dasso, M. & Newport, J.W. (1990). Completion of DNA replication is monitored by a feedback system that controls the initiation of mitosis in vitro: studies in Xenopus. Cell 61, 811–23.CrossRefGoogle ScholarPubMed
Del Bino, G., Skierski, J.S. & Darzynkiewicz, Z. (1991). The concentration-dependent diversity of effects of DNA topoisomerase I and II inhibitors on the cell cycle of HL-60 cells. Exp. Cell Res. 195, 485–91.Google Scholar
Devlin, R.H., McNeil, B.K., Solar, I.I. & Donaldson, E.M. (1994). A rapid PCR-based test for Y-chromosomal DNA allows simple production of all-female strains of chinook salmon. Aquaculture 128, 211–20.CrossRefGoogle Scholar
DiNardo, S., Voelkel, K. & Sternglanz, R. (1984). DNA topoisomerase II mutant of Saccharomyces cerevisiae: topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication. Proc. Natl. Acad. Sci. USA 81, 2616–20.Google Scholar
Downes, C.S., Clarke, D.J., Mullinger, A.M., Gimenez-Abian, J.F., Creighton, A.M. & Johnson, R.T. (1994). A topoisomerase II dependent G2 cycle checkpoint in mammalian cells. Nature 372, 467–70.CrossRefGoogle ScholarPubMed
Driever, W., Solnica-Krezel, L., Schier, A.F., Neuhauss, S.C.F., Malicki, J., Stemple, D.L., Stanier, D.Y.R., Zwart-kruis, F., Abdelilah, S., Rangini, Z., Belak, J. & Boggs, C. (1996). A genetic screen for mutations affecting embryo-genesis in zebrafish. Development 123, 37–46.Google Scholar
Du, S.J., Devlin, R.H. & Hew, C.L. (1993). Genomic structure of growth hormone genes in chinook salmon (Onco-rhynchus tshawytscha): presence of two functional genes, GH-I and GH-II, and a male-specific pseudogene GH-psi. DNA Cell Biol. 12, 739–51.Google Scholar
Edgar, B.A. & Datar, S.A. (1996). Zygotic degradation of two maternal cdc25 mRNAs terminates Drosophila's early cell cycle program. Genes Dev. 10, 1966–77.Google Scholar
Felsenfeld, A.L. (1996). Defining the boundaries of zebrafish developmental genetics. Nature Genet. 14, 258–63.CrossRefGoogle ScholarPubMed
Forbes, S.H., Knudsen, K.L., North, T.W. & Allendorf, F.W. (1994). One of two growth hormone genes in coho salmon is sex-linked. Proc. Natl. Acad. Sci. USA 91, 1628–31.CrossRefGoogle ScholarPubMed
Francesconi, S., De Recondo, A.M. & Baldacci, G. (1995). DNA polymerase delta is required for the replication feedback control of cell-cycle progression in Schizo-saccharomyces pombe. Mol. Gen. Genet. 246, 561–9.CrossRefGoogle ScholarPubMed
Friedberg, E.C., Walker, G.C. & Siede, W. (eds.) (1995). DNA Repair and Mutagenesis. Washington, DC: ASM Press.Google Scholar
Fritz, A., Rozowski, M., Walker, C. & Westerfield, M. (1996). Identification of selected gamma-ray induced deficiencies in zebrafish using multiplex polymerase chain reaction. Genetics 144, 1735–45.Google Scholar
Gaiano, N., Amsterdam, A., Kawakami, K., Allende, M., Becker, T. & Hopkins, N. (1996). Insertional mutagenesis and rapid cloning of essential genes in zebrafish. Nature 383, 829–32.Google Scholar
Gasser, S.M., Laroche, T., Falquet, J., Boy de la Tour, E. & Laemmli, U.K. (1986). Metaphase chromosome structure involvement of topoisomerase II. J. Mol. Biol. 188, 613–29.Google Scholar
Glover, T.W. & Stein, C.K. (1988). Chromosome breakage and recombination at fragile sites. Am. J. Hum. Genet. 43, 265–73.Google Scholar
Gromova, I.I., Thomsen, B. & Razin, S.V. (1995). Different topoisomerase II antitumor drugs direct similar specific long-range fragmentation of an amplified c-MYC gene locus in living cells and in high-salt-extracted nuclei. Proc. Natl. Acad. Sci. USA 92, 102–6.Google Scholar
Haaf, T. & Schmid, M. (1991). Chromosome topology in mammalian interphase nuclei. Exp. Cell Res. 192, 325–32.Google Scholar
Haffter, P., Granato, M., Brand, M., Mullins, M.C., Ham-merschmidt, M., Kane, D.A., Odenthal, J., van Eeden, F.J.M., Jiang, Y.-J., Heisenberg, C.-P, Kelsh, R.N., Furu-tani-Seiki, M., Vogelsang, E., Beuchle, D., Schach, U., Fabian, C. & Nusslein-Volhard, C. (1996). The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123, 1–36.Google ScholarPubMed
Hally, M.K., Rasch, E.M., Mainwaring, H.R. & Bruce, R.C. (1986). Cytophotometric evidence of variation in genome size of desmognathine salamanders. Histochemistry 85, 185–92.Google Scholar
Hartwell, L.H. & Kastan, M.B. (1994). Cell-cycle control and cancer. Science 266, 1821–8.Google Scholar
Heichman, K. A. & Roberts, J.M. (1994). Rules to replicate by. Cell 79, 557–62.Google Scholar
Hinegardner, R. & Rosen, D.E. (1972). Cellular DNA content and the evolution of teleostean fishes. Am. Nat. 166, 621–44.Google Scholar
Hofferer, L., Winterhalter, K.H. & Althaus, F.R. (1995). Xenopus eggs lysates repair heat-generated DNA nicks with an average patch size of 36 nucleotides. Nucleic Acids Res. 23, 1396–7.CrossRefGoogle Scholar
Horiguchi, T. & Tanida, S. (1995). Rescue of Schizosaccharo-myces pombe from camptothecin-mediated death by a DNA topoisomerase I inhibitor, TAN-1518 A. Biochem. Pharmacol. 49, 1395–401.Google Scholar
Howe, J.A. & Newport, J.W. (1996). A developmental timer regulates degradation of cyclin E1 at the midblastula transition during Xenopus embryogenesis. Proc. Natl. Acad. Sci. USA 93, 2060–4.Google Scholar
Iarovaia, O., Hancock, R., Lagarkova, M., Miassod, R. & Razin, S.V. (1996). Mapping of genomic DNA loop organization in a 500-kilobase region of the Drosophila X chromosome by the topoisomerase II-mediated DNA loop excision protocol. Mol. Cell. Biol. 16, 302–8.CrossRefGoogle Scholar
Johnson, S.L., Gates, M.A., Johnson, M., Talbot, W.S., Home, S., Baik, K., Rude, S., Wong, J.R. & Postlethwait, J.H. (1996). Centromere-linkage analysis and consolidation of the zebrafish genetic map. Genetics 142, 1277–88.Google Scholar
Kane, D.A. & Kimmel, C.B. (1993). The zebrafish midblastula transition. Development 119, 447–56.Google Scholar
Kane, D.A., Maischein, H.M., Brand, M., van Eeden, F.J., Furutani-Seiki, M., Granato, M., Haffter, P., Hammer-schmidt, M., Heisenberg, C.P, Jiang, Y.T., Kelsh, R.N., Mullins, M.C., Odenthal, J., Warga, R.M. & Nusslein-Volhard, C. (1996). The zebrafish early arrest mutants. Development 123, 57–66.Google Scholar
Kane, D.A., Warga, R.M. & Kimmel, C.B. (1992). Mitotic domains in the early embryo of the zebrafish. Nature 360, 735–7.CrossRefGoogle ScholarPubMed
Kim, R.A. & Wang, J.C. (1989). Function of DNA topoiso-merases as replication swivels in Saccharomyces cerevisiae. J. Mol. Biol. 208, 257–67.Google Scholar
Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B. & Schilling, T.F. (1995). Stages of embryonic development of the zebrafish. Dev. Dynam. 203, 253–310.Google Scholar
King, R.W., Peters, J.M., Tugendreich, A., Rolfe, M., Hieter, P. & Kirschner, M.W. (1995). A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 81, 279–88.CrossRefGoogle ScholarPubMed
Knapik, E.W., Goodman, A., Atkinson, S.O., Roberts, C.T., Shiozawa, M., Sim, C.U., Weksler-Zangen, S., Trolliet, M.R., Futrell, C, Innes, B.A., Koike, G., McLaughlin, M.G., Pierre, L, Simon, J.S., Vilallonga, E., Roy, M., Chiang, P.-W., Fishman, M.C., Driever, W. & Jacob, H.J. (1996). A reference cross DNA panel for zebrafish (Danio rerio) anchored with simple sequence length polymorphisms. Development 123, 451–60.Google Scholar
Kumagai, A. & Dunphy, W.G. (1995). Control of the Cdc2/ cyclin B complex in Xenopus egg extracts arrested at a G2/ M checkpoint with DNA synthesis inhibitors. Mol. Biol. Cell 6, 199–213.Google Scholar
Lam, W.L., Lee, T.-S. & Gilbert, W. (1996). Active transposition in zebrafish. Proc. Natl. Acad. Sci. USA 93, 10870–5.CrossRefGoogle ScholarPubMed
Lee, S.-H., Kim, D.-K. & Drissi, R. (1995). Human xeroderma pigmentosum Group A protein interacts with human replication protein A and inhibits DNA replication. J. Biol. Chem. 270, 21800–5.Google Scholar
Lehman, C.W., Jeong-Yu, S., Trautman, J.K. & Carroll, D. (1994). Repair of heteroduplex DNA in Xenopus laevis oocytes. Genetics 138, 459–70.CrossRefGoogle ScholarPubMed
Li, J.J. & Deshaies, R.J. (1993). Exercising self-restraint: discouraging illicit acts of S and M in eukaryotes. Cell 74, 223–6.Google Scholar
Li, C.J., Averboukh, L. & Pardee, A.B. (1993 a). β-Lapachone, a novel DNA topoisomerase I inhibitor with a mode of action different from camptothecin. J. Biol. Chem. 268, 22463–8.Google Scholar
Li, C, Cao, L.-G., Wand, Y.-L. & Baril, E.F. (1993 b). Further purification and characterization of a multienzyme complex for DNA synthesis in human cells. J. Cell. Biochem. 53, 405–19.CrossRefGoogle ScholarPubMed
Lincke, C.R., Broeks, A., The, I., Plasterk, R.H.A. & Borst, P. (1993). The expression of two P-glycoprotein (pgp) genes in transgenic Caenorhabditis elegans is confined to intestinal cells. EMBO J. 12, 1615–20.Google Scholar
Malkas, L.H., Hickey, R.J., Li, C, Pedersen, N. & Baril, E.F. (1990). A 21S enzyme complex from HeLa cells that functions in Simian Virus 40 DNA replication in vitro. Biochemistry 29, 6362–74.CrossRefGoogle ScholarPubMed
Margolis, R.L. & Andreassen, P.R. (1993). The telophase disc: its possible role in mammalian cell cleavage. Bio-Essays 15, 201–7.Google Scholar
Matsumoto, Y, Kim, K. & Bogenhagen, D.F. (1994). Proliferating cell nuclear antigen-dependent abasic site repair in Xenopus laevis oocytes: an alternative pathway of base excision DNA repair. Mol. Cell. Biol. 14, 6187–97.Google Scholar
Mullins, M.C., Hammerschmidt, M, Haffter, P. & Nusselin-Volhard, C. (1994). Large-scale mutagenesis in the zebra-fish: in search of genes controlling development in a vertebrate. Curr. Biol. 4, 189–202.Google Scholar
Murakami, H. & Okayama, H. (1995). A kinase from fission yeast responsible for blocking mitosis in S phase. Nature 374, 817–19.Google Scholar
Nagano, H., Hirai, S., Okano, K. & Ikegami, S. (1981). Achromosomal cleavage of fertilization starfish eggs in the presence of aphidicolin. Dev. Biol. 85, 409–15.CrossRefGoogle ScholarPubMed
Navas, T.A., Zhou, Z. & Elledge, S.J. (1995). DNA poly-merase e links the DNA replication machinery to the S phase checkpoint. Cell 80, 29–39.Google Scholar
Nelson, D.R., Kamataki, T., Waxman, D.J., Gugngerich, F.P., Estabrook, R.W., Feyereisen, R., Gonzalez, F.J., Coon, M.J., Gunsalus, I.C., Gotoh, O., et al. (1993). The P450 super-family: update on new sequences, gene mapping, accession numbers, early trivial names of enzymes, and nomenclature. DNA Cell Biol. 12, 1–51.Google Scholar
Neter, J., Wasserman, W. & Whitmore, G.A. (1978). Applied Statistics. Boston: Allyn and Bacon.Google Scholar
Newport, J. & Dasso, M. (1989). On the coupling between DNA replication and mitosis. J. Cell Sci. (Suppl.) 12, 149–60.CrossRefGoogle ScholarPubMed
Nicklas, R.B. (1988). The forces that move chromosomes in mitosis. Annu. Rev. Biophys. Biophys. Chem. 17, 431–49.CrossRefGoogle ScholarPubMed
Nurse, P. (1994). Ordering S phase and M phase in the cell cycle. Cell 79, 547–50.CrossRefGoogle Scholar
Patel, N.H., Martin-Bianco, E., Coleman, K.G., Poole, S.J., Ellis, M.C., Kornberg, T.B. & Goodman, C.S. (1989). Expression of engrailed proteins in arthropods, annelids and chordates. Cell 58, 955–68.CrossRefGoogle ScholarPubMed
Paulovich, A.G. & Hartwell, L.H. (1995). A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82, 841–7.CrossRefGoogle Scholar
Pijnacker, L.P. & Ferwerda, M.A. (1995). Zebrafish chromosome banding. Genome 38, 1052–5.CrossRefGoogle ScholarPubMed
Pommier, Y. (1996). Eukaryotic DNA topoisomerase I: genome gatekeeper and its intruders, camptothecins. Semin. Oncol. 23, 3–10.Google Scholar
Raff, J.W. & Glover, D.M. (1988). Nuclear and cytoplasmic mitotic cycles continue in Drosophila embryos in which DNA synthesis is inhibited with aphidicolin. J. Cell Biol. 107, 2009–19.CrossRefGoogle ScholarPubMed
Raff, M.C. (1992). Social controls on cell survival and cell death. Nature 356, 397–400.CrossRefGoogle ScholarPubMed
Raff, M.C. (1996). Size control: the regulation of cell numbers in animal development. Cell 86, 173–5.CrossRefGoogle ScholarPubMed
Razin, S.V., Petrov, P. & Hancock, R. (1991). Precise localization of the alpha-globin gene cluster within one of the 20-to 300-kilobase DNA fragments released by cleavage of chicken chromosomal DNA at topoisomerase II sites in vivo: evidence that the fragments are DNA loops or domains. Proc. Natl. Acad. Sci. USA 88, 8515–19.CrossRefGoogle ScholarPubMed
Richardson, H.E., O'Keefe, L.V., Reed, S.I. & Saint, R. (1993). A Drosophila G1-specific cyclin E homolog exhibits different modes of expression during embryogenesis. Development 119, 673–90.Google Scholar
Rieder, C.L., Cole, R.W., Khodjakov, A. & Sluder, G. (1995). The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by inhibitory signal produced by unattached kinetochores. J. Cell Biol. 130, 941–8.Google Scholar
Romanowski, P. & Madine, M.A. (1996). Mechanisms restricting DNA replication to one per cell cycle: MCMs, pre-replicative complexes and kinases. Trends Cell Biol. 6, 184–8.CrossRefGoogle Scholar
Saiki, T, Kyozuka, K., Osanai, K. & Hamaguchi, Y (1991). Chromosomal behavior in starfish (Asterina pectinifera) zygotes under the effect of aphidicolin, an inhibitor of DNA polymerase. Exp. Cell Res. 192, 380–8.CrossRefGoogle ScholarPubMed
Sanchez, Y. & Elledge, S.J. (1995). Stopped for repairs. Bioessays 17, 545–8.Google Scholar
Schinkel, A.H., Smit, J.J., van Tellingen, O., Beijnen, J.H., Wagenaar, E., van Deemter, L., Mol, C.A., van der Valk, M.A., Robanus-Maandag, E.C., te Riele, H.P., et al. (1994). Disruption of the mouse mdrla P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77, 491–502.Google Scholar
Shamu, C.E. & Murray, A.W. (1992). Sister chromatid separation in frog egg extracts requires DNA topoisomerase II activity during anaphase. J. Cell Biol. 117, 921–34.Google Scholar
Sheaff, R. & Kuchta, R. (1991). Mechanism of DNA polymerase alpha inhibition by aphidicolin. Biochemistry 30, 8590–7.Google Scholar
Sheldrick, K.S. & Carr, A.M. (1993). Feedback controls and G2 checkpoints: fission yeast as a model system. Bioessays 15, 775–81.Google Scholar
Shima, A. & Shimada, A. (1991). Development of a possible nonmammalian test system for radiation-induced germ-cell mutagenesis using a fish, the Japanese medaka (Oryzias latipes). Proc. Natl. Acad. Sci. USA 88, 2545–9.Google Scholar
Shima, A. & Shimada, A. (1994). The Japanese medaka, Oryzias latipes, as a new model organism for studying environmental germ-cell mutagenesis. Environ. Health Perspect. 102 (Suppl. 12), 33–5.Google Scholar
Shimizu, T. (1994). The prevention of smaller blastomeres of early Tubifex embryos from entering mitosis by unrepli-cated DNA. Dev. Biol. 161, 274–8.CrossRefGoogle ScholarPubMed
Shivji, M.K., Grey, S.J., Strausfeld, U.P., Wood, R.D. & Blow, J.J. (1994). Cipl inhibits DNA replication but not PCNA-dependent nucleotide excision-repair. Curr. Biol. 4, 1062–8.CrossRefGoogle Scholar
Simbulan-Rosenthal, C.M., Rosenthal, D.S., Hilz, H., Hickey, R., Malkas, L., Applegren, N., Wu, Y, Bers, G. & Smulson, M.E. (1996). The expression of poly(ADP-ribose) poly-merase during differentiation-linked DNA replication reveals that it is a component of the multiprotein DNA replication complex. Biochemistry 35, 11622–33.Google Scholar
Sluder, G. & Lewis, K. (1987). Relationship between nuclear DNA synthesis and centrosome reproduction in sea urchin eggs. J. Exp. Zool. 244, 89–100.Google Scholar
Smythe, C. & Newport, J.W. (1992). Coupling of mitosis to the completion of S phase in Xenopus occurs via modulation of the tyrosine kinase that phosphorylates p34cdc2. Cell 68, 787–97.Google Scholar
Svejstrup, J.Q., Christiansen, K., Gromova, I.I., et al. (1991). New techniques for uncoupling the cleavage and religation reactions of eukaryotic topoisomerase I. The mode of action of camptothecin at a specific recognition site. J. Mol. Biol. 222, 669–78.Google Scholar
Tsao, Y.P., D'Arpa, P. & Liu, L.F. (1992). The involvement of active DNA synthesis in camptothecin-induced G2 arrest: altered regulation of p34cdc2/cyclin B. Cancer Res. 52, 1823–9.Google Scholar
Uemura, T., Ohkura, H., Adachi, Y, Morino, K., Shiozaki, K. & Yanagida, M. (1987). DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50, 917–25.Google Scholar
Walker, C. & Streisinger, G. (1983). Induction of mutagenesis by gamma-rays in pregonial germ cells of zebrafish embryos. Genetics 103, 125–36.Google Scholar
Walker, D.H., DePaoli-Roach, A.A. & Mailer, J.L. (1992). Multiple roles for protein phosphatase 1 in regulating the Xenopus early embryonic cell cycle. Mol. Biol. Cell 3, 687–98.CrossRefGoogle ScholarPubMed
Wang, Y & Burke, D.J. (1995). Checkpoint genes required to delay cell division in response to nocodazole respond to impaired Kinetochore function in the yeast Saccharomyces cerevisiae. Mol. Cell Biol. 15, 6838–44.CrossRefGoogle ScholarPubMed
Westerfield, M. (1995). The Zebrafish Book, 3rd edn. Eugene, OR: University of Oregon Press.Google Scholar
Wright, S.J. & Schatten, G. (1990). Teniposide, a topoisomerase II inhibitor, prevents chromosome condensation and separation but not decondensation in fertilized surf clam (Spisula solidissima) oocytes. Dev. Biol. 142, 224–32.Google Scholar
Zachariae, W., Shin, T.H., Galova, M., Obermaier, B. & Nasmyth, K. (1996). Identification of subunits of the anaphase-promoting complex of Saccharomyces cerevisiae. Science 274, 1201–4.Google ScholarPubMed
Zhang, Y, Wang, Z. & Ravid, K. (1996). The cell cycle in polyploid megakaryocytes is associated with reduced activity of cyclin Bl-dependent cdc2 kinase. J. Biol. Chem. 217, 4266–72.CrossRefGoogle Scholar