DOI: 10.1242/dev.120.11.3131. Transcriptional regulation of <i>string (cdc25)</i>: a link between developmental programming and the cell cycle

Transcriptional regulation of string (cdc25): a link between developmental programming and the cell cycle

10.1242/dev.120.11.3131

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT During postblastoderm embryogenesis in Drosophila, cell cycles progress in an invariant spatiotemporal pattern. Most of these cycles are differentially timed by bursts of transcription of string (cdc25), a gene encoding a phosphatase that triggers mitosis by activating the Cdc2 kinase. An analysis of string expression in 36 pattern-formation mutants shows that known patterning genes act locally to influence string transcription. Embryonic expression of string gene fragments shows that the complete pattern of string transcription requires extensive cis-acting regulatory sequences (&gt;15.3 kb), but that smaller segments of this regulatory region can drive proper temporal expression in defined spatial domains. We infer that string upstream sequences integrate many local signals to direct string’s transcriptional program. Finally, we show that the spatiotemporal progression of string transcription is largely unaffected in mutant embryos specifically arrested in G2 of cycles 14, 15, or 16, or G1 of cycle 17. Thus, there is a regulatory hierarchy in which developmental inputs, not cell cycle inputs, control the timing of string transcription and hence cell cycle progression.

Bibliography

Edgar, B. A., Lehman, D. A., & OâFarrell, P. H. (1994). Transcriptional regulation of string (cdc25): a link between developmental programming and the cell cycle. Development, 120(11), 3131â3143.

Authors 3

Bruce A. Edgar (first)
Dara A. Lehman (additional)
Patrick H. O’Farrell (additional)

References 47 Referenced 162

10.1242/dev.114.4.1003 / Development / Altered mitotic domains reveal fate map changes in Drosophila embryos mutant for zygotic dorsoventral patterning genes by Arora (1992)
{'year': '1989', 'author': 'Ashburner', 'key': '2024121723550728800_DEVELOP_120_11_3131C2'} by Ashburner (1989)
{'volume-title': 'The Development of Drosophila melanogaster', 'year': '1993', 'author': 'Bate', 'key': '2024121723550728800_DEVELOP_120_11_3131C3'} / The Development of Drosophila melanogaster by Bate (1993)
10.1016/0896-6273(89)90112-8 / Neuron / Neurogenesis of the Peripheral Nervous System in Drosophila Embryos: DNA Replication Patterns and Cell Lineages by Bodmer (1989)
10.1038/330395a0 / Nature / The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers by Boulay (1987)
10.1007/978-3-662-02454-6 / The Embryonic Development of Drosophila melanogaster by Campos-Ortega (1985)
10.1016/0092-8674(94)90384-0 / Cell / A putative cell signal encoded by the folded gastrulation gene coordinates cell shape changes during Drosophila gastrulation by Costa (1994)
10.1242/dev.120.6.1503 / Development / Developmental control of a G1-S transcriptional program in Drosophila by Duronio (1994)
10.1016/0092-8674(89)90183-9 / Cell / Genetic control of cell division patterns in the Drosophila embryo by Edgar (1989)
10.1016/0092-8674(90)90012-4 / Cell / The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2 by string by Edgar (1990)
10.1101/gad.8.4.440 / Genes Dev / Distinct molecular mechanisms regulate cell cycle timing at successive stages of Drosophila Embryogenesis by Edgar (1994)
10.1242/dev.107.1.1 / Development / Mitotic domains reveal early commitment of cells in Drosophila embryos by Foe (1989)
10.1093/icb/29.2.617 / Am. J. Zool / Mitotic domains partition fly embryos, reflecting early biological consequences of determination in progress by Foe (1989)
{'key': '2024121723550728800_DEVELOP_120_11_3131C14', 'first-page': '149', 'volume-title': 'Mitosis and morphogenesis in the Drosophila embryo: Point and counterpoint', 'author': 'Foe', 'year': '1993'} / Mitosis and morphogenesis in the Drosophila embryo: Point and counterpoint by Foe (1993)
10.1016/0092-8674(91)90583-K / Cell / Cdc25 is a specific tyrosine phosphatase that directly activates p34cdc2 by Gautier (1991)
10.1242/dev.110.4.1319 / Development / Blocking cell division does not remove the requirement for Polycomb function in Drosophila embryogenesis by Gould (1990)
10.1007/BF00848246 / Wilelm Roux Arch. Dev. Biol / Fate-mapping in wild-type Drosophila melanogaster I. The spatio-temporal pattern of embryonic cell divisions by Hartenstein (1985)
10.1016/0012-1606(90)90184-K / Dev. Biol / Sensillum development in the absence of cell division: The sensillum phenotype of the Drosophila mutant string by Hartenstein (1990)
10.1007/BF00848157 / Roux’s Arch. Dev. Biol / Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the third chromosome by Jürgens (1984)
10.1101/gad.6.4.578 / Genes Dev / A mouse cdc25 homolog is differentially and developmentally expressed by Kakizuka (1992)
10.1073/pnas.89.8.3414 / Proc. Natl. Acad. Sci. USA / Dorsal-ventral patterning in Drosophila: DNA binding of snail protein to the single-minded gene by Kasai (1992)
10.1002/j.1460-2075.1993.tb05632.x / EMBO J / Synergistic action of Drosophila cyclins A and B during the G2-M transition by Knoblich (1993)
10.1016/0092-8674(94)90239-9 / Cell / Cyclin E controls progression through S-phase and its downregulation during Drosophila embryogenesis is required for the arrest of cell proliferation by Knoblich (1994)
10.1016/0092-8674(91)90315-P / Cell / The cdc25 protein controls tyrosine dephosporylation of the cdc2 protein in a cell-free system by Kumagai (1991)
{'volume-title': 'The Making of a Fly: The Genetics of Animal Design', 'year': '1992', 'author': 'Lawrence', 'key': '2024121723550728800_DEVELOP_120_11_3131C25'} / The Making of a Fly: The Genetics of Animal Design by Lawrence (1992)
10.1016/0092-8674(89)90629-6 / Cell / Expression and function of Drosophila cyclin A during embryonic cell cycle progression by Lehner (1989)
10.1016/0092-8674(90)90535-M / Cell / The roles of Drosophila cyclins A and B in mitotic control by Lehner (1990)
{'key': '2024121723550728800_DEVELOP_120_11_3131C28', 'first-page': '3573', 'volume': '9', 'author': 'Lehner', 'year': '1990', 'journal-title': 'Drosophila cdc2 homologs: a functional homolog is coexpressed with a cognate variant. EMBO J'} / Drosophila cdc2 homologs: a functional homolog is coexpressed with a cognate variant. EMBO J by Lehner (1990)
10.1016/0092-8674(92)90177-E / Cell / The cdc25 M-phase inducer: An unconventional phosphatase by Millar (1992)
10.1038/344549a0 / Nature / Regulation of mitosis by cyclic accumulation of p80cdc25 mitotic inducer in fission yeast by Moreno (1990)
10.1016/0092-8674(91)90292-7 / Cell / The Drosophila single-minded gene encodes a helix-loop-helix protein that acts as a master regulator of CNS midline development by Nambu (1991)
10.1016/0955-0674(93)90101-U / Current Opin. Cell Biol / Targets of cyclin-dependent protein kinases by Nigg (1993)
10.1007/BF00848156 / Roux’s Arch. Dev. Biol / Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster by Nüsslein-Volhard (1984)
10.1126/science.2683080 / Science / Directing cell division during development by O’Farrell (1989)
{'volume-title': 'Blastoderm Segmentation', 'year': '1993', 'author': 'Pankratz', 'key': '2024121723550728800_DEVELOP_120_11_3131C35'} / Blastoderm Segmentation by Pankratz (1993)
10.1242/dev.119.3.673 / Development / A Drosophila G1-specific cyclin E homolog exhibits different modes of expression during embryogenesis by Richardson (1993)
{'key': '2024121723550728800_DEVELOP_120_11_3131C37', 'first-page': '137', 'article-title': 'Dorsal ventral polarity and pattern formation in the Drosophila embryo', 'volume': '1', 'author': 'Rushlow', 'year': '1990', 'journal-title': 'Sem. in Cell Biol'} / Sem. in Cell Biol / Dorsal ventral polarity and pattern formation in the Drosophila embryo by Rushlow (1990)
10.1073/pnas.87.13.5139 / Proc. Natl. Acad. Sci. USA / Cdc25Hs, a putative mitotic inducer gene in human cells, is predominantly expressed in G2 by Sadhu (1990)
10.1016/S0959-437X(05)80079-6 / Curr. Opin. Genet. Devel / The initiation of pair-rule stripes in the Drosophila blastoderm by Small (1991)
10.1002/j.1460-2075.1992.tb05498.x / EMBO J / Regulation of even-skipped stripe 2 in the Drosophila embryo by Small (1992)
{'key': '2024121723550728800_DEVELOP_120_11_3131C41', 'first-page': '175', 'volume-title': 'P-element-mediated transformation', 'author': 'Spradling', 'year': '1986'} / P-element-mediated transformation by Spradling (1986)
10.1242/dev.117.1.219 / Development / Genetic analysis of the Drosophila cdc2 homolog by Stern (1993)
10.1007/BF00291041 / Chromosoma / A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback by Tautz (1989)
10.1101/gad.1.7.709 / Genes Dev / Genes of the Drosophila maternal dorsal group control the specific expression of the zygotic gene twist in presumptive mesodermal cells by Thisse (1987)
10.1002/j.1460-2075.1988.tb03056.x / EMBO J / Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos by Thisse (1988)
10.1007/BF00848158 / Roux’s Arch. Dev. Biol / Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. III. Zygotic loci on the X-chromosome and fourth chromosome by Wieschaus (1984)
10.1038/366690a0 / Nature / A Drosophila homolog of human Sp1 is a head-specific segmentation gene by Wimmer (1993)

Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 9:57 p.m.)
Deposited	8 months, 2 weeks ago (Dec. 17, 2024, 6:56 p.m.)
Indexed	21 hours, 39 minutes ago (Sept. 3, 2025, 6:05 a.m.)
Issued	30 years, 10 months ago (Nov. 1, 1994)
Published	30 years, 10 months ago (Nov. 1, 1994)
Published Online	30 years, 10 months ago (Nov. 1, 1994)
Published Print	30 years, 10 months ago (Nov. 1, 1994)

Funders 0

None

BibTeX

@article{Edgar_1994, title={Transcriptional regulation of string (cdc25): a link between developmental programming and the cell cycle}, volume={120}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.120.11.3131}, DOI={10.1242/dev.120.11.3131}, number={11}, journal={Development}, publisher={The Company of Biologists}, author={Edgar, Bruce A. and Lehman, Dara A. and O’Farrell, Patrick H.}, year={1994}, month=nov, pages={3131–3143} }

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