DOI: 10.1126/science.2683080. Directing Cell Division During Development

Directing Cell Division During Development

10.1126/science.2683080

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Several evolutionarily conserved proteins constitute a universal mitotic trigger that is precisely controlled during the orderly cell divisions of embryogenesis. As development progresses, the mechanisms controlling this trigger change. Early divisions are executed by maternally synthesized gene products, and in Xenopus they are timed by the accumulation and periodic degradation of cyclin, a trigger component. Later, the zygotic genome assumes control, and in Drosophila , zygotic transcription is required for production of another trigger protein, the product of string . After this transition to zygotic control, pulses of string transcription define the timing of highly patterned embryonic cell divisions and cyclin accumulation is not rate limiting.

Bibliography

OâFarrell, P. H., Edgar, B. A., Lakich, D., & Lehner, C. F. (1989). Directing Cell Division During Development. Science, 246(4930), 635â640.

Authors 4

Patrick H. O'Farrell (first)
Bruce A. Edgar (additional)
Delia Lakich (additional)
Christian F. Lehner (additional)

References 61 Referenced 127

AKAM, M, THE MOLECULAR-BASIS FOR METAMERIC PATTERN IN THE DROSOPHILA EMBRYO, DEVELOPMENT 101: 1 (1987). / DEVELOPMENT (1987)
ARION, D, CDC2 IS A COMPONENT OF THE M-PHASE SPECIFIC HISTONE-H1 KINASE - EVIDENCE FOR IDENTITY WITH MPF, CELL 55: 371 (1988). (10.1016/0092-8674(88)90060-8) / CELL (1988)
BISSEN, S.T., THE DURATIONS AND COMPOSITIONS OF CELL-CYCLES IN EMBRYOS OF THE LEECH, HELOBDELLA-TRISERIALIS, DEVELOPMENT 106: 105 (1989). (10.1242/dev.106.1.105) / DEVELOPMENT (1989)
BOOHER, R, INTERACTION BETWEEN CDC13+ AND CDC2+ IN THE CONTROL OF MITOSIS IN FISSION YEAST - DISSOCIATION OF THE G1-ROLE AND G2-ROLE OF THE CDC2+ PROTEIN-KINASE, EMBO JOURNAL 6: 3441 (1987). (10.1002/j.1460-2075.1987.tb02667.x) / EMBO JOURNAL (1987)
BOOHER, R.N., THE FISSION YEAST CDC2 CDC13 SUC1 PROTEIN-KINASE - REGULATION OF CATALYTIC ACTIVITY AND NUCLEAR-LOCALIZATION, CELL 58: 485 (1989). (10.1016/0092-8674(89)90429-7) / CELL (1989)
10.1038/318630a0
DNPHY, W.G., CELL 58: 181 (1989). (10.1016/0092-8674(89)90414-5) / CELL (1989)
DOE, C.Q., EARLY EVENTS IN INSECT NEUROGENESIS .1. DEVELOPMENT AND SEGMENTAL DIFFERENCES IN THE PATTERN OF NEURONAL PRECURSOR CELLS, DEVELOPMENTAL BIOLOGY 111: 193 (1985). (10.1016/0012-1606(85)90445-2) / DEVELOPMENTAL BIOLOGY (1985)
10.1016/0092-8674(88)90175-4
DRAETTA, G, CDC2 PROTEIN-KINASE IS COMPLEXED WITH BOTH CYCLIN-A AND CYCLIN-B - EVIDENCE FOR PROTEOLYTIC INACTIVATION OF MPF, CELL 56: 829 (1989). (10.1016/0092-8674(89)90687-9) / CELL (1989)
DUNPHY, W.G., THE XENOPUS CDC2 PROTEIN IS A COMPONENT OF MPF, A CYTOPLASMIC REGULATOR OF MITOSIS, CELL 54: 423 (1988). (10.1016/0092-8674(88)90205-X) / CELL (1988)
10.1016/0092-8674(86)90771-3
10.1016/0092-8674(86)90009-7
EDGAR, B.A., GENETIC-CONTROL OF CELL-DIVISION PATTERNS IN THE DROSOPHILA EMBRYO, CELL 57: 177 (1989). (10.1016/0092-8674(89)90183-9) / CELL (1989)
10.1016/0092-8674(83)90420-8
FOE, V.E., MITOTIC DOMAINS PARTITION FLY EMBRYOS, REFLECTING EARLY CELL BIOLOGICAL CONSEQUENCES OF DETERMINATION IN PROGRESS, AMERICAN ZOOLOGIST 29: 617 (1989). (10.1093/icb/29.2.617) / AMERICAN ZOOLOGIST (1989)
FOE, V.E., MITOTIC DOMAINS REVEAL EARLY COMMITMENT OF CELLS IN DROSOPHILA EMBRYOS, DEVELOPMENT 107: 1 (1989). / DEVELOPMENT (1989)
FOE, V.E., STUDIES OF NUCLEAR AND CYTOPLASMIC BEHAVIOR DURING THE 5 MITOTIC-CYCLES THAT PRECEDE GASTRULATION IN DROSOPHILA EMBRYOGENESIS, JOURNAL OF CELL SCIENCE 61: 31 (1983). (10.1242/jcs.61.1.31) / JOURNAL OF CELL SCIENCE (1983)
GARCIA-BELLIDO, A, CIBA FOUNDATION SYMPOSIUM 29: 161 (1975). / CIBA FOUNDATION SYMPOSIUM (1975)
GAUTIER, J, PURIFIED MATURATION-PROMOTING FACTOR CONTAINS THE PRODUCT OF A XENOPUS HOMOLOG OF THE FISSION YEAST-CELL CYCLE CONTROL GENE CDC2+, CELL 54: 433 (1988). (10.1016/0092-8674(88)90206-1) / CELL (1988)
GAUTIER, J, DEPHOSPHORYLATION AND ACTIVATION OF XENOPUS-P34CDC2 PROTEIN-KINASE DURING THE CELL-CYCLE, NATURE 339: 626 (1989). (10.1038/339626a0) / NATURE (1989)
GOEBL, M, CYCLIN IN FISSION YEAST, CELL 54: 739 (1988). / CELL (1988)
HAFEN, E, SPATIAL-DISTRIBUTION OF TRANSCRIPTS FROM THE SEGMENTATION GENE FUSHI-TARAZU DURING DROSOPHILA EMBRYONIC-DEVELOPMENT, CELL 37: 833 (1984). (10.1016/0092-8674(84)90418-5) / CELL (1984)
HARA, K, A CYTOPLASMIC CLOCK WITH THE SAME PERIOD AS THE DIVISION CYCLE IN XENOPUS EGGS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 77: 462 (1980). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1980)
HARTENSTEIN, V, W ROUXS ARCH 194: 181 (1985). (10.1007/BF00848246) / W ROUXS ARCH (1985)
INGHAM, P.W., THE MOLECULAR-GENETICS OF EMBRYONIC PATTERN-FORMATION IN DROSOPHILA, NATURE 335: 25 (1988). (10.1038/335025a0) / NATURE (1988)
JAN Y.N. COMMUNICATION.
JAYNES, J.B., ACTIVATION AND REPRESSION OF TRANSCRIPTION BY HOMEODOMAIN-CONTAINING PROTEINS THAT BIND A COMMON SITE, NATURE 336: 744 (1988). (10.1038/336744a0) / NATURE (1988)
JURGENS, G, W ROUX ARCH DEV BIOL 193: 283 (1984). (10.1007/BF00848157) / W ROUX ARCH DEV BIOL (1984)
10.1016/0092-8674(87)90191-7
KOBAYAKAWA, Y, TEMPORAL PATTERN OF CLEAVAGE AND THE ONSET OF GASTRULATION IN AMPHIBIAN EMBRYOS DEVELOPED FROM EGGS WITH THE REDUCED CYTOPLASM, JOURNAL OF EMBRYOLOGY AND EXPERIMENTAL MORPHOLOGY 62: 83 (1981). / JOURNAL OF EMBRYOLOGY AND EXPERIMENTAL MORPHOLOGY (1981)
LABBE, J.C., PURIFICATION OF MPF FROM STARFISH - IDENTIFICATION AS THE H-1 HISTONE KINASE P34CDC2 AND A POSSIBLE MECHANISM FOR ITS PERIODIC ACTIVATION, CELL 57: 253 (1989). (10.1016/0092-8674(89)90963-X) / CELL (1989)
10.1038/327031a0
LEHNER, C.F., EXPRESSION AND FUNCTION OF DROSOPHILA CYCLIN-A DURING EMBRYONIC-CELL CYCLE PROGRESSION, CELL 56: 957 (1989). (10.1016/0092-8674(89)90629-6) / CELL (1989)
LEHNER C.F. unpublished data.
MEIJER, L, CYCLIN IS A COMPONENT OF THE SEA-URCHIN EGG M-PHASE SPECIFIC HISTONE H-1 KINASE, EMBO JOURNAL 8: 2275 (1989). (10.1002/j.1460-2075.1989.tb08353.x) / EMBO JOURNAL (1989)
MINSHULL, J, TRANSLATION OF CYCLIN MESSENGER-RNA IS NECESSARY FOR EXTRACTS OF ACTIVATED XENOPUS EGGS TO ENTER MITOSIS, CELL 56: 947 (1989). (10.1016/0092-8674(89)90628-4) / CELL (1989)
MITA, I, TIMING OF EARLY MORPHOGENETIC EVENTS IN TETRAPLOID STARFISH EMBRYOS, JOURNAL OF EXPERIMENTAL ZOOLOGY 229: 215 (1984). (10.1002/jez.1402290206) / JOURNAL OF EXPERIMENTAL ZOOLOGY (1984)
MORENO, S, REGULATION OF P34CDC2 PROTEIN-KINASE DURING MITOSIS, CELL 58: 361 (1989). (10.1016/0092-8674(89)90850-7) / CELL (1989)
MORTA, A.O., CELL 58: 193 (1989). (10.1016/0092-8674(89)90415-7) / CELL (1989)
MURRAY, A.W., CYCLIN SYNTHESIS DRIVES THE EARLY EMBRYONIC-CELL CYCLE, NATURE 339: 275 (1989). (10.1038/339275a0) / NATURE (1989)
MURRAY, A.W., THE ROLE OF CYCLIN SYNTHESIS AND DEGRADATION IN THE CONTROL OF MATURATION PROMOTING FACTOR ACTIVITY, NATURE 339: 280 (1989). (10.1038/339280a0) / NATURE (1989)
10.1126/science.2683077
10.1016/0092-8674(82)90272-0
10.1016/0092-8674(82)90273-2
10.1038/287795a0
10.1126/science.2683075
READY, D.F., DEVELOPMENT OF DROSOPHILA RETINA, A NEUROCRYSTALLINE LATTICE, DEVELOPMENTAL BIOLOGY 53: 217 (1976). (10.1016/0012-1606(76)90225-6) / DEVELOPMENTAL BIOLOGY (1976)
RUSSELL, P, CDC25+ FUNCTIONS AS AN INDUCER IN THE MITOTIC CONTROL OF FISSION YEAST, CELL 45: 145 (1986). (10.1016/0092-8674(86)90546-5) / CELL (1986)
10.1016/0092-8674(87)90458-2
SCOTT, M.P., SPATIAL PROGRAMMING OF GENE-EXPRESSION IN EARLY DROSOPHILA EMBRYOGENESIS, ANNUAL REVIEW OF CELL BIOLOGY 2: 49 (1986). (10.1146/annurev.cb.02.110186.000405) / ANNUAL REVIEW OF CELL BIOLOGY (1986)
SIGNORET, J, ANNALS OF EMBRYOLOGY AND MORPHOLOGY 4: 113 (1971). / ANNALS OF EMBRYOLOGY AND MORPHOLOGY (1971)
SLUDER, G.F., DEV BIOL 24: 248 (1986). / DEV BIOL (1986)
SOLOMON, M, CYCLIN IN FISSION YEAST, CELL 54: 738 (1988). (10.1016/S0092-8674(88)90933-6) / CELL (1988)
STEWARD, R, THE DORSAL PROTEIN IS DISTRIBUTED IN A GRADIENT IN EARLY DROSOPHILA EMBRYOS, CELL 55: 487 (1988). (10.1016/0092-8674(88)90035-9) / CELL (1988)
SWENSON, K.I., THE CLAM EMBRYO PROTEIN CYCLIN-A INDUCES ENTRY INTO M-PHASE AND THE RESUMPTION OF MEIOSIS IN XENOPUS OOCYTES, CELL 47: 861 (1986). (10.1016/0092-8674(86)90801-9) / CELL (1986)
TAUTZ, D, A NON-RADIOACTIVE INSITU HYBRIDIZATION METHOD FOR THE LOCALIZATION OF SPECIFIC RNAS IN DROSOPHILA EMBRYOS REVEALS TRANSLATIONAL CONTROL OF THE SEGMENTATION GENE HUNCHBACK, CHROMOSOMA 98: 81 (1989). (10.1007/BF00291041) / CHROMOSOMA (1989)
TEARLE R COMMUNICATION.
WESTENDORF, J.M., THE ROLE OF CYCLIN-B IN MEIOSIS-I, JOURNAL OF CELL BIOLOGY 108: 1431 (1989). (10.1083/jcb.108.4.1431) / JOURNAL OF CELL BIOLOGY (1989)
WHITFIELD, WGF, TRANSCRIPTS OF ONE OF 2 DROSOPHILA CYCLIN GENES BECOME LOCALIZED IN POLE CELLS DURING EMBRYOGENESIS, NATURE 338: 337 (1989). (10.1038/338337a0) / NATURE (1989)
WOODLAND, H, THE TRANSLATIONAL CONTROL PHASE OF EARLY DEVELOPMENT - REVIEW, BIOSCIENCE REPORTS 2: 471 (1982). (10.1007/BF01115246) / BIOSCIENCE REPORTS (1982)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 5:21 p.m.)
Deposited	1 year, 7 months ago (Jan. 12, 2024, 3:59 p.m.)
Indexed	2 months, 2 weeks ago (June 5, 2025, 6:30 a.m.)
Issued	35 years, 9 months ago (Nov. 3, 1989)
Published	35 years, 9 months ago (Nov. 3, 1989)
Published Print	35 years, 9 months ago (Nov. 3, 1989)

Funders 0

None

BibTeX

@article{O_Farrell_1989, title={Directing Cell Division During Development}, volume={246}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.2683080}, DOI={10.1126/science.2683080}, number={4930}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={O’Farrell, Patrick H. and Edgar, Bruce A. and Lakich, Delia and Lehner, Christian F.}, year={1989}, month=nov, pages={635–640} }

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