Student or educator? Sign up with your school email and get 6 months of Pro free.
Cited by 3,021

The DOI matches its Crossref record.

Checkpoints: Controls That Ensure the Order of Cell Cycle Events

Hartwell, Leland H., Weinert, Ted A.·1989·Science

Abstract

The events of the cell cycle of most organisms are ordered into dependent pathways in which the initiation of late events is dependent on the completion of early events. In eukaryotes, for example, mitosis is dependent on the completion of DNA synthesis. Some dependencies can be relieved by mutation (mitosis may then occur before completion of DNA synthesis), suggesting that the dependency is due to a control mechanism and not an intrinsic feature of the events themselves. Control mechanisms enforcing dependency in the cell cycle are here called checkpoints. Elimination of checkpoints may result in cell death, infidelity in the distribution of chromosomes or other organelles, or increased susceptibility to environmental perturbations such as DNA damaging agents. It appears that some checkpoints are eliminated during the early embryonic development of some organisms; this fact may pose special problems for the fidelity of embryonic cell division.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1126/science.2683079

Cites

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

No references could be resolved yet.

Research works printed but not linked: 86

  1. BAJER, A, CINE-MICROGRAPHIC STUDIES ON MITOSIS IN ENDOSPERM .2. CHROMOSOME, CYTOPLASMIC AND BROWNIAN MOVEMENTS, CHROMOSOMA 7: 558 (1956).
  2. BAKER, B.S., PROG TOP CYTOGENET 7: 273 (1987).
  3. BARBER, H.N., PROCEEDINGS OF THE ROYAL SOCIETY OF LONDON. SERIES B 131: 258 (1942).
  4. BARKER, D. G., MOLECULAR & GENERAL GENETICS 200: 458 (1985). · DOI
  5. BAUM, P, A YEAST GENE ESSENTIAL FOR REGULATION OF SPINDLE POLE DUPLICATION, MOLECULAR AND CELLULAR BIOLOGY 8: 5386 (1988).
  6. BAUM, P, YEAST GENE REQUIRED FOR SPINDLE POLE BODY DUPLICATION - HOMOLOGY OF ITS PRODUCT WITH CA-2+-BINDING PROTEINS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 83: 5512 (1986).
  7. Berget, P. B., Bacteriophage T4: 246 (1983).
  8. Berget, P., Virus Structure and Assembly: 149 (1985).
  9. BIRKY, C. W., INTERNATIONAL REVIEW OF CYTOLOGY 15: 49 (1983).
  10. 10.1126/science.3541204 · DOI · Paper page
  11. BLOW, J.J., A ROLE FOR THE NUCLEAR-ENVELOPE IN CONTROLLING DNA-REPLICATION WITHIN THE CELL-CYCLE, NATURE 332: 546 (1988). · DOI · Paper page
  12. BRIGGS, R, JOURNAL OF EXPERIMENTAL ZOOLOGY 116: 455 (1951). · doi:10.1002/jez.1401160307
  13. BUDD, M, TEMPERATURE-SENSITIVE MUTATIONS IN THE YEAST DNA-POLYMERASE-I GENE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 84: 2838 (1987).
  14. BURNS, V. W., RADIATION RESEARCH 4: 394 (1956). · DOI
  15. BUSSE, P.M., ACTION OF CAFFEINE ON X-IRRADIATED HELA-CELLS .3. ENHANCEMENT OF X-RAY-INDUCED KILLING DURING G2 ARREST, RADIATION RESEARCH 76: 292 (1978). · DOI
  16. Byers, B., Cold Spring Harbor Symposia on Quantitative Biology 38: 123 (1974). · DOI · Paper page
  17. CARLSON, J.G., Some effects of x- radiation on the neuroblast chromosomes of the grasshopper, Chortophaga viridifasciata, GENETICS 23: 596 (1938). · doi:10.1093/genetics/23.6.596
  18. CULOTTI, J, GENETIC CONTROL OF CELL DIVISION CYCLE IN YEAST .3. 7 GENES CONTROLLING NUCLEAR DIVISION, EXPERIMENTAL CELL RESEARCH 67: 389 (1971). · DOI
  19. 10.1016/0092-8674(86)90009-7 · DOI · Paper page
  20. Epstein C. J. The Consequences of Chromosome Imbalance: Principles Mechanisms and Models 18 (1986). · DOI · Paper page
  21. FREEMAN, M, THE DISSOCIATION OF NUCLEAR AND CENTROSOMAL DIVISION IN GNU, A MUTATION CAUSING GIANT NUCLEI IN DROSOPHILA, CELL 46: 457 (1986). · DOI · Paper page
  22. GASSER, S.M., A GLIMPSE AT CHROMOSOMAL ORDER, TRENDS IN GENETICS 3: 16 (1987). · DOI · Paper page
  23. GRANT, S.G., MECHANISMS OF X-CHROMOSOME REGULATION, ANNUAL REVIEW OF GENETICS 22: 199 (1988). · DOI
  24. 10.1016/0092-8674(87)90237-6 · DOI
  25. Hand, R., Cell Biology: A Comprehensive Treatise 2: 389 (1979).
  26. Hara, K., Proceedings of the National Academy of Sciences of the United States of America 77: 462 (1980).
  27. Hirano, T., Molecular and Cell Biology of Yeasts: 223 (1988).
  28. HOLLIDAY, R, CHROMOSOME ERROR PROPAGATION AND CANCER, TRENDS IN GENETICS 5: 42 (1989). · DOI
  29. HOLM, C, DNA TOPOISOMERASE-II IS REQUIRED AT THE TIME OF MITOSIS IN YEAST, CELL 41: 553 (1985). · DOI · Paper page
  30. HOWE, W.E., PRODUCTION OF CELLS WITHOUT DEOXYRIBONUCLEIC-ACID DURING THYMIDINE STARVATION OF LEXA CULTURES OF ESCHERICHIA-COLI-K-12, JOURNAL OF BACTERIOLOGY 124: 1113 (1975). · DOI
  31. HUFFAKER, T.C., DIVERSE EFFECTS OF BETA-TUBULIN MUTATIONS ON MICROTUBULE FORMATION AND FUNCTION, JOURNAL OF CELL BIOLOGY 106: 1997 (1988). · DOI · Paper page
  32. JAFFE, A, SOS-INDEPENDENT COUPLING BETWEEN DNA-REPLICATION AND CELL-DIVISION IN ESCHERICHIA-COLI, JOURNAL OF BACTERIOLOGY 165: 66 (1986). · DOI
  33. JAFFE, E, DOSAGE COMPENSATION IN DROSOPHILA, TRENDS IN GENETICS 2: 316 (1986). · doi:10.1016/0168-9525(86)90287-8
  34. JOHNSTON, L.H., SACCHAROMYCES-CEREVISIAE CELL-CYCLE MUTANT CDC9 IS DEFECTIVE IN DNA-LIGASE, NATURE 274: 891 (1978). · DOI · Paper page
  35. KILLIAN, C.E., EFFECTS OF APHIDICOLIN ON PREMATURE CONDENSATION OF SPERM CHROMOSOMES IN FERTILIZED SEA-URCHIN EGGS, EXPERIMENTAL CELL RESEARCH 158: 519 (1985). · doi:10.1016/0014-4827(85)90475-6
  36. 10.1016/0092-8674(87)90191-7 · DOI · Paper page
  37. Kornberg A. DNA Replication (1988). · DOI
  38. 10.1126/science.3317838 · DOI
  39. KUHN, E.M., CYTOGENETICS OF BLOOMS SYNDROME, CANCER GENETICS AND CYTOGENETICS 22: 1 (1986). · DOI
  40. KURIYAMA, R, JOURNAL OF CELL BIOLOGY 91: 814 (1981). · DOI · Paper page
  41. LAEMMLI, U.K., FORM-DETERMINING FUNCTION OF GENES REQUIRED FOR ASSEMBLY OF HEAD OF BACTERIOPHAGE-T4, JOURNAL OF MOLECULAR BIOLOGY 49: 99 (1970). · DOI
  42. 10.1126/science.2683076 · DOI · Paper page
  43. Lau, C. C., Proceedings of the National Academy of Sciences of the United States of America 79: 2942 (1982).
  44. LAU, Y.F., STUDIES OF MAMMALIAN CHROMOSOME-REPLICATION .2. EVIDENCE FOR THE EXISTENCE OF DEFINED CHROMOSOME REPLICATING UNITS, CHROMOSOMA 83: 721 (1981). · DOI
  45. LITTLE, J.W., THE SOS REGULATORY SYSTEM OF ESCHERICHIA-COLI, CELL 29: 11 (1982). · DOI · Paper page
  46. LUCKEHUHLE, C, DRASTIC G2 ARREST IN MAMMALIAN-CELLS AFTER IRRADIATION WITH HEAVY-ION BEAMS, RADIATION RESEARCH 79: 97 (1979). · DOI
  47. MAZIA, D, THE CHROMOSOME CYCLE AND THE CENTROSOME CYCLE IN THE MITOTIC-CYCLE, INTERNATIONAL REVIEW OF CYTOLOGY-A SURVEY OF CELL BIOLOGY 100: 49 (1987).
  48. McIntosh, J. R., Aneuploidy: Etiology and Mechanisms: 197 (1985).
  49. MCINTOSH, J.R., MODERN CELL BIOLOGY 2: 115 (1983).
  50. Minden, J. S., Journal of Cell Biology 109: 505 (1989). · DOI
  51. MITCHISON, J.M., GROWTH IN CELL LENGTH IN THE FISSION YEAST SCHIZOSACCHAROMYCES-POMBE, JOURNAL OF CELL SCIENCE 75: 357 (1985). · DOI
  52. MITCHISON, T.J., MICROTUBULE DYNAMICS AND KINETOCHORE FUNCTION IN MITOSIS, ANNUAL REVIEW OF CELL BIOLOGY 4: 527 (1988). · DOI · Paper page
  53. MITELMAN, F, RESTRICTED NUMBER OF CHROMOSOMAL REGIONS IMPLICATED IN ETIOLOGY OF HUMAN CANCER AND LEUKEMIA, NATURE 310: 325 (1984). · doi:10.1038/310325a0
  54. MURIALDO, H, SYNTHESIS OF A TRANS-ACTING INHIBITOR OF DNA MATURATION BY PROHEAD MUTANTS OF PHAGE-LAMBDA, GENETICS 115: 3 (1987). · doi:10.1093/genetics/115.1.3
  55. 10.1126/science.2683077 · DOI · Paper page
  56. NEWLON, C.S., YEAST CHROMOSOME-REPLICATION AND SEGREGATION, MICROBIOLOGICAL REVIEWS 52: 568 (1988). · doi:10.1128/mr.52.4.568-601.1988 · Paper page
  57. NEWPORT, J.W., THE NUCLEUS - STRUCTURE, FUNCTION, AND DYNAMICS, ANNUAL REVIEW OF BIOCHEMISTRY 56: 535 (1987). · doi:10.1146/annurev.bi.56.070187.002535
  58. NISHIMOTO, T, THE SYNTHESIS OF PROTEIN(S) FOR CHROMOSOME CONDENSATION MAY BE REGULATED BY A POST-TRANSCRIPTIONAL MECHANISM, JOURNAL OF CELLULAR PHYSIOLOGY 109: 299 (1981). · DOI
  59. Ogura, T., Proceedings of the National Academy of Sciences of the United States of America 80: 4784 (1983).
  60. OLIVIERI, G, MITOTIC DELAY AND REPAIR IN HUMAN-LYMPHOCYTES, MUTATION RESEARCH 122: 65 (1983).
  61. 10.1016/0092-8674(88)90513-2 · DOI · Paper page
  62. PAINTER, R.B., FORMATION OF NASCENT DNA-MOLECULES DURING INHIBITION OF REPLICON INITIATION IN MAMMALIAN-CELLS, BIOCHIMICA ET BIOPHYSICA ACTA 418: 146 (1976). · DOI
  63. PAINTER, R.B., KROC FOUNDATION SERIES 19: 89 (1985).
  64. Painter, R. B., Proceedings of the National Academy of Sciences of the United States of America 77: 7315 (1980).
  65. POVIRK, L.F., LOCALIZATION OF INHIBITION OF REPLICON INITIATION TO DAMAGED REGIONS OF DNA, JOURNAL OF MOLECULAR BIOLOGY 114: 141 (1977). · doi:10.1016/0022-2836(77)90288-1
  66. Pringle, J. R., Molecular Biology of the Yeast Saccharomyces: Life Cycle and Inheritance 1: 97 (1981).
  67. RAFF, J.W., NUCLEAR AND CYTOPLASMIC MITOTIC-CYCLES CONTINUE IN DROSOPHILA EMBRYOS IN WHICH DNA-SYNTHESIS IS INHIBITED WITH APHIDICOLIN, JOURNAL OF CELL BIOLOGY 107: 2009 (1988). · DOI · Paper page
  68. Rao, P. N., Premature Chromosome Condensation: Application in Basic, Clinical and Mutation Research: 1 (1982).
  69. RATTNER, J.B., INDEPENDENCE OF CENTRIOLE FORMATION AND DNA-SYNTHESIS, JOURNAL OF CELL BIOLOGY 57: 359 (1973). · DOI
  70. ROSE, M.D., KAR1, A GENE REQUIRED FOR FUNCTION OF BOTH INTRANUCLEAR AND EXTRANUCLEAR MICROTUBULES IN YEAST, CELL 48: 1047 (1987). · DOI · Paper page
  71. 10.1016/0092-8674(87)90458-2 · DOI · Paper page
  72. SCHIERENBERG, E, CONTROL OF CELL-CYCLE TIMING IN EARLY EMBRYOS OF CAENORHABDITIS-ELEGANS, DEVELOPMENTAL BIOLOGY 107: 337 (1985). · DOI
  73. SCHIESTL, R.H., CLONING AND SEQUENCE-ANALYSIS OF THE SACCHAROMYCES-CEREVISIAE RAD9 GENE AND FURTHER EVIDENCE THAT ITS PRODUCT IS REQUIRED FOR CELL-CYCLE ARREST INDUCED BY DNA DAMAGE, MOLECULAR AND CELLULAR BIOLOGY 9: 1882 (1989).
  74. SCHNEIDERMINDER, A, CYTOLOGISCHE UNTERSUCHUNG DER EMBRYONALENTWICKLUNG VON DROSOPHILA MELANOGASTER NACH RONTGENBESTRAHLUNG IN FRUHEN ENTWICKLUNGSSTADIEN, INTERNATIONAL JOURNAL OF RADIATION BIOLOGY AND RELATED STUDIES IN PHYSICS CHEMISTRY AND MEDICINE 11: 1 (1966).
  75. SHILOH, Y, KROC FOUNDATION SERIES 19: 111 (1985).
  76. SITNEY, K.C., DNA POLYMERASE-III, A 2ND ESSENTIAL DNA-POLYMERASE, IS ENCODED BY THE S-CEREVISIAE CDC2 GENE, CELL 56: 599 (1989). · DOI
  77. SLUDER, G, THE REPRODUCTION OF CENTROSOMES - NUCLEAR VERSUS CYTOPLASMIC CONTROLS, JOURNAL OF CELL BIOLOGY 103: 1873 (1986). · DOI
  78. Sullivan, W, Development 110: 311 (1990). · doi:10.1242/dev.110.2.311
  79. THOMAS, J.H., A GENE REQUIRED FOR THE SEPARATION OF CHROMOSOMES ON THE SPINDLE APPARATUS IN YEAST, CELL 44: 65 (1986). · DOI
  80. WALKER, G.C., MUTAGENESIS AND INDUCIBLE RESPONSES TO DEOXYRIBONUCLEIC-ACID DAMAGE IN ESCHERICHIA-COLI, MICROBIOLOGICAL REVIEWS 48: 60 (1984). · doi:10.1128/mr.48.1.60-93.1984 · Paper page
  81. WANG, R.J., FURTHER-STUDIES ON A MUTANT MAMMALIAN-CELL LINE DEFECTIVE IN MITOSIS, EXPERIMENTAL CELL RESEARCH 101: 331 (1976). · doi:10.1016/0014-4827(76)90385-2
  82. WATANABE, I, RADIATION EFFECTS ON DNA CHAIN GROWTH IN MAMMALIAN-CELLS, RADIATION RESEARCH 58: 541 (1974). · DOI
  83. 10.1126/science.2422760 · DOI · Paper page
  84. 10.1126/science.3291120 · DOI · Paper page
  85. 10.1126/science.6336310 · DOI · Paper page
  86. ZIRKLE, R.E., ULTRAVIOLET-MICROBEAM IRRADIATION OF NEWT-CELL CYTOPLASM - SPINDLE DESTRUCTION, FALSE ANAPHASE, AND DELAY OF TRUE ANAPHASE, RADIATION RESEARCH 41: 516 (1970). · doi:10.2307/3572841

Cited by

See all 3,021

Metadata

Authors
Hartwell, L. H., & Weinert, T. A.
Venue
Science
Published
1989-11-03
Volume
246
Issue
4930
Pages
629-634
ISSN
  • 0036-8075 (ISSN-L)
  • 1095-9203
OpenAlex
W2004008931
Cited by
3,021
References
0
FWCI
29.39
Type
journal article
Language
en
Open access
closed

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Checkpoints: Controls That Ensure the Order of Cell Cycle Events. https://app.cochat.ai/papers/10.1126/science.2683079
The paper
Hartwell, L. H., & Weinert, T. A. (1989). Checkpoints: Controls That Ensure the Order of Cell Cycle Events. Science. https://doi.org/10.1126/science.2683079

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.