p21 Waf1/Cip1 Inhibition of Cyclin E/Cdk2 Activity Prevents Endoreduplication after Mitotic Spindle Disruption

Stewart, Zoe A.; Leach, Steven D.; Pietenpol, Jennifer A.

doi:10.1128/mcb.19.1.205

Cited by 168Cancer-related Molecular PathwaysMicrotubule and mitosis dynamicsDNA Repair Mechanisms

p21 Waf1/Cip1 Inhibition of Cyclin E/Cdk2 Activity Prevents Endoreduplication after Mitotic Spindle Disruption

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Stewart, Zoe A., Leach, Steven D., Pietenpol, Jennifer A.·1999·Molecular and Cellular Biology

DOI 10.1128/mcb.19.1.205PMC PMC83879

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Abstract

During a normal cell cycle, entry into S phase is dependent on completion of mitosis and subsequent activation of cyclin-dependent kinases (Cdks) in G1. These events are monitored by checkpoint pathways. Recent studies and data presented herein show that after treatment with microtubule inhibitors (MTIs), cells deficient in the Cdk inhibitor p21(Waf1/Cip1) enter S phase with a >/=4N DNA content, a process known as endoreduplication, which results in polyploidy. To determine how p21 prevents MTI-induced endoreduplication, the G1/S and G2/M checkpoint pathways were examined in two isogenic cell systems: HCT116 p21(+/+) and p21(-/-) cells and H1299 cells containing an inducible p21 expression vector (HIp21). Both HCT116 p21(-/-) cells and noninduced HIp21 cells endoreduplicated after MTI treatment. Analysis of G1-phase Cdk activities demonstrated that the induction of p21 inhibited endoreduplication through direct cyclin E/Cdk2 regulation. The kinetics of p21 inhibition of cyclin E/Cdk2 activity and binding to proliferating-cell nuclear antigen in HCT116 p21(+/+) cells paralleled the onset of endoreduplication in HCT116 p21(-/-) cells. In contrast, loss of p21 did not lead to deregulated cyclin D1-dependent kinase activities, nor did p21 directly regulate cyclin B1/Cdc2 activity. Furthermore, we show that MTI-induced endoreduplication in p53-deficient HIp21 cells was due to levels of p21 protein below a threshold required for negative regulation of cyclin E/Cdk2, since ectopic expression of p21 restored cyclin E/Cdk2 regulation and prevented endoreduplication. Based on these findings, we propose that p21 plays an integral role in the checkpoint pathways that restrain normal cells from entering S phase after aberrant mitotic exit due to defects in microtubule dynamics.

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Mdm2 expression can lead to degradation of p21, and loss of p21 results in endoreduplication and polyploid cells.
“Moreover, Mdm2 expression can lead to the degradation of the p53 transcriptional target gene and cell cycle inhibitor p21, and loss of p21 results in endoreduplication and polyploid cells (Jin et al., 2003, Stewart et al., 1999).”
From Aging mice have increased chromosome instability that is exacerbated by elevated Mdm2 expression (2011) · cites this paper as Stewart et al., 1999

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Authors: Stewart, Z. A., Leach, S. D., & Pietenpol, J. A.
Affiliations: Vanderbilt University (US)
ORCID: Stewart, Zoe A.
Leach, Steven D.
Pietenpol, Jennifer A.
Venue: Molecular and Cellular Biology
Publisher: Informa UK Limited
Published: 1999-01
Volume: 19
Issue: 1
Pages: 205-215
ISSN: 0270-7306 (ISSN-L)
1098-5549
DOI: 10.1128/mcb.19.1.205
PMC: PMC83879
OpenAlex: W2099682050
Cited by: 168
References: 65
Citations by year: 2026: 1 · 2024: 2 · 2023: 2 · 2022: 1 · 2021: 3 · 2020: 3 · 2018: 2 · 2017: 4 · 2016: 5 · 2015: 6 · 2014: 9 · 2013: 6 · 2012: 2
FWCI: 7.45
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Molecular and Cellular Biology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (ES00267, CA68485)
National Cancer Institute (R01CA070856, CA70856, P30CA068485)
National Institute of General Medical Sciences (GM 07347, T32GM007347)
National Institute of Environmental Health Sciences (P30ES000267, ES00267)
Topics: Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Keywords: p21, cyclin E/CDK2, endoreduplication, mitotic spindle disruption, microtubule inhibitors, G1/S checkpoint, G2/M checkpoint, polyploidy, p53 deficiency, proliferating cell nuclear antigen, cell cycle checkpoints
MeSH terms: DNA Replication, Enzyme Inhibitors, Humans, Spindle Apparatus, Proto-Oncogene Proteins, Tumor Cells, Cultured, Tumor Suppressor Protein p53, G1 Phase, S Phase, Cyclins, Mutagenesis, Protein Serine-Threonine Kinases, Proliferating Cell Nuclear Antigen, Cyclin-Dependent Kinases, Cyclin B, Cyclin E, CDC2-CDC28 Kinases, Cyclin-Dependent Kinase Inhibitor p21, Cyclin-Dependent Kinase 2, Cyclin-Dependent Kinase 4, Cyclin-Dependent Kinase 6, Cyclin B1

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p21 Waf1/Cip1 Inhibition of Cyclin E/Cdk2 Activity Prevents Endoreduplication after Mitotic Spindle Disruption

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