Abstract
We previously reported that the p53 tumor suppressor protein plays an essential role in the induction of tetraploid G1 arrest in response to perturbation of the actin cytoskeleton, termed actin damage. In this study, we investigated the role of p53, ataxia telangiectasia mutated protein (ATM), and catalytic subunit of DNA-dependent protein kinase (DNA-PKcs) in tetraploid G1 arrest induced by actin damage. Treatment with actin- damaging agents including pectenotoxin-2 (PTX-2) increases phosphorylation of Ser-15 and Ser-37 residues of p53, but not Ser-20 residue. Knockdown of ATM and DNA-PKcs do not affect p53 phosphorylation induced by actin damage. However, while ATM knockdown does not affect tetraploid G1 arrest, knockdown of DNA-PKcs not only perturbs tetraploid G1 arrest, but also results in formation of polyploidy and induction of apoptosis. These results indicate that DNA-PKcs is essential for the maintenance of actin damage induced- tetraploid G1 arrest in a p53-independent manner. Furthermore, actin damage-induced p53 expression is not observed in cells synchronized at G1/S of the cell cycle, implying that p53 induction is due to actin damage-induced tetraploidy rather than perturbation of actin cytoskeleton. Therefore, these results suggest that p53 and DNA- PKcs independently function for tetraploid G1 arrest and preventing polyploidy formation.
MeSH Terms
Actins/metabolism
Apoptosis
Ataxia Telangiectasia Mutated Proteins
Catalytic Domain
Cell Cycle Proteins/genetics,metabolism
Cell Line
Cell Line, Tumor
DNA-Activated Protein Kinase/chemistry,genetics,metabolism
DNA-Binding Proteins/genetics,metabolism
Furans/pharmacology
G1 Phase
Gene Knockdown Techniques
Humans
Macrolides
Phosphorylation/drug effects
Protein Serine-Threonine Kinases/genetics,metabolism
Pyrans/pharmacology
Tumor Suppressor Protein p53/metabolism
Tumor Suppressor Proteins/genetics,metabolism
Chemicals
Actins
Cell Cycle Proteins
DNA-Binding Proteins
Furans
Macrolides
Pyrans
Tumor Suppressor Protein p53
Tumor Suppressor Proteins
pectenotoxin 2
ATM protein, human
Ataxia Telangiectasia Mutated Proteins
DNA-Activated Protein Kinase
Protein Serine-Threonine Kinases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Chae Hee-Don
Department of Microbiology and Immunology, Dankook University College of Medicine, Cheonan 330-714, Korea.
Kim So Youn
Park Sang Eun
Kim Jeongbin
Shin Deug Y
References (28)
28 references, click to expand
-
Regulation of p53 function and stability by phosphorylation.
Mol Cell Biol. 1999 Mar;19(3):1751-8
PMID: 10022862
-
Wortmannin as a unique probe for an intracellular signalling protein, phosphoinositide 3-kinase.
Trends Biochem Sci. 1995 Aug;20(8):303-7
PMID: 7667888
-
Expression of Bcl-xL and loss of p53 can cooperate to overcome a cell cycle checkpoint induced by mitotic spindle damage.
Genes Dev. 1996 Oct 15;10(20):2621-31
PMID: 8895663
-
Mechanism of inhibition of cell proliferation by Vinca alkaloids.
Cancer Res. 1991 Apr 15;51(8):2212-22
PMID: 2009540
-
Cdk2-dependent phosphorylation of the NF-Y transcription factor is essential for the expression of the cell cycle-regulatory genes and cell cycle G1/S and G2/M transitions.
Oncogene. 2004 May 20;23(23):4084-8
PMID: 15064732
-
Constitutive activation of cyclin B1-associated cdc2 kinase overrides p53-mediated G2-M arrest.
Cancer Res. 2000 Feb 1;60(3):542-5
PMID: 10676633
-
The spindle assembly checkpoint.
Curr Opin Cell Biol. 1996 Dec;8(6):773-80
PMID: 8939672
-
p53 and its homologues, p63 and p73, induce a replicative senescence through inactivation of NF-Y transcription factor.
Oncogene. 2001 Sep 13;20(41):5818-25
PMID: 11593387
-
Mechanisms of Taxol-induced cell death are concentration dependent.
Cancer Res. 1998 Aug 15;58(16):3620-6
PMID: 9721870
-
G1 tetraploidy checkpoint and the suppression of tumorigenesis.
J Cell Biochem. 2003 Mar 1;88(4):673-83
PMID: 12577301
-
Bcl-xL and E1B-19K proteins inhibit p53-induced irreversible growth arrest and senescence by preventing reactive oxygen species-dependent p38 activation.
J Biol Chem. 2004 Apr 23;279(17):17765-71
PMID: 14764594
-
Checkpoints: controls that ensure the order of cell cycle events.
Science. 1989 Nov 3;246(4930):629-34
PMID: 2683079
-
When checkpoints fail.
Cell. 1997 Feb 7;88(3):315-21
PMID: 9039258
-
Deregulation of Cdk2 causes Bim-mediated apoptosis in p53-deficient tumors following actin damage.
Oncogene. 2008 Jul 3;27(29):4115-21
PMID: 18345036
-
Requirement for p53 and p21 to sustain G2 arrest after DNA damage.
Science. 1998 Nov 20;282(5393):1497-501
PMID: 9822382
-
Oocyte-based screening of cytokinesis inhibitors and identification of pectenotoxin-2 that induces Bim/Bax-mediated apoptosis in p53-deficient tumors.
Oncogene. 2005 Jul 14;24(30):4813-9
PMID: 15870701
-
Characterization of the p53-dependent postmitotic checkpoint following spindle disruption.
Mol Cell Biol. 1998 Feb;18(2):1055-64
PMID: 9448003
-
The complexity of p53 modulation: emerging patterns from divergent signals.
Genes Dev. 1998 Oct 1;12(19):2973-83
PMID: 9765199
-
The spindle checkpoint.
Curr Opin Genet Dev. 1999 Feb;9(1):69-75
PMID: 10072359
-
Caffeine and human DNA metabolism: the magic and the mystery.
Mutat Res. 2003 Nov 27;532(1-2):85-102
PMID: 14643431
-
Tetraploidy and tumor development.
Cancer Cell. 2005 Nov;8(5):353-4
PMID: 16286243
-
Wild-type p53 is a cell cycle checkpoint determinant following irradiation.
Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7491-5
PMID: 1323840
-
Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1.
Mol Biol Cell. 2001 May;12(5):1315-28
PMID: 11359924
-
Regulation of the p53 tumor suppressor protein.
J Biol Chem. 1999 Dec 17;274(51):36031-4
PMID: 10593882
-
Cell cycle checkpoints as therapeutic targets.
J Mammary Gland Biol Neoplasia. 1999 Oct;4(4):389-400
PMID: 10705922
-
Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine.
Cancer Res. 1999 Sep 1;59(17):4375-82
PMID: 10485486
-
p53 mutations in human cancers.
Science. 1991 Jul 5;253(5015):49-53
PMID: 1905840
-
Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death.
Cancer Res. 1996 Feb 15;56(4):816-25
PMID: 8631019