ATM is activated by mitotic stress and suppresses centrosome amplification in primary but not in tumor cells

Journal of Cellular Biochemistry

Volumn 99, Issue 5, 2006, Pages 1267-1274

  Shen, Kate ^a   Wang, Yaolin ^b   Brooks, S C ^a   Raz, Avraham ^a   Wang, Y Alan ^a,c  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

^c KARMANOS CANCER INSTITUTE   (United States)

Author keywords

Ataxia Telangiectasia; ATM; Centrosomes; Micronuclei; Mitotic spindle checkpoint; Mitotic stress; p53

Indexed keywords

ATM PROTEIN; GAMMA TUBULIN; PROTEIN P21; PROTEIN P53;

ANEUPLOIDY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOGENESIS; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL TRANSFORMATION; CENTROSOME; CENTROSOME AMPLIFICATION; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; FIBROBLAST; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; MITOSIS; MITOSIS SPINDLE; MITOTIC STRESS; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; REGULATORY MECHANISM; STRESS; TUMOR CELL;

ANIMALS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELLS, CULTURED; CENTROSOME; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; DNA-BINDING PROTEINS; ENZYME ACTIVATION; FIBROBLASTS; GENOMIC INSTABILITY; MICE; MICE, KNOCKOUT; MICRONUCLEI, CHROMOSOME-DEFECTIVE; MITOSIS; MITOTIC SPINDLE APPARATUS; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

ATAXIA TELANGIECTASIA;

EID: 33751171109     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.20848     Document Type: Article

References (29)

1. Bakkenist CJ, Kastan MB. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation, [see comment]. Nature 421:499-506.
2. Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K, Guldberg P, Sehested M, Nesland JM, Lukas C, Orntoft T, Lukas J, Bartek J. 2005. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434:864-870.
3. Chiba S, Okuda M, Mussman JG, Fukasawa K. 2000. Genomic convergence and suppression of centrosome hyperamplification in primary p53-/- cells in prolonged culture. Exp Cell Res 258:310-321.
4. D'Assoro AB, Lingle WL, Salisbury JL. 2002. Centrosome amplification and the development of cancer. Oncogene 21:6146-6153.
5. Deng CX. 2002. Roles of BRCA1 in centrosome duplication. Oncogene 21:6222-6227.
6. Dodson H, Bourke E, Jeffers LJ, Vagnarelli P, Sonoda E, Takeda S, Earnshaw WC, Merdes A, Morrison C. 2004. Centrosome amplification induced by DNA damage occurs during a prolonged G2 phase and involves ATM. Embo J 23:3864-3873.
7. Doxsey S. 2001. Re-evaluating centrosome function. Nat Rev Mol Cell Biol 2:688-698.
8. Fukasawa K, Choi T, Kuriyama R, Rulong S, Vande Woude GF. 1996. Abnormal centrosome amplification in the absence of p53. Science 271:1744-1747.
9. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T, Venere M, Ditullio RA, Jr., Kastrinakis NG, Levy B, Kletsas D, Yoneta A, Herlyn M, Kittas C, Halazonetis TD. 2005. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434:907-913.
10. Harlow E, Lane D. 1988. Antibodies, A Laboratory Manual.
11. Hinchcliffe EH, Sluder G. 2001. "It takes two to tango": Understanding how centrosome duplication is regulated throughout the cell cycle. Genes Dev 15:1167-1181.
12. Hinchcliffe EH, Sluder G. 2002. Two for two: Cdk2 and its role in centrosome doubling. Oncogene 21:6154-6160.
13. Hsu LC, White RL. 1998. BRCA1 is associated with the centrosome during mitosis. Proc Natl Acad Sci USA 95:12983-12988.
14. Kanai M, Tong WM, Sugihara E, Wang ZQ, Fukasawa K, Miwa M. 2003. Involvement of poly(ADP-Ribose) polymerase 1 and poly(ADP-Ribosyl)ation in regulation of centrosome function. Mol Cell Biol 23:2451-2462.
15. Lingle WL, Barrett SL, Negron VC, D'Assoro AB, Boeneman K, Liu W, Whitehead CM, Reynolds C, Salisbury JL. 2002. Centrosome amplification drives chromosomal instability in breast tumor development. Proc Natl Acad Sci USA 99:1978-1983.
16. Liu X, Erikson RL. 2003. Polo-like kinase (Plk)1 depletion induces apoptosis in cancer cells. Proc Natl Acad Sci USA 100:5789-5794.
17. Meraldi P, Honda R, Nigg EA. 2004. Aurora kinases link chromosome segregation and cell division to cancer susceptibility. Curr Opin Genet Dev 14:29-36.
18. Morita T, Asano N, Awogi T, Sasaki YF, Sato S, Shimada H, Sutou S, Suzuki T, Wakata A, Sofuni T, Hayashi M. 1997. Evaluation of the rodent micronucleus assay in the screening of IARC carcinogens (groups 1, 2A and 2B) the summary report of the 6th collaborative study by CSGMT/JEMS MMS. Collaborative Study of the Micronucleus Group Test. Mammalian Mutagenicity Study Group. Mutat Res 389:3-122.
19. Nigg EA. 2002. Centrosome aberrations: Cause or consequence of cancer progression? Nat Rev Cancer 2:815-825.
20. Pihan GA, Purohit A, Wallace J, Knecht H, Woda B, Quesenberry P, Doxsey SJ. 1998. Centrosome defects and genetic instability in malignant tumors. Cancer Res 58:3974-3985.
21. Shen KC, Heng H, Wang Y, Lu S, Liu G, Deng CX, Brooks SC, Wang YA. 2005. ATM and p21 cooperate to suppress aneuploidy and subsequent tumor development. Cancer Res 65:8747-8753.
22. Shiloh Y. 2003. ATM and related protein kinases: Safeguarding genome integrity. Nat Rev Cancer 3:155-168.
23. Sibon OC, Kelkar A, Lemstra W, Theurkauf WE. 2000. DNA-replication/DNA- damage-dependent centrosome inactivation in Drosophila embryos [see comments]. Nat Cell Biol 2:90-95.
24. Smits VA, Klompmaker R, Arnaud L, Rijksen G, Nigg EA, Medema RH. 2000. Polo-like kinase-1 is a target of the DNA damage checkpoint. Nat Cell Biol 2:672-676.
25. Su TT, Vidwans SJ. 2000. DNA defects target the centrosome. Nat Cell Biol 2:E28-E29.
26. Tritarelli A, Oricchio E, Ciciarello M, Mangiacasale R, Palena A, Lavia P, Soddu S, Cundari E. 2004. p53 localization at centrosomes during mitosis and postmitotic checkpoint are ATM-dependent and require serine 15 phosphorylation. Mol Biol Cell 15:3751-3757.
27. Tutt A, Gabriel A, Bertwistle D, Connor F, Paterson H, Peacock J, Ross G, Ashworth A. 1999. Absence of Brca2 causes genome instability by chromosome breakage and loss associated with centrosome amplification. Curr Biol 9:1107-1110.
28. Wang YA, Elson A, Leder P. 1997. Loss of p21 increases sensitivity to ionizing radiation and delays the onset of lymphoma in atm-deficient mice. Proc Natl Acad Sci USA 94:14590-14595.
29. Westphal CH, Schmaltz C, Rowan S, Elson A, Fisher DE, Leder P. 1997. Genetic interactions between atm and p53 influence cellular proliferation and irradiation-induced cell cycle checkpoints. Cancer Res 57:1664-1667.