Mitotic catastrophe occurs in the absence of apoptosis in p53-null cells with a defective G1 checkpoint

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Fragkos, Michalis ^a,b   Beard, Peter ^a  

^a EPFL   (Switzerland)

^b INSTITUTE OF HUMAN GENETICS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; APOPTOSIS INDUCING FACTOR; CASPASE 3; DACTINOMYCIN; DOXORUBICIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN P53; CASPASE;

ADENO ASSOCIATED VIRUS; ADENOVIRUS INFECTION; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL DEATH; CELL POPULATION; CELL STRUCTURE; CENTROSOME; CHROMOSOME CONDENSATION; CONTROLLED STUDY; DNA DAMAGE; DNA FRAGMENTATION; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; MITOSIS; MITOSIS SPINDLE; NULL CELL; OSTEOSARCOMA CELL; PROTEIN CLEAVAGE; TIME LAPSE IMAGING; ANIMAL; BIOLOGICAL MODEL; G1 PHASE CELL CYCLE CHECKPOINT; GENETICS; METABOLISM; MOUSE; NECROSIS; TUMOR CELL LINE;

PARVOVIRUS;

ANIMALS; APOPTOSIS; AUTOPHAGY; CASPASES; CELL LINE, TUMOR; DEPENDOVIRUS; DNA FRAGMENTATION; G1 PHASE CELL CYCLE CHECKPOINTS; HUMANS; MICE; MITOSIS; MODELS, BIOLOGICAL; NECROSIS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 80051519133     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022946     Document Type: Article

References (53)

1. Meier P, Vousden KH, (2007) Lucifer's labyrinth- ten years of path finding in cell death. Mol Cell 28: 746-754.
2. Cohen G, (1997) Caspases: the executioners of apoptosis. Biochem J 326: 1-16.
3. Janicke RU, Sprengart ML, Wati MR, Porter AG, (1998) Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 273: 9357-9360.
4. Porter AG, Janicke RU, (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6: 99-104.
5. Bouchard VJ, Rouleau M, Poirier GG, (2003) PARP-1, a determinant of cell survival in response to DNA damage. Exp Hematol 31: 446-454.
6. Broker LE, Kruyt FAE, Giaccone G, (2005) Cell death independent of caspases: a review. Clin Cancer Res 11: 3155-3162.
7. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, et al. (1999) Molecular characterisation of mitochondrial apoptosis-inducing factor. Nature 397: 441-446.
8. Borner C, Monney L, (1999) Apoptosis without caspases: an efficient molecular guillotine. Cell Death Differ 6: 497-507.
9. Daugas E, Nochy D, Ravagnan L, Loeffler M, Susin SA, et al. (2000) Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett 476: 118-123.
10. Okada H, Mak TW, (2004) Pathways of apoptotic and non-apoptotic death in tumour cells. Nat Rev Cancer 4: 592-603.
11. Levine B, Kroemer G, (2008) Autophagy in the pathogenesis of disease. Cell 132: 27-42.
12. Mizushima N, (2008) Autophagy: process and function. Genes Dev 21: 2861-2873.
13. Tasdemir E, Maiuri MC, Galluzzi L, Vitale I, Djavaheri-Mergny M, et al. (2008) Regulation of autophagy by cytoplasmic p53. Nat Cell Biol 10: 676-687.
14. Zong W-X, Thompson CB, (2006) Necrotic death as a cell fate. Genes Dev 20: 1-15.
15. Degterev A, Hitomi J, Germscheid M, Chen IL, Korkina O, et al. (2008) Identification of RIP1 kinase as a specific cellular target of necrostatins. Nature Chem Biol 5: 313-321.
16. Castedo M, Perfettini JL, Roumier T, Andreau K, Medema R, et al. (2004) Cell death by mitotic catastrophe: a molecular definition. Oncogene 23: 2825-2837.
17. Fukasawa K, (2007) Oncogenes and tumour suppressors take on centrosomes. Nat Rev Cancer 7: 911-924.
18. Huang H, Fletcher L, Beeharry N, Daniel R, Kao G, et al. (2008) Abnormal cytokinesis after X-irradiation in tumor cells that override the G2 DNA damage checkpoint. Cancer Res 68: 3724-3732.
19. Jordan MA, Wendell K, Gardiner S, Derry WB, Copp H, et al. (1996) Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death. Cancer Res 56: 816-825.
20. Merritt AJ, Allen TD, Potten CS, Hickman JA, (1997) Apoptosis in small intestinal epithelial from p53-null mice: evidence for a delayed, p53-independent G2/M-associated cell death after gamma-irradiation. Oncogene 14: 2759-2766.
21. Castedo M, Perfettini JL, Roumier T, Valent A, Raslova H, et al. (2004) Mitotic catastrophe constitutes a special case of apoptosis whose suppression entails aneuploidy. Oncogene 23: 4362-4370.
22. Vakifahmetoglu H, Olsson M, Zhivotovsky B, (2008) Death through a tragedy: mitotic catastrophe. Cell Death Differ 15: 1153-1162.
23. Lock RB, Stribinskiene L, (1996) Dual modes of death induced by etoposide in human epithelial tumor cells allow Bcl-2 to inhibit apoptosis without affecting clonogenic survival. Cancer Res 56: 4006-4012.
24. Roninson IB, Broude EV, Chang B-D, (2001) If not apoptosis, then what? Treatment-induced senescence and mitotic catastrophe in tumor cells. Drug Resist Updat 4: 303-313.
25. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, et al. (2009) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16: 3-11.
26. Berns KI, Linden RM, (1995) The cryptic life style of adeno-associated virus. Bioessays 17: 237-245.
27. Jurvansuu J, Raj K, Stasiak A, Beard P, (2005) Viral transport of DNA damage that mimics a stalled replication fork. J Virol 79: 569-580.
28. Jurvansuu J, Fragkos M, Ingemarsdotter C, Beard P, (2007) Chk1 instability is coupled to mitotic cell death of p53-deficient cells in response to virus-induced DNA damage signaling. J Mol Biol 372: 397-406.
29. Ingemarsdotter C, Keller D, Beard P, (2010) The DNA damage response to non-replicating adeno-associated virus: Centriole overduplication and mitotic catastrophe independent of the spindle checkpoint. Virology 400: 271-286.
30. Raj K, Ogston P, Beard P, (2001) Virus-mediated killing of cells that lack p53 activity. Nature 412: 914-917.
31. Finkel E, (1999) Does cancer therapy trigger cell suicide? Science 286: 2256-2258.
32. Fragkos M, Jurvansuu J, Beard P, (2009) H2AX is required for cell cycle arrest via the p53/p21 pathway. Mol Cell Biol 29: 2828-2840.
33. Eom YW, Kim MA, Park SS, Goo MJ, Kwon HJ, et al. (2005) Two distinct modes of cell death induced by doxorubicin: apoptosis and cell death through mitotic catastrophe accompanied by senescence-like phenotype. Oncogene 24: 4765-4777.
34. Strasser A, Harris AW, Jacks T, Cory S, (1994) DNA damage can induce apoptosis in proliferating lymphoid cells via p53-independent mechanisms inhibitable by Bcl-2. Cell 79: 329-339.
35. Dou QP, An B, Will PL, (1995) Induction of a retinoblastoma phosphatase activity by anticancer drugs accompanies p53-independent G1 arrest and apoptosis. Proc Natl Acad Sci U S A 92: 9019-9023.
36. Bartek J, Lukas J, (2001) Pathways governing G1/S transition and their response to DNA damage. FEBS Lett 490: 117-122.
37. Anderson CW, Allalunis-Turner MJ, (2000) Human TP53 from the malignant glioma-derived cell lines M059J and M059K has a cancer-associated mutation in exon 8. Radiat Res 154: 473-476.
38. Massague J, (2004) G1 cell-cycle control and cancer. Nature 432: 298-306.
39. Park YB, Park MJ, Kimura K, Shimizu K, Lee SH, et al. (2002) Alterations in the INK4a/ARF locus and their effects on the growth of human osteosarcoma cell lines. Cancer Genet Cytogenet 133: 105-111.
40. Fragkos M, Breuleux M, Clément N, Beard P, (2008) Recombinant adeno-associated viral vectors are deficient in provoking a DNA damage response. J Virol 82: 7379-7387.
41. Shapiro GI, Edwards CD, Rollins BJ, (2000) The physiology of p16(INK4A)-mediated G1 proliferative arrest. Cell Biochem Biophys 33: 189-197.
42. Ivanchuk SM, Mondal S, Dirks PB, Rutka JT, (2001) The INK4A/ARF locus: role in cell cycle control and apoptosis and implications for glioma growth. J Neurooncol 51: 219-229.
43. Giacinti C, Giordano A, (2006) RB and cell cycle progression. Oncogene 25: 5220-5227.
44. Kim JS, Pirnia F, Choi YH, Nguyen PM, Knepper B, et al. (2000) Lovastatin induces apoptosis in a primitive neuroectodermal tumor cell line in association with RB down-regulation and loss of the G1 checkpoint. Oncogene 19: 6082-6090.
45. Santiago-Walker AE, Fikaris AJ, Kao GD, Brown EJ, Kazanietz MG, et al. (2005) Protein kinase C delta stimulates apoptosis by initiating G1 phase cell cycle progression and S phase arrest. J Biol Chem 280: 32107-32114.
46. Garner E, Martinon F, Tschopp J, Beard P, Raj K, (2007) Cells with defective p53-p21-pRb pathway are susceptible to apoptosis induced by p84N5 via caspase-6. Cancer Res 67: 7631-7637.
47. Emanuele S, D'Anneo A, Bellavia G, Vassallo B, Lauricella M, et al. (2004) Sodium butyrate induces apoptosis in human hepatoma cells by a mitochondria/caspase pathway, associated with degradation of beta-catenin, pRb and Bcl-XL. Eur J Cancer 40: 1441-1452.
48. Jin Y, Leung WK, Sung JJ, Wu JR, (2005) p53-independent pRB degradation contributes to a drug-induced apoptosis in AGS cells. Cell Res 15: 695-703.
49. Niida H, Tsuge S, Katsuno Y, Konishi A, Takeda N, et al. (2005) Depletion of Chk1 leads to premature activation of Cdc2-cyclin B and mitotic catastrophe. J Biol Chem 280: 39246-39252.
50. Dodson H, Bourke E, Jeffers LJ, Vagnarelli P, Sonoda E, et al. (2004) Centrosome amplification induced by DNA damage occurs during a prolonged G2 phase and involves ATM. EMBO J 23: 3864-3873.
51. Garner E, Raj K, (2008) Protective mechanisms of p53-p21-pRb proteins against DNA damage-induced cell death. Cell Cycle 7: 277-282.
52. Holland AJ, Cleveland DW, (2009) Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat Revs Mol Cell Biol 10: 478-487.
53. Xie Q, Hare J, Turnigan J, Chapman MS, (2004) Large-scale production, purification and crystallization of wild-type adeno-associated virus-2. J Virol Methods 122: 17-27.