Homeostatic control of polo-like kinase-1 engenders non-genetic heterogeneity in G2 checkpoint fidelity and timing

Nature Communications

Volumn 5, Issue , 2014, Pages

  Liang, Hongqing ^a,b,c   Esposito, Alessandro ^a   De, Siddharth ^a   Ber, Suzan ^a   Collin, Philippe ^d   Surana, Uttam ^b,c   Venkitaraman, Ashok R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^c AGENCY FOR SCIENCE   (Singapore)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

POLO LIKE KINASE 1; CELL CYCLE PROTEIN; ONCOPROTEIN; POLO-LIKE KINASE 1; PROTEIN SERINE THREONINE KINASE;

DNA; ENZYME ACTIVITY; GENETIC VARIATION; HETEROGENEITY; HOMEOSTASIS; IMAGING METHOD; PATHOGENICITY;

ARTICLE; CARCINOGENICITY; DNA DAMAGE; FLUORESCENCE IMAGING; G2 PHASE CELL CYCLE CHECKPOINT; GENETIC HETEROGENEITY; HOMEOSTASIS; MITOSIS; MOLECULAR MECHANICS; DOUBLE STRANDED DNA BREAK; HUMAN; METABOLISM; TIME; TUMOR CELL LINE;

CELL CYCLE PROTEINS; CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; G2 PHASE CELL CYCLE CHECKPOINTS; GENETIC HETEROGENEITY; HOMEOSTASIS; HUMANS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; TIME FACTORS;

EID: 84901980169     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5048     Document Type: Article

References (62)

1. Zhou, B. B. &Elledge, S. J. The DNA damage response: putting checkpoints in perspective. Nature 408, 433-439 (2000).
2. Huen, M. S. &Chen, J. Assembly of checkpoint and repair machineries at DNA damage sites. Trends Biochem. Sci. 35, 101-108 (2010).
3. Giglia-Mari, G., Zotter, A. &Vermeulen, W. DNA damage response. Cold Spring Harb. Perspect. Biol. 3, a000745 (2011).
4. Langerak, P. &Russell, P. Regulatory networks integrating cell cycle control with DNA damage checkpoints and double-strand break repair. Philos. Trans. R. Soc. Lond. B Biol. Sci 366, 3562-3571 (2011).
5. Varon, R. et al. Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell 93, 467-476 (1998). (Pubitemid 28232090)
6. Carney, J. P. et al. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93, 477-486 (1998). (Pubitemid 28232091)
7. Lee, J. H. &Paull, T. T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308, 551-554 (2005). (Pubitemid 40570585)
8. Smith, G. C. &Jackson, S. P. The DNA-dependent protein kinase. Genes Dev. 13, 916-934 (1999). (Pubitemid 29200976)
9. Zou, L. &Elledge, S. J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300, 1542-1548 (2003). (Pubitemid 36682880)
10. Matsuoka, S. et al. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc. Natl Acad. Sci. USA 97, 10389-10394 (2000).
11. Liu, Q. et al. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev. 14, 1448-1459 (2000). (Pubitemid 30421838)
12. Shieh, S. Y., Ahn, J., Tamai, K., Taya, Y. &Prives, C. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev. 14, 289-300 (2000). (Pubitemid 30106484)
13. Banin, S. et al. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281, 1674-1677 (1998).
14. Marples, B., Wouters, B. G., Collis, S. J., Chalmers, A. J. &Joiner, M. C. Lowdose hyper-radiosensitivity: a consequence of ineffective cell cycle arrest of radiation-damaged G2-phase cells. Radiat. Res. 161, 247-255 (2004). (Pubitemid 40797066)
15. Syljuasen, R. G., Jensen, S., Bartek, J. &Lukas, J. Adaptation to the ionizing radiation-induced G2 checkpoint occurs in human cells and depends on checkpoint kinase 1 and Polo-like kinase 1 kinases. Cancer Res. 66, 10253-10257 (2006). (Pubitemid 44799740)
16. Toczyski, D. P., Galgoczy, D. J. &Hartwell, L. H. CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90, 1097-1106 (1997). (Pubitemid 27408523)
17. Lupardus, P. J. &Cimprich, K. A. Checkpoint adaptation; molecular mechanisms uncovered. Cell 117, 555-556 (2004). (Pubitemid 38692520)
18. Buscemi, G. et al. Activation of ATM and Chk2 kinases in relation to the amount of DNA strand breaks. Oncogene 23, 7691-7700 (2004). (Pubitemid 39424927)
19. Deckbar, D. et al. Chromosome breakage after G2 checkpoint release. J. Cell. Biol. 176, 749-755 (2007). (Pubitemid 46425534)
20. Ishikawa, A., Yamauchi, M., Suzuki, K. &Yamashita, S. Image-based quantitative determination of DNA damage signal reveals a threshold for G2 checkpoint activation in response to ionizing radiation. Genome Integr 1, 10 (2010).
21. Smits, V. A. et al. Polo-like kinase-1 is a target of the DNA damage checkpoint. Nat. Cell Biol. 2, 672-676 (2000).
22. Chiyoda, T. et al. LATS1/WARTS phosphorylates MYPT1 to counteract PLK1 and regulate mammalian mitotic progression. J. Cell Biol. 197, 625-641 (2012).
23. Bassermann, F. et al. The Cdc14B-Cdh1-Plk1 axis controls the G2 DNAdamage- response checkpoint. Cell 134, 256-267 (2008). (Pubitemid 352010329)
24. Toyoshima, F., Moriguchi, T., Wada, A., Fukuda, M. &Nishida, E. Nuclear export of cyclin B1 and its possible role in the DNA damage-induced G2 checkpoint. EMBO J. 17, 2728-2735 (1998). (Pubitemid 28227119)
25. Jin, P., Hardy, S. &Morgan, D. O. Nuclear localization of cyclin B1 controls mitotic entry after DNA damage. J. Cell Biol. 141, 875-885 (1998). (Pubitemid 28243956)
26. Innocente, S. A., Abrahamson, J. L., Cogswell, J. P. &Lee, J. M. p53 regulates a G2 checkpoint through cyclin B1. Proc. Natl Acad. Sci. USA 96, 2147-2152 (1999). (Pubitemid 29117882)
27. Manni, I. et al. NF-Y mediates the transcriptional inhibition of the cyclin B1, cyclin B2, and cdc25C promoters upon induced G2 arrest. J. Biol. Chem. 276, 5570-5576 (2001).
28. Fletcher, L., Yen, T. J. &Muschel, R. J. DNA damage in HeLa cells induced arrest at a discrete point in G2 phase as defined by CENP-F localization. Radiat. Res. 159, 604-611 (2003). (Pubitemid 36539239)
29. van Vugt, M. A., Bras, A. &Medema, R. H. Polo-like kinase-1 controls recovery from a G2 DNA damage-induced arrest in mammalian cells. Mol. Cell 15, 799-811 (2004). (Pubitemid 39194909)
30. Alvarez-Fernandez, M. et al. Recovery from a DNA-damage-induced G2 arrest requires Cdk-dependent activation of FoxM1. EMBO Rep. 11, 452-458 (2010).
31. Loewer, A., Batchelor, E., Gaglia, G. &Lahav, G. Basal dynamics of p53 reveal transcriptionally attenuated pulses in cycling cells. Cell 142, 89-100 (2010).
32. Tay, S. et al. Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Nature 466, 267-271 (2010).
33. Spencer, S. L., Gaudet, S., Albeck, J. G., Burke, J. M. &Sorger, P. K. Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 459, 428-432 (2009).
34. Gascoigne, K. E. &Taylor, S. S. Cancer cells display profound intra- and interline variation following prolonged exposure to antimitotic drugs. Cancer Cell 14, 111-122 (2008).
35. Loewer, A. &Lahav, G. We are all individuals: causes and consequences of non-genetic heterogeneity in mammalian cells. Curr. Opin. Genet. Dev 21, 753-758 (2011).
36. Lobrich, M. et al. gammaH2AX foci analysis for monitoring DNA doublestrand break repair: strengths, limitations and optimization. Cell Cycle 9, 662-669 (2010).
37. Stewart, G. S., Wang, B., Bignell, C. R., Taylor, A. M. &Elledge, S. J. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421, 961-966 (2003). (Pubitemid 36288029)
38. Stucki, M. et al. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123, 1213-1226 (2005). (Pubitemid 41821780)
39. Costes, S. V., Chiolo, I., Pluth, J. M., Barcellos-Hoff, M. H. &Jakob, B. Spatiotemporal characterization of ionizing radiation induced DNA damage foci and their relation to chromatin organization. Mutat. Res. 704, 78-87 (2010).
40. Soutoglou, E. &Misteli, T. Activation of the cellular DNA damage response in the absence of DNA lesions. Science 320, 1507-1510 (2008). (Pubitemid 351929432)
41. Nakada, S., Chen, G. I., Gingras, A. C. &Durocher, D. PP4 is a gamma H2AX phosphatase required for recovery from the DNA damage checkpoint. EMBO Rep. 9, 1019-1026 (2008).
42. Suzuki, K. et al. Qualitative and quantitative analysis of phosphorylated ATM foci induced by low-dose ionizing radiation. Radiat. Res. 165, 499-504 (2006).
43. Keogh, M. C. et al. A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature 439, 497-501 (2006).
44. Giunta, S., Belotserkovskaya, R. &Jackson, S. P. DNA damage signaling in response to double-strand breaks during mitosis. J. Cell Biol. 190, 197-207 (2010).
45. Nelson, G., Buhmann, M. &von Zglinicki, T. DNA damage foci in mitosis are devoid of 53BP1. Cell Cycle 8, 3379-3383 (2009).
46. Dalton, W. B., Nandan, M. O., Moore, R. T. &Yang, V. W. Human cancer cells commonly acquire DNA damage during mitotic arrest. Cancer Res. 67, 11487-11492 (2007).
47. Hayashi, M. T., Cesare, A. J., Fitzpatrick, J. A., Lazzerini-Denchi, E. &Karlseder, J. A telomere-dependent DNA damage checkpoint induced by prolonged mitotic arrest. Nat. Struct. Mol. Biol. 19, 387-394 (2012).
48. Orth, J. D., Loewer, A., Lahav, G. &Mitchison, T. J. Prolonged mitotic arrest triggers partial activation of apoptosis, resulting in DNA damage and p53 induction. Mol. Biol. Cell. 23, 567-576 (2012).
49. van Vugt, M. A., Smits, V. A., Klompmaker, R. &Medema, R. H. Inhibition of Polo-like kinase-1 by DNA damage occurs in an ATM- or ATR-dependent fashion. J. Biol. Chem. 276, 41656-41660 (2001).
50. Macurek, L. et al. Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature 455, 119-123 (2008).
51. Karanam, K., Kafri, R., Loewer, A. &Lahav, G. Quantitative live cell imaging reveals a gradual shift between DNA repair mechanisms and a maximal use of HR in Mid S phase. Mol. Cell 47, 320-329 (2012).
52. Zhou, B. B. et al. Caffeine abolishes the mammalian G(2)/M DNA damage checkpoint by inhibiting ataxia-telangiectasia-mutated kinase activity. J. Biol. Chem. 275, 10342-10348 (2000).
53. Fu, Z. et al. Plk1-dependent phosphorylation of FoxM1 regulates a transcriptional programme required for mitotic progression. Nat. Cell Biol. 10, 1076-1082 (2008).
54. Steegmaier, M. et al. BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth in vivo. Curr. Biol. 17, 316-322 (2007). (Pubitemid 46241881)
55. Vassilev, L. T. et al. Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc. Natl Acad. Sci. USA 103, 10660-10665 (2006). (Pubitemid 44078033)
56. Toyoshima-Morimoto, F., Taniguchi, E. &Nishida, E. Plk1 promotes nuclear translocation of human Cdc25C during prophase. EMBO Rep. 3, 341-348 (2002). (Pubitemid 34467604)
57. Nakajima, H., Toyoshima-Morimoto, F., Taniguchi, E. &Nishida, E. Identification of a consensus motif for Plk (Polo-like kinase) phosphorylation reveals Myt1 as a Plk1 substrate. J. Biol. Chem. 278, 25277-25280 (2003). (Pubitemid 36835273)
58. Gavet, O. &Pines, J. Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev. Cell 18, 533-543 (2010).
59. Collin, P., Nashchekina, O., Walker, R. &Pines, J. The spindle assembly checkpoint works like a rheostat rather than a toggle switch. Nat. Cell Biol. 15, 1378-1385 (2013).
60. Brito, D. A. &Rieder, C. L. Mitotic checkpoint slippage in humans occurs via cyclin B destruction in the presence of an active checkpoint. Curr. Biol. 16, 1194-1200 (2006). (Pubitemid 43867292)
61. Varetti, G., Guida, C., Santaguida, S., Chiroli, E. &Musacchio, A. Homeostatic control of mitotic arrest. Mol. Cell 44, 710-720 (2011).
62. Topham, C. H. &Taylor, S. S. Mitosis and apoptosis: how is the balance set? Curr. Opin. Cell Biol. 25, 780-785 (2013).