Topoisomerase II and histone deacetylase inhibitors delay the G2/M transition by triggering the p38 MAPK checkpoint pathway

Journal of Cell Biology

Volumn 166, Issue 4, 2004, Pages 517-526

  Mikhailov, Alexei ^a   Shinohara, Mio ^a,b   Rieder, Conly L ^a,b,c  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

Aclarubicin; Apicidin; DNA; ICRF 193; Merbarone; Mitosis

Indexed keywords

2,3 BIS(3,5 DIOXO 1 PIPERAZINYL)BUTANE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 4 ETHYL 2 (4 METHOXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ACLARUBICIN; ANISOMYCIN; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; ATM PROTEIN; CAFFEINE; CHECKPOINT KINASE 2; DNA TOPOISOMERASE INHIBITOR; DOXORUBICIN; HISTONE DEACETYLASE INHIBITOR; MERBARONE; MITOGEN ACTIVATED PROTEIN KINASE; NOCODAZOLE; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CELL CYCLE G2 PHASE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; ENZYME INHIBITION; HUMAN; HUMAN CELL; INHIBITION KINETICS; MEMBRANE STRUCTURE; METAPHASE; MITOSIS; MITOSIS SPINDLE; OSMOSIS; PHASE TRANSITION; PRIORITY JOURNAL; PROPHASE; PROTEIN MODIFICATION;

ACLARUBICIN; ANAPHASE; ANTIBIOTICS, ANTINEOPLASTIC; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CATALYSIS; CELL LINE, TUMOR; CHROMATIN; CHROMOSOMES; DNA DAMAGE; DNA TOPOISOMERASES, TYPE II; DOXORUBICIN; ENZYME ACTIVATION; G2 PHASE; HELA CELLS; HISTONE DEACETYLASES; HISTONES; HUMANS; IMMUNOHISTOCHEMISTRY; LASERS; MICROSCOPY, VIDEO; MITOGEN-ACTIVATED PROTEIN KINASES; MITOSIS; MITOTIC SPINDLE APPARATUS; OSMOSIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PIPERAZINES; THIOBARBITURATES; TIME FACTORS;

MUNTIACUS MUNTJAK;

EID: 4143057046     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200405167     Document Type: Article

References (57)

1. Bakkenist, CJ., and M.B. Kastan. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature. 421:499-506.
2. Bennett, B.L., D.T. Sasaki, B.W. Murray, E.G. O'Leary, S.T. Sakata, X. Xu, J.C. Leisten, A. Motiwala, S. Pierce, Y. Satoh, et al. 2001. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. USA. 98:13681-13686.
3. Brancho, D., N. Tanaka, A. Jaeschke, J.-J. Ventura, N. Kelkar, Y. Tanaka, M. Kyuuma, T. Takeshita, R.A. Flavel, and RJ. Davis. 2003. Mechanism of p38 MAP kinase activation in vivo. Genes Dev. 17:1969-1978.
4. Bulavin, D.V., Y. Higashimoto, I.J. Popoff, W.A. Gaarde, V. Basrur, O. Potapova, E. Appella, and AJ. Fornace. 2001. Initiation of a G2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature. 411:102-107.
5. Bulavin, D.V., S.A. Amudson, and A.J. Fornace. 2002. p38 and Chk1 kinases: different conductors for the G2/M checkpoint symphony. Curr. Opin. Genet. Dev. 12:92-97.
6. Bullough, W.S., and M. Johnson. 1951. The energy relations of mitotic activity in adult mouse epidermis. Proc. R. Soc. Land. B. Biol. Sci. 138:562-575.
7. Bunyard, P., M. Handley, G. Pollara, K. Rutault, I. Wood, M. Chaudry, C. Alderman, J. Foreman, D.R. Katz, and B.M. Chain. 2003. Ribotoxic stress activates p38 and JNK kinases and modulates the antigen-presenting activity of dendritic cells. Mol. Immunol. 39:815-827.
8. Campos, C.B.L., P.A. Bedard, and R. Linden. 2002. Activation of p38 mitogen-activated protein kinase during normal mitosis in the developing retina. Neuroscience. 112:583-591.
9. Caspari, T., and A.M. Carr. 2002. Checkpoints: how to flag up double-strand breaks. Curr. Biol. 12:R105-R107.
10. Chaturvedi, P., V. Sudakin, M.L. Bobiak, P.W. Fisher, M.R. Mattern, S.A. Jablonski, M.R. Hurle, Y. Zhu, TJ. Yen, and B.-B.S. Zhou. 2002. Chfr regulates a mitotic stress pathway through its RING-finger domain with ubiquitin ligase activity. Cancer Res. 62:1797-1801.
11. Christensen, M.O., M.K. Larsen, H.U. Bartheimes, R. Hock, C.L. Andersen, E. Kjeldsen, B.R. Knudsen, O. Westergaard, F. Boege, and C. Mielke. 2002. Dynamics of human DNA topoisomerase IIα and IIβ in living cells. J. Cell Biol. 157:31-44.
12. Cimini, D., M. Mattiuzzo, L. Torosantucci, and F. Degrassi. 2003. Histone hyperacetylation in mitosis prevents sister chromatid separation and produces chromosomal segregation defects. Mol. Biol. Cell. 14:3821-3833.
13. Clifford, B., M. Beljin, G.R. Stark, and W.R. Taylor. 2003. G2 arrest in response to topoisomerase II inhibitors: the role of p53. Cancer Res. 63:4074-4081.
14. de Laszlo, S.E., D. Visco, L. Agarwal, L. Chang, J. Chin, G. Croft, A. Forsyth, D. Fletcher, B. Franz, C. Hacker, et al. 1998. Pyrroles and other heterocycles as inhibitors of p38 kinase. Bioorg. Med. Chem. Lett. 8:2689-2694.
15. Deacon, K., P. Mistry, J. Chernoff, J.L. Blank, and R. Patel. 2003. p38 mitogen-activated protein kinase mediates cell death and p21-activated kinase mediates cell survival during chemotherapeutic drug-induced mitotic arrest. Mol. Biol. Cell. 14:2071-2087.
16. Deming, P.B., C.A. Cistulli, H. Zhao, P.R. Graves, H. Piwnica-Worms, R.S. Paules, C.S. Downes, and W.K. Kaufmann. 2001. The human decatenation checkpoint. Proc. Natl. Acad. Sci. USA. 98:12044-12049.
17. Deming, P.B., K.G. Flores, CS. Downes, R.S. Paules, and W.K. Kaufmann. 2002. ATR enforces the topoisomerase II-dependent G2 checkpoint through inhibition of Plk1 kinase. J. Biol. Chem. 277:36832-36838.
18. Dmitrieva, N.I., D.V. Bulavin, A.J. Fornace, and M.B. Burg. 2002. Rapid activation of G2/M checkpoint after hyperronic stress in renal inner medullary epithelial (IME) cells is protective and requires p38 kinase. Proc. Natl. Acad. Sci. USA. 99:184-189.
19. Downes, C.S., DJ. Clarke, A.M. Mullinger, G. Gimenez-Martin, A.M. Creighton, and R.T. Johnson. 1994. A topoisomerase II-dependent G2 cell cycle checkpoint in mammalian cells. Nature. 372:467-470.
20. Durocher, D., and S.P. Jackson. 2001. DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme? Curr. Opin. Cell Biol. 13:225-231.
21. Fernandez-Capetillo, O., H.-T. Chen, A. Celeste, I. Ward, P.J. Romanienko, J.C. Morales, K. Naka, Z. Xia, R.D. Camerini-Otero, N. Motoyama, et al. 2002. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4:993-997.
22. Froelich-Ammon, SJ., and N. Osheroff. 1995. Topoisomerase poisons: harnessing the darkside of enzyme mechanism. J. Biol. Chem. 270:21429-21432.
23. Fukunaga, R., and T. Hunter. 1997. Mnk1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. EMBO J. 16:1921-1933.
24. Goldstone, S., S. Pavey, A. Forrest, J. Sinnamon, and B.C. Gabrielli. 2001. Cdc25-dependent activation of cyclinA/cdk2 is blocked in G2 phase arrested cells independently of ATM/ATR. Oncogene. 20:921-932.
25. Gorbsky, G.J. 1994. Cell cycle progression and chromosome segregation in mammalian cells cultured in the presence of topoisomerase II inhibitors ICRG-187 (+) 1,2-bis (3,4-dioxopiperazinyl-propane; ADR-529) and ICRF-159 (Razoxane). Cancer Res. 54:1042-1048.
26. Grunstein, M. 1997. Histone acetylation in chromatin structure and transcription. Nature. 389:349-352.
27. Gum, RJ., M.M. McLaughlin, S. Kumar, Z. Wang, M.J. Bower, J.C. Lee, J.L. Adams, G.P. Livi, E.J. Goldsmith, and P.R. Young, 1998. Acquisition of sensitivity of stress-activated protein kinases to the p38 inhibitor, SB 203580, by alteration of one or more amino acids within the ATP binding pocket. J. Biol. Chem. 273:15605-15610.
28. Han, J., J.-D. Lee, L. Bibbs, and R.J. Ulevitch. 1994. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science. 265:808-811.
29. Huang, K.-C., H. Gao, E.F. Yamasaki, D.R. Grabowski, S. Liu, L.L. Shen, K.K. Chan, and R.M. Snapka. 2001. Topoisomerase poisoning by ICRF-193. J. Biol. Chem. 276:44488-44494.
30. Illidge, T.M., M.S. Cragg, B. Fringes, P. Olive, and J.A. Erenpreisa. 2000. Polyploid giant cells provide a survival mechanism for p53 murant cells after DNA damage. Cell Biol. Internat. 24:621-633.
31. Jha, M.N., J.R. Bamburg, B.W. Bernstein, and J.S. Bedford. 2002. Caffeine eliminates gamma-ray-induced G2-phase delay in human tumor cells but not in normal cells. Radiat. Res. 157:26-31.
32. Kaufmann, W.K., C.B. Campbell, D.A. Simpson, P.B. Deming, L. Filatov, D.A. Galloway, X.J. Zhao, A.M. Creighton, and C.S. Downes. 2002. Degradation of ATM-independent decatenation checkpoint function in human cells is secondary to inactivation of p53 and correlated with chromosomal destabilization. Cell Cycle. 1:210-219.
33. Kellner, U., M. Sehested, P.B. Jensen, F. Giesseler, and P. Rudolph. 2002. Culprit and victim-DNA topoisomerase II. Lancet Oncol. 3:235-243.
34. Kharbanda, S., P. Pandey, S. Jln, S. Inoue, A. Bhareti, Z.-M. Yuan, R. Welchselbaum, D. Weaver, and SJ. Kuerbitz. 1997. Functional interaction between DNA-PK and c-Abl in response to DNA damage. Nature. 386:732-735.
35. Khodjakov, A., and C.L. Rieder. 2004. Imaging the division process in living tissue culture cells. Methods in Enzymology. In press.
36. Kyriakis, J.M., and J. Avruch. 2001. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81:807-869.
37. Lisnock, J., A. Tebben, B. Franz, E.A. O'Neill, G. Croft, S.J. O'Keefe, B. Li, C. Hacker, S.E. de Laszlo, A. Smith, et al. 1998. Molecular basis for p38 protein kinase inhibitor specificity. Biochemistry. 37:16573-16581.
38. Matsusaka, T., and J. Pines. 2004. Chfr acts with the p38 stress kinases to block entry into mitosis in mammalian cells. J. Cell Biol. 166:507-516.
39. Mikhailov, A., and C.L. Rieder. 2002. Stressed out of mitosis. Curr. Biol. 12: R331-R333.
40. Mikhailov, A., R.W. Cole, and C.L. Rieder. 2002. DNA damage during mitosis in human cells delays the metaphase/anaphase transition via the spindle-assembly checkpoint. Curr. Biol. 12:1797-1806.
41. Mitra, J., and G.H. Enders. 2004. Cyclin A/Cdk2 complexes regulate activation of Cdk1 and Cdc25 phosphacase in human cells. Oncogene. 23:3361-3367.
42. Perrin, D., B. van Hille, and B.T. Hill. 1998. Differential sensitivities of recombinant human topoisomerase II α and β to various classes of topoisomerase II-interacting agents. Biochem. Pharmacol. 56:503-507.
43. Pines, J., and C.L. Rieder. 2001. Re-staging mitosis: a contemporary view of mitotic progression. Nat. Cell Biol. 3:E3-E6.
44. Qiu, L., A. Burgess, D.P. Fairlie, H. Leonard, P.G. Parsons, and B.G. Gabrielli. 2000. Histone deacetylase inhibitors trigger a G2 checkpoint in normal cells that is defective in tumor cells. Mol. Biol. Cell. 11:2069-2083.
45. Rieder, C.L., and R.W. Cole. 1998. Entry into mitosis in vertebrate somatic cells is guarded by a chromosome damage checkpoint that reverses the cell cycle when triggered during early but not late prophase. J. Cell Biol. 142:1013-1022.
46. 2/M transition invertebrates. Curr. Biol. 10:1067-1070.
47. Rogakou, E.P., D.R. Pilch, A.H. Orr, V.S. Ivanova, and W.M. Bonner. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on Serine 139. J. Boil. Chem. 273:5858-5868.
48. Rogakou, E.P., C. Boone, C. Redon, and W.M. Bonner. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146: 905-915.
49. Scolnick, D.M., and T.D. Halazonetis, 2000. Chfr defines a mitotic stress checkpoint that delays entry into metaphase. Nature. 406:430-434.
50. Takenaka, K., T. Moriguchi, and E. Nishida. 1998. Activation of the protein kinase p38 in the spindle assembly checkpoint and mitotic arrest. Science. 280: 599-602.
51. Tavormina, P.A., M.-G. Come, J.R. Hudson, Y.-Y. Mo, W.T. Beck, and G.J. Gorbsky. 2002. Rapid exchange of mammalian topoisomerase IIa at kinetochores and chromosome arms in mitosis. J. Cell Biol. 158:23-29.
52. Teillaud, J.L., N. Gruel, J. Moncuit, Z. Mishal, W.H. Fridman, T.J. Lampidis, and H. Tapiero. 1998. Structurally different anthracyclines provoke different effects on cell cycle and tumor B cell differentiation. Biomed. Pharmacother. 52:282-290.
53. Tsuiki, H., M. Nitta, M. Tada, M. Inagaki, Y. Ushio, and H. Saya. 2001. Mechanism of hyperploid cell formation induced by microtubule inhibiting drug in glioma cell lines. Oncogene. 20:420-429.
54. Wang, L., and D.A. Eastmond. 2002. Catalytic inhibitors of topoisomerase II are DNA-damaging agents: induction of chromosomal damage by merbarone and ICRF-187. Environ. Mol. Mutagen. 39:348-356.
55. Witt, O., S. Monkemeyer, G. Ronndahl, B. Erdlenbruch, D. Reinhardt, K. Kanbach, and A. Pekrun. 2003. Induction of fetal hemoglobin expression by the histone deacetylase inhibitor apicidin. Blood. 101:2001-2007.
56. 2/M checkpoints are induced by ionizing irradiation. Mol. Cell. Biol. 22: 1049-1059.
57. Zhou, B.-B.S., P. Chaturvedi, K. Spring, S.P. Scott, R.A. Johanson, R. Mishra, M.R. Mattern, J.D. Winkler, and K.K. Khanna. 2000. Caffeine abolishes the mammalian G2/M DNA damage checkpoint by inhibiting Ataxia-Tangiectasia- mutated kinase activity. J. Biol. Chem. 275:10342-10348.