FK228 induces mitotic catastrophe in A549 cells by mistargeting chromosomal passenger complex localization through changing centromeric H3K9 hypoacetylation

Acta Biochimica et Biophysica Sinica

Volumn 42, Issue 10, 2010, Pages 677-687

  Zhang, Xuhui ^a   Zhang, Zhiyi ^b   Chen, Guozhu ^a   Zhao, Ming ^a   Wang, Di ^a   Zhang, Xuemin ^b   Du, Zhiyan ^a   Xu, Yuanji ^a   Yu, Xiaodan ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b NATIONAL CENTER OF BIOMEDICAL ANALYSIS   (China)

Author keywords

acetylation; centromere; chromosomal passenger complex; epigenetic; histone; mitosis

Indexed keywords

ANTINEOPLASTIC ANTIBIOTIC; AUTOANTIGEN; CENTROMERE PROTEIN A; DEPSIPEPTIDE; HISTONE; LYSINE; NONHISTONE PROTEIN; ROMIDEPSIN; SERINE;

ACETYLATION; ARTICLE; CELL SURVIVAL; CENTROMERE; DRUG EFFECT; FLUORESCENCE MICROSCOPY; HUMAN; METABOLISM; METHYLATION; MITOSIS; MITOSIS SPINDLE; PHOSPHORYLATION; TIME; TUMOR CELL LINE; WESTERN BLOTTING;

ACETYLATION; ANTIBIOTICS, ANTINEOPLASTIC; AUTOANTIGENS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; CENTROMERE; CHROMOSOMAL PROTEINS, NON-HISTONE; DEPSIPEPTIDES; HISTONES; HUMANS; LYSINE; METHYLATION; MICROSCOPY, FLUORESCENCE; MITOSIS; MITOTIC SPINDLE APPARATUS; PHOSPHORYLATION; SERINE; TIME FACTORS;

EID: 77957294998     PISSN: 16729145     EISSN: 17457270     Source Type: Journal    
DOI: 10.1093/abbs/gmq077     Document Type: Article

References (54)

1. Cooke CA, Heck MM and Earnshaw WC. The inner centromere protein (INCENP) antigens: Movement from inner centromere to midbody during mitosis. J Cell Biol 1987, 105: 2053-2067.
2. Andrews PD, Knatko E, Moore WJ and Swedlow JR. Mitotic mechanics: The auroras come into view. Curr Opin Cell Biol 2003, 15: 672-683.
3. Uren AG, Wong L, Pakusch M, Fowler KJ, Burrows FJ, Vaux DL and Choo KH. Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype. Curr Biol 2000, 10: 1319-1328.
4. Vagnarelli P and Earnshaw WC. Chromosomal passengers: The fourdimensional regulation of mitotic events. Chromosoma 2004, 113: 211-222.
5. Carvalho A, Carmena M, Sambade C, Earnshaw WC and Wheatley SP. Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J Cell Sci 2003, 116: 2987-2998.
6. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T and Mortlock A, et al. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. Cell Biol 2003, 161: 267-280.
7. Gassmann R, Carvalho A, Henzing AJ, Ruchaud S, Hudson DF, Honda R and Nigg EA, et al. Borealin: A novel chromosomal passenger required for stability of the bipolar mitotic spindle. J Cell Biol 2004, 166: 179-191.
8. Ricci MS and Zong WX. Chemotherapeutic approaches for targeting cell death pathways. Oncologist 2006, 11: 342-357.
9. Budillon A, Bruzzese F, Di Gennaro E and Caraglia M. Multiple-target drugs: Inhibitors of heat shock protein 90 and of histone deacetylase. Curr Drug Targets 2005, 6: 337-351.
10. Ueda H, Nakajima H, Hori Y, Fujita T, Nishimura M, Goto T and Okuhara M. FR901228, a novel antitumor bicyclic depsipeptide produced by Chromobacterium violaceum No. 968. I. Taxonomy, fermentation, isolation, physico-chemical and biological properties, and antitumor activity. J Antibiot (Tokyo) 1994, 47: 301-310.
11. Furumai R, Matsuyama A, Kobashi N, Lee KH, Nishiyama M, Nakajima H and Tanaka A, et al. FK228 (Depsipeptide) as a natural prodrug that inhibits class I histone deacetylases. Cancer Res 2002, 62: 4916-4921.
12. Sasakawa Y, Naoe Y, Inoue T, Sasakawa T, Matsuo M, Manda T and Mutoh S. Effects of FK228, a novel histone deacetylase inhibitor, on human lymphoma U-937 cells in vitro and in vivo. Biochem Pharmacol 2002, 64: 1079-1090.
13. Zhao Y, Lu S, Wu L, Chai G, Wang H, Chen Y and Sun J, et al. Acetylation of p53 at lysine 373/382 by the histone deacetylase inhibitor depsipeptide induces expression of p21(Waf1/Cip1). Mol Cell Biol 2006, 26: 2782-2790.
14. Yu X, Guo ZS, Marcu MG, Neckers L, Nguyen DM, Chen GA and Schrump DS. Modulation of p53, ErbB1, ErbB2, and Raf-1 expression in lung cancer cells by depsipeptide FR901228. J Natl Cancer Inst 2002, 94: 504-513.
15. Wang Y, Wang SY, Zhang XH, Zhao M, Hou CM, Xu YJ and Du ZY, et al. FK228 inhibits Hsp90 chaperone function in K562 cells via hyperacetylation of Hsp70. Biochem Biophys Res Commun 2007, 356: 998-1003.
16. Zhou W and Zhu WG. The changing face of HDAC inhibitor depsipeptide. Curr Cancer Drug Targets 2009, 9: 91-100.
17. Sandor V, Robbins AR, Robey R, Myers T, Sausville E, Bates SE and Sackett DL. FR901228 causes mitotic arrest but does not alter microtubule polymerization. Anticancer Drugs 2000, 11: 445-454.
18. Turner BM. Decoding the nucleosome. Cell 1993, 75: 5-8.
19. Cimini D, Mattiuzzo M, Torosantucci L and Degrassi F. Histone hyperacetylation in mitosis prevents sister chromatid separation and produces chromosome segregation defects. Mol Biol Cell 2003, 14: 3821-3833.
20. Shin HJ, Baek KH, Jeon AH, Kim SJ, Jang KL, Sung YC and Kim CM, et al. Inhibition of histone deacetylase activity increases chromosomal instability by the aberrant regulation of mitotic checkpoint activation. Oncogene 2003, 22: 3853-3858.
21. Stevens FE, Beamish H, Warrener R and Gabrielli B. Histone deacetylase inhibitors induce mitotic slippage. Oncogene 2008, 27: 1345-1354.
22. Zhang XH, Rao M, Loprieato JA, Hong JA, Zhao M, Chen GZ and Humphries AE. Aurora A, aurora B and survivin are novel targets of transcriptional regulation by histone deacetylase inhibitors in non-small cell lung cancer. Cancer Biol Ther 2008, 7: 1387-1396.
23. Cheeseman IM and Desai A. Molecular architecture of the kinetochoremicrotubule interface. Nat Rev Mol Cell Biol 2008, 9: 33-46.
24. Holliday R. The inheritance of epigenetic defects. Science 1987, 238: 163-170.
25. Turner BM. Reading signals on the nucleosome with a new nomenclature for modified histones. Nat Struct Mol Biol 2005, 12: 110-112.
26. Richards EJ and Elgin SC. Epigenetic codes for heterochromatin formation and silencing: Rounding up the usual suspects. Cell 2002, 108: 489-500.
27. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR and Bazett-Jones DP, et al. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 1997, 106: 348-360.
28. Vader G, Kauw JJ, Medema RH and Lens SM. Survivin mediates targeting of the chromosomal passenger complex to the centromere and midbody. EMBO Rep 2006, 7: 85-92.
29. Monier K, Mouradian S and Sullivan KF. DNA methylation promotes Aurora B-driven phosphorylation of histone H3 in chromosomal subdomains. J Cell Sci 2007, 120: 101-114.
30. Johnson VL, Scott MI, Holt SV, Hussein D and Taylor SS. Bub1 is required for kinetochore localization of BubR1, Cenp-E, Cenp-F and Mad2, and chromosome congression. J Cell Sci 2004, 117: 1577-1589.
31. Strahl BD and Allis CD. The language of covalent histone modifications. Nature 2000, 403: 41-45.
32. Aron JL, Parthun MR, Marcucci G, Kitada S, Mone AP, Davis ME and Shen T, et al. Depsipeptide (FR901228) induces histone acetylation and inhibition of histone deacetylase in chronic lymphocytic leukemia cells concurrent with activation of caspase 8-mediated apoptosis and downregulation of c-FLIP protein. Blood 2003, 102: 652-658.
33. Robbins AR, Jablonski SA, Yen TJ, Yoda K, Robey R, Bates SE and Sackett DL. Inhibitors of histone deacetylases alter kinetochore assembly by disrupting pericentromeric heterochromatin. Cell Cycle 2005, 4: 717-726.
34. Wu R, Terry AV, Singh PB and Gilbert DM. Differential subnuclear localization and replication timing of histone H3 lysine 9 methylation states. Mol Biol Cell 2005, 16: 2872-2881.
35. Lange BM, Rebollo E, Herold A and González C. Cdc37 is essential for chromosome segregation and cytokinesis in higher eukaryotes. EMBO J 2002, 21: 5364-5374.
36. Fortugno P, Beltrami E, Plescia J, Fontana J, Pradhan D, Marchisio PC and Sessa WC, et al. Regulation of survivin function by Hsp90. Proc Natl Acad Sci USA 2003, 100: 13791-13796.
37. Klein UR, Nigg EA and Gruneberg U. Centromere targeting of the chromosomal passenger complex equires a ternary subcomplex of Borealin, Survivin, and the N-terminal domain of INCENP. Mol Biol Cell 2006, 17: 2547-2558.
38. Hammond JW, Cai D and Verhey KJ. Tubulin modifications and their cellular functions. Curr Opin Cell Biol 2008, 20: 71-76.
39. Piperno G, LeDizet M and Chang XJ. Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J Cell Biol 1987, 104: 289-302.
40. Blagosklonny MV, Robey R, Sackett DL, Du L, Traganos F, Darzynkiewicz Z and Fojo T, et al. Histone deacetylase inhibitors all induce p21 but differentially cause tubulin acetylation, mitotic arrest, and cytotoxicity. Mol Cancer Ther 2002, 1: 937-941.
41. Greiner D, Bonaldi T, Eskeland R, Roemer E and Imhof A. Identification of a specific inhibitor of the histone methyltransferase SU(VAR)3-9. Nat Chem Biol 2005, 1: 143-145.
42. Bebbington D, Binch H, Charrier JD, Everitt S, Fraysse D, Golec J and Kay D, et al. The discovery of the potent aurora inhibitor MK-0457 (VX-680). Bioorg Med Chem Lett 2009, 19: 3586-3592.
43. Earnshaw WC and Bernat RL. Chromosomal passengers: Toward an integrated view of mitosis. Chromosoma 1991, 100: 139-146.
44. Heit R, Underhill DA, Chan G and Hendzel MJ. Epigenetic regulation of centromere formation and kinetochore function. Biochem Cell Biol 2006, 84: 605-618.
45. Zeitlin SG, Shelby RD and Sullivan KF. CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis. J Cell Biol 2001, 155: 1147-1157.
46. Vernarecci S, Ornaghi P, Bâgu A, Cundari E, Ballario P and Filetici P. Gcn5p plays an important role in centromere kinetochore function in budding yeast. Mol Cell Biol 2008, 28: 988-996.
47. Fischle W, Tseng BS, Dormann HL, Ueberheide BM, Garcia BA, Shabanowitz J and Hunt DF, et al. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 2005, 438: 1116-1122.
48. Wu LP, Wang X, Li L, Zhao Y, Lu S, Yu Y and Zhou W, et al. Histone deacetylase inhibitor depsipeptide activates silenced genes through decreasing both CpG and H3K9 methylation on the promoter. Mol Cell Biol 2008, 28: 3219-3235.
49. Taddei A, Maison C, Roche D and Almouzni G. Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat Cell Biol 2001, 3: 114-120.
50. Zhang R, Liu ST, Chen W, Bonner M, Pehrson J, Yen TJ and Adams PD. HP1 proteins are essential for a dynamic nuclear response that rescues the function of perturbed heterochromatin in primary human cells. Mol Cell Biol 2007, 27: 949-962.
51. Kunitoku N, Sasayama T, Marumoto T, Zhang D, Honda S, Kobayashi O and Hatakeyama K, et al. CENP-A phosphorylation by Aurora-A in prophase is required for enrichment of Aurora-B at inner centromeres and for kinetochore function. Dev Cell 2003, 5: 853-864.
52. Ruchaud S, Carmena M and Earnshaw WC. Chromosomal passengers: Conducting cell division. Nat Rev Mol Cell Biol 2007, 8: 798-812.
53. Murata-Hori M and Wang YL. The kinase activity of aurora B is required for kinetochore-microtubule interactions during mitosis. Curr Biol 2002, 12: 894-899.
54. Honda R, Korner R and Nigg EA. Exploring the functional interactions between Aurora B, INCENP, and survivin in mitosis. Mol Biol Cell 2003, 14: 3325-3341.