Concurrent inhibition of enzymatic activity and NF-Y-mediated transcription of Topoisomerase-IIa by bis-DemethoxyCurcumin in cancer cells

Cell Death and Disease

Volumn 4, Issue 8, 2013, Pages

  Belluti, S ^a   Basile, V ^a   Benatti, P ^a   Ferrari, E ^a   Marverti, G ^b   Imbriano, C ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b Dipartimento di Scienze Biomediche Metaboliche e Neuroscienze   (Italy)

Author keywords

CCAAT box; Curcuminoids; Gene transcription; NF Y; TOP2A

Indexed keywords

ACETYLCYSTEINE; CCAAT BINDING FACTOR; CURCUMIN; DEMETHOXYCURCUMIN; DNA TOPOISOMERASE 2ALPHA; ETOPOSIDE; HISTONE H2AX; NUCLEAR FACTOR Y; SMALL INTERFERING RNA; TOP2A PROTEIN; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL DEATH; CELL PROLIFERATION; CELL STRAIN HCT116; CELL VIABILITY; CELLULAR DISTRIBUTION; CHROMATIN; CHROMOSOME ABERRATION; CONTROLLED STUDY; CURCUMA LONGA; DEACETYLATION; DNA DAMAGE; DNA METABOLISM; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME INHIBITION; FERTILITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IC 50; INTERPHASE; MITOSIS; ORGANIZATION; PRIORITY JOURNAL; PROTEIN BINDING;

ANTIGENS, NEOPLASM; APOPTOSIS; CCAAT-BINDING FACTOR; CELL PROLIFERATION; COLORECTAL NEOPLASMS; CURCUMIN; DNA BREAKS, DOUBLE-STRANDED; DNA TOPOISOMERASES, TYPE II; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HCT116 CELLS; HUMANS; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE;

EID: 84882727195     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.287     Document Type: Article

References (60)

1. Yang X, Li W, Prescott ED, Burden SJ, Wang JC. DNA topoisomerase IIbeta and neural development. Science 2000; 287: 131-134 (Pubitemid 30033236)
2. Khelifa T, Casabianca-Pignede MR, Rene B, Jacquemin-Sablon A. Expression of topoisomerases II alpha and beta in Chinese hamster lung cells resistant to topoisomerase II inhibitors. Mol Pharmacol 1994; 46: 323-328 (Pubitemid 24271428)
3. Laemmli UK, Kas E, Poljak L, Adachi Y. Scaffold-Associated regions: Cis-Acting determinants of chromatin structural loops and functional domains. Curr Opin Genet Dev 1992; 2: 275-285
4. Warburton PE, Earnshaw WC. Untangling the role of DNA topoisomerase II in mitotic chromosome structure and function. Bioessays 1997; 19: 97-99 (Pubitemid 27114957)
5. Akimitsu N, Adachi N, Hirai H, Hossain MS, Hamamoto H, Kobayashi M et al. Enforced cytokinesis without complete nuclear division in embryonic cells depleting the activity of DNA topoisomerase IIalpha. Genes Cells 2003; 8: 393-402 (Pubitemid 36504014)
6. Heck MM, Hittelman WN, Earnshaw WC. Differential expression of DNA topoisomerases I and II during the eukaryotic cell cycle. Proc Natl Acad Sci USA 1988; 85: 1086-1090 (Pubitemid 18073961)
7. Woessner RD, Mattern MR, Mirabelli CK, Johnson RK, Drake FH. Proliferation-And cell cycle-dependent differences in expression of the 170 kilodalton and 180 kilodalton forms of topoisomerase II in NIH-3T3 cells. Cell Growth Differ 1991; 2: 209-214
8. Negri C, Chiesa R, Cerino A, Bestagno M, Sala C, Zini N et al. Monoclonal antibodies to human DNA topoisomerase I and the two isoforms of DNA topoisomerase II: 170-And 180-kDa isozymes. Exp Cell Res 1992; 200: 452-459
9. Hochhauser D, Stanway CA, Harris AL, Hickson ID. Cloning and characterization of the 5'-flanking region of the human topoisomerase II alpha gene. J Biol Chem 1992; 267: 18961-18965
10. Adachi N, Nomoto M, Kohno K, Koyama H. Cell-cycle regulation of the DNA topoisomerase IIalpha promoter is mediated by proximal CCAAT boxes: Possible involvement of acetylation. Gene 2000; 245: 49-57 (Pubitemid 30125363)
11. Falck J, Jensen PB, Sehested M. Evidence for repressional role of an inverted CCAAT box in cell cycle-dependent transcription of the human DNA topoisomerase IIalpha gene. J Biol Chem 1999; 274: 18753-18758
12. Yoon JH, Kim JK, Rha GB, Oh M, Park SH, Seong RH et al. Sp1 mediates cell proliferation-dependent regulation of rat DNA topoisomerase IIalpha gene promoter. Biochem J 1999; 344(Pt 2): 367-374 (Pubitemid 30011591)
13. Mantovani R. The molecular biology of the CCAAT-binding factor NF-Y. Gene 1999; 239: 15-27 (Pubitemid 29462565)
14. Isaacs RJ, Harris AL, Hickson ID. Regulation of the human topoisomerase IIalpha gene promoter in confluence-Arrested cells. J Biol Chem 1996; 271: 16741-16747 (Pubitemid 26239038)
15. Joshi AA, Wu Z, Reed RF, Suttle DP. Nuclear factor-Y binding to the topoisomerase IIalpha promoter is inhibited by both the p53 tumor suppressor and anticancer drugs. Mol Pharmacol 2003; 63: 359-367 (Pubitemid 36158371)
16. Wang Q, Zambetti GP, Suttle DP. Inhibition of DNA topoisomerase II alpha gene expression by the p53 tumor suppressor. Mol Cell Biol 1997; 17: 389-397 (Pubitemid 26425628)
17. Turley H, Comley M, Houlbrook S, Nozaki N, Kikuchi A, Hickson ID et al. The distribution and expression of the two isoforms of DNA topoisomerase II in normal and neoplastic human tissues. Br J Cancer 1997; 75: 1340-1346 (Pubitemid 27179826)
18. Nitiss JL. Targeting DNA topoisomerase II in cancer chemotherapy. Nat Rev Cancer 2009; 9: 338-350
19. McClendon AK, Osheroff N. DNA topoisomerase II, genotoxicity, and cancer. Mutat Res 2007; 623: 83-97 (Pubitemid 47368578)
20. Kaufmann SH. Cell death induced by topoisomerase-Targeted drugs: More questions than answers. Biochim Biophys Acta 1998; 1400: 195-211 (Pubitemid 28475104)
21. Limbo O, Chahwan C, Yamada Y, de Bruin RA, Wittenberg C, Russell P. Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol Cell 2007; 28: 134-146 (Pubitemid 47531975)
22. Mao Y, Desai SD, Ting CY, Hwang J, Liu LF. 26 S proteasome-mediated degradation of topoisomerase II cleavable complexes. J Biol Chem 2001; 276: 40652-40658
23. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J et al. Human CtIP promotes DNA end resection. Nature 2007; 450: 509-514 (Pubitemid 350190253)
24. Felix CA. Secondary leukemias induced by topoisomerase-Targeted drugs. Biochim Biophys Acta 1998; 1400: 233-255 (Pubitemid 28475107)
25. Mistry AR, Felix CA, Whitmarsh RJ, Mason A, Reiter A, Cassinat B et al. DNA topoisomerase II in therapy-related acute promyelocytic leukemia. N Engl J Med 2005; 352: 1529-1538 (Pubitemid 40517093)
26. Myers CE, McGuire WP, Liss RH, Ifrim I, Grotzinger K, Young RC. Adriamycin: The role of lipid peroxidation in cardiac toxicity and tumor response. Science 1977; 197: 165-167 (Pubitemid 8140036)
27. Velez JM, Miriyala S, Nithipongvanitch R, Noel T, Plabplueng CD, Oberley T et al. p53 Regulates oxidative stress-mediated retrograde signaling: A novel mechanism for chemotherapy-induced cardiac injury. PLoS One 2011; 6: E18005
28. Chauhan DP. Chemotherapeutic potential of curcumin for colorectal cancer. Curr Pharm Des 2002; 8: 1695-1706 (Pubitemid 34846196)
29. Jiang MC, Yang-Yen HF, Yen JJ, Lin JK. Curcumin induces apoptosis in immortalized NIH 3T3 and malignant cancer cell lines. Nutr Cancer 1996; 26: 111-120 (Pubitemid 26268581)
30. Song G, Mao YB, Cai QF, Yao LM, Ouyang GL, Bao SD. Curcumin induces human HT-29 colon adenocarcinoma cell apoptosis by activating p53 and regulating apoptosisrelated protein expression. Braz J Med Biol Res 2005; 38: 1791-1798 (Pubitemid 43078608)
31. Martin-Cordero C, Lopez-Lazaro M, Galvez M, Ayuso MJ. Curcumin as a DNA topoisomerase II poison. J Enzyme Inhib Med Chem 2003; 18: 505-509 (Pubitemid 37493386)
32. Lopez-Lazaro M, Willmore E, Jobson A, Gilroy KL, Curtis H, Padget K et al. Curcumin induces high levels of topoisomerase I-And II-DNA complexes in K562 leukemia cells. J Nat Prod 2007; 70: 1884-1888
33. Magalska A, Brzezinska A, Bielak-Zmijewska A, Piwocka K, Mosieniak G, Sikora E. Curcumin induces cell death without oligonucleosomal DNA fragmentation in quiescent and proliferating human CD8 cells. Acta Biochim Pol 2006; 53: 531-538 (Pubitemid 44563721)
34. Korwek Z, Bielak-Zmijewska A, Mosieniak G, Alster O, Moreno-Villanueva M, Burkle A et al. DNA damage-independent apoptosis induced by curcumin in normal resting human T cells and leukaemic Jurkat cells. Mutagenesis 2013; 28: 411-416
35. Bielak-Zmijewska A, Sikora-Polaczek M, Nieznanski K, Mosieniak G, Kolano A, Maleszewski M et al. Curcumin disrupts meiotic and mitotic divisions via spindle impairment and inhibition of CDK1 activity. Cell Prolif 2010; 43: 354-364
36. Basile V, Ferrari E, Lazzari S, Belluti S, Pignedoli F, Imbriano C. Curcumin derivatives: Molecular basis of their anti-cancer activity. Biochem Pharmacol 2009; 78: 1305-1315
37. Yodkeeree S, Chaiwangyen W, Garbisa S, Limtrakul P. Curcumin, demethoxycurcumin and bisdemethoxycurcumin differentially inhibit cancer cell invasion through the down-regulation of MMPs and uPA. J Nutr Biochem 2009; 20: 87-95
38. Anand P, Thomas SG, Kunnumakkara AB, Sundaram C, Harikumar KB, Sung B et al. Biological activities of curcumin and its analogues (Congeners) made by man and Mother Nature. Biochem Pharmacol 2008; 76: 1590-1611
39. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 2000; 10: 886-895 (Pubitemid 30647617)
40. Bakkenist CJ, Kastan MB. Initiating cellular stress responses. Cell 2004; 118: 9-17 (Pubitemid 38902810)
41. Shiloh Y. ATM and related protein kinases: Safeguarding genome integrity. Nat Rev Cancer 2003; 3: 155-168 (Pubitemid 37328868)
42. 3 mutants. Oncogene 2000; 19: 5788-5800
43. Block WD, Merkle D, Meek K, Lees-Miller SP. Selective inhibition of the DNA-dependent protein kinase (DNA-PK) by the radiosensitizing agent caffeine. Nucleic Acids Res 2004; 32: 1967-1972 (Pubitemid 38849355)
44. Deplanque G, Ceraline J, Mah-Becherel MC, Cazenave JP, Bergerat JP, Klein-Soyer C. Caffeine and the G2/M block override: A concept resulting from a misleading cell kinetic delay, independent of functional p53. Int J Cancer 2001; 94: 363-369 (Pubitemid 32906066)
45. Kesharwani KR, Misra K. Prediction of binding site for curcuminoids at human toposomerase II a protein; an in silico approach. Curr Sci 2011; 101: 1060-1065
46. Agostinho M, Rino J, Braga J, Ferreira F, Steffensen S, Ferreira J. Human topoisomerase IIalpha: Targeting to subchromosomal sites of activity during interphase and mitosis. Mol Biol Cell 2004; 15: 2388-2400 (Pubitemid 38580654)
47. Ceribelli M, Dolfini D, Merico D, Gatta R, Vigano AM, Pavesi G et al. The histone-like NF-Y is a bifunctional transcription factor. Mol Cell Biol 2008; 28: 2047-2058 (Pubitemid 351342634)
48. 4 trimethylation on CCAAT promoters. PLoS One 2011; 6: E17220
49. Frontini M, Imbriano C, Manni I, Mantovani R. Cell cycle regulation of NF-YC nuclear localization. Cell Cycle 2004; 3: 217-222 (Pubitemid 40268700)
50. Magan N, Szremska AP, Isaacs RJ, Stowell KM. Modulation of DNA topoisomerase II alpha promoter activity by members of the Sp (specificity protein) and NF-Y (nuclear factor Y) families of transcription factors. Biochem J 2003; 374(Pt 3): 723-729 (Pubitemid 37163917)
51. Romero A, Martin M, Cheang MC, Lopez Garcia-Asenjo JA, Oliva B, He X et al. Assessment of Topoisomerase II alpha status in breast cancer by quantitative PCR, gene expression microarrays, immunohistochemistry, and fluorescence in situ hybridization. Am J Pathol 2011; 178: 1453-1460
52. Zaczek AJ, Markiewicz A, Seroczynska B, Skokowski J, Jaskiewicz J, Pienkowski T et al. Prognostic significance of TOP2A gene dosage in HER-2-negative breast cancer. Oncologist 2012; 17: 1246-1255
53. Miettinen HE, Jarvinen TA, Kellner U, Kauraniemi P, Parwaresch R, Rantala I et al. High topoisomerase IIalpha expression associates with high proliferation rate and and poor prognosis in oligodendrogliomas. Neuropathol Appl Neurobiol 2000; 26: 504-512 (Pubitemid 32049849)
54. Basile V, Belluti S, Ferrari E, Gozzoli C, Ganassi S, Quaglino D et al. bis-dehydroxycurcumin triggers mitochondrial-Associated cell death in human colon cancer cells through ER-stress induced autophagy. PLoS One 2013; 8: E53664
55. Ravindran J, Prasad S, Aggarwal BB. Curcumin and cancer cells: How many ways can curry kill tumor cells selectively? AAPS J 2009; 11: 495-510
56. Hajji N, Pastor N, Mateos S, Dominguez I, Cortes F. DNA strand breaks induced by the anti-Topoisomerase II bis-dioxopiperazine ICRF-193. Mutat Res 2003; 530: 35-46 (Pubitemid 37237506)
57. Benatti P, Dolfini D, Vigano A, Ravo M, Weisz A, Imbriano C. Specific inhibition of NF-Y subunits triggers different cell proliferation defects. Nucleic Acids Res 2011; 39: 5356-5368
58. Goodarzi H, Elemento O, Tavazoie S. Revealing global regulatory perturbations across human cancers. Mol Cell 2009; 36: 900-911
59. Rhodes DR, Kalyana-Sundaram S, Mahavisno V, Barrette TR, Ghosh D, Chinnaiyan AM. Mining for regulatory programs in the cancer transcriptome. Nat Genet 2005; 37: 579-583 (Pubitemid 40770410)
60. Yamanaka K, Mizuarai S, Eguchi T, Itadani H, Hirai H, Kotani H. Expression levels of NF-Y target genes changed by CDKN1B correlate with clinical prognosis in multiple cancers. Genomics 2009; 94: 219-227