An Iridium(III) Complex Inhibits JMJD2 Activities and Acts as a Potential Epigenetic Modulator

Journal of Medicinal Chemistry

Volumn 58, Issue 16, 2015, Pages 6697-6703

  Liu, Li Juan ^a   Lu, Lihua ^b   Zhong, Hai Jing ^a   He, Bingyong ^b   Kwong, Daniel W J ^b   Ma, Dik Lung ^b   Leung, Chung Hang ^a  

^a University of Macau   (Macao)

^b HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

EPIGENETIC READER DOMAIN INHIBITOR; HISTONE DEMETHYLASE; IRIDIUM COMPLEX; IRIDIUM COMPLEX 1; JMJD2 PROTEIN; JMJD3 PROTEIN; PROTEIN P21; UNCLASSIFIED DRUG; HISTONE; IRIDIUM; IRON; KDM4D PROTEIN, HUMAN; ORGANOMETALLIC COMPOUND;

APOPTOSIS; ARTICLE; BIOLOGICAL ACTIVITY; CANCER INHIBITION; CARBON NUCLEAR MAGNETIC RESONANCE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG SYNTHESIS; ENZYME INHIBITION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; MASS SPECTROMETRY; PROTEIN PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; GENETIC EPIGENESIS; GENETICS; METABOLISM; TUMOR CELL LINE;

APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; EPIGENESIS, GENETIC; HISTONES; HUMANS; IRIDIUM; IRON; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; ORGANOMETALLIC COMPOUNDS;

EID: 84940539379     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/acs.jmedchem.5b00375     Document Type: Article

References (59)

1. Chavain, N.; Biot, C. Organometallic complexes: new tools for chemotherapy Curr. Med. Chem. 2010, 17, 2729-2745 10.2174/092986710791859306
2. Gasser, G.; Ott, I.; Metzler-Nolte, N. Organometallic anticancer compounds J. Med. Chem. 2011, 54, 3-25 10.1021/jm100020w
3. Patra, M.; Gasser, G. Organometallic compounds: an opportunity for chemical biology? ChemBioChem 2012, 13, 1232-1252 10.1002/cbic.201200159
4. Groessl, M.; Hartinger, C. G. Anticancer metallodrug research analytically painting the "omics" picture-current developments and future trends Anal. Bioanal. Chem. 2013, 405, 1791-1808 10.1007/s00216-012-6450-4
5. Hartinger, C. G.; Phillips, A. D.; Nazarov, A. A. Polynuclear ruthenium, osmium and gold complexes. The quest for innovative anticancer chemotherapeutics Curr. Top. Med. Chem. 2011, 11, 2688-2702 10.2174/156802611798040769
6. Gao, F.; Chao, H.; Ji, L. N. DNA Binding, photocleavage, and topoisomerase inhibition of functionalized ruthenium(II)-polypyridine complexes Chem. Biodiversity 2008, 5, 1962-1979 10.1002/cbdv.200890181
7. Huang, H.; Zhang, P.; Yu, B.; Chen, Y.; Wang, J.; Ji, L.; Chao, H. Targeting nucleus DNA with a cyclometalated dipyridophenazineruthenium(II) complex J. Med. Chem. 2014, 57, 8971-8983 10.1021/jm501095r
8. Feng, L.; Geisselbrecht, Y.; Blanck, S.; Wilbuer, A.; Atilla-Gokcumen, G. E.; Filippakopoulos, P.; Kraling, K.; Celik, M. A.; Harms, K.; Maksimoska, J.; Marmorstein, R.; Frenking, G.; Knapp, S.; Essen, L. O.; Meggers, E. Structurally sophisticated octahedral metal complexes as highly selective protein kinase inhibitors J. Am. Chem. Soc. 2011, 133, 5976-5986 10.1021/ja1112996
9. Meggers, E. Targeting proteins with metal complexes Chem. Commun. 2009, 1001-1010 10.1039/b813568a
10. Farrell, N. P. Platinum formulations as anticancer drugs clinical and pre-clinical studies Curr. Top. Med. Chem. 2011, 11, 2623-2631 10.2174/156802611798040714
11. Chui, S. S. Y.; Chen, R.; Che, C. M. A chiral [2]catenane precursor of the antiarthritic gold(I) drug auranofin Angew. Chem., Int. Ed. 2006, 45, 1621-1624 10.1002/anie.200503431
12. Gasser, G.; Metzler-Nolte, N. The potential of organometallic complexes in medicinal chemistry Curr. Opin. Chem. Biol. 2012, 16, 84-91 10.1016/j.cbpa.2012.01.013
13. Lin, Y.; Huang, Y. D.; Zheng, W.; Wang, F. Y.; Habtemariam, A.; Luo, Q.; Li, X. C.; Wu, K.; Sadler, P. J.; Xiong, S. X. Organometallic ruthenium anticancer complexes inhibit human glutathione-S-transferase pi J. Inorg. Biochem. 2013, 128, 77-84 10.1016/j.jinorgbio.2013.07.029
14. Kostrhunova, H.; Florian, J.; Novakova, O.; Peacock, A. F. A.; Sadler, P. J.; Brabec, V. DNA interactions of monofunctional organometallic osmium(II) antitumor complexes in cell-free media J. Med. Chem. 2008, 51, 3635-3643 10.1021/jm701538w
15. Ma, D.-L.; Chan, D. S.-H.; Leung, C.-H. Group 9 Organometallic compounds for therapeutic and bioanalytical applications Acc. Chem. Res. 2014, 47, 3614-3631 10.1021/ar500310z
16. Leung, C.-H.; Lin, S.; Zhong, H.-J.; Ma, D.-L. Metal complexes as potential modulators of inflammatory and autoimmune responses Chem. Sci. 2015, 6, 871-884 10.1039/C4SC03094J
17. Zhong, H.-J.; Lu, L.; Wong, C. C. L.; Peng, C.; Yan, S.-C.; Ma, D.-L.; Cai, Z.; Wang, H. M.; Leung, C.-H. An iridium(III)-based irreversible protein-protein interaction inhibitor of BRD4 as a potent anticancer agent Chem. Commun. 2015, 51, 11178 10.1039/C5SC02321A
18. Leung, C.-H.; Liu, L.-J.; Lu, L.; He, B.; Kwong, D. W. J.; Wong, C. Y.; Ma, D.-L. A metal-based tumour necrosis factor-alpha converting enzyme inhibitor Chem. Commun. 2015, 51, 3973-3976 10.1039/C4CC09251A
19. Ma, D.-L.; He, H.-Z.; Zhong, H.-J.; Lin, S.; Chan, D. S.-H.; Wang, L.; Lee, S. M. Y.; Leung, C.-H.; Wong, C. Y. Visualization of Zn2+ Ions in Live Zebrafish Using a Luminescent Iridium(III) Chemosenso ACS Appl. Mater. Interfaces 2014, 6, 14008-14015 10.1021/am504369b
20. Ma, D.-L.; Liu, L.-J.; Leung, K.-H.; Chen, Y. T.; Zhong, H.-J.; Chan, D. S.-H.; Wang, H. M. D.; Leung, C.-H. Antagonizing STAT3 dimerization with a rhodium(III) complex Angew. Chem., Int. Ed. 2014, 53, 9178-9182 10.1002/anie.201404686
21. Zhong, H.-J.; Leung, K.-H.; Liu, L.-J.; Lu, L.; Chan, D. S.-H.; Leung, C.-H.; Ma, D.-L. Antagonism of mTOR Activity by a Kinetically Inert Rhodium(III) Complex ChemPlusChem 2014, 79, 508-511 10.1002/cplu.201400014
22. Zhong, H.-J.; Yang, H.; Chan, D. S.-H.; Leung, C.-H.; Wang, H. M. A Metal-Based Inhibitor of NEDD8-Activating Enzyme PLoS One 2012, 7, e49574 10.1371/journal.pone.0049574
23. Leung, C. H.; Zhong, H. J.; Yang, H.; Cheng, Z.; Chan, D. S. H.; Ma, V. P. Y.; Abagyan, R.; Wong, C. Y.; Ma, D. L. A Metal-based inhibitor of tumor necrosis factor-alpha Angew. Chem., Int. Ed. 2012, 51, 9010-9014 10.1002/anie.201202937
24. Yang, H.; Ma, V. P.-Y.; Chan, D. S.-H.; He, H.-Z.; Leung, C.-H.; Ma, D.-L. A cyclometallated iridium(III) complex as a c-myc G-quadruplex stabilizer and down-regulator of c-myc oncogene expression Curr. Med. Chem. 2013, 20, 576-582 10.2174/092986713804910175
25. Kastl, A.; Wilbuer, A.; Merkel, A. L.; Feng, L.; Di Fazio, P.; Ocker, M.; Meggers, E. Dual anticancer activity in a single compound: visible-light-induced apoptosis by an antiangiogenic iridium complex Chem. Commun. 2012, 48, 1863-1865 10.1039/C1CC15378A
26. Blanck, S.; Geisselbrecht, Y.; Kraling, K.; Middel, S.; Mietke, T.; Harms, K.; Essen, L. O.; Meggers, E. Bioactive cyclometalated phthalimides: design, synthesis and kinase inhibition Dalton Trans. 2012, 41, 9337-9348 10.1039/c2dt30940h
27. Wilbuer, A.; Vlecken, D. H.; Schmitz, D. J.; Kraling, K.; Harms, K.; Bagowski, C. P.; Meggers, E. Iridium complex with antiangiogenic properties Angew. Chem., Int. Ed. 2010, 49, 3839-3842 10.1002/anie.201000682
28. Gobel, P.; Ritterbusch, F.; Helms, M.; Bischof, M.; Harms, K.; Jung, M.; Meggers, E. Probing chiral recognition of enzyme active sites with octahedral iridium(III) propeller complexes Eur. J. Inorg. Chem. 2015, 2015, 1654-1659 10.1002/ejic.201500087
29. He, H.-Z.; Chan, W.-I.; Mak, T.-Y.; Liu, L.-J.; Wang, M.; Chan, D. S.-H.; Ma, D.-L.; Leung, C.-H. Detection of 3′ -> 5′ exonuclease activity using a metal-based luminescent switch-on probe Methods 2013, 64, 218-223 10.1016/j.ymeth.2013.08.011
30. Ma, D.-L.; He, H.-Z.; Chan, D. S.-H.; Leung, C.-H. Simple DNA-based logic gates responding to biomolecules and metal ions Chem. Sci. 2013, 4, 3366-3380 10.1039/c3sc50924a
31. Ma, D.-L.; He, H.-Z.; Leung, K.-H.; Chan, D. S.-H.; Leung, C.-H. Bioactive luminescent transition-metal complexes for biomedical applications Angew. Chem., Int. Ed. 2013, 52, 7666-7682 10.1002/anie.201208414
32. Ma, D.-L.; Ma, V. P.-Y.; Chan, D. S.-H.; Leung, K.-H.; He, H.-Z.; Leung, C.-H. Recent advances in luminescent heavy metal complexes for sensing Coord. Chem. Rev. 2012, 256, 3087-3113 10.1016/j.ccr.2012.07.005
33. Ma, D.-L.; Chan, D. S.-H.; Man, B. Y.-W.; Leung, C.-H. Oligonucleotide-based luminescent detection of metal ions Chem.-Asian J. 2011, 6, 986-1003 10.1002/asia.201000870
34. Strahl, B. D.; Allis, C. D. The language of covalent histone modifications Nature 2000, 403, 41-45 10.1038/47412
35. Gupta, J.; Kumar, S.; Li, J. T.; Karuturi, R. K. M.; Tikoo, K. Histone H3 lysine 4 monomethylation (H3K4me1) and H3 lysine 9 monomethylation (H3K9me1): Distribution and their association in regulating gene expression under hyperglycaemic/hyperinsulinemic conditions in 3T3 cells Biochimie 2012, 94, 2656-2664 10.1016/j.biochi.2012.08.011
36. Jenuwein, T.; Allis, C. D. Translating the histone code Science 2001, 293, 1074-1080 10.1126/science.1063127
37. Turner, B. M. Cellular memory and the histone code Cell 2002, 111, 285-291 10.1016/S0092-8674(02)01080-2
38. Benveniste, D.; Sonntag, H. J.; Sanguinetti, G.; Sproul, D. Transcription factor binding predicts histone modifications in human cell lines Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 13367-13372 10.1073/pnas.1412081111
39. Handy, D. E.; Castro, R.; Loscalzo, J. Epigenetic modifications basic mechanisms and role in cardiovascular disease Circulation 2011, 123, 2145-2156 10.1161/CIRCULATIONAHA.110.956839
40. Bannister, A. J.; Kouzarides, T. Regulation of chromatin by histone modifications Cell Res. 2011, 21, 381-395 10.1038/cr.2011.22
41. Hillringhaus, L.; Yue, W. W.; Rose, N. R.; Ng, S. S.; Gileadi, C.; Loenarz, C.; Bello, S. H.; Bray, J. E.; Schofield, C. J.; Oppermann, U. Structural and evolutionary basis for the dual substrate selectivity of human KDM4 histone demethylase family J. Biol. Chem. 2011, 286, 41616-41625 10.1074/jbc.M111.283689
42. Shin, S.; Janknecht, R. Diversity within the JMJD2 histone demethylase family Biochem. Biophys. Res. Commun. 2007, 353, 973-977 10.1016/j.bbrc.2006.12.147
43. Martin, C.; Zhang, Y. The diverse functions of histone lysine methylation Nat. Rev. Mol. Cell Biol. 2005, 6, 838-849 10.1038/nrm1761
44. Chen, Z. Z.; Zang, J. Y.; Whetstine, J.; Hong, X.; Davrazou, F.; Kutateladze, T. G.; Simpson, M.; Mao, Q. L.; Pan, C. H.; Dai, S. D.; Hagman, J.; Hansen, K.; Shi, Y.; Zhang, G. Y. Structural insights into histone demethylation by JMJD2 family members Cell 2006, 125, 691-702 10.1016/j.cell.2006.04.024
45. Krishnan, S.; Trievel, R. C. Structural and functional analysis of JMJD2D reveals molecular basis for site-specific demethylation among JMJD2 demethylases Structure 2013, 21, 98-108 10.1016/j.str.2012.10.018
46. Berry, W. L.; Janknecht, R. KDM4/JMJD2 Histone demethylases: epigenetic regulators in cancer cells Cancer Res. 2013, 73, 2936-2942 10.1158/0008-5472.CAN-12-4300
47. Northcott, P. A.; Nakahara, Y.; Wu, X. C.; Feuk, L.; Ellison, D. W.; Croul, S.; Mack, S.; Kongkham, P. N.; Peacock, J.; Dubuc, A.; Ra, Y. S.; Zilberberg, K.; Mcleod, J.; Scherer, S. W.; Rao, J. S.; Eberhart, C. G.; Grajkowska, W.; Gillespie, Y.; Lach, B.; Grundy, R.; Pollack, I. F.; Hamilton, R. L.; Van Meter, T.; Carlotti, C. G.; Boop, F.; Bigner, D.; Gilbertson, R. J.; Rutka, J. T.; Taylor, M. D. Multiple recurrent genetic events converge on control of histone lysine methylation in medulloblastoma Nat. Genet. 2009, 41, 465-472 10.1038/ng.336
48. Harrison, C. EPIGENETIC DRUGS New modulators of readers and erasers Nat. Rev. Drug Discovery 2013, 12, 188-189 10.1038/nrd3961
49. Wang, L.; Chang, J. J.; Varghese, D.; Dellinger, M.; Kumar, S.; Best, A. M.; Ruiz, J.; Bruick, R.; Pena-Llopis, S.; Xu, J. J.; Babinski, D. J.; Frantz, D. E.; Brekken, R. A.; Quinn, A. M.; Simeonov, A.; Easmon, J.; Martinez, E. D. A small molecule modulates Jumonji histone demethylase activity and selectively inhibits cancer growth Nat. Commun. 2013, 4, 2035-2045 10.1038/ncomms3035
50. Hamada, S.; Suzuki, T.; Mino, K.; Koseki, K.; Oehme, F.; Flamme, I.; Ozasa, H.; Itoh, Y.; Ogasawara, D.; Komaarashi, H.; Kato, A.; Tsumoto, H.; Nakagawa, H.; Hasegawa, M.; Sasaki, R.; Mizukami, T.; Miyata, N. Design, Synthesis, Enzyme-inhibitory activity, and effect on human cancer cells of a novel series of Jumonji domain-containing protein 2 histone demethylase inhibitors J. Med. Chem. 2010, 53, 5629-5638 10.1021/jm1003655
51. Liang, Y.; Vogel, J. L.; Arbuckle, J. H.; Rai, G.; Jadhav, A.; Simeonov, A.; Maloney, D. J.; Kristie, T. M. Targeting the JMJD2 histone demethylases to epigenetically control herpesvirus infection and reactivation from latency Sci. Transl. Med. 2013, 5, 2167ra5 10.1126/scitranslmed.3005145
52. Sprouse, S.; King, K. A.; Spellane, P. J.; Watts, R. J. Photophysical effects of metal-carbon c bonds in ortho-metalated complexes of Ir(III) and Rh(III) J. Am. Chem. Soc. 1984, 106, 6647-6653 10.1021/ja00334a031
53. Zhao, Q.; Liu, S.; Shi, M.; Wang, C.; Yu, M.; Li, L.; Li, F.; Yi, T.; Huang, C. Series of new cationic iridium(III) complexes with tunable emission wavelength and excited state properties: structures, theoretical calculations, and photophysical and electrochemical properties Inorg. Chem. 2006, 45, 6152-6160 10.1021/ic052034j
54. Schneider, J.; Shilatifard, A. Histone demethylation by hydroxylation: Chemistry in action ACS Chem. Biol. 2006, 1, 75-U3 10.1021/cb600030b
55. Pogribny, I. P.; Tryndyak, V. P.; Pogribna, M.; Shpyleva, S.; Surratt, G.; Da Costa, G. G.; Beland, F. A. Modulation of intracellular iron metabolism by iron chelation affects chromatin remodeling proteins and corresponding epigenetic modifications in breast cancer cells and increases their sensitivity to chemotherapeutic agents Int. J. Oncol. 2013, 42, 1822-1832 10.3892/ijo.2013.1855
56. Kim, T. D.; Oh, S.; Shin, S.; Janknecht, R. Regulation of tumor suppressor p53 and HCT116 cell physiology by histone demethylase JMJD2D/KDM4D PLoS One 2012, 7, e34618 10.1371/journal.pone.0034618
57. Rondinelli, B.; Schwerer, H.; Antonini, E.; Gaviraghi, M.; Lupi, A.; Frenquelli, M.; Cittaro, D.; Segalla, S.; Lemaitre, J. M.; Tonon, G. H3K4me3 demethylation by the histone demethylase KDM5C/JARID1C promotes DNA replication origin firing Nucleic Acids Res. 2015, 43, 2560-2574 10.1093/nar/gkv090
58. Agger, K.; Cloos, P. A. C.; Christensen, J.; Pasini, D.; Rose, S.; Rappsilber, J.; Issaeva, I.; Canaani, E.; Salcini, A. E.; Helin, K. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development Nature 2007, 449, 731-U10 10.1038/nature06145
59. Vanhaecke, T.; Papeleu, P.; Elaut, G.; Rogiers, V. Trichostatin A-like hydroxamate histone deacetylase inhibitors as therapeutic agents: Toxicological point of view Curr. Med. Chem. 2004, 11, 1629-1643 10.2174/0929867043365099