Copper(II), cobalt(II) and nickel(II) complexes of juglone: synthesis, structure, DNA interaction and enhanced cytotoxicity

BioMetals

Volumn 29, Issue 6, 2016, Pages 981-993

  Tabrizi, Leila ^a   Fooladivanda, Mahrokh ^a   Chiniforoshan, Hossein ^a  

^a ISFAHAN UNIVERSITY OF TECHNOLOGY   (Iran)

Author keywords

Cytotoxicity; DNA binding; Juglone; Metal complex

Indexed keywords

1,10 PHENANTHROLINE; ANTINEOPLASTIC AGENT; CISPLATIN; COBALT; COPPER COMPLEX; DIAZEPAM; JUGLONE; NICKEL COMPLEX; 1,10-PHENANTHROLINE; CALF THYMUS DNA; COORDINATION COMPOUND; COPPER; DNA; NAPHTHOQUINONE; NICKEL; PHENANTHROLINE DERIVATIVE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CATALYSIS; CATALYST; CONTROLLED STUDY; CYTOTOXICITY; DNA BINDING; DNA CLEAVAGE; DRUG STABILITY; DRUG STRUCTURE; DRUG SYNTHESIS; FLUORESCENCE SPECTROSCOPY; HELA CELL LINE; HEPG2 CELL LINE; HT 29 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; ULTRAVIOLET SPECTROSCOPY; VISCOMETRY; CHEMICAL STRUCTURE; CHEMISTRY; HEP-G2 CELL LINE; HT-29 CELL LINE; IC50; METABOLISM; SPECTROFLUOROMETRY; SYNTHESIS;

ANTINEOPLASTIC AGENTS; COBALT; COORDINATION COMPLEXES; COPPER; DNA; DNA CLEAVAGE; DRUG STABILITY; HELA CELLS; HEP G2 CELLS; HT29 CELLS; HUMANS; INHIBITORY CONCENTRATION 50; MOLECULAR STRUCTURE; NAPHTHOQUINONES; NICKEL; PHENANTHROLINES; SPECTROMETRY, FLUORESCENCE;

EID: 84986253345     PISSN: 09660844     EISSN: 15728773     Source Type: Journal    
DOI: 10.1007/s10534-016-9970-0     Document Type: Article

References (63)

1. Alagesan M, Sathyadevi P, Krishnamoorthy P, Bhuvanesh NSP, Dharmaraj N (2014) DMSO containing ruthenium(II) hydrazone complexes: in vitro evaluation of biomolecular interaction and anticancer activity. Dalton Trans 43:15829–15840. doi:10.1039/C4DT01032A
2. Barton JK, Goldberg JM, Kumar CV, Turro NJ (1986) Binding modes and base specificity of tris(phenanthroline) ruthenium(II) enantiomers with nucleic acids: tuning the stereoselectivity. J Am Chem Soc 108:2081–2088. doi:10.1021/ja00268a057
3. Bernhardt PV, Lawrance GA (2003) In: McCleverty JA, Meyer TJ (eds) Comprehensive coordination chemistry II, vol 6. Elsevier/Pergamon, Amsterdam, pp 1–45
4. Bhatia BM, Kapila SD, Pathak KK, Chakarborty R (1983) Stability constants and thermodynamics functions of cadmium(III), praseodymium(III), and neodymium(III) with juglone (5-hydroxy 1,4 naphthquinone). Thermochim Acta 64:387–389. doi:10.1016/0040-6031(83)85014-X
5. Bokola-Christianopolou MN (1984) Synthesis and studies of bivalent metal chelate of 1,2 dihydroxy-9,10 anthracenedione and 5-hydroxy 1,4 naphthalenedione. Polyhedron 3:729–734. doi:10.1016/S0277-5387(00)88013-4
6. Bottei RS, McEachern CP (1970) Thermal and spectral studies of some divalent metal chelate of lawsone and juglone. J Inorg Nucl Chem 32:2653–2663. doi:10.1016/0022-1902(70)80314-1
7. Bustamante FLS, Miranda FS, Castro FAV, Resende JALC, Pereira MD, Lanznaster M (2014) A study on the properties and reactivity of naphthoquinone–cobalt(III) prototypes for bioreductive prodrugs. J Inorg Biochem 132:37–44. doi:10.1016/j.jinorgbio.2013.11.007
8. Carter MT, Rodriguez M, Bard AJ (1989) Voltammetric studies of the interaction of metal chelates with DNA. 2. Tris-chelated complexes of cobalt(III) and iron(II) with 1,10-phenanthroline and 2,2′-bipyridine. J Am Chem Soc 111:8901–8911. doi:10.1021/ja00206a020
9. Cater MA, Pearson HB, Wolyniec K, Klaver P, Bilandzic M, Paterson BM, Bush AI, Humbert PO, Fontaine SL, Donnelly PS, Haupt Y (2013) Increasing intracellular bioavailable copper selectively targets prostate cancer cells. ACS Chem Biol 8:1621–1631. doi:10.1021/cb400198p
10. Chattopadhyay T, Mukherjee M, Mondal A, Maiti P, Banerjee A, Banu KS, Bhattacharya S, Roy B, Chattopadhyay DJ, Mondal TK, Nethaji M, Zangrando E, Das D (2010) A unique nickel system having versatile catalytic activity of biological significance. Inorg Chem 49:3121–3129. doi:10.1021/ic901546t
11. Chilin A, Dodoni G, Frezza C, Guiotto A, Barbieri V, Lisa FD (2005) 4-Hydroxymethyl-1,6,8-trimethylfuro[2,3-h]quinolin-2(1H)-one induces mitochondrial dysfunction and apoptosis upon its intracellular oxidation. J Med Chem 48:192–197. doi:10.1021/jm0493919
12. Dimiza F, Fountoulaki S, Papadopoulos AN, Kontogiorgis CA, Tangoulis V, Raptopoulou CP, Psycharis V, Terzis A, Kessissoglou DP, Psomas G (2011) Non-steroidal antiinflammatory drug–copper(II) complexes: structure and biological perspectives. Dalton Trans 40:8555–8568. doi:10.1039/C1DT10714C
13. Dimiza F, Papadopoulos AN, Tangoulis V, Psycharis V, Raptopoulou CP, Kessissoglou DP, Psomas G (2012) Biological evaluation of cobalt(II) complexes with non-steroidal anti-inflammatory drug naproxen. J Inorg Biochem 107:54–64. doi:10.1016/j.jinorgbio.2011.10.014
14. Efthimiadou EK, Karaliota A, Psomas G (2008) Structure, antimicrobial activity and DNA-binding properties of the cobalt(II)–sparfloxacin complex. Bioorg Med Chem Lett 18:4033–4037. doi:10.1016/j.bmcl.2008.05.115
15. El-Hendawy AM (1991) Complexes of lawsone with uranium, molybdenum, ruthenium and osmium, and their use as organic oxidants. Polyhedron 10:2511–2518. doi:10.1016/S0277-5387(00)86217-8
16. Erkkila KE, Odom DT, Barton JK (1999) Recognition and reaction of metallointercalators with DNA. Chem Rev 99:2777–2796. doi:10.1021/cr9804341
17. Finney L, Vogt S, Fukai T, Glesne D (2009) Copper and angiogenesis: unravelling a relationship key to cancer progression. Clin Exp Pharmacol Physiol 36:88–94. doi:10.1111/j.1440-1681.2008.04969.x
18. Frezza M, Hindo SS, Tomco D, Allard MM, Cui QC, Heeg MJ, Chen D, Dou QP, Verani CN (2009) Comparative activities of nickel(II) and zinc(II) complexes of asymmetric [NN′O] ligands as 26S proteasome inhibitors. Inorg Chem 48:5928–5937. doi:10.1021/ic900276g
19. Friedman AE, Kumar CV, Turro NJ, Barton JK (1991) Luminescence of ruthenium(II) polypyridyls: evidence for intercalative binding to Z-DNA. Nucleic Acids Res 19:2595–2602
20. Garge P, Padhye S, Tauchagues JP (1989) Iron(II) complexes of ortho-functionalized para-naphthoquinones 1. Synthesis, characterization, electronic structure and magnetic properties. Inorg Chim Acta 157:239–249. doi:10.1016/S0020-1693(00)80548-4
21. Gokhale NH, Shirisha K, Padhye SB, Croft SL, Kendrick HD, Davies W, Anson CE, Powell AK (2003) Transition metal complexes of buparvaquone as potent new antimalarial agents: 1. Synthesis, X-ray crystal-structures, electrochemistry and antimalarial activity against Plasmodium falciparum. J Inorg Biochem 95:249–258. doi:10.1016/S0162-0134(03)00134-X
22. Gokhale NH, Shirisha K, Padhye SB, Croft SL, Kendrick HD, Mckee V (2006) Metalloantimalarials: synthesis, X-ray crystal structure of potent antimalarial copper(II) complex of arylazo-4-hydroxy-1,2-naphthoquinone. Bioorg Med Chem Lett 16:430–432. doi:10.1016/j.bmcl.2005.09.061
23. Goswami TK, Chakravarthi BV, Roy M, Karande AA, Chakravarty AR (2011) Ferrocene-conjugated l-tryptophan copper(II) complexes of phenanthroline bases showing DNA photocleavage activity and cytotoxicity. Inorg Chem 50:8452–8464. doi:10.1021/ic201028e
24. ®. Toxicol In Vitro 25:1376–1384. doi:10.1016/j.tiv.2011.05.008
25. Hadjiliadis N, Sletten E (eds) (2009) Metal complex–DNA interactions. Wiley, Hoboken
26. Hill JM, Sper RJ (1981) Organo-platinum complexes as antitumor agents. Anticancer Res 2:173–186
27. Ishida S, Andreux P, Poitry-Yamate C, Auwerx J, Hanahan D (2013) Bioavailable copper modulates oxidative phosphorylation and growth of tumors. PNAS USA 110:19507–19512. doi:10.1073/pnas.1318431110
28. Kelly TM, Tossi AB, McConnell DJ, Strekas TC (1985) A study of the interactions of some polypyridylruthenium(II) complexes with DNA using fluorescence spectroscopy, topoisomerisation and thermal denaturation. Nucleic Acids Res 13:6017–6034
29. Kido H, Fernelius WC, Hass CG Jr (1960) Coordination compound (XVIII), formation constants of some metal salts of hydroxyquinone. Anal Chim Acta 23:116–123. doi:10.1016/S0003-2670(60)80028-1
30. Koptenko EP, Aizenberg RN, Shvartsman BA (1971) Complexing of juglone with zinc and nickel in an alcohol–water medium. Tr Kishinev Sel-Khoz Inst 72:31–36
31. Krygowski TM, Stepien BT (2005) Sigma- and pi-electron delocalization: focus on substituent effects. Chem Rev 105:3482–3512. doi:10.1021/cr030081s
32. Lakowicz JR, Weber G (1973) Quenching of fluorescence by oxygen. Probe for structural fluctuations in macromolecules. Biochemistry 12:4161–4170. doi:10.1021/bi00745a020
33. Lalia Kantouri M, Bakola-Christainopolou M (1986) Spectra and thermal studies of some divalent metal chelates of various hydroxyquinons. Thermochim Acta 104:39–60
34. 2+ with DNA: effects of the ancillary ligands on the DNA-binding behaviors. Inorg Chem 40:5045–5050. doi:10.1021/ic001124f
35. Liu Y, Chao H, Tan L, Yuan Y, Wei W, Ji L (2005) Interaction of polypyridyl ruthenium(II) complex containing asymmetric ligand with DNA. J Inorg Biochem 99:530–537. doi:10.1016/j.jinorgbio.2004.10.030
36. Liu Y-H, Li A, Shao J, Xie C-Z, Song X-Q, Bao W-G, Xu J-Y (2016) Four Cu(II) complexes based on antitumor chelators: synthesis, structure, DNA binding/damage, HSA interaction and enhanced cytotoxicity. Dalton Trans 45:8036–8049. doi:10.1039/C6DT00451B
37. Lopez-Sandoval H, Londono-Lemos ME, Garza-Velasco R, Poblano-Melendez I, Granada-Macias P, Gracia-Mora I, Barba-Behrens N (2008) Synthesis, structure and biological activities of cobalt(II) and zinc(II) coordination compounds with 2-benzimidazole derivatives. J Inorg Biochem 102:1267–1276. doi:10.1016/j.jinorgbio.2008.01.016
38. Lv J, Liu T, Cai S, Wang X, Liu L, Wang Y (2006) Synthesis, structure and biological activity of cobalt(II) and copper(II) complexes of valine-derived Schiff bases. J Inorg Biochem 100:1888–1896. doi:10.1016/j.jinorgbio.2006.07.014
39. Mangini A (1931) Some complex compounds of hydroxyquinones. Gazz Chim Ital 61:820–826
40. II polypyridyl complexes as effective photosensitizers in photodynamic therapy. Chem Eur J 20:14421–14436. doi:10.1002/chem.201402796
41. McGhee JD, von Hippel PH (1974) Theoretical aspects of DNA–protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice. J Mol Biol 86:469–489. doi:10.1016/0022-2836(74)90031-X
42. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63. doi:10.1016/0022-1759(83)90303-4
43. Neves AP, Barbosa CC, Greco SJ, Vargas MD, Visentin LC, Pinheiro CB, Mangrich AS, Barbosa JP, da Costa GL (2009) Novel aminonaphthoquinone Mannich bases derived from lawsone and their copper(II) complexes: synthesis, characterization and antibacterial activity. J Braz Chem Soc 20:712–727. doi:10.1590/S0103-50532009000400015
44. Oramas-Royo S, Torrejon C, Cuadrado I, Hernandez-Molina R, Hortelano S, Estevez-Braun A, de las Heras B (2013) Synthesis and cytotoxic activity of metallic complexes of lawsone. Bioorg Med Chem 21:2471–2477. doi:10.1016/j.bmc.2013.03.002
45. Pawar AB, Bamane SR, Jadhav KD, Sarawadekar RG (2012) Spectral, thermal, X-ray diffraction and antimicrobial studies of some bivalent metal chelates of juglone. J Curr Chem Pharm Sci 2:277–290
46. Pelosi G (2010) Thiosemicarbazone metal complexes: from structure to activity. Open Crystallogr J 3:16–28
47. Polonik SG, Prokofeva NG, Agafonova IG, Uvarova NI (2003) Antitumor and immunostimulating activity of 5-hydroxy-1,4-naphthoquinone (juglone) O-and S-acetylglycosides. Pharm Chem J 37:397–398
48. Pyle AM, Morri T, Barton JK (1990) Probing microstructures in double-helical DNA with chiral metal complexes: recognition of changes in base-pair propeller twisting in solution. J Am Chem Soc 112:9432–9434. doi:10.1021/ja00181a077
49. Ravelo AG, Estevez-Braun A, Chavez-Orellana H, Perez-Sacau E, Mesa-Siverio D (2004) Recent studies on natural products as anticancer agents. Curr Top Med Chem 4:241–265
50. Reichmann ME, Rice SA, Thomas P (1954) A further examination of the molecular weight and size of desoxypentose nucleic acid. J Am Chem Soc 76:3047–3053. doi:10.1021/ja01640a067
51. Rosenberg B (1977) Noble metal complexes in cancer chemotherapy. Adv Exp Med Biol 91:129–150
52. Saha S, Majumdar R, Roy M, Dighe RR, Chakravarty AR (2009) An iron complex of dipyridophenazine as a potent photocytotoxic agent in visible light. Inorg Chem 48:2652–2663. doi:10.1021/ic8022612
53. Silva TFS, Martins LMDRS, da Silva MFCG, Fernandes AR, Silva A, Borralho PM, Santos S, Rodrigues CMP, Pombeiro AJL (2012) Cobalt complexes bearing scorpionate ligands: synthesis, characterization, cytotoxicity and DNA cleavage. Dalton Trans 41:12888–12897. doi:10.1039/C2DT11577H
54. Sun H, England CG, Hernandez R, Graves SA, Majewski RL, Kamkaew A, Jiang D, Barnhart TE, Yang Y (2016) Immuno PET for assessing the differential uptake of a CD146-specific monoclonal antibody in lung cancer. Eur J Nucl Med Mol Imaging. doi:10.1007/s00259-016-3442-1
55. Takeuchi T, Bottcher A, Quezada CM, Meade TJ, Gray HB (1999) Inhibition of thermolysin and human α-thrombin by cobalt(III) Schiff base complexes. Bioorg Med Chem 7:815–819. doi:10.1016/S0968-0896(98)00272-7
56. Thirumurugan RS, Kavimani S, Srivastava RS (2000) Antitumour activity of rhinacanthone against Dalton’s ascitic lymphoma. Biol Pharm Bull 23:1438–1440
57. Tiwari SB, Pai RM, Udupa N (2002) Temperature sensitive liposomes of plumbagin: characterization and in vivo evaluation in mice bearing melanoma B16F1. J Drug Target 10:585–591
58. Trawick BN, Danihe AT, Bashkin JK (1998) Inorganic mimics of ribonucleases and ribozymes: from random cleavage to sequence-specific chemistry to catalytic antisense drugs. Chem Rev 98:939–960. doi:10.1021/cr960422k
59. 2+ with calf thymus DNA. J Phys Chem 97:1707–1711. doi:10.1021/j100110a038
60. Ullah MF, Ahmad A, Bhat SH, Khan HY, Zubair H, Sarkar FH, Hadi SM (2016) Simulating hypoxia-induced acidic environment in cancer cells facilitates mobilization and redox-cycling of genomic copper by daidzein leading to pro-oxidant cell death: implications for the sensitization of resistant hypoxic cancer cells to therapeutic challenges. Biometals 29:299–310. doi:10.1007/s10534-016-9916-6
61. Yin HD, Liu H, Hong M (2012) Synthesis, structural characterization and DNA-binding properties of organotin(IV) complexes based on Schiff base ligands derived from 2-hydroxy-1-naphthaldy and 3- or 4-aminobenzoic acid. J Organomet Chem 713:11–19. doi:10.1016/j.jorganchem.2012.03.027
62. Yuzo N, Matsamoto U (1961) Naphthoquinone derivatives as organic reagents. III Precipitation and colour reactions of lawsone, juglone and 3-hydroxy juglone with metal ions. Yakugaku Zasshi 86:631–635
63. Zowczak M, Iskra M, Torlinski L, Cofta S (2001) Analysis of serum copper and zinc concentrations in cancer patients. Biol Trace Elem Res 82:1. doi:10.1385/BTER:82:1-3:001