Generic placeholder image

Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

Research Article

Oxidovanadium(IV) Complex Disrupts Mitochondrial Membrane Potential and Induces Apoptosis in Pancreatic Cancer Cells

Author(s): Szymon Kowalski, Aleksandra Tesmar, Artur Sikorski and Iwona Inkielewicz-Stępniak*

Volume 21, Issue 1, 2021

Published on: 24 June, 2020

Page: [71 - 83] Pages: 13

DOI: 10.2174/1871520620666200624145217

Price: $65

Abstract

Background: At the present time, there is a growing interest in metal-based anticancer agents. Metal complexes exhibit many valuable clinical properties, however, due to toxicity, only a few clinically useful complexes have been discovered. It has been demonstrated that synthetic vanadium complexes exhibit many biological activities, including anti-cancer properties, however, cellular and molecular mechanisms still are not fully understood.

Objective: This investigation examined the potential effects of three newly synthesized oxidovanadium(IV) complexes with 2-amino-3-hydroxypyridine against pancreatic cancer cells.

Methods: We measured cytotoxicity by using 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide, antiproliferative activity by bromodeoxyuridine assay and necrosis as well as late apoptosis by lactate dehydrogenase assay. Reactive oxygen species generation, apoptosis and mitochondrial membrane potential were determined by a flow cytometry technique. Cell morphology was evaluated by using a transmission electron microscope.

Results: The results showed that oxidovanadium(IV) complexes were cytotoxic on pancreatic cancer cells (PANC-1 and MIA PaCa2) over the concentration range of 12.5-200μM, following 48h incubation. Additionally, the cellular mechanism of cytotoxic activity of [2-NH2-3-OH(py)H]4[V2O2(pmida)2]·6H2O (V3) complex was dependent on ROS generation, induction apoptosis with simultaneous disruption of mitochondrial membrane potential.

Conclusion: We have proven that oxidovanadium (IV) complexes show therapeutic potential in pancreatic cancer therapy. The results of our research will help to understand the cellular mechanisms of the cytotoxic activity of the vanadium complexes and will allow a more effective design structure of new vanadium-based compounds in the future.

Keywords: Pancreatic cancer, vanadium complex, oxidative stress, mitochondrial membrane potential, apoptosis, 2-amino-3- hydroxypyridine.

Graphical Abstract

[1]
Bradford, S.S.; Cowan, J.A. From traditional drug design to catalytic metallodrugs: A brief history of the use of metals in medicine. Metallodrugs, 2014, 1(1), 10-23.
[http://dx.doi.org/10.2478/medr-2014-0002]
[2]
Feng, L.; Geisselbrecht, Y.; Blanck, S.; Wilbuer, A.; Atilla-Gokcumen, G.E.; Filippakopoulos, P.; Kräling, 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(15), 5976-5986.
[http://dx.doi.org/10.1021/ja1112996] [PMID: 21446733]
[3]
Pessoa, J.C.; Etcheverry, S.; Gambino, D. Vanadium compounds in medicine. Coord. Chem. Rev., 2015, 301, 24-48.
[http://dx.doi.org/10.1016/j.ccr.2014.12.002] [PMID: 32226091]
[4]
Budzisz, E. Role of metal ions complexes and their ligands in medicine, pharmacy and cosmetology. Curr. Med. Chem., 2019, 26(4), 578-579.
[http://dx.doi.org/10.2174/092986732604190401100950] [PMID: 30968767]
[5]
Imtiaz, M.; Rizwan, M.S.; Xiong, S.; Li, H.; Ashraf, M.; Shahzad, S.M.; Shahzad, M.; Rizwan, M.; Tu, S. Vanadium, recent advancements and research prospects: A review. Environ. Int., 2015, 80, 79-88.
[http://dx.doi.org/10.1016/j.envint.2015.03.018] [PMID: 25898154]
[6]
Byrne, A.R.; Kosta, L. Vanadium in foods and in human body fluids and tissues. Sci. Total Environ., 1978, 10(1), 17-30.
[http://dx.doi.org/10.1016/0048-9697(78)90046-3] [PMID: 684404]
[7]
Rehder, D. The role of vanadium in biology. Metallomics, 2015, 7(5), 730-742.
[http://dx.doi.org/10.1039/C4MT00304G] [PMID: 25608665]
[8]
Lu, L.; Zhu, M. Metal-based inhibitors of protein tyrosine phosphatases. Anticancer. Agents Med. Chem., 2011, 11(1), 164-171.
[http://dx.doi.org/10.2174/187152011794941271] [PMID: 21269257]
[9]
Heneberg, P. Use of protein tyrosine phosphatase inhibitors as promising targeted therapeutic drugs. Curr. Med. Chem., 2009, 16(6), 706-733.
[http://dx.doi.org/10.2174/092986709787458407] [PMID: 19199933]
[10]
Irving, E.; Stoker, A.W.; Irving, E.; Stoker, A.W. Vanadium compounds as PTP inhibitors. Molecules, 2017, 22(12), 2269.
[http://dx.doi.org/10.3390/molecules22122269] [PMID: 29257048]
[11]
Rehder, D. Perspectives for vanadium in health issues. Future Med. Chem., 2016, 8(3), 325-338.
[http://dx.doi.org/10.4155/fmc.15.187] [PMID: 26898507]
[12]
Sava, G.; Jaouen, G.; Hillard, E.A.; Bergamo, A. Targeted therapy vs. DNA-adduct formation-guided design: Thoughts about the future of metal-based anticancer drugs. Dalton Trans., 2012, 41(27), 8226-8234.
[http://dx.doi.org/10.1039/c2dt30075c] [PMID: 22614531]
[13]
Weidmann, A.G.; Komor, A.C.; Barton, J.K. Targeted chemotherapy with metal complexes. Comm. Mod. Chem. A Comm. Inorg. Chem., 2014, 34(3-4), 114-123.
[http://dx.doi.org/10.1080/02603594.2014.890099] [PMID: 25642012]
[14]
Block, K.I.; Gyllenhaal, C.; Lowe, L.; Amedei, A.; Amin, A.R.M.R.; Amin, A.; Aquilano, K.; Arbiser, J.; Arreola, A.; Arzumanyan, A.; Ashraf, S.S.; Azmi, A.S.; Benencia, F.; Bhakta, D.; Bilsland, A.; Bishayee, A.; Blain, S.W.; Block, P.B.; Boosani, C.S.; Carey, T.E.; Carnero, A.; Carotenuto, M.; Casey, S.C.; Chakrabarti, M.; Chaturvedi, R.; Chen, G.Z.; Chen, H.; Chen, S.; Chen, Y.C.; Choi, B.K.; Ciriolo, M.R.; Coley, H.M.; Collins, A.R.; Connell, M.; Crawford, S.; Curran, C.S.; Dabrosin, C.; Damia, G.; Dasgupta, S.; DeBerardinis, R.J.; Decker, W.K.; Dhawan, P.; Diehl, A.M.E.; Dong, J.T.; Dou, Q.P.; Drew, J.E.; Elkord, E.; El-Rayes, B.; Feitelson, M.A.; Felsher, D.W.; Ferguson, L.R.; Fimognari, C.; Firestone, G.L.; Frezza, C.; Fujii, H.; Fuster, M.M.; Generali, D.; Georgakilas, A.G.; Gieseler, F.; Gilbertson, M.; Green, M.F.; Grue, B.; Guha, G.; Halicka, D.; Helferich, W.G.; Heneberg, P.; Hentosh, P.; Hirschey, M.D.; Hofseth, L.J.; Holcombe, R.F.; Honoki, K.; Hsu, H.Y.; Huang, G.S.; Jensen, L.D.; Jiang, W.G.; Jones, L.W.; Karpowicz, P.A.; Keith, W.N.; Kerkar, S.P.; Khan, G.N.; Khatami, M.; Ko, Y.H.; Kucuk, O.; Kulathinal, R.J.; Kumar, N.B.; Kwon, B.S.; Le, A.; Lea, M.A.; Lee, H.Y.; Lichtor, T.; Lin, L.T.; Locasale, J.W.; Lokeshwar, B.L.; Longo, V.D.; Lyssiotis, C.A.; MacKenzie, K.L.; Malhotra, M.; Marino, M.; Martinez-Chantar, M.L.; Matheu, A.; Maxwell, C.; McDonnell, E.; Meeker, A.K.; Mehrmohamadi, M.; Mehta, K.; Michelotti, G.A.; Mohammad, R.M.; Mohammed, S.I.; Morre, D.J.; Muralidhar, V.; Muqbil, I.; Murphy, M.P.; Nagaraju, G.P.; Nahta, R.; Niccolai, E.; Nowsheen, S.; Panis, C.; Pantano, F.; Parslow, V.R.; Pawelec, G.; Pedersen, P.L.; Poore, B.; Poudyal, D.; Prakash, S.; Prince, M.; Raffaghello, L.; Rathmell, J.C.; Rathmell, W.K.; Ray, S.K.; Reichrath, J.; Rezazadeh, S.; Ribatti, D.; Ricciardiello, L.; Robey, R.B.; Rodier, F.; Rupasinghe, H.P.V.; Russo, G.L.; Ryan, E.P.; Samadi, A.K.; Sanchez-Garcia, I.; Sanders, A.J.; Santini, D.; Sarkar, M.; Sasada, T.; Saxena, N.K.; Shackelford, R.E.; Shantha Kumara, H.M.C.; Sharma, D.; Shin, D.M.; Sidransky, D.; Siegelin, M.D.; Signori, E.; Singh, N.; Sivanand, S.; Sliva, D.; Smythe, C.; Spagnuolo, C.; Stafforini, D.M.; Stagg, J.; Subbarayan, P.R.; Sundin, T.; Talib, W.H.; Thompson, S.K.; Tran, P.T.; Ungefroren, H.; Vander Heiden, M.G.; Venkateswaran, V.; Vinay, D.S.; Vlachostergios, P.J.; Wang, Z.; Wellen, K.E.; Whelan, R.L.; Yang, E.S.; Yang, H.; Yang, X.; Yaswen, P.; Yedjou, C.; Yin, X.; Zhu, J.; Zollo, M. Designing a broad-spectrum integrative approach for cancer prevention and treatment. Semin. Cancer Biol., 2015, 35(Suppl.), S276-S304.
[http://dx.doi.org/10.1016/j.semcancer.2015.09.007] [PMID: 26590477]
[15]
Kioseoglou, E.; Petanidis, S.; Gabriel, C.; Salifoglou, A. The chemistry and biology of vanadium compounds in cancer therapeutics. Coord. Chem. Rev., 2015, 301-302, 87-105.
[http://dx.doi.org/10.1016/j.ccr.2015.03.010]
[16]
Pisano, M.; Arru, C.; Serra, M.; Galleri, G.; Sanna, D.; Garribba, E.; Palmieri, G.; Rozzo, C. Antiproliferative activity of vanadium compounds: Effects on the major malignant melanoma molecular pathways. Metallomics, 2019, 11(10), 1687-1699.
[http://dx.doi.org/10.1039/C9MT00174C] [PMID: 31490510]
[17]
León, I.E.; Díez, P.; Etcheverry, S.B.; Fuentes, M. Deciphering the effect of an oxovanadium(iv) complex with the flavonoid chrysin (VOChrys) on intracellular cell signalling pathways in an osteosarcoma cell line. Metallomics, 2016, 8(8), 739-749.
[http://dx.doi.org/10.1039/C6MT00045B] [PMID: 27175625]
[18]
León, I.E.; Díez, P.; Baran, E.J.; Etcheverry, S.B.; Fuentes, M. Decoding the anticancer activity of VO-clioquinol compound: The mechanism of action and cell death pathways in human osteosarcoma cells. Metallomics, 2017, 9(7), 891-901.
[http://dx.doi.org/10.1039/C7MT00068E] [PMID: 28581009]
[19]
Tesmar, A.; Inkielewicz-Stępniak, I.; Sikorski, A.; Wyrzykowski, D.; Jacewicz, D.; Zięba, P.; Pranczk, J.; Ossowski, T.; Chmurzyński, L. Structure, physicochemical and biological properties of new complex salt of aqua-(nitrilotriacetato-N,O,O′,O”)-oxidovanadium(IV) anion with 1,10-phenanthrolinium cation. J. Inorg. Biochem., 2015, 152, 53-61.
[http://dx.doi.org/10.1016/j.jinorgbio.2015.08.002] [PMID: 26349013]
[20]
Sheldrick, G.M. Crystal structure refinement with SHELXL. Acta Crystallogr. C Struct. Chem., 2015, 71(Pt 1), 3-8.
[http://dx.doi.org/10.1107/S2053229614024218] [PMID: 25567568]
[21]
CrysAlis CCD. CrysAlis Red; Xcalibur PX Software, Oxford Diffraction Ltd: Abingdon, 2008.
[22]
Farrugia, L.J. IUCr. ORTEP -3 for Windows - a version of ORTEP -III with a Graphical User Interface (GUI). J. Appl. Cryst., 1997, 30, 565-565.
[http://dx.doi.org/10.1107/S0021889897003117]
[23]
Macrae, C.F.; Bruno, I.J.; Chisholm, J.A.; Edgington, P.R.; McCabe, P.; Pidcock, E.; Rodriguez-Monge, L.; Taylor, R.; van de Streek, J.; Wood, P.A. Mercury CSD 2.0-New features for the visualization and investigation of crystal structures. J. Appl. Cryst., 2008, 41, 466-470.
[http://dx.doi.org/10.1107/S0021889807067908]
[24]
Spek, A.L. Structure validation in chemical crystallography. Acta Crystallogr. D Biol. Crystallogr., 2009, 65(Pt 2), 148-155.
[http://dx.doi.org/10.1107/S090744490804362X] [PMID: 19171970]
[25]
Kowalski, S.; Hać, S.; Wyrzykowski, D.; Zauszkiewicz-Pawlak, A.; Inkielewicz-Stępniak, I. Selective cytotoxicity of vanadium complexes on human pancreatic ductal adenocarcinoma cell line by inducing necroptosis, apoptosis and mitotic catastrophe process. Oncotarget, 2017, 8(36), 60324-60341.
[http://dx.doi.org/10.18632/oncotarget.19454] [PMID: 28947974]
[26]
Kowalski, S.; Wyrzykowski, D.; Hac, S.; Rychlowski, M.; Radomski, M.W.; Inkielewicz-Stepniak, I. New Oxidovanadium(IV) coordination complex containing 2-methylnitrilotriacetate ligands induces cell cycle arrest and autophagy in human pancreatic ductal adenocarcinoma cell lines. Int. J. Mol. Sci., 2019, 20(2), 261.
[http://dx.doi.org/10.3390/ijms20020261] [PMID: 30634697]
[27]
Reers, M.; Smiley, S.T.; Mottola-Hartshorn, C.; Chen, A.; Lin, M.; Chen, L.B. Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol., 1995, 260, 406-417.
[http://dx.doi.org/10.1016/0076-6879(95)60154-6] [PMID: 8592463]
[28]
Tesmar, A.; Ferenc, W.; Wyrzykowski, D. Structural characterization and biological properties of a new dinuclear oxidovanadium(IV) N-(phosphonomethyl)iminodiacetate complex with the 4-amino-2-methylquinolinium cation. Polyhedron, 2017, 133, 75-81.
[http://dx.doi.org/10.1016/j.poly.2017.05.020]
[29]
Paz, F.A.A.; Rocha, J.; Klinowski, J.; Trindade, T.; Shi, F-N.; Mafra, L. Optimised hydrothermal synthesis of multi-dimensional hybrid coordination polymers containing flexible organic ligands. Prog. Solid State Chem., 2005, 33, 113-125.
[http://dx.doi.org/10.1016/j.progsolidstchem.2005.11.033]
[30]
Chan, F.K-M.; Moriwaki, K.; De Rosa, M.J. Detection of Necrosis by Release of Lactate Dehydrogenase Activity; Humana Press: Totowa, NJ, 2013, pp. 65-70.
[http://dx.doi.org/10.1007/978-1-62703-290-2_7]
[31]
Vermes, I.; Haanen, C.; Steffens-Nakken, H.; Reutelingsperger, C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods, 1995, 184(1), 39-51.
[http://dx.doi.org/10.1016/0022-1759(95)00072-I] [PMID: 7622868]
[32]
Bishayee, A.; Waghray, A.; Patel, M.A.; Chatterjee, M. Vanadium in the detection, prevention and treatment of cancer: The in vivo evidence. Cancer Lett., 2010, 294(1), 1-12.
[http://dx.doi.org/10.1016/j.canlet.2010.01.030] [PMID: 20206439]
[33]
Evangelou, A.M. Vanadium in cancer treatment. Crit. Rev. Oncol. Hematol., 2002, 42(3), 249-265.
[http://dx.doi.org/10.1016/S1040-8428(01)00221-9] [PMID: 12050018]
[34]
Kostova, I. Titanium and vanadium complexes as anticancer agents. Anticancer. Agents Med. Chem., 2009, 9(8), 827-842.
[http://dx.doi.org/10.2174/187152009789124646] [PMID: 19538167]
[35]
Levina, A.; Lay, P.A. Stabilities and biological activities of vanadium drugs: What is the Nature of the active species? Chem. Asian J., 2017, 12(14), 1692-1699.
[http://dx.doi.org/10.1002/asia.201700463] [PMID: 28401668]
[36]
Wu, J-X.; Hong, Y-H.; Yang, X-G. Bis(acetylacetonato)-oxidovanadium(IV) and sodium metavanadate inhibit cell proliferation via ROS-induced sustained MAPK/ERK activation but with elevated AKT activity in human pancreatic cancer AsPC-1 cells. J. Biol. Inorg. Chem., 2016, 21(8), 919-929.
[http://dx.doi.org/10.1007/s00775-016-1389-0] [PMID: 27614430]
[37]
Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2018, 68(6), 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[38]
Scalese, G.; Mosquillo, M.F.; Rostán, S.; Castiglioni, J.; Alho, I.; Pérez, L.; Correia, I.; Marques, F.; Costa Pessoa, J.; Gambino, D. Heteroleptic oxidovanadium(IV) complexes of 2-hydroxynaphtylaldimine and polypyridyl ligands against Trypanosoma cruzi and prostate cancer cells. J. Inorg. Biochem., 2017, 175, 154-166.
[http://dx.doi.org/10.1016/j.jinorgbio.2017.07.014] [PMID: 28755573]
[39]
Naso, L.; Martínez, V.R.; Lezama, L.; Salado, C.; Valcarcel, M.; Ferrer, E.G.; Williams, P.A.M. Antioxidant, anticancer activities and mechanistic studies of the flavone glycoside diosmin and its oxidovanadium(IV) complex. Interactions with bovine serum albumin. Bioorg. Med. Chem., 2016, 24(18), 4108-4119.
[http://dx.doi.org/10.1016/j.bmc.2016.06.053] [PMID: 27374881]
[40]
Yu, Q.; Jiang, W.; Li, D.; Gu, M.; Liu, K.; Dong, L.; Wang, C.; Jiang, H.; Dai, W. Sodium orthovanadate inhibits growth and triggers apoptosis of human anaplastic thyroid carcinoma cells in vitro and in vivo. Oncol. Lett., 2019, 17(5), 4255-4262.
[http://dx.doi.org/10.3892/ol.2019.10090] [PMID: 30944619]
[41]
Reytman, L.; Hochman, J.; Tshuva, E.Y. Anticancer diaminotris (phenolato) vanadium (V) complexes: Ligand-metal interplay. J. Coord. Chem., 2018, 71, 2003-2011.
[http://dx.doi.org/10.1080/00958972.2018.1461848]
[42]
Valko, M.; Morris, H.; Cronin, M.T. Metals, toxicity and oxidative stress. Curr. Med. Chem., 2005, 12(10), 1161-1208.
[http://dx.doi.org/10.2174/0929867053764635] [PMID: 15892631]
[43]
Stohs, S.J.; Bagchi, D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med., 1995, 18(2), 321-336.
[http://dx.doi.org/10.1016/0891-5849(94)00159-H] [PMID: 7744317]
[44]
Leon, I.E.; Di Virgilio, A.L.; Porro, V.; Muglia, C.I.; Naso, L.G.; Williams, P.A.; Bollati-Fogolin, M.; Etcheverry, S.B. Antitumor properties of a vanadyl(IV) complex with the flavonoid chrysin [VO(chrysin)2EtOH]2 in a human osteosarcoma model: The role of oxidative stress and apoptosis. Dalton Trans., 2013, 42(33), 11868-11880.
[http://dx.doi.org/10.1039/c3dt50524c] [PMID: 23760674]
[45]
Sinha, A.; Banerjee, K.; Banerjee, A.; Sarkar, A.; Ahir, M.; Adhikary, A.; Chatterjee, M.; Choudhuri, S.K. Induction of apoptosis in human colorectal cancer cell line, HCT-116 by a vanadium- Schiff base complex. Biomed. Pharmacother., 2017, 92, 509-518.
[http://dx.doi.org/10.1016/j.biopha.2017.05.108] [PMID: 28575808]
[46]
Martínez Medina, J.J.; Naso, L.G.; Pérez, A.L.; Rizzi, A.; Ferrer, E.G.; Williams, P.A.M. Antioxidant and anticancer effects and bioavailability studies of the flavonoid baicalin and its oxidovanadium(IV) complex. J. Inorg. Biochem., 2017, 166, 150-161.
[http://dx.doi.org/10.1016/j.jinorgbio.2016.11.005] [PMID: 27863301]
[47]
Hong, X-L.; Liu, L-J.; Lu, W-G.; Wang, X-B. A vanadium(V) terpyridine complex: Synthesis, characterization, cytotoxicity in vitro and induction of apoptosis in cancer cells. Transit. Met. Chem., 2017, 42, 459-467.
[http://dx.doi.org/10.1007/s11243-017-0150-z]
[48]
Hengartner, M.O. The biochemistry of apoptosis. Nature, 2000, 407(6805), 770-776.
[http://dx.doi.org/10.1038/35037710] [PMID: 11048727]
[49]
Häcker, G. The morphology of apoptosis. Cell Tissue Res., 2000, 301(1), 5-17.
[http://dx.doi.org/10.1007/s004410000193] [PMID: 10928277]
[50]
Mohammad, R.M.; Muqbil, I.; Lowe, L.; Yedjou, C.; Hsu, H.Y.; Lin, L.T.; Siegelin, M.D.; Fimognari, C.; Kumar, N.B.; Dou, Q.P.; Yang, H.; Samadi, A.K.; Russo, G.L.; Spagnuolo, C.; Ray, S.K.; Chakrabarti, M.; Morre, J.D.; Coley, H.M.; Honoki, K.; Fujii, H.; Georgakilas, A.G.; Amedei, A.; Niccolai, E.; Amin, A.; Ashraf, S.S.; Helferich, W.G.; Yang, X.; Boosani, C.S.; Guha, G.; Bhakta, D.; Ciriolo, M.R.; Aquilano, K.; Chen, S.; Mohammed, S.I.; Keith, W.N.; Bilsland, A.; Halicka, D.; Nowsheen, S.; Azmi, A.S. Broad targeting of resistance to apoptosis in cancer. Semin. Cancer Biol., 2015, 35(Suppl.), S78-S103.
[http://dx.doi.org/10.1016/j.semcancer.2015.03.001] [PMID: 25936818]
[51]
Rui, W.; Tian, X.; Zeng, P. The anti-tumor activity of novel oxovanadium complexes derived from thiosemicarbazones and fluoro-phenanthroline derivatives. Polyhedron, 2016, 117, 803-816.
[http://dx.doi.org/10.1016/j.poly.2016.07.021]
[52]
León, I.E.; Cadavid-Vargas, J.F.; Tiscornia, I.; Porro, V.; Castelli, S.; Katkar, P.; Desideri, A.; Bollati-Fogolin, M.; Etcheverry, S.B. Oxidovanadium(IV) complexes with chrysin and silibinin: Anticancer activity and mechanisms of action in a human colon adenocarcinoma model. J. Biol. Inorg. Chem., 2015, 20(7), 1175-1191.
[http://dx.doi.org/10.1007/s00775-015-1298-7] [PMID: 26404080]
[53]
Šebestová, L.; Havelek, R.; Řezáčová, M.; Honzíček, J.; Kročová, Z.; Vinklárek, J. Study of antitumor effect of selected vanadium and molybdenum organometallic complexes in human leukemic T-cells. Chem. Biol. Interact., 2015, 242, 61-70.
[http://dx.doi.org/10.1016/j.cbi.2015.09.017] [PMID: 26391003]
[54]
León, I.E.; Butenko, N.; Di Virgilio, A.L.; Muglia, C.I.; Baran, E.J.; Cavaco, I.; Etcheverry, S.B. Vanadium and cancer treatment: Antitumoral mechanisms of three oxidovanadium(IV) complexes on a human osteosarcoma cell line. J. Inorg. Biochem., 2014, 134, 106-117.
[http://dx.doi.org/10.1016/j.jinorgbio.2013.10.009] [PMID: 24199985]
[55]
Abyar, F.; Tabrizi, L. Experimental and theoretical investigations of novel oxidovanadium(IV) juglone complex: DNA/HSA interaction and cytotoxic activity. J. Biomol. Struct. Dyn., 2020, 38(2), 474-487.
[http://dx.doi.org/10.1080/07391102.2019.1580221] [PMID: 30831056]
[56]
Green, D.R.; Reed, J.C. Mitochondria and apoptosis. Science, 1998, 281(5381), 1309-1312.
[http://dx.doi.org/10.1126/science.281.5381.1309] [PMID: 9721092]
[57]
Zhang, Y.L.; Wang, X.S.; Fang, W.; Cai, X.Y.; Li, H.Z.; Mao, J.W.; Jin, X.B.; Bai, Y.L.; Lu, J.Z. In vitro study of the cytotoxicities of two mixed-ligand oxovanadium complexes on human hepatoma cells. Pharmazie, 2013, 68(10), 827-834.
[PMID: 24273888]
[58]
Dankhoff, K.; Ahmad, A.; Weber, B.; Biersack, B.; Schobert, R. Anticancer properties of a new non-oxido vanadium(IV) complex with a catechol-modified 3,3′-diindolylmethane ligand. J. Inorg. Biochem., 2019, 194, 1-6.
[http://dx.doi.org/10.1016/j.jinorgbio.2019.02.005] [PMID: 30784705]
[59]
Goyal, S.; Amar, S.K.; Dwivedi, A.; Mujtaba, S.F.; Kushwaha, H.N.; Chopra, D.; Pal, M.K.; Singh, D.; Chaturvedi, R.K.; Ray, R.S. Photosensitized 2-amino-3-hydroxypyridine-induced mitochondrial apoptosis via Smac/DIABLO in human skin cells. Toxicol. Appl. Pharmacol., 2016, 297, 12-21.
[http://dx.doi.org/10.1016/j.taap.2016.02.022] [PMID: 26933830]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy