Ukr.Biochem.J. 2017; Volume 89, Issue 2, Mar-Apr, pp. 5-30
doi: https://doi.org/10.15407/ubj89.02.005
Rhenium–platinum antitumor systems
A. V. Shtemenko1, N. I. Shtemenko2
1Ukrainian State University of Chemical Technology, Dnipro, Ukraine;
2Palladin Institute of Biochemistry, National Academy of Sciences of Ukraine, Kyiv;
e-mail: n.shtemenko@i.ua
This review provides an overlook of design (in short), antitumor and other biological activity of quadruple-bonded cluster dirhenium(III) compounds and their synergism with cisplatin. In particular, we describe the work of the rhenium-platinum antitumor system (introduction of rhenium and platinum compounds). Among known metal-based anticancer drugs and drug candidates dirhenium(III) compounds differ profoundly due to their strong antiradical and antioxidant properties determined by quadruple bond unsaturation. Such advantages of metal complexes as more expressed redox chemical propertie should be exploited for creating more efficient anticancer drugs. Combination of drugs leads to synergistic effects and/or to lowering toxicity of platinides and is very promising in cancer chemotherapy. The review covers the following items: design of quadruple bonded dirhenium(III) clusters, their spectral and antiradical properties (in short); interaction of the dirhenium(III) compounds with lipids and formation of liposomes; interaction of the dirhenium(III) compounds with erythrocytes and their antihemolytic activity in the models of hemolytic anemia; anticancer activity of dirhenium clusters and work of the rhenium-platinum antitumor system; antianemic and antioxidant properties of the dirhenium(III) compounds in the model of tumor growth; interaction of the dirhenium(III) compounds with nucleobases and DNA. Some modern trends in the field of bioinorganic and medicinal chemistry are also considered regarding their connection to the rhenium-platinum system efficiency: use of combinational therapy and nanomaterials; involvement of some biologically active ligands and redox-activation strategy, etc.
Keywords: antihemolytic, antioxidant, antitumor activity, hepato-, nephrostabilizing activity, platinum, rhenium
References:
- Lippert B. Cisplatin: Chemistry and Biochemistry of a Leading Anticancer Drug. Germany: Wiley-VCH: Weinheim, 1999; 576 p. CrossRef
- Graf N, Lippard SJ. Redox activation of metal-based prodrugs as a strategy for drug delivery. Adv Drug Deliv Rev. 2012 Aug;64(11):993-1004. Review. PubMed, PubMedCentral, CrossRef
- Hambley TW. Chemistry. Metal-based therapeutics. Science. 2007 Nov 30;318(5855):1392-3. PubMed, CrossRef
- Bruijnincx PC, Sadler PJ. New trends for metal complexes with anticancer activity. Curr Opin Chem Biol. 2008 Apr;12(2):197-206. Review. PubMed, PubMedCentral, CrossRef
- Hambley TW. Developing new metal-based therapeutics: challenges and opportunities. Dalton Trans. 2007 Nov 21;(43):4929-37. Review. PubMed, CrossRef
- Reisner E, Arion VB, Keppler BK, Pombeiro AJL. Electron-transfer activated metal-based anticancer drugs. Inorg Chim Acta. 2008;361(6):1569-1583. CrossRef
- Hillard EA, Jaouen G. Bioorganometallics: future trends in drug discovery, analytical chemistry, and catalysis. Organometallics. 2011;30(1):20-27. CrossRef
- Clarke MJ, Zhu F, Frasca DR. Non-platinum chemotherapeutic metallopharmaceuticals. Chem Rev. 1999 Sep 8;99(9):2511-34. PubMed, CrossRef
- Jakupec MA, Galanski M, Arion VB, Hartinger CG, Keppler BK. Antitumour metal compounds: more than theme and variations. Dalton Trans. 2008 Jan 14;(2):183-94. Review. PubMed, CrossRef
- Sun RW, Ma DL, Wong EL, Che CM. Some uses of transition metal complexes as anti-cancer and anti-HIV agents. Dalton Trans. 2007 Nov 21;(43):4884-92. PubMed, CrossRef
- Sorasaenee K, Fu PK, Angeles-Boza AM, Dunbar KR, Turro C. Inhibition of transcription in vitro by anticancer active dirhodium(II) complexes. Inorg Chem. 2003 Feb 24;42(4):1267-71. PubMed, CrossRef
- Chifotides HT, Fu PK, Dunbar KR, Turro C. Effect of equatorial ligands of dirhodium(II,II) complexes on the efficiency and mechanism of transcription inhibition in vitro. Inorg Chem. 2004 Feb 9;43(3):1175-83. PubMed, CrossRef
- Chifotides HT, Dunbar KR. Interactions of metal-metal-bonded antitumor active complexes with DNA fragments and DNA. Acc Chem Res. 2005 Feb;38(2):146-56. Review. PubMed, CrossRef
- Guo Z, Sadler PJ. Metals in medicine. Angew Chem Int Ed. 1999;38(11):1512-1531. CrossRef
- Oliynik SA, Shtemenko NI, Gorchakova NO, Shtemenko AV, Zatovski IV, Pirozhkova-Patalah IV, Patalah DD, Pedan LI. Toxicology of rhenium compounds: a glance on the problem. Modern Probl Toxicol. 2001;(1):3-12.(In Ukrainian).
- Jung Y, Lippard SJ. Direct cellular responses to platinum-induced DNA damage. Chem Rev. 2007 May;107(5):1387-407. Review. PubMed, CrossRef
- van Zutphen S, Reedijk J. Targeting platinum anti-tumour drugs: Overview of strategies employed to reduce systemic toxicity. Coord Chem Rev. 2005;249(24):2845-2853. CrossRef
- Wang D, Lippard SJ. Cellular processing of platinum anticancer drugs. Nat Rev Drug Discov. 2005 Apr;4(4):307-20. Review. PubMed, CrossRef
- Fuertes MA, Castilla J, Alonso C, Pérez JM. Cisplatin biochemical mechanism of action: from cytotoxicity to induction of cell death through interconnections between apoptotic and necrotic pathways. Curr Med Chem. 2003 Feb;10(3):257-66. Review. PubMed, CrossRef
- Denny WA. Prodrug strategies in cancer therapy. Eur J Med Chem. 2001 Jul-Aug;36(7-8):577-95. Review. PubMed
- Fuertes MA, Alonso C, Pérez JM. Biochemical modulation of Cisplatin mechanisms of action: enhancement of antitumor activity and circumvention of drug resistance. Chem Rev. 2003 Mar;103(3):645-62. Review. PubMed, CrossRef
- Lee MS. Systematic prioritization of cancer combination therapies: are we really on target? Future Med Chem. 2012 Mar;4(4):387-9. PubMed, CrossRef
- Facy O, Radais F, Ladoire S, Delroeux D, Tixier H, Ghiringhelli F, Rat P, Chauffert B, Ortega-Deballon P. Comparison of hyperthermia and adrenaline to enhance the intratumoral accumulation of cisplatin in a murine model of peritoneal carcinomatosis. J Exp Clin Cancer Res. 2011 Jan 7;30:4. PubMed, PubMedCentral, CrossRef
- Jiang M, Liu Z, Xiang Y, Ma H, Liu S, Liu Y, Zheng D. Synergistic antitumor effect of AAV-mediated TRAIL expression combined with cisplatin on head and neck squamous cell carcinoma. BMC Cancer. 2011 Feb 3;11:54. PubMed, PubMedCentral, CrossRef
- Rattan R, Graham RP, Maguire JL, Giri S, Shridhar V. Metformin suppresses ovarian cancer growth and metastasis with enhancement of cisplatin cytotoxicity in vivo. Neoplasia. 2011 May;13(5):483-91. PubMed, PubMedCentral, CrossRef
- Kotel’nikova A. S., Tronev V. G. Investigation complex compounds of bivalence rhenium. Zhurn Neorg Khim. 1958;3(4):1008-1027. (In Russian).
- Cotton FA, Harris CB. Molecular orbital calculations for complexes of heavier transition elements. III. The metal-metal bonding and electron structure of Re2Cl82-. Inorg Chem. 1967;6(5):924-929. CrossRef
- Koz’min PA. Quadruple metal-metal bond: history and outlook. Chemic Intelligencer. 1996;4:32-36.
- Cotton FA, Murillo CA, Walton RA. Multiple bonds between metal atoms (3rd Edition). Springer Science and Business Media, New York, NY, USA, 2005; 818 p. CrossRef
- Haycock DE, Urch DS, Garner CD, Hillier IH, Mitcheson GR. Direct evidence for the quadruple metal–metal bond in the octachlorodimolybdenum(II) ion, [Mo2Cl8]4–, using X-ray emission spectroscopy. J Chem Soc Chem Commun. 1978;(6):262-263. CrossRef
- Shtemenko AV, Kozhura OV, Pasenko AA, Domasevitch KV. New octachlorodirhenate(III) salts: solid state manifestation for a certain conformational flexibility of the [Re2Cl8]2- ion. Polyhedron. 2003;22(12):1547-1552. CrossRef
- Golovaneva IF, Bovykin BA, Shtemenko AV, Kotelnikova AS, Misailova TV, Shram VP. Spectrophotometric study of the process of formation binuclear rhenium(III) halogenocarboxylates under reducing KReO4 in the mixture of acids. Zhurn Neorg Khim. 1987;32(2):387-393.(In Russian).
- Shtemenko AV, Golichenko AA, Domasevitch KV. Synthesis of novel tetracarboxylato dirhenium(III) compounds and crystal structure of [Re2(1 Adamantylcarboxylate)4Cl2]·4CHCl3. Z. Naturforsch B. 2001;56(4/5):381-385.
- Golichenko AA, Shtemenko AV. Cluster rhenium(III) complexes with adamantanecarboxylic acids: Synthesis and properties. Russ J Coord Chem. 2006;32(4):242-249. CrossRef
- Shtemenko NI, Zabitskaya ED, Berzenina OV, Yegorova DE, Shtemenko AV. Liposomal forms of rhenium cluster compounds: enhancement of biological activity. Chem Biodivers. 2008 Aug;5(8):1660-7. PubMed, CrossRef
- Kovtun GA, Kameneva TM, Golichenko AA, Shtemenko AV. Catalysis of benzyl alcohol oxidation chains breaking with rhenium dinuclear cluster [Re2(O2CCH3)2Cl4·2H2O]. Dopovidi NANU. 2005;(5), 141–144.( In Russian).
- Shtemenko AV, Tretyak SY, Golichenko AA. Interaction of quadruple bonding rhenium unit with free radicals. Chem J Mold. 2007;2(1):93–97. CrossRef
- Shtemenko A, Golichenko A, Tretyak S, Shtemenko N, Randarevich M. Synthesis and antiradical properties of dirhenium cluster compounds. Metal ions in biology and medicine. John Libbey Eurotext Ltd. 2008;10:229-234.
- Stathopoulos GP, Antoniou D, Dimitroulis J, Stathopoulos J, Marosis K, Michalopoulou P. Comparison of liposomal cisplatin versus cisplatin in non-squamous cell non-small-cell lung cancer. Cancer Chemother Pharmacol. 2011 Oct;68(4):945-50. PubMed, PubMedCentral, CrossRef
- Ramachandran S, Quist AP, Kumar S, Lal R. Cisplatin nanoliposomes for cancer therapy: AFM and fluorescence imaging of cisplatin encapsulation, stability, cellular uptake, and toxicity. Langmuir. 2006 Sep 12;22(19):8156-62. PubMed, CrossRef
- Carvalho Júnior AD, Vieira FP, Melo VJ, Lopes MT, Silveira JN, Ramaldes GA, Garnier-Suillerot A, Pereira-Maia EC, Oliveira MC. Preparation and cytotoxicity of cisplatin-containing liposomes. Braz J Med Biol Res. 2007 Aug;40(8):1149-57. PubMed, CrossRef
- Kulik GJ, Pivnyuk VM, Nosko MM, Todor IN, Chekhun VF. Liposomal drugs approach to overcome drug resistance to cisplatin. Onkologiia. 2009;11(1):76-80.
- de Kroon AI, Staffhorst RW, Kruijff Bd, Burger KN. Cisplatin nanocapsules. Methods Enzymol. 2005;391:118-25. PubMed, CrossRef
- Li Z, Shtemenko NI, Yegorova DY, Babiy SO, Brown AJ, Yang T, Shtemenko AV, Dunbar KR. Liposomes loaded with a dirhenium compound and cisplatin: preparation, properties and improved in vivo anticancer activity. J Liposome Res. 2015 Mar;25(1):78-87. PubMed, CrossRef
- Shtemenko OV, Zeleniuk MA, Shtemenko NI, Verbyts’ka IaS. Spectrophotometric study of the interaction between rhenium complexes and phosphatidylcholine during liposome formation. Ukr Biokhim Zhurn. 2002 Nov-Dec;74(6):91-6. (In Ukrainian). PubMed
- Sowemimo-Coker SO. Red blood cell hemolysis during processing. Transfus Med Rev. 2002 Jan;16(1):46-60. Review. PubMed, CrossRef
- Shtemenko N, Oliinik S, Shtemenko O, Pirozhkova-Patalakh I. Antihemolytic activity of cluster complexes of rhenium with organic ligands. Dopovidi NANU. 2001;(6):194–198. (In Ukrainian).
- Shraer TI, Krejnes VM, Golubchikova NA, Ustjantzeva IM, Meljantzeva LP, Lagunova NT. Biological action of liposomes on main pathogenetic mechanisms of inflammation. J Liposome Res. 1994;4(1):281-288. CrossRef
- Shtemenko N, Collery P, Shtemenko A. Dichlorotetra-mu-Isobutyratodirhenium(III): enhancement of cisplatin action and RBC-stabilizing properties. Anticancer Res. 2007 Jul-Aug;27(4B):2487-92. PubMed
- Eastland GW Jr, Yang G, Thompson T. Studies of rhenium carboxylates as antitumor agents. Part II. Antitumor studies of bis (mu-propionato) diaquotetrabromodirhenium (III) in tumor-bearing mice. Methods Find Exp Clin Pharmacol. 1983 Sep;5(7):435-8. PubMed
- Chekhun VF, Lebed OI, Tryndyak VP, Makovetsky VP, Todor IN, Kulik GI. Structural alterations of plasma membranes of Guerin’s carcinoma cells upon the development of resistance to doxorubcine. Exp Oncol. 2002;24:279-283.
- Yurchenko OV, Todor IN, Tryndyak VP, Kovtonyuk OV, Solyanik GI, Kulik GI, Chekhun VF. Resistance of Guerin’s carcinoma cells to cisplatin: biochemical and morphological aspects. Exp Oncol. 2003;25:64-68.
- Shtemenko NI, Collery P, Shtemenko AV. The novel rhenium and platinum antitumor systems. J Biol Inorg Chem. 2007;12(Suppl 1):S22.
- Shtemenko AV, Collery P, Shtemenko NI, Domasevitch KV, Zabitskaya ED, Golichenko AA. Synthesis, characterization, in vivo antitumor properties of the cluster rhenium compound with GABA ligands and its synergism with cisplatin. Dalton Trans. 2009 Jul 14;(26):5132-6. PubMed, CrossRef
- Shtemenko NI, Chifotides HT, Domasevitch KV, Golichenko AA, Babiy SA, Li Z, Paramonova KV, Shtemenko AV, Dunbar KR. Synthesis, X-ray structure, interactions with DNA, remarkable in vivo tumor growth suppression and nephroprotective activity of cis-tetrachloro-dipivalato dirhenium(III). J Inorg Biochem. 2013 Dec;129:127-34. PubMed, CrossRef
- Leus IV, Shamelashvili KL, Skoryk OD, Tretiak SIu, Golichenko OA, Shtemenko OV, Shtemenko NI. Antioxidant and antitumor activity of dirhenium dicarboxylates in animals with Guerin carcinoma. Ukr Biokhim Zhurn. 2012 May-Jun;84(3):72-81. (In Ukrainian). PubMed
- Estensen RD, Jordan MM, Wiedmann TS, Galbraith AR, Steele VE, Wattenberg LW. Effect of chemopreventive agents on separate stages of progression of benzo[alpha]pyrene induced lung tumors in A/J mice. Carcinogenesis. 2004 Feb;25(2):197-201. PubMed, CrossRef
- Jung Y, Lippard SJ. Direct cellular responses to platinum-induced DNA damage. Chem Rev. 2007 May;107(5):1387-407. Review. PubMed, CrossRef
- Angeles-Boza AM, Chifotides HT, Aguirre JD, Chouai A, Fu PK, Dunbar KR, Turro C. Dirhodium(II,II) complexes: molecular characteristics that affect in vitro activity. J Med Chem. 2006 Nov 16;49(23):6841-7. PubMed, CrossRef
- Aguirre JD, Angeles-Boza AM, Chouai A, Pellois JP, Turro C, Dunbar KR. Live cell cytotoxicity studies: documentation of the interactions of antitumor active dirhodium compounds with nuclear DNA. J Am Chem Soc. 2009 Aug 19;131(32):11353-60. PubMed, CrossRef
- Chifotides HT, Lutterman DA, Dunbar KR, Turro C. Insight into the photoinduced ligand exchange reaction pathway of cis-[Rh2(μ-O2CCH3)2(CH3CN)6]2+ with a DNA model chelate. Inorg Chem. 2011 Dec 5;50(23):12099-107. PubMed, CrossRef
- Lee MS. Systematic prioritization of cancer combination therapies: are we really on target? Future Med Chem. 2012 Mar;4(4):387-9. PubMed, CrossRef“]
- Barder TJ, Walton RA, Cotton FA, Powell GL. Tetrabutylammonium octachlorodirhenate(III). Inorg Synth. 1985; 23: 116-118. CrossRef
- Lippman SM, Hong WK. Cancer prevention by delay. Clin Cancer Res. 2002 Feb;8(2):305-13. PubMed
- Kreuser ED, Keppler BK, Berdel WE, Piest A, Thiel E. Synergistic antitumor interactions between newly synthesized ruthenium complexes and cytokines in human colon carcinoma cell lines. Semin Oncol. 1992 Apr;19(2 Suppl 3):73-81. PubMed
- Grivicich I, Mans DR, Peters GJ, Schwartsmann G. Irinotecan and oxaliplatin: an overview of the novel chemotherapeutic options for the treatment of advanced colorectal cancer. Braz J Med Biol Res. 2001 Sep;34(9):1087-103. Review. PubMed, CrossRef
- Lin WL, Li DG, Chen Q, Lu HM. Clinical and experimental study of oxaliplatin in treating human gastric carcinoma. World J Gastroenterol. 2004 Oct 1;10(19):2911-5. PubMed, PubMedCentral, CrossRef
- Fuertes MA, Alonso C, Pérez JM. Biochemical modulation of Cisplatin mechanisms of action: enhancement of antitumor activity and circumvention of drug resistance. Chem Rev. 2003 Mar;103(3):645-62. PubMed, CrossRef
- Yu F, Megyesi J, Price PM. Cytoplasmic initiation of cisplatin cytotoxicity. Am J Physiol Renal Physiol. 2008 Jul;295(1):F44-52. PubMed, PubMedCentral, CrossRef
- Bovykin AM, Omel’chenko АМ, Chasova EA, Shtemenko AV. The effects of o-phenantroline-containing rhenium complexes on the properties of the bilayer lipid membranes. Membr Cell Biol. 1995;8:471-476.
- Bovykin AM., Omel’chenko АМ, Shtemenko AV, Chasova EV. The unusial ability of a rhenium(V) complex containing nicotinamide to raise the conductivity of lipid membranes. Biophysics. 1995;40(3):525-529.
- Tomas ML, Coyle KV, Sultan M, Vaghar-Kashani A, Marcato P. Chemoresistance in cancer stem cells and strategies to overcome resistance. Chemotherapy. 2014;3(1):2-10. CrossRef
- Wu A, Zheng L, Xiao Q. How cancer outsmarts treatments: assessing drug resistance in tumors. J Cancer Biol Res. 2013;1(3):1-4.
- Alama A, Orengo AM, Ferrini S, Gangemi R. Targeting cancer-initiating cell drug-resistance: a roadmap to a new-generation of cancer therapies? Drug Discov Today. 2012 May;17(9-10):435-42. Review. PubMed, CrossRef
- Chechun BF, Shishova UV. Contemporary glance on the mechanisms of tumor drug resistance. Oncology. 2000;2(1-2):11-15. (In Russian).
- Kuluk GI, Pivnuk VM, Nosko MM. Liposomal preparations: a way to overcome drug resistance to cisplatin. Oncology. 2009;11(1):76-80. (In Russian).
- Pande V, Ramos MJ. NF-kappaB in human disease: current inhibitors and prospects for de novo structure based design of inhibitors. Curr Med Chem. 2005;12(3):357-74. Review. PubMed, CrossRef
- Wheatley D. Regrowth of tumour cells from supposedly terminal giant cells. Oncology News. 2006;1(3): 3.
- Moliterno AR, Spivak JL. Anemia of cancer. Hematol Oncol Clin North Am. 1996 Apr;10(2):345-63. PubMed
- Blohmer JU, Dunst J, Harrison L, Johnston P, Khayat D, Ludwig H, O’Brien M, Van Belle S, Vaupel P. Cancer-related anemia: biological findings, clinical implications and impact on quality of life. Oncology. 2005;68 Suppl 1:12-21. PubMed, CrossRef
- Park SH, Lee J, Lee SH, Park JO, Kim K, Kim WS, Jung CW, Park YS, Kang WK, Park K, Kim S, Bang SM, Cho EK, Shin DB, Lee JH. Anemia is the strongest prognostic factor for outcomes of 5-fluorouracil-based first-line chemotherapy in patients with advanced gastric cancer. Cancer Chemother Pharmacol. 2006 Jan;57(1):91-6. PubMed, CrossRef
- Varlotto J, Stevenson MA. Anemia, tumor hypoxemia, and the cancer patient. Int J Radiat Oncol Biol Phys. 2005 Sep 1;63(1):25-36. Review. PubMed, CrossRef
- Krzystek-Korpacka M, Matusiewicz M, Diakowska D, Grabowski K, Blachut K, Kustrzeba-Wojcicka I, Gamian A. Even a mild anemia is related to tumor aggressiveness mediated by angiogenic factors. Exp Oncol. 2009 Mar;31(1):52-6. PubMed
- Glaspy J, Bukowski R, Steinberg D, Taylor C, Tchekmedyian S, Vadhan-Raj S. Impact of therapy with epoetin alfa on clinical outcomes in patients with nonmyeloid malignancies during cancer chemotherapy in community oncology practice. Procrit Study Group. J Clin Oncol. 1997 Mar;15(3):1218-34. PubMed
- Taylor SK. Is recombinant human erythropoietin (rh-epo) more than just a treatment of anemia in cancer and chemotherapy? Med Hypotheses. 2003 Jan;60(1):89-93. Review. PubMed, CrossRef
- Henke M, Laszig R, Rübe C, Schäfer U, Haase KD, Schilcher B, Mose S, Beer KT, Burger U, Dougherty C, Frommhold H. Erythropoietin to treat head and neck cancer patients with anaemia undergoing radiotherapy: randomised, double-blind, placebo-controlled trial. Lancet. 2003 Oct 18;362(9392):1255-60. PubMed, CrossRef
- Voronkova YS, Babiy SO, Ivans’kar LV, Shtemenko OV, Shtemenko NI. Antioxidant properties of cluster rhenium compounds and their effect on erythropoiesis of rats with guerin carcinoma. Ukr Biochem J. 2015 Jan-Feb;87(1):99-108. (In Ukrainian). PubMed, CrossRef
- Wondrak GT. Redox-directed cancer therapeutics: molecular mechanisms and opportunities. Antioxid Redox Signal. 2009 Dec;11(12):3013-69. Review. PubMed, PubMedCentral, CrossRef
- Hybertson BM, Gao B, Bose SK, McCord JM. Oxidative stress in health and disease: the therapeutic potential of Nrf2 activation. Mol Aspects Med. 2011 Aug;32(4-6):234-46. Review. PubMed, CrossRef
- Sainz RM, Lombo F, Mayo JC. Radical decisions in cancer: redox control of cell growth and death. Cancers (Basel). 2012 Apr 25;4(2):442-74. PubMed, PubMedCentral, CrossRef
- Leus IV, Shamelashvili KL, Skoryk OD, Tretiak SIu, Golichenko OA, Shtemenko OV, Shtemenko NI. Antioxidant and antitumor activity of dirhenium dicarboxylates in animals with guerin carcinoma. Ukr Biokhim Zhurn. 2012 May-Jun;84(3):72-81. (In Ukrainian). PubMed
- Ratnam DV, Ankola DD, Bhardwaj V, Sahana DK, Kumar MN. Role of antioxidants in prophylaxis and therapy: A pharmaceutical perspective. J Control Release. 2006 Jul 20;113(3):189-207. Review. PubMed, CrossRef
- Jungwirth U, Kowol CR, Keppler BK, Hartinger CG, Berger W, Heffeter P. Anticancer activity of metal complexes: involvement of redox processes. Antioxid Redox Signal. 2011 Aug 15;15(4):1085-127. Review. PubMed, PubMedCentral, CrossRef
- Leus IV, Klenina IV, Zablotska KA, Golichenko OA, Shtemenko OV, Shtemenko NI. Interaction of serum albumins with cluster rhenium compounds of cis- and trans-configuration. Biopolym Cell. 2011;27(6):465-471. (In Ukrainian). CrossRef
- Shamelashvili KL, Shtemenko NI, Leus ІV, Babiy SO, Shtemenko OV. Changes in oxidative stress intensity in blood of tumor-bearing rats following different modes of administration of rhenium-platinum system. Ukr Biochem J. 2016; 88(4):29-39. CrossRef
- Howard MD, Greineder CF, Hood ED, Muzykantov VR. Endothelial targeting of liposomes encapsulating SOD/catalase mimetic EUK-134 alleviates acute pulmonary inflammation. J Control Release. 2014 Mar 10;177:34-41. PubMed, PubMedCentral, CrossRef
- Pirmohamed T, Dowding JM, Singh S, Wasserman B, Heckert E, Karakoti AS, King JE, Seal S, Self WT. Nanoceria exhibit redox state-dependent catalase mimetic activity. Chem Commun (Camb). 2010 Apr 28;46(16):2736-8. PubMed, PubMedCentral, CrossRef
- Gupta SC, Sundaram C, Reuter S, Aggarwal BB. Inhibiting NF-κB activation by small molecules as a therapeutic strategy. Biochim Biophys Acta. 2010 Oct-Dec;1799(10-12):775-87. Review. PubMed, PubMedCentral, CrossRef
- Gilmore TD, Herscovitch M. Inhibitors of NF-kappaB signaling: 785 and counting. Oncogene. 2006 Oct 30;25(51):6887-99. Review. PubMed, CrossRef
- Olivera A, Moore TW, Hu F, Brown AP, Sun A, Liotta DC, Snyder JP, Yoon Y, Shim H, Marcus AI, Miller AH, Pace TW. Inhibition of the NF-κB signaling pathway by the curcumin analog, 3,5-Bis(2-pyridinylmethylidene)-4-piperidone (EF31): anti-inflammatory and anti-cancer properties. Int Immunopharmacol. 2012 Feb;12(2):368-77. PubMed, PubMedCentral, CrossRef
- Wilken R, Veena MS, Wang MB, Srivatsan ES. Curcumin: A review of anti-cancer properties and therapeutic activity in head and neck squamous cell carcinoma. Mol Cancer. 2011 Feb 7;10:12. Review. PubMed, PubMedCentral, CrossRef
- Ivchuk VV, Polishko TM, Golichenko OA, Shtemenko OV, Shtemenko NI. Influence of antitumor system rhenium-platinum on biochemical state of the liver. Ukr Biokhim Zhurn. 2011 May-Jun;83(3):76-84. (In Ukrainian). PubMed
- Babiy SA, Loskutova TF, Shtemenko NI. Changes of the state of rat kidneys under Guerin carcinoma development and use of cytostatics. Ukr Biokhim Zhurn. 2012 May-Jun;84(3):63-71. (In Ukrainian). PubMed
- Lu Y, Cederbaum AI. Cisplatin-induced hepatotoxicity is enhanced by elevated expression of cytochrome P450 2E1. Toxicol Sci. 2006 Feb;89(2):515-23. PubMed, CrossRef
- Liao Y, Lu X, Lu C, Li G, Jin Y, Tang H. Selection of agents for prevention of cisplatin-induced hepatotoxicity. Pharmacol Res. 2008 Feb;57(2):125-31. PubMed CrossRef
- Avci A, Cetin R, Erguder IB, Devrim E, Kilicoglu B, Candir O, Ozturk HS, Durak I. Cisplatin causes oxidation in rat liver tissues: possible protective effects of antioxidant food supplementation. Turk J Med Sci. 2008;38(2):117-120.
- Abdel Wahab SI, Abdul AB, Alzubairi AS, Mohamed Elhassan M, Mohan S. In vitro ultramorphological assessment of apoptosis induced by zerumbone on (HeLa). J Biomed Biotechnol. 2009;2009:769568. PubMed, PubMedCentral, CrossRef
- Shtemenko NI, Chifotides HT, Domasevitch KV, Golichenko AA, Babiy SA, Zhanyong Li, Paramonova KV, Shtemenko AV, Dunbar KR. Synthesis, X-ray structure, interactions with DNA, remarkable in vivo tumor growth suppression and nephroprotective activity of cis-tetrachloro-dipivalato dirhenium(III). J Inorg Biochem. 2013 Dec;129:127-134. CrossRef
