Top

Published in:

Open Access 01-08-2015 | PRECLINICAL STUDIES

Antitumor activity of a rhenium (I)-diselenoether complex in experimental models of human breast cancer

Authors: Philippe Collery, Ahmed Mohsen, Anthony Kermagoret, Samantha Corre, Gérard Bastian, Alain Tomas, Ming Wei, François Santoni, Nadia Guerra, Didier Desmaële, Jean d’Angelo

Published in: Investigational New Drugs | Issue 4/2015

Summary

Rhenium (I)-diselenother (Re-diselenoether) is a water soluble metal-based compound, combining one atom of rhenium and two atoms of selenium. This compound has been reported to exhibit marked activities against several solid tumor cell lines. We now disclose an improved synthesis of this complex. The Re-diselenoether showed a potent inhibitory effect on MDA-MB231 cell division in vitro, which lasted when the complex was no longer present in the culture. Re-diselenoether induced a remarkable reduction of the volume of the primitive breast tumors and of the pulmonary metastases without clinical signs of toxicity, in mice-bearing a MDA-MB231 Luc+ tumor, orthotopically transplanted, after a daily oral administration at the dose of 10 mg/kg/d. Interestingly, an antagonism was observed when cisplatin was administered as a single i.p. injection 1 week after the end of the Re-diselenoether administration. In an effort to gain insight of the mechanisms of action of Re-diselenoether complex, interaction with 9-methylguanine as a nucleic acid base model was studied. We have shown that Re-diselenoether gave both mono- and bis-guanine Re adducts, the species assumed to be responsible for the DNA intrastrand lesions.

Available only for authorised users

Gasser G, Ott I, Metzler-Nolte N (2011) Organometallic anticancer compounds. J Med Chem 54(1):3–25. doi:10.1021/jm100020w PubMedCentralPubMedCrossRef

Leonidova A, Gasser G (2014) Underestimated potential of organometallic rhenium complexes as anticancer agents. ACS Chem Biol 9(10):2180–2193. doi:10.1021/cb500528c PubMedCrossRef

Parson C, Smith V, Krauss C, Banerjee HN, Reilly C, Krause JA, Wachira JM, Giri D, Winstead A, Mandal SK (2014) Anticancer properties of novel rhenium pentylcarbanato compounds against MDA-MB-468(HTB-132) triple node negative human breast cancer cell lines. Br J Pharm Res 4(3):362–367. doi:10.9734/BJPR/2014/4697 CrossRef

Fernandez-Herrera MA, Sandoval-Ramirez J, Sanchez-Sanchez L, Lopez-Munoz H, Escobar-Sanchez ML (2014) Probing the selective antitumor activity of 22-oxo-26-selenocyanocholestane derivatives. Eur J Med Chem 74:451–460. doi:10.1016/j.ejmech.2013.12.059 PubMedCrossRef

Guo P, Zhao P, Liu J, Ma H, Bai J, Cao Y, Liu Y, He H, Qi C (2013) Preparation of a novel organoselenium compound and its anticancer effects on cervical cancer cell line HeLa. Biol Trace Elem Res 151(2):301–306. doi:10.1007/s12011-012-9563-x PubMedCrossRef

Ibanez E, Plano D, Font M, Calvo A, Prior C, Palop JA, Sanmartin C (2011) Synthesis and antiproliferative activity of novel symmetrical alkylthio- and alkylseleno-imidocarbamates. Eur J Med Chem 46(1):265–274. doi:10.1016/j.ejmech.2010.11.013 PubMedCrossRef

Wallenberg M, Misra S, Bjornstedt M (2014) Selenium cytotoxicity in cancer. Basic Clin Pharmacol 114(5):377–386. doi:10.1111/bcpt.12207 CrossRef

Kermagoret A, Morgant G, D’Angelo J, Tomas A, Roussel P, Bastian G, Collery P, Desmaële D (2011) Synthesis, structural characterization and biological activity against several human tumor cell lines of four rhenium(I) diseleno-ethers complexes: Re(CO)3Cl(PhSe(CH2)2SePh), Re(CO)3Cl(PhSe(CH2)3SePh), Re(CO)3Cl(HO2C–CH2Se(CH2)2SeCH2–CO2H) and Re(CO)3Cl(HO2C–CH2Se(CH2)3SeCH2–CO2H). Polyhedron 30:347–354CrossRef

Collery P, Bastian G, Santoni S, Mohsen A, Wei M, Collery T, Tomas A, Desmaele D, d’Angelo J (2014) Uptake and efflux of rhenium in cells exposed to rhenium diseleno-ether and tissue distribution of rhenium and selenium after rhenium diseleno-ether treatment in mice. Anticancer Res 34(4):1679–1690PubMed

10.

Collery P, Mohsen A, Kermagoret A, d’Angelo J, Morgant G, Desmaele D, Tomas A, Collery T, Wei M, Badawi A (2012) Combination of Three Metals for the Treatment of Cancer: Gallium, Rhenium and Platinum. 1- Determination of the Optimal Schedule of Treatment. Anticancer Res 32(7):2769–2782PubMed

11.

Walker MK, Boberg JR, Walsh MT, Wolf V, Trujillo A, Duke MS, Palme R, Felton LA (2012) A less stressful alternative to oral gavage for pharmacological and toxicological studies in mice. Toxicol Appl Pharmacol 260(1):65–69. doi:10.1016/j.taap.2012.01.025 PubMedCentralPubMedCrossRef

12.

Uehara T, Koike M, Nakata H, Miyamoto S, Motoishi S, Hashimoto K, Oku N, Nakayama M, Arano Y (2003) In vivo recognition of cyclopentadienyltricarbonylrhenium (CpTR) derivatives. Nucl Med Biol 30(3):327–334PubMedCrossRef

13.

Novotny L, Rauko P, Kombian SB, Edafiogho IO (2010) Selenium as a chemoprotective anti-cancer agent: reality or wishful thinking? Neoplasma 57(5):383–391PubMedCrossRef

14.

Desai D, Kaushal N, Gandhi UH, Arner RJ, D’Souza C, Chen G, Vunta H, El-Bayoumy K, Amin S, Prabhu KS (2010) Synthesis and evaluation of the anti-inflammatory properties of selenium-derivatives of celecoxib. Chem Biol Interact 188(3):446–456. doi:10.1016/j.cbi.2010.09.021 PubMedCentralPubMedCrossRef

15.

Facompre ND, El-Bayoumy K, Sun YW, Pinto JT, Sinha R (2010) 1,4-phenylenebis(methylene)selenocyanate, but not selenomethionine, inhibits androgen receptor and Akt signaling in human prostate cancer cells. Cancer Prev Res (Phila) 3(8):975–984. doi:10.1158/1940-6207.CAPR-10-0054 CrossRef

16.

Facompre ND, Sinha I, El-Bayoumy K, Pinto JT, Sinha R (2012) Remarkable inhibition of mTOR signaling by the combination of rapamycin and 1,4-phenylenebis(methylene)selenocyanate in human prostate cancer cells. Int J Cancer 131(9):2134–2142. doi:10.1002/ijc.27468 PubMedCentralPubMedCrossRef

17.

Sanmartin C, Plano D, Font M, Palop JA (2011) Kinase regulation by sulfur and selenium containing compounds. Curr Cancer Drug Targets 11(4):496–523PubMedCrossRef

18.

Moreno E, Plano D, Lamberto I, Font M, Encio I, Palop JA, Sanmartin C (2012) Sulfur and selenium derivatives of quinazoline and pyrido[2,3-d]pyrimidine: synthesis and study of their potential cytotoxic activity in vitro. Eur J Med Chem 47(1):283–298. doi:10.1016/j.ejmech.2011.10.056 PubMedCrossRef

19.

Sanmartin C, Plano D, Sharma AK, Palop JA (2012) Selenium compounds, apoptosis and other types of cell death: an overview for cancer therapy. Int J Mol Sci 13(8):9649–9672. doi:10.3390/ijms13089649 PubMedCentralPubMedCrossRef

20.

Zobi F, Blacque O, Schmalle HW, Spingler B, Alberto R (2004) Head-to-head (HH) and head-to-tail (HT) conformers of cis-bis guanine ligands bound to the [Re(CO)₃] + core. Inorg Chem 43(6):2087–2096. doi:10.1021/ic035012a PubMedCrossRef

21.

Zobi F, Spingler B, Alberto R (2005) Guanine and plasmid DNA binding of mono- and trinuclear fac-[Re(CO)3] + complexes with amino acid ligands. Chembiochem 6(8):1397–1405. doi:10.1002/cbic.200400453 PubMedCrossRef

22.

Ho J, Lee WY, Koh KJ, Lee PP, Yan YK (2013) Rhenium(I) tricarbonyl complexes of salicylaldehyde semicarbazones: synthesis, crystal structures and cytotoxicity. J Inorg Biochem 119:10–20. doi:10.1016/j.jinorgbio.2012.10.011 PubMedCrossRef

23.

Shtemenko N, Collery Ph, Shtemenko A (2006) Synergistic effect of cisplatin and cis-rhenium (III) diadamantate on tumor growth. In: Alpoim M C,Vasconcellos Morais P, Santos M A, Cristovao A J, Centeno J A, Collery P H (ed) Metal Ions in Biology and Medicine John Libbey Eurotext, Paris 9:374–381

24.

Shtemenko N, Collery P, Shtemenko A (2007) Dichlorotetra-μ-isobutyratodirhenium (III): enhancement of cisplatin action and RBC-stabilizing properties. Anticancer Res 27:2487–2492PubMed

25.

Shtemenko AV, Collery P, Shtemenko NI, Domasevitch KV, Zabitskaya ED, Golichenko AA (2009) Synthesis, characterization, in vivo antitumor properties of the cluster rhenium compound with GABA ligands and its synergism with cisplatin. Dalton Trans 26:5132–5136. doi:10.1039/b821041a PubMedCrossRef

26.

Zobi F, Blacque O, Sigel RK, Alberto R (2007) Binding interaction of [Re(H2O)3(CO)3] + with the DNA fragment d(CpGpG). Inorg Chem 46(25):10458–10460. doi:10.1021/ic701647m PubMedCrossRef

27.

Zobi F, Spingler B (2012) Post-protein-binding reactivity and modifications of the fac-[Re(CO)3] + core. Inorg Chem 51(3):1210–1212. doi:10.1021/ic2023314 PubMedCrossRef

28.

Prater ME, Mindiola DJ, Ouyang X, Dunbar KR (1998) A quadruply-bonded dirhenium complex bridged by two N1/N6 adenate ligands. Inorg Chem Commun 1:475–477CrossRef

29.

Adams KM, Marzilli LG (2007) fac-[Re(CO)3(H2O)3] + nucleoside monophosphate adducts investigated in aqueous solution by multinuclear NMR spectroscopy. Inorg Chem 46(12):4926–4936. doi:10.1021/ic062410f PubMedCrossRef

30.

Adams KM, Marzilli PA, Marzilli LG (2007) Reactions of fac-[Re(CO)3(H2O)3] + with nucleoside diphosphates and thiamine diphosphate in aqueous solution investigated by multinuclear NMR spectroscopy. Inorg Chem 46(22):9172–9181. doi:10.1021/ic701038f PubMedCrossRef

31.

Mencalha A, Victorino VJ, Cecchini R, Panis C (2014) Mapping oxidative changes in breast cancer: understanding the basic to reach the clinics. Anticancer Res 34(3):1127–1140PubMed

32.

Panis C, Victorino VJ, Herrera AC, Freitas LF, De Rossi T, Campos FC, Simao AN, Barbosa DS, Pinge-Filho P, Cecchini R, Cecchini AL (2012) Differential oxidative status and immune characterization of the early and advanced stages of human breast cancer. Breast Cancer Res Treat 133(3):881–888. doi:10.1007/s10549-011-1851-1 PubMedCrossRef

33.

Herrera AC, Panis C, Victorino VJ, Campos FC, Colado-Simao AN, Cecchini AL, Cecchini R (2012) Molecular subtype is determinant on inflammatory status and immunological profile from invasive breast cancer patients. Cancer Immunol Immunother 61(11):2193–2201. doi:10.1007/s00262-012-1283-8 PubMedCrossRef

34.

Kim J, Mizokami A, Shin M, Izumi K, Konaka H, Kadono Y, Kitagawa Y, Keller ET, Zhang J, Namiki M (2014) SOD3 acts as a tumor suppressor in PC-3 prostate cancer cells via hydrogen peroxide accumulation. Anticancer Res 34(6):2821–2831PubMed

35.

Pons DG, Sastre-Serra J, Nadal-Serrano M, Oliver A, Garcia-Bonafe M, Bover I, Roca P, Oliver J (2012) Initial activation status of the antioxidant response determines sensitivity to carboplatin/paclitaxel treatment of ovarian cancer. Anticancer Res 32(11):4723–4728PubMed

36.

Panis C, Herrera AC, Victorino VJ, Campos FC, Freitas LF, De Rossi T, Colado Simao AN, Cecchini AL, Cecchini R (2012) Oxidative stress and hematological profiles of advanced breast cancer patients subjected to paclitaxel or doxorubicin chemotherapy. Breast Cancer Res Treat 133(1):89–97. doi:10.1007/s10549-011-1693-x PubMedCrossRef

37.

Lee KH, Jeong D (2012) Bimodal actions of selenium essential for antioxidant and toxic pro-oxidant activities: the selenium paradox (review). Mol Med Rep 5(2):299–304. doi:10.3892/mmr.2011.651 PubMed

38.

Jamier V, Ba LA, Jacob C (2010) Selenium- and tellurium-containing multifunctional redox agents as biochemical redox modulators with selective cytotoxicity. Chem Eur J 16(36):10920–10928. doi:10.1002/chem.201000884 PubMedCrossRef

39.

Park E-M, Choi K-S, Park S-Y, Kong E-S, Zu K, Wu Y, Zhang H, Ip C, Y-M P (2005) A display thiol-proteomics approach to characterize global redox modification of proteins by selenium: implications for the anticancer action of selenium. Cancer Genomics Proteomics 2:25–36

40.

Huang Z, Rose AH, Hoffmann PR (2012) The role of selenium in inflammation and immunity: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 16(7):705–743. doi:10.1089/ars.2011.4145 PubMedCentralPubMedCrossRef

41.

Duntas LH (2009) Selenium and inflammation: underlying anti-inflammatory mechanisms. Horm Metab Res 41(6):443–447. doi:10.1055/s-0029-1220724 PubMedCrossRef

42.

Poplawska B, Bielawska A, Surazynski A, Czarnomysy R, Bielawski K (2009) Novel dinuclear platinum(II) complexes targets NFkappaB signaling pathway to induce apoptosis and inhibit metabolism of MCF-7 breast cancer cells. Folia Histochem Cytobiol 47(5):S141–S146. doi:10.2478/v10042-009-0084-1 PubMed

43.

Kretz-Remy C, Arrigo AP (2001) Selenium: a key element that controls NF-kappa B activation and I kappa B alpha half life. Biofactors 14(1–4):117–125PubMedCrossRef

44.

Youn HS, Lim HJ, Choi YJ, Lee JY, Lee MY, Ryu JH (2008) Selenium suppresses the activation of transcription factor NF-kappa B and IRF3 induced by TLR3 or TLR4 agonists. Int Immunopharmacol 8(3):495–501. doi:10.1016/j.intimp.2007.12.008 PubMedCrossRef

45.

Shigdar S, Li Y, Bhattacharya S, O’Connor M, Pu C, Lin J, Wang T, Xiang D, Kong L, Wei MQ, Zhu Y, Zhou S, Duan W (2014) Inflammation and cancer stem cells. Cancer Lett 345(2):271–278. doi:10.1016/j.canlet.2013.07.031 PubMedCrossRef

46.

Petrie HT, Klassen LW, Kay HD (1989) Selenium and the immune response: 1. Modulation of alloreactive human lymphocyte functions in vitro. J Leukoc Biol 45(3):207–214PubMed

47.

Arthur JR, McKenzie RC, Beckett GJ (2003) Selenium in the immune system. J Nutr 133(5 Suppl 1):1457S–1459SPubMed

48.

Broome CS, McArdle F, Kyle JA, Andrews F, Lowe NM, Hart CA, Arthur JR, Jackson MJ (2004) An increase in selenium intake improves immune function and poliovirus handling in adults with marginal selenium status. Am J Clin Nutr 80(1):154–162PubMed

49.

Petrie HT, Klassen LW, Klassen PS, O’Dell JR, Kay HD (1989) Selenium and the immune response: 2. Enhancement of murine cytotoxic T-lymphocyte and natural killer cell cytotoxicity in vivo. J Leukoc Biol 45(3):215–220PubMed

50.

Kiremidjian-Schumacher L, Roy M, Wishe HI, Cohen MW, Stotzky G (1996) Supplementation with selenium augments the functions of natural killer and lymphokine-activated killer cells. Biol Trace Elem Res 52(3):227–239. doi:10.1007/BF02789164 PubMedCrossRef

51.

Kiremidjian-Schumacher L, Roy M (1998) Selenium and immune function. Z Ernaehrungswiss 37(Suppl 1):50–56

52.

Hagemann-Jensen M, Uhlenbrock F, Kehlet S, Andresen L, Gabel-Jensen C, Ellgaard L, Gammelgaard B, Skov S (2014) The selenium metabolite methylselenol regulates the expression of ligands that trigger immune activation through the lymphocyte receptor NKG2D. J Biol Chem 289(45):31576–31590. doi:10.1074/jbc.M114.591537 PubMedCrossRef

53.

Bae DS, Hwang YK, Lee JK (2012) Importance of NKG2D-NKG2D ligands interaction for cytolytic activity of natural killer cell. Cell Immunol 276(1–2):122–127. doi:10.1016/j.cellimm.2012.04.011 PubMedCrossRef

54.

Billadeau DD, Upshaw JL, Schoon RA, Dick CJ, Leibson PJ (2003) NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway. Nat Immunol 4(6):557–564. doi:10.1038/ni929 PubMedCrossRef

55.

de Kruijf EM, Sajet A, van Nes JG, Putter H, Smit VT, Eagle RA, Jafferji I, Trowsdale J, Liefers GJ, van de Velde CJ, Kuppen PJ (2012) NKG2D ligand tumor expression and association with clinical outcome in early breast cancer patients: an observational study. BMC Cancer 12:24. doi:10.1186/1471-2407-12-24 PubMedCentralPubMedCrossRef

56.

Karimi M, Cao TM, Baker JA, Verneris MR, Soares L, Negrin RS (2005) Silencing human NKG2D, DAP10, and DAP12 reduces cytotoxicity of activated CD8+ T cells and NK cells. J Immunol 175(12):7819–7828PubMedCrossRef

57.

Raulet DH, Gasser S, Gowen BG, Deng W, Jung H (2013) Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol 31:413–441. doi:10.1146/annurev-immunol-032712-095951 PubMedCentralPubMedCrossRef

58.

Zafirova B, Wensveen FM, Gulin M, Polic B (2011) Regulation of immune cell function and differentiation by the NKG2D receptor. Cell Mol Life Sci 68(21):3519–3529. doi:10.1007/s00018-011-0797-0 PubMedCentralPubMedCrossRef

59.

Shrimali RK, Irons RD, Carlson BA, Sano Y, Gladyshev VN, Park JM, Hatfield DL (2008) Selenoproteins mediate T cell immunity through an antioxidant mechanism. J Biol Chem 283(29):20181–20185. doi:10.1074/jbc.M802559200 PubMedCentralPubMedCrossRef

60.

Vunta H, Belda BJ, Arner RJ, Channa Reddy C, Vanden Heuvel JP, Sandeep Prabhu K (2008) Selenium attenuates pro-inflammatory gene expression in macrophages. Mol Nutr Food Res 52(11):1316–1323. doi:10.1002/mnfr.200700346 PubMedCrossRef

61.

Plano D, Ibanez E, Calvo A, Palop JA, Sanmartin C (2011) Novel library of selenocompounds as kinase modulators. Molecules 16(8):6349–6364. doi:10.3390/molecules16086349 PubMedCrossRef

62.

Ibanez E, Agliano A, Prior C, Nguewa P, Redrado M, Gonzalez-Zubeldia I, Plano D, Palop AJ, Sanmartin C, Calvo A (2012) The quinoline imidoselenocarbamate EI201 blocks the AKT/mTOR pathway and targets cancer stem cells leading to a strong antitumor activity. Curr Med Chem 19(1):3031–3043PubMedCrossRef

63.

Bhattacharya A, Turowski SG, San Martin ID, Rajput A, Rustum YM, Hoffman RM, Seshadri M (2011) Magnetic resonance and fluorescence-protein imaging of the anti-angiogenic and anti-tumor efficacy of selenium in an orthotopic model of human colon cancer. Anticancer Res 31(2):387–393PubMedCentralPubMed

64.

Li Z, Carrier L, Belame A, Thiyagarajah A, Salvo VA, Burow ME, Rowan BG (2009) Combination of methylselenocysteine with tamoxifen inhibits MCF-7 breast cancer xenografts in nude mice through elevated apoptosis and reduced angiogenesis. Breast Cancer Res Treat 118(1):33–43. doi:10.1007/s10549-008-0216-x PubMedCrossRef

65.

Chen YC, Prabhu KS, Mastro AM (2013) Is selenium a potential treatment for cancer metastasis? Nutrients 5(4):1149–1168. doi:10.3390/nu5041149 PubMedCentralPubMedCrossRef

66.

Franca CA, Nogueira CR, Ramalho A, Carvalho AC, Vieira SL, Penna AB (2011) Serum levels of selenium in patients with breast cancer before and after treatment of external beam radiotherapy. Ann Oncol 22(5):1109–1112. doi:10.1093/annonc/mdq547 PubMedCrossRef

67.

Collery P, D’Angelo J, Morgant G (2015) Rhenium complexes and their pharmaceutical use. Eur Patent 2575800

Title: Antitumor activity of a rhenium (I)-diselenoether complex in experimental models of human breast cancer
Authors: Philippe Collery
Ahmed Mohsen
Anthony Kermagoret
Samantha Corre
Gérard Bastian
Alain Tomas
Ming Wei
François Santoni
Nadia Guerra
Didier Desmaële
Jean d’Angelo
Publication date: 01-08-2015
Publisher: Springer US
Published in: Investigational New Drugs / Issue 4/2015
Print ISSN: 0167-6997
Electronic ISSN: 1573-0646
DOI: https://doi.org/10.1007/s10637-015-0265-z

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras

Prof. Fabrice Barlesi

Developed by: Springer Medicine

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Summary

Please log in to get access to this content

Other articles of this Issue 4/2015

Multicenter phase II study of the AKT inhibitor MK-2206 in recurrent or metastatic nasopharyngeal carcinoma from patients in the mayo phase II consortium and the cancer therapeutics research group (MC1079)

Phase I study of the heat shock protein 90 (Hsp90) inhibitor onalespib (AT13387) administered on a daily for 2 consecutive days per week dosing schedule in patients with advanced solid tumors

Phase 1 dose escalation trial of ilorasertib, a dual Aurora/VEGF receptor kinase inhibitor, in patients with hematologic malignancies

Generation and tumor recognition properties of two human monoclonal antibodies specific to cell surface anionic phospholipids

Phase I study of ipilimumab in phased combination with paclitaxel and carboplatin in Japanese patients with non-small-cell lung cancer

A phase 1 study with dose expansion of the CDK inhibitor dinaciclib (SCH 727965) in combination with epirubicin in patients with metastatic triple negative breast cancer

Keynote webinar | Spotlight on antibody–drug conjugates in cancer