Generic placeholder image

Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

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

Research Article

Oxidative Stress Modulation and Radiosensitizing Effect of Quinoxaline-1,4-Dioxides Derivatives

Author(s): Liliana Silva, Pedro Coelho, Dulce Teixeira, Armanda Monteiro, Gabriela Pinto, Raquel Soares, Cristina Prudêncio and Mónica Vieira*

Volume 20, Issue 1, 2020

Page: [111 - 120] Pages: 10

DOI: 10.2174/1871520619666191028091547

Price: $65

Abstract

Background: Quinoxaline-1,4-dioxide (QNX) derivatives are synthetic heterocyclic compounds with multiple biological and pharmacological effects.

Objective: In this study, we investigated the oxidative status of quinoxaline-1,4-dioxides derivatives in modulating melanoma and glioma cell lines, based on previous results from the research group and their capability to promote cell damage by the production of Reactive Oxygen Species (ROS).

Methods: Using in vitro cell cultures, the influence of 2-amino-3-cyanoquinoxaline-1,4-dioxide (2A3CQNX), 3- methyl-2-quinoxalinecarboxamide-1,4-dioxide (3M2QNXC) and 2-hydroxyphenazine-1,4-dioxide (2HF) was evaluated in metabolic activity, catalase activity, glutathione and 3-nitrotyrosine (3-NT) quantitation by HPLC in malignant melanocytes (B16-F10, MeWo) and brain tumor cells (GL-261 and BC3H1) submitted to radiotherapy treatments (total dose of 6 Gy).

Results: 2HF increased the levels of 3-NT in non-irradiated MeWo and glioma cell lines and decreased cell viability in these cell lines with and without irradiation.

Conclusion: Quinoxaline-1,4-dioxides derivatives modulate the oxidative status in malignant melanocytes and brain tumor cell lines and exhibited a potential radiosensitizer in vitro action on the tested radioresistant cell lines.

Keywords: Quinoxaline-1, 4-dioxides derivatives, oxidative stress, radiation resistance, melanoma, glioma, radiosensitizing.

Graphical Abstract
[1]
Zhang, Y.; Chang, F-M.; Huang, J.; Junco, J.J.; Maffi, S.K.; Pridgen, H.I. DSSylation, a novel protein modification targets proteins induced by oxidative stress, and facilitates their degradation in cells. Protein Cell, 2014, 5(2), 124-140.
[http://dx.doi.org/10.1007/s13238-013-0018-8]
[2]
Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: the next generation. Cell, 2011, 144(5), 646-674.
[http://dx.doi.org/10.1016/j.cell.2011.02.013] [PMID: 21376230]
[3]
Xu, X.D.; Shao, S.X.; Jiang, H.P.; Cao, Y.W.; Wang, Y.H.; Yang, X.C.; Wang, Y.L.; Wang, X.S.; Niu, H.T. Warburg effect or reverse Warburg effect? A review of cancer metabolism. Oncol. Res. Treat., 2015, 38(3), 117-122.
[http://dx.doi.org/10.1159/000375435] [PMID: 25792083]
[4]
Cencioni, C.; Spallotta, F.; Martelli, F.; Valente, S.; Mai, A.; Zeiher, A.M.; Gaetano, C. Oxidative stress and epigenetic regulation in ageing and age-related diseases. Int. J. Mol. Sci., 2013, 14(9), 17643-17663.
[http://dx.doi.org/10.3390/ijms140917643] [PMID: 23989608]
[5]
Riley, P.A. Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int. J. Radiat. Biol., 1994, 65(1), 27-33.
[http://dx.doi.org/10.1080/09553009414550041] [PMID: 7905906]
[6]
Robey, R.B.; Weisz, J.; Kuemmerle, N.B.; Salzberg, A.C.; Berg, A.; Brown, D.G.; Kubik, L.; Palorini, R.; Al-Mulla, F.; Al-Temaimi, R.; Colacci, A.; Mondello, C.; Raju, J.; Woodrick, J.; Scovassi, A.I.; Singh, N.; Vaccari, M.; Roy, R.; Forte, S.; Memeo, L.; Salem, H.K.; Amedei, A.; Hamid, R.A.; Williams, G.P.; Lowe, L.; Meyer, J.; Martin, F.L.; Bisson, W.H.; Chiaradonna, F.; Ryan, E.P. Metabolic reprogramming and dysregulated metabolism: cause, consequence and/or enabler of environmental carcinogenesis? Carcinogenesis, 2015, 36(Suppl. 1), S203-S231.
[http://dx.doi.org/10.1093/carcin/bgv037] [PMID: 26106140]
[7]
Kroemer, G.; Galluzzi, L.; Brenner, C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev., 2007, 87(1), 99-163.
[8]
Pettersen, E.O.; Ebbesen, P.; Gieling, R.G.; Williams, K.J.; Dubois, L.; Lambin, P.; Ward, C.; Meehan, J.; Kunkler, I.H.; Langdon, S.P.; Ree, A.H.; Flatmark, K.; Lyng, H.; Calzada, M.J.; Peso, L.D.; Landazuri, M.O.; Görlach, A.; Flamm, H.; Kieninger, J.; Urban, G.; Weltin, A.; Singleton, D.C.; Haider, S.; Buffa, F.M.; Harris, A.L.; Scozzafava, A.; Supuran, C.T.; Moser, I.; Jobst, G.; Busk, M.; Toustrup, K.; Overgaard, J.; Alsner, J.; Pouyssegur, J.; Chiche, J.; Mazure, N.; Marchiq, I.; Parks, S.; Ahmed, A.; Ashcroft, M.; Pastorekova, S.; Cao, Y.; Rouschop, K.M.; Wouters, B.G.; Koritzinsky, M.; Mujcic, H.; Cojocari, D. Targeting tumour hypoxia to prevent cancer metastasis. From biology, biosensing and technology to drug development: the METOXIA consortium. J. Enzyme Inhib. Med. Chem., 2015, 30(5), 689-721.
[http://dx.doi.org/10.3109/14756366.2014.966704] [PMID: 25347767]
[9]
Wu, Y-S.; Chen, S-N. Apoptotic cell: linkage of inflammation and wound healing. Front. Pharmacol., 2014, 5(17), 1.
[http://dx.doi.org/10.3389/fphar.2014.00001] [PMID: 24478702]
[10]
Møller, I.M.; Rogowska-Wrzesinska, A.; Rao, R.S.P. Protein carbonylation and metal-catalyzed protein oxidation in a cellular perspective. J. Proteomics, 2011, 74(11), 2228-2242.
[http://dx.doi.org/10.1016/j.jprot.2011.05.004] [PMID: 21601020]
[11]
Poulsen, H.E.; Nadal, L.L.; Broedbaek, K.; Nielsen, P.E.; Weimann, A. Detection and interpretation of 8-oxodG and 8-oxoGua in urine, plasma and cerebrospinal fluid. Biochim. Biophys. Acta, 2014, 1840(2), 801-808.
[http://dx.doi.org/10.1016/j.bbagen.2013.06.009] [PMID: 23791936]
[12]
Huang, K-J.; Jing, Q-S.; Wei, C-Y.; Wu, Y-Y. Spectrofluorimetric determination of glutathione in human plasma by solid-phase extraction using graphene as adsorbent. Spectrochim. Acta A Mol. Biomol. Spectrosc., 2011, 79(5), 1860-1865.
[http://dx.doi.org/10.1016/j.saa.2011.05.076] [PMID: 21684195]
[13]
Hart, P.C.; Mao, M.; de Abreu, A.L.P.; Ansenberger-Fricano, K.; Ekoue, D.N.; Ganini, D.; Kajdacsy-Balla, A.; Diamond, A.M.; Minshall, R.D.; Consolaro, M.E.L.; Santos, J.H.; Bonini, M.G. MnSOD upregulation sustains the Warburg effect via mitochondrial ROS and AMPK-dependent signalling in cancer. Nat. Commun., 2015, 6(1), 6053.
[http://dx.doi.org/10.1038/ncomms7053] [PMID: 25651975]
[14]
Ahn, J.; Ambrosone, C.B.; Kanetsky, P.A.; Tian, C.; Lehman, T.A.; Kropp, S.; Helmbold, I.; von Fournier, D.; Haase, W.; Sautter-Bihl, M.L.; Wenz, F.; Chang-Claude, J. Polymorphisms in genes related to oxidative stress (CAT, MnSOD, MPO, and eNOS) and acute toxicities from radiation therapy following lumpectomy for breast cancer. Clin. Cancer Res., 2006, 12(23), 7063-7070.
[http://dx.doi.org/10.1158/1078-0432.CCR-06-0039] [PMID: 17145829]
[15]
Klement, R.J.; Champ, C.E. Calories, carbohydrates, and cancer therapy with radiation: exploiting the five R’s through dietary manipulation. Cancer Metastasis Rev., 2014, 33(1), 217-229.
[http://dx.doi.org/10.1007/s10555-014-9495-3] [PMID: 24436017]
[16]
Housman, G.; Byler, S.; Heerboth, S.; Lapinska, K.; Longacre, M.; Snyder, N.; Sarkar, S. Drug resistance in cancer: an overview. Cancers (Basel), 2014, 6(3), 1769-1792.
[http://dx.doi.org/10.3390/cancers6031769] [PMID: 25198391]
[17]
Pereira, J.A.; Pessoa, A.M.; Cordeiro, M.N.D.S.; Fernandes, R.; Prudêncio, C.; Noronha, J.P.; Vieira, M. Quinoxaline, its derivatives and applications: A State of the Art review. Eur. J. Med. Chem., 2015, 97, 664-672.
[http://dx.doi.org/10.1016/j.ejmech.2014.06.058] [PMID: 25011559]
[18]
Cheng, G.; Sa, W.; Cao, C.; Guo, L.; Hao, H.; Liu, Z.; Wang, X.; Yuan, Z. Quinoxaline 1,4-di-N-oxides: Biological activities and mechanisms of actions. Front. Pharmacol., 2016, 7, 64.
[http://dx.doi.org/10.3389/fphar.2016.00064] [PMID: 27047380]
[19]
Vicente, E.; Villar, R.; Pérez-Silanes, S.; Aldana, I.; Goldman, R.C.; Mong, A. Quinoxaline 1,4-di-N-oxide and the potential for treating tuberculosis. Infect. Disord. Drug Targets, 2011, 11(2), 196-204.
[http://dx.doi.org/10.2174/187152611795589735] [PMID: 21470099]
[20]
Huang, A.; Liu, F.; Zhan, C.; Liu, Y.; Ma, C. One-pot synthesis of pyrrolo[1,2-a]quinoxalines. Org. Biomol. Chem., 2011, 9(21), 7351-7357.
[http://dx.doi.org/10.1039/c1ob05936j] [PMID: 21894335]
[21]
Vieira, M.; Pinheiro, C.; Fernandes, R.; Noronha, J.P.; Prudêncio, C. Antimicrobial activity of quinoxaline 1,4-dioxide with 2- and 3-substituted derivatives. Microbiol. Res., 2014, 169(4), 287-293.
[http://dx.doi.org/10.1016/j.micres.2013.06.015] [PMID: 23928379]
[22]
Santivañez-Veliz, M.; Pérez-Silanes, S.; Torres, E.; Moreno-Viguri, E. Design and synthesis of novel quinoxaline derivatives as potential candidates for treatment of multidrug-resistant and latent tuberculosis. Bioorg. Med. Chem. Lett., 2016, 26(9), 2188-2193.
[http://dx.doi.org/10.1016/j.bmcl.2016.03.066] [PMID: 27025343]
[23]
Gu, W.; Wang, S.; Jin, X.; Zhang, Y.; Hua, D.; Miao, T.; Tao, X.; Wang, S. Synthesis and evaluation of new quinoxaline derivatives of dehydroabietic acid as potential antitumor agents. Molecules, 2017, 22(7), 1154.
[http://dx.doi.org/10.3390/molecules22071154] [PMID: 28696365]
[24]
Patel, N.B.; Patel, J.N.; Purohit, A.C.; Patel, V.M.; Rajani, D.P.; Moo-Puc, R.; Lopez-Cedillo, J.C.; Nogueda-Torres, B.; Rivera, G. In vitro and in vivo assessment of newer quinoxaline-oxadiazole hybrids as antimicrobial and antiprotozoal agents. Int. J. Antimicrob. Agents, 2017, 50(3), 413-418.
[http://dx.doi.org/10.1016/j.ijantimicag.2017.04.016] [PMID: 28687457]
[25]
Miller, E.M.; Xia, Q.; Cella, M.E.; Nenninger, A.W.; Mruzik, M.N.; Brillos-Monia, K.A.; Hu, Y.Z.; Sheng, R.; Ragain, C.M.; Crawford, P.W. Voltammetric study of some 3-aryl-quinoxaline-2-carbonitrile 1,4-di-N-oxide Derivatives with anti-tumor activities. Molecules, 2017, 22(9), 1442.
[http://dx.doi.org/10.3390/molecules22091442] [PMID: 28858261]
[26]
Tariq, S.; Somakala, K.; Amir, M. Quinoxaline: An insight into the recent pharmacological advances. Eur. J. Med. Chem., 2018, 143, 542-557.
[http://dx.doi.org/10.1016/j.ejmech.2017.11.064] [PMID: 29207337]
[27]
Huang, X.J.; Zhang, H.H.; Wang, X.; Huang, L.L.; Zhang, L.Y.; Yan, C.X.; Liu, Y.; Yuan, Z.H. ROS mediated cytotoxicity of porcine adrenocortical cells induced by QdNOs derivatives in vitro. Chem. Biol. Interact., 2010, 185(3), 227-234.
[http://dx.doi.org/10.1016/j.cbi.2010.02.030] [PMID: 20188712]
[28]
Wang, X.; Martínez, M.A.; Cheng, G.; Liu, Z.; Huang, L.; Dai, M.; Chen, D.; Martínez-Larrañaga, M.R.; Anadón, A.; Yuan, Z. The critical role of oxidative stress in the toxicity and metabolism of quinoxaline 1,4-di-N-oxides in vitro and in vivo. Drug Metab. Rev., 2016, 48(2), 159-182.
[http://dx.doi.org/10.1080/03602532.2016.1189560] [PMID: 27285897]
[29]
Muz, B.; de la Puente, P.; Azab, F.; Azab, A.K. The role of hypoxia in cancer progression, angiogenesis, metastasis, and resistance to therapy. Hypoxia (Auckl.), 2015, 3, 83-92.
[http://dx.doi.org/10.2147/HP.S93413] [PMID: 27774485]
[30]
Vieites, M.; Noblía, P.; Torre, M.H.; Cerecetto, H.; Laura Lavaggi, M.; Costa-Filho, A.J.; Azqueta, A.; de Cerain, A.L.; Monge, A.; Parajón-Costa, B.; González, M.; Gambino, D. Selective hypoxia-cytotoxins based on vanadyl complexes with 3-aminoquinoxaline-2-carbonitrile-N1,N4-dioxide derivatives. J. Inorg. Biochem., 2006, 100(8), 1358-1367.
[http://dx.doi.org/10.1016/j.jinorgbio.2006.03.012] [PMID: 16698084]
[31]
Lingli, H.; Ning, X.; Harnud, S.; Yuanhu, P.; Dongmei, C.; Yanfei, T.; Zhenli, L.; Zonghui, Y. Metabolic disposition and elimination of cyadox in pigs, chickens, carp, and rats. J. Agric. Food Chem., 2015, 63(22), 5557-5569.
[http://dx.doi.org/10.1021/acs.jafc.5b01745] [PMID: 25973850]
[32]
Yang, Y.; Jiang, L.; She, Y.; Chen, M.; Li, Q.; Yang, G.; Geng, C.; Tang, L.; Zhong, L.; Jiang, L.; Liu, X. Olaquindox induces DNA damage via the lysosomal and mitochondrial pathway involving ROS production and p53 activation in HEK293 cells. Environ. Toxicol. Pharmacol., 2015, 40(3), 792-799.
[http://dx.doi.org/10.1016/j.etap.2015.09.008] [PMID: 26453893]
[33]
Sumedha, N.C.; Miltonprabu, S. Cardiac mitochondrial oxidative stress and dysfunction induced by arsenic and its amelioration by diallyl trisulphide. Toxicol. Res. (Camb.), 2015, 4(2), 291-301.
[http://dx.doi.org/10.1039/C4TX00097H]
[34]
Pedruzzi, L.M.; Stockler-Pinto, M.B.; Leite, M., Jr; Mafra, D. Nrf2-keap1 system versus NF-κB: the good and the evil in chronic kidney disease? Biochimie, 2012, 94(12), 2461-2466.
[http://dx.doi.org/10.1016/j.biochi.2012.07.015] [PMID: 22874821]
[35]
Dai, C.; Tang, S.; Li, D.; Zhao, K.; Xiao, X. Curcumin attenuates quinocetone-induced oxidative stress and genotoxicity in human hepatocyte L02 cells. Toxicol. Mech. Methods, 2015, 25(4), 340-346.
[http://dx.doi.org/10.3109/15376516.2015.1045659] [PMID: 25996037]
[36]
Gu, Z.; Li, Y.; Ma, S.; Li, S.; Zhou, G.; Ding, S.; Zhang, J.; Wang, S.; Zhou, C. Synthesis, cytotoxic evaluation and DNA binding study of 9-fluoro-6H-indolo[2,3-b]quinoxaline derivatives. RSC Advances, 2017, 7(66), 41869-41879.
[http://dx.doi.org/10.1039/C7RA08138C]
[37]
Anderson, R.F.; Yadav, P.; Shinde, S.S.; Hong, C.R.; Pullen, S.M.; Reynisson, J.; Wilson, W.R.; Hay, M.P. Radical Chemistry and cytotoxicity of bioreductive 3-substituted quinoxaline Di-N-oxides. Chem. Res. Toxicol., 2016, 29(8), 1310-1324.
[http://dx.doi.org/10.1021/acs.chemrestox.6b00133] [PMID: 27380897]
[38]
Hajri, M.; Esteve, M-A.; Khoumeri, O.; Abderrahim, R.; Terme, T.; Montana, M.; Vanelle, P. Synthesis and evaluation of in vitro antiproliferative activity of new ethyl 3-(arylethynyl)quinoxaline-2-carboxylate and pyrido[4,3-b]quinoxalin-1(2H)-one derivatives. Eur. J. Med. Chem., 2016, 124, 959-966.
[http://dx.doi.org/10.1016/j.ejmech.2016.10.025] [PMID: 27770736]
[39]
Zou, D-J. Potential benefits of quinoxaline 1, 4-dioxides in aldosterone dysmetabolism disease —A medical hypothesis. Open J. Anim. Sci., 2011, 01(03), 121-127.
[http://dx.doi.org/10.4236/ojas.2011.13016]
[40]
Silva, L.; Coelho, P.; Soares, R.; Prudêncio, C.; Vieira, M. Quinoxaline-1,4-dioxide derivatives inhibitory action in melanoma and brain tumor cells. Future Med. Chem., 2019, 11(7)
[http://dx.doi.org/10.4155/fmc-2018-0251]
[41]
Coelho, P.; Silva, L.; Faria, I.; Vieria, M.; Monteiro, A.; Pinto, G.; Prudêncio, C.; Fernandes, R.; Soares, R. Adipocyte secretome increases radioresistance of malignant melanocytes by improving cell survival and decreasing oxidative status. Radiat. Res., 2017, 187(5), 581-588.
[http://dx.doi.org/10.1667/RR14551.1] [PMID: 28362167]
[42]
Teixeira, D.; Prudêncio, C.; Vieira, M. Development of a new HPLC-based method for 3-nitrotyrosine quantification in different biological matrices. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 2017, 1046, 48-57.
[http://dx.doi.org/10.1016/j.jchromb.2017.01.035] [PMID: 28131027]
[43]
Frustaci, A.; Neri, M.; Cesario, A.; Adams, J.B.; Domenici, E.; Dalla Bernardina, B.; Bonassi, S. Oxidative stress-related biomarkers in autism: systematic review and meta-analyses. Free Radic. Biol. Med., 2012, 52(10), 2128-2141.
[http://dx.doi.org/10.1016/j.freeradbiomed.2012.03.011] [PMID: 22542447]
[44]
Siamak Haghdoost. Biomarkers of Oxidative Stress and Their Application for Assessment of Individual Radiosensitivity; Universitet Stockholms, 2005.
[45]
Pastore, A.; Federici, G.; Bertini, E.; Piemonte, F. Analysis of glutathione: implication in redox and detoxification. Clin. Chim. Acta, 2003, 333(1), 19-39.
[http://dx.doi.org/10.1016/S0009-8981(03)00200-6] [PMID: 12809732]
[46]
Kimura, M.; Rabbani, Z.N.; Zodda, A.R.; Yan, H.; Jackson, I.L.; Polascik, T.J.; Donatucci, C.F.; Moul, J.W.; Vujaskovic, Z.; Koontz, B.F. Role of oxidative stress in a rat model of radiation-induced erectile dysfunction. J. Sex. Med., 2012, 9(6), 1535-1549.
[http://dx.doi.org/10.1111/j.1743-6109.2012.02716.x] [PMID: 22489731]
[47]
Navarro, J.; Obrador, E.; Carretero, J.; Petschen, I.; Aviñó, J.; Perez, P.; Estrela, J.M. Changes in glutathione status and the antioxidant system in blood and in cancer cells associate with tumour growth in vivo. Free Radic. Biol. Med., 1999, 26(3-4), 410-418.
[http://dx.doi.org/10.1016/S0891-5849(98)00213-5] [PMID: 9895233]
[48]
Sharma, P.; Hu-Lieskovan, S.; Wargo, J.A.; Ribas, A. Primary, adaptive, and acquired resistance to cancer immunotherapy. Cell, 2017, 168(4), 707-723.
[http://dx.doi.org/10.1016/j.cell.2017.01.017] [PMID: 28187290]
[49]
Smith, P.S.; Zhao, W.; Spitz, D.R.; Robbins, M.E. Inhibiting catalase activity sensitizes 36B10 rat glioma cells to oxidative stress. Free Radic. Biol. Med., 2007, 42(6), 787-797.
[http://dx.doi.org/10.1016/j.freeradbiomed.2006.11.032] [PMID: 17320761]
[50]
Obenauf, A.C.; Zou, Y.; Ji, A.L.; Vanharanta, S.; Shu, W.; Shi, H.; Kong, X.; Bosenberg, M.C.; Wiesner, T.; Rosen, N.; Lo, R.S.; Massagué, J. Therapy-induced tumour secretomes promote resistance and tumour progression. Nature, 2015, 520(7547), 368-372.
[http://dx.doi.org/10.1038/nature14336] [PMID: 25807485]
[51]
Suntharalingan, N.; Podgorsak, E.B.; Hendry, J.H. Basic radiobiology. Am. J. Clin. Oncol., 1988, 11(3), 220-252.
[52]
Joiner, M.C.; van der Kogel, A. Basic Clinical Radiobiology, 4th ed; Taylor & Francis Group: London, 2009.
[http://dx.doi.org/10.1201/b15450]
[53]
Perry, R.R.; Mazetta, J.A.; Levin, M.; Barranco, S.C. Glutathione levels and variability in breast tumors and normal tissue. Cancer, 1993, 72(3), 783-787.
[http://dx.doi.org/10.1002/1097-0142(19930801)72:3<783:AID-CNCR2820720325>3.0.CO;2-U] [PMID: 8392905]
[54]
Bagchi, M.; Zafra-Stone, S.; Bagchi, D.; Patel, S. Oxidative stress and neurodegeneration. In: Veterinary Toxicology; Elsevier Ltd, 2007; pp. 313-334.
[http://dx.doi.org/10.1016/B978-012370467-2/50117-6]
[55]
Obrador, E.; Carretero, J.; Ortega, A.; Medina, I.; Rodilla, V.; Pellicer, J.A.; Estrela, J.M. γ-Glutamyl transpeptidase overexpression increases metastatic growth of B16 melanoma cells in the mouse liver. Hepatology, 2002, 35(1), 74-81.
[http://dx.doi.org/10.1053/jhep.2002.30277] [PMID: 11786961]
[56]
Hanot, M.; Boivin, A.; Malésys, C.; Beuve, M.; Colliaux, A.; Foray, N.; Douki, T.; Ardail, D.; Rodriguez-Lafrasse, C. Glutathione depletion and carbon ion radiation potentiate clustered DNA lesions, cell death and prevent chromosomal changes in cancer cells progeny. PLoS One, 2012, 7(11)e44367
[http://dx.doi.org/10.1371/journal.pone.0044367] [PMID: 23185232]
[57]
Jayaraman, S.; Jasuja, R.; Zakharov, M.N.; Gursky, O.; States, U.; States, U. Pressure perturbation calorimetry of lipoproteins reveals an endothermic transition without detectable volume changes. Implications for adsorption of apolipoprotein to a phospholipid surface. Biochemistry, 2011, 50(19), 3919-3927.
[http://dx.doi.org/10.1021/bi200090y] [PMID: 21452855]
[58]
Benathan, M.; Alvero-Jackson, H.; Mooy, A.M.; Scaletta, C.; Frenk, E. Relationship between melanogenesis, glutathione levels and melphalan toxicity in human melanoma cells. Melanoma Res., 1992, 2(5-6), 305-314.
[http://dx.doi.org/10.1097/00008390-199212000-00003] [PMID: 1337997]
[59]
Meyskens, F.L., Jr; Farmer, P.; Fruehauf, J.P. Redox regulation in human melanocytes and melanoma. Pigment Cell Res., 2001, 14(3), 148-154.
[http://dx.doi.org/10.1034/j.1600-0749.2001.140303.x] [PMID: 11434561]
[60]
Navarro, J.; Obrador, E.; Pellicer, J.A.; Aseni, M.; Viña, J.; Estrela, J.M. Blood glutathione as an index of radiation-induced oxidative stress in mice and humans. Free Radic. Biol. Med., 1997, 22(7), 1203-1209.
[http://dx.doi.org/10.1016/S0891-5849(96)00554-0] [PMID: 9098094]
[61]
Ramli, Y.; Moussaif, A.; Karrouchi, K.; Essassi, E.M. Pharmacological profile of quinoxalinone. J. Chem., 2014, 1-21.
[http://dx.doi.org/10.1155/2014/563406]
[62]
Mielcke, T.R.; Mascarello, A.; Filippi-Chiela, E.; Zanin, R.F.; Lenz, G.; Leal, P.C.; Chiaradia, L.D.; Yunes, R.A.; Nunes, R.J.; Battastini, A.M.O.; Morrone, F.B.; Campos, M.M. Activity of novel quinoxaline-derived chalcones on in vitro glioma cell proliferation. Eur. J. Med. Chem., 2012, 48, 255-264.
[http://dx.doi.org/10.1016/j.ejmech.2011.12.023] [PMID: 22209415]
[63]
Zhang, M.; Dai, Z.C.; Qian, S.S.; Liu, J.Y.; Xiao, Y.; Lu, A.M.; Zhu, H.L.; Wang, J.X.; Ye, Y.H. Design, synthesis, antifungal, and antioxidant activities of (E)-6-((2-phenylhydrazono)methyl)quinoxaline derivatives. J. Agric. Food Chem., 2014, 62(40), 9637-9643.
[http://dx.doi.org/10.1021/jf504359p] [PMID: 25229541]
[64]
Moarbess, G.; Deleuze-Masquefa, C.; Bonnard, V.; Gayraud-Paniagua, S.; Vidal, J.R.; Bressolle, F.; Pinguet, F.; Bonnet, P.A. In vitro and in vivo anti-tumoral activities of imidazo[1,2-a]quinoxaline, imidazo[1,5-a]quinoxaline, and pyrazolo[1,5-a]quinoxaline derivatives. Bioorg. Med. Chem., 2008, 16(13), 6601-6610.
[http://dx.doi.org/10.1016/j.bmc.2008.05.022] [PMID: 18513976]
[65]
Abbas, H-A.S.; Al-Marhabi, A.R.; Eissa, S.I.; Ammar, Y.A. Molecular modeling studies and synthesis of novel quinoxaline derivatives with potential anticancer activity as inhibitors of c-Met kinase. Bioorg. Med. Chem., 2015, 23(20), 6560-6572.
[http://dx.doi.org/10.1016/j.bmc.2015.09.023] [PMID: 26420384]
[66]
Urosevic-Maiwald, M.; Barysch, M.J.; Cheng, P.F.; Karpova, M.B.; Steinert, H.; Okoniewski, M.J.; Dummer, R. In vivo profiling reveals immunomodulatory effects of sorafenib and dacarbazine on melanoma. OncoImmunology, 2015, 4(2)e988458
[http://dx.doi.org/10.4161/2162402X.2014.988458] [PMID: 25949886]
[67]
Husain, A.; Madhesia, D. Recent advances in pharmacological activities of quinoxaline derivatives. J. Pharm. Res., 2011, 4(3), 924-929.
[68]
Song, Y.S.; Narasimhan, P.; Kim, G.S.; Jung, J.E.; Park, E.H.; Chan, P.H. The role of Akt signaling in oxidative stress mediates NF-kappaB activation in mild transient focal cerebral ischemia. J. Cereb. Blood Flow Metab., 2008, 28(12), 1917-1926.
[http://dx.doi.org/10.1038/jcbfm.2008.80] [PMID: 18628779]
[69]
Lingappan, K. NF-κB in oxidative stress. Curr. Opin. Toxicol., 2018, 7, 81-86.
[http://dx.doi.org/10.1016/j.cotox.2017.11.002] [PMID: 29862377]
[70]
Kim, J-H.; Choi, T.G.; Park, S.; Yun, H.R.; Nguyen, N.N.Y.; Jo, Y.H.; Jang, M.; Kim, J.; Kim, J.; Kang, I.; Ha, J.; Murphy, M.P.; Tang, D.G.; Kim, S.S. Mitochondrial ROS-derived PTEN oxidation activates PI3K pathway for mTOR-induced myogenic autophagy. Cell Death Differ., 2018, 25(11), 1921-1937.
[http://dx.doi.org/10.1038/s41418-018-0165-9] [PMID: 30042494]
[71]
Deleuze-Masquefa, C.; Moarbess, G.; Khier, S.; David, N.; Gayraud-Paniagua, S.; Bressolle, F.; Pinguet, F.; Bonnet, P-A. New imidazo[1,2-a]quinoxaline derivatives: synthesis and in vitro activity against human melanoma. Eur. J. Med. Chem., 2009, 44(9), 3406-3411.
[http://dx.doi.org/10.1016/j.ejmech.2009.02.007] [PMID: 19278757]
[72]
Tseng, C-H.; Chen, Y-R.; Tzeng, C-C.; Liu, W.; Chou, C-K.; Chiu, C-C.; Chen, Y-L. Discovery of indeno[1,2-b]quinoxaline derivatives as potential anticancer agents. Eur. J. Med. Chem., 2016, 108, 258-273.
[http://dx.doi.org/10.1016/j.ejmech.2015.11.031] [PMID: 26686931]

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