Synergistic Activity of Ketoconazole and Miconazole with Prochloraz in Inducing Oxidative Stress, GSH Depletion, Mitochondrial Dysfunction, and Apoptosis in Mouse Sertoli TM4 Cells
Triazole and imidazole fungicides represent an emerging class of pollutants with endocrine-disrupting properties. Concerning mammalian reproduction, a possible causative role of antifungal compounds in inducing toxicity has been reported, although currently, there is little evidence about potential...
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Published in | International journal of molecular sciences Vol. 23; no. 10; p. 5429 |
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Format | Journal Article |
Language | English |
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Abstract | Triazole and imidazole fungicides represent an emerging class of pollutants with endocrine-disrupting properties. Concerning mammalian reproduction, a possible causative role of antifungal compounds in inducing toxicity has been reported, although currently, there is little evidence about potential cooperative toxic effects. Toxicant-induced oxidative stress (OS) may be an important mechanism potentially involved in male reproductive dysfunction. Thus, to clarify the molecular mechanism underlying the effects of azoles on male reproduction, the individual and combined potential of fluconazole (FCZ), prochloraz (PCZ), miconazole (MCZ), and ketoconazole (KCZ) in triggering in vitro toxicity, redox status alterations, and OS in mouse TM4 Sertoli cells (SCs) was investigated. In the present study, we demonstrate that KCZ and MCZ, alone or in synergistic combination with PCZ, strongly impair SC functions, and this event is, at least in part, ascribed to OS. In particular, azoles-induced cytotoxicity is associated with growth inhibitory effects, G0/G1 cell cycle arrest, mitochondrial dysfunction, reactive oxygen species (ROS) generation, imbalance of the superoxide dismutase (SOD) specific activity, glutathione (GSH) depletion, and apoptosis. N-acetylcysteine (NAC) inhibits ROS accumulation and rescues SCs from azole-induced apoptosis. PCZ alone exhibits only cytostatic and pro-oxidant properties, while FCZ, either individually or in combination, shows no cytotoxic effects up to 320 µM. |
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AbstractList | Triazole and imidazole fungicides represent an emerging class of pollutants with endocrine-disrupting properties. Concerning mammalian reproduction, a possible causative role of antifungal compounds in inducing toxicity has been reported, although currently, there is little evidence about potential cooperative toxic effects. Toxicant-induced oxidative stress (OS) may be an important mechanism potentially involved in male reproductive dysfunction. Thus, to clarify the molecular mechanism underlying the effects of azoles on male reproduction, the individual and combined potential of fluconazole (FCZ), prochloraz (PCZ), miconazole (MCZ), and ketoconazole (KCZ) in triggering in vitro toxicity, redox status alterations, and OS in mouse TM4 Sertoli cells (SCs) was investigated. In the present study, we demonstrate that KCZ and MCZ, alone or in synergistic combination with PCZ, strongly impair SC functions, and this event is, at least in part, ascribed to OS. In particular, azoles-induced cytotoxicity is associated with growth inhibitory effects, G0/G1 cell cycle arrest, mitochondrial dysfunction, reactive oxygen species (ROS) generation, imbalance of the superoxide dismutase (SOD) specific activity, glutathione (GSH) depletion, and apoptosis. N-acetylcysteine (NAC) inhibits ROS accumulation and rescues SCs from azole-induced apoptosis. PCZ alone exhibits only cytostatic and pro-oxidant properties, while FCZ, either individually or in combination, shows no cytotoxic effects up to 320 µM. |
Author | Iorio, Roberto Celenza, Giuseppe Luzi, Carla Cinque, Benedetta Festuccia, Claudio Franceschini, Nicola Petricca, Sabrina Lizzi, Anna Rita |
AuthorAffiliation | 2 Department of Life, Health and Environmental Sciences, University of L’Aquila, Via Vetoio, 67100 L’Aquila, Italy; benedetta.cinque@univaq.it 1 Department of Biotechnological and Applied Clinical Sciences, University of L’Aquila, Via Vetoio, 67100 L’Aquila, Italy; sabrina.petricca@univaq.it (S.P.); giuseppe.celenza@univaq.it (G.C.); carla.luzi@univaq.it (C.L.); annarita.lizzi@univaq.it (A.R.L.); nicola.franceschini@univaq.it (N.F.); claudio.festuccia@univaq.it (C.F.) |
AuthorAffiliation_xml | – name: 1 Department of Biotechnological and Applied Clinical Sciences, University of L’Aquila, Via Vetoio, 67100 L’Aquila, Italy; sabrina.petricca@univaq.it (S.P.); giuseppe.celenza@univaq.it (G.C.); carla.luzi@univaq.it (C.L.); annarita.lizzi@univaq.it (A.R.L.); nicola.franceschini@univaq.it (N.F.); claudio.festuccia@univaq.it (C.F.) – name: 2 Department of Life, Health and Environmental Sciences, University of L’Aquila, Via Vetoio, 67100 L’Aquila, Italy; benedetta.cinque@univaq.it |
Author_xml | – sequence: 1 givenname: Sabrina orcidid: 0000-0002-9794-3632 surname: Petricca fullname: Petricca, Sabrina organization: Department of Biotechnological and Applied Clinical Sciences, University of L'Aquila, Via Vetoio, 67100 L'Aquila, Italy – sequence: 2 givenname: Giuseppe orcidid: 0000-0003-2796-9228 surname: Celenza fullname: Celenza, Giuseppe organization: Department of Biotechnological and Applied Clinical Sciences, University of L'Aquila, Via Vetoio, 67100 L'Aquila, Italy – sequence: 3 givenname: Carla surname: Luzi fullname: Luzi, Carla organization: Department of Biotechnological and Applied Clinical Sciences, University of L'Aquila, Via Vetoio, 67100 L'Aquila, Italy – sequence: 4 givenname: Benedetta surname: Cinque fullname: Cinque, Benedetta organization: Department of Life, Health and Environmental Sciences, University of L'Aquila, Via Vetoio, 67100 L'Aquila, Italy – sequence: 5 givenname: Anna Rita surname: Lizzi fullname: Lizzi, Anna Rita organization: Department of Biotechnological and Applied Clinical Sciences, University of L'Aquila, Via Vetoio, 67100 L'Aquila, Italy – sequence: 6 givenname: Nicola surname: Franceschini fullname: Franceschini, Nicola organization: Department of Biotechnological and Applied Clinical Sciences, University of L'Aquila, Via Vetoio, 67100 L'Aquila, Italy – sequence: 7 givenname: Claudio orcidid: 0000-0002-3463-6475 surname: Festuccia fullname: Festuccia, Claudio organization: Department of Biotechnological and Applied Clinical Sciences, University of L'Aquila, Via Vetoio, 67100 L'Aquila, Italy – sequence: 8 givenname: Roberto orcidid: 0000-0003-1863-5752 surname: Iorio fullname: Iorio, Roberto organization: Department of Biotechnological and Applied Clinical Sciences, University of L'Aquila, Via Vetoio, 67100 L'Aquila, Italy |
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Keywords | ROS generation and apoptosis fluconazole prochloraz GSH homeostasis mouse Sertoli TM4 cells synergistic effects miconazole and ketoconazole enzymatic activity SOD oxidative stress mitochondrial activity |
Language | English |
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SubjectTerms | Acetylcysteine Antifungal agents Antioxidants Apoptosis Azoles Cell cycle Cooperation Cytotoxicity Depletion DNA damage Drugs Endocrine disruptors Enzymes Fertility Fluconazole Fungicides Heterocyclic compounds Imidazole Infertility Ketoconazole Lipid peroxidation Males Miconazole miconazole and ketoconazole Mitochondria mouse Sertoli TM4 cells Oxidants Oxidative stress Oxidizing agents Pesticides Pollutants Prochloraz Proteins Sertoli cells Sperm Spermatogenesis Steroids Superoxide dismutase synergistic effects Toxicants Toxicity |
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Title | Synergistic Activity of Ketoconazole and Miconazole with Prochloraz in Inducing Oxidative Stress, GSH Depletion, Mitochondrial Dysfunction, and Apoptosis in Mouse Sertoli TM4 Cells |
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