Searching for alternative toxicology testing systems: The response of isolated mitochondria from Saccharomyces cerevisiae, potato tuber, and mouse liver to a toxic insult

Document Type : Original Article

Authors

1 Pharmaceutical Sciences Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

2 College of Life Sciences, Shanxi Agricultural University, Taigu, Shanxi 030801, China

3 Department of Pharmacology and Toxicology, School of Pharmacy, Shiraz University of Medical Sciences, Shiraz, Iran.

4 Department of quality control, Faculty of pharmacy, Shiraz University of Medical Sciences, Shiraz, Iran

5 Department of Pharmaceutical Biotechnology, School of Pharmacy, Shiraz University of Medical Sciences, Shiraz, Iran.

6 Shiraz University of Medical Sciences, Pharmaceutical Sciences Research Center

Abstract

Mitochondria are cellular power plants known as essential organelles for energy (ATP) metabolism. However, today it is evident that various vital compounds are partially or exclusively synthesized in mitochondria. Moreover, this organelle plays a pivotal role in essential processes such as cell death. The isolated mitochondrion is an excellent experimental model for evaluating the role of mitochondria in the pathogenesis of diseases. Various in vitro and in vivo experimental models have been developed to study mitochondria. On the other hand, some alternative models could also help decrease the use of animal models. In the current study, we compared the response of mitochondria isolated from mouse liver, saccharomyces cerevisiae (S.c), and potato tuber to various concentrations of calcium (Ca2+) as a robust mitochondrial disturbing agent. The current study found that significant mitochondrial depolarization, decreased ATP levels, mitochondrial permeabilization, and decreased mitochondrial dehydrogenases activity were found in all isolated mitochondrial preparations. No significant difference between mouse liver, S.c, and potato tuber mitochondria were detected in experiments carried out in the current investigation. We are aware that mitochondria from different species have a huge structural and enzymatic variance. Hence, these models could just estimate the effect of xenobiotics in biological systems. However, the data derived from this study could finally help to decrease the use of experimental animals and provide new approaches for evaluating mitochondrial function.

Keywords

References

1. Osellame LD, Blacker TS, Duchen MR. Cellular and molecular mechanisms of mitochondrial function. Best Pract Res Clin Endocrinol Metab. 2012 Dec;26(6):711-23. doi: 10.1016/j.beem.2012.05.003. Epub 2012 Jun 23. PMID: 23168274; PMCID: PMC3513836.
2. Duchen MR, Szabadkai G. Roles of mitochondria in human disease. Essays Biochem. 2010;47:115-37. doi: 10.1042/bse0470115. PMID: 20533904.
3. Majd H, King MS, Smith AC, Kunji ERS. Pathogenic mutations of the human mitochondrial citrate carrier SLC25A1 lead to impaired citrate export required for lipid, dolichol, ubiquinone and sterol synthesis. Biochim Biophys Acta Bioenerg. 2018 Jan;1859(1):1-7. doi: 10.1016/j.bbabio.2017.10.002. Epub 2017 Oct 12. PMID: 29031613.
4. Edvardson S, Porcelli V, Jalas C, Soiferman D, Kellner Y, Shaag A, et al. Agenesis of corpus callosum and optic nerve hypoplasia due to mutations in SLC25A1 encoding the mitochondrial citrate transporter. J Med Genet. 2013 Apr;50(4):240-5. doi: 10.1136/jmedgenet-2012-101485. Epub 2013 Feb 7. PMID: 23393310.
5. Zaki HF, Salem HA, El-Yamany MF. Taurine: A promising agent of therapeutic potential in experimentally-induced arthritis. Egypt Rheumatol. 2011;33;131-7. doi: 10.1016/j.ejr.2011.05.002.
6. Swenson SA, Moore CM, Marcero JR, Medlock AE, Reddi AR, Khalimonchuk O. From Synthesis to Utilization: The Ins and Outs of Mitochondrial Heme. Cells. 2020;9(3):579. Published 2020 Feb 29. doi:10.3390/cells9030579
7. Javadov S, Kozlov AV, Camara AKS. Mitochondria in Health and Diseases. Cells. 2020;9(5):1177. Published 2020 May 9. doi:10.3390/cells9051177
8. Heidari R. Brain mitochondria as potential therapeutic targets for managing hepatic encephalopathy. Life Sci. 2019 Feb 1;218:65-80. doi: 10.1016/j.lfs.2018.12.030. Epub 2018 Dec 19. PMID: 30578865.
9. Heidari R, Ghanbarinejad V, Ommati MM, Jamshidzadeh A, Niknahad H. Mitochondria protecting amino acids: Application against a wide range of mitochondria-linked complications. PharmaNutrition. 2018;6;180-90. doi: 10.1016/j.phanu.2018.09.001.
10. Heidari R, Niknahad H, Jamshidzadeh A, Eghbal MA, Abdoli N. An overview on the proposed mechanisms of antithyroid drugs-induced liver injury. Adv Pharm Bull. 2015;5(1):1-11. doi:10.5681/apb.2015.001
11. Heidari R, Babaei H, Eghbal MA. Cytoprotective effects of taurine against toxicity induced by isoniazid and hydrazine in isolated rat hepatocytes. Arh Hig Rada Toksikol. 2013 Jun;64(2):15-24. doi: 10.2478/10004-1254-64-2013-2297. PMID: 23819928.
12. Heidari R, Niknahad H, Jamshidzadeh A, Abdoli N. Factors affecting drug-induced liver injury: antithyroid drugs as instances. Clin Mol Hepatol. 2014 Sep;20(3):237-48. doi: 10.3350/cmh.2014.20.3.237. Epub 2014 Sep 25. PMID: 25320726; PMCID: PMC4197171.
13. Heidari R, Taheri V, Rahimi HR, Shirazi Yeganeh B, Niknahad H, Najibi A. Sulfasalazine-induced renal injury in rats and the protective role of thiol-reductants. Ren Fail. 2016;38(1):137-41. doi: 10.3109/0886022X.2015.1096731. Epub 2015 Oct 19. PMID: 26479898.
14. Ommati MM, Mobasheri A, Heidari R. Drug-induced organ injury in coronavirus disease 2019 pharmacotherapy: Mechanisms and challenges in differential diagnosis and potential protective strategies. J Biochem Mol Toxicol. 2021;35;e22795. doi: 10.1002/jbt.22795.
15. Ahmadi N, Ghanbarinejad V, Ommati MM, Jamshidzadeh A, Heidari R. Taurine prevents mitochondrial membrane permeabilization and swelling upon interaction with manganese: Implication in the treatment of cirrhosis-associated central nervous system complications. J Biochem Mol Toxicol. 2018 Nov;32(11):e22216. doi: 10.1002/jbt.22216. Epub 2018 Aug 28. PMID: 30152904.
16. Emadi E, Abdoli N, Ghanbarinejad V, Mohammadi HR, Mousavi Mobarakeh K, et al. The potential role of mitochondrial impairment in the pathogenesis of imatinib-induced renal injury. Heliyon. 2019 Jun 22;5(6):e01996. doi: 10.1016/j.heliyon.2019.e01996. PMID: 31294126; PMCID: PMC6595238.
17. Heidari R. The footprints of mitochondrial impairment and cellular energy crisis in the pathogenesis of xenobiotics-induced nephrotoxicity, serum electrolytes imbalance, and Fanconi's syndrome: A comprehensive review. Toxicology. 2019 Jul 1;423:1-31. doi: 10.1016/j.tox.2019.05.002. Epub 2019 May 13. PMID: 31095988.
18. Heidari R, Babaei H, Eghbal MA. Amodiaquine-induced toxicity in isolated rat hepatocytes and the cytoprotective effects of taurine and/or N-acetyl cysteine. Res Pharm Sci. 2014 Mar-Apr;9(2):97-105. PMID: 25657778; PMCID: PMC4311296.
19. Heidari R, Jamshidzadeh A, Ommati MM, Rashidi E, Khodaei F, Sadeghi A, et al. Ammonia-induced mitochondrial impairment is intensified by manganese co-exposure: relevance to the management of subclinical hepatic encephalopathy and cirrhosis-associated brain injury. Clin Exp Hepatol. 2019 May;5(2):109-117. doi: 10.5114/ceh.2019.85071. Epub 2019 May 13. PMID: 31501786; PMCID: PMC6728860.
20. Heidari R, Niknahad H. The role and study of mitochondrial impairment and oxidative stress in cholestasis. In: Vinken M, editor. Experimental Cholestasis Research. Methods in Molecular Biology. New York, NY: Springer New York; 2019. p. 117-32. doi: https://doi.org/10.1007/978-1-4939-9420-5_8
21. Heidari R, Niknahad H, Sadeghi A, Mohammadi H, Ghanbarinejad V, Ommati MM, et al. Betaine treatment protects liver through regulating mitochondrial function and counteracting oxidative stress in acute and chronic animal models of hepatic injury. Biomed Pharmacother. 2018 Jul;103:75-86. doi: 10.1016/j.biopha.2018.04.010. Epub 2018 Apr 7. PMID: 29635131.
22. Niknahad H, Heidari R, Mohammadzadeh R, Ommati MM, Khodaei F, Azarpira N, et al. Sulfasalazine induces mitochondrial dysfunction and renal injury. Ren Fail. 2017 Nov;39(1):745-753. doi: 10.1080/0886022X.2017.1399908. PMID: 29214868; PMCID: PMC6446160.
23. Ommati MM, Heidari R, Ghanbarinejad V, Abdoli N, Niknahad H. Taurine Treatment Provides Neuroprotection in a Mouse Model of Manganism. Biol Trace Elem Res. 2019 Aug;190(2):384-395. doi: 10.1007/s12011-018-1552-2. Epub 2018 Oct 24. PMID: 30357569.
24. Ommati MM, Jamshidzadeh A, Heidari R, Sun Z, Zamiri MJ, Khodaei F, et al. Carnosine and Histidine Supplementation Blunt Lead-Induced Reproductive Toxicity through Antioxidative and Mitochondria-Dependent Mechanisms. Biol Trace Elem Res. 2019 Jan;187(1):151-162. doi: 10.1007/s12011-018-1358-2. Epub 2018 May 16. PMID: 29767280.
25. Ommati MM, Manthari RK, Tikka C, Niu R, Sun Z, Sabouri S, et al. Arsenic-induced autophagic alterations and mitochondrial impairments in HPG-S axis of mature male mice offspring (F1-generation): A persistent toxicity study. Toxicol Lett. 2020 Jun 15;326:83-98. doi: 10.1016/j.toxlet.2020.02.013. Epub 2020 Feb 26. PMID: 32112876.
26. Vazin A, Heidari R, Khodami Z. Curcumin Supplementation Alleviates Polymyxin E-Induced Nephrotoxicity. J Exp Pharmacol. 2020;12:129-136. Published 2020 Jun 4. doi:10.2147/JEP.S255861
27. Abdoli N, Heidari R, Azarmi Y, Eghbal MA. Mechanisms of the statins cytotoxicity in freshly isolated rat hepatocytes. J Biochem Mol Toxicol. 2013 Jun;27(6):287-94. doi: 10.1002/jbt.21485. Epub 2013 Apr 23. PMID: 23761184.
28. Heidari R, Babaei H, Eghbal M. Mechanisms of methimazole cytotoxicity in isolated rat hepatocytes. Drug Chem Toxicol. 2013 Oct;36(4):403-11. doi: 10.3109/01480545.2012.749272. Epub 2012 Dec 21. PMID: 23256569.
29. Heidari R, Moezi L, Asadi B, Ommati MM, Azarpira N. Hepatoprotective effect of boldine in a bile duct ligated rat model of cholestasis/cirrhosis. PharmaNutrition. 2017;5;109-17. doi: 10.1016/j.phanu.2017.07.001.
30. Jamshidzadeh A, Heidari R, Mohammadi-Samani S, Azarpira N, Najbi A, Jahani P, et al. A comparison between the nephrotoxic profile of gentamicin and gentamicin nanoparticles in mice. J Biochem Mol Toxicol. 2015 Feb;29(2):57-62. doi: 10.1002/jbt.21667. Epub 2014 Oct 8. PMID: 25293820.
31. Heidari R, Jamshidzadeh A, Niknahad H, Safari F, Azizi H, Abdoli N, et al. The hepatoprotection provided by taurine and glycine against antineoplastic drugs induced liver injury in an ex vivo model of normothermic recirculating isolated perfused rat liver. Trend Pharm Sci. 2016;2;59-76. doi.
32. Niknahad H, Jamshidzadeh A, Heidari R, Zarei M, Ommati MM. Ammonia-induced mitochondrial dysfunction and energy metabolism disturbances in isolated brain and liver mitochondria, and the effect of taurine administration: relevance to hepatic encephalopathy treatment. Clin Exp Hepatol. 2017;3(3):141-151. doi:10.5114/ceh.2017.68833
33. Jamshidzadeh A, Niknahad H, Heidari R, Zarei M, Ommati MM, Khodaei F. Carnosine protects brain mitochondria under hyperammonemic conditions: Relevance to hepatic encephalopathy treatment. PharmaNutrition. 2017;5;58-63. doi: 10.1016/j.phanu.2017.02.004.
34. Ommati MM, Heidari R, Manthari RK, Tikka Chiranjeevi S, Niu R, Sun Z, et al. Paternal exposure to arsenic resulted in oxidative stress, autophagy, and mitochondrial impairments in the HPG axis of pubertal male offspring. Chemosphere. 2019 Dec;236:124325. doi: 10.1016/j.chemosphere.2019.07.056. Epub 2019 Jul 15. PMID: 31326754.
35. Ommati MM, Heidari R, Zamiri MJ, Sabouri S, Zaker L, Farshad O, et al. The Footprints of Oxidative Stress and Mitochondrial Impairment in Arsenic Trioxide-Induced Testosterone Release Suppression in Pubertal and Mature F1-Male Balb/c Mice via the Downregulation of 3β-HSD, 17β-HSD, and CYP11a Expression. Biol Trace Elem Res. 2020 May;195(1):125-134. doi: 10.1007/s12011-019-01815-2. Epub 2019 Jul 16. PMID: 31313246.
36. Ommati MM, Shi X, Li H, Zamiri MJ, Farshad O, Jamshidzadeh A, et al. The mechanisms of arsenic-induced ovotoxicity, ultrastructural alterations, and autophagic related paths: An enduring developmental study in folliculogenesis of mice. Ecotoxicol Environ Saf. 2020 Nov;204:110973. doi: 10.1016/j.ecoenv.2020.110973. Epub 2020 Aug 8. PMID: 32781346.
37. Ommati MM, Niknahad H, Farshad O, Azarpira N, Heidari R. In Vitro and In Vivo Evidence on the Role of Mitochondrial Impairment as a Mechanism of Lithium-Induced Nephrotoxicity. Biol Trace Elem Res. 2021 May;199(5):1908-1918. doi: 10.1007/s12011-020-02302-9. Epub 2020 Jul 25. Erratum in: Biol Trace Elem Res. 2021 Jun;199(6):2429. PMID: 32712907.
38. Ommati MM, Farshad O, Azarpira N, Ghazanfari E, Niknahad H, Heidari R. Silymarin mitigates bile duct obstruction-induced cholemic nephropathy. Naunyn Schmiedebergs Arch Pharmacol. 2021 Jun;394(6):1301-1314. doi: 10.1007/s00210-020-02040-8. Epub 2021 Feb 4. PMID: 33538845.
39. Ghanbarinejad V, Jamshidzadeh A, Khalvati B, Farshad O, Li H, Shi X, et al. Apoptosis-inducing factor plays a role in the pathogenesis of hepatic and renal injury during cholestasis. Naunyn Schmiedebergs Arch Pharmacol. 2021 Jun;394(6):1191-1203. doi: 10.1007/s00210-020-02041-7. Epub 2021 Feb 1. PMID: 33527194.
40. Caro AA, Adlong LW, Crocker SJ, Gardner MW, Luikart EF, Gron LU. Effect of garlic-derived organosulfur compounds on mitochondrial function and integrity in isolated mouse liver mitochondria. Toxicol Lett. 2012 Oct 17;214(2):166-74. doi: 10.1016/j.toxlet.2012.08.017. Epub 2012 Aug 29. PMID: 22960305; PMCID: PMC3535879.
41. Ommati MM, Arabnezhad MR, Farshad O, Jamshidzadeh A, Niknahad H, Retana-Marquez S, et al. The Role of Mitochondrial Impairment and Oxidative Stress in the Pathogenesis of Lithium-Induced Reproductive Toxicity in Male Mice. Front Vet Sci. 2021 Mar 24;8:603262. doi: 10.3389/fvets.2021.603262. PMID: 33842567; PMCID: PMC8025583.
42. Ommati MM, Farshad O, Azarpira N, Shafaghat M, Niknahad H, Heidari R. Betaine alleviates cholestasis-associated renal injury by mitigating oxidative stress and enhancing mitochondrial function. Biologia. 2021;76;351-65. doi: 10.2478/s11756-020-00576-x.
43. Heidari R, Ghanbarinejad V, Mohammadi H, Ahmadi A, Esfandiari A, Azarpira N, et al. Dithiothreitol supplementation mitigates hepatic and renal injury in bile duct ligated mice: Potential application in the treatment of cholestasis-associated complications. Biomed Pharmacother. 2018 Mar;99:1022-1032. doi: 10.1016/j.biopha.2018.01.018. Epub 2018 Jan 5. PMID: 29307496.
44. Heidari R, Ahmadi A, Mohammadi H, Ommati MM, Azarpira N, Niknahad H. Mitochondrial dysfunction and oxidative stress are involved in the mechanism of methotrexate-induced renal injury and electrolytes imbalance. Biomed Pharmacother. 2018 Nov;107:834-840. doi: 10.1016/j.biopha.2018.08.050. Epub 2018 Aug 22. PMID: 30142545.
45. Heidari R, Ghanbarinejad V, Ommati MM, Jamshidzadeh A, Niknahad H. Regulation of mitochondrial function and energy metabolism: A primary mechanism of cytoprotection provided by carnosine. Trend Pharm Sci. 2018;4:41-50.
46. Iravanpour F, Dargahi L, Rezaei M, Haghani M, Heidari R, Valian N, et al. Intranasal insulin improves mitochondrial function and attenuates motor deficits in a rat 6-OHDA model of Parkinson's disease. CNS Neurosci Ther. 2021 Mar;27(3):308-319. doi: 10.1111/cns.13609. Epub 2021 Jan 26. PMID: 33497031; PMCID: PMC7871791.
47. Abdoli N, Sadeghian I, Azarpira N, Ommati MM, Heidari R. Taurine mitigates bile duct obstruction-associated cholemic nephropathy: effect on oxidative stress and mitochondrial parameters. Clin Exp Hepatol. 2021;7;30-40. doi: 10.5114/ceh.2021.104675.
48. Abdoli N, Sadeghian I, Mousavi K, Azarpira N, Ommati MM, Heidari R. Suppression of cirrhosis-related renal injury by N-acetyl cysteine. Curr Res Pharmacol Drug Disc. 2020;1;30-8. doi: 10.1016/j.crphar.2020.100006.
49. Heidari R, Behnamrad S, Khodami Z, Ommati MM, Azarpira N, Vazin A. The nephroprotective properties of taurine in colistin-treated mice is mediated through the regulation of mitochondrial function and mitigation of oxidative stress. Biomed Pharmacother. 2019 Jan;109:103-111. doi: 10.1016/j.biopha.2018.10.093. Epub 2018 Nov 2. PMID: 30396066.
50. Heidari R, Jafari F, Khodaei F, Shirazi Yeganeh B, Niknahad H. Mechanism of valproic acid-induced Fanconi syndrome involves mitochondrial dysfunction and oxidative stress in rat kidney. Nephrology (Carlton). 2018 Apr;23(4):351-361. doi: 10.1111/nep.13012. PMID: 28141910.
51. Hossein N, Akram J, Reza H, Narges A, Mohammad Mehdi O, Faezeh J, et al. The postulated hepatotoxic metabolite of methimazole causes mitochondrial dysfunction and energy metabolism disturbances in liver. Pharm Sci. 2016;22;217-26. doi: 10.15171/PS.2016.35.
52. Jamshidzadeh A, Heidari R, Abasvali M, Zarei M, Ommati MM, Abdoli N, et al. Taurine treatment preserves brain and liver mitochondrial function in a rat model of fulminant hepatic failure and hyperammonemia. Biomed Pharmacother. 2017 Feb;86:514-520. doi: 10.1016/j.biopha.2016.11.095. Epub 2016 Dec 23. PMID: 28024286.
53. Ommati MM, Farshad O, Ghanbarinejad V, Mohammadi HR, Khadijeh M, Negar A, et al. The Nephroprotective Role of Carnosine Against Ifosfamide-Induced Renal Injury and Electrolytes Imbalance is Mediated Via the Regulation of Mitochondrial Function and Alleviation of Oxidative Stress. Drug Res (Stuttg). 2020 Jan;70(1):49-56. doi: 10.1055/a-1017-5085. Epub 2019 Oct 31. PMID: 31671464.
54. Ommati MM, Farshad O, Jamshidzadeh A, Heidari R. Taurine enhances skeletal muscle mitochondrial function in a rat model of resistance training. PharmaNutrition. 2019;9;100161. doi: 10.1016/j.phanu.2019.100161.
55. Ommati MM, Heidari R, Ghanbarinejad V, Aminian A, Abdoli N, Niknahad H. The neuroprotective properties of carnosine in a mouse model of manganism is mediated via mitochondria regulating and antioxidative mechanisms. Nutr Neurosci. 2020;23;731-43. doi: 10.1080/1028415X.2018.1552399.
56. Ommati MM, Mohammadi H, Mousavi K, Azarpira N, Farshad O, Dehghani R, et al. Metformin alleviates cholestasis-associated nephropathy through regulating oxidative stress and mitochondrial function. Liver Res. 2020;In-Press. doi: 10.1016/j.livres.2020.12.001.
57. Mohammadi H, Ommati MM, Farshad O, Jamshidzadeh A, Nikbakht MR, Niknahad H, Heidari R. Taurine and isolated mitochondria: A concentration-response study. Trend Pharm Sci. 2019;5;197-206. doi: 10.30476/tips.2020.84851.1037.
58. Meisinger C, Pfanner N, Truscott KN. Isolation of yeast mitochondria. Methods Mol Biol. 2006;313:33-9. doi: 10.1385/1-59259-958-3:033. PMID: 16118422.
59. Havelund JF, Salvato F, Chen M, Rao RSP, Rogowska-Wrzesinska A, Jensen ON, et al. Isolation of Mitochondria from Potato Tubers. Bio-Protocol. 2014;4;e1226-e. doi: 10.21769/BioProtoc.1226.
60. Niknahad H, Heidari R, Alzuhairi AM, Najibi A. Mitochondrial dysfunction as a mechanism for pioglitazone-induced injury toward HepG2 cell. Pharm Sci. 2015;20;169-74.
61. Ommati MM, Heidari R, Jamshidzadeh A, Zamiri MJ, Sun Z, Sabouri S, et al. Dual effects of sulfasalazine on rat sperm characteristics, spermatogenesis, and steroidogenesis in two experimental models. Toxicol Lett. 2018 Mar 1;284:46-55. doi: 10.1016/j.toxlet.2017.11.034. Epub 2017 Dec 22. PMID: 29197623.
62. Heidari R, Rasti M, Shirazi Yeganeh B, Niknahad H, Saeedi A, Najibi A. Sulfasalazine-induced renal and hepatic injury in rats and the protective role of taurine. Bioimpacts. 2016;6(1):3-8. doi: 10.15171/bi.2016.01. Epub 2016 Mar 28. PMID: 27340618; PMCID: PMC4916549.
63. Heidari R, Ghanbarinejad V, Mohammadi H, Ahmadi A, Ommati MM, Abdoli N, et al. Mitochondria protection as a mechanism underlying the hepatoprotective effects of glycine in cholestatic mice. Biomed Pharmacother. 2018 Jan;97:1086-1095. doi: 10.1016/j.biopha.2017.10.166. Epub 2017 Nov 10. PMID: 29136945.
64. Ommati MM, Attari H, Siavashpour A, Shafaghat M, Azarpira N, Ghaffari H, et al. Mitigation of cholestasis-associated hepatic and renal injury by edaravone treatment: Evaluation of its effects on oxidative stress and mitochondrial function. Liver Res. 2020;In Press. doi: 10.1016/j.livres.2020.10.003.
65. Jamshidzadeh A, Heidari R, Razmjou M, Karimi F, Moein MR, Farshad O, et al. An in vivo and in vitro investigation on hepatoprotective effects of Pimpinella anisum seed essential oil and extracts against carbon tetrachloride-induced toxicity. Iran J Basic Med Sci. 2015 Feb;18(2):205-11. PMID: 25825639; PMCID: PMC4366734.
66. Farshad O, Ommati MM, Yüzügülen J, Jamshidzadeh A, Mousavi K, Ahmadi Z, et al. Carnosine mitigates biomarkers of oxidative stress, improves mitochondrial function, and alleviates histopathological alterations in the renal tissue of cholestatic rats. Pharm Sci. 2020;27;32-45. doi: 10.34172/PS.2020.60.
67. Akram J, Hossein N, Reza H, Maryam A, Forouzan K, Mohammad Reza A, Omid F. Propylthiouracil-induced mitochondrial dysfunction in liver and its relevance to drug-induced hepatotoxicity. Pharm Sci. 2017;23;95-102. doi: 10.15171/PS.2017.15.
68. Heidari R, Babaei H, Eghbal MA. Cytoprotective Effects of Organosulfur Compounds against Methimazole Induced Toxicity in Isolated Rat Hepatocytes. Adv Pharm Bull. 2013;3(1):135-42. doi: 10.5681/apb.2013.023. Epub 2013 Feb 7. PMID: 24312826; PMCID: PMC3846059.
69. Khodaei F, Rashedinia M, Heidari R, Rezaei M, Khoshnoud MJ. Ellagic acid improves muscle dysfunction in cuprizone-induced demyelinated mice via mitochondrial Sirt3 regulation. Life Sci. 2019 Nov 15;237:116954. doi: 10.1016/j.lfs.2019.116954. Epub 2019 Oct 11. PMID: 31610192.
70. Mousavi K, Niknahad H, Li H, Jia Z, Manthari RK, Zhao Y, Shi X, Chen Y, Ahmadi A, Azarpira N, Khalvati B, Ommati MM, Heidari R. The activation of nuclear factor-E2-related factor 2 (Nrf2)/heme oxygenase-1 (HO-1) signaling blunts cholestasis-induced liver and kidney injury. Toxicol Res. 2021;10;911-27. doi: 10.1093/toxres/tfab073.
71. Ommati MM, Farshad O, Mousavi K, Khalili M, Jamshidzadeh A, Heidari R. Chlorogenic acid supplementation improves skeletal muscle mitochondrial function in a rat model of resistance training. Biologia. 2020;1221-1230. doi: 10.2478/s11756-020-00429-7.
72. Ommati MM, Farshad O, Mousavi K, Taghavi R, Farajvajari S, Azarpira N, et al. Agmatine alleviates hepatic and renal injury in a rat model of obstructive jaundice. PharmaNutrition. 2020;13;100212. doi: 10.1016/j.phanu.2020.100212.
73. Ommati MM, Farshad O, Niknahad H, Arabnezhad MR, Azarpira N, Mohammadi HR, et al. Cholestasis-associated reproductive toxicity in male and female rats: The fundamental role of mitochondrial impairment and oxidative stress. Toxicol Lett. 2019 Nov;316:60-72. doi: 10.1016/j.toxlet.2019.09.009. Epub 2019 Sep 11. PMID: 31520699.
74. Siavashpour A, Khalvati B, Azarpira N, Mohammadi H, Niknahad H, Heidari R. Poly (ADP-Ribose) polymerase-1 (PARP-1) overactivity plays a pathogenic role in bile acids-induced nephrotoxicity in cholestatic rats. Toxicol Lett. 2020 May 16;330:144-158. doi: 10.1016/j.toxlet.2020.05.012. Epub ahead of print. PMID: 32422328.
75. Eftekhari A, Heidari R, Ahmadian E, Eghbal MA. Cytoprotective properties of carnosine against isoniazid-induced toxicity in primary cultured rat hepatocytes. Pharm Sci. 2018;24;257-63. doi: 10.15171/PS.2018.38.
76. Heidari R, Babaei H, Eghbal MA. Ameliorative effects of taurine against methimazole-induced cytotoxicity in isolated rat hepatocytes. Sci Pharm. 2012 Oct-Dec;80(4):987-99. doi: 10.3797/scipharm.1205-16. Epub 2012 Aug 6. PMID: 23264945; PMCID: PMC3528057.
77. Heidari R, Mousavi K, Amin S, Ommati MM, Niknahad H. N-acetylcysteine treatment protects intestinal mitochondria in a surgical stress model. Trend Pharm Sci. 2020;6;87-96. doi: 10.30476/tips.2020.85960.1042.
78. Eghbal MA, Anoush M, Ghoreyshi A, Heidari R. The cytoprotective effects of Allium cepa methanolic extract in freshly isolated hepatocytes. Trend Pharm Sci. 2019;5;207-16. doi: 10.30476/tips.2020.84848.1036.
79. Niknahad H, Jamshidzadeh A, Heidari R, Hosseini Z, Mobini K, Khodaei F, et al. Paradoxical effect of methimazole on liver mitochondria: In vitro and in vivo. Toxicol Lett. 2016;259;108-15. doi: 10.1016/j.toxlet.2016.08.003.
80. Ommati MM, Farshad O, Mousavi K, Jamshidzadeh A, Azmoon M, Heidari S, et al. Betaine supplementation mitigates intestinal damage and decreases serum bacterial endotoxin in cirrhotic rats. PharmaNutrition. 2020;12;100179. doi: 10.1016/j.phanu.2020.100179.
81. Ghanbarinejad V, Ommati MM, Jia Z, Farshad O, Jamshidzadeh A, Heidari R. Disturbed mitochondrial redox state and tissue energy charge in cholestasis. J Biochem Mol Toxicol. 2021;In Press. doi: 10.1002/jbt.22846.
82. Ommati MM, Azarpira N, Khodaei F, Niknahad H, Gozashtegan V, Heidari R. Methylene blue treatment enhances mitochondrial function and locomotor activity in a C57BL/6 mouse model of multiple sclerosis. Trend Pharm Sci. 2020;6;29-42. doi: 10.30476/tips.2020.85962.1044.
83. Farshad O, Ommati MM, uuml, uuml, uuml, Len J, Alizadeh S, Mousavi K, Azarpira N, Marhonian A, Jamshidzadeh A, Heidari R. Skeletal muscle mitochondrial impairment in cirrhosis-induced sarcopenia. Trend Pharm Sci. 2020;6;189-204. doi: 10.30476/tips.2020.87789.1067.
84. Heidari R, Arabnezhad MR, Ommati MM, Azarpira N, Ghodsimanesh E, Niknahad H. Boldine supplementation regulates mitochondrial function and oxidative stress in a rat model of hepatotoxicity. Pharm Sci. 2019;25;1-10. doi: 10.15171/PS.2019.1.
85. Mousavi K, Niknahad H, Ghalamfarsa A, Mohammadi H, Azarpira N, Ommati MM, et al. Taurine mitigates cirrhosis-associated heart injury through mitochondrial-dependent and antioxidative mechanisms. Clin Exp Hepatol. 2020 Sep;6(3):207-219. doi: 10.5114/ceh.2020.99513. Epub 2020 Sep 30. PMID: 33145427; PMCID: PMC7592093.
86. Heidari R, Mandegani L, Ghanbarinejad V, Siavashpour A, Ommati MM, Azarpira N, et al. Mitochondrial dysfunction as a mechanism involved in the pathogenesis of cirrhosis-associated cholemic nephropathy. Biomed Pharmacother. 2019 Jan;109:271-280. doi: 10.1016/j.biopha.2018.10.104. Epub 2018 Nov 3. PMID: 30396085.
87. Ahmadi A, Niknahad H, Li H, Mobasheri A, Manthari RK, Azarpira N, et al. The inhibition of NFкB signaling and inflammatory response as a strategy for blunting bile acid-induced hepatic and renal toxicity. Toxicol Lett. 2021 Oct 1;349:12-29. doi: 10.1016/j.toxlet.2021.05.012. Epub 2021 Jun 2. PMID: 34089816.
88. Chen Y, Xing D, Wang W, Ding Y, Du L. Development of an ion-pair HPLC method for investigation of energy charge changes in cerebral ischemia of mice and hypoxia of Neuro-2a cell line. Biomed Chromatogr. 2007 Jun;21(6):628-34. doi: 10.1002/bmc.798. PMID: 17385810.
89. Farshad O, Heidari R, Zamiri MJ, Retana-Márquez S, Khalili M, Ebrahimi M, et al. Spermatotoxic Effects of Single-Walled and Multi-Walled Carbon Nanotubes on Male Mice. Front Vet Sci. 2020 Dec 17;7:591558. doi: 10.3389/fvets.2020.591558. PMID: 33392285; PMCID: PMC7775657.
90. Seifi K, Rezaei M, Yansari AT, Riazi GH, Zamiri MJ, Heidari R. Saturated fatty acids may ameliorate environmental heat stress in broiler birds by affecting mitochondrial energetics and related genes. J Therm Biol. 2018;78;1-9. doi: 10.1016/j.jtherbio.2018.08.018.
91. Slater TF, Sawyer B, Sträuli U. Studies on succinate-tetrazolium reductase systems: III. Points of coupling of four different tetrazolium salts III. Points of coupling of four different tetrazolium salts. Biochim Biophys Acta. 1963;77;383-93. doi: 10.1016/0006-3002(63)90513-4.
92. Dykens JA, Will Y. The significance of mitochondrial toxicity testing in drug development. Drug Discov Today. 2007 Sep;12(17-18):777-85. doi: 10.1016/j.drudis.2007.07.013. Epub 2007 Aug 22. PMID: 17826691.
93. Ghanbarinejad V, Jamshidzadeh A, Khalvati B, Farshad O, Li H, Shi X, et al. Apoptosis-inducing factor plays a role in the pathogenesis of hepatic and renal injury during cholestasis. Naunyn Schmiedebergs Arch Pharmacol. 2021;394;1191-203. doi: 10.1007/s00210-020-02041-7.
94. Ommati MM, Heidari R. Chapter 38 - Betaine, heavy metal protection, oxidative stress, and the liver. In: Patel VB, Preedy VR, editors. Toxicology: Academic Press; 2021. p. 387-95.
95. Kola I. The state of innovation in drug development. Clin Pharmacol Ther. 2008 Feb;83(2):227-30. doi: 10.1038/sj.clpt.6100479. PMID: 18202690.
96. Hughes JP, Rees S, Kalindjian SB, Philpott KL. Principles of early drug discovery. Br J Pharmacol. 2011 Mar;162(6):1239-49. doi: 10.1111/j.1476-5381.2010.01127.x. PMID: 21091654; PMCID: PMC3058157.
Trends in Pharmaceutical Sciences
Volume 7, Issue 3
September 2021
Pages 179-190

Files

Share

How to cite

Statistics