Abstract
Lung injury is a significant complication associated with cholestasis/cirrhosis. This problem significantly increases the risk of cirrhosis-related morbidity and mortality. Hence, finding effective therapeutic options in this field has significant clinical value. Severe inflammation and oxidative stress are involved in the mechanism of cirrhosis-induced lung injury. Taurine (TAU) is an abundant amino acid with substantial anti-inflammatory and antioxidative properties. The current study was designed to evaluate the role of TAU in cholestasis-related lung injury. For this purpose, bile duct ligated (BDL) rats were treated with TAU (0.5 and 1% w: v in drinking water). Significant increases in the broncho-alveolar lavage fluid (BALF) level of inflammatory cells (lymphocytes, neutrophils, basophils, monocytes, and eosinophils), increased IgG, and TNF-α were detected in the BDL animals (14 and 28 days after the BDL surgery). Alveolar congestion, hemorrhage, and fibrosis were the dominant pulmonary histopathological changes in the BDL group. Significant increases in the pulmonary tissue biomarkers of oxidative stress, including reactive oxygen species formation, lipid peroxidation, increased oxidized glutathione levels, and decreased reduced glutathione, were also detected in the BDL rats. Moreover, significant myeloperoxidase activity and nitric oxide levels were seen in the lung of BDL rats. It was found that TAU significantly blunted inflammation, alleviated oxidative stress, and mitigated lung histopathological changes in BDL animals. These data suggest TAU as a potential protective agent against cholestasis/cirrhosis-related lung injury.
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All data generated or analyzed during this study are included in this published article. Any supplementary data could be available from the corresponding author at reasonable request.
References
Abdel-Moneim AM, Al-Kahtani MA, El-Kersh MA, Al-Omair MA (2015) Free radical-scavenging, anti-inflammatory/anti-fibrotic and hepatoprotective actions of taurine and silymarin against CCl4 induced rat liver damage. PLoS ONE 10(12):e0144509
Abdoli N, Sadeghian I, Azarpira N, Ommati MM, Heidari R (2021) Taurine mitigates bile duct obstruction-associated cholemic nephropathy: effect on oxidative stress and mitochondrial parameters. Clin Exp Hepatol 7(1):30–40
Acharya M, Lau-Cam CA (2013) Comparative evaluation of the effects of taurine and thiotaurine on activities of antioxidant and glutathione-related enzymes by acetaminophen in the rat. In: Idrissi AE, L’Amoreaux WJ (eds) Taurine 8. Springer, New York, pp 199–215
Ahmadi N, Rezaee Z, Azarpira N, Zahedi S, Saeedi A, Jamshidzadeh A, Heidari R (2021) A histopathological evaluation on the effect of captopril in cyclophosphamide-induced hemorrhagic cystitis. Trend Pharm Sci 7(1):35–48
Ahmadi A, Niknahad H, Li H, Mobasheri A, Manthari RK, Azarpira N, Mousavi K, Khalvati B, Zhao Y, Sun J, Zong Y, Ommati MM, Heidari R (2021a) The inhibition of NFкB signaling and inflammatory response as a strategy for blunting bile acid-induced hepatic and renal toxicity. Toxicol Lett 34912–29
Alhumaidha KA, Saleh DO, Abd El Fattah MA, El-Eraky WI, Moawad H (2015) Cardiorenal protective effect of taurine against cyclophosphamide-induced toxicity in albino rats. Canadian Journal of Physiology and Pharmacology 1–9
Al-Hussaini A, Taylor RM, Samyn M, Bansal S, Heaton N, Rela M, Mieli-Vergani G, Dhawan A (2010) Long-term outcome and management of hepatopulmonary syndrome in children. Pediatr Transplant 14(2):276–282
Aniort J, Poyet A, Kemeny J-L, Philipponnet C, Heng A-E (2017) Bile cast nephropathy caused by obstructive cholestasis. Am J Kidney Dis 69(1):143–146
Aratani Y (2018) Myeloperoxidase: its role for host defense, inflammation, and neutrophil function. Archives of Biochemistry and Biophysics 64047–52
Aruoma OI, Halliwell B, Hoey BM, Butler J (1988) The antioxidant action of taurine, hypotaurine and their metabolic precursors. Biochemical Journal 256(1):251–255
Bedard K, Krause K-H (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87(1):245–313
Bhavsar TM, Cantor JO, Patel SN, Lau-Cam CA (2009) Attenuating effect of taurine on lipopolysaccharide-induced acute lung injury in hamsters. Pharmacol Res 60(5):418–428
Bomzon A, Holt S, Moore K (1997) Bile acids, oxidative stress, and renal function in biliary obstruction. Semin Nephrol 17(6):549–562
Carrera-Quintanar L, Funes L, Herranz-López M, Martínez-Peinado P, Pascual-García S, Sempere JM, Boix-Castejón M, Córdova A, Pons A, Micol V, Roche E (2020) Antioxidant supplementation modulates neutrophil inflammatory response to exercise-induced stress. Antioxidants 9(12):E1242
Chen B, You Wen J, Liu Xue Q, Xue S, Qin H, Jiang Han D (2017) Chronic microaspiration of bile acids induces lung fibrosis through multiple mechanisms in rats. Clin Sci 131(10):951–963
Chen S, Chen H, Du Q, Shen J (2020) Targeting myeloperoxidase (MPO) mediated oxidative stress and inflammation for reducing brain ischemia injury: potential application of natural compounds. Front Physiol 0
Cheresh P, Kim S-J, Tulasiram S, Kamp DW (2013) Oxidative stress and pulmonary fibrosis. Biochim Biophys Acta 1832(7):1028–1040
Cozzi R, Ricordy R, Bartolini F, Ramadori L, Perticone P, De Salvia R (1995) Taurine and ellagic acid: two differently-acting natural antioxidants. Environ Mol Mutagen 26(3):248–254
Das J, Ghosh J, Manna P, Sinha M, Sil PC (2009) Taurine protects rat testes against NaAsO2-induced oxidative stress and apoptosis via mitochondrial dependent and independent pathways. Toxicol Lett 187(3):201–210
Daubeuf F, Frossard N (2014) Eosinophils and the ovalbumin mouse model of asthma. Methods Mol Biol 1178283–293
Ding Y-L, Zhang L-J, Wang X, Zhou Q-C, Li N, Wang C-X, Zhang X-Q (2014) Fetal lung surfactant and development alterations in intrahepatic cholestasis of pregnancy. World J Obstet Gynecol 3(2):78–84
Ekremoğlu M, Türközkan N, Erdamar H, Kurt Y, Yaman H (2007) Protective effect of taurine on respiratory burst activity of polymorphonuclear leukocytes in endotoxemia. Amino Acids 32(3):413–417
Enrico Z, Daniele DL, Marco M, Giada B, Costantino R (2007) Intrahepatic cholestasis of pregnancy and bile acids induced lung injury in newborn infants. Curr Pediatr Rev 3(2):167–176
Erlinger S (2014) Bile acids in cholestasis: bad for the liver, not so good for the kidney. Clin Res Hepatol Gastroenterol 38(4):392–394
Farshad O, Ommati MM, Yüzügülen J, Jamshidzadeh A, Mousavi K, Ahmadi Z, Azarpira N, Ghaffari H, Najibi A, Shafaghat M, Niknahad H, Heidari R (2020) Carnosine mitigates biomarkers of oxidative stress, improves mitochondrial function, and alleviates histopathological alterations in the renal tissue of cholestatic rats. Pharm Sci 27(1):32–45
Filippa VP, Mohamed FH (2019) Lithium therapy effects on the reproductive system. Psychiatry and Neuroscience Update. Springer 187–200
Forrester Steven J, Kikuchi Daniel S, Hernandes Marina S, Xu Q, Griendling Kathy K (2018) Reactive oxygen species in metabolic and inflammatory signaling. Circ Res 122(6):877–902
Ghanbarinejad V, Jamshidzadeh A, Khalvati B, Farshad O, Li H, Shi X, Chen Y, Ommati MM, Heidari R (2021) Apoptosis-inducing factor plays a role in the pathogenesis of hepatic and renal injury during cholestasis. Naunyn-Schmiedeberg’s Arch Pharmacol 394(6):1191–1203
Gordon RE, Shaked AA, Solano DF (1986) Taurine protects hamster bronchioles from acute NO2-induced alterations. A histologic, ultrastructural, and freeze-fracture study. Am J Pathol 125(3):585–600
Guizoni DM, Vettorazzi JF, Carneiro EM, Davel AP (2020) Modulation of endothelium-derived nitric oxide production and activity by taurine and taurine-conjugated bile acids. Nitric Oxide 9448–53
Guler L, Tavlasoglu M, Yucel O, Guler A, Sahin MA, Kurkluoglu M, Sirin Y, Eken A, Gamsizkan M, Dakak M, Gurkok S, Genc O (2014) Taurine attenuates lung ischemia–reperfusion injury after lung transplantation in rats. J Anesth 28(3):347–353
Gürer H, Ozgünes H, Saygin E, Ercal N (2001) Antioxidant effect of taurine against lead-induced oxidative stress. Arch Environ Contam Toxicol 41(4):397–402
Gurujeyalakshmi G, Hollinger MA, Giri SN (1998) Regulation of transforming growth factor- β1 mRNA expression by taurine and niacin in the bleomycin hamster hodel of lung fibrosis. Am J Respir Cell Mol Biol 18(3):334–342
Hamza RZ, El-Shenawy NS (2017) Anti-inflammatory and antioxidant role of resveratrol on nicotine-induced lung changes in male rats. Toxicology Reports 4399–407
Heidari R, Niknahad H (2019) The role and study of mitochondrial impairment and oxidative stress in cholestasis. In: Vinken M (ed) Experimental Cholestasis Research. Springer, New York, NY, pp 117–132
Heidari R, Babaei H, Eghbal MA (2012) Ameliorative effects of taurine against methimazole-induced cytotoxicity in isolated rat hepatocytes. Sci Pharm 80(4):987–1000
Heidari R, Babaei H, Eghbal MA (2013) Cytoprotective effects of taurine against toxicity induced by isoniazid and hydrazine in isolated rat hepatocytes. Arh Hig Rada Toksikol 64(2):201–210
Heidari R, Babaei H, Eghbal MA (2014) Amodiaquine-induced toxicity in isolated rat hepatocytes and the cytoprotective effects of taurine and/or N-acetyl cysteine. Res Pharm Sci 9(2):97–105
Heidari R, Jamshidzadeh A, Keshavarz N, Azarpira N (2015) Mitigation of methimazole-induced hepatic injury by taurine in mice. Sci Pharm 83(1):143–158
Heidari R, Niknahad H, Jamshidzadeh A, Azarpira N, Bazyari M, Najibi A (2015) Carbonyl traps as potential protective agents against methimazole-induced liver injury. J Biochem Mol Toxicol 29(4):173–181
Heidari R, Sadeghi N, Azarpira N, Niknahad H (2015) Sulfasalazine-induced hepatic injury in an ex vivo model of isolated perfused rat liver and the protective role of taurine. Pharm Sci 21(4):211–219
Heidari R, Esmailie N, Azarpira N, Najibi A, Niknahad H (2016) Effect of thiol-reducing agents and antioxidants on sulfasalazine-induced hepatic injury in normotermic recirculating isolated perfused rat liver. Toxicol Res 32(2):133–140
Heidari R, Jamshidzadeh A, Niknahad H, Safari F, Azizi H, Abdoli N, Ommati MM, Khodaei F, Saeedi A, Najibi A (2016) 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 2(1):59–76
Heidari R, Rasti M, ShiraziYeganeh B, Niknahad H, Saeedi A, Najibi A (2016) Sulfasalazine-induced renal and hepatic injury in rats and the protective role of taurine. BioImpacts 6(1):3–8
Heidari R, Moezi L, Asadi B, Ommati MM, Azarpira N (2017) Hepatoprotective effect of boldine in a bile duct ligated rat model of cholestasis/cirrhosis. PharmaNutrition 5(3):109–117
Heidari R, Jafari F, Khodaei F, ShiraziYeganeh B, Niknahad H (2018) Mechanism of valproic acid-induced Fanconi syndrome involves mitochondrial dysfunction and oxidative stress in rat kidney. Nephrology 23(4):351–361
Heidari R, Jamshidzadeh A, Ghanbarinejad V, Ommati MM, Niknahad H (2018) Taurine supplementation abates cirrhosis-associated locomotor dysfunction. Clin Exp Hepatol 4(2):72–82
Heidari R, Ommati MM, Alahyari S, Azarpira N, Niknahad H (2018) Amino acid-containing Krebs-Henseleit buffer protects rat liver in a long-term organ perfusion model. Pharm Sci 24(3):168–179
Heidari R, Ahmadi A, Ommati MM, Niknahad H (2020) Methylene blue improves mitochondrial function in the liver of cholestatic rats. Trend Pharm Sci 6(2):73–86
Heidari R, Jamshidzadeh A, Niknahad H, Mardani E, Ommati MM, Azarpira N, Khodaei F, Zarei A, Ayarzadeh M, Mousavi S, Abdoli N, Yeganeh BS, Saeedi A, Najibi A (2016b) Effect of taurine on chronic and acute liver injury: focus on blood and brain ammonia. Toxicology Reports 3870–879
Heidari R, Ghanbarinejad V, Mohammadi H, Ahmadi A, Esfandiari A, Azarpira N, Niknahad H (2018a) Dithiothreitol supplementation mitigates hepatic and renal injury in bile duct ligated mice: potential application in the treatment of cholestasis-associated complications. Biomed Pharmacother 991022–1032
Heidari R, Ghanbarinejad V, Mohammadi H, Ahmadi A, Ommati MM, Abdoli N, Aghaei F, Esfandiari A, Azarpira N, Niknahad H (2018b) Mitochondria protection as a mechanism underlying the hepatoprotective effects of glycine in cholestatic mice. Biomed Pharmacother 971086–1095
Heidari R, Behnamrad S, Khodami Z, Ommati MM, Azarpira N, Vazin A (2019a) The nephroprotective properties of taurine in colistin-treated mice is mediated through the regulation of mitochondrial function and mitigation of oxidative stress. Biomed Pharmacother 109103–111
Heidari R, Mandegani L, Ghanbarinejad V, Siavashpour A, Ommati MM, Azarpira N, Najibi A, Niknahad H (2019b) Mitochondrial dysfunction as a mechanism involved in the pathogenesis of cirrhosis-associated cholemic nephropathy. Biomed Pharmacother 109271–280
Heinrich TA, Silva RSd, Miranda KM, Switzer CH, Wink DA, Fukuto JM (2013) Biological nitric oxide signalling: chemistry and terminology. Br J Pharmacol 169(7):1417–1429
Herraez E, Lozano E, Poli E, Keitel V, De Luca D, Williamson C, Marin JJG, Macias RIR (2014) Role of macrophages in bile acid-induced inflammatory response of fetal lung during maternal cholestasis. J Mol Med 92(4):359–372
Horvatits T, Drolz A, Rutter K, Roedl K, Fauler G, Müller C, Kluge S, Trauner M, Schenk P, Fuhrmann V (2017) Serum bile acids in patients with hepatopulmonary syndrome. Z Gastroenterol 55(4):361–367
Hsieh Y-L, Yeh Y-H, Lee Y-T, Huang C-Y (2014) Effect of taurine in chronic alcoholic patients. Food Funct 5(7):1529–1535
Hu Z-H, Kong Y-Y, Ren J-J, Huang T-J, Wang Y-Q, Liu L-X (2020) Kidney and lung tissue modifications after BDL-induced liver injury in mice are associated with increased expression of IGFBPrP1 and activation of the NF-κB inflammation pathway. Int J Clin Exp Pathol 13(2):192–202
Huxtable RJ et al (1992) Physiological actions of taurine. Physiol Rev 72(1):101–163
Islambulchilar M, Asvadi I, Sanaat Z, Esfahani A, Sattari M (2015) Taurine attenuates chemotherapy-induced nausea and vomiting in acute lymphoblastic leukemia. Amino Acids 47(1):101–109
Jamshidzadeh A, Heidari R, Abasvali M, Zarei M, Ommati MM, Abdoli N, Khodaei F, Yeganeh Y, Jafari F, Zarei A, Latifpour Z, Mardani E, Azarpira N, Asadi B, Najibi A (2017) Taurine treatment preserves brain and liver mitochondrial function in a rat model of fulminant hepatic failure and hyperammonemia. Biomed Pharmacother 86514–520
Jüngst C, Lammert F (2013) Cholestatic liver disease. Dig Dis 31(1):152–154
Karamikhah R, Jamshidzadeh A, Azarpira N, Saeidi A, Heidari R (2016) Propylthiouracil-induced liver injury in mice and the protective role of taurine. Pharm Sci 21(2):94–101
Kato T, Okita S, Wang S, Tsunekawa M, Ma N (2015) The effects of taurine administration against inflammation in heavily exercised skeletal muscle of rats. Advances in Experimental Medicine and Biology 803773–784
Kim C, Cha Y-N (2014) Taurine chloramine produced from taurine under inflammation provides anti-inflammatory and cytoprotective effects. Amino Acids 46(1):89–100
Kinnula VL, Fattman CL, Tan RJ, Oury TD (2005) Oxidative stress in pulmonary fibrosis. Am J Respir Crit Care Med 172(4):417–422
Kolli VK, Abraham P, Isaac B, Selvakumar D (2009) Neutrophil infiltration and oxidative stress may play a critical role in methotrexate-induced renal damage. Chemotherapy 55(2):83–90
Krones E, Wagner M, Eller K, Rosenkranz AR, Trauner M, Fickert P (2015) Bile acid-induced cholemic nephropathy. Dig Dis 33(3):367–375
Krowka MJ, Cortese DA (1985) Pulmonary aspects of chronic liver disease and liver transplantation. Mayo Clin Proc 60(6):407–418
Levy C (2013) Cholestatic liver diseases, an issue of clinics in liver disease. Elsevier Health Sciences
Li Y, Arnold JMO, Pampillo M, Babwah AV, Peng T (2009) Taurine prevents cardiomyocyte death by inhibiting NADPH oxidase-mediated calpain activation. Free Radic Biol Med 46(1):51–61
Li X, Yang H, Sun H, Lu R, Zhang C, Gao N, Meng Q, Wu S, Wang S, Aschner M, Wu J, Tang B, Gu A, Kay SA, Chen R (2017) Taurine ameliorates particulate matter-induced emphysema by switching on mitochondrial NADH dehydrogenase genes. Proc Natl Acad Sci U S A 114(45):E9655–E9664
Lin C-J, Chiu C-C, Chen Y-C, Chen M-L, Hsu T-C, Tzang B-S (2015) Taurine attenuates hepatic inflammation in chronic alcohol-fed rats through inhibition of TLR4/MyD88 signaling. J Med Food 18(12):1291–1298
Liu SF, Ye X, Malik AB (1999) Pyrrolidine dithiocarbamate prevents I-κB degradation and reduces microvascular injury induced by lipopolysaccharide in multiple organs. Mol Pharmacol 55(4):658–667
Liu Y, Li F, Zhang L, Wu J, Wang Y, Yu H (2017) Taurine alleviates lipopolysaccharide-induced liver injury by anti-inflammation and antioxidants in rats. Mol Med Report 16(5):6512–6517
Lv W, Booz GW, Fan F, Wang Y, Roman RJ (2018) Oxidative stress and renal fibrosis: recent insights for the development of novel therapeutic strategies. Front Physiol 9
MacNee W (2001) Oxidative stress and lung inflammation in airways disease. Eur J Pharmacol 429(1):195–207
Maleki V, Mahdavi R, Hajizadeh-Sharafabad F, Alizadeh M (2020) The effects of taurine supplementation on oxidative stress indices and inflammation biomarkers in patients with type 2 diabetes: a randomized, double-blind, placebo-controlled trial. Diabetol Metab Syndr 12(1):9
Marcinkiewicz J, Kurnyta M, Biedroń R, Bobek M, Kontny E, Maśliński W (2006) Anti-inflammatory effects of taurine derivatives (taurine chloramine, taurine bromamine, and taurolidine) are mediated by different mechanisms. Advances in Experimental Medicine and Biology 583481–492
Marcinkiewicz J, Kontny E (2014) Taurine and inflammatory diseases. Amino Acids 46(1):7–20
Meeks RG, Harrison S (1991) Hepatotoxicology. CRC Press
Merli M, Lucidi C, Giannelli V, Giusto M, Riggio O, Falcone M, Ridola L, Attili AF, Venditti M (2010) Cirrhotic patients are at risk for health care–associated bacterial infections. Clin Gastroenterol Hepatol 8(11):979-985.e971
Miao J, Zhang J, Ma Z, Zheng L (2013) The role of NADPH oxidase in taurine attenuation of Streptococcus uberis-induced mastitis in rats. Int Immunopharmacol 16(4):429–435
Militante JD, Lombardini JB (2002) Treatment of hypertension with oral taurine: experimental and clinical studies. Amino Acids 23(4):381–393
Miyazaki T, Matsuzaki Y (2014) Taurine and liver diseases: a focus on the heterogeneous protective properties of taurine. Amino Acids 46(1):101–110
Moezi L, Heidari R, Amirghofran Z, Nekooeian AA, Monabati A, Dehpour AR (2013) Enhanced anti-ulcer effect of pioglitazone on gastric ulcers in cirrhotic rats: the role of nitric oxide and IL-1β. Pharmacol Rep 65(1):134–143
Mohammadi H, Sayad A, Mohammadi M, Niknahad H, Heidari R (2020) N-acetyl cysteine treatment preserves mitochondrial indices of functionality in the brain of hyperammonemic mice. Clin Exp Hepatol 6(2):106–115
Mousavi K, Niknahad H, Ghalamfarsa A, Mohammadi H, Azarpira N, Ommati MM, Heidari R (2020) Taurine mitigates cirrhosis-associated heart injury through mitochondrial-dependent and antioxidative mechanisms. Clin Exp Hepatol 6(3):207–219
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 (2021) 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 10(4):911–927
Muroya M, Chang K, Uchida K, Bougaki M, Yamada Y (2012) Analysis of cytotoxicity induced by proinflammatory cytokines in the human alveolar epithelial cell line A549. Biosci Trends 6(2):70–80
Ndrepepa G (2019) Myeloperoxidase - a bridge linking inflammation and oxidative stress with cardiovascular disease. Clin Chim Acta 49336–51
Nikkhah E, Shirani K, Rezaee R, Karimi G (2021) Protective effects of taurine against hepatotoxicity induced by pharmaceuticals and environmental chemicals. Toxicol Environ Chem 103(1):56–84
Niknahad H, Heidari R, Alzuhairi AM, Najibi A (2014) Mitochondrial dysfunction as a mechanism for pioglitazone-induced injury toward HepG2 cell line. Pharm Sci 20(4):169–174
Niknahad H, Heidari R, Mohammadzadeh R, Ommati MM, Khodaei F, Azarpira N, Abdoli N, Zarei M, Asadi B, Rasti M, Yeganeh BS, Taheri V, Saeedi A, Najibi A (2017) Sulfasalazine induces mitochondrial dysfunction and renal injury. Ren Fail 39(1):745–753
Niknahad H, Jamshidzadeh A, Heidari R, Zarei M, Ommati MM (2017) 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 3(3):141–151
Okada S, Hasegawa S, Hasegawa H, Ainai A, Atsuta R, Ikemoto K, Sasaki K, Toda S, Shirabe K, Takahara M, Harada S, Morishima T, Ichiyama T (2013) Analysis of bronchoalveolar lavage fluid in a mouse model of bronchial asthma and H1N1 2009 infection. Cytokine 63(2):194–200
Ommati MM, Jamshidzadeh A, Niknahad H, Mohammadi H, Sabouri S, Heidari R, Abdoli N (2017) N-acetylcysteine treatment blunts liver failure-associated impairment of locomotor activity. PharmaNutrition 5(4):141–147
Ommati MM, Amjadinia A, Mousavi K, Azarpira N, Jamshidzadeh A, Heidari R (2021) N-acetyl cysteine treatment mitigates biomarkers of oxidative stress in different tissues of bile duct ligated rats. Stress 24(2):213–228
Ommati MM, Farshad O, Azarpira N, Ghazanfari E, Niknahad H, Heidari R (2021) Silymarin mitigates bile duct obstruction-induced cholemic nephropathy. Naunyn-Schmiedeberg’s Arch Pharmacol 394(6):1301–1314
Ommati MM, Farshad O, Azarpira N, Shafaghat M, Niknahad H, Heidari R (2021) Betaine alleviates cholestasis-associated renal injury by mitigating oxidative stress and enhancing mitochondrial function. Biologia 76(1):351–365
Ommati MM, Hojatnezhad S, Abdoli N, Manthari RK, Jia Z, Najibi A, Akbarizadeh AR, Sadeghian I, Farshad O, Azarpira N, Niknahad H, Heidari R (2021) Pentoxifylline mitigates cholestasis-related cholemic nephropathy. Clinical and Experimental Hepatology 7(4):377–389
Ommati MM, Niknahad H, Farshad O, Azarpira N, Heidari R (2021) In vitro and in vivo evidence on the role of mitochondrial impairment as a mechanism of lithium-induced nephrotoxicity. Biol Trace Elem Res 199(5):1908–1918
Ommati MM, Li H, Jamshidzadeh A, Khoshghadam F, Retana-Márquez S, Lu Y, Farshad O, Nategh Ahmadi MH, Gholami A, Heidari R (2022) The crucial role of oxidative stress in non-alcoholic fatty liver disease-induced male reproductive toxicity: the ameliorative effects of Iranian indigenous probiotics. Naunyn-Schmiedeberg’s Arch Pharmacol 395(2):247–265
Ommati MM, Farshad O, Niknahad H, Arabnezhad MR, Azarpira N, Mohammadi HR, Haghnegahdar M, Mousavi K, Akrami S, Jamshidzadeh A, Heidari R (2019) Cholestasis-associated reproductive toxicity in male and female rats: the fundamental role of mitochondrial impairment and oxidative stress. Toxicol Lett 31660–72
Ommati MM, Attari H, Siavashpour A, Shafaghat M, Azarpira N, Ghaffari H, Moezi L, Heidari R (2020a) Mitigation of cholestasis-associated hepatic and renal injury by edaravone treatment: evaluation of its effects on oxidative stress and mitochondrial function. Liver Res In-Press
Ommati MM, Farshad O, Mousavi K, Jamshidzadeh A, Azmoon M, Heidari S, Azarpira N, Niknahad H, Heidari R (2020b) Betaine supplementation mitigates intestinal damage and decreases serum bacterial endotoxin in cirrhotic rats. PharmaNutrition 12100179
Ommati MM, Farshad O, Mousavi K, Taghavi R, Farajvajari S, Azarpira N, Moezi L, Heidari R (2020c) Agmatine alleviates hepatic and renal injury in a rat model of obstructive jaundice. PharmaNutrition 13100212
Ommati MM, Farshad O, Niknahad H, Mousavi K, Moein M, Azarpira N, Mohammadi H, Jamshidzadeh A, Heidari R (2020d) Oral administration of thiol-reducing agents mitigates gut barrier disintegrity and bacterial lipopolysaccharide translocation in a rat model of biliary obstruction. Curr Res Pharmacol Drug Discov 110–18
Ommati MM, Mohammadi H, Mousavi K, Azarpira N, Farshad O, Dehghani R, Najibi A, Kamran S, Niknahad H, Heidari R (2020e) Metformin alleviates cholestasis-associated nephropathy through regulating oxidative stress and mitochondrial function. Liver Res
Ommati MM, Shi X, Li H, Zamiri MJ, Farshad O, Jamshidzadeh A, Heidari R, Ghaffari H, Zaker L, Sabouri S, Chen Y (2020f) The mechanisms of arsenic-induced ovotoxicity, ultrastructural alterations, and autophagic related paths: an enduring developmental study in folliculogenesis of mice. Ecotoxicology and Environmental Safety 204110973
Ommati MM, Arabnezhad MR, Farshad O, Jamshidzadeh A, Niknahad H, Retana-Marquez S, Jia Z, Nateghahmadi MH, Mousavi K, Arazi A, Azmoon MR, Azarpira N, Heidari R (2021b) The role of mitochondrial impairment and oxidative stress in the pathogenesis of lithium-induced reproductive toxicity in male mice. Frontiers in Veterinary Science 8(125):
Ommati MM, Arabnezhad MR, Farshad O, Jamshidzadeh A, Niknahad H, Retana-Marquez S, Jia Z, Nateghahmadi MH, Mousavi K, Arazi A, Azmoon MR, Azarpira N, Heidari R (2021c) The role of mitochondrial impairment and oxidative stress in the pathogenesis of lithium-induced reproductive toxicity in male mice. Front Vet Sci 8603262
Orellana M, Rodrigo R, Thielemann L, Guajardo V (2000) Bile duct ligation and oxidative stress in the rat: effects in liver and kidney. Comp Biochem Physiol 126(2):105–111
Pushpakiran G, Mahalakshmi K, Anuradha CV (2004) Taurine restores ethanol-induced depletion of antioxidants and attenuates oxidative stress in rat tissues. Amino Acids 27(1):91–96
Ramos CdO, Campos KKD, Costa GdP, Cangussú SD, Talvani A, Bezerra FS (2018) Taurine treatment decreases inflammation and oxidative stress in lungs of adult mice exposed to cigarette smoke. Regulatory Toxicology and Pharmacology 9850–57
Rashid K, Das J, Sil PC (2013) Taurine ameliorate alloxan induced oxidative stress and intrinsic apoptotic pathway in the hepatic tissue of diabetic rats. Food and Chemical Toxicology 51317–329
Redmond HP, Stapleton PP, Neary P, Bouchier-Hayes D (1998) Immunonutrition: the role of taurine. Nutrition 14(7):599–604
Ruiz-Feria CA, Wideman RF (2001) Taurine, cardiopulmonary hemodynamics, and pulmonary hypertension syndrome in broilers. Poult Sci 80(11):1607–1618
Saad AB, Rjeibi I, Alimi H, Ncib S, Smida A, Zouari N, Zourgui L (2017) Lithium induced, oxidative stress and related damages in testes and heart in male rats: the protective effects of Malva sylvestris extract. Biomed Pharmacother 86127–135
Salatti Ferrari R, da Rosa DP, Forgiarini LF, Bona S, Simões Dias A, Marroni NP (2012) Oxidative stress and pulmonary changes in experimental liver cirrhosis. Oxid Med Cell Longev 2012e486190
Santangelo F, Cortijo J, Morcillo E (2003) Taurine and the lung. In: Lombardini JB, Schaffer SW, Azuma J (eds) Taurine 5: Beginning the 21st Century. Springer, US, Boston, MA, pp 403–410
Schaffer S, Kim HW (2018) Effects and mechanisms of taurine as a therapeutic agent. Biomol Ther (seoul) 26(3):225–241
Schuller-Levis GB, Gordon RE, Wang C, Park E (2003) Taurine reduces lung inflammation and fibrosis caused by bleomycin. Advances in Experimental Medicine and Biology 526395–402
Schuller-Levis GB, Park E (2003) Taurine: new implications for an old amino acid. FEMS Microbiol Lett 226(2):195–202
Schwarzer R, Kivaranovic D, Mandorfer M, Paternostro R, Wolrab D, Heinisch B, Reiberger T, Ferlitsch M, Gerner C, Trauner M, Peck-Radosavljevic M, Ferlitsch A (2018) Randomised clinical study: the effects of oral taurine 6g/day vs placebo on portal hypertension. Aliment Pharmacol Ther 47(1):86–94
Shi X, Flynn DC, Porter DW, Leonard SS, Vallyathan V, Castranova V (1997) Efficacy of taurine based compounds as hydroxyl radical scavengers in silica induced peroxidation. Ann Clin Lab Sci 27(5):365–374
Shikata F, Sakaue T, Nakashiro K-i, Okazaki M, Kurata M, Okamura T, Okura M, Ryugo M, Nakamura Y, Yasugi T, Higashiyama S, Izutani H (2014) Pathophysiology of lung injury induced by common bile duct ligation in mice. PLoS ONE 9(4):e94550
Shimada K, Jong CJ, Takahashi K, Schaffer SW (2015) Role of ROS production and turnover in the antioxidant activity of taurine.
Siavashpour A, Khalvati B, Azarpira N, Mohammadi H, Niknahad H, Heidari R (2020) Poly (ADP-Ribose) polymerase-1 (PARP-1) overactivity plays a pathogenic role in bile acids-induced nephrotoxicity in cholestatic rats. Toxicol Lett 330144–158
Stamp LK, Khalilova I, Tarr JM, Senthilmohan R, Turner R, Haigh RC, Winyard PG, Kettle AJ (2012) Myeloperoxidase and oxidative stress in rheumatoid arthritis. Rheumatology 51(10):1796–1803
Su Y, Fan W, Ma Z, Wen X, Wang W, Wu Q, Huang H (2014) Taurine improves functional and histological outcomes and reduces inflammation in traumatic brain injury. Neuroscience 26656–65
Todd NW, Luzina IG, Atamas SP (2012) Molecular and cellular mechanisms of pulmonary fibrosis. Fibrogenesis & Tissue Repair 5(1):11
Truong DH, Eghbal MA, Hindmarsh W, Roth SH, O’Brien PJ (2006) Molecular mechanisms of hydrogen sulfide toxicity. Drug Metab Rev 38(4):733–744
Tu S, Zhang X-L, Wan H-F, Xia Y-Q, Liu Z-Q, Yang X-H, Wan F-S (2018) Effect of taurine on cell proliferation and apoptosis human lung cancer A549 cells. Oncol Lett 15(4):5473–5480
Vazin A, Heidari R, Khodami Z (2020) Curcumin supplementation alleviates polymyxin E-induced nephrotoxicity. J Exp Pharmacol 12129–136
Wójcik OP, Koenig KL, Zeleniuch-Jacquotte A, Costa M, Chen Y (2010) The potential protective effects of taurine on coronary heart disease. Atherosclerosis 208(1):19–25
Wright CE, Tallan HH, Lin YY (1986) Taurine: biological update. Annu Rev Biochem 55(1):427–453
Yang K, Wu Y, Xie H, Li M, Ming S, Li L, Li M, Wu M, Gong S, Huang X (2016) Macrophage-mediated inflammatory response decreases mycobacterial survival in mouse MSCs by augmenting NO production. Sci Rep 6(1):27326
Yang L, Tang J, Chen H, Ge D, Sui T, Que J, Cao X, Ge Y (2016) Taurine reduced epidural fibrosis in rat models after laminectomy via downregulating EGR1. Cell Physiol Biochem 38(6):2261–2271
You JS, Chang KJ (1998) Taurine protects the liver against lipid peroxidation and membrane disintegration during rat hepatocarcinogenesis. Advances in Experimental Medicine and Biology 442105–112
Yu L, Ding Y, Huang T, Huang X (2014) Effect of bile acid on fetal lung in rat model of intrahepatic cholestasis of pregnancy. Int J Endocrinol 2014e308274
Zaki HF, Salem HA, El-Yamany MF (2011) Taurine: a promising agent of therapeutic potential in experimentally-induced arthritis. Egypt Rheumatol 33(3):131–137
Zecca E, De Luca D, Baroni S, Vento G, Tiberi E, Romagnoli C (2008) Bile acid-induced lung injury in newborn infants: a bronchoalveolar lavage fluid study. Pediatrics 121(1):e146-149
Acknowledgements
The authors acknowledge the Pharmaceutical Sciences Research Center of Shiraz University of Medical Sciences for providing technical facilities for this investigation.
Funding
This study was financially supported by the Vice-Chancellor of Research Affairs of Shiraz University of Medical Sciences, Shiraz, Iran (grants #23701/23031/23040/23028/16428), Shanxi Agricultural University (Youth Fund project of Applied Basic Research in Shanxi Province; K272104065), and Natural Science Foundation of Shanxi Province (grant no. 201901D111232). Ali Mobasheri is supported by the Academy of Finland Profi6 336449 grant awarded to the University of Oulu, the European Commission, and the European Structural and Social Funds (ES Struktūrinės Paramos) awarded through the Research Council of Lithuania (Lietuvos Mokslo Taryba) and the funding program: Attracting Foreign Researchers for Research Implementation (2018–2022), grant no 01.2.2-LMT-K-718–02-0022.
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M.M. Ommati, R. Heidari, H. Niknahad, RK Manthari, N. Azarpira, and A. Mobasheri were involved in subject conceptualization, funding acquisition, methodology, data analysis, validation, project administration, resources, and supervision, writing the original draft, and review and editing the manuscript. Y. Ma, D. Xu, Zh. Tang, Y. Lu, RK. Manthari, N. Abdoli, I. Sadeghian, A. Mousavifaraz, H. Xin, and Y. Mingyu were involved in data visualization, literature review, data analysis, and writing the original manuscript draft. I. Sadeghian, A. Mousavifaraz, A. Nadgaran, A. Nikoozadeh, S. Mazloomi, P. Mehrabani, M. Rezaei, N. Azarpira, and R. Heidari were involved in data collection. All authors read and approved the final version of the manuscript. The authors declare that all data were generated in-house, and no paper mill was used.
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All procedures using experimental animals were approved by the institutional ethics committee at Shiraz University of Medical Sciences, Shiraz, Iran (IR.SUMS.REC.1399.1353). This study does not include any human participants.
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Ommati, M.M., Mobasheri, A., Ma, Y. et al. Taurine mitigates the development of pulmonary inflammation, oxidative stress, and histopathological alterations in a rat model of bile duct ligation. Naunyn-Schmiedeberg's Arch Pharmacol 395, 1557–1572 (2022). https://doi.org/10.1007/s00210-022-02291-7
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DOI: https://doi.org/10.1007/s00210-022-02291-7