Pioglitazone ameliorates hepatic damage in irradiated rats via regulating anti-inflammatory and antifibrogenic signalling pathways

References

• Liang S-X, Zhu X-D, Xu Z-Y, et al. Radiation-induced liver disease in three-dimensional conformal radiation therapy for primary liver carcinoma: the risk factors and hepatic radiation tolerance. Int J Radiat Oncol Biol Phys. 2006;65:426–434.
   PubMed Web of Science ®Google Scholar
• Kim H-G, Jang S-S, Lee J-S, et al. Panax ginseng Meyer prevents radiation-induced liver injury via modulation of oxidative stress and apoptosis. J Ginseng Res. 2017;41:159–168.
   PubMed Web of Science ®Google Scholar
• Abd El-Haleim EA, Bahgat AK, Saleh S. Resveratrol and fenofibrate ameliorate fructose-induced nonalcoholic steatohepatitis by modulation of genes expression. World J Gastroenterol. 2016;22:2931–2948.
   PubMed Web of Science ®Google Scholar
• Farrell GC, Larter CZ. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology. 2006;43:S99–S112.
   PubMed Web of Science ®Google Scholar
• Lee WM. Drug-induced hepatotoxicity. N Engl J Med. 2003;349:474–485.
   PubMed Web of Science ®Google Scholar
• Bongartz T, Coras B, Vogt T, et al. Treatment of active psoriatic arthritis with the PPARgamma ligand pioglitazone: an open-label pilot study. Rheumatol Oxf Engl. 2005;44:126–129.
   PubMed Web of Science ®Google Scholar
• Somi MH, Hajipour B, Asl NA, et al. Pioglitazone attenuates ischemia/reperfusion-induced liver injury in rats. Transplant Proc. 2009;41:4105–4109.
   PubMed Web of Science ®Google Scholar
• Schwabl P, Payer BA, Grahovac J, et al. Pioglitazone decreases portosystemic shunting by modulating inflammation and angiogenesis in cirrhotic and non-cirrhotic portal hypertensive rats. J Hepatol. 2014;60:1135–1142.
   PubMed Web of Science ®Google Scholar
• Bundscherer A, Reichle A, Hafner C, et al. Targeting the tumor stroma with peroxisome proliferator activated receptor (PPAR) agonists. ACAMC. 2009;9:816–821.
   Google Scholar
• Saremi A, Schwenke DC, Buchanan TA, et al. Pioglitazone slows progression of atherosclerosis in prediabetes independent of changes in cardiovascular risk factors. Arterioscler Thromb Vasc Biol. 2013;33:393–399.
   PubMed Web of Science ®Google Scholar
• Galli A, Crabb DW, Ceni E, et al. Antidiabetic thiazolidinediones inhibit collagen synthesis and hepatic stellate cell activation in vivo and in vitro. Gastroenterology. 2002;122:1924–1940.
   PubMed Web of Science ®Google Scholar
• Uto H, Nakanishi C, Ido A, et al. The peroxisome proliferator-activated receptor-gamma agonist, pioglitazone, inhibits fat accumulation and fibrosis in the livers of rats fed a choline-deficient, l-amino acid-defined diet. Hepatol Res. 2005;32:235–242.
   PubMed Web of Science ®Google Scholar
• Koc M, Taysi S, Buyukokuroglu ME, et al. Melatonin protects rat liver against irradiation-induced oxidative injury. J Radiat Res. 2003;44:211–215.
   PubMed Web of Science ®Google Scholar
• Cheng T-Y, Lee W-S, Huang H-C, et al. The effects of pioglitazone in cirrhotic rats with hepatopulmonary syndrome. J Chin Med Assoc. 2017;80:683–689.
   PubMed Web of Science ®Google Scholar
• Reitman S, Frankel S. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol. 1957;28:56–63.
   PubMed Web of Science ®Google Scholar
• Woessner JF. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys. 1961;93:440–447.
   PubMed Web of Science ®Google Scholar
• Xu Z-Y, Liang S-X, Zhu J, et al. Prediction of radiation-induced liver disease by Lyman normal-tissue complication probability model in three-dimensional conformal radiation therapy for primary liver carcinoma. Int J Radiat Oncol Biol Phys. 2006;65:189–195.
   PubMed Web of Science ®Google Scholar
• Xu P, Zhang X-g, Li Y-m, et al. Research on the protection effect of pioglitazone for non-alcoholic fatty liver disease (NAFLD) in rats. J Zhejiang Univ Sci B. 2006;7:627–633.
   PubMedGoogle Scholar
• Wong FL, Yamada M, Sasaki H, et al. Effect of radiation on the longitudinal trend of total serum cholesterol levels in the atomic bomb survivors. Radiat Res. 1999;151:736–746.
   PubMed Web of Science ®Google Scholar
• El-Missiry MA, Fayed TA, El-Sawy MR, et al. Ameliorative effect of melatonin against gamma-irradiation-induced oxidative stress and tissue injury. Ecotoxicol Environ Saf. 2007;66:278–286.
   PubMed Web of Science ®Google Scholar
• Abou-Zeid SM, El-Bialy BE, El-Borai NB, et al. Radioprotective effect of date syrup on radiation-induced damage in rats. Sci Rep. 2018;8:7423.
   PubMed Web of Science ®Google Scholar
• Nicholls SJ, Tuzcu EM, Wolski K, et al. Lowering the triglyceride/high-density lipoprotein cholesterol ratio is associated with the beneficial impact of pioglitazone on progression of coronary atherosclerosis in diabetic patients: insights from the PERISCOPE (pioglitazone Effect on Regression of Intravascular Sonographic Coronary Obstruction Prospective Evaluation) study. J Am Coll Cardiol. 2011;57:153–159.
   PubMed Web of Science ®Google Scholar
• Bhargava A, Gleason S, Vaughan AG, et al. The effect of pioglitazone and extended-release niacin on HDL-cholesterol in diabetes patients in a real-world setting. Int J Clin Pract. 2013;67:1151–1158.
   PubMed Web of Science ®Google Scholar
• Zhao W, Robbins ME. Inflammation and chronic oxidative stress in radiation-induced late normal tissue injury: therapeutic implications. CMC. 2009;16:130–143.
   PubMed Web of Science ®Google Scholar
• Pratheeshkumar P, Raphael TJ, Kuttan G. Protective role of perillic acid against radiation-induced oxidative stress, cytokine profile, DNA damage, and intestinal toxicity in mice. J Environ Pathol Toxicol Oncol. 2010;29:199–212.
   PubMed Web of Science ®Google Scholar
• Radwan RR, Mohamed HA. Nigella sativa oil modulates the therapeutic efficacy of mesenchymal stem cells against liver injury in irradiated rats. J Photochem Photobiol B Biol. 2018;178:447–456.
   PubMed Web of Science ®Google Scholar
• Pantano C, Reynaert NL, Vliet AVD, et al. Redox-sensitive kinases of the nuclear factor-kappaB signaling pathway. Antioxid Redox Signal. 2006;8:1791–1806.
   PubMed Web of Science ®Google Scholar
• Ha YM, Chung SW, Kim JM, et al. Molecular activation of NF-κB, pro-inflammatory mediators, and signal pathways in γ-irradiated mice. Biotechnol Lett. 2010;32:373–378.
   PubMed Web of Science ®Google Scholar
• Aldaba-Muruato LR, Moreno MG, Shibayama M, et al. Protective effects of allopurinol against acute liver damage and cirrhosis induced by carbon tetrachloride: modulation of NF-κB, cytokine production and oxidative stress. Biochim Biophys Acta. 2012;1820:65–75.
   PubMed Web of Science ®Google Scholar
• Collino M, Aragno M, Castiglia S, et al. Pioglitazone improves lipid and insulin levels in overweight rats on a high cholesterol and fructose diet by decreasing hepatic inflammation. Br J Pharmacol. 2010;160:1892–1902.
   PubMed Web of Science ®Google Scholar
• Jin X, Liu L, Zhou Z, et al. Pioglitazone alleviates inflammation in diabetic mice fed a high-fat diet via inhibiting advanced glycation end-product-induced classical macrophage activation. FEBS J. 2016;283:2295–2308.
   PubMed Web of Science ®Google Scholar
• Bull AW. The role of peroxisome proliferator-activated receptor gamma in colon cancer and inflammatory bowel disease. Arch Pathol Lab Med. 2003;127:1121–1123.
   PubMed Web of Science ®Google Scholar
• Shiojiri T, Wada K, Nakajima A, et al. PPAR gamma ligands inhibit nitrotyrosine formation and inflammatory mediator expressions in adjuvant-induced rheumatoid arthritis mice. Eur J Pharmacol. 2002;448:231–238.
   PubMed Web of Science ®Google Scholar
• Gorbunov NV, Pogue-Geile KL, Epperly MW, et al. Activation of the nitric oxide synthase 2 pathway in the response of bone marrow stromal cells to high doses of ionizing radiation. Radiat Res. 2000;154:73–86.
   PubMed Web of Science ®Google Scholar
• Li R, Xu L, Liang T, et al. Puerarin mediates hepatoprotection against CCL4-induced hepatic fibrosis rats through attenuation of inflammation response and amelioration of metabolic function. Food Chem Toxicol. 2013;52:69–75.
   PubMed Web of Science ®Google Scholar
• Zorrilla Zubilete MA, Ríos H, Silberman DM, et al. Altered nitric oxide synthase and PKC activities in cerebellum of gamma-irradiated neonatal rats. Brain Res. 2005;1051:8–16.
   PubMed Web of Science ®Google Scholar
• Nishio K, Shigemitsu M, Kodama Y, et al. The effect of pioglitazone on nitric oxide synthase in patients with type 2 diabetes mellitus. J Cardiometab Syndr. 2008;3:200–204.
   PubMedGoogle Scholar
• Dehmer T, Heneka MT, Sastre M, et al. Protection by pioglitazone in the MPTP model of Parkinson’s disease correlates with IκBα induction and block of NFκB and iNOS activation. J Neurochem. 2003;88:494–501.
   Web of Science ®Google Scholar
• Wu J, Zern MA. Hepatic stellate cells: a target for the treatment of liver fibrosis. J Gastroenterol. 2000;35:665–672.
   PubMed Web of Science ®Google Scholar
• Hu Z, Qin F, Gao S, et al. Paeoniflorin exerts protective effect on radiation-induced hepatic fibrosis in rats via TGF-β1/Smads signaling pathway. Am J Transl Res. 2018;10:1012–1021.
   PubMed Web of Science ®Google Scholar
• Yuan GJ, Zhang ML, Gong ZJ. Effects of PPARg agonist pioglitazone on rat hepatic fibrosis. World J Gastroenterol. 2004;10:1047–1051.
   PubMed Web of Science ®Google Scholar
• Boettcher E, Csako G, Pucino F, et al. Meta-analysis: pioglitazone improves liver histology and fibrosis in patients with non-alcoholic steatohepatitis. Aliment Pharmacol Ther. 2012;35:66–75.
   PubMed Web of Science ®Google Scholar
• Hessin A, Hegazy R, Hassan A, et al. Lactoferrin enhanced apoptosis and protected against thioacetamide-induced liver fibrosis in rats. Open Access Maced J Med Sci. 2015;3:195–201.
   PubMedGoogle Scholar
• Cheng W, Xiao L, Ainiwaer A, et al. Molecular responses of radiation-induced liver damage in rats. Mol Med Rep. 2015;11:2592–2600.
   PubMed Web of Science ®Google Scholar
• Hong S-W, Jung KH, Zheng H-M, et al. The protective effect of resveratrol on dimethyl nitrosamine-induced liver fibrosis in rats. Arch Pharm Res. 2010;33:601–609.
   PubMed Web of Science ®Google Scholar
• Meng XM, Nikolic-Paterson DJ, Lan HY. TGF-β: the master regulator of fibrosis. Nat Rev Nephrol. 2016;12:325–338.
   PubMed Web of Science ®Google Scholar
• Dancea HC, Shareef MM, Ahmed MM. Role of radiation-induced TGF-beta signaling in cancer therapy. Mol Cell Pharmacol. 2009;1:44–56.
   PubMedGoogle Scholar
• Peters CA, Stock RG, Cesaretti JA, et al. TGFβ1 single nucleotide polymorphisms are associated with adverse quality of life in prostate cancer patients treated with radiotherapy. Int J Radiat Oncol Biol Phys. 2008;70:752–759.
   PubMed Web of Science ®Google Scholar
• Haydont V, Riser BL, Aigueperse J, et al. Specific signals involved in the long-term maintenance of radiation-induced fibrogenic differentiation: a role for CCN2 and low concentration of TGF-beta1. Am J Physiol Cell Physiol. 2008;294:C1332–C1341.
   PubMed Web of Science ®Google Scholar
• Bartram U, Speer CP. The role of transforming growth factor beta in lung development and disease. Chest. 2004;125:754–765.
   PubMed Web of Science ®Google Scholar
• Tsuchiya S, Amano Y, Isono O, et al. Pharmacological evaluation of pioglitazone and candesartan cilexetil in a novel mouse model of non-alcoholic steatohepatitis, modified choline-deficient, amino acid-defined diet fed low-density lipoprotein receptor knockout mice. Hepatol Res. 2017;47:584–592.
   PubMed Web of Science ®Google Scholar