Oxidative Stress and Antioxidant Biomarkers in Clinical and Experimental Models of Non-Alcoholic Fatty Liver Disease

Ayokanmi Ore, Oluseyi Adeboye Akinloye, Ayokanmi Ore, Oluseyi Adeboye Akinloye

Abstract

Non-alcoholic fatty liver disease (NAFLD) is a term that covers a range of hepatic disorders involving fat deposits in the liver. NAFLD begins with simple steatosis and progresses into non-alcoholic steatohepatitis (NASH) characterised by inflammation, fibrosis, apoptosis, oxidative stress, lipid peroxidation, mitochondrial dysfunction and release of adipokines and pro-inflammatory cytokines. Oxidative stress and antioxidants are known to play a vital role in the pathogenesis and severity of NAFLD/NASH. A number of oxidative stress and antioxidant markers are employed in the assessment of the pathological state and progression of the disease. In this article, we review several biomarkers of oxidative stress and antioxidants that have been measured at clinical and experimental levels. Also included is a comprehensive description of oxidative stress, sources and contribution to the pathogenesis of NAFLD/NASH.

Keywords: NAFLD; NASH; antioxidants; biomarkers; lipid peroxidation; liver; oxidative stress; reactive species.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Pathophysiology of NASH and the multi-hit hypothesis.

References

    1. Angulo P. Non-alcoholic fatty liver disease. N. Engl. J. Med. 2002;346:1221–1231. doi: 10.1056/NEJMra011775.
    1. Manne V., Handa P., Kowdley K.V. Pathophysiology of Nonalcoholic Fatty Liver Disease/Nonalcoholic Steatohepatitis. Clin. Liver Dis. 2018;22:23–37. doi: 10.1016/j.cld.2017.08.007.
    1. Ludwig J., Viggiano T.R., McGill D.B., Oh B.J. Non-alcoholic steatohepatitis: Mayo clinic experiences with a hitherto unnamed disease. Mayo Clin. Proc. 1980;55:434–438.
    1. Kim W.R., Lake J.R., Smith J.M., Skeans M.A., Schladt D.P., Edwards E.B., Harper A.M., Wainright J.L., Snyder J.J., Israni A.K., et al. OPTN/SRTR 2015 Annual Data Report: Liver. Am. J. Transplant. 2017;17:174–251. doi: 10.1111/ajt.14126.
    1. European Association for the Study of Liver (EASL) Background Media Information: Fast facts about liver disease. Int. Liver Congr. 2016:1–5.
    1. Day C.P., James O. Steatohepatitis: A tale of two ‘hits’? Gastroenterol. 1998;114:842–845. doi: 10.1016/S0016-5085(98)70599-2.
    1. Buzzetti E., Pinzani M., Tsochatzis E.A. The multiple-hit pathogenesis of nonalcoholic fatty liver disease (NAFLD) Metabolism. 2016;65:1038–1048. doi: 10.1016/j.metabol.2015.12.012.
    1. Dongiovanni P., Anstee Q.M., Valenti L. Genetic Predisposition in NAFLD and NASH: Impact on Severity of Liver Disease and Response to Treatment. Curr. Pharm. Des. 2013;19:5219–5238. doi: 10.2174/13816128113199990381.
    1. Sies H., Berndt C., Jones D.C. Oxidative stress. Annu. Rev. Biochem. 2017;86:715–748. doi: 10.1146/annurev-biochem-061516-045037.
    1. Sies H. On the history of oxidative stress: Concept and some aspects of current development. Curr. Opin. Toxicol. 2018;7:122–126. doi: 10.1016/j.cotox.2018.01.002.
    1. Lushchak V.I. Free radicals, reactive oxygen species, oxidative stress and its classification. Chem. Biol. Interact. 2014;224C:164–175. doi: 10.1016/j.cbi.2014.10.016.
    1. Li S., Hong M., Tan H., Wang N., Feng Y. Insights into the Role and Interdependence of Oxidative Stress and Inflammation in Liver Diseases. Oxid. Med. Cell. Longev. 2016:1–21. doi: 10.1155/2016/4234061.
    1. Li S., Tan H., Wang N., Zhang Z., Lao L., Wong C., Feng Y. The Role of Oxidative Stress and Antioxidants in Liver Diseases. Int. J. Mol. Sci. 2015;16:26087–26124. doi: 10.3390/ijms161125942.
    1. Cichoż-Lach H., Michalak A. Oxidative stress as a crucial factor in liver diseases. World J. Gastroenterol. 2014;20:8082–8091. doi: 10.3748/wjg.v20.i25.8082.
    1. Muriel P. Role of free radicals in liver diseases. Hepatol. Int. 2009;3:526–536. doi: 10.1007/s12072-009-9158-6.
    1. Barzilai A., Yamamoto K. DNA damage responses to oxidative stress. Dna Repair. 2004;3:1109–1115. doi: 10.1016/j.dnarep.2004.03.002.
    1. d’Ischia M., Manini P., Napolitano A. Oxidative Stress, Disease and Cancer. Word Scientific; Singapore: 2006. Oxidative Damage to Carbohydrates and Amino Acids; pp. 333–356.
    1. Hassan H.A., El-Aal M.A. Lipid Peroxidation End-Products as a Key of Oxidative Stress: Effect of Antioxidant on Their Production and Transfer of Free Radicals. In: Catala A., editor. Lipid Peroxidation. InTech; Rijeka, Croatia: 2012. pp. 63–88.
    1. Sitte N. Oxidative Damage to Proteins. In: Zglinicki T., editor. Aging at the Molecular Level. Springer-Science; Newcastle, UK: 2003.
    1. Gackowski D., Speina E., Zielinska M., Kowalewski J., Rozalski R., Siomek A., Paciorek T., Tudek B., Olinski R. Products of oxidative DNA damage and repair as possible biomarkers of susceptibility to lung cancer. Cancer Res. 2003;15:4899–4902.
    1. Nishida N., Arizumi T., Takita M., Kitai S., Yada N., Hagiwara S., Inoue T., Minami Y., Ueshima K., Sakurai T., et al. Reactive oxygen species induce epigenetic instability through the formation of 8-hydroxydeoxyguanosine in human hepatocarcinogenesis. Dig. Dis. 2013;31:459–466. doi: 10.1159/000355245.
    1. Simioni C., Zauli G., Martelli A.M., Vitale M., Sacchetti G., Gonelli A., Neri L.M. Oxidative stress: Role of physical exercise and antioxidant nutraceuticals in adulthood and aging. Oncotarget. 2018;9:17181–17198. doi: 10.18632/oncotarget.24729.
    1. Valko M., Leibfritz D., Moncola J., Cronin M.T.D., Mazura M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007;39:44–84. doi: 10.1016/j.biocel.2006.07.001.
    1. Koek G.H., Liedorp P.R., Bast A. The role of oxidative stress in non-alcoholic steatohepatitis. Clin. Chim. Acta. 2011;412:1297–1305. doi: 10.1016/j.cca.2011.04.013.
    1. Tariq Z., Green C.J., Hodson L. Are oxidative stress mechanisms the common denominator in the progression from hepatic steatosis towards non-alcoholic steatohepatitis (NASH)? Liver Int. 2014;34:180–190. doi: 10.1111/liv.12523.
    1. Serviddio G., Sastre J., Bellanti F., Viña J., Vendemiale G., Altomare E. Mitochondrial involvement in non-alcoholic steatohepatitis. Mol. Asp. Med. 2008;29:22–35. doi: 10.1016/j.mam.2007.09.014.
    1. Vendemiale G., Grattagliano I., Caraceni P., Caraccio G., Domenicali M., Dall’Agata M., Trevisani F., Guerrieri F., Bernardi M., Altomare E. Mitochondrial oxidative injury and energy metabolism alteration in rat fatty liver: Effect of the nutritional status. Hepatology. 2001;33:808–815. doi: 10.1053/jhep.2001.23060.
    1. Satapati S., Kucejova B., Duarte J.A., Fletcher J.A., Reynolds L., Sunny N.E., He T., Nair L.A., Livingston K.A., Fu X., et al. Mitochondrial metabolism mediates oxidative stress and inflammation in fatty liver. J. Clin. Investig. 2015;125:4447–4462. doi: 10.1172/JCI82204.
    1. Haque M., Sanya A.J. The metabolic abnormalities associated with non-alcoholic fatty liver disease. Best Pract. Res. Clin. Gastroenterol. 2002;16:709–731. doi: 10.1053/bega.2002.0325.
    1. Angulo P., Lindor K.D. Insulin resistance and mitochondrial abnormalities in NASH: A cool look into a burning issue. Gastroenterology. 2001;120:1281–1285. doi: 10.1053/gast.2001.23591.
    1. Gonzalez F.J., Peters J.M., Cattley R.C. Mechanism of action of the nongenotoxic peroxisome proliferators: Role of the peroxisome proliferator-activator receptor alpha. J. Natl. Cancer Inst. 1998;90:1702–1709. doi: 10.1093/jnci/90.22.1702.
    1. Pessayre D., Mansouri A., Fromenty B. Nonalcoholic steatosis and steatohepatitis. V. Mitochondrial dysfunction in steatohepatitis. Am. J. Physiol. Gastrointest. Liv. Physiol. 2002;282:193–199. doi: 10.1152/ajpgi.00426.2001.
    1. Caldwell S.H., Swerdlow R.H., Khan E.M., Iezzoni J.C., Hespenheide E.E., Parks J.K., Parker W.D. Mitochondrial abnormalities in non-alcoholic steatohepatitis. J. Hepatol. 1999;31:430–434. doi: 10.1016/S0168-8278(99)80033-6.
    1. Weltman M.D., Farrell G.C., Hall P., Ingelman-Sundberg M., Liddle C. Hepatic cytochrome P450 2E1 is increased in patients with nonalcoholic steatohepatitis. Hepatology. 1998;27:128–133. doi: 10.1002/hep.510270121.
    1. Chalasani N., Gorski J.C., Asghar M.S., Asghar A., Foresman B., Hall S.D., Crabb D.W. Hepatic cytochrome P450 2E1 activity in nondiabetic patients with nonalcoholic steatohepatitis. Hepatology. 2003;37:544–550. doi: 10.1053/jhep.2003.50095.
    1. Matsunami T., Sato Y., Ariga S., Sato T., Kashimura H., Hasegawa Y., Yukawa M. Regulation of oxidative stress and inflammation by hepatic adiponectin receptor 2 in an animal model of nonalcoholic steatohepatitis. Int. J. Clin. Exp. Pathol. 2010;22:472–481.
    1. Leclercq A., Farrell G.C., Field J., Bell D.R., Gonzalez F.J., Robertson G.R. CYP2E1 and CYP4A as microsomal catalysts of lipid peroxides in murine nonalcoholic steatohepatitis. J. Clin. Investig. 2000;105:1067–1075. doi: 10.1172/JCI8814.
    1. Yang L., Jhaveri R., Huang J. Endoplasmic reticulum stress, hepatocyte CD1 and NKT cell abnormalities in murine fatty livers. Lab. Investig. 2007;87:927–937. doi: 10.1038/labinvest.3700603.
    1. Sakuma S., Negoro M., Kitamura T., Fujimoto Y. Xanthine oxidase-derived reactive oxygen species mediate 4-oxo-2-nonenal-induced hepatocyte cell death. Toxicol. Appl. Pharmacol. 2010;249:127–131. doi: 10.1016/j.taap.2010.08.025.
    1. Baskol G., Baskol M., Kocer D. Oxidative stress and antioxidant defenses in serum of patients with non-alcoholic steatohepatitis. Clin. Biochem. 2007;40:776–780. doi: 10.1016/j.clinbiochem.2007.02.006.
    1. Crespo J., Cayon A., Fernandez-Gil P., Hernández-Guerra M., Mayorga M., Domínguez-Díez A., Fernández-Escalante J.C., Pons-Romero F. Gene expression of tumor necrosis factor alpha and TNF-receptors, p55 and p75, in nonalcoholic steatohepatitis patients. Hepatology. 2001;34:1158–1163. doi: 10.1053/jhep.2001.29628.
    1. Imajo K., Fujita K., Yoneda M., Nozaki Y., Ogawa Y., Shinohara Y., Kato S., Mawatari H., Shibata W., Kitani H., et al. Hyperresponsivity to low-dose endotoxin during progression to nonalcoholic steatohepatitis is regulated by leptin-mediated signaling. Cell Metab. 2012;16:44–54. doi: 10.1016/j.cmet.2012.05.012.
    1. Dostert K., Dorn C., Weiss T., Gabele E., Hellerbrand C. Enhanced TLR4 expression in steatotic hepatocytes. Z. Gastroenterol. 2012;50:1–11. doi: 10.1055/s-0031-1295741.
    1. Ucar F., Sezer S., Erdogan S., Akyol S., Armutcu F., Akyol O. The relationship between oxidative stress and nonalcoholic fatty liver disease: Its effects on the development of nonalcoholic steatohepatitis. Redox Rep. 2013;18:127–133. doi: 10.1179/1351000213Y.0000000050.
    1. Gambino R., Musso G., Cassader M. Redox Balance in the Pathogenesis of Nonalcoholic Fatty Liver Disease: Mechanisms and Therapeutic Opportunities. Antioxid. Redox Signal. 2011;15:1325–1365. doi: 10.1089/ars.2009.3058.
    1. Rolo A.P., Teodoro J.S., Palmeira C.M. Role of oxidative stress in the pathogenesis of nonalcoholic steatohepatitis. Free Radic. Biol. Med. 2012;52:59–69. doi: 10.1016/j.freeradbiomed.2011.10.003.
    1. Stiuso P., Scognamiglio I., Murolo M., Ferranti P., De Simone C., Rizzo M.R., Tuccillo C., Caraglia M., Loguercio C., Federico A. Serum Oxidative Stress Markers and Lipidomic Profile to Detect NASH Patients Responsive to an Antioxidant Treatment: A Pilot Study. Oxidat. Med. Cell. Longev. 2014;2014:1–8. doi: 10.1155/2014/169216.
    1. Leghi G.E., Domenici F.A., Vannucchi H. Influence of oxidative stress and obesity in patients with nonalcoholic steatohepatitis. ARQ Gastroenterol. 2015;52:228–233. doi: 10.1590/S0004-28032015000300014.
    1. Koruk M., Taysi S., Savas M.C., Yilmaz O., Akcay F., Karakok M. Oxidative stress and enzymatic antioxidant status in patients with nonalcoholic steatohepatitis. Ann. Clin. Lab. Sci. 2004;34:57–62.
    1. Köroğlu E., Canbakan B., Atay K., Hatemi I., Tuncer M., Dobrucalı A., Sonsuz A., Gültepe I., Şentürk H. Role of oxidative stress and insulin resistance in disease severity of non-alcoholic fatty liver disease. Turk. J. Gastroenterol. 2016;27:361–366. doi: 10.5152/tjg.2016.16106.
    1. Yesilova Z., Yaman H., Oktenli C., Ozcan A., Uygun A., Cakir E., Sanisoglu S.Y., Erdil A., Ates Y., Aslan M., et al. Systemic markers of lipid peroxidation and antioxidants in patients with nonalcoholic Fatty liver disease. Am. J. Gastroenterol. 2005;100:850–855. doi: 10.1111/j.1572-0241.2005.41500.x.
    1. Ergün Y., Kurutaş E.B., Özdil B., Güneşaçar R., Ergün Y. Nitric Oxide and Nitrotyrosine Levels in Relation with Oxidative Stress-Related Markers in Non-Alcoholic Fatty Liver Disease. Turk. Klin. J. Gastroenterohepatol. 2011;18:1–8.
    1. Videla L.A., Rodrigo R., Orellana M., Fernandez V., Tapia G., Quiñones L., Varela N., Contreras J., Lazarte R., Csendes A., et al. Oxidative stress-related parameters in the liver of non-alcoholic fatty liver disease patients. Clin. Sci. 2004;106:261–268. doi: 10.1042/CS20030285.
    1. Kumar A., Sharma A., Duseja A., Das A., Dhiman R.K., Chawla Y.K., Kohli K.K., Bhansali A. Patients with Nonalcoholic Fatty Liver Disease (NAFLD) have Higher Oxidative Stress in Comparison to Chronic Viral Hepatitis. J. Clin. Exp. Hepatol. 2013;3:12–28. doi: 10.1016/j.jceh.2012.10.009.
    1. Sumida Y., Nakashima T., Yoh T., Furutani M., Hirohama A., Kakisaka Y., Nakajima Y., Ishikawa H., Mitsuyoshi H., Okanoue T., et al. Serum thioredoxin levels as a predictor of steatohepatitis in patients with nonalcoholic fatty liver disease. J. Hepatol. 2003;38:32–38. doi: 10.1016/S0168-8278(02)00331-8.
    1. Salomone F., Volti G.L., Rosso C., Grosso G., Bugianesi E. Unconjugated bilirubin, a potent endogenous antioxidant, is decreased in patients with nonalcoholic steatohepatitis and advanced fibrosis. J. Gastroenterol. Hepatol. 2013;28:1202–1208. doi: 10.1111/jgh.12155.
    1. Hjelkrem M., Morales A., Williams C.D., Harrison S.A. Unconjugated hyperbilirubinemia is inversely associated with non-alcoholic steatohepatitis (NASH) Aliment. Pharmacol. Ther. 2012;35:1416–1423. doi: 10.1111/j.1365-2036.2012.05114.x.
    1. Kumar R., Rastogi A., Maras J.S., Sarin S.K. Unconjugated hyperbilirubinemia in patients with non-alcoholic fatty liver disease: A favorable endogenous response. Clin. Biochem. 2012;45:272–274. doi: 10.1016/j.clinbiochem.2011.11.017.
    1. Horoz M., Bolukbas C., Bolukbas F.F., Sabuncu T., Aslan M., Sarifakiogullari S., Gunaydin N., Erel O. Measurement of the total antioxidant response using a novel automated method in subjects with nonalcoholic steatohepatitis. BMC Gastroenterol. 2005;5:35. doi: 10.1186/1471-230X-5-35.
    1. Farhan A.R. Evaluation of Melatonin Hormone and Nitric oxide Levels in Non-alcoholic Fatty Liver Patients in Relation to Obesity and Oxidative Stress. J. Pharm. Sci. Res. 2018;10:1167–1169.
    1. Loguercio C., De Girolamo V., de Sio I., Tuccillo C., Ascione A., Baldi F., Budillon G., Cimino L., Di Carlo A., Di Marino M.P., et al. Non-alcoholic fatty liver disease in an area of southern Italy: Main clinical, histological, and pathophysiological aspects. J. Hepatol. 2001;35:568–574. doi: 10.1016/S0168-8278(01)00192-1.
    1. Oliveira C.P., Faintuch J., Rascovski A., Furuya C.K., Jr., Bastos M.S., Matsuda M., Della Nina B.I., Yahnosi K., Abdala D.S., Vezozzo D.C., et al. Lipid peroxidation in bariatric candidates with nonalcoholic fatty liver disease (NAFLD)—Preliminary findings. Obes. Surg. 2005;15:502–505. doi: 10.1381/0960892053723493.
    1. Seki S., Kitada T., Yamada T., Sakaguchi H., Nakatani K., Wakasa K. In situ detection of lipid peroxidation and oxidative DNA damage in non-alcoholic fatty liver diseases. J. Hepatol. 2002;37:56–62. doi: 10.1016/S0168-8278(02)00073-9.
    1. Fujita N., Miyachi H., Tanaka H., Takeo M., Nakagawa N., Kobayashi Y., Iwasa M., Watanabe S., Takei Y. Iron overload is associated with hepatic oxidative damage to DNA in nonalcoholic steatohepatitis. Cancer Epidemiol. Biomark. Prev. 2009;18:424–432. doi: 10.1158/1055-9965.EPI-08-0725.
    1. Nobili V., Parola M., Alisi A., Marra F., Piemonte F., Mombello C., Sutti S., Povero D., Maina V., Novo E., et al. Oxidative stress parameters in paediatric non-alcoholic fatty liver disease. Int. J. Mol. Med. 2010;26:471–476. doi: 10.3892/ijmm_00000487.
    1. Chtioui H., Semela D., Ledermann M., Zimmermann A., Dufour J.F. Expression and activity of the cytochrome P450 2E1 in patients with non-alcoholic steatosis and steatohepatitis. Liver Int. 2007;27:764–771. doi: 10.1111/j.1478-3231.2007.01524.x.
    1. Yoshioka S., Hamada A., Jobu K., Yokota J., Onogawa M., Kyotani S., Miyamura M., Saibara T., Onishi S., Nishioka Y. Effects of Eriobotrya japonica seed extract on oxidative stress in rats with non-alcoholic steatohepatitis. J. Pharm. Pharmacol. 2010;62:241–246. doi: 10.1211/jpp.62.02.0012.
    1. Marcolin E., Forgiarini L.F., Rodrigues G., Tieppo J., Borghetti G.S., Bassani V.L., Picada J.N., Marroni N.P. Quercetin Decreases Liver Damage in Mice with Non-Alcoholic Steatohepatitis. Basic Clin. Pharmacol. Toxicol. 2013;112:385–391. doi: 10.1111/bcpt.12049.
    1. Marcolin E., Forgiarini L.F., Tieppo J., Dias A.S., Freitas L.A.R., Marroni N.P. Methione- and choline-deficient diet induces hepatic changes characteristic of non-alcoholic steatohepatitis. Arq. Gastroenterol. 2011;48:72–79. doi: 10.1590/S0004-28032011000100015.
    1. Nan Y.M., Wu W.J., Fu N., Liang B.L., Wang R.Q., Li L.X., Zhao S.X., Zhao J.M., Yu J. Antioxidants vitamin E and 1-aminobenzotriazole prevent experimental non-alcoholic steatohepatitis in mice. Scand. J. Gastroenterol. 2009;44:1121–1131. doi: 10.1080/00365520903114912.
    1. Nosrati N., Aghazadeh S., Yazdanparast R. Effects of Teucrium polium on Insulin Resistance in Nonalcoholic Steatohepatitis. J. Acupunct. Meridian Stud. 2010;3:104–110. doi: 10.1016/S2005-2901(10)60019-2.
    1. Huang F., Wang J., Yu F., Tang Y., Ding G., Yang Z., Sun Y. Protective Effect of Meretrix meretrix Oligopeptides on High-Fat-Diet-Induced Non-Alcoholic Fatty Liver Disease in Mice. Mar. Drugs. 2018;16:39. doi: 10.3390/md16020039.
    1. Li W., Lu Y. Hepatoprotective Effects of Sophoricoside against Fructose-Induced Liver Injury via Regulating Lipid Metabolism, Oxidation, and Inflammation in Mice. J. Food Sci. 2018;83:552–558. doi: 10.1111/1750-3841.14047.
    1. Song L., Qu D., Zhang Q., Jiang J., Zhou H., Jiang R., Li Y., Zhang Y., Yan H. Phytosterol esters attenuate hepatic steatosis in rats with nonalcoholic fatty liver disease rats fed a high-fat diet. Sci. Rep. 2017;7:41604. doi: 10.1038/srep41604.
    1. Korish A.A., Arafah M.M. Camel milk ameliorates steatohepatitis, insulin resistance and lipid peroxidation in experimental non-alcoholic fatty liver disease. BMC Complement. Altern. Med. 2013;13:264–276. doi: 10.1186/1472-6882-13-264.
    1. Elshazly S.M. Ameliorative effect of nicorandil on high fat diet induced non-alcoholic fatty liver disease in rats. Eur. J. Pharmacol. 2015;748:123–132. doi: 10.1016/j.ejphar.2014.12.017.
    1. Janevski M., Antonas K.N., Sullivan-Gunn M.J., McGlynn M.A., Lewandowski P.A. The effect of cocoa supplementation on hepatic steatosis, reactive oxygen species and LFABP in a rat model of NASH. Comp. Hepatol. 2011;10:10. doi: 10.1186/1476-5926-10-10.
    1. Caballero F., Fernández A., Matías N., Martínez L., Fucho R., Elena M., Caballeria J., Morales A., Fernández-Checa J.C., García-Ruiz C. Specific Contribution of Methionine and Choline in Nutritional Nonalcoholic Steatohepatitis. J. Biol. Chem. 2010;285:18528–18536. doi: 10.1074/jbc.M109.099333.
    1. Schröder T., Kucharczyk D., Bär F., Page R., Derer S., Jendrek T., Sünderhauf A., Brethack A.K., Hirose M., Möller S., et al. Mitochondrial gene polymorphisms alter hepatic cellular energy metabolism and aggravate diet-induced non-alcoholic steatohepatitis. Mol. Metab. 2016;5:283–295. doi: 10.1016/j.molmet.2016.01.010.
    1. Sutti S., Jindal A., Locatelli I., Vacchiano M., Gigliotti L., Bozzola C., Albano E. Adaptive Immune Responses Triggered by Oxidative Stress Contribute to Hepatic Inflammation in NASH. Hepatology. 2014;59:886–897. doi: 10.1002/hep.26749.
    1. Nazmy M.H., Abdel-Ghany M.I. Serum markers versus histopathological scoring for discrimination between experimental fatty liver and non-alcoholic steatohepatitis. Int. Res. J. Med. Med. Sci. 2015;3:51–59.
    1. Sugatani J., Wada T., Osabe M., Yamakawa K., Yoshinari K., Miwa M. Dietary Inulin Alleviates Hepatic Steatosis and Xenobiotics-Induced Liver Injury in Rats Fed a High-Fat and High-Sucrose Diet: Association with the Suppression of Hepatic Cytochrome P450 and Hepatocyte Nuclear Factor 4α Expression. Drug Metab. Dispos. 2006;34:1677–1687. doi: 10.1124/dmd.106.010645.
    1. Takahashi Y., Sugimoto K., Soejima Y., Kumagai A., Koeda T., Shojo A., Nakagawa K., Harada N., Yamaji R., Inui H., et al. Inhibitory Effects of Eucalyptus and Banaba Leaf Extracts on Nonalcoholic Steatohepatitis Induced by a High-Fructose/High-Glucose Diet in Rats. Biomed. Res. Int. 2015;2015:1–9. doi: 10.1155/2015/296207.
    1. Watanabe M., Fuda H., Okabe H., Joko S., Miura Y., Hui S., Hamaoka Y.N., Miki E., Chiba H. Oyster extracts attenuate pathological changes in non-alcoholic steatohepatitis (NASH) mouse model. J. Funct. Foods. 2016;20:516–531. doi: 10.1016/j.jff.2015.11.029.
    1. Ji G., Wang Y., Deng Y., Li X., Jiangm Z. Resveratrol ameliorates hepatic steatosis and inflammation in methionine/choline deficient diet-induced steatohepatitis through regulating autophagy. Lipids Health Dis. 2015;14:134. doi: 10.1186/s12944-015-0139-6.
    1. Sakaida I., Okita K. The role of oxidative stress in NASH and fatty liver model. Hepatol. Res. 2005;33:128–131. doi: 10.1016/j.hepres.2005.09.019.
    1. Nakamoto K., Takayama F., Mankura M., Hidaka Y., Egashira T., Ogino T., Kawasaki H., Morim A. Beneficial effects of fermented green tea extract in a rat model of non-alcoholic steatohepatitis. J. Clin. Biochem. Nutr. 2009;44:239–246. doi: 10.3164/jcbn.08-256.
    1. Lieber C.S., Leo M.A., Mak K.M., Xu Y., Cao Q., Ren C., Ponomarenko A., DeCarli L.M. Model of nonalcoholic steatohepatitis. Am. J. Clin. Nutr. 2004;79:502–509. doi: 10.1093/ajcn/79.3.502.
    1. Chung M.Y., Park H.J., Manautou J.E., Koo S.I., Bruno R.S. Green tea extract protects against nonalcoholic steatohepatitis in ob/ob mice by decreasing oxidative and nitrative stress responses induced by proinflammatory enzymes. J. Nutr. Biochem. 2012;23:361–367. doi: 10.1016/j.jnutbio.2011.01.001.
    1. Verbeek J., Spincemaille P., Vanhorebeek I., Van den Berghe G., Vander Elst I., Windmolders P., van Pelt J., van der Merwe S., Bedossa P., Nevens F., et al. Dietary intervention, but not losartan, completely reverses non-alcoholic steatohepatitis in obese and insulin resistant mice. Lipids Health Dis. 2017;23:46–56. doi: 10.1186/s12944-017-0432-7.
    1. Lee S.J., Kang J.H., Iqbal W., Kwon O.S. Proteomic Analysis of Mice Fed Methionine and Choline Deficient Diet Reveals Marker Proteins Associated with Steatohepatitis. PLoS ONE. 2015;10:e0120577. doi: 10.1371/journal.pone.0120577.
    1. Jung Y.A., Choi Y.K., Jung G.S., Seo H.Y., Kim H.S., Jang B.K., Kim J.G., Lee I.K., Kim M.K., Park K.G. Sitagliptin attenuates methionine/choline-deficient diet-induced steatohepatitis. Diabetes Res. Clin. Pract. 2014;105:47–57. doi: 10.1016/j.diabres.2014.04.028.
    1. Kathirve E., Chen P., Morgan K., French S.W., Morgan T.R. Oxidative stress and regulation of anti-oxidant enzymes in cytochrome P4502E1 transgenic mouse model of non-alcoholic fatty liver. J. Gastroenterol. Hepatol. 2010;25:1136–1143. doi: 10.1111/j.1440-1746.2009.06196.x.
    1. Lieber C.S., Leo M.A., Mak K.M., Xu Y., Cao Q., Ren C., Ponomarenko A., DeCarli L.M. Acarbose attenuates experimental non-alcoholic steatohepatitis. Biochem. Biophys. Res. Commun. 2004;12:699–703. doi: 10.1016/j.bbrc.2004.01.116.
    1. Wang Y., Ausman L.M., Greenberg A.S., Russell R.M., Wang X. Dietary lycopene and tomato extract supplementations inhibit nonalcoholic steatohepatitis-promoted hepatocarcinogenesis in rats. Int. J. Cancer. 2010;126:1788–1796. doi: 10.1002/ijc.24689.
    1. Murakami S., Takayama F., Egashira T., Imao M., Mori A. Fermented papaya preparation halts the progression of non-alcoholic steatohepatitis in rats. J. Biophys. Chem. 2013;4:84–90. doi: 10.4236/jbpc.2013.42012.

Source: PubMed

3
購読する