A review of the therapeutic effects of polyphenols on non-alcoholic fatty liver disease: Focus on oxidative stress
Abstract
A large amount of research suggests that polyphenols may have health benefits, particularly in metabolic disorders associated with obesity, such as non-alcoholic fatty liver (NAFLD), type 2 diabetes, and cardiovascular disease. Because of the importance of oxidative stress in the pathogenesis of metabolic disorders, great emphasis has recently been paid to the characteristics of polyphenols in obesity-related problems. This narrative review summarizes the current knowledge on the inhibitory effects of polyphenols, including curcumin, resveratrol, baicalin, nobiletin, and quercetin, on oxidative stress by focusing on the role of the Nrf2 pathway. This review gathered the data of the articles showing that the aforementioned polyphenols improve health in metabolic diseases via regulating Nrf2 and its target proteins involved in ameliorating oxidative stress. However, due to the limitations of in vitro and in vivo investigations, as well as lack of long-term human clinical trial trials studies, further high-quality research is required to definitively show polyphenols’ clinical usefulness for the prevention and management of NAFLD.
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7. Schuppan D, Schattenberg JM. Non-alcoholic steatohepatitis: pathogenesis and novel therapeutic approaches. J Gastroenterol Hepatol. 2013;28 Suppl 1:68-76.
8. Angulo P. Long-term mortality in nonalcoholic fatty liver disease: is liver histology of any prognostic significance? Hepatology. 2010;51(2):373-5.
9. Yu J, Marsh S, Hu J, Feng W, Wu C. The Pathogenesis of Nonalcoholic Fatty Liver Disease: Interplay between Diet, Gut Microbiota, and Genetic Background. Gastroenterol Res Pract. 2016;2016:2862173.
10. Zamani‐Garmsiri F, Ghasempour G, Aliabadi M, Hashemnia SMR, Emamgholipour S, Meshkani R. Combination of metformin and chlorogenic acid attenuates hepatic steatosis and inflammation in high‐fat diet fed mice. IUBMB life. 2021;73(1):252-63.
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24. de Araújo FF, de Paulo Farias D, Neri-Numa IA, Pastore GM. Polyphenols and their applications: An approach in food chemistry and innovation potential. Food Chem. 2021;338:127535.
25. Abenavoli L, Milic N, Luzza F, Boccuto L, De Lorenzo A. Polyphenols Treatment in Patients with Nonalcoholic Fatty Liver Disease. J Transl Int Med. 2017;5(3):144-7.
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30. Jafarzadeh E, Shoeibi S, Bahramvand Y, Nasrollahi E, Maghsoudi AS, Yazdi F, et al. Turmeric for treatment of irritable bowel syndrome: a systematic review of population-based evidence. Iranian Journal of Public Health. 2022;51(6):1223.
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32. Lee SC, Jee SC, Kim M, Kim S, Shin MK, Kim Y, et al. Curcumin Suppresses the Lipid Accumulation and Oxidative Stress Induced by Benzo[a]pyrene Toxicity in HepG2 Cells. Antioxidants (Basel). 2021;10(8).
33. Yu Q, Liu Y, Wu Y, Chen Y. Dihydrocurcumin ameliorates the lipid accumulation, oxidative stress and insulin resistance in oleic acid-induced L02 and HepG2 cells. Biomed Pharmacother. 2018;103:1327-36.
34. Yan C, Zhang Y, Zhang X, Aa J, Wang G, Xie Y. Curcumin regulates endogenous and exogenous metabolism via Nrf2-FXR-LXR pathway in NAFLD mice. Biomed Pharmacother. 2018;105:274-81.
35. Zakaria SS, ElBatsh MM, Mowafy SE. Effects of curcumin on autophagy and Nrf2 signaling pathway in a rat model of high fructose diet induced steatohepatitis. Bulletin of Egyptian Society for Physiological Sciences. 2017;37(2):208-26.
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38. Wei S, Yu X. Efficacy of resveratrol supplementation on liver enzymes in patients with non-alcoholic fatty liver disease: A systematic review and meta-analysis. Complementary therapies in medicine. 2021;57:102635.
39. Rafiee S, Mohammadi H, Ghavami A, Sadeghi E, Safari Z, Askari G. Efficacy of resveratrol supplementation in patients with nonalcoholic fatty liver disease: A systematic review and meta-analysis of clinical trials. Complementary Therapies in Clinical Practice. 2021;42:101281.
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43. Kulkarni SS, Cantó C. The molecular targets of resveratrol. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease. 2015;1852(6):1114-23.
44. BinMowyna MN, AlFaris NA, Al-Sanea EA, AlTamimi JZ, Aldayel TS. Resveratrol attenuates against high-fat-diet-promoted non-alcoholic fatty liver disease in rats mainly by targeting the miR-34a/SIRT1 axis. Archives of Physiology and Biochemistry. 2022:1-16.
45. Farkhondeh T, Folgado SL, Pourbagher-Shahri AM, Ashrafizadeh M, Samarghandian S. The therapeutic effect of resveratrol: Focusing on the Nrf2 signaling pathway. Biomedicine & Pharmacotherapy. 2020;127:110234.
46. Rubiolo JA, Mithieux G, Vega FV. Resveratrol protects primary rat hepatocytes against oxidative stress damage:: Activation of the Nrf2 transcription factor and augmented activities of antioxidant enzymes. European journal of pharmacology. 2008;591(1-3):66-72.
47. Tan X, Li L, Wang J, Zhao B, Pan J, Wang L, et al. Resveratrol prevents acrylamide-induced mitochondrial dysfunction and inflammatory responses via targeting circadian regulator Bmal1 and Cry1 in hepatocytes. Journal of agricultural and food chemistry. 2019;67(31):8510-9.
48. Sahin K, Orhan C, Akdemir F, Tuzcu M, Iben C, Sahin N. Resveratrol protects quail hepatocytes against heat stress: modulation of the Nrf2 transcription factor and heat shock proteins. Journal of animal physiology and animal nutrition. 2012;96(1):66-74.
49. Bao M, Ma Y, Liang M, Sun X, Ju X, Yong Y, et al. Research progress on pharmacological effects and new dosage forms of baicalin. Vet Med Sci. 2022;8(6):2773-84.
50. Shi H, Qiao F, Lu W, Huang K, Wen Y, Ye L, et al. Baicalin improved hepatic injury of NASH by regulating NRF2/HO-1/NRLP3 pathway. European Journal of Pharmacology. 2022;934:175270.
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2. Chahkandi S, Dabiri R, Mirmohammadkhani M, Amiri-Dashatan N, Koushki M. The effect of silymarin on liver enzymes and serum lipid profiles in Iranian patients with non-alcoholic fatty liver disease: A double-blind randomized controlled trial. Acta Biochimica Iranica. 2023.
3. Pouwels S, Sakran N, Graham Y, Leal A, Pintar T, Yang W, et al. Non-alcoholic fatty liver disease (NAFLD): a review of pathophysiology, clinical management and effects of weight loss. BMC Endocr Disord. 2022;22(1):63.
4. Goodarzi G, Tehrani SS, Panahi G, Bahramzadeh A, Meshkani R. Combination therapy of metformin and p-coumaric acid mitigates metabolic dysfunction associated with obesity and nonalcoholic fatty liver disease in high-fat diet obese C57BL/6 mice. The Journal of Nutritional Biochemistry. 2023;118:109369.
5. Khorzoughi RB, Meshkani R. Beneficial effect of metformin, quercetin, and resveratrol combination on high glucose-induced lipogenesis in HepG2 cells. Acta Biochimica Iranica. 2023.
6. Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, et al. The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology. 2012;55(6):2005-23.
7. Schuppan D, Schattenberg JM. Non-alcoholic steatohepatitis: pathogenesis and novel therapeutic approaches. J Gastroenterol Hepatol. 2013;28 Suppl 1:68-76.
8. Angulo P. Long-term mortality in nonalcoholic fatty liver disease: is liver histology of any prognostic significance? Hepatology. 2010;51(2):373-5.
9. Yu J, Marsh S, Hu J, Feng W, Wu C. The Pathogenesis of Nonalcoholic Fatty Liver Disease: Interplay between Diet, Gut Microbiota, and Genetic Background. Gastroenterol Res Pract. 2016;2016:2862173.
10. Zamani‐Garmsiri F, Ghasempour G, Aliabadi M, Hashemnia SMR, Emamgholipour S, Meshkani R. Combination of metformin and chlorogenic acid attenuates hepatic steatosis and inflammation in high‐fat diet fed mice. IUBMB life. 2021;73(1):252-63.
11. Day CP, James OF. Steatohepatitis: a tale of two "hits"? Gastroenterology. 1998;114(4):842-5.
12. Tilg H, Moschen AR. Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology. 2010;52(5):1836-46.
13. Tiniakos DG, Vos MB, Brunt EM. Nonalcoholic Fatty Liver Disease: Pathology and Pathogenesis. Annual Review of Pathology: Mechanisms of Disease. 2010;5(1):145-71.
14. Pizzino G, Irrera N, Cucinotta M, Pallio G, Mannino F, Arcoraci V, et al. Oxidative stress: harms and benefits for human health. Oxidative medicine and cellular longevity. 2017;2017.
15. Arroyave-Ospina JC, Wu Z, Geng Y, Moshage H. Role of Oxidative Stress in the Pathogenesis of Non-Alcoholic Fatty Liver Disease: Implications for Prevention and Therapy. Antioxidants (Basel). 2021;10(2).
16. Qu LL, Yu B, Li Z, Jiang WX, Jiang JD, Kong WJ. Gastrodin Ameliorates Oxidative Stress and Proinflammatory Response in Nonalcoholic Fatty Liver Disease through the AMPK/Nrf2 Pathway. Phytother Res. 2016;30(3):402-11.
17. Al-Asmari A, Khan A, Al-Masri N. Mitigation of 5-fluorouracil–induced liver damage in rats by vitamin C via targeting redox–sensitive transcription factors. Human & experimental toxicology. 2016;35(11):1203-13.
18. Hosseini H, Teimouri M, Shabani M, Koushki M, Babaei Khorzoughi R, Namvarjah F, et al. Resveratrol alleviates non-alcoholic fatty liver disease through epigenetic modification of the Nrf2 signaling pathway. Int J Biochem Cell Biol. 2020;119:105667.
19. Arabnezhad M-R, Haghani F, Ghaffarian-Bahraman A, Jafarzadeh E, Mohammadi H, Yadegari JG, et al. Involvement of Nrf2 signaling in lead-induced toxicity. Current Medicinal Chemistry. 2023.
20. Teimouri M, Hosseini H, Shabani M, Koushki M, Noorbakhsh F, Meshkani R. Inhibiting miR‐27a and miR‐142‐5p attenuate nonalcoholic fatty liver disease by regulating Nrf2 signaling pathway. IUBMB life. 2020;72(3):361-72.
21. Wang R, Liang L, Matsumoto M, Iwata K, Umemura A, He F. Reactive Oxygen Species and NRF2 Signaling, Friends or Foes in Cancer? Biomolecules. 2023;13(2):353.
22. Galicia-Moreno M, Lucano-Landeros S, Monroy-Ramirez HC, Silva-Gomez J, Gutierrez-Cuevas J, Santos A, et al. Roles of Nrf2 in liver diseases: molecular, pharmacological, and epigenetic aspects. Antioxidants. 2020;9(10):980.
23. Ghahremani H, Bahramzadeh A, Bolandnazar K, Emamgholipor S, Hosseini H, Meshkani R. Resveratrol as a potential protective compound against metabolic inflammation. Acta Biochimica Iranica. 2023;1(2):50-64.
24. de Araújo FF, de Paulo Farias D, Neri-Numa IA, Pastore GM. Polyphenols and their applications: An approach in food chemistry and innovation potential. Food Chem. 2021;338:127535.
25. Abenavoli L, Milic N, Luzza F, Boccuto L, De Lorenzo A. Polyphenols Treatment in Patients with Nonalcoholic Fatty Liver Disease. J Transl Int Med. 2017;5(3):144-7.
26. Larussa T, Suraci E, Marasco R, Imeneo M, Abenavoli L, Luzza F. Self-Prescribed Dietary Restrictions are Common in Inflammatory Bowel Disease Patients and Are Associated with Low Bone Mineralization. Medicina (Kaunas). 2019;55(8).
27. Zou T, Wang B, Li S, Liu Y, You J. Dietary apple polyphenols promote fat browning in high-fat diet-induced obese mice through activation of adenosine monophosphate-activated protein kinase α. J Sci Food Agric. 2020;100(6):2389-98.
28. Goodarzi G, Yadollahi M, Tehrani SS, Meshkani R. Genistein in combination with Chlorogenic acid ameliorates insulin resistance and oxidative stress in skeletal muscle of high-fat diet fed mice. Acta Biochimica Iranica. 2023;1(3):145-53.
29. Bahramzadeh A, Samavarchi Tehrani S, Goodarzi G, Seyyedebrahimi S, Meshkani R. Combination therapy of metformin and morin attenuates insulin resistance, inflammation, and oxidative stress in skeletal muscle of high‐fat diet‐fed mice. Phytotherapy Research. 2023.
30. Jafarzadeh E, Shoeibi S, Bahramvand Y, Nasrollahi E, Maghsoudi AS, Yazdi F, et al. Turmeric for treatment of irritable bowel syndrome: a systematic review of population-based evidence. Iranian Journal of Public Health. 2022;51(6):1223.
31. White CM, Lee J-Y. The impact of turmeric or its curcumin extract on nonalcoholic fatty liver disease: a systematic review of clinical trials. Pharmacy Practice (Granada). 2019;17(1).
32. Lee SC, Jee SC, Kim M, Kim S, Shin MK, Kim Y, et al. Curcumin Suppresses the Lipid Accumulation and Oxidative Stress Induced by Benzo[a]pyrene Toxicity in HepG2 Cells. Antioxidants (Basel). 2021;10(8).
33. Yu Q, Liu Y, Wu Y, Chen Y. Dihydrocurcumin ameliorates the lipid accumulation, oxidative stress and insulin resistance in oleic acid-induced L02 and HepG2 cells. Biomed Pharmacother. 2018;103:1327-36.
34. Yan C, Zhang Y, Zhang X, Aa J, Wang G, Xie Y. Curcumin regulates endogenous and exogenous metabolism via Nrf2-FXR-LXR pathway in NAFLD mice. Biomed Pharmacother. 2018;105:274-81.
35. Zakaria SS, ElBatsh MM, Mowafy SE. Effects of curcumin on autophagy and Nrf2 signaling pathway in a rat model of high fructose diet induced steatohepatitis. Bulletin of Egyptian Society for Physiological Sciences. 2017;37(2):208-26.
36. Izzo C, Annunziata M, Melara G, Sciorio R, Dallio M, Masarone M, et al. The role of resveratrol in liver disease: A comprehensive review from in vitro to clinical trials. Nutrients. 2021;13(3):933.
37. Honari M, Shafabakhsh R, Reiter RJ, Mirzaei H, Asemi Z. Resveratrol is a promising agent for colorectal cancer prevention and treatment: focus on molecular mechanisms. Cancer Cell International. 2019;19(1):1-8.
38. Wei S, Yu X. Efficacy of resveratrol supplementation on liver enzymes in patients with non-alcoholic fatty liver disease: A systematic review and meta-analysis. Complementary therapies in medicine. 2021;57:102635.
39. Rafiee S, Mohammadi H, Ghavami A, Sadeghi E, Safari Z, Askari G. Efficacy of resveratrol supplementation in patients with nonalcoholic fatty liver disease: A systematic review and meta-analysis of clinical trials. Complementary Therapies in Clinical Practice. 2021;42:101281.
40. Tejada S, Capó X, Mascaró CM, Monserrat-Mesquida M, Quetglas-Llabrés MM, Pons A, et al. Hepatoprotective effects of resveratrol in non-alcoholic fatty live disease. Current pharmaceutical design. 2021;27(22):2558-70.
41. Meng X, Zhou J, Zhao C-N, Gan R-Y, Li H-B. Health benefits and molecular mechanisms of resveratrol: a narrative review. Foods. 2020;9(3):340.
42. Lu MC, Ji JA, Jiang ZY, You QD. The Keap1–Nrf2–ARE pathway as a potential preventive and therapeutic target: an update. Medicinal research reviews. 2016;36(5):924-63.
43. Kulkarni SS, Cantó C. The molecular targets of resveratrol. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease. 2015;1852(6):1114-23.
44. BinMowyna MN, AlFaris NA, Al-Sanea EA, AlTamimi JZ, Aldayel TS. Resveratrol attenuates against high-fat-diet-promoted non-alcoholic fatty liver disease in rats mainly by targeting the miR-34a/SIRT1 axis. Archives of Physiology and Biochemistry. 2022:1-16.
45. Farkhondeh T, Folgado SL, Pourbagher-Shahri AM, Ashrafizadeh M, Samarghandian S. The therapeutic effect of resveratrol: Focusing on the Nrf2 signaling pathway. Biomedicine & Pharmacotherapy. 2020;127:110234.
46. Rubiolo JA, Mithieux G, Vega FV. Resveratrol protects primary rat hepatocytes against oxidative stress damage:: Activation of the Nrf2 transcription factor and augmented activities of antioxidant enzymes. European journal of pharmacology. 2008;591(1-3):66-72.
47. Tan X, Li L, Wang J, Zhao B, Pan J, Wang L, et al. Resveratrol prevents acrylamide-induced mitochondrial dysfunction and inflammatory responses via targeting circadian regulator Bmal1 and Cry1 in hepatocytes. Journal of agricultural and food chemistry. 2019;67(31):8510-9.
48. Sahin K, Orhan C, Akdemir F, Tuzcu M, Iben C, Sahin N. Resveratrol protects quail hepatocytes against heat stress: modulation of the Nrf2 transcription factor and heat shock proteins. Journal of animal physiology and animal nutrition. 2012;96(1):66-74.
49. Bao M, Ma Y, Liang M, Sun X, Ju X, Yong Y, et al. Research progress on pharmacological effects and new dosage forms of baicalin. Vet Med Sci. 2022;8(6):2773-84.
50. Shi H, Qiao F, Lu W, Huang K, Wen Y, Ye L, et al. Baicalin improved hepatic injury of NASH by regulating NRF2/HO-1/NRLP3 pathway. European Journal of Pharmacology. 2022;934:175270.
51. Gao Y, Liu J, Hao Z, Sun N, Guo J, Zheng X, et al. Baicalin ameliorates high fat diet-induced nonalcoholic fatty liver disease in mice via adenosine monophosphate-activated protein kinase-mediated regulation of SREBP1/Nrf2/NF-κB signaling pathways. Phytother Res. 2023;37(6):2405-18.
52. Liu WJ, Chen WW, Chen JY, Sun YB, Chang D, Wang CX, et al. Baicalin attenuated metabolic dysfunction-associated fatty liver disease by suppressing oxidative stress and inflammation via the p62-Keap1-Nrf2 signalling pathway in db/db mice. Phytother Res. 2023.
53. Morrow NM, Trzaskalski NA, Hanson AA, Fadzeyeva E, Telford DE, Chhoker SS, et al. Nobiletin Prevents High-Fat Diet-Induced Dysregulation of Intestinal Lipid Metabolism and Attenuates Postprandial Lipemia. Arterioscler Thromb Vasc Biol. 2022;42(2):127-44.
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| Files | ||
| Issue | Vol 2 No 1 (2024) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/abi.v2i1.16242 | |
| Keywords | ||
| Polyphenol non-alcoholic fatty liver disease Oxidative stress Resveratrol nuclear factor erythroid 2-related factor | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Soleimani AA, Omidi Sarajar B, Aliabadi M, Azmon M, Meshkani R. A review of the therapeutic effects of polyphenols on non-alcoholic fatty liver disease: Focus on oxidative stress. ABI. 2024;2(1):4-10.
