Download PDF
Semin Liver Dis
DOI: 10.1055/a-2490-4278
Review Article

Alcohol Plus Additional Risk Factors: Rodent Model of Liver Injury

Qixiang Wu    *
1   Inflammation and Immune Mediated Diseases Laboratory of Anhui Province, School of Pharmacy, Anhui Medical University, Hefei, Anhui, P.R. China
2   Institute for Liver Diseases of Anhui Medical University, Hefei, Anhui, P.R. China
,
Dashuai Yang    *
1   Inflammation and Immune Mediated Diseases Laboratory of Anhui Province, School of Pharmacy, Anhui Medical University, Hefei, Anhui, P.R. China
2   Institute for Liver Diseases of Anhui Medical University, Hefei, Anhui, P.R. China
,
Chixiang Liu    *
3   Department of Blood Transfusion, Southern Medical University, Nanfang Hospital, Guangzhou, P.R. China
4   School of Laboratory and Biotechnology, Institute of Antibody Engineering, Southern Medical University, Guangzhou, Guangdong, P.R. China
,
Tao Xu 
1   Inflammation and Immune Mediated Diseases Laboratory of Anhui Province, School of Pharmacy, Anhui Medical University, Hefei, Anhui, P.R. China
2   Institute for Liver Diseases of Anhui Medical University, Hefei, Anhui, P.R. China
› Author Affiliations Funding This work was supported by the National Natural Science Foundation of China (82373932); Natural Science Foundation of Anhui Province (2208085MH203); Anhui Translational Medicine Research Institute Project (2022-zhyx-C09); Anhui Outstanding Young Teachers Cultivation Program (YQZD2023023); Anhui Province University Outstanding Youth Research Project (2024AH020006); Anhui Medical University Youth Shuangpei Program (2024); The Open Fund of Key Laboratory of Anti-inflammatory and Immune Medicine, Ministry of Education, P.R. China (Anhui Medical University), KFJJ-2023–11.
› Further Information
   Permissions and Reprints


Abstract

Alcohol-associated liver disease (ALD), primarily caused by chronic excessive alcohol consumption, is a leading cause of chronic liver disease worldwide. ALD includes alcohol-associated steatotic liver, alcohol-associated hepatitis (AH), fibrosis, cirrhosis, and can even progress to hepatocellular carcinoma (HCC). Existing research indicates that the risk factors of ALD are quite numerous. In addition to drinking patterns, factors such as aldehyde dehydrogenase 2 (ALDH2) deficiency, smoking, medication administration, high-fat diet (HFD), hepatitis virus infection, and disruption of circadian rhythms can also increase susceptibility to ALD. However, there is limited understanding regarding the exacerbation of liver injury by alcohol plus additional risk factors. This review presents rodent models of EtOH + “X,” which simulate the synergistic effects of alcohol and additional risk factors in causing liver injury. These models offer a further exploration of the interactions between alcohol and additional risk factors, advancing the simulation of human ALD and providing a more reliable platform for studying disease mechanisms and exploring therapeutic interventions. We summarize the modeling methods, relevant indicators of liver injury, and focus on the targets of the synergistic effects as well as the associated mechanisms.

Keywords

alcohol consumption - ALD - MetALD - animal model - liver injury

Author Contributions

Q.W.: Conceptualization; writing—original draft, reviewing, and editing; visualization.


D.Y.: Conceptualization; writing—original draft, reviewing, and editing.


C.L.: Conceptualization; writing—original draft, reviewing, and editing.


T.X.: Conceptualization; supervision; funding acquisition; writing—original draft, reviewing, and editing.


Data Availability Statement

The authors declare that all the data supporting the findings of this study are contained within the paper.


Authorship

Guarantor of the article: T.X. All authors approved the final version of the manuscript.


* Qixiang Wu, Dashuai Yang, and Chixiang Liu contributed equally to this study.




Publication History

Article published online:
24 December 2024

© 2024. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Manthey J, Shield KD, Rylett M, Hasan OSM, Probst C, Rehm J. Global alcohol exposure between 1990 and 2017 and forecasts until 2030: a modelling study. Lancet 2019; 393 (10190): 2493-2502
    CrossrefPubMedSearch in Google Scholar
  • 2 Huang DQ, Mathurin P, Cortez-Pinto H, Loomba R. Global epidemiology of alcohol-associated cirrhosis and HCC: trends, projections and risk factors. Nat Rev Gastroenterol Hepatol 2023; 20 (01) 37-49
    CrossrefPubMedSearch in Google Scholar
  • 3 Hyun J, Han J, Lee C, Yoon M, Jung Y. Pathophysiological aspects of alcohol metabolism in the liver. Int J Mol Sci 2021; 22 (11) 5717
    CrossrefPubMedSearch in Google Scholar
  • 4 Wu X, Fan X, Miyata T. et al. Recent advances in understanding of pathogenesis of alcohol-associated liver disease. Annu Rev Pathol 2023; 18: 411-438
    CrossrefPubMedSearch in Google Scholar
  • 5 Fu Y, Mackowiak B, Lin Y-H. et al. Coordinated action of a gut-liver pathway drives alcohol detoxification and consumption. Nat Metab 2024; 6 (07) 1380-1396
    CrossrefPubMedSearch in Google Scholar
  • 6 Singal AK, Mathurin P. Diagnosis and treatment of alcohol-associated liver disease: a review. JAMA 2021; 326 (02) 165-176
    CrossrefPubMedSearch in Google Scholar
  • 7 Niu X, Zhu L, Xu Y. et al. Global prevalence, incidence, and outcomes of alcohol related liver diseases: a systematic review and meta-analysis. BMC Public Health 2023; 23 (01) 859
    CrossrefPubMedSearch in Google Scholar
  • 8 Mackowiak B, Fu Y, Maccioni L, Gao B. Alcohol-associated liver disease. J Clin Invest 2024; 134 (03) e176345
    CrossrefPubMedSearch in Google Scholar
  • 9 Liu SY, Tsai IT, Hsu YC. Alcohol-related liver disease: basic mechanisms and clinical perspectives. Int J Mol Sci 2021; 22 (10) 5170
    CrossrefPubMedSearch in Google Scholar
  • 10 Morgan MY, Sharma M, Atkinson SR. Genetic and environmental susceptibility to alcoholic hepatitis. Clin Liver Dis 2021; 25 (03) 517-535
    CrossrefPubMedSearch in Google Scholar
  • 11 Huang WC, Xu JW, Li S, Ng XE, Tung YT. Effects of exercise on high-fat diet-induced non-alcoholic fatty liver disease and lipid metabolism in ApoE knockout mice. Nutr Metab (Lond) 2022; 19 (01) 10
    CrossrefPubMedSearch in Google Scholar
  • 12 Jia W, Liu F. Obesity: causes, consequences, treatments, and challenges. J Mol Cell Biol 2021; 13 (07) 463-465
    CrossrefPubMedSearch in Google Scholar
  • 13 Zakhari S. Bermuda Triangle for the liver: alcohol, obesity, and viral hepatitis. J Gastroenterol Hepatol 2013; 28 (Suppl. 01) 18-25
    CrossrefPubMedSearch in Google Scholar
  • 14 Klatsky AL, Armstrong MA. Alcohol, smoking, coffee, and cirrhosis. Am J Epidemiol 1992; 136 (10) 1248-1257
    CrossrefPubMedSearch in Google Scholar
  • 15 Ghosh A, Berger I, Remien CH, Mubayi A. The role of alcohol consumption on acetaminophen induced liver injury: implications from a mathematical model. J Theor Biol 2021; 519: 110559
    CrossrefPubMedSearch in Google Scholar
  • 16 Federico A, Dallio M, Ormando VM. et al. Alcoholic liver disease and hepatitis C chronic infection. Rev Recent Clin Trials 2016; 11 (03) 201-207
    CrossrefPubMedSearch in Google Scholar
  • 17 Lamas-Paz A, Hao F, Nelson LJ. et al. Alcoholic liver disease: utility of animal models. World J Gastroenterol 2018; 24 (45) 5063-5075
    CrossrefPubMedSearch in Google Scholar
  • 18 Ghosh Dastidar S, Warner JB, Warner DR, McClain CJ, Kirpich IA. Rodent models of alcoholic liver disease: role of binge ethanol administration. Biomolecules 2018; 8 (01) 3
    CrossrefPubMedSearch in Google Scholar
  • 19 Bertola A, Mathews S, Ki SH, Wang H, Gao B. Mouse model of chronic and binge ethanol feeding (the NIAAA model). Nat Protoc 2013; 8 (03) 627-637
    CrossrefPubMedSearch in Google Scholar
  • 20 Landmann M, Wagnerberger S, Kanuri G, Ziegenhardt D, Bergheim I. Beer is less harmful for the liver than plain ethanol: studies in male mice using a binge-drinking model. Alcohol Alcohol 2015; 50 (05) 493-500
    CrossrefPubMedSearch in Google Scholar
  • 21 Shukla SD, Pruett SB, Szabo G, Arteel GE. Binge ethanol and liver: new molecular developments. Alcohol Clin Exp Res 2013; 37 (04) 550-557
    CrossrefPubMedSearch in Google Scholar
  • 22 Guo F, Zheng K, Benedé-Ubieto R, Cubero FJ, Nevzorova YA. The Lieber-DeCarli diet—a flagship model for experimental alcoholic liver disease. Alcohol Clin Exp Res 2018; 42 (10) 1828-1840
    CrossrefPubMedSearch in Google Scholar
  • 23 Zhu L, Li HD, Xu JJ. et al. Advancements in the alcohol-associated liver disease model. Biomolecules 2022; 12 (08) 1035
    CrossrefPubMedSearch in Google Scholar
  • 24 Liu SX, Du YC, Zeng T. A mini-review of the rodent models for alcoholic liver disease: shortcomings, application, and future prospects. Toxicol Res (Camb) 2021; 10 (03) 523-530
    CrossrefPubMedSearch in Google Scholar
  • 25 Nawroth JC, Petropolis DB, Manatakis DV. et al. Modeling alcohol-associated liver disease in a human Liver-Chip. Cell Rep 2021; 36 (03) 109393
    CrossrefPubMedSearch in Google Scholar
  • 26 Ashfaq UA, Javed T, Rehman S, Nawaz Z, Riazuddin S. An overview of HCV molecular biology, replication and immune responses. Virol J 2011; 8: 161
    CrossrefPubMedSearch in Google Scholar
  • 27 Torrents de la Peña A, Sliepen K, Eshun-Wilson L. et al. Structure of the hepatitis C virus E1E2 glycoprotein complex. Science 2022; 378 (6617) 263-269
    CrossrefPubMedSearch in Google Scholar
  • 28 Mueller S, Millonig G, Seitz HK. Alcoholic liver disease and hepatitis C: a frequently underestimated combination. World J Gastroenterol 2009; 15 (28) 3462-3471
    PubMedSearch in Google Scholar
  • 29 Tumurbaatar B, Tikhanovich I, Li Z. et al. Hepatitis C and alcohol exacerbate liver injury by suppression of FOXO3. Am J Pathol 2013; 183 (06) 1803-1814
    CrossrefPubMedSearch in Google Scholar
  • 30 Fondevila F, Fernández-Palanca P, Méndez-Blanco C. et al. Association of FOXO3 expression with tumor pathogenesis, prognosis and clinicopathological features in hepatocellular carcinoma: a systematic review with meta-analysis. Cancers (Basel) 2021; 13 (21) 5349
    CrossrefPubMedSearch in Google Scholar
  • 31 Li Z, Zhao J, Zhang S, Weinman SA. FOXO3-dependent apoptosis limits alcohol-induced liver inflammation by promoting infiltrating macrophage differentiation. Cell Death Discov 2018; 4: 16
    CrossrefPubMedSearch in Google Scholar
  • 32 Ni HM, Du K, You M, Ding WX. Critical role of FoxO3a in alcohol-induced autophagy and hepatotoxicity. Am J Pathol 2013; 183 (06) 1815-1825
    CrossrefPubMedSearch in Google Scholar
  • 33 Lee YH, Lin Q, Boelsterli UA, Chung MC. The Sod2 mutant mouse as a model for oxidative stress: a functional proteomics perspective. Mass Spectrom Rev 2010; 29 (02) 179-196
    CrossrefPubMedSearch in Google Scholar
  • 34 Patke A, Young MW, Axelrod S. Molecular mechanisms and physiological importance of circadian rhythms. Nat Rev Mol Cell Biol 2020; 21 (02) 67-84
    CrossrefPubMedSearch in Google Scholar
  • 35 Summa KC, Voigt RM, Forsyth CB. et al. Disruption of the circadian clock in mice increases intestinal permeability and promotes alcohol-induced hepatic pathology and inflammation. PLoS One 2013; 8 (06) e67102
    CrossrefPubMedSearch in Google Scholar
  • 36 Seo W, Gao Y, He Y. et al. ALDH2 deficiency promotes alcohol-associated liver cancer by activating oncogenic pathways via oxidized DNA-enriched extracellular vesicles. J Hepatol 2019; 71 (05) 1000-1011
    CrossrefPubMedSearch in Google Scholar
  • 37 Rungratanawanich W, Lin Y, Wang X, Kawamoto T, Chidambaram SB, Song BJ. ALDH2 deficiency increases susceptibility to binge alcohol-induced gut leakiness, endotoxemia, and acute liver injury in mice through the gut-liver axis. Redox Biol 2023; 59: 102577
    CrossrefPubMedSearch in Google Scholar
  • 38 Chang JS, Hsiao JR, Chen CH. ALDH2 polymorphism and alcohol-related cancers in Asians: a public health perspective. J Biomed Sci 2017; 24 (01) 19
    CrossrefPubMedSearch in Google Scholar
  • 39 Kwon HJ, Won YS, Park O. et al. Aldehyde dehydrogenase 2 deficiency ameliorates alcoholic fatty liver but worsens liver inflammation and fibrosis in mice. Hepatology 2014; 60 (01) 146-157
    CrossrefPubMedSearch in Google Scholar
  • 40 Shen B, Deng L, Liu Y. et al. Effects of novel Fufang Biejia Ruangan Tablets with sheep placenta as substitute for Hominis Placenta on CCl4-induced liver fibrosis. Chin Herb Med 2021; 14 (01) 104-110
    PubMedSearch in Google Scholar
  • 41 Gao B, Bataller R. Alcoholic liver disease: pathogenesis and new therapeutic targets. Gastroenterology 2011; 141 (05) 1572-1585
    CrossrefPubMedSearch in Google Scholar
  • 42 Buyco DG, Martin J, Jeon S, Hooks R, Lin C, Carr R. Experimental models of metabolic and alcoholic fatty liver disease. World J Gastroenterol 2021; 27 (01) 1-18
    CrossrefPubMedSearch in Google Scholar
  • 43 Brol MJ, Rösch F, Schierwagen R. et al. Combination of CCl4 with alcoholic and metabolic injuries mimics human liver fibrosis. Am J Physiol Gastrointest Liver Physiol 2019; 317 (02) G182-G194
    CrossrefPubMedSearch in Google Scholar
  • 44 Zhang G, Wang X, Chung TY. et al. Carbon tetrachloride (CCl4) accelerated development of non-alcoholic fatty liver disease (NAFLD)/steatohepatitis (NASH) in MS-NASH mice fed western diet supplemented with fructose (WDF). BMC Gastroenterol 2020; 20 (01) 339
    CrossrefPubMedSearch in Google Scholar
  • 45 Liput KP, Lepczyński A, Ogłuszka M. et al. Effects of dietary n-3 and n-6 polyunsaturated fatty acids in inflammation and cancerogenesis. Int J Mol Sci 2021; 22 (13) 6965
    CrossrefPubMedSearch in Google Scholar
  • 46 Nanji AA, French SW. Dietary linoleic acid is required for development of experimentally induced alcoholic liver injury. Life Sci 1989; 44 (03) 223-227
    CrossrefPubMedSearch in Google Scholar
  • 47 Warner DR, Liu H, Miller ME. et al. Dietary linoleic acid and its oxidized metabolites exacerbate liver injury caused by ethanol via induction of hepatic proinflammatory response in mice. Am J Pathol 2017; 187 (10) 2232-2245
    CrossrefPubMedSearch in Google Scholar
  • 48 Bromfield EG, Mihalas BP, Dun MD. et al. Inhibition of arachidonate 15-lipoxygenase prevents 4-hydroxynonenal-induced protein damage in male germ cells. Biol Reprod 2017; 96 (03) 598-609
    CrossrefPubMedSearch in Google Scholar
  • 49 Fan X, Wang X, Hui Y. et al. Genipin protects against acute liver injury by abrogating ferroptosis via modification of GPX4 and ALOX15-launched lipid peroxidation in mice. Apoptosis 2023; 28 (9-10): 1469-1483
    CrossrefPubMedSearch in Google Scholar
  • 50 Singh NK, Rao GN. Emerging role of 12/15-Lipoxygenase (ALOX15) in human pathologies. Prog Lipid Res 2019; 73: 28-45
    CrossrefPubMedSearch in Google Scholar
  • 51 Snodgrass RG, Brüne B. Regulation and functions of 15-lipoxygenases in human macrophages. Front Pharmacol 2019; 10: 719
    CrossrefPubMedSearch in Google Scholar
  • 52 Schuster S, Johnson CD, Hennebelle M. et al. Oxidized linoleic acid metabolites induce liver mitochondrial dysfunction, apoptosis, and NLRP3 activation in mice. J Lipid Res 2018; 59 (09) 1597-1609
    CrossrefPubMedSearch in Google Scholar
  • 53 Marti-Aguado D, Clemente-Sanchez A, Bataller R. Cigarette smoking and liver diseases. J Hepatol 2022; 77 (01) 191-205
    CrossrefPubMedSearch in Google Scholar
  • 54 Chen X, Owoseni E, Salamat J, Cederbaum AI, Lu Y. Nicotine enhances alcoholic fatty liver in mice: Role of CYP2A5. Arch Biochem Biophys 2018; 657: 65-73
    CrossrefPubMedSearch in Google Scholar
  • 55 Poça KS, Parente TE, Chagas LF. et al. Interstrain differences in the expression and activity of Cyp2a5 in the mouse liver. BMC Res Notes 2017; 10 (01) 125
    CrossrefPubMedSearch in Google Scholar
  • 56 Lu Y, Zhuge J, Wu D, Cederbaum AI. Ethanol induction of CYP2A5: permissive role for CYP2E1. Drug Metab Dispos 2011; 39 (02) 330-336
    CrossrefPubMedSearch in Google Scholar
  • 57 Lu Y, Zhang XH, Cederbaum AI. Ethanol induction of CYP2A5: role of CYP2E1-ROS-Nrf2 pathway. Toxicol Sci 2012; 128 (02) 427-438
    CrossrefPubMedSearch in Google Scholar
  • 58 Zeng T, Liu Y, Jiang Y. et al. Advanced materials design for adsorption of toxic substances in cigarette smoke. Adv Sci (Weinh) 2023; 10 (22) e2301834
    CrossrefPubMedSearch in Google Scholar
  • 59 Ohashi N, Kohno T. Analgesic effect of acetaminophen: a review of known and novel mechanisms of action. Front Pharmacol 2020; 11: 580289
    CrossrefPubMedSearch in Google Scholar
  • 60 Shan S, Shen Z, Song F. Autophagy and acetaminophen-induced hepatotoxicity. Arch Toxicol 2018; 92 (07) 2153-2161
    CrossrefPubMedSearch in Google Scholar
  • 61 Miao X, Jin C, Liu J, Wang J, Chen Y. Honokiol attenuates acetaminophen-induced acute liver injury by inhibiting hepatic CYP1A2 activity and improving liver mitochondrial dysfunction. Chin Herb Med 2023; 15 (02) 231-239
    PubMedSearch in Google Scholar
  • 62 Chao X, Wang H, Jaeschke H, Ding WX. Role and mechanisms of autophagy in acetaminophen-induced liver injury. Liver Int 2018; 38 (08) 1363-1374
    CrossrefPubMedSearch in Google Scholar
  • 63 Hu S, Yao Y, Wei ZY. et al. Deletion of p38γ attenuates ethanol consumption- and acetaminophen-induced liver injury in mice through promoting Dlg1. Acta Pharmacol Sin 2022; 43 (07) 1733-1748
    CrossrefPubMedSearch in Google Scholar
  • 64 Yong HY, Koh MS, Moon A. The p38 MAPK inhibitors for the treatment of inflammatory diseases and cancer. Expert Opin Investig Drugs 2009; 18 (12) 1893-1905
    CrossrefPubMedSearch in Google Scholar
  • 65 Qi XM, Chen G. p38γ MAPK inflammatory and metabolic signaling in physiology and disease. Cells 2023; 12 (13) 1674
    CrossrefPubMedSearch in Google Scholar
  • 66 Salama RM, Abbas SS, Darwish SF, Sallam AA, Elmongy NF, El Wakeel SA. Regulation of NOX/p38 MAPK/PPARα pathways and miR-155 expression by boswellic acids reduces hepatic injury in experimentally-induced alcoholic liver disease mouse model: novel mechanistic insight. Arch Pharm Res 2023; 46 (04) 323-338
    CrossrefPubMedSearch in Google Scholar
  • 67 Zhang X, Dong Z, Fan H. et al. [Scutellarin prevents acute alcohol-induced liver injury via inhibiting oxidative stress by regulating the Nrf2/HO-1 pathway and inhibiting inflammation by regulating the AKT, p38 MAPK/NF-κB pathways] [in Chinese]. J Zhejiang Univ Sci B 2023; 24 (07) 617-631
    CrossrefPubMedSearch in Google Scholar
  • 68 Kulda V. Metabolizmus vitaminu D [Vitamin D metabolism] [in Czech]. Vnitr Lek 2012; 58 (05) 400-404
    PubMedSearch in Google Scholar
  • 69 Lin S, Wang W, Shi L. et al. Severe vitamin D deficiency is strongly associated with liver dysfunction and disease severity in hepatitis B virus related cirrhosis and liver failure patients. J Nutr Sci Vitaminol (Tokyo) 2022; 68 (01) 16-22
    CrossrefPubMedSearch in Google Scholar
  • 70 Tardelli VS, Lago MPPD, Silveira DXD, Fidalgo TM. Vitamin D and alcohol: a review of the current literature. Psychiatry Res 2017; 248: 83-86
    CrossrefPubMedSearch in Google Scholar
  • 71 Shibamoto A, Kaji K, Nishimura N. et al. Vitamin D deficiency exacerbates alcohol-related liver injury via gut barrier disruption and hepatic overload of endotoxin. J Nutr Biochem 2023; 122: 109450
    CrossrefPubMedSearch in Google Scholar
  • 72 Rinella ME, Lazarus JV, Ratziu V. et al; NAFLD Nomenclature consensus group. A multisociety Delphi consensus statement on new fatty liver disease nomenclature. J Hepatol 2023; 79 (06) 1542-1556
    CrossrefPubMedSearch in Google Scholar
  • 73 Li Y, Yang P, Ye J, Xu Q, Wu J, Wang Y. Updated mechanisms of MASLD pathogenesis. Lipids Health Dis 2024; 23 (01) 117
    CrossrefPubMedSearch in Google Scholar
  • 74 Chiang DJ, McCullough AJ. The impact of obesity and metabolic syndrome on alcoholic liver disease. Clin Liver Dis 2014; 18 (01) 157-163
    CrossrefPubMedSearch in Google Scholar
  • 75 Chen Y, Wang W, Morgan MP, Robson T, Annett S. Obesity, non-alcoholic fatty liver disease and hepatocellular carcinoma: current status and therapeutic targets. Front Endocrinol (Lausanne) 2023; 14: 1148934
    CrossrefPubMedSearch in Google Scholar
  • 76 Eslam M, George J. Two years on, a perspective on MAFLD. eGastroenterology 2023; 1(2): e100019
    CrossrefPubMedSearch in Google Scholar
  • 77 Iturriaga H, Bunout D, Hirsch S, Ugarte G. Overweight as a risk factor or a predictive sign of histological liver damage in alcoholics. Am J Clin Nutr 1988; 47 (02) 235-238
    CrossrefPubMedSearch in Google Scholar
  • 78 Everitt H, Hu M, Ajmo JM. et al. Ethanol administration exacerbates the abnormalities in hepatic lipid oxidation in genetically obese mice. Am J Physiol Gastrointest Liver Physiol 2013; 304 (01) G38-G47
    CrossrefPubMedSearch in Google Scholar
  • 79 Hao Z, Münzberg H, Rezai-Zadeh K. et al. Leptin deficient ob/ob mice and diet-induced obese mice responded differently to Roux-en-Y bypass surgery. Int J Obes (Lond) 2015; 39 (05) 798-805
    CrossrefPubMedSearch in Google Scholar
  • 80 Matsumoto-Miyai K, Yoshizumi M, Kawatani M. Regulatory effects of 5-hydroxytryptamine receptors on voiding function. Adv Ther 2015; 32 (Suppl. 01) 3-15
    CrossrefPubMedSearch in Google Scholar
  • 81 Amith M, Onye C, Ledoux T, Xiong G, Tao C. The ontology of fast food facts: conceptualization of nutritional fast food data for consumers and semantic web applications. BMC Med Inform Decis Mak 2021; 21 (Suppl. 07) 275
    CrossrefPubMedSearch in Google Scholar
  • 82 Kardashian A, Dodge JL, Terrault NA. Quantifying the negative impact of fast-food consumption on liver steatosis among United States adults with diabetes and obesity. Clin Gastroenterol Hepatol 2023; 21 (12) 3176-3178.e3
    CrossrefPubMedSearch in Google Scholar
  • 83 Malnick SDH, Alin P, Somin M, Neuman MG. Fatty liver disease-alcoholic and non-alcoholic: similar but different. Int J Mol Sci 2022; 23 (24) 16226
    CrossrefPubMedSearch in Google Scholar
  • 84 Sharma RR, Rashid H, Tasduq Abdullah S. A small animal model of NASH with progressive steatohepatitis-induced by fast food diet and alcohol in C57BL/6J mouse with high human pathophysiological proximity. Food Chem Toxicol 2023; 178: 113851
    CrossrefPubMedSearch in Google Scholar
  • 85 Recena Aydos L, Aparecida do Amaral L, Serafim de Souza R, Jacobowski AC, Freitas Dos Santos E, Rodrigues Macedo ML. Nonalcoholic fatty liver disease induced by high-fat diet in C57bl/6 models. Nutrients 2019; 11 (12) 3067
    CrossrefPubMedSearch in Google Scholar
  • 86 Zhan ZY, Wu M, Shang Y. et al. Taxifolin ameliorate high-fat-diet feeding plus acute ethanol binge-induced steatohepatitis through inhibiting inflammatory caspase-1-dependent pyroptosis. Food Funct 2021; 12 (01) 362-372
    CrossrefPubMedSearch in Google Scholar
  • 87 Adolph TE, Tilg H. Western diets and chronic diseases. Nat Med 2024; 30 (08) 2133-2147
    CrossrefPubMedSearch in Google Scholar
  • 88 Buyco DG, Dempsey JL, Scorletti E. et al. Concomitant western diet and chronic-binge alcohol dysregulate hepatic metabolism. PLoS One 2023; 18 (05) e0281954
    CrossrefPubMedSearch in Google Scholar
  • 89 Wang S, Friedman SL. Found in translation-Fibrosis in metabolic dysfunction-associated steatohepatitis (MASH). Sci Transl Med 2023; 15 (716) eadi0759
    CrossrefPubMedSearch in Google Scholar
  • 90 Babuta M, Nagesh PT, Datta AA. et al. Combined insults of a MASH diet and alcohol binges activate intercellular communication and neutrophil recruitment via the NLRP3-IL-1β axis in the liver. Cells 2024; 13 (11) 960
    CrossrefPubMedSearch in Google Scholar
  • 91 Huang Z, Tian Z, Zhao Y, Zhu F, Liu W, Wang X. MAPK signaling pathway is essential for female reproductive regulation in the cabbage beetle, Colaphellus bowringi . Cells 2022; 11 (10) 1602
    CrossrefPubMedSearch in Google Scholar
  • 92 Park HB, Baek KH. E3 ligases and deubiquitinating enzymes regulating the MAPK signaling pathway in cancers. Biochim Biophys Acta Rev Cancer 2022; 1877 (03) 188736
    CrossrefPubMedSearch in Google Scholar
  • 93 Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 1995; 270 (5240) 1326-1331
    CrossrefPubMedSearch in Google Scholar
  • 94 Hao Y, Song S, Li T. et al. Oxidative stress promotes liver fibrosis by modulating the microRNA-144 and SIN3A-p38 pathways in hepatic stellate cells. Int J Biol Sci 2024; 20 (07) 2422-2439
    CrossrefPubMedSearch in Google Scholar
  • 95 Liu F, Liu Y, Peng Q. et al. Creatinine accelerates APAP-induced liver damage by increasing oxidative stress through ROS/JNK signaling pathway. Front Pharmacol 2022; 13: 959497
    CrossrefPubMedSearch in Google Scholar
  • 96 Iorga A, Donovan K, Shojaie L. et al. Interaction of RIPK1 and A20 modulates MAPK signaling in murine acetaminophen toxicity. J Biol Chem 2021; 296: 100300
    CrossrefPubMedSearch in Google Scholar
  • 97 Wang M, Zhang F, Zhou J. et al. Glabridin ameliorates alcohol-caused liver damage by reducing oxidative stress and inflammation via p38 MAPK/Nrf2/NF-κB pathway. Nutrients 2023; 15 (09) 2157
    CrossrefPubMedSearch in Google Scholar
  • 98 Jaramillo MC, Zhang DD. The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev 2013; 27 (20) 2179-2191
    CrossrefPubMedSearch in Google Scholar
  • 99 Mirzaei S, Mohammadi AT, Gholami MH. et al. Nrf2 signaling pathway in cisplatin chemotherapy: potential involvement in organ protection and chemoresistance. Pharmacol Res 2021; 167: 105575
    CrossrefPubMedSearch in Google Scholar
  • 100 Harjumäki R, Pridgeon CS, Ingelman-Sundberg M. CYP2E1 in alcoholic and non-alcoholic liver injury. Roles of ROS, reactive intermediates and lipid overload. Int J Mol Sci 2021; 22 (15) 8221
    CrossrefPubMedSearch in Google Scholar
  • 101 Zhou J, Zheng Q, Chen Z. The Nrf2 pathway in liver diseases. Front Cell Dev Biol 2022; 10: 826204
    CrossrefPubMedSearch in Google Scholar
  • 102 Zhang YP, Yang XQ, Yu DK, Xiao HY, Du JR. Nrf2 signalling pathway and autophagy impact on the preventive effect of green tea extract against alcohol-induced liver injury. J Pharm Pharmacol 2021; 73 (07) 986-995
    CrossrefPubMedSearch in Google Scholar
  • 103 Yu H, Lin L, Zhang Z, Zhang H, Hu H. Targeting NF-κB pathway for the therapy of diseases: mechanism and clinical study. Signal Transduct Target Ther 2020; 5 (01) 209
    CrossrefPubMedSearch in Google Scholar
  • 104 Nowak AJ, Relja B. The impact of acute or chronic alcohol intake on the NF-κB signaling pathway in alcohol-related liver disease. Int J Mol Sci 2020; 21 (24) 9407
    CrossrefPubMedSearch in Google Scholar
  • 105 Herzig S, Shaw RJ. AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol 2018; 19 (02) 121-135
    CrossrefPubMedSearch in Google Scholar
  • 106 You Y, Liu C, Liu T. et al. FNDC3B protects steatosis and ferroptosis via the AMPK pathway in alcoholic fatty liver disease. Free Radic Biol Med 2022; 193 (Pt 2): 808-819
    CrossrefPubMedSearch in Google Scholar
  • 107 Yang Y, Liu Y, Wang Y. et al. Regulation of SIRT1 and its roles in inflammation. Front Immunol 2022; 13: 831168
    CrossrefPubMedSearch in Google Scholar
  • 108 Zhong Y, Dambach DM, Maher JM. Using genetically modified rodent models in drug development to explore target physiology and potential drug effects. Vet Pathol 2018; 55 (02) 193-194
    CrossrefPubMedSearch in Google Scholar
  • 109 Nuciforo S, Heim MH. Organoids to model liver disease. JHEP Rep Innov Hepatol 2020; 3 (01) 100198
    CrossrefPubMedSearch in Google Scholar
  • 110 Deguchi S, Takayama K. State-of-the-art liver disease research using liver-on-a-chip. Inflamm Regen 2022; 42 (01) 62
    CrossrefPubMedSearch in Google Scholar
  • 111 Lee J, Mun SJ, Shin Y, Lee S, Son MJ. Advances in liver organoids: model systems for liver disease. Arch Pharm Res 2022; 45 (06) 390-400
    CrossrefPubMedSearch in Google Scholar
  • 112 Wang S, Wang X, Tan Z. et al. Human ESC-derived expandable hepatic organoids enable therapeutic liver repopulation and pathophysiological modeling of alcoholic liver injury. Cell Res 2019; 29 (12) 1009-1026
    CrossrefPubMedSearch in Google Scholar
  • 113 Hu Y, Zhang Y, Liu Y. et al. Advances in application of single-cell RNA sequencing in cardiovascular research. Front Cardiovasc Med 2022; 9: 905151
    CrossrefPubMedSearch in Google Scholar
  • 114 Cross A, Harris JM, Arbe-Barnes E. et al. Characterisation of HBV and co-infection with HDV and HIV through spatial transcriptomics. eGastroenterology 2024; 2 (03) e100067
    CrossrefPubMedSearch in Google Scholar
  • 115 He J, Deng C, Krall L, Shan Z. ScRNA-seq and ST-seq in liver research. Cell Regen (Lond) 2023; 12 (01) 11
    CrossrefPubMedSearch in Google Scholar