Partial validation of a six-month high-fat diet and fructose-glucose drink combination as a mouse model of nonalcoholic fatty liver disease.
Fast food diet
Fibrosis
Mouse model
Nonalcoholic fatty liver disease
Nonalcoholic steatohepatitis
Steatosis
Journal
Endocrine
ISSN: 1559-0100
Titre abrégé: Endocrine
Pays: United States
ID NLM: 9434444
Informations de publication
Date de publication:
20 Mar 2024
20 Mar 2024
Historique:
received:
18
11
2023
accepted:
29
02
2024
medline:
20
3
2024
pubmed:
20
3
2024
entrez:
20
3
2024
Statut:
aheadofprint
Résumé
The need to investigate the pathogenesis and treatment of nonalcoholic fatty liver disease (NAFLD) has led to the development of multiple mouse models. The aim of this study was to validate a fast food diet (FFD) mouse model that is introduced as being close to the human disease. Eight to nine weeks old male and female C57BL/6 J mice were randomly allocated to a FFD group or to a chow diet (CD) group. Every four weeks, mice were weighed, and blood samples were collected for the measurement of glucose, alanine aminotransferase (ALT), aspartate aminotransferase (AST), triglycerides (TGs) and total cholesterol. After 25 weeks, mice were sacrificed, and liver tissue was histologically evaluated. FFD mice gained more weight (p = 0.049) and presented a higher liver-to-body weight ratio (p < 0.001) compared to CD mice. FFD group presented with greater steatosis, hepatocellular ballooning and NAFLD activity score (NAS), whereas lobular inflammation and fibrosis were not significantly different compared to CD. When stratified by sex, NAS was different between FFD and CD groups in both male and female mice. Group by time interaction was significant for weight, ALT and cholesterol, but not for glucose, AST and TGs. FFD mice presented with morphologic and biochemical features of NAFLD and with greater hepatic steatosis, hepatocellular ballooning and NAS, but not lobular inflammation and fibrosis, compared to CD mice. These results only partly validate the FFD mouse model for NAFLD, at least for a 6-month feeding period.
Identifiants
pubmed: 38507181
doi: 10.1007/s12020-024-03769-5
pii: 10.1007/s12020-024-03769-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
L. Henry, J. Paik, Z.M. Younossi, Review article: the epidemiologic burden of non-alcoholic fatty liver disease across the world. Aliment. Pharmacol. Ther. 56, 942–956 (2022). https://doi.org/10.1111/apt.17158
doi: 10.1111/apt.17158
pubmed: 35880713
E. Makri, A. Goulas, S.A. Polyzos, Epidemiology, pathogenesis, diagnosis and emerging treatment of nonalcoholic fatty liver disease. Arch. Med. Res. 52, 25–37 (2021). https://doi.org/10.1016/j.arcmed.2020.11.010
doi: 10.1016/j.arcmed.2020.11.010
pubmed: 33334622
S.A. Polyzos, C.S. Mantzoros, Nonalcoholic fatty future disease. Metab. Clin. Exp. 65, 1007–1016 (2016). https://doi.org/10.1016/j.metabol.2015.12.009
doi: 10.1016/j.metabol.2015.12.009
pubmed: 26805015
S.A. Polyzos, J. Kountouras, C.S. Mantzoros, Adipose tissue, obesity and non-alcoholic fatty liver disease. Minerva Endocrinol. 42, 92–108 (2017). https://doi.org/10.23736/s0391-1977.16.02563-3
doi: 10.23736/s0391-1977.16.02563-3
pubmed: 27711029
G. Targher, C.D. Byrne, A. Lonardo, G. Zoppini, C. Barbui, Non-alcoholic fatty liver disease and risk of incident cardiovascular disease: A meta-analysis. J. Hepatol. 65, 589–600 (2016). https://doi.org/10.1016/j.jhep.2016.05.013
doi: 10.1016/j.jhep.2016.05.013
pubmed: 27212244
E. Makri, M. Kita, A. Goulas, P. Papaioannidou, Z.A. Efstathiadou, F. Adamidou et al. Comparative effectiveness of glucagon-like peptide-1 receptor agonists versus dipeptidyl peptidase-4 inhibitors on noninvasive indices of hepatic steatosis and fibrosis in patients with type 2 diabetes mellitus. Diabetes Metab. Syndr. 14, 1913–1919 (2020). https://doi.org/10.1016/j.dsx.2020.09.030
doi: 10.1016/j.dsx.2020.09.030
pubmed: 33011499
E.S. Makri, A. Goulas, S.A. Polyzos, Sodium-glucose co-transporter 2 inhibitors in nonalcoholic fatty liver disease. Eur. J. Pharmacol. 907, 174272 (2021). https://doi.org/10.1016/j.ejphar.2021.174272
doi: 10.1016/j.ejphar.2021.174272
pubmed: 34147478
E.S. Makri, E. Makri, S.A. Polyzos, Combination therapies for nonalcoholic fatty liver disease. J. Personalized Med. 12, 1166 (2022). https://doi.org/10.3390/jpm12071166
doi: 10.3390/jpm12071166
S.A. Polyzos, E.S. Kang, C. Boutari, E.J. Rhee, C.S. Mantzoros, Current and emerging pharmacological options for the treatment of nonalcoholic steatohepatitis. Metab. Clin. Exp. 111S, 154203 (2020). https://doi.org/10.1016/j.metabol.2020.154203
doi: 10.1016/j.metabol.2020.154203
pubmed: 32151660
S.A. Polyzos, J. Kountouras, C. Zavos, G. Deretzi, Nonalcoholic fatty liver disease: multimodal treatment options for a pathogenetically multiple-hit disease. J. Clin. Gastroenterol. 46, 272–284 (2012). https://doi.org/10.1097/MCG.0b013e31824587e0
doi: 10.1097/MCG.0b013e31824587e0
pubmed: 22395062
P.K. Santhekadur, D.P. Kumar, A.J. Sanyal, Preclinical models of non-alcoholic fatty liver disease. J. Hepatol. 68, 230–237 (2018). https://doi.org/10.1016/j.jhep.2017.10.031
doi: 10.1016/j.jhep.2017.10.031
pubmed: 29128391
I. Rubio-Aliaga, B.D. Roos, M. Sailer, G.A. McLoughlin, M.V. Boekschoten, M. van Erk et al. Alterations in hepatic one-carbon metabolism and related pathways following a high-fat dietary intervention. Physiol. Genomics 43, 408–416 (2011). https://doi.org/10.1152/physiolgenomics.00179.2010
doi: 10.1152/physiolgenomics.00179.2010
pubmed: 21303933
G.J.P. Rautureau, B. Morio, S. Guibert, C. Lefevre, J. Perrier, A. Alves et al. Dietary obesity in mice is associated with lipid deposition and metabolic shifts in the lungs sharing features with the liver. Sci. Rep. 11, 8712 (2021). https://doi.org/10.1038/s41598-021-88097-8
doi: 10.1038/s41598-021-88097-8
pubmed: 33888788
pmcid: 8062462
J.K. Lau, X. Zhang, J. Yu, Animal models of non-alcoholic fatty liver disease: current perspectives and recent advances. J. Pathol. 241, 36–44 (2017). https://doi.org/10.1002/path.4829
doi: 10.1002/path.4829
pubmed: 27757953
K.T. Velázquez, R.T. Enos, J.E. Bader, A.T. Sougiannis, M.S. Carson, I. Chatzistamou et al. Prolonged high-fat-diet feeding promotes non-alcoholic fatty liver disease and alters gut microbiota in mice. World J. Hepatol. 11, 619–637 (2019). https://doi.org/10.4254/wjh.v11.i8.619
doi: 10.4254/wjh.v11.i8.619
pubmed: 31528245
pmcid: 6717713
H. Jürgens, W. Haass, T.R. Castañeda, A. Schürmann, C. Koebnick, F. Dombrowski et al. Consuming fructose-sweetened beverages increases body adiposity in mice. Obesity research 13, 1146–1156 (2005). https://doi.org/10.1038/oby.2005.136
doi: 10.1038/oby.2005.136
pubmed: 16076983
R. Kohli, M. Kirby, S.A. Xanthakos, S. Softic, A.E. Feldstein, V. Saxena et al. High-fructose, medium chain trans fat diet induces liver fibrosis and elevates plasma coenzyme Q9 in a novel murine model of obesity and nonalcoholic steatohepatitis. Hepatology (Baltimore, Md) 52, 934–944 (2010). https://doi.org/10.1002/hep.23797
doi: 10.1002/hep.23797
pubmed: 20607689
pmcid: 2932817
M. Charlton, A. Krishnan, K. Viker, S. Sanderson, S. Cazanave, A. McConico et al. Fast food diet mouse: novel small animal model of NASH with ballooning, progressive fibrosis, and high physiological fidelity to the human condition. Am. J. Physiol. Gastrointestinal Liver Physiol. 301, 825–834 (2011). https://doi.org/10.1152/ajpgi.00145.2011
doi: 10.1152/ajpgi.00145.2011
A. Krishnan, T.S. Abdullah, T. Mounajjed, S. Hartono, A. McConico, T. White et al. A longitudinal study of whole body, tissue, and cellular physiology in a mouse model of fibrosing NASH with high fidelity to the human condition. Am. J. Physiol. Gastrointestinal Liver Physiol. 312, 666 (2017). https://doi.org/10.1152/ajpgi.00213.2016
doi: 10.1152/ajpgi.00213.2016
M. Charlton, A. Krishnan, K. Viker, S. Sanderson, S. Cazanave, A. McConico et al. Corrigendum in: Fast food diet mouse: novel small animal model of NASH with ballooning, progressivefibrosis, and high physiological fidelity to the human condition. Am. J. Physiol. Gastrointestinal Liver Physiol. 308, G159 (2015). https://doi.org/10.1152/ajpgi.zh3-6827-corr.2014
doi: 10.1152/ajpgi.zh3-6827-corr.2014
N. Percie du Sert, V. Hurst, A. Ahluwalia, S. Alam, M.T. Avey, M. Baker et al. The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol. 18, 3000410 (2020). https://doi.org/10.1371/journal.pbio.3000410
doi: 10.1371/journal.pbio.3000410
A.J. Smith, R.E. Clutton, E. Lilley, K.E.A. Hansen, T. Brattelid, PREPARE: guidelines for planning animal research and testing. Lab. Anim. 52, 135–141 (2018). https://doi.org/10.1177/0023677217724823
doi: 10.1177/0023677217724823
pubmed: 28771074
D.E. Kleiner, E.M. Brunt, M. Van Natta, C. Behling, M.J. Contos, O.W. Cummings et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology (Baltimore, Md) 41, 1313–1321 (2005). https://doi.org/10.1002/hep.20701
doi: 10.1002/hep.20701
pubmed: 15915461
I. Vachliotis, A. Goulas, P. Papaioannidou, S.A. Polyzos, Nonalcoholic fatty liver disease: lifestyle and quality of life. Hormones (Athens, Greece) 21, 41–49 (2022). https://doi.org/10.1007/s42000-021-00339-6
doi: 10.1007/s42000-021-00339-6
pubmed: 34854066
T. Jensen, M.F. Abdelmalek, S. Sullivan, K.J. Nadeau, M. Green, C. Roncal et al. Fructose and sugar: A major mediator of non-alcoholic fatty liver disease. J. Hepatol. 68, 1063–1075 (2018). https://doi.org/10.1016/j.jhep.2018.01.019
doi: 10.1016/j.jhep.2018.01.019
pubmed: 29408694
pmcid: 5893377
S. Jung, H. Bae, W.S. Song, C. Jang, Dietary fructose and fructose-induced pathologies. Ann. Rev. Nutr. 42, 45–66 (2022). https://doi.org/10.1146/annurev-nutr-062220-025831
doi: 10.1146/annurev-nutr-062220-025831
M.K. Pickens, J.S. Yan, R.K. Ng, H. Ogata, J.P. Grenert, C. Beysen et al. Dietary sucrose is essential to the development of liver injury in the methionine-choline-deficient model of steatohepatitis[S]. J. Lipid Res. 50, 2072–2082 (2009). https://doi.org/10.1194/jlr.M900022-JLR200
doi: 10.1194/jlr.M900022-JLR200
pubmed: 19295183
pmcid: 2739762
M.N. Kristiansen, S.S. Veidal, K.T. Rigbolt, K.S. Tølbøl, J.D. Roth, J. Jelsing et al. Obese diet-induced mouse models of nonalcoholic steatohepatitis-tracking disease by liver biopsy. World J. Hepatol. 8, 673–684 (2016). https://doi.org/10.4254/wjh.v8.i16.673
doi: 10.4254/wjh.v8.i16.673
pubmed: 27326314
pmcid: 4909429
C.M. Flessa, N. Nasiri-Ansari, I. Kyrou, B.M. Leca, M. Lianou, A. Chatzigeorgiou et al. Genetic and Diet-Induced Animal Models for Non-Alcoholic Fatty Liver Disease (NAFLD) Research. Int. J. Mol. Sci. 23, 15791 (2022). https://doi.org/10.3390/ijms232415791
doi: 10.3390/ijms232415791
pubmed: 36555433
pmcid: 9780957
M. Ito, J. Suzuki, S. Tsujioka, M. Sasaki, A. Gomori, T. Shirakura et al. Longitudinal analysis of murine steatohepatitis model induced by chronic exposure to high-fat diet. Hepatol. Res. 37(1), 50–57 (2007). https://doi.org/10.1111/j.1872-034X.2007.00008.x
doi: 10.1111/j.1872-034X.2007.00008.x
pubmed: 17300698
W. Liang, A.L. Menke, A. Driessen, G.H. Koek, J.H. Lindeman, R. Stoop et al. Establishment of a general NAFLD scoring system for rodent models and comparison to human liver pathology. PloS One 9, 115922 (2014). https://doi.org/10.1371/journal.pone.0115922
doi: 10.1371/journal.pone.0115922
N. Abe, S. Kato, T. Tsuchida, K. Sugimoto, R. Saito, L. Verschuren et al. Longitudinal characterization of diet-induced genetic murine models of non-alcoholic steatohepatitis with metabolic, histological, and transcriptomic hallmarks of human patients. Biology Open 8, bio041251 (2019). https://doi.org/10.1242/bio.041251
doi: 10.1242/bio.041251
pubmed: 31023717
pmcid: 6550083
G.N. Ioannou, S. Subramanian, A. Chait, W.G. Haigh, M.M. Yeh, G.C. Farrell et al. Cholesterol crystallization within hepatocyte lipid droplets and its role in murine NASH. J. Lipid Res. 58, 1067–1079 (2017). https://doi.org/10.1194/jlr.M072454
doi: 10.1194/jlr.M072454
pubmed: 28404639
pmcid: 5456359
A. Asgharpour, S.C. Cazanave, T. Pacana, M. Seneshaw, R. Vincent, B.A. Banini et al. A diet-induced animal model of non-alcoholic fatty liver disease and hepatocellular cancer. J. Hepatol. 65, 579–588 (2016). https://doi.org/10.1016/j.jhep.2016.05.005
doi: 10.1016/j.jhep.2016.05.005
pubmed: 27261415
pmcid: 5012902
Fei, N., Miyoshi, S., Hermanson, J.B., Miyoshi, J., Xie, B., DeLeon, O., et al. (2023) Imbalanced gut microbiota predicts and drives the progression of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis in a fast-food diet mouse model. bioRxiv : the preprint server for biology https://doi.org/10.1101/2023.01.09.523249 .
T.H. Kim, D. Choi, J.Y. Kim, J.H. Lee, S.-H. Koo, Fast food diet-induced non-alcoholic fatty liver disease exerts early protective effect against acetaminophen intoxication in mice. BMC Gastroenterol. 17, 124 (2017). https://doi.org/10.1186/s12876-017-0680-z
doi: 10.1186/s12876-017-0680-z
pubmed: 29179698
pmcid: 5704433
L.H. Tetri, M. Basaranoglu, E.M. Brunt, L.M. Yerian, B.A. Neuschwander-Tetri, Severe NAFLD with hepatic necroinflammatory changes in mice fed trans fats and a high-fructose corn syrup equivalent. Am. J. Physiol. Gastrointestinal Liver Physiol. 295, 987–995 (2008). https://doi.org/10.1152/ajpgi.90272.2008
doi: 10.1152/ajpgi.90272.2008
S. Chitturi, S. Abeygunasekera, G.C. Farrell, J. Holmes-Walker, J.M. Hui, C. Fung et al. NASH and insulin resistance: Insulin hypersecretion and specific association with the insulin resistance syndrome. Hepatology (Baltimore, Md) 35, 373–379 (2002). https://doi.org/10.1053/jhep.2002.30692
doi: 10.1053/jhep.2002.30692
pubmed: 11826411
S.E. Keating, D.A. Hackett, J. George, N.A. Johnson, Exercise and non-alcoholic fatty liver disease: A systematic review and meta-analysis. J. Hepatol. 57, 157–166 (2012). https://doi.org/10.1016/j.jhep.2012.02.023
doi: 10.1016/j.jhep.2012.02.023
pubmed: 22414768
M. Matsumoto, N. Hada, Y. Sakamaki, A. Uno, T. Shiga, C. Tanaka et al. An improved mouse model that rapidly develops fibrosis in non-alcoholic steatohepatitis. Int. J. Exp. Pathol. 94, 93–103 (2013). https://doi.org/10.1111/iep.12008
doi: 10.1111/iep.12008
pubmed: 23305254
pmcid: 3607137
M. Maersk, A. Belza, J.J. Holst, M. Fenger-Grøn, S.B. Pedersen, A. Astrup et al. Satiety scores and satiety hormone response after sucrose-sweetened soft drink compared with isocaloric semi-skimmed milk and with non-caloric soft drink: a controlled trial. Eur. J. Clin. Nutr. 66, 523–529 (2012). https://doi.org/10.1038/ejcn.2011.223
doi: 10.1038/ejcn.2011.223
pubmed: 22252107
K. Lowette, L. Roosen, J. Tack, P. Vanden Berghe, Effects of high-fructose diets on central appetite signaling and cognitive function. Front. Nutr. 2, 5 (2015). https://doi.org/10.3389/fnut.2015.00005
doi: 10.3389/fnut.2015.00005
pubmed: 25988134
pmcid: 4429636
K. Riazi, H. Azhari, J.H. Charette, F.E. Underwood, J.A. King, E.E. Afshar et al. The prevalence and incidence of NAFLD worldwide: a systematic review and meta-analysis. Lancet Gastroenterol. Hepatol. 7, 851–861 (2022). https://doi.org/10.1016/s2468-1253(22)00165-0
doi: 10.1016/s2468-1253(22)00165-0
pubmed: 35798021
J.D. Yang, M.F. Abdelmalek, H. Pang, C.D. Guy, A.D. Smith, A.M. Diehl et al. Gender and menopause impact severity of fibrosis among patients with nonalcoholic steatohepatitis. Hepatology (Baltimore, Md) 59, 1406–1414 (2014). https://doi.org/10.1002/hep.26761
doi: 10.1002/hep.26761
pubmed: 24123276
S.A. Mondal, S.N. Mann, C. van der Linden, R. Sathiaseelan, M. Kamal, S. Das et al. Metabolic benefits of 17α-estradiol in liver are partially mediated by ERβ in male mice. Sci. Rep. 13, 9841 (2023). https://doi.org/10.1038/s41598-023-37007-1
doi: 10.1038/s41598-023-37007-1
pubmed: 37330610
pmcid: 10276872
S. Ganguly, G.A. Muench, L. Shang, S.B. Rosenthal, G. Rahman, R. Wang et al. Nonalcoholic steatohepatitis and HCC in a hyperphagic mouse accelerated by western diet. Cellular Mol. Gastroenterol. Hepatol. 12, 891–920 (2021). https://doi.org/10.1016/j.jcmgh.2021.05.010
doi: 10.1016/j.jcmgh.2021.05.010
S. Smati, A. Polizzi, A. Fougerat, S. Ellero-Simatos, Y. Blum, Y. Lippi et al. Integrative study of diet-induced mouse models of NAFLD identifies PPARα as a sexually dimorphic drug target. Gut 71, 807–821 (2022). https://doi.org/10.1136/gutjnl-2020-323323
doi: 10.1136/gutjnl-2020-323323
pubmed: 33903148
M.E. Rinella, J.V. Lazarus, V. Ratziu, S.M. Francque, A.J. Sanyal, F. Kanwal et al. A multisociety Delphi consensus statement on new fatty liver disease nomenclature. Hepatology (Baltimore, Md) 78, 1966–1986 (2023). https://doi.org/10.1097/hep.0000000000000520
doi: 10.1097/hep.0000000000000520
pubmed: 37363821
S.A. Polyzos, E.S. Kang, E.A. Tsochatzis, S. Kechagias, M. Ekstedt, S. Xanthakos et al. Commentary: Nonalcoholic or metabolic dysfunction-associated fatty liver disease? The epidemic of the 21st century in search of the most appropriate name. Metab. 113, 154413 (2020). https://doi.org/10.1016/j.metabol.2020.154413
doi: 10.1016/j.metabol.2020.154413