Utility of Human Relevant Preclinical Animal Models in Navigating NAFLD to MAFLD Paradigm
Abstract
:1. Introduction
2. MAFLD Definitions
3. Clinical Landscape with New MAFLD Criteria
4. Pathogenesis of MAFLD
4.1. Ectopic Lipid Spillover Impairs Insulin Sensitivity and Generates Lipotoxicity in the Liver
4.2. MAFLD Risk Amplification by Genetic Predisposition and Adiposity
4.3. Steatosis Causes Endoplasmic Reticulum and Mitochondrial Dysfunction in Hepatocytes
4.4. Unresolved Stresses Can Trigger Apoptosis, Contributing to Inflammation and Fibrosis
4.5. Gut Dysbiosis Is Implicated in Disrupted Energy Homeostasis and Hepatic Inflammation
4.6. Recognizing the Role of Excessive Alcohol Intake in Contributing to MAFLD Progression
4.7. Chronic Viral Hepatitis Is Implicated in Impaired Lipid Metabolism in Hepatocytes
4.8. Deficiency in Choline Results in Mitochondrial Dysfunction in MAFLD
5. MAFLD Preclinical Models
5.1. Metabolic Dysregulation Models
5.1.1. Diet-Induced Models
5.1.2. Genetic and DIO Combination Models
5.1.3. Summary Remarks for Metabolic-Dysregulation Models
5.2. Liver Disease-Centric Models
5.2.1. Diet-Induced Models (Nutrient Depletion)
5.2.2. Chemically Induced Models
5.2.3. Summary Remarks for Liver Disease-Centric Models
5.3. Pathogenesis-Driven Models
5.3.1. From Genetic Studies
5.3.2. ER Stress
5.3.3. Immune System and Inflammation in MAFLD
5.3.4. Gut Dysbiosis in MAFLD
5.3.5. Summary Remarks for Pathogenesis-Driven Models
6. Perspectives
6.1. Comparison with the Right Control Diet
6.2. Keeping It Warm
6.3. Landscape of Preclinical Models in the NAFLD-to-MAFLD Transition
6.4. Applications of Preclinical Models in Basic and Translational Research
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Model Characteristics | Liver Phenotype | Metabolic Disorder Phenotype | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Category | Subcategory | Model | Diet | Steatosis | Hepatic Ballooning | NASH | Fibrosis | HCC | Obesity | Impaired Glucose Tolerance | Dyslipidemia | Extrahepatic Comorbidities |
Mouse Models | ||||||||||||
Metabolic | DIO | HFD | 60% kcal fat | ✓ 10 wks | ✓ 36 wks | ✓ 52 wks | ✓ F1 only 50 wks | x | ✓ | ✓ 10–12 wks | ✓ 10–12 wks | ✓ CKD |
Metabolic | DIO | HFC (HFD + cholesterol) | >40% kcal fat, >1% cholesterol | ✓ 12 wks | ✓ 12 wks | ✓ | ✓ F1 30 wks | ✓ 56 wks | ✓ | x | ✓ | ✓ Atherosclerosis |
Metabolic | DIO | HFD + Atherogenic | 60% fat, 1.25% cholesterol, 0.5% cholate | ✓ 6 wks | ✓ 6 wks | ✓ 6 wks | ✓ F3 24 wks | x | ✓ | ✓ 24 wks | ✓ 6 wks | ✓ Atherosclerosis |
Metabolic | DIO | ALIOS | 45% kcal fat (34% (w/w) trans-fat), 20% sucrose, high-fructose corn syrup drinking water (42 g/L). | ✓ 8 wks | ✓ 8–16 wks | ✓ 16–24 wks | ✓ F3 52 wks | ✓ 52 wks | ✓ | ✓ 6 wks | ✓ 8 wks | |
Metabolic | DIO | Western Diet (WD) | ~42% kcal fat, 0.2–1% cholesterol, high sucrose | ✓ | ✓ | ✓ depends on diet | ✓ F1 52 wks | x | ✓ | ✓ | ✓ | ✓ CKD |
Metabolic | DIO | AMLN/GAN | 4% kcal fat, 22% fructose, 10% sucrose, 2% cholesterol. AMLN: ~28% (w/w) trans-fat; GAN: 46% saturated fatty acids | ✓ | ✓ | ✓ | ✓ F1–F2 28 wks, ✓ F3 50 wks | ✓ 80 wks | ✓ | ✓ | ✓ | |
Metabolic | Genetic | Leptin (ob/ob); LepR (db/db) Deficiency | Normal diet | ✓ 12 wks | x | ✓ 30 wks | x | x | ✓ | ✓ | ✓ | |
Metabolic | DIO-Genetic | HFD + ob/ob or db/db | HFD | ✓ 8 wks | ✓ | ✓ 18 wks | ✓ F2 30 wks | ✓ | ✓ | ✓ 2 wks | ||
Metabolic | DIO-Genetic | KK-Ay | HFD + fructose + atherogenic | n.r. | n.r. | ✓ 4 wks | x | x | ✓ | ✓ | ✓ 4 wks | |
Metabolic | DIO-Genetic | AMLN/GAN + ob/ob | AMLN/GAN | ✓ | ✓ | ✓ | ✓ F2-F3 16 wks | ✓ 3 wks | ✓ 16 wks | ✓ | ||
Metabolic | DIO-Genetic | HFC + LDR Deficiency (ldr−/−) | HFC | ✓ 3 wks | ✓ | ✓ 3 wks | x | ✓ | ✓ 3 wks | ✓ 3 wks | ✓ Atherosclerosis ~16 wks | |
Metabolic | DIO-Genetic | HFD + LDR Deficiency (ldr−/−) | HFD | ✓ | ✓ | ✓ 6 wks | ✓ F3 37 wks | x | ✓ | ✓ | ✓ | ✓ Atherosclerosis ~16–24 wks |
Metabolic | DIO-Strain | MS-NASH (C57Bl/6 x AKR/J) | WD (21% kcal fat, 0.2% cholesterol, 5% fructose, drinking water | ✓ 4–8 wks | ✓ 16 wks | ✓ 16 wks | ✓ F1 20 wks | x | ✓ | ✓ | ✓ | |
Metabolic | Diet-Strain | Diamond (C57Bl/6 × S129S1/SvImJ) | WD (42% kcal fat, 0.1% cholesterol, 3.1 g/L d-fructose, 18.9 g/L d-glucose | ✓ | ✓ 24 wks | ✓ 24 wks | ✓ F2 24–36 wks, ✓ F3 52 wks | ✓ 52 wks | ✓ 16 wks | ✓ 16 wks | ✓ 16 wks | |
FLD-progression | Nutrient depletion | MCD | no methionine and choline, 40% ucrose, 10% kcal fat | ✓ 2 wks | x | ✓ 6 wks | ✓ F1 7 wks, ✓ F2 14 wks, ✓ F3 16 wks | x | x | x (enhanced sensitivity) | x | |
FLD-progression | Nutrient depletion | CDAA | choline-deficient, 68.5% carbohydrate, 17.4% proteins, 14% kcal fat | ✓ | x | ✓ | ✓ F1 20 wks | x | x | x | x | |
FLD-progression | Nutrient depletion | CDAA-HFD | CDAA + 60% kcal fat, 0.1% methionine | ✓ | x | ✓ F1 8 wks, ✓ F3 48 wks | ✓ F2 24 wks, ✓ F3 48 wks | ✓ 52–60 wks | x | x | x | |
FLD-progression | Chemical | HFD + CCl4 (simultaneous) | 60% kcal fat | ✓ (CCl4-dose dependent | ✓ (CCl4-dose dependent) | ✓ (CCl4-dose dependent) | ✓ possible severe fibrosis, CCl4-dose dependent | ✓ 24 wks | ✓ | ✓ | x | |
FLD-progression | Chemical | WD + CCl4 (sequential) | 40% kcal fat + 5% fructose | n.r. | n.r. | n.r. | ✓ F2–3 2–6 wks, ✓ F4 9 wks | ✓ 24 wks | ✓ | ✓ | ✓ | |
FLD-progression | Chemical | HFD + DEN | 60% kcal fat | n.r. | n.r. | x | x | ✓ 20 wks | ✓ | ✓ | ✓ | |
Pathogenesis | Genetic | MUP-uPA | HFD | ✓ | ✓ | ✓ 16 wks | ✓ 24 wks | ✓ 40 wks | ✓ | ✓ | ✓ | |
Rat Models | ||||||||||||
Metabolic | DIO | HFD | ~60% kcal fat | ✓ 6–8 wks | x | ✓ limited | ✓ limited | x | ✓ ~7 wks | ✓ | ✓ 7 wks | |
Metabolic | DIO | HFD + cholesterol | ~65% kcal fat, 1% cholesterol, 0.25% cholate | ✓ | ✓ 16 wks (mild) | ✓ limited | ✓ F2 16–20 wks | x | ✓ ~7 wks | ✓ ~4 wks | ✓ ~12 wks | |
Metabolic | DIO-Genetic | SHR | Chow diet | ✓ 8 wks | ✓ 16 months | ✓ 16 months | x | x | x | ✓ ~16 months | ✓ 10 wks | |
Metabolic | Genetic | OLETF rats | Chow diet | ✓ 22–38 wks | x | x | x | x | ✓ 8 wks | ✓ 18 wks | ✓ 18 wks | |
Metabolic | DIO-Genetic | OLETF + MCDD | MCDD at 24 wks age | ✓ 8 wks | ✓ 8 wks | ✓ 8 wks | ✓ F2 8 wks | x | ✓ 8 wks | ✓ 8 wks | ✓ 8 wks | |
Metabolic | DIO-Genetic | Zucker fatty rats (ZFR) | HFD | ✓ | x | ✓ | ||||||
FLD-progression | Nutrient depletion | Wistar rats + MCD | MCD | ✓ 13 wks | x | x | x | x | x (weight loss) | x | x | |
FLD-progression | Nutrient depletion | Wistar rats + CDAA | CDAA | ✓ 6–12 wks | ✓ | ✓ | ✓ F3 12 wks | ✓ 40 wks (50% of cases) | x | x | x | |
Rabbit Models | ||||||||||||
Metabolic | DIO | HFD + cholesterol | 10% lard + 2% cholesterol | ✓ 12 wks | ✓ | ✓ | ✓ F3–F4 36 wks (12% oil + 0.75% cholesterol) | x | x | x | ✓ | |
Pig Models | ||||||||||||
Metabolic | DIO | Ossabow pigs + High fructose diet | 10.5% kcal fat, 20% kcal fructose | x | x | x | x | x | ✓ 24 wks | ✓ 24 wks | ✓ 24 wks | |
Metabolic | DIO | Ossabow pigs + HFD + fructose diet | 43% kcal fat, 18% kcal fructose | x | ✓ 24 wks | x | ✓ 24 wks | x | ✓ 24 wks | ✓ 24 wks | ✓ 24 wks | |
Metabolic | DIO | Ossabow pigs + HFC + atherogenic | 43% kcal fat, 18–20% kcal fructose + 2% cholesterol + reduced cholate | ✓ 8 wks | ✓16–24 wks | x | ✓ F2 16–24 wks | x | ✓ 8 wks | x | ✓ 8 wks | |
Metabolic | DIO-Genetic | LEPTIN−/− | Chow diet | ✓ 6–12 months | ✓ 12–22 months | ✓ 12–22 months, limited | ✓ F1–F2 22–35 months | x | ✓ 8 wks | x | ✓ 12–18 months |
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Chua, D.; Low, Z.S.; Cheam, G.X.; Ng, A.S.; Tan, N.S. Utility of Human Relevant Preclinical Animal Models in Navigating NAFLD to MAFLD Paradigm. Int. J. Mol. Sci. 2022, 23, 14762. https://doi.org/10.3390/ijms232314762
Chua D, Low ZS, Cheam GX, Ng AS, Tan NS. Utility of Human Relevant Preclinical Animal Models in Navigating NAFLD to MAFLD Paradigm. International Journal of Molecular Sciences. 2022; 23(23):14762. https://doi.org/10.3390/ijms232314762
Chicago/Turabian StyleChua, Damien, Zun Siong Low, Guo Xiang Cheam, Aik Seng Ng, and Nguan Soon Tan. 2022. "Utility of Human Relevant Preclinical Animal Models in Navigating NAFLD to MAFLD Paradigm" International Journal of Molecular Sciences 23, no. 23: 14762. https://doi.org/10.3390/ijms232314762