Multi-Omics Nutritional Approaches Targeting Metabolic-Associated Fatty Liver Disease
Abstract
1. Introduction
1.1. Nutrigenetics
1.2. Nutriepigenetics
1.3. Nutrimetagenomics
1.4. Nutritranscriptomics
1.5. Nutrimetabolomics
2. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Eslam, M.; Sanyal, A.J.; George, J.; International Consensus Panel. MAFLD: A Consensus-Driven Proposed Nomenclature for Metabolic Associated Fatty Liver Disease. Gastroenterology 2020, 158, 1999–2014.e1. [Google Scholar] [CrossRef]
- Heeren, J.; Scheja, L. Metabolic-associated fatty liver disease and lipoprotein metabolism. Mol. Metab. 2021, 50, 101238. [Google Scholar] [CrossRef] [PubMed]
- Gill, M.G.; Majumdar, A. Metabolic associated fatty liver disease: Addressing a new era in liver transplantation. World J. Hepatol. 2020, 12, 1168–1181. [Google Scholar] [CrossRef] [PubMed]
- Qu, W.; Ma, T.; Cai, J.; Zhang, X.; Zhang, P.; She, Z.; Wan, F.; Li, H. Liver Fibrosis and MAFLD: From Molecular Aspects to Novel Pharmacological Strategies. Front. Med. 2021, 8, 761538. [Google Scholar] [CrossRef] [PubMed]
- Jonas, W.; Schürmann, A. Genetic and epigenetic factors determining NAFLD risk. Mol. Metab. 2021, 50, 101111. [Google Scholar] [CrossRef] [PubMed]
- Du, X.; DeForest, N.; Majithia, A.R. Human Genetics to Identify Therapeutic Targets for NAFLD: Challenges and Opportunities. Front. Endocrinol. 2021, 12, 777075. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez-Sanabria, J.S.; Escutia-Gutiérrez, R.; Rosas-Campos, R.; Armendáriz-Borunda, J.S.; Sandoval-Rodríguez, A. An Update in Epigenetics in Metabolic-Associated Fatty Liver Disease. Front. Med. 2022, 8, 770504. [Google Scholar] [CrossRef] [PubMed]
- Leung, C.; Rivera, L.; Furness, J.B.; Angus, P.W. The role of the gut microbiota in NAFLD. Nat. Rev. Gastroenterol. Hepatol. 2016, 13, 412–425. [Google Scholar] [CrossRef]
- Masoodi, M.; Gastaldelli, A.; Hyötyläinen, T.; Arretxe, E.; Alonso, C.; Gaggini, M.; Brosnan, J.; Anstee, Q.M.; Millet, O.; Ortiz, P.; et al. Metabolomics and lipidomics in NAFLD: Biomarkers and non-invasive diagnostic tests. Nat. Rev. Gastroenterol. Hepatol. 2021, 18, 835–856. [Google Scholar] [CrossRef]
- Meroni, M.; Longo, M.; Rustichelli, A.; Dongiovanni, P. Nutrition and Genetics in NAFLD: The Perfect Binomium. Int. J. Mol. Sci. 2020, 21, 2986. [Google Scholar] [CrossRef]
- Sevastianova, K.; Santos, A.; Kotronen, A.; Hakkarainen, A.; Makkonen, J.; Silander, K.; Peltonen, M.; Romeo, S.; Lundbom, J.; Lundbom, N.; et al. Effect of short-term carbohydrate overfeeding and long-term weight loss on liver fat in overweight humans. Am. J. Clin. Nutr. 2012, 96, 727–734. [Google Scholar] [CrossRef] [PubMed]
- Davis, J.N.; Lê, K.A.; Walker, R.W.; Vikman, S.; Spruijt-Metz, D.; Weigensberg, M.J.; Allayee, H.; Goran, M.I. Increased hepatic fat in overweight Hispanic youth influenced by interaction between genetic variation in PNPLA3 and high dietary carbohydrate and sugar consumption. Am. J. Clin. Nutr. 2010, 92, 1522–1527. [Google Scholar] [CrossRef] [PubMed]
- Nobili, V.; Liccardo, D.; Bedogni, G.; Salvatori, G.; Gnani, D.; Bersani, I.; Alisi, A.; Valenti, L.; Raponi, M. Influence of dietary pattern, physical activity, and I148M PNPLA3 on steatosis severity in at-risk adolescents. Genes Nutr. 2014, 9, 392. [Google Scholar] [CrossRef] [PubMed]
- Santoro, N.; Savoye, M.; Kim, G.; Marotto, K.; Shaw, M.M.; Pierpont, B.; Caprio, S. Hepatic fat accumulation is modulated by the interaction between the rs738409 variant in the PNPLA3 gene and the dietary omega6/omega3 PUFA intake. PLoS ONE 2012, 7, e37827. [Google Scholar] [CrossRef]
- Jones, R.B.; Arenaza, L.; Rios, C.; Plows, J.F.; Berger, P.K.; Alderete, T.L.; Fogel, J.L.; Nayak, K.; Mohamed, P.; Hwang, D.; et al. PNPLA3 Genotype, Arachidonic Acid Intake, and Unsaturated Fat Intake Influences Liver Fibrosis in Hispanic Youth with Obesity. Nutrients 2021, 13, 1621. [Google Scholar] [CrossRef]
- Vilar-Gomez, E.; Pirola, C.J.; Sookoian, S.; Wilson, L.A.; Belt, P.; Liang, T.; Liu, W.; Chalasani, N. Impact of the Association Between PNPLA3 Genetic Variation and Dietary Intake on the Risk of Significant Fibrosis in Patients with NAFLD. Am. J. Gastroenterol. 2021, 116, 994–1006. [Google Scholar] [CrossRef]
- Salari, N.; Darvishi, N.; Mansouri, K.; Ghasemi, H.; Hosseinian-Far, M.; Darvishi, F.; Mohammadi, M. Association between PNPLA3 rs738409 polymorphism and nonalcoholic fatty liver disease: A systematic review and meta-analysis. BMC Endocr. Disord. 2021, 21, 125. [Google Scholar] [CrossRef]
- Santoro, N.; Caprio, S.; Pierpont, B.; Van Name, M.; Savoye, M.; Parks, E.J. Hepatic De Novo Lipogenesis in Obese Youth Is Modulated by a Common Variant in the GCKR Gene. J. Clin. Endocrinol. Metab. 2015, 100, E1125–E1132. [Google Scholar] [CrossRef]
- Park, S.; Kang, S. High carbohydrate and noodle/meat-rich dietary patterns interact with the minor haplotype in the 22q13 loci to increase its association with non-alcoholic fatty liver disease risk in Koreans. Nutr. Res. 2020, 82, 88–98. [Google Scholar] [CrossRef]
- Miele, L.; Dall’armi, V.; Cefalo, C.; Nedovic, B.; Arzani, D.; Amore, R.; Rapaccini, G.; Gasbarrini, A.; Ricciardi, W.; Grieco, A.; et al. A case-control study on the effect of metabolic gene polymorphisms, nutrition, and their interaction on the risk of non-alcoholic fatty liver disease. Genes Nutr. 2014, 9, 383. [Google Scholar] [CrossRef]
- Kalafati, I.P.; Dimitriou, M.; Borsa, D.; Vlachogiannakos, J.; Revenas, K.; Kokkinos, A.; Ladas, S.D.; Dedoussis, G.V. Fish intake interacts with TM6SF2 gene variant to affect NAFLD risk: Results of a case-control study. Eur. J. Nutr. 2019, 58, 1463–1473. [Google Scholar] [CrossRef] [PubMed]
- Sevastianova, K.; Kotronen, A.; Gastaldelli, A.; Perttilä, J.; Hakkarainen, A.; Lundbom, J.; Suojanen, L.; Orho-Melander, M.; Lundbom, N.; Ferrannini, E.; et al. Genetic variation in PNPLA3 (adiponutrin) confers sensitivity to weight loss-induced decrease in liver fat in humans. Am. J. Clin. Nutr. 2011, 94, 104–111. [Google Scholar] [CrossRef] [PubMed]
- Van Name, M.A.; Savoye, M.; Chick, J.M.; Galuppo, B.T.; Feldstein, A.E.; Pierpont, B.; Johnson, C.; Shabanova, V.; Ekong, U.; Valentino, P.L.; et al. A Low ω-6 to ω-3 PUFA Ratio (n-6:n-3 PUFA) Diet to Treat Fatty Liver Disease in Obese Youth. J. Nutr. 2020, 150, 2314–2321. [Google Scholar] [CrossRef] [PubMed]
- Perez-Diaz-Del-Campo, N.; Marin-Alejandre, B.A.; Cantero, I.; Monreal, J.I.; Elorz, M.; Herrero, J.I.; Benito-Boillos, A.; Riezu-Boj, J.I.; Milagro, F.I.; Tur, J.A.; et al. Differential response to a 6-month energy-restricted treatment depending on SH2B1 rs7359397 variant in NAFLD subjects: Fatty Liver in Obesity (FLiO) Study. Eur. J. Nutr. 2021, 60, 3043–3057. [Google Scholar] [CrossRef]
- Aller, R.; Laserna, C.; Rojo, M.Á.; Mora, N.; García Sánchez, C.; Pina, M.; Sigüenza, R.; Durà, M.; Primo, D.; Izaola, O.; et al. Role of the PNPLA3 polymorphism rs738409 on silymarin + vitamin E response in subjects with non-alcoholic fatty liver disease. Rev. Esp. Enferm. Dig. 2018, 110, 634–640. [Google Scholar] [CrossRef]
- Scorletti, E.; West, A.L.; Bhatia, L.; Hoile, S.P.; McCormick, K.G.; Burdge, G.C.; Lillycrop, K.A.; Clough, G.F.; Calder, P.C.; Byrne, C.D. Treating liver fat and serum triglyceride levels in NAFLD, effects of PNPLA3 and TM6SF2 genotypes: Results from the WELCOME trial. J. Hepatol. 2015, 63, 1476–1483. [Google Scholar] [CrossRef]
- Nobili, V.; Bedogni, G.; Donati, B.; Alisi, A.; Valenti, L. The I148M variant of PNPLA3 reduces the response to docosahexaenoic acid in children with non-alcoholic fatty liver disease. J. Med. Food 2013, 16, 957–960. [Google Scholar] [CrossRef]
- Ramos-Lopez, O.; Milagro, F.I.; Allayee, H.; Chmurzynska, A.; Choi, M.S.; Curi, R.; De Caterina, R.; Ferguson, L.R.; Goni, L.; Kang, J.X.; et al. Guide for Current Nutrigenetic, Nutrigenomic, and Nutriepigenetic Approaches for Precision Nutrition Involving the Prevention and Management of Chronic Diseases Associated with Obesity. J. Nutrigenet. Nutr. 2017, 10, 43–62. [Google Scholar] [CrossRef]
- Wu, N.; Yuan, F.; Yue, S.; Jiang, F.; Ren, D.; Liu, L.; Bi, Y.; Guo, Z.; Ji, L.; Han, K.; et al. Effect of exercise and diet intervention in NAFLD and NASH via GAB2 methylation. Cell Biosci. 2021, 11, 189. [Google Scholar] [CrossRef]
- Yaskolka Meir, A.; Keller, M.; Müller, L.; Bernhart, S.H.; Tsaban, G.; Zelicha, H.; Rinott, E.; Kaplan, A.; Gepner, Y.; Shelef, I.; et al. Effects of lifestyle interventions on epigenetic signatures of liver fat: Central randomized controlled trial. Liver Int. 2021, 41, 2101–2111. [Google Scholar] [CrossRef]
- Hosseini, H.; Teimouri, M.; Shabani, M.; Koushki, M.; Babaei Khorzoughi, R.; Namvarjah, F.; Izadi, P.; Meshkani, R. Resveratrol alleviates non-alcoholic fatty liver disease through epigenetic modification of the Nrf2 signaling pathway. Int. J. Biochem. Cell Biol. 2020, 119, 105667. [Google Scholar] [CrossRef] [PubMed]
- Chung, M.Y.; Song, J.H.; Lee, J.; Shin, E.J.; Park, J.H.; Lee, S.H.; Hwang, J.T.; Choi, H.K. Tannic acid, a novel histone acetyltransferase inhibitor, prevents non-alcoholic fatty liver disease both in vivo and in vitro model. Mol. Metab. 2019, 19, 34–48. [Google Scholar] [CrossRef] [PubMed]
- Chung, M.Y.; Kim, H.J.; Choi, H.K.; Park, J.H.; Hwang, J.T. Black Mulberry Extract Elicits Hepatoprotective Effects in Nonalcoholic Fatty Liver Disease Models by Inhibition of Histone Acetylation. J. Med. Food 2021, 24, 978–986. [Google Scholar] [CrossRef] [PubMed]
- Chung, M.Y.; Shin, E.J.; Choi, H.K.; Kim, S.H.; Sung, M.J.; Park, J.H.; Hwang, J.T. Schisandra chinensis berry extract protects against steatosis by inhibiting histone acetylation in oleic acid-treated HepG2 cells and in the livers of diet-induced obese mice. Nutr. Res. 2017, 46, 1–10. [Google Scholar] [CrossRef]
- MacDonald-Ramos, K.; Martínez-Ibarra, A.; Monroy, A.; Miranda-Ríos, J.; Cerbón, M. Effect of Dietary Fatty Acids on MicroRNA Expression Related to Metabolic Disorders and Inflammation in Human and Animal Trials. Nutrients 2021, 13, 1830. [Google Scholar] [CrossRef]
- Ali, O.; Darwish, H.A.; Eldeib, K.M.; Abdel Azim, S.A. miR-26a Potentially Contributes to the Regulation of Fatty Acid and Sterol Metabolism In Vitro Human HepG2 Cell Model of Nonalcoholic Fatty Liver Disease. Oxid. Med. Cell. Longev. 2018, 2018, 8515343. [Google Scholar] [CrossRef]
- Latorre, J.; Moreno-Navarrete, J.M.; Mercader, J.M.; Sabater, M.; Rovira, Ò.; Gironès, J.; Ricart, W.; Fernández-Real, J.M.; Ortega, F.J. Decreased lipid metabolism but increased FA biosynthesis are coupled with changes in liver microRNAs in obese subjects with NAFLD. Int. J. Obes. 2017, 41, 620–630. [Google Scholar] [CrossRef]
- Long, J.K.; Dai, W.; Zheng, Y.W.; Zhao, S.P. miR-122 promotes hepatic lipogenesis via inhibiting the LKB1/AMPK pathway by targeting Sirt1 in non-alcoholic fatty liver disease. Mol. Med. 2019, 25, 26. [Google Scholar] [CrossRef]
- Wang, L.; Sun, M.; Cao, Y.; Ma, L.; Shen, Y.; Velikanova, A.A.; Li, X.; Sun, C.; Zhao, Y. miR-34a regulates lipid metabolism by targeting SIRT1 in non-alcoholic fatty liver disease with iron overload. Arch. Biochem. Biophys. 2020, 695, 108642. [Google Scholar] [CrossRef]
- Yousefi, Z.; Nourbakhsh, M.; Abdolvahabi, Z.; Ghorbanhosseini, S.S.; Hesari, Z.; Yarahmadi, S.; Ezzati-Mobasser, S.; Seiri, P.; Borji, M.; Meshkani, R.; et al. microRNA-141 is associated with hepatic steatosis by downregulating the sirtuin1/AMP-activated protein kinase pathway in hepatocytes. J. Cell. Physiol. 2020, 235, 880–890. [Google Scholar] [CrossRef]
- Borji, M.; Nourbakhsh, M.; Shafiee, S.M.; Owji, A.A.; Abdolvahabi, Z.; Hesari, Z.; Ilbeigi, D.; Seiri, P.; Yousefi, Z. Down-Regulation of SIRT1 Expression by mir-23b Contributes to Lipid Accumulation in HepG2 Cells. Biochem. Genet. 2019, 57, 507–521. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Tang, T.; Wang, G.D.; Liu, B. LncRNA-H19 promotes hepatic lipogenesis by directly regulating miR-130a/PPARγ axis in non-alcoholic fatty liver disease. Biosci. Rep. 2019, 39, BSR20181722. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Z.; Moon, R.; Thorne, J.L.; Moore, J.B. NAFLD and vitamin D: Evidence for intersection of microRNA-regulated pathways. Nutr. Res. Rev. 2021, 9, 1–20. [Google Scholar] [CrossRef] [PubMed]
- Peterson, D.; Bonham, K.S.; Rowland, S.; Pattanayak, C.W.; RESONANCE Consortium; Klepac-Ceraj, V. Comparative Analysis of 16S rRNA Gene and Metagenome Sequencing in Pediatric Gut Microbiomes. Front. Microbiol. 2021, 12, 670336. [Google Scholar] [CrossRef]
- Quesada-Vázquez, S.; Aragonès, G.; Del Bas, J.M.; Escoté, X. Diet, Gut Microbiota and Non-Alcoholic Fatty Liver Disease: Three Parts of the Same Axis. Cells 2020, 9, 176. [Google Scholar] [CrossRef]
- Pan, Y.; Zhang, X. Diet and gut microbiome in fatty liver and its associated liver cancer. J. Gastroenterol. Hepatol. 2022, 37, 7–14. [Google Scholar] [CrossRef]
- Moszak, M.; Szulińska, M.; Walczak-Gałęzewska, M.; Bogdański, P. Nutritional Approach Targeting Gut Microbiota in NAFLD-To Date. Int. J. Environ. Res. Public Health 2021, 18, 1616. [Google Scholar] [CrossRef]
- Krawczyk, M.; Maciejewska, D.; Ryterska, K.; Czerwińka-Rogowska, M.; Jamioł-Milc, D.; Skonieczna-Żydecka, K.; Milkiewicz, P.; Raszeja-Wyszomirska, J.; Stachowska, E. Gut Permeability Might be Improved by Dietary Fiber in Individuals with Nonalcoholic Fatty Liver Disease (NAFLD) Undergoing Weight Reduction. Nutrients 2018, 10, 1793. [Google Scholar] [CrossRef]
- Vrieze, A.; Holleman, F.; Zoetendal, E.G.; de Vos, W.M.; Hoekstra, J.B.; Nieuwdorp, M. The environment within: How gut microbiota may influence metabolism and body composition. Diabetologia 2010, 53, 606–613. [Google Scholar] [CrossRef]
- Dewulf, E.M.; Cani, P.D.; Claus, S.P.; Fuentes, S.; Puylaert, P.G.; Neyrinck, A.M.; Bindels, L.B.; de Vos, W.M.; Gibson, G.R.; Thissen, J.P.; et al. Insight into the prebiotic concept: Lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut 2013, 62, 1112–1121. [Google Scholar] [CrossRef]
- Nicolucci, A.C.; Hume, M.P.; Martínez, I.; Mayengbam, S.; Walter, J.; Reimer, R.A. Prebiotics Reduce Body Fat and Alter Intestinal Microbiota in Children Who Are Overweight or with Obesity. Gastroenterology 2017, 153, 711–722. [Google Scholar] [CrossRef] [PubMed]
- Cho, M.S.; Kim, S.Y.; Suk, K.T.; Kim, B.Y. Modulation of gut microbiome in nonalcoholic fatty liver disease: Pro-, pre-, syn-, and antibiotics. J. Microbiol. 2018, 56, 855–867. [Google Scholar] [CrossRef] [PubMed]
- Houghton, D.; Stewart, C.J.; Day, C.P.; Trenell, M. Gut Microbiota and Lifestyle Interventions in NAFLD. Int. J. Mol. Sci. 2016, 17, 447. [Google Scholar] [CrossRef] [PubMed]
- Ji, Y.; Yin, Y.; Li, Z.; Zhang, W. Gut Microbiota-Derived Components and Metabolites in the Progression of Non-Alcoholic Fatty Liver Disease (NAFLD). Nutrients 2019, 11, 1712. [Google Scholar] [CrossRef]
- Salazar, N.; Dewulf, E.M.; Neyrinck, A.M.; Bindels, L.B.; Cani, P.D.; Mahillon, J.; de Vos, W.M.; Thissen, J.P.; Gueimonde, M.; de Los Reyes-Gavilán, C.G.; et al. Inulin-type fructans modulate intestinal Bifidobacterium species populations and decrease fecal short-chain fatty acids in obese women. Clin. Nutr. 2015, 34, 501–507. [Google Scholar] [CrossRef]
- Wang, X.; Qi, Y.; Zheng, H. Dietary Polyphenol, Gut Microbiota, and Health Benefits. Antioxidants 2022, 11, 1212. [Google Scholar] [CrossRef]
- Annunziata, G.; Maisto, M.; Schisano, C.; Ciampaglia, R.; Narciso, V.; Tenore, G.C.; Novellino, E. Effects of Grape Pomace Polyphenolic Extract (Taurisolo®) in Reducing TMAO Serum Levels in Humans: Preliminary Results from a Randomized, Placebo-Controlled, Cross-Over Study. Nutrients 2019, 11, 139. [Google Scholar] [CrossRef]
- Jinato, T.; Chayanupatkul, M.; Dissayabutra, T.; Chutaputti, A.; Tangkijvanich, P.; Chuaypen, N. Litchi-Derived Polyphenol Alleviates Liver Steatosis and Gut Dysbiosis in Patients with Non-Alcoholic Fatty Liver Disease: A Randomized Double-Blinded, Placebo-Controlled Study. Nutrients 2022, 14, 2921. [Google Scholar] [CrossRef]
- Yang, G.; Bibi, S.; Du, M.; Suzuki, T.; Zhu, M.J. Regulation of the intestinal tight junction by natural polyphenols: A mechanistic perspective. Crit. Rev. Food Sci. Nutr. 2017, 57, 3830–3839. [Google Scholar] [CrossRef]
- Yaskolka Meir, A.; Rinott, E.; Tsaban, G.; Zelicha, H.; Kaplan, A.; Rosen, P.; Shelef, I.; Youngster, I.; Shalev, A.; Blüher, M.; et al. Effect of green-Mediterranean diet on intrahepatic fat: The DIRECT PLUS randomised controlled trial. Gut 2021, 70, 2085–2095. [Google Scholar] [CrossRef]
- Shama, S.; Liu, W. Omega-3 Fatty Acids and Gut Microbiota: A Reciprocal Interaction in Nonalcoholic Fatty Liver Disease. Dig. Dis. Sci. 2020, 65, 906–910. [Google Scholar] [CrossRef]
- Costantini, L.; Molinari, R.; Farinon, B.; Merendino, N. Impact of Omega-3 Fatty Acids on the Gut Microbiota. Int. J. Mol. Sci. 2017, 18, 2645. [Google Scholar] [CrossRef] [PubMed]
- Parolini, C. Effects of Fish n-3 PUFAs on Intestinal Microbiota and Immune System. Mar. Drugs 2019, 17, 374. [Google Scholar] [CrossRef] [PubMed]
- Zaiou, M.; Amrani, R.; Rihn, B.; Hajri, T. Dietary Patterns Influence Target Gene Expression through Emerging Epigenetic Mechanisms in Nonalcoholic Fatty Liver Disease. Biomedicines 2021, 9, 1256. [Google Scholar] [CrossRef] [PubMed]
- Thuy, S.; Ladurner, R.; Volynets, V.; Wagner, S.; Strahl, S.; Königsrainer, A.; Maier, K.P.; Bischoff, S.C.; Bergheim, I. Nonalcoholic fatty liver disease in humans is associated with increased plasma endotoxin and plasminogen activator inhibitor 1 concentrations and with fructose intake. J. Nutr. 2008, 138, 1452–1455. [Google Scholar] [CrossRef]
- Ouyang, X.; Cirillo, P.; Sautin, Y.; McCall, S.; Bruchette, J.L.; Diehl, A.M.; Johnson, R.J.; Abdelmalek, M.F. Fructose consumption as a risk factor for non-alcoholic fatty liver disease. J. Hepatol. 2008, 48, 993–999. [Google Scholar] [CrossRef]
- Hao, L.; Ito, K.; Huang, K.H.; Sae-tan, S.; Lambert, J.D.; Ross, A.C. Shifts in dietary carbohydrate-lipid exposure regulate expression of the non-alcoholic fatty liver disease-associated gene PNPLA3/adiponutrin in mouse liver and HepG2 human liver cells. Metabolism 2014, 63, 1352–1362. [Google Scholar] [CrossRef]
- Rafiei, H.; Omidian, K.; Bandy, B. Dietary Polyphenols Protect Against Oleic Acid-Induced Steatosis in an In Vitro Model of NAFLD by Modulating Lipid Metabolism and Improving Mitochondrial Function. Nutrients 2019, 11, 541. [Google Scholar] [CrossRef] [PubMed]
- Rafiei, H.; Omidian, K.; Bandy, B. Comparison of dietary polyphenols for protection against molecular mechanisms underlying nonalcoholic fatty liver disease in a cell model of steatosis. Mol. Nutr. Food Res. 2017, 61, 1600781. [Google Scholar] [CrossRef] [PubMed]
- LeMieux, M.J.; Aljawadi, A.; Moustaid-Moussa, N. Nutrimetabolomics. Adv. Nutr. 2014, 5, 792–794. [Google Scholar] [CrossRef]
- Bordoni, A.; Capozzi, F. Foodomics for healthy nutrition. Curr. Opin. Clin. Nutr. Metab. Care 2014, 17, 418–424. [Google Scholar] [CrossRef] [PubMed]
- Piras, C.; Noto, A.; Ibba, L.; Deidda, M.; Fanos, V.; Muntoni, S.; Leoni, V.P.; Atzori, L. Contribution of Metabolomics to the Understanding of NAFLD and NASH Syndromes: A Systematic Review. Metabolites 2021, 11, 694. [Google Scholar] [CrossRef] [PubMed]
- Troisi, J.; Pierri, L.; Landolfi, A.; Marciano, F.; Bisogno, A.; Belmonte, F.; Palladino, C.; Guercio Nuzio, S.; Campiglia, P.; Vajro, P. Urinary Metabolomics in Pediatric Obesity and NAFLD Identifies Metabolic Pathways/Metabolites Related to Dietary Habits and Gut-Liver Axis Perturbations. Nutrients 2017, 9, 485. [Google Scholar] [CrossRef]
- Bhupathiraju, S.N.; Guasch-Ferré, M.; Gadgil, M.D.; Newgard, C.B.; Bain, J.R.; Muehlbauer, M.J.; Ilkayeva, O.R.; Scholtens, D.M.; Hu, F.B.; Kanaya, A.M.; et al. Dietary Patterns among Asian Indians Living in the United States Have Distinct Metabolomic Profiles That Are Associated with Cardiometabolic Risk. J. Nutr. 2018, 148, 1150–1159. [Google Scholar] [CrossRef] [PubMed]
- Sun, T.; Deng, Y.; Geng, X.; Fang, Q.; Li, X.; Chen, L.; Zhan, M.; Li, D.; Zhu, K.; Li, H.; et al. Plasma Alkylresorcinol Metabolite, a Biomarker for Whole-Grain Intake, Is Inversely Associated with Risk of Nonalcoholic Fatty Liver Disease in a Case-Control Study of Chinese Adults. J. Nutr. 2022, 152, 1052–1058. [Google Scholar] [CrossRef] [PubMed]
- Troisi, J.; Belmonte, F.; Bisogno, A.; Pierri, L.; Colucci, A.; Scala, G.; Cavallo, P.; Mandato, C.; Di Nuzzi, A.; Di Michele, L.; et al. Metabolomic Salivary Signature of Pediatric Obesity Related Liver Disease and Metabolic Syndrome. Nutrients 2019, 11, 274. [Google Scholar] [CrossRef]
- Masarone, M.; Troisi, J.; Aglitti, A.; Torre, P.; Colucci, A.; Dallio, M.; Federico, A.; Balsano, C.; Persico, M. Untargeted metabolomics as a diagnostic tool in NAFLD: Discrimination of steatosis, steatohepatitis and cirrhosis. Metabolomics 2021, 17, 12. [Google Scholar] [CrossRef] [PubMed]
- Sookoian, S.; Castaño, G.O.; Scian, R.; Fernández Gianotti, T.; Dopazo, H.; Rohr, C.; Gaj, G.; San Martino, J.; Sevic, I.; Flichman, D.; et al. Serum aminotransferases in nonalcoholic fatty liver disease are a signature of liver metabolic perturbations at the amino acid and Krebs cycle level. Am. J. Clin. Nutr. 2016, 103, 422–434. [Google Scholar] [CrossRef]
- Feldman, A.; Eder, S.K.; Felder, T.K.; Paulweber, B.; Zandanell, S.; Stechemesser, L.; Schranz, M.; Strebinger, G.; Huber-Schönauer, U.; Niederseer, D.; et al. Clinical and metabolic characterization of obese subjects without non-alcoholic fatty liver: A targeted metabolomics approach. Diabetes Metab. 2019, 45, 132–139. [Google Scholar] [CrossRef]
- Kordy, K.; Li, F.; Lee, D.J.; Kinchen, J.M.; Jew, M.H.; La Rocque, M.E.; Zabih, S.; Saavedra, M.; Woodward, C.; Cunningham, N.J.; et al. Metabolomic Predictors of Non-Alcoholic Steatohepatitis and Advanced Fibrosis in Children. Front. Microbiol. 2021, 12, 713234. [Google Scholar] [CrossRef]
- Zhong, G.; Kirkwood, J.; Won, K.J.; Tjota, N.; Jeong, H.; Isoherranen, N. Characterization of Vitamin A Metabolome in Human Livers with and without Nonalcoholic Fatty Liver Disease. J. Pharmacol. Exp. Ther. 2019, 370, 92–103. [Google Scholar] [CrossRef] [PubMed]
- Czuba, L.C.; Wu, X.; Huang, W.; Hollingshead, N.; Roberto, J.B.; Kenerson, H.L.; Yeung, R.S.; Crispe, I.N.; Isoherranen, N. Altered vitamin A metabolism in human liver slices corresponds to fibrogenesis. Clin. Transl. Sci. 2021, 14, 976–989. [Google Scholar] [CrossRef] [PubMed]
- Von Schönfels, W.; Patsenker, E.; Fahrner, R.; Itzel, T.; Hinrichsen, H.; Brosch, M.; Erhart, W.; Gruodyte, A.; Vollnberg, B.; Richter, K.; et al. Metabolomic tissue signature in human non-alcoholic fatty liver disease identifies protective candidate metabolites. Liver Int. 2015, 35, 207–214. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ramos-Lopez, O. Multi-Omics Nutritional Approaches Targeting Metabolic-Associated Fatty Liver Disease. Genes 2022, 13, 2142. https://doi.org/10.3390/genes13112142
Ramos-Lopez O. Multi-Omics Nutritional Approaches Targeting Metabolic-Associated Fatty Liver Disease. Genes. 2022; 13(11):2142. https://doi.org/10.3390/genes13112142
Chicago/Turabian StyleRamos-Lopez, Omar. 2022. "Multi-Omics Nutritional Approaches Targeting Metabolic-Associated Fatty Liver Disease" Genes 13, no. 11: 2142. https://doi.org/10.3390/genes13112142
APA StyleRamos-Lopez, O. (2022). Multi-Omics Nutritional Approaches Targeting Metabolic-Associated Fatty Liver Disease. Genes, 13(11), 2142. https://doi.org/10.3390/genes13112142