Thermoneutral housing promotes hepatic steatosis in standard diet-fed C57BL/6N mice, with a less pronounced effect on NAFLD progression upon high-fat feeding

. 2023 ; 14 () : 1205703. [epub] 20230712

Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37501785

INTRODUCTION: Non-alcoholic fatty liver disease (NAFLD) can progress to more severe stages, such as steatohepatitis and fibrosis. Thermoneutral housing together with high-fat diet promoted NAFLD progression in C57BL/6J mice. Due to possible differences in steatohepatitis development between different C57BL/6 substrains, we examined how thermoneutrality affects NAFLD progression in C57BL/6N mice. METHODS: Male mice were fed standard or high-fat diet for 24 weeks and housed under standard (22°C) or thermoneutral (30°C) conditions. RESULTS: High-fat feeding promoted weight gain and hepatic steatosis, but the effect of thermoneutral environment was not evident. Liver expression of inflammatory markers was increased, with a modest and inconsistent effect of thermoneutral housing; however, histological scores of inflammation and fibrosis were generally low (<1.0), regardless of ambient temperature. In standard diet-fed mice, thermoneutrality increased weight gain, adiposity, and hepatic steatosis, accompanied by elevated de novo lipogenesis and changes in liver metabolome characterized by complex decreases in phospholipids and metabolites involved in urea cycle and oxidative stress defense. CONCLUSION: Thermoneutrality appears to promote NAFLD-associated phenotypes depending on the C57BL/6 substrain and/or the amount of dietary fat.

Zobrazit více v PubMed

Younossi Z, Tacke F, Arrese M, Chander Sharma B, Mostafa I, Bugianesi E, et al. . Global perspectives on nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Hepatology (2019) 69:2672–82. doi: 10.1002/hep.30251 PubMed DOI

Byrne CD, Targher G. NAFLD: a multisystem disease. J Hepatol (2015) 62:S47–64. doi: 10.1016/j.jhep.2014.12.012 PubMed DOI

Eslam M, Sanyal AJ, George J, International Consensus P. MAFLD: a consensus-driven proposed nomenclature for metabolic associated fatty liver disease. Gastroenterology (2020) 158:1999–2014 e1. doi: 10.1053/j.gastro.2019.11.312 PubMed DOI

Ibrahim SH, Hirsova P, Malhi H, Gores GJ. Animal models of nonalcoholic steatohepatitis: eat, delete, and inflame. Dig Dis Sci (2016) 61:1325–36. doi: 10.1007/s10620-015-3977-1 PubMed DOI PMC

Im YR, Hunter H, de Gracia Hahn D, Duret A, Cheah Q, Dong J, et al. . A systematic review of animal models of NAFLD finds high-fat, high-fructose diets most closely resemble human NAFLD. Hepatology (2021) 74:1884–901. doi: 10.1002/hep.31897 PubMed DOI

Eng JM, Estall JL. Diet-induced models of non-alcoholic fatty liver disease: food for thought on sugar, fat, and cholesterol. Cells (2021) 10:1805. doi: 10.3390/cells10071805 PubMed DOI PMC

Fengler VH, Macheiner T, Kessler SM, Czepukojc B, Gemperlein K, Muller R, et al. . Susceptibility of different mouse wild type strains to develop diet-induced NAFLD/AFLD-associated liver disease. PloS One (2016) 11:e0155163. doi: 10.1371/journal.pone.0155163 PubMed DOI PMC

Asgharpour A, Cazanave SC, Pacana T, Seneshaw M, Vincent R, Banini BA, et al. . A diet-induced animal model of non-alcoholic fatty liver disease and hepatocellular cancer. J Hepatol (2016) 65:579–88. doi: 10.1016/j.jhep.2016.05.005 PubMed DOI PMC

Neff EP. Farewell, FATZO: a NASH mouse update. Lab Anim (NY) (2019) 48:151. doi: 10.1038/s41684-019-0311-0 PubMed DOI

Sun G, Jackson CV, Zimmerman K, Zhang LK, Finnearty CM, Sandusky GE, et al. . The FATZO mouse, a next generation model of type 2 diabetes and NASH when fed a Western diet supplemented with fructose. BMC Gastroenterol (2019) 19:41. doi: 10.1186/s12876-019-0958-4 PubMed DOI PMC

Simon MM, Greenaway S, White JK, Fuchs H, Gailus-Durner V, Wells S, et al. . A comparative phenotypic and genomic analysis of C57BL/6J and C57BL/6N mouse strains. Genome Biol (2013) 14:R82. doi: 10.1186/gb-2013-14-7-r82 PubMed DOI PMC

Hull RL, Willard JR, Struck MD, Barrow BM, Brar GS, Andrikopoulos S, et al. . High fat feeding unmasks variable insulin responses in male C57BL/6 mouse substrains. J Endocrinol (2017) 233:53–64. doi: 10.1530/JOE-16-0377 PubMed DOI PMC

Fisher-Wellman KH, Ryan TE, Smith CD, Gilliam LA, Lin CT, Reese LR, et al. . A direct comparison of metabolic responses to high-fat diet in C57BL/6J and C57BL/6NJ mice. Diabetes (2016) 65:3249–61. doi: 10.2337/db16-0291 PubMed DOI PMC

Rendina-Ruedy E, Hembree KD, Sasaki A, Davis MR, Lightfoot SA, Clarke SL, et al. . A comparative study of the metabolic and skeletal response of C57BL/6J and C57BL/6N mice in a diet-induced model of type 2 diabetes. J Nutr Metab (2015) 2015:758080. doi: 10.1155/2015/758080 PubMed DOI PMC

Kawashita E, Ishihara K, Nomoto M, Taniguchi M, Akiba S. A comparative analysis of hepatic pathological phenotypes in C57BL/6J and C57BL/6N mouse strains in non-alcoholic steatohepatitis models. Sci Rep (2019) 9:204. doi: 10.1038/s41598-018-36862-7 PubMed DOI PMC

Giles DA, Moreno-Fernandez ME, Stankiewicz TE, Graspeuntner S, Cappelletti M, Wu D, et al. . Thermoneutral housing exacerbates nonalcoholic fatty liver disease in mice and allows for sex-independent disease modeling. Nat Med (2017) 23:829–38. doi: 10.1038/nm.4346 PubMed DOI PMC

Bezdek S, Hdnah A, Sezin T, Mousavi S, Zillikens D, Ibrahim S, et al. . The genetic difference between C57Bl/6J and C57Bl/6N mice significantly impacts aldara-induced psoriasiform dermatitis. Exp Dermatol (2017) 26:349–51. doi: 10.1111/exd.13131 PubMed DOI

Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al. . Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology (2005) 41:1313–21. doi: 10.1002/hep.20701 PubMed DOI

Lackner C, Stauber RE, Davies S, Denk H, Dienes HP, Gnemmi V, et al. . Development and prognostic relevance of a histologic grading and staging system for alcohol-related liver disease. J Hepatol (2021) 75:810–9. doi: 10.1016/j.jhep.2021.05.029 PubMed DOI

Itoh M, Kato H, Suganami T, Konuma K, Marumoto Y, Terai S, et al. . Hepatic crown-like structure: a unique histological feature in non-alcoholic steatohepatitis in mice and humans. PloS One (2013) 8:e82163. doi: 10.1371/journal.pone.0082163 PubMed DOI PMC

Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E, et al. . Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res (2005) 46:2347–55. doi: 10.1194/jlr.M500294-JLR200 PubMed DOI

Medrikova D, Jilkova ZM, Bardova K, Janovska P, Rossmeisl M, Kopecky J. Sex differences during the course of diet-induced obesity in mice: adipose tissue expandability and glycemic control. Int J Obes (Lond) (2012) 36:262–72. doi: 10.1038/ijo.2011.87 PubMed DOI

Rossmeisl M, Pavlisova J, Bardova K, Kalendova V, Buresova J, Kuda O, et al. . Increased plasma levels of palmitoleic acid may contribute to beneficial effects of krill oil on glucose homeostasis in dietary obese mice. Biochim Biophys Acta Mol Cell Biol Lipids (2020) 1865:158732. doi: 10.1016/j.bbalip.2020.158732 PubMed DOI

Flachs P, Ruhl R, Hensler M, Janovska P, Zouhar P, Kus V, et al. . Synergistic induction of lipid catabolism and anti-inflammatory lipids in white fat of dietary obese mice in response to calorie restriction and n-3 fatty acids. Diabetologia (2011) 54:2626–38. doi: 10.1007/s00125-011-2233-2 PubMed DOI

Sistilli G, Kalendova V, Cajka T, Irodenko I, Bardova K, Oseeva M, et al. . Krill oil supplementation reduces exacerbated hepatic steatosis induced by thermoneutral housing in mice with diet-induced obesity. Nutrients (2021) 13:437. doi: 10.3390/nu13020437 PubMed DOI PMC

Pang Z, Zhou G, Ewald J, Chang L, Hacariz O, Basu N, et al. . Using MetaboAnalyst 5.0 for LC-HRMS spectra processing, multi-omics integration and covariate adjustment of global metabolomics data. Nat Protoc (2022) 17:1735–61. doi: 10.1038/s41596-022-00710-w PubMed DOI

Sanders FWB, Acharjee A, Walker C, Marney L, Roberts LD, Imamura F, et al. . Hepatic steatosis risk is partly driven by increased de novo lipogenesis following carbohydrate consumption. Genome Biol (2018) 19:79. doi: 10.1186/s13059-018-1439-8 PubMed DOI PMC

Goodman ZD. Hepatic expression of galectin-3, a pro-fibrotic and proinflammatory marker. An immunohistochemical survey. Hepatology (2022) 76:S419–20. doi: 10.1002/hep.32697 DOI

Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, et al. . A lineage of myeloid cells independent of myb and hematopoietic stem cells. Science (2012) 336:86–90. doi: 10.1126/science.1219179 PubMed DOI

McCracken JM, Chalise P, Briley SM, Dennis KL, Jiang L, Duncan FE, et al. . C57BL/6 substrains exhibit different responses to acute carbon tetrachloride exposure: implications for work involving transgenic mice. Gene Expr (2017) 17:187–205. doi: 10.3727/105221617X695050 PubMed DOI PMC

Toye AA, Lippiat JD, Proks P, Shimomura K, Bentley L, Hugill A, et al. . A genetic and physiological study of impaired glucose homeostasis control in C57BL/6J mice. Diabetologia (2005) 48:675–86. doi: 10.1007/s00125-005-1680-z PubMed DOI

Zhang H, Leveille M, Courty E, Gunes A, Nguyen. NB, Estall JL. Differences in metabolic and liver pathobiology induced by two dietary mouse models of nonalcoholic fatty liver disease. Am J Physiol Endocrinol Metab (2020) 319:E863–76. doi: 10.1152/ajpendo.00321.2020 PubMed DOI

Cui X, Nguyen NL, Zarebidaki E, Cao Q, Li F, Zha L, et al. . Thermoneutrality decreases thermogenic program and promotes adiposity in high-fat diet-fed mice. Physiol Rep (2016) 4:e12799. doi: 10.14814/phy2.12799 PubMed DOI PMC

Kus V, Prazak T, Brauner P, Hensler M, Kuda O, Flachs P, et al. . Induction of muscle thermogenesis by high-fat diet in mice: association with obesity-resistance. Am J Physiol Endocrinol Metab (2008) 295:E356–67. doi: 10.1152/ajpendo.90256.2008 PubMed DOI

Martin-Mateos R, Albillos A. The role of the gut-liver axis in metabolic dysfunction-associated fatty liver disease. Front Immunol (2021) 12:660179. doi: 10.3389/fimmu.2021.660179 PubMed DOI PMC

Giles DA, Moreno-Fernandez ME, Stankiewicz TE, Cappelletti M, Huppert SS, Iwakura Y, et al. . Regulation of inflammation by IL-17A and IL-17F modulates non-alcoholic fatty liver disease pathogenesis. PloS One (2016) 11:e0149783. doi: 10.1371/journal.pone.0149783 PubMed DOI PMC

Smoczek M, Vital M, Wedekind D, Basic M, Zschemisch NH, Pieper DH, et al. . A combination of genetics and microbiota influences the severity of the obesity phenotype in diet-induced obesity. Sci Rep (2020) 10:6118. doi: 10.1038/s41598-020-63340-w PubMed DOI PMC

Huang E, Kang S, Park H, Park S, Ji Y, Holzapfel WH. Differences in anxiety levels of various murine models in relation to the gut microbiota composition. Biomedicines (2018) 6:113. doi: 10.3390/biomedicines6040113 PubMed DOI PMC

Tomkovich S, Stough JMA, Bishop L, Schloss PD. The initial gut microbiota and response to antibiotic perturbation influence clostridioides difficile clearance in mice. mSphere (2020) 5:e00869–20. doi: 10.1128/mSphere.00869-20 PubMed DOI PMC

Scherer PE. The many secret lives of adipocytes: implications for diabetes. Diabetologia (2019) 62:223–32. doi: 10.1007/s00125-018-4777-x PubMed DOI PMC

Masoodi M, Kuda O, Rossmeisl M, Flachs P, Kopecky J. Lipid signaling in adipose tissue: connecting inflammation & metabolism. Biochim Biophys Acta (2015) 1851:503–18. doi: 10.1016/j.bbalip.2014.09.023 PubMed DOI

Zhang J, Yang A, Wu Y, Guan W, Xiong B, Peng X, et al. . Stachydrine ameliorates carbon tetrachloride-induced hepatic fibrosis by inhibiting inflammation, oxidative stress and regulating MMPs/TIMPs system in rats. BioMed Pharmacother (2018) 97:1586–94. doi: 10.1016/j.biopha.2017.11.117 PubMed DOI

Sharma L, Lone NA, Knott RM, Hassan A, Abdullah T. Trigonelline prevents high cholesterol and high fat diet induced hepatic lipid accumulation and lipo-toxicity in C57BL/6J mice, via restoration of hepatic autophagy. Food Chem Toxicol (2018) 121:283–96. doi: 10.1016/j.fct.2018.09.011 PubMed DOI

Halliwell B, Cheah IK, Tang RMY. Ergothioneine - a diet-derived antioxidant with therapeutic potential. FEBS Lett (2018) 592:3357–66. doi: 10.1002/1873-3468.13123 PubMed DOI

Lavallard VJ, Gual P. Autophagy and non-alcoholic fatty liver disease. BioMed Res Int (2014) 2014:120179. doi: 10.1155/2014/120179 PubMed DOI PMC

Horton JD, Goldstein JL, Brown MS. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest (2002) 109:1125–31. doi: 10.1172/JCI0215593 PubMed DOI PMC

McKie GL, Medak KD, Knuth CM, Shamshoum H, Townsend LK, Peppler WT, et al. . Housing temperature affects the acute and chronic metabolic adaptations to exercise in mice. J Physiol (2019) 597:4581–600. doi: 10.1113/JP278221 PubMed DOI

Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin.Invest (2005) 115:1343–51. doi: 10.1172/JCI23621 PubMed DOI PMC

Cabre N, Camps J, Joven J. Inflammation, mitochondrial metabolism and nutrition: the multi-faceted progression of non-alcoholic fatty liver disease to hepatocellular carcinoma. Hepatobiliary Surg Nutr (2016) 5:438–43. doi: 10.21037/hbsn.2016.09.11 PubMed DOI PMC

Elmore CL, Matthews RG. The many flavors of hyperhomocyst(e)inemia: insights from transgenic and inhibitor-based mouse models of disrupted one-carbon metabolism. Antioxid Redox Signal (2007) 9:1911–21. doi: 10.1089/ars.2007.1795 PubMed DOI PMC

Aissa AF, Tryndyak V, de Conti A, Melnyk S, Gomes TD, Bianchi ML, et al. . Effect of methionine-deficient and methionine-supplemented diets on the hepatic one-carbon and lipid metabolism in mice. Mol Nutr Food Res (2014) 58:1502–12. doi: 10.1002/mnfr.201300726 PubMed DOI

Heidari R, Niknahad H, Sadeghi A, Mohammadi H, Ghanbarinejad V, Ommati MM, et al. . Betaine treatment protects liver through regulating mitochondrial function and counteracting oxidative stress in acute and chronic animal models of hepatic injury. BioMed Pharmacother (2018) 103:75–86. doi: 10.1016/j.biopha.2018.04.010 PubMed DOI

Craig SA. Betaine in human nutrition. Am J Clin Nutr (2004) 80:539–49. doi: 10.1093/ajcn/80.3.539 PubMed DOI

De Chiara F, Heeboll S, Marrone G, Montoliu C, Hamilton-Dutoit S, Ferrandez A, et al. . Urea cycle dysregulation in non-alcoholic fatty liver disease. J Hepatol (2018) 69:905–15. doi: 10.1016/j.jhep.2018.06.023 PubMed DOI

Gallego-Duran R, Ampuero J, Pastor-Ramirez H, Alvarez-Amor L, Del Campo JA, Maya-Miles D, et al. . Liver injury in non-alcoholic fatty liver disease is associated with urea cycle enzyme dysregulation. Sci Rep (2022) 12:3418. doi: 10.1038/s41598-022-06614-9 PubMed DOI PMC

Liu Y, Hyde AS, Simpson MA, Barycki JJ. Emerging regulatory paradigms in glutathione metabolism. Adv Cancer Res (2014) 122:69–101. doi: 10.1016/B978-0-12-420117-0.00002-5 PubMed DOI PMC

Lee SW, Lee YJ, Baek SM, Kang KK, Kim TU, Yim JH, et al. . Mega-dose vitamin c ameliorates nonalcoholic fatty liver disease in a mouse fast-food diet model. Nutrients (2022) 14:2195. doi: 10.3390/nu14112195 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...