Fasting-mimicking diet prevents high-fat diet effect on cardiometabolic risk and lifespan.

[en] Diet-induced obesity is a major risk factor for metabolic syndrome, diabetes and cardiovascular disease. Here, we show that a 5-d fasting-mimicking diet (FMD), administered every 4 weeks for a period of 2 years, ameliorates the detrimental changes caused by consumption of a high-fat, high-calorie diet (HFCD) in female mice. We demonstrate that monthly FMD cycles inhibit HFCD-mediated obesity by reducing the accumulation of visceral and subcutaneous fat without causing loss of lean body mass. FMD cycles increase cardiac vascularity and function and resistance to cardiotoxins, prevent HFCD-dependent hyperglycaemia, hypercholesterolaemia and hyperleptinaemia and ameliorate impaired glucose and insulin tolerance. The effect of monthly FMD cycles on gene expression associated with mitochondrial metabolism and biogenesis in adipocytes and the sustained ketogenesis in HFCD-fed mice indicate a role for fat cell reprogramming in obesity prevention. These effects of an FMD on adiposity and cardiac ageing could explain the protection from HFCD-dependent early mortality.

Disciplines :

Human health sciences: Multidisciplinary, general & others

Author, co-author :

Mishra, Amrendra

Mirzaei, Hamed

Guidi, Novella

Vinciguerra, Manlio

Mouton, Alice ; Université de Liège - ULiège > Département des sciences de la vie > Laboratoire de génétique de la conservation

Linardic, Marina

Rappa, Francesca

Barone, Rosario

Navarrete, Gerardo

Wei, Min

More authors (9 more)

Language :

English

Title :

Fasting-mimicking diet prevents high-fat diet effect on cardiometabolic risk and lifespan.

Publication date :

2021

Journal title :

Nature metabolism

ISSN :

2522-5812

eISSN :

2522-5812

Peer reviewed :

Peer reviewed

Commentary :

Available on ORBi :

since 17 January 2022

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Bibliography

National Center for Health Statistics: National Health and Nutrition Examination Survey 2020 (CDC, 2020).
Fryar, C. D., Carroll, M. D. & Ogden, C. L. Prevalence of overweight, obesity, and extreme obesity among adults aged 20 and over: United States, 1960–1962 through 2013–2014 (National Center for Health Statistics, CDC, 2016).
Schrauwen, P. & Westerterp, K. R. The role of high-fat diets and physical activity in the regulation of body weight. Br. J. Nutr. 84, 417–427 (2000). DOI: 10.1017/S0007114500001720
Després, J.-P. & Lemieux, I. Abdominal obesity and metabolic syndrome. Nature 444, 881–887 (2006). DOI: 10.1038/nature05488
Astrup, A. The role of dietary fat in obesity. Semin. Vasc. Med. 5, 40–47 (2005). DOI: 10.1055/s-2005-871740
Buettner, R., Schölmerich, J. & Bollheimer, L. C. High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity 15, 798–808 (2007). DOI: 10.1038/oby.2007.608
Hu, S. et al. Dietary fat, but not protein or carbohydrate, regulates energy intake and causes adiposity in mice. Cell Metab. 28, 415–431 (2018). DOI: 10.1016/j.cmet.2018.06.010
Longo, V. D. & Mattson, M. P. Fasting: molecular mechanisms and clinical applications. Cell Metab. 19, 181–192 (2014). DOI: 10.1016/j.cmet.2013.12.008
Wei, M. et al. Fasting-mimicking diet and markers/risk factors for aging, diabetes, cancer, and cardiovascular disease. Sci. Transl. Med. 9, eaai8700 (2017). DOI: 10.1126/scitranslmed.aai8700
Brandhorst, S. et al. A periodic diet that mimics fasting promotes multi-system regeneration, enhanced cognitive performance, and healthspan. Cell Metab. 22, 86–99 (2015). DOI: 10.1016/j.cmet.2015.05.012
Choi, I. Y. et al. A diet mimicking fasting promotes regeneration and reduces autoimmunity and multiple sclerosis symptoms. Cell Rep. 15, 2136–2146 (2016). DOI: 10.1016/j.celrep.2016.05.009
Cheng, C.-W. et al. Fasting-mimicking diet promotes Ngn3-driven β-cell regeneration to reverse diabetes. Cell 168, 775–788 (2017). DOI: 10.1016/j.cell.2017.01.040
Di Biase, S. et al. Fasting-mimicking diet reduces HO-1 to promote T cell-mediated tumor cytotoxicity. Cancer Cell 30, 136–146 (2016). DOI: 10.1016/j.ccell.2016.06.005
Rangan, P. et al. Supplementary-fasting-mimicking diet modulates microbiota and promotes intestinal regeneration to reduce inflammatory bowel disease pathology. Cell Rep. 26, 2704–2719 (2019). DOI: 10.1016/j.celrep.2019.02.019
Ingvorsen, C., Karp, N. A. & Lelliott, C. J. The role of sex and body weight on the metabolic effects of high-fat diet in C57BL/6N mice. Nutr. Diabetes 7, e261 (2017). DOI: 10.1038/nutd.2017.6
Guo, J., Jou, W., Gavrilova, O. & Hall, K. D. Persistent diet-induced obesity in male C57BL/6 mice resulting from temporary obesigenic diets. PLoS ONE 4, e5370 (2009). DOI: 10.1371/journal.pone.0005370
Klok, M. D., Jakobsdottir, S. & Drent, M. L. The role of leptin and ghrelin in the regulation of food intake and body weight in humans: a review. Obes. Rev. 8, 21–34 (2007). DOI: 10.1111/j.1467-789X.2006.00270.x
Ioannou, G. N., Weiss, N. S., Boyko, E. J., Mozaffarian, D. & Lee, S. P. Elevated serum alanine aminotransferase activity and calculated risk of coronary heart disease in the United States. Hepatology 43, 1145–1151 (2006). DOI: 10.1002/hep.21171
Kleiner, D. E. et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41, 1313–1321 (2005). DOI: 10.1002/hep.20701
Fontana, L. et al. Aging promotes the development of diet-induced murine steatohepatitis but not steatosis. Hepatology 57, 995–1004 (2013). DOI: 10.1002/hep.26099
Goedecke, J. H. et al. Determinants of the variability in respiratory exchange ratio at rest and during exercise in trained athletes. Am. J. Physiol. Endocrinol. Metab. 279, 1325–1334 (2000). DOI: 10.1152/ajpendo.2000.279.6.E1325
Shiojima, I. Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J. Clin. Invest. 115, 2108–2118 (2005). DOI: 10.1172/JCI24682
Xu, X. et al. Age-related impairment of vascular structure and functions. Aging Dis. 8, 590–610 (2017). DOI: 10.14336/AD.2017.0430
Lakatta, E. G. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: part III: cellular and molecular clues to heart and arterial aging. Circulation 107, 490–497 (2003). DOI: 10.1161/01.CIR.0000048894.99865.02
Horn, M. A. & Trafford, A. W. Aging and the cardiac collagen matrix: novel mediators of fibrotic remodelling. J. Mol. Cell. Cardiol. 93, 175–185 (2016). DOI: 10.1016/j.yjmcc.2015.11.005
Nadruz, W. Myocardial remodeling in hypertension. J. Hum. Hypertens. 29, 1–6 (2015). DOI: 10.1038/jhh.2014.36
Houser, S. R. et al. Animal models of heart failure. Circ. Res. 111, 131–150 (2012). DOI: 10.1161/RES.0b013e3182582523
Marwick, T. H. Stress echocardiography. In Echocardiography (eds Nihoyannopoulos, P. & Kisslo, J.) 491–519 (Springer, 2018).
Vallet, B., Dupuis, B. & Chopin, C. [Dobutamine: mechanisms of action and use in acute cardiovascular pathology]. Ann. Cardiol. Angeiol. 40, 397–402 (1991).
Pellikka, P. A. et al. Guidelines for performance, interpretation, and application of stress echocardiography in ischemic heart disease: from the American Society of Echocardiography. J. Am. Soc. Echocardiogr. 33, 1–41 (2020). DOI: 10.1016/j.echo.2019.07.001
Zhang, Y. et al. Obesity-induced oxidative stress, accelerated functional decline with age and increased mortality in mice. Arch. Biochem. Biophys. 576, 39–48 (2015). DOI: 10.1016/j.abb.2014.12.018
Leontieva, O. V., Paszkiewicz, G. M. & Blagosklonny, M. V. Weekly administration of rapamycin improves survival and biomarkers in obese male mice on high-fat diet. Aging Cell 13, 616–622 (2014). DOI: 10.1111/acel.12211
Aires, V. et al. Healthy adiposity and extended lifespan in obese mice fed a diet supplemented with a polyphenol-rich plant extract. Sci. Rep. 9, 9116–9134 (2019). DOI: 10.1038/s41598-019-45547-8
Zhu, B. et al. Alogliptin improves survival and health of mice on a high-fat diet. Aging Cell 18, e12883 (2019). DOI: 10.1111/acel.12883
Brandhorst, S. & Longo, V. D. Dietary restrictions and nutrition in the prevention and treatment of cardiovascular disease. Circ. Res. 124, 952–965 (2019). DOI: 10.1161/CIRCRESAHA.118.313352
Fanti, M., Mishra, A., Longo, V. D. & Brandhorst, S. Time-restricted eating, intermittent fasting, and fasting-mimicking diets in weight loss. Curr. Obes. Rep. 10, 70–80 (2021). DOI: 10.1007/s13679-021-00424-2
Newman, J. C. et al. Ketogenic diet reduces midlife mortality and improves memory in aging mice. Cell Metab. 26, 547–557 (2017). DOI: 10.1016/j.cmet.2017.08.004
Rusli, F. et al. Intermittent calorie restriction largely counteracts the adverse health effects of a moderate-fat diet in aging C57BL/6J mice. Mol. Nutr. Food Res. 61, 1600677 (2017). DOI: 10.1002/mnfr.201600677
Stamler, J. et al. Relationship of baseline serum cholesterol levels in 3 large cohorts of younger men to long-term coronary, cardiovascular, and all-cause mortality and to longevity. JAMA 284, 311–318 (2000). DOI: 10.1001/jama.284.3.311
Sedej, S. Ketone bodies to the rescue for an aging heart? Cardiovasc. Res. 114, e1–e2 (2018). DOI: 10.1093/cvr/cvx218
Veech, R. L. et al. Ketone bodies mimic the life span extending properties of caloric restriction. IUBMB Life 69, 305–314 (2017). DOI: 10.1002/iub.1627
Greenway, F. L. Physiological adaptations to weight loss and factors favouring weight regain. Int. J. Obes. 39, 1188–1196 (2015). DOI: 10.1038/ijo.2015.59
Graham, B., Chang, S., Lin, D., Yakubu, F. & Hill, J. O. Effect of weight cycling on susceptibility to dietary obesity. Am. J. Physiol. 259, R1096–R1102 (1990).
Simonds, S. E., Pryor, J. T. & Cowley, M. A. Repeated weight cycling in obese mice causes increased appetite and glucose intolerance. Physiol. Behav. 194, 184–190 (2018). DOI: 10.1016/j.physbeh.2018.05.026
O’Connor, K. L. et al. Altered appetite-mediating hormone concentrations precede compensatory overeating after severe, short-term energy deprivation in healthy adults. J. Nutr. 146, 209–217 (2016). DOI: 10.3945/jn.115.217976
Coutinho, S. R. et al. Compensatory mechanisms activated with intermittent energy restriction: a randomized control trial. Clin. Nutr. 37, 815–823 (2018). DOI: 10.1016/j.clnu.2017.04.002
Kondo, M. et al. Caloric restriction stimulates revascularization in response to ischemia via adiponectin-mediated activation of endothelial nitric-oxide synthase. J. Biol. Chem. 284, 1718–1724 (2009). DOI: 10.1074/jbc.M805301200
Claudio, deL. et al. Long-term caloric restriction improves cardiac function, remodeling, adrenergic responsiveness, and sympathetic innervation in a model of postischemic heart failure. Circ. Heart Fail. 11, e004153 (2018).
Ahmet, I., Tae, H.-J., de Cabo, R., Lakatta, E. G. & Talan, M. I. Effects of calorie restriction on cardioprotection and cardiovascular health. J. Mol. Cell. Cardiol. 51, 263–271 (2011). DOI: 10.1016/j.yjmcc.2011.04.015
Kim, S. S. et al. Whole-transcriptome analysis of mouse adipose tissue in response to short‑term caloric restriction. Mol. Genet. Genomics 291, 831–847 (2016). DOI: 10.1007/s00438-015-1150-3
Nisoli, E. et al. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310, 314–317 (2005). DOI: 10.1126/science.1117728
Pardo, R. et al. Calorie restriction prevents diet-induced insulin resistance independently of PGC-1-driven mitochondrial biogenesis in white adipose tissue. FASEB J. 33, 2343–2358 (2018). DOI: 10.1096/fj.201800310R
Kusminski, C. M. & Scherer, P. E. Mitochondrial dysfunction in white adipose tissue. Trends Endocrinol. Metab. 23, 435–443 (2012). DOI: 10.1016/j.tem.2012.06.004
Katic, M. et al. Mitochondrial gene expression and increased oxidative metabolism: role in increased lifespan of fat-specific insulin receptor knock-out mice. Aging Cell 6, 827–839 (2007). DOI: 10.1111/j.1474-9726.2007.00346.x
Edgar, R., Domrachev, M. & Lash, A. E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207–210 (2002). DOI: 10.1093/nar/30.1.207
Vinué, Á. & González-Navarro, H. Glucose and insulin tolerance tests in the mouse. In Methods in Mouse Atherosclerosis (eds Andrés, V. & Dorado, B.) 247–254 (Springer, 2015).
Lancellotti, P. et al. The clinical use of stress echocardiography in non-ischaemic heart disease: recommendations from the European Association of Cardiovascular Imaging and the American Society of Echocardiography. Eur. Heart J. Cardiovasc. Imaging 17, 1191–1229 (2016). DOI: 10.1093/ehjci/jew190
Barone, R. et al. Skeletal muscle heat shock protein 60 increases after endurance training and induces peroxisome proliferator-activated receptor γ coactivator 1 α1 expression. Sci. Rep. 6, 19781 (2016). DOI: 10.1038/srep19781
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013). DOI: 10.1093/bioinformatics/bts635
Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015). DOI: 10.1093/nar/gkv007
Robinson, M. D. & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25 (2010). DOI: 10.1186/gb-2010-11-3-r25
Law, C. W., Chen, Y., Shi, W. & Smyth, G. voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 15, R29 (2014). DOI: 10.1186/gb-2014-15-2-r29
Chen, H. & Boutros, P. C. VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics 12, 35 (2011). DOI: 10.1186/1471-2105-12-35
Chen, E. Y. et al. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 14, 128 (2013). DOI: 10.1186/1471-2105-14-128
Kuleshov, M. V. et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 44, W90–W97 (2016). DOI: 10.1093/nar/gkw377
Walter, W., Sánchez-Cabo, F. & Ricote, M. GOplot: an R package for visually combining expression data with functional analysis. Bioinformatics 31, 2912–2914 (2015). DOI: 10.1093/bioinformatics/btv300