The Impact of Caloric Restriction on the Epigenetic Signatures of Aging

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2019 Apr 27

PMID 31022953

Citations 35

Authors

Noemie Gensous

Claudio Franceschi

Aurelia Santoro

Maddalena Milazzo

Paolo Garagnani

Maria Giulia Bacalini

Affiliations

Soon will be listed here.

Abstract

Aging is characterized by an extensive remodeling of epigenetic patterns, which has been implicated in the physiopathology of age-related diseases. Nutrition plays a significant role in modulating the epigenome, and a growing amount of data indicate that dietary changes can modify the epigenetic marks associated with aging. In this review, we will assess the current advances in the relationship between caloric restriction, a proven anti-aging intervention, and epigenetic signatures of aging. We will specifically discuss the impact of caloric restriction on epigenetic regulation and how some of the favorable effects of caloric restriction on lifespan and healthspan could be mediated by epigenetic modifications.

Citing Articles

The Genetic and Epigenetic Arms of Human Ageing and Longevity.

Ciaglia E, Montella F, Lopardo V, Basile C, Esposito R, Maglio C Biology (Basel). 2025; 14(1).

PMID: 39857322 PMC: 11762130. DOI: 10.3390/biology14010092.

Epigenetic Mechanisms in Aging: Extrinsic Factors and Gut Microbiome.

Borrego-Ruiz A, Borrego J Genes (Basel). 2025; 15(12.

PMID: 39766866 PMC: 11675900. DOI: 10.3390/genes15121599.

Chemokine CXCL9, a marker of inflammaging, is associated with changes of muscle strength and mortality in older men.

Seo D, Corr M, Patel S, Lui L, Cauley J, Evans D Osteoporos Int. 2024; 35(10):1789-1796.

PMID: 38965121 PMC: 11427528. DOI: 10.1007/s00198-024-07160-y.

Renin-angiotensin system inhibitors positively impact on multiple aging regulatory pathways: Could they be used to protect against human aging?.

de Cavanagh E, Inserra F, Ferder L Physiol Rep. 2024; 12(12):e16094.

PMID: 38924381 PMC: 11200104. DOI: 10.14814/phy2.16094.

Harnessing Genetics to Extend Lifespan and Healthspan: Current Progress and Future Directions.

Ankrah P, Mensah E, Dabie K, Mensah C, Akangbe B, Essuman J Cureus. 2024; 16(3):e55495.

PMID: 38571872 PMC: 10990068. DOI: 10.7759/cureus.55495.

References

Lee C, Klopp R, Weindruch R, Prolla T . Gene expression profile of aging and its retardation by caloric restriction. Science. 1999; 285(5432):1390-3. DOI: 10.1126/science.285.5432.1390. View

Lin S, Defossez P, Guarente L . Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science. 2000; 289(5487):2126-8. DOI: 10.1126/science.289.5487.2126. View

Lopatina N, Haskell J, Andrews L, Poole J, Saldanha S, Tollefsbol T . Differential maintenance and de novo methylating activity by three DNA methyltransferases in aging and immortalized fibroblasts. J Cell Biochem. 2002; 84(2):324-34. DOI: 10.1002/jcb.10015. View

Cohen H, Miller C, Bitterman K, Wall N, Hekking B, Kessler B . Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science. 2004; 305(5682):390-2. DOI: 10.1126/science.1099196. View

Nemoto S, Fergusson M, Finkel T . Nutrient availability regulates SIRT1 through a forkhead-dependent pathway. Science. 2004; 306(5704):2105-8. DOI: 10.1126/science.1101731. View

Fraga M, Ballestar E, Paz M, Ropero S, Setien F, Ballestar M . Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A. 2005; 102(30):10604-9. PMC: 1174919. DOI: 10.1073/pnas.0500398102. View

Longo V, Kennedy B . Sirtuins in aging and age-related disease. Cell. 2006; 126(2):257-68. DOI: 10.1016/j.cell.2006.07.002. View

Ressler S, Bartkova J, Niederegger H, Bartek J, Scharffetter-Kochanek K, Jansen-Durr P . p16INK4A is a robust in vivo biomarker of cellular aging in human skin. Aging Cell. 2006; 5(5):379-89. DOI: 10.1111/j.1474-9726.2006.00231.x. View

Maalouf M, Rho J, Mattson M . The neuroprotective properties of calorie restriction, the ketogenic diet, and ketone bodies. Brain Res Rev. 2008; 59(2):293-315. PMC: 2649682. DOI: 10.1016/j.brainresrev.2008.09.002. View

10.

Heijmans B, Tobi E, Stein A, Putter H, Blauw G, Susser E . Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008; 105(44):17046-9. PMC: 2579375. DOI: 10.1073/pnas.0806560105. View

11.

Bollati V, Schwartz J, Wright R, Litonjua A, Tarantini L, Suh H . Decline in genomic DNA methylation through aging in a cohort of elderly subjects. Mech Ageing Dev. 2009; 130(4):234-9. PMC: 2956267. DOI: 10.1016/j.mad.2008.12.003. View

12.

Sun L, Sadighi Akha A, Miller R, Harper J . Life-span extension in mice by preweaning food restriction and by methionine restriction in middle age. J Gerontol A Biol Sci Med Sci. 2009; 64(7):711-22. PMC: 2691799. DOI: 10.1093/gerona/glp051. View

13.

Campion J, Milagro F, Goyenechea E, Martinez J . TNF-alpha promoter methylation as a predictive biomarker for weight-loss response. Obesity (Silver Spring). 2009; 17(6):1293-7. DOI: 10.1038/oby.2008.679. View

14.

Colman R, Anderson R, Johnson S, Kastman E, Kosmatka K, Beasley T . Caloric restriction delays disease onset and mortality in rhesus monkeys. Science. 2009; 325(5937):201-4. PMC: 2812811. DOI: 10.1126/science.1173635. View

15.

Christensen B, Houseman E, Marsit C, Zheng S, Wrensch M, Wiemels J . Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet. 2009; 5(8):e1000602. PMC: 2718614. DOI: 10.1371/journal.pgen.1000602. View

16.

Calvanese V, Lara E, Kahn A, Fraga M . The role of epigenetics in aging and age-related diseases. Ageing Res Rev. 2009; 8(4):268-76. DOI: 10.1016/j.arr.2009.03.004. View

17.

Bouchard L, Rabasa-Lhoret R, Faraj M, Lavoie M, Mill J, Perusse L . Differential epigenomic and transcriptomic responses in subcutaneous adipose tissue between low and high responders to caloric restriction. Am J Clin Nutr. 2009; 91(2):309-20. DOI: 10.3945/ajcn.2009.28085. View

18.

Swindell W . Genes and gene expression modules associated with caloric restriction and aging in the laboratory mouse. BMC Genomics. 2009; 10:585. PMC: 2795771. DOI: 10.1186/1471-2164-10-585. View

19.

Li Y, Liu L, Tollefsbol T . Glucose restriction can extend normal cell lifespan and impair precancerous cell growth through epigenetic control of hTERT and p16 expression. FASEB J. 2009; 24(5):1442-53. PMC: 2996891. DOI: 10.1096/fj.09-149328. View

20.

Rakyan V, Down T, Maslau S, Andrew T, Yang T, Beyan H . Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res. 2010; 20(4):434-9. PMC: 2847746. DOI: 10.1101/gr.103101.109. View