Impact of Combined Exercise on Blood DNA Methylation and Physical Health in Older Women with Obesity

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2024 Dec 16

PMID 39680552

Authors

Atchara Dawangpa

Pitaksin Chitta

Guilherme da Silva Rodrigues

Nutta Iadsee

Natalia Y Noronha

Carla B Nonino

Carlos R Bueno Junior

Chanachai Sae-Lee

Affiliations

Soon will be listed here.

Abstract

This study examined the effects of a 14-week combined exercise program on blood DNA methylation (DNAm) and its potential biological pathways in normal-weight, overweight, and obese older women. A total of 41 participants were assessed at baseline, 7 weeks, and 14 weeks into the training. Their whole-blood DNAm profiles were measured using the Infinitum MethylationEPIC BeadChip, alongside physical and biochemical health evaluations. The results showed notable health improvements, with decreases in blood pressure and cholesterol levels in the overweight and obese groups. Blood triglycerides were reduced only in the overweight group. Physical performance also improved across all groups. At 14 weeks, 1,043 differentially methylated positions (DMPs) were identified, affecting 744 genes. The genes were linked to biological processes, such as cellular metabolism, with significant pathway enrichment related to oxidative phosphorylation and chemical carcinogenesis. Additionally, the overweight group experienced significant reductions in methylation levels at eight lipogenesis-related genes. Protein EpiScore analysis revealed decreased levels of CCL11, VEGFA, and NTRK3 proteins at 14 weeks compared to baseline. Despite these significant molecular changes, there was no observable difference in DNAm age after the intervention. This study highlights how combined exercise can modify DNAm patterns in older women, particularly in lipogenesis-related genes, but suggests that further research is needed to understand the full implications for biological ageing.

References

Menzies-Gow A, Ying S, Sabroe I, Stubbs V, Soler D, Williams T . Eotaxin (CCL11) and eotaxin-2 (CCL24) induce recruitment of eosinophils, basophils, neutrophils, and macrophages as well as features of early- and late-phase allergic reactions following cutaneous injection in human atopic and nonatopic volunteers. J Immunol. 2002; 169(5):2712-8. DOI: 10.4049/jimmunol.169.5.2712. View

Luttropp K, Nordfors L, Ekstrom T, Lind L . Physical activity is associated with decreased global DNA methylation in Swedish older individuals. Scand J Clin Lab Invest. 2012; 73(2):184-5. DOI: 10.3109/00365513.2012.743166. View

Pileggi C, Blondin D, Hooks B, Parmar G, Alecu I, Patten D . Exercise training enhances muscle mitochondrial metabolism in diet-resistant obesity. EBioMedicine. 2022; 83:104192. PMC: 9482931. DOI: 10.1016/j.ebiom.2022.104192. View

Stallknecht B, Vissing J, Galbo H . Lactate production and clearance in exercise. Effects of training. A mini-review. Scand J Med Sci Sports. 1998; 8(3):127-31. DOI: 10.1111/j.1600-0838.1998.tb00181.x. View

Jamart C, Benoit N, Raymackers J, Kim H, Kim C, Francaux M . Autophagy-related and autophagy-regulatory genes are induced in human muscle after ultraendurance exercise. Eur J Appl Physiol. 2011; 112(8):3173-7. DOI: 10.1007/s00421-011-2287-3. View

Ritchie M, Phipson B, Wu D, Hu Y, Law C, Shi W . limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015; 43(7):e47. PMC: 4402510. DOI: 10.1093/nar/gkv007. View

Hoier B, Nordsborg N, Andersen S, Jensen L, Nybo L, Bangsbo J . Pro- and anti-angiogenic factors in human skeletal muscle in response to acute exercise and training. J Physiol. 2011; 590(3):595-606. PMC: 3379703. DOI: 10.1113/jphysiol.2011.216135. View

Mahmoud A . An Overview of Epigenetics in Obesity: The Role of Lifestyle and Therapeutic Interventions. Int J Mol Sci. 2022; 23(3). PMC: 8836029. DOI: 10.3390/ijms23031341. View

Rogers C, Colbert L, Greiner J, Perkins S, Hursting S . Physical activity and cancer prevention : pathways and targets for intervention. Sports Med. 2008; 38(4):271-96. DOI: 10.2165/00007256-200838040-00002. View

10.

Kaushik S, Cuervo A . Chaperones in autophagy. Pharmacol Res. 2012; 66(6):484-93. PMC: 3502706. DOI: 10.1016/j.phrs.2012.10.002. View

11.

Gunga H, Kirsch K, Rocker L, Behn C, Koralewski E, Davila E . Vascular endothelial growth factor in exercising humans under different environmental conditions. Eur J Appl Physiol Occup Physiol. 1999; 79(6):484-90. DOI: 10.1007/s004210050541. View

12.

Hochberg Y, Benjamini Y . More powerful procedures for multiple significance testing. Stat Med. 1990; 9(7):811-8. DOI: 10.1002/sim.4780090710. View

13.

Dick K, Nelson C, Tsaprouni L, Sandling J, Aissi D, Wahl S . DNA methylation and body-mass index: a genome-wide analysis. Lancet. 2014; 383(9933):1990-8. DOI: 10.1016/S0140-6736(13)62674-4. View

14.

Villeda S, Luo J, Mosher K, Zou B, Britschgi M, Bieri G . The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature. 2011; 477(7362):90-4. PMC: 3170097. DOI: 10.1038/nature10357. View

15.

Ulgen E, Ozisik O, Sezerman O . pathfindR: An R Package for Comprehensive Identification of Enriched Pathways in Omics Data Through Active Subnetworks. Front Genet. 2019; 10:858. PMC: 6773876. DOI: 10.3389/fgene.2019.00858. View

16.

Leek J, Johnson W, Parker H, Jaffe A, Storey J . The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics. 2012; 28(6):882-3. PMC: 3307112. DOI: 10.1093/bioinformatics/bts034. View

17.

Powers S, Deminice R, Ozdemir M, Yoshihara T, Bomkamp M, Hyatt H . Exercise-induced oxidative stress: Friend or foe?. J Sport Health Sci. 2020; 9(5):415-425. PMC: 7498668. DOI: 10.1016/j.jshs.2020.04.001. View

18.

Villicana S, Bell J . Genetic impacts on DNA methylation: research findings and future perspectives. Genome Biol. 2021; 22(1):127. PMC: 8086086. DOI: 10.1186/s13059-021-02347-6. View

19.

Simmen F, Alhallak I, Simmen R . Malic enzyme 1 (ME1) in the biology of cancer: it is not just intermediary metabolism. J Mol Endocrinol. 2020; 65(4):R77-R90. PMC: 7577320. DOI: 10.1530/JME-20-0176. View

20.

McTiernan A, Yasui Y, Sorensen B, Irwin M, Morgan A, Rudolph R . Effect of a 12-month exercise intervention on patterns of cellular proliferation in colonic crypts: a randomized controlled trial. Cancer Epidemiol Biomarkers Prev. 2006; 15(9):1588-97. DOI: 10.1158/1055-9965.EPI-06-0223. View