Subscribe to RSS
DOI: 10.1055/a-0592-7691
microRNAs in High and Low Responders to Resistance Training in Breast Cancer Survivors
Publication History
accepted 28 February 2018
Publication Date:
26 April 2018 (online)
Abstract
Accounting for one in three cancer diagnoses, breast cancer is the second most commonly diagnosed cancer in women. Exercise has a well-accepted role in the multi-disciplinary approach to rehabilitating breast cancer survivors. Despite the many known benefits of resistance training on women recovering from breast cancer, the molecular mechanisms are poorly understood. MicroRNAs are small non-coding RNAs that have crucial roles in growth and development. Here, we analysed the abundance of 9 miRNAs, with known roles in muscle physiology and some linked to cancer, in serum samples from 24 breast cancer survivors before and after a 16-week resistance training or usual care intervention. The resistance training group completed supervised thrice-weekly training. miRNA abundance was assessed before and after the intervention period using qPCR. There were no statistically significant changes in any of the miRNAs between groups after the intervention period (all p>0.05). After assessing miRNA abundance in context with high and low responders to resistance training, we observed that relative to low responders, high responders exhibited increased miR-133a-3p and a borderline statistically significant increase in miR-370-3p. Findings from our controlled study indicate the diverse interindividual miRNA responses to resistance training and reveal a discordant regulation between high and low responders.
-
References
- 1 Backes C, Kehl T, Stockel D, Fehlmann T, Schneider L, Meese E, Lenhof HP, Keller A. miRPathDB: A new dictionary on microRNAs and target pathways. Nucleic Acids Res 2017; 45: D90-D96
- 2 Batista PJ, Chang HY. Long noncoding RNAs: Cellular address codes in development and disease. Cell 2013; 152: 1298-1307
- 3 Beermann J, Piccoli MT, Viereck J, Thum T. Non-coding RNAs in development and disease: Background, mechanisms, and therapeutic approaches. Physiol Rev 2016; 96: 1297-1325
- 4 Bhaskaran M, Mohan M. MicroRNAs: History, biogenesis, and their evolving role in animal development and disease. Vet Pathol 2014; 51: 759-774
- 5 Camera DM, Ong JN, Coffey VG, Hawley JA. Selective modulation of microRNA expression with protein ingestion following concurrent resistance and endurance exercise in human skeletal muscle. Front Physiol 2016; 7: 87
- 6 Cheema B, Gaul C. Full-body exercise training improves fitness and quality of life in survivors of breast cancer. J Strength Cond Res 2006; 20: 14-21
- 7 D'Souza RF, Markworth JF, Aasen KMM, Zeng N, Cameron-Smith D, Mitchell CJ. Acute resistance exercise modulates microRNA expression profiles: Combined tissue and circulatory targeted analyses. PLoS One 2017; 12: e0181594
- 8 Davidsen PK, Gallagher IJ, Hartman JW, Tarnopolsky MA, Dela F, Helge JW, Timmons JA, Phillips SM. High responders to resistance exercise training demonstrate differential regulation of skeletal muscle microRNA expression. J Appl Physiol 2011; 110: 309-317
- 9 Denham J. Exercise and epigenetic inheritance of disease risk. Acta Physiol (Oxf) 2018; 222: e12881
- 10 Denham J, Marques FZ, Bruns EL, O'Brien BJ, Charchar FJ. Epigenetic changes in leukocytes after 8 weeks of resistance exercise training. Eur J Appl Physiol 2016; 116: 1245-1253
- 11 Denham J, Marques FZ, O'Brien BJ, Charchar FJ. Exercise: Putting action into our epigenome. Sports Med 2014; 44: 189-209
- 12 Denham J, Prestes PR. Muscle-enriched microRNAs isolated from whole blood are regulated by exercise and are potential biomarkers of cardiorespiratory fitness. Front Genet 2016; 7: 196
- 13 Drummond MJ, McCarthy JJ, Fry CS, Esser KA, Rasmussen BB. Aging differentially affects human skeletal muscle microRNA expression at rest and after an anabolic stimulus of resistance exercise and essential amino acids. Am J Physiol Endocrinol Metab 2008; 295: E1333-E1340
- 14 Fernandes T, Barauna VG, Negrao CE, Phillips MI, Oliveira EM. Aerobic exercise training promotes physiological cardiac remodeling involving a set of microRNAs. Am J Physiol Heart Circ Physiol 2015; 309: H543-H552
- 15 Hagstrom A, Marshall P, Lonsdale C, Cheema B, Singh F, Green S. Resistance training improves fatigue and quality of life in previously sedentary breast cancer survivors: A randomised controlled trial. Eur J Cancer Care 2016; 25: 784-794
- 16 Hagstrom AD, Marshall PW, Lonsdale C, Papalia S, Cheema BS, Toben C, Baune BT, Fiatarone Singh MA, Green S. The effect of resistance training on markers of immune function and inflammation in previously sedentary women recovering from breast cancer: A randomized controlled trial. Breast Cancer Res Treat 2016; 155: 471-482
- 17 Hagstrom AD, Shorter KA, Marshall PWM. Changes in unilateral upper limb muscular strength and EMG activity following a 16 week strength training intervention survivors of breast cancer. J Strength Cond Res 2017; DOI: 10.1519/JSC.0000000000001890.
- 18 Harriss DJ, Macsween A, Atkinson G. Standards for ethics in sport and exercise science research: 2018 update. Int J Sports Med 2017; 38: 1126-1131
- 19 Hoppe R, Fan P, Buttner F, Winter S, Tyagi AK, Cunliffe H, Jordan VC, Brauch H. Profiles of miRNAs matched to biology in aromatase inhibitor resistant breast cancer. Oncotarget 2016; 7: 71235-71254
- 20 Kirby TJ, McCarthy JJ. MicroRNAs in skeletal muscle biology and exercise adaptation. Free Radic Biol Med 2013; 64: 95-105
- 21 Kumar AS, Jagadeeshan S, Pitani RS, Ramshankar V, Venkitasamy K, Venkatraman G, Rayala SK. Snail-modulated microRNA 493 forms a negative feedback loop with the insulin-like growth factor 1 receptor pathway and blocks tumorigenesis. Mol Cell Biol 2017; 37: e00510-e00516
- 22 Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75: 843-854
- 23 Liang C, Ding J, Yang Y, Deng L, Li X. MicroRNA-433 inhibits cervical cancer progression by directly targeting metadherin to regulate the AKT and beta-catenin signalling pathways. Oncol Rep 2017; 38: 3639-3649
- 24 McCarthy JJ, Esser KA. MicroRNA-1 and microRNA-133a expression are decreased during skeletal muscle hypertrophy. J Appl Physiol 2007; 102: 306-313
- 25 Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, Baty CJ, Gibson GA, Erdos G, Wang Z, Milosevic J, Tkacheva OA, Divito SJ, Jordan R, Lyons-Weiler J, Watkins SC, Morelli AE. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 2012; 119: 756-766
- 26 Mueller M, Breil FA, Lurman G, Klossner S, Fluck M, Billeter R, Dapp C, Hoppeler H. Different molecular and structural adaptations with eccentric and conventional strength training in elderly men and women. Gerontology 2011; 57: 528-538
- 27 Nie Y, Sato Y, Wang C, Yue F, Kuang S, Gavin TP. Impaired exercise tolerance, mitochondrial biogenesis, and muscle fiber maintenance in miR-133a-deficient mice. FASEB J 2016; 30: 3745-3758
- 28 Ogasawara R, Akimoto T, Umeno T, Sawada S, Hamaoka T, Fujita S. MicroRNA expression profiling in skeletal muscle reveals different regulatory patterns in high and low responders to resistance training. Physiol Genomics 2016; 48: 320-324
- 29 Ohira T, Schmitz KH, Ahmed RL, Yee D. Effects of weight training on quality of life in recent breast cancer survivors: The Weight Training for Breast Cancer Survivors (WTBS) study. Cancer 2006; 106: 2076-2083
- 30 Raposo G, Stoorvogel W. Extracellular vesicles: Exosomes, microvesicles, and friends. J Cell Biol 2013; 200: 373-383
- 31 Rowlands DS, Page RA, Sukala WR, Giri M, Ghimbovschi SD, Hayat I, Cheema BS, Lys I, Leikis M, Sheard PW, Wakefield SJ, Breier B, Hathout Y, Brown K, Marathi R, Orkunoglu-Suer FE, Devaney JM, Leiken B, Many G, Krebs J, Hopkins WG, Hoffman EP. Multi-omic integrated networks connect DNA methylation and miRNA with skeletal muscle plasticity to chronic exercise in Type 2 diabetic obesity. Physiol Genomics 2014; 46: 747-765
- 32 Schwarzenbach H, Nishida N, Calin GA, Pantel K. Clinical relevance of circulating cell-free microRNAs in cancer. Nat Rev Clin Oncol 2014; 11: 145-156
- 33 Seven M, Karatas OF, Duz MB, Ozen M. The role of miRNAs in cancer: From pathogenesis to therapeutic implications. Future Oncol 2014; 10: 1027-1048
- 34 Stefani G, Slack FJ. Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 2008; 9: 219-230
- 35 Tan YY, Xu XY, Wang JF, Zhang CW, Zhang SC. MiR-654-5p attenuates breast cancer progression by targeting EPSTI1. Am J Cancer Res 2016; 6: 522-532
- 36 Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 2011; 13: 423-433
- 37 Volaklis KA, Halle M, Tokmakidis SP. Exercise in the prevention and rehabilitation of breast cancer. Wien Klin Wochenschr 2013; 125: 297-301
- 38 Xu H, Wu F, Cao H, Kan G, Zhang H, Yeung EW, Shang P, Dai Z, Li Y. Effects of simulated microgravity on microRNA and mRNA expression profile of rat soleus. Acta Astronaut 2015; 107: 40-49
- 39 Yamane K, Naito H, Wakabayashi T, Yoshida H, Muramatsu F, Iba T, Kidoya H, Takakura N. Regulation of SLD5 gene expression by miR-370 during acute growth of cancer cells. Sci Rep 2016; 6: 30941
- 40 Zhang L, Xu Y, Jin X, Wang Z, Wu Y, Zhao D, Chen G, Li D, Wang X, Cao H, Xie Y, Liang Z. A circulating miRNA signature as a diagnostic biomarker for non-invasive early detection of breast cancer. Breast Cancer Res Treat 2015; 154: 423-434