The role of physical activity and miRNAs in the vascular aging and cardiac health of dialysis patients
Language English Country United States Media print
Document type Journal Article, Multicenter Study, Research Support, Non-U.S. Gov't
PubMed
34042291
PubMed Central
PMC8157788
DOI
10.14814/phy2.14879
Knihovny.cz E-resources
- Keywords
- calcification, cardiovascular health, dialysis, exercise, inactivity, microRNA,
- MeSH
- Endothelium, Vascular metabolism MeSH
- Exercise physiology MeSH
- Renal Dialysis * MeSH
- Cardiovascular Diseases blood genetics therapy MeSH
- Middle Aged MeSH
- Humans MeSH
- MicroRNAs biosynthesis blood genetics MeSH
- Sedentary Behavior MeSH
- Aged MeSH
- Gene Expression Profiling methods MeSH
- Aging blood genetics MeSH
- Check Tag
- Middle Aged MeSH
- Humans MeSH
- Male MeSH
- Aged MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Multicenter Study MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- MicroRNAs MeSH
Cardiovascular comorbidities are independent risk factors for mortality in dialysis patients. MicroRNA signaling has an important role in vascular aging and cardiac health, while physical activity is a primary nonpharmacologic treatment for cardiovascular comorbidities in dialysis patients. To identify the relationships between muscle function, miRNA signaling pathways, the presence of vascular calcifications and the severity of cardiovascular comorbidities, we initially enrolled 90 subjects on hemodialysis therapy and collected complete data from 46 subjects. A group of 26 subjects inactiv group (INC) was monitored during 12 weeks of physical inactivity and another group of 20 patients exercise group (EXC) was followed during 12 weeks of intradialytic, moderate intensity, resistance training intervention applied three times per week. In both groups, we assessed the expression levels of myo-miRNAs, proteins, and muscle function (MF) before and after the 12-week period. Data on the presence of vascular calcifications and the severity of cardiac comorbidities were collected from the patients' EuCliD® records. Using a full structural equitation modelling of the total study sample, we found that the higher the increase in MF was observed in patients, the higher the probability of a decrease in the expression of miR-206 and TRIM63 and the lower severity of cardiac comorbidities. A reduced structural model in INC patients showed that the higher the decrease in MF, the higher the probability of the presence of calcifications and the higher severity of cardiac comorbidities. In EXC patients, we found that the higher the increase in MF, the lower the probability of higher severity of cardiovascular comorbidities.
Fresenius Medical Care Dialysis Services Kosice Kosice Slovakia
Olomouc University Social Health Institute Palacky University Olomouc Czech Republic
See more in PubMed
Ahmadmehrabi, S. , & Tang, W. H. W. (2018). Hemodialysis‐induced cardiovascular disease. Seminars in Dialysis, 31(3), 258–267. 10.1111/sdi.12694. PubMed DOI PMC
Andrade, F. P. , Rezende, P. S. , Ferreira, T. S. , Borba, G. C. , Müller, A. M. , & Rovedder, P. M. E. (2019). Effects of intradialytic exercise on cardiopulmonary capacity in chronic kidney disease: systematic review and meta‐analysis of randomized clinical trials. Scientific Reports, 9(1), 18470. 10.1038/s41598-019-54953-x. PubMed DOI PMC
Armstrong, T. , & Bull, F. (2006). Development of the World Health Organization global physical activity questionnaire (GPAQ). Journal of Public Health, 14, 66–70. 10.1007/s10389-006-0024-x. DOI
Arocho, A. , Chen, B. , Ladanyi, M. , & Pan, Q. (2006). Validation of the 2‐DeltaDeltaCt calculation as an alternate method of data analysis for quantitative PCR of BCR‐ABL P210 transcripts. Diagnostic Molecular Pathology, 15(1), 56–61. 10.1097/00019606-200603000-00009. PubMed DOI
Babaee, M. , Chamani, E. , Ahmadi, R. , Bahreini, E. , Balouchnejadmojarad, T. , Nahrkhalaji, A. S. , & Fallah, S. (2020). The expression levels of miRNAs‐ 27a and 23a in the peripheral blood mononuclear cells (PBMCs) and their correlation with FOXO1 and some inflammatory and anti‐inflammatory cytokines in the patients with coronary artery disease (CAD). Life Sciences, 256, 117898. 10.1016/j.lfs.2020.117898. PubMed DOI
Boettger, T. , Wust, S. , Nolte, H. , & Braun, T. (2014). The miR‐206/133b cluster is dispensable for development, survival and regeneration of skeletal muscle. Skeletal Muscle, 4(1), 23. 10.1186/s13395-014-0023-5. PubMed DOI PMC
Borg, G. A. (1982). Psychophysical bases of perceived exertion. Medicine and Science in Sports and Exercise, 14(5), 377–381. PubMed
Brandenburger, T. , Salgado Somoza, A. , Devaux, Y. , & Lorenzen, J. M. (2018). Noncoding RNAs in acute kidney injury. Kidney International, 94(5), 870–881. 10.1016/j.kint.2018.06.033. PubMed DOI
Bull, F. C. , Al‐Ansari, S. S. , Biddle, S. , Borodulin, K. , Buman, M. P. , Cardon, G. , Carty, C. , Chaput, J. P. , Chastin, S. , Chou, R. , Dempsey, P. C. , DiPietro, L. , Ekelund, U. , Firth, J. , Friedenreich, C. M. , Garcia, L. , Gichu, M. , Jago, R. , Katzmarzyk, P. T. … Willumsen, J. F. (2020). World Health Organization 2020 guidelines on physical activity and sedentary behaviour. British Journal of Sports Medicine, 54(24), 1451–1462. 10.1136/bjsports-2020-102955. PubMed DOI PMC
Celis‐Morales, C. A. , Lyall, D. M. , Anderson, J. , Iliodromiti, S. , Fan, Y. , Ntuk, U. E. , Mackay, D. F. , Pell, J. P. , Sattar, N. , & Gill, J. M. R. (2017). The association between physical activity and risk of mortality is modulated by grip strength and cardiorespiratory fitness: evidence from 498 135 UK‐Biobank participants. European Heart Journal, 38(2), 116–122. 10.1093/eurheartj/ehw249. PubMed DOI PMC
Charlson, M. E. , Pompei, P. , Ales, K. L. , & MacKenzie, C. R. (1987). A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. Journal of Chronic Diseases, 40(5), 373–383. 10.1016/0021-9681(87)90171-8. PubMed DOI
Choi, W. , Lee, J. , Lee, J. , Ko, K. R. , & Kim, S. (2018). Hepatocyte growth factor regulates the miR‐206‐HDAC4 cascade to control neurogenic muscle atrophy following surgical denervation in mice. Molecular Therapy ‐ Nucleic Acids, 12, 568–577. 10.1016/j.omtn.2018.06.013. PubMed DOI PMC
Cockwell, P. , & Fisher, L. A. (2020). The global burden of chronic kidney disease. Lancet, 395(10225), 662–664. 10.1016/S0140-6736(19)32977-0. PubMed DOI
Colpaert, R. M. W. , & Calore, M. (2019). MicroRNAs in Cardiac Diseases. Cells, 8(7), 737–10.3390/cells8070737. PubMed DOI PMC
Cozzolino, M. , Galassi, A. , Pivari, F. , Ciceri, P. , & Conte, F. (2017). The cardiovascular burden in end‐stage renal disease. Contributions to Nephrology, 191, 44–57. 10.1159/000479250. PubMed DOI
Cozzolino, M. , Mangano, M. , Stucchi, A. , Ciceri, P. , Conte, F. , & Galassi, A. (2018). Cardiovascular disease in dialysis patients. Nephrology Dialysis Transplantation, 33(suppl_3), iii28–iii34. 10.1093/ndt/gfy174. PubMed DOI PMC
Di Lullo, L. , House, A. , Gorini, A. , Santoboni, A. , Russo, D. , & Ronco, C. (2015). Chronic kidney disease and cardiovascular complications. Heart Failure Reviews, 20(3), 259–272. 10.1007/s10741-014-9460-9. PubMed DOI
Farina, N. H. , Wood, M. E. , Perrapato, S. D. , Francklyn, C. S. , Stein, G. S. , Stein, J. L. , & Lian, J. B. (2014). Standardizing analysis of circulating microRNA: clinical and biological relevance. Journal of Cellular Biochemistry, 115(5), 805–811. 10.1002/jcb.24745. PubMed DOI PMC
Feldman, A. , Moreira, D. A. R. , Gun, C. , Wang, H. T. L. , Hirata, M. H. , de Freitas Germano, J. , Leite, G. G. S. , & Farsky, P. (2017). Analysis of circulating miR‐1, miR‐23a, and miR‐26a in atrial fibrillation patients undergoing coronary bypass artery grafting surgery. Annals of Human Genetics, 81(3), 99–105. 10.1111/ahg.12188. PubMed DOI
Fu, X. , Liu, P. , Dimopoulos, G. , & Zhu, J. (2020). Dynamic miRNA‐mRNA interactions coordinate gene expression in adult Anopheles gambiae. PLoS Genetics, 16, e1008765. 10.1371/journal.pgen.1008765. PubMed DOI PMC
Gevaert, A. B. , Witvrouwen, I. , Vrints, C. J. , Heidbuchel, H. , Van Craenenbroeck, E. M. , Van Laere, S. J. , & Van Craenenbroeck, A. H. (2018). MicroRNA profiling in plasma samples using qPCR arrays: Recommendations for correct analysis and interpretation. PLoS One, 13(2), e0193173. 10.1371/journal.pone.0193173. PubMed DOI PMC
Han, H. , Qu, G. , Han, C. , Wang, Y. , Sun, T. , Li, F. , Wang, J. , & Luo, S. (2015). MiR‐34a, miR‐21 and miR‐23a as potential biomarkers for coronary artery disease: a pilot microarray study and confirmation in a 32 patient cohort. Experimental & Molecular Medicine, 47(2), e138. 10.1038/emm.2014.81. PubMed DOI PMC
Hong, S. , & Kim, M. M. (2018). IGFBP‐3 plays an important role in senescence as an aging marker. Environmental Toxicology and Pharmacology, 59, 138–145. 10.1016/j.etap.2018.03.014. PubMed DOI
Hu, X. , Ma, R. , Fu, W. , Zhang, C. , & Du, X. (2019). LncRNA UCA1 sponges miR‐206 to exacerbate oxidative stress and apoptosis induced by ox‐LDL in human macrophages. Journal of Cellular Physiology, 234(8), 14154–14160. 10.1002/jcp.28109. PubMed DOI
IBM Corp . (2013). IBM SPSS Statistics for Windows, Version 22.0. IBM Corp.
Jin, P. , Gu, W. , Lai, Y. , Zheng, W. , Zhou, Q. , & Wu, X. (2017). The circulating microRNA‐206 level predicts the severity of pulmonary hypertension in patients with left heart diseases. Cellular Physiology and Biochemistry, 41(6), 2150–2160. 10.1159/000475569. PubMed DOI
Jin, Y. , Zhou, T. Y. , Cao, J. N. , Feng, Q. T. , Fu, Y. J. , Xu, X. , & Yang, C. J. (2019). MicroRNA‐206 downregulates Connexin43 in cardiomyocytes to induce cardiac arrhythmias in a transgenic mouse model. Heart, Lung & Circulation, 28(11), 1755–1761. 10.1016/j.hlc.2018.09.008. PubMed DOI
Kirby, T. J. , Chaillou, T. , & McCarthy, J. J. (2015). The role of microRNAs in skeletal muscle health and disease. Frontiers in Bioscience, 20, 37–77. 10.2741/4298. PubMed DOI PMC
Kleeberger, J. A. , Neuser, J. , de Gonzalo‐Calvo, D. , Kempf, T. , Bauersachs, J. , Thum, T. , & Widder, J. D. (2017). MicroRNA‐206 correlates with left ventricular function after transcatheter aortic valve implantation. American Journal of Physiology. Heart and Circulatory Physiology, 313(6), H1261–H1266. 10.1152/ajpheart.00432.2017. PubMed DOI
Kölling, M. , Seeger, H. , Haddad, G. , Kistler, A. , Nowak, A. , Faulhaber‐Walter, R. , Kielstein, J. , Haller, H. , Fliser, D. , Mueller, T. , Wüthrich, R. P. , & Lorenzen, J. M. (2018). The circular RNA ciRs‐126 predicts survival in critically ill patients with acute kidney injury. Kidney International Reports, 3(5), 1144–1152. 10.1016/j.ekir.2018.05.012. PubMed DOI PMC
Lee, K. J. , & Carlin, J. B. (2010). Multiple imputation for missing data: fully conditional specification versus multivariate normal imputation. American Journal of Epidemiology, 171(5), 624–632. 10.1093/aje/kwp425. PubMed DOI
Li, H. , Xiang, Y. , Fan, L. J. , Zhang, X. Y. , Li, J. P. , Yu, C. X. , Bao, L. Y. , Cao, D. S. , Xing, W. B. , Liao, X. H. , & Zhang, T. C. (2017). Myocardin inhibited the gap protein connexin 43 via promoted miR‐206 to regulate vascular smooth muscle cell phenotypic switch. Gene, 616, 22–30. 10.1016/j.gene.2017.03.029. PubMed DOI
Li, M. , Chen, X. , Chen, L. , Chen, K. , Zhou, J. , & Song, J. (2018). MiR‐1‐3p that correlates with left ventricular function of HCM can serve as a potential target and differentiate HCM from DCM. Journal of Translational Medicine, 16(1), 161. 10.1186/s12967-018-1534-3. PubMed DOI PMC
Limana, F. , Esposito, G. , D'Arcangelo, D. , Di Carlo, A. , Romani, S. , Melillo, G. , Mangoni, A. , Bertolami, C. , Pompilio, G. , Germani, A. , & Capogrossi, M. C. (2011). HMGB1 attenuates cardiac remodelling in the failing heart via enhanced cardiac regeneration and miR‐206‐mediated inhibition of TIMP‐3. PLoS One, 6(6), e19845. 10.1371/journal.pone.0019845. PubMed DOI PMC
Lin, Z. , Murtaza, I. , Wang, K. , Jiao, J. , Gao, J. , & Li, P. F. (2009). MiR‐23a functions downstream of NFATc3 to regulate cardiac hypertrophy. Proceedings of the National Academy of Sciences, 106(29), 12103–12108. 10.1073/pnas.0811371106. PubMed DOI PMC
Liu, T. J. , Wang, B. , Li, Q. X. , Dong, X. L. , Han, X. L. , & Zhang, S. B. (2018). Effects of microRNA‐206 and its target gene IGF‐1 on sevoflurane‐induced activation of hippocampal astrocytes in aged rats through the PI3K/AKT/CREB signaling pathway. Journal of Cellular Physiology, 233(5), 4294–4306. 10.1002/jcp.26248. PubMed DOI
Liu, W. , Ling, S. , Sun, W. , Liu, T. , Li, Y. , Zhong, G. , Zhao, D. , Zhang, P. , Song, J. , Jin, X. , Xu, Z. , Song, H. , Li, Q. , Liu, S. , Chai, M. , Dai, Q. , He, Y. , Fan, Z. , Zhou, Y. J. , & Li, Y. (2015). Circulating microRNAs correlated with the level of coronary artery calcification in symptomatic patients. Scientific Reports, 5, 16099. 10.1038/srep16099. PubMed DOI PMC
Livak, K. J. , & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real‐time quantitative PCR and the 2(‐Delta Delta C(T)) Method. Methods, 25(4), 402–408. 10.1006/meth.2001.1262. PubMed DOI
Martin, N. , Smith, A. C. , Dungey, M. R. , Young, H. M. L. , Burton, J. O. , & Bishop, N. C. (2018). Exercise during hemodialysis does not affect the phenotype or prothrombotic nature of microparticles but alters their proinflammatory function. Physiological Reports, 6(19), e13825. 10.14814/phy2.13825. PubMed DOI PMC
McCarthy, J. J. (2008). MicroRNA‐206: the skeletal muscle‐specific myomiR. Biochimica Et Biophysica Acta, 1779, 682–691. 10.1016/j.bbagrm.2008.03.001. PubMed DOI PMC
Mercatelli, N. , Fittipaldi, S. , De Paola, E. , Dimauro, I. , Paronetto, M. P. , Jackson, M. J. , & Caporossi, D. (2017). MiR‐23‐TrxR1 as a novel molecular axis in skeletal muscle differentiation. Scientific Reports, 7(1), 7219. 10.1038/s41598-017-07575-0. PubMed DOI PMC
Moraes, L. N. , Fernandez, G. J. , Vechetti‐Junior, I. J. , Freire, P. P. , Souza, R. W. A. , Villacis, R. A. R. , Rogatto, S. R. , Reis, P. P. , Dal‐Pai‐Silva, M. , & Carvalho, R. F. (2017). Integration of miRNA and mRNA expression profiles reveals microRNA‐regulated networks during muscle wasting in cardiac cachexia. Scientific Reports, 7, 6998. 10.1038/s41598-017-07236-2. PubMed DOI PMC
Moresi, V. , Williams, A. H. , Meadows, E. , Flynn, J. M. , Potthoff, M. J. , McAnally, J. , Shelton, J. M. , Backs, J. , Klein, W. H. , Richardson, J. A. , Bassel‐Duby, R. , & Olson, E. N. (2010). Myogenin and class II HDACs control neurogenic muscle atrophy by inducing E3 ubiquitin ligases. Cell, 143(1), 35–45. 10.1016/j.cell.2010.09.004. PubMed DOI PMC
Myers, W. R. (2000). Handling missing data in clinical trials: an overview. Drug Information Journal, 34(2), 525–533. 10.1177/009286150003400221. DOI
Novak, J. , Kruzliak, P. , Bienertova‐Vasku, J. , Slaby, O. , & Novak, M. (2014). MicroRNA‐206: a promising theranostic marker. Theranostics, 4(2), 119–133. 10.7150/thno.7552. PubMed DOI PMC
Nystoriak, M. A. , & Bhatnagar, A. (2018). Cardiovascular effects and benefits of exercise. Frontiers in Cardiovascular Medicine, 5, 135. 10.3389/fcvm.2018.00135. PubMed DOI PMC
Peris‐Moreno, D. , Taillandier, D. , & Polge, C. (2020). MuRF1/TRIM63, master regulator of muscle mass. International Journal of Molecular Sciences, 21(18), 6663. 10.3390/ijms21186663. PubMed DOI PMC
Qiao, Y. , Wang, C. , Kou, J. , Wang, L. , Han, D. , Huo, D. , Li, F. , Zhou, X. , Meng, D. , Xu, J. , Murtaza, G. , Artyom, B. , Ma, N. , & Luo, S. (2020). MicroRNA‐23a suppresses the apoptosis of inflammatory macrophages and foam cells in atherogenesis by targeting HSP90. Gene, 729, 144319. 10.1016/j.gene.2019.144319. PubMed DOI
Roberts, T. C. , Coenen‐Stass, A. M. , & Wood, M. J. (2014). Assessment of RT‐qPCR normalization strategies for accurate quantification of extracellular microRNAs in murine serum. PLoS One, 9(2), e89237. 10.1371/journal.pone.0089237. PubMed DOI PMC
Sapp, R. M. , Chesney, C. A. , Eagan, L. E. , Evans, W. S. , Zietowski, E. M. , Prior, S. J. , Hagberg, J. M. , & Ranadive, S. M. (2020). Changes in circulating microRNA and arterial stiffness following high‐intensity interval and moderate intensity continuous exercise. Physiological Reports, 8(9), e14431. 10.14814/phy2.14431. PubMed DOI PMC
Sarrion, I. , Milian, L. , Juan, G. , Ramon, M. , Furest, I. , Carda, C. , Cortijo Gimeno, J. , & Mata Roig, M. (2015). Role of circulating miRNAs as biomarkers in idiopathic pulmonary arterial hypertension: possible relevance of miR‐23a. Oxidative Medicine and Cellular Longevity, , 2015, 1–10. 10.1155/2015/792846. PubMed DOI PMC
Satoh, M. , Nasu, T. , Takahashi, Y. , Osaki, T. , Hitomi, S. , Morino, Y. , & Nakamura, M. (2017). Expression of miR‐23a induces telomere shortening and is associated with poor clinical outcomes in patients with coronary artery disease. Clinical Science (Lond), 131(15), 2007–2017. 10.1042/CS20170242. PubMed DOI
Shan, Z. X. , Lin, Q. X. , Fu, Y. H. , Deng, C. H. , Zhou, Z. L. , Zhu, J. N. , Liu, X. Y. , Zhang, Y. Y. , Li, Y. , Lin, S. G. , & Yu, X. Y. (2009). Upregulated expression of miR‐1/miR‐206 in a rat model of myocardial infarction. Biochemical and Biophysical Research Communications, 381(4), 597–601. 10.1016/j.bbrc.2009.02.09717. PubMed DOI
Sharma, M. , Juvvuna, P. K. , Kukreti, H. , & McFarlane, C. (2014). Mega roles of microRNAs in regulation of skeletal muscle health and disease. Frontiers in Physiology, 5, 239. 10.3389/fphys.2014.00239. PubMed DOI PMC
Shlipak, M. G. , Tummalapalli, S. L. , Boulware, L. E. , Grams, M. E. , Ix, J. H. , Jha, V. , Kengne, A.‐P. , Madero, M. , Mihaylova, B. , Tangri, N. , Cheung, M. , Jadoul, M. , Winkelmayer, W. C. , Zoungas, S. , Abraham, G. , Ademi, Z. , Alicic, R. Z. , de Boer, I. , Deo, R. , … Zomer, E. (2021). The case for early identification and intervention of chronic kidney disease: conclusions from a Kidney Disease: Improving Global Outcomes (KDIGO) Controversies Conference. Kidney International, 99(1), 34–47. 10.1016/j.kint.2020.10.012. PubMed DOI
Sierra‐Johnson, J. , Romero‐Corral, A. , Somers, V. K. , Lopez‐Jimenez, F. , Mälarstig, A. , Brismar, K. , Hamsten, A. , Fisher, R. M. , & Hellénius, M.‐L. (2009). IGF‐I/IGFBP‐3 ratio: a mechanistic insight into the metabolic syndrome. Clinical Science (Lond), 116(6), 507–512. 10.1042/CS20080382. PubMed DOI
Spakova, I. , Zelko, A. , Rabajdova, M. , Kolarcik, P. , Rosenberger, J. , Zavacka, M. , Marekova, M. , Madarasova Geckova, A. , van Dijk, J. P. , & Reijneveld, S. A. (2020). MicroRNA molecules as predictive biomarkers of adaptive responses to strength training and physical inactivity in haemodialysis patients. Scientific Reports, 10(1), 15597. 10.1038/s41598-020-72542-1. PubMed DOI PMC
Subbiah, A. K. , Chhabra, Y. K. , & Mahajan, S. (2016). Cardiovascular disease in patients with chronic kidney disease: a neglected subgroup. Heart Asia, 8(2), 56–61. 10.1136/heartasia-2016-010809. PubMed DOI PMC
Thivel, D. , Tremblay, A. , Genin, P. M. , Panahi, S. , Rivière, D. , & Duclos, M. (2018). Physical activity, inactivity, and sedentary behaviors: Definitions and implications in occupational health. Frontiers in Public Health, 6, 288. 10.3389/fpubh.2018.00288. PubMed DOI PMC
Thum, T. , Catalucci, D. , & Bauersachs, J. (2008). MicroRNAs: novel regulators in cardiac development and disease. Cardiovascular Research, 79(4), 562–570. 10.1093/cvr/cvn137. PubMed DOI
Toshima, T. , Watanabe, T. , Narumi, T. , Otaki, Y. , Shishido, T. , Aono, T. , Goto, J. , Watanabe, K. , Sugai, T. , Takahashi, T. , Yokoyama, M. , Kinoshita, D. , Tamura, H. , Kato, S. , Nishiyama, S. , Arimoto, T. , Takahashi, H. , Miyamoto, T. , Sadahiro, M. , & Watanabe, M. (2020). Therapeutic inhibition of microRNA‐34a ameliorates aortic valve calcification via modulation of Notch1‐Runx2 signalling. Cardiovascular Research, 116(5), 983–994. 10.1093/cvr/cvz210. PubMed DOI
Valencia‐Sanchez, M. A. , Liu, J. , Hannon, G. J. , & Parker, R. (2006). Control of translation and mRNA degradation by miRNAs and siRNAs. Genes & Development, 20, 515–524. 10.1101/gad.1399806. PubMed DOI
van Rooij, E. , Sutherland, L. B. , Liu, N. , Williams, A. H. , McAnally, J. , Gerard, R. D. , Richardson, J. A. , & Olson, E. N. (2006). A signature pattern of stress‐responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proceedings of the National Academy of Sciences, 103(48), 18255–18260. 10.1073/pnas.0608791103. PubMed DOI PMC
Varma Shrivastav, S. , Bhardwaj, A. , Pathak, K. A. , & Shrivastav, A. (2020). Insulin‐like growth factor binding protein‐3 (IGFBP‐3): Unraveling the role in mediating IGF‐independent effects within the cell. Frontiers in Cell and Developmental Biology, 8, 286. 10.3389/fcell.2020.00286. PubMed DOI PMC
Wang, F. , Wang, J. , He, J. , Li, W. , Li, J. , Chen, S. , Zhang, P. , Liu, H. , & Chen, X. (2017). Serum miRNAs miR‐23a, 206, and 499 as potential biomarkers for skeletal muscle atrophy. BioMed Research International, 2017, 8361237. 10.1155/2017/8361237. PubMed DOI PMC
Wang, L. , Chen, X. , Zheng, Y. , Li, F. , Lu, Z. , Chen, C. , Liu, J. , Wang, Y. , Peng, Y. , Shen, Z. , Gao, J. , Zhu, M. , & Chen, H. (2012). MiR‐23a inhibits myogenic differentiation through down regulation of fast myosin heavy chain isoforms. Experimental Cell Research, 318(18), 2324–2334. 10.1016/j.yexcr.2012.06.018. PubMed DOI
Wang, S. , He, W. , & Wang, C. (2016). MiR‐23a Regulates the vasculogenesis of coronary artery disease by targeting epidermal growth factor receptor. Cardiovascular Therapeutics, 34(4), 199–208. 10.1111/1755-5922.12187. PubMed DOI
Wang, X. H. (2013). MicroRNA in myogenesis and muscle atrophy. Current Opinion in Clinical Nutrition and Metabolic Care, 16(3), 258–266. 10.1097/MCO.0b013e32835f81b9. PubMed DOI PMC
Wang, X. H. , & Price, S. R. (2020). Going micro in CKD‐related cachexia. Nephrology, Dialysis, Transplantation, 35(9), 1462–1464. 10.1093/ndt/gfaa025. PubMed DOI PMC
Westendorp, B. , Major, J. L. , Nader, M. , Salih, M. , Leenen, F. H. , & Tuana, B. S. (2012). The E2F6 repressor activates gene expression in myocardium resulting in dilated cardiomyopathy. The FASEB Journal, 26(6), 2569–2579. 10.1096/fj.11-203174. PubMed DOI
Wu, F. , Wang, F. , Yang, Q. , Zhang, Y. , Cai, K. , Liu, L. , Li, S. , Zheng, Y. Z. , Zhang, J. , Gui, Y. , Wang, Y. , Wang, X. , Gui, Y. , & Li, Q. (2020). Upregulation of miRNA‐23a‐3p rescues high glucose‐induced cell apoptosis and proliferation inhibition in cardiomyocytes. In Vitro Cellular & Developmental Biology ‐ Animal, 56(10), 866–877. 10.1007/s11626-020-00518-6. PubMed DOI PMC
Xing, T. , Du, L. , Zhuang, X. , Zhang, L. , Hao, J. , & Wang, J. (2017). Upregulation of microRNA‐206 induces apoptosis of vascular smooth muscle cells and decreases risk of atherosclerosis through modulating FOXP1. Experimental and Therapeutic Medicine, 14(5), 4097–4103. 10.3892/etm.2017.5071. PubMed DOI PMC
Yang, Y. , Del Re, D. P. , Nakano, N. , Sciarretta, S. , Zhai, P. , Park, J. , Sayed, D. , Shirakabe, A. , Matsushima, S. , Park, Y. , Tian, B. , Abdellatif, M. , & Sadoshima, J. (2015). miR‐206 mediates YAP‐induced cardiac hypertrophy and survival. Circulation Research, 117(10), 891–904. 10.1161/CIRCRESAHA.115.306624. PubMed DOI PMC
Zelko, A. , Skoumalova, I. , Kolarcik, P. , Rosenberger, J. , Rabajdova, M. , Marekova, M. , Geckova, A. M. , van Dijk, J. P. , & Reijneveld, S. A. (2019). The effects of intradialytic resistance training on muscle strength, psychological well‐being, clinical outcomes and circulatory micro‐ribonucleic acid profiles in haemodialysis patients: Protocol for a quasi‐experimental study. Medicine (Baltimore), 98(19), e15570. 10.1097/MD.0000000000015570. PubMed DOI PMC
Zhao, X. , Gu, H. , Wang, L. , Zhang, P. , Du, J. , Shen, L. , Jiang, D. , Wang, J. , Li, X. , Zhang, S. , Li, M. , & Zhu, L. (2020). MicroRNA‐23a‐5p mediates the proliferation and differentiation of C2C12 myoblasts. Molecular Medicine Reports, 22(5), 3705–3714. 10.3892/mmr.2020.11475. PubMed DOI PMC
Zhou, J. , Shao, G. , Chen, X. , Yang, X. , Huang, X. , Peng, P. , Ba, Y. , Zhang, L. , Jehangir, T. , Bu, S. , Liu, N. , & Lian, J. (2015). miRNA 206 and miRNA 574–5p are highly expression in coronary artery disease. Bioscience Reports, 36(1), e00295. 10.1042/BSR20150206. PubMed DOI PMC
Zununi Vahed, S. , Mostafavi, S. , Hosseiniyan Khatibi, S. M. , Shoja, M. M. , & Ardalan, M. (2020). Vascular calcification: an important understanding in nephrology. Vascular Health and Risk Management, 16, 167–180. 10.2147/VHRM.S242685. PubMed DOI PMC