Identification of regulatory elements directing miR-23a–miR-27a–miR-24-2 transcriptional regulation in response to muscle hypertrophic stimuli

Hernandez-Torres, Francisco; Aranega, Amelia E.; Franco, Diego

doi:10.1016/j.bbagrm.2014.07.009

Cited by 36MicroRNA in disease regulationMuscle Physiology and DisordersGenomics and Chromatin Dynamics

Identification of regulatory elements directing miR-23a–miR-27a–miR-24-2 transcriptional regulation in response to muscle hypertrophic stimuli

Hernandez-Torres, Francisco, Aranega, Amelia E., Franco, Diego·2014·Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms

DOI 10.1016/j.bbagrm.2014.07.009

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Abstract

MiRNAs are small non-coding RNAs that significantly regulate the translation of protein coding genes in higher organisms. MicroRNAs are involved in almost every biological process, including early development, lineage commitment, growth and differentiation, cell death, and metabolic control. Misregulation of miRNAs belonging to the intergenic miR-23a-miR-27a-miR-24-2 cluster has been recently associated to cardiac and skeletal muscle diseases, and they are up-regulated in hypertrophic cardiomyopathy and skeletal muscle atrophy. Despite these facts, the basal transcriptional regulation of miR-23a/miR-27-a/miR-24-2 cluster and how it is altered under pathological conditions remain unclear. In this study, we identified and functionally characterized conserved upstream and downstream regulatory sequences from the miR-23a-miR-27a-miR-24-2 locus that are implicated on its transcriptional control. Our data demonstrate that Srf plays a pivotal role in modulating miR-23a-miR-27a-miR-24-2 cluster proximal promoter activity. Importantly, pro-hypertrophic signalling pathways such as those driven by angiotensin II and norepinephrine also regulate miR-23a-miR-27a-miR-24-2 cluster proximal promoter activity. Taking together, our results provide new insights into the regulatory networks driving miR-23a-miR-27a-miR-24-2 cluster expression in cardiac and skeletal muscles.

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Angiotensin II and norepinephrine in pro-hypertrophic signaling pathways can upregulate miR-23-24-27 cluster expression levels in hypertrophic cardiomyopathy and skeletal muscle atrophy.
“Among other upstream regulatory signals, angiotensin II and norepinephrine in the pro-hypertrophic signaling pathways can also regulate the proximal promoter of miRNA. Together, they can upregulate miR-23-24-27 cluster expression levels in hypertrophic cardiomyopathy and skeletal muscle atrophy [50].”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [50]

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Untitled work
Bartel (2004) · doi:10.1016/s0092-8674(04)00045-5 · Cited by 34,714 · see citing works
The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., et al. (2009) · Clinical Chemistry · doi:10.1373/clinchem.2008.112797 · Cited by 16,303 · see citing works
MicroRNA genes are transcribed by RNA polymerase II
Lee, Y., Kim, M., Han, J., Yeom, K.-H., Lee, S., Baek, S. H., & Kim, V. N. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600385 · Cited by 4,355 · see citing works
QUANTITATIVE STUDIES OF THE GROWTH OF MOUSE EMBRYO CELLS IN CULTURE AND THEIR DEVELOPMENT INTO ESTABLISHED LINES
Todaro, G. J., & Green, H. (1963) · The Journal of Cell Biology · doi:10.1083/jcb.17.2.299 · Cited by 2,725 · see citing works
c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism
Gao, P., Tchernyshyov, I., Chang, T.-C., Lee, Y.-S., Kita, K., Ochi, T., Zeller, K. I., De Marzo, A. M., Van Eyk, J. E., Mendell, J. T., et al. (2009) · Nature · doi:10.1038/nature07823 · Cited by 2,124 · see citing works
Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development.
Murry, C., & Keller, G. (2008) · Cell · doi:10.1016/j.cell.2008.02.008 · Cited by 1,805 · see citing works
HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte
Claycomb, W. C., Lanson, N. A., Stallworth, B. S., Egeland, D. B., Delcarpio, J. B., Bahinski, A., & Izzo, N. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.2979 · Cited by 1,546 · see citing works
SMAD proteins control DROSHA-mediated microRNA maturation
Davis‐Dusenbery, B. N., Hilyard, A. C., Lagna, G., & Hata, A. (2008) · Nature · doi:10.1038/nature07086 · Cited by 1,243 · see citing works
Pervasive roles of microRNAs in cardiovascular biology
Small, E. M., & Olson, E. N. (2011) · Nature · doi:10.1038/nature09783 · Cited by 1,180 · see citing works
Direct stimulation of Jak/STAT pathway by the angiotensin II AT1 receptor
Marrero, M. B., Schieffer, B., Paxton, W. G., Heerdt, L., Berk, B. C., Delafontaine, P., & Bernstein, K. E. (1995) · Nature · doi:10.1038/375247a0 · Cited by 744 · see citing works
Posttranscriptional Regulation of MicroRNA Biogenesis in Animals
Siomi, H., & Siomi, M. C. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.03.013 · Cited by 574 · see citing works
MicroRNA-24 Regulates Vascularity After Myocardial Infarction
Fiedler, J., Jazbutyte, V., Kirchmaier, B. C., Gupta, S. K., Lorenzen, J. M., Hartmann, D., Galuppo, P., Kneitz, S., Pena, J., Sohn-Lee, C., et al. (2011) · Circulation · doi:10.1161/circulationaha.111.039008 · Cited by 391 · see citing works
Smad Proteins Bind a Conserved RNA Sequence to Promote MicroRNA Maturation by Drosha
Davis‐Dusenbery, B. N., Hilyard, A. C., Nguyen, P. H., Lagna, G., & Hata, A. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.07.011 · Cited by 384 · see citing works
Structure and activity of putative intronic miRNA promoters
Monteys, A. M., Spengler, R. M., Wan, J., Tecedor, L., Lennox, K. A., Xing, Y., & Davidson, B. L. (2010) · RNA · doi:10.1261/rna.1731910 · Cited by 379 · see citing works
Embryonic stem cells: a model to study structural and functional properties in cardiomyogenesis
Hescheler, J. (1997) · Cardiovascular Research · doi:10.1016/s0008-6363(97)00193-4 · Cited by 366 · see citing works
Skeletal muscle hypertrophy and regeneration: interplay between the myogenic regulatory factors (MRFs) and insulin-like growth factors (IGFs) pathways
Zanou, N., & Gailly, P. L. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1330-4 · Cited by 361 · see citing works
miR-23a functions downstream of NFATc3 to regulate cardiac hypertrophy
Lin, Z., Murtaza, I., Wang, K., Jiao, J., Gao, J., & Li, P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811371106 · Cited by 360 · see citing works
Regulation of MicroRNA Biogenesis: A miRiad of mechanisms
Davis‐Dusenbery, B. N., & Hata, A. (2009) · Cell Communication and Signaling · doi:10.1186/1478-811x-7-18 · Cited by 332 · see citing works
miR-24 inhibits apoptosis and represses Bim in mouse cardiomyocytes
Li, Q., Laake, L. W. V., Huang, Y., Liu, S. J., Wendland, M. F., & Srivastava, D. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20101547 · Cited by 321 · see citing works
Features of Mammalian microRNA Promoters Emerge from Polymerase II Chromatin Immunoprecipitation Data
Corcoran, D. L., Pandit, K. V., Gordon, B., Bhattacharjee, A., Kaminski, N., & Benos, P. V. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005279 · Cited by 300 · see citing works
Muscle stem cell behavior is modified by microRNA-27 regulation of Pax3 expression
Crist, C. G., Montarras, D., Pallafacchina, G., Rocancourt, D., Cumano, A., Conway, S. J., & BUCKINGHAM, M. E. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900210106 · Cited by 298 · see citing works
Transforming growth factor- -regulated miR-24 promotes skeletal muscle differentiation
Sun, Q., Zhang, Y., Yang, G., Chen, X., Zhang, Y., Cao, G., Wang, J., Sun, Y., Zhang, Y., Fan, M., et al. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn032 · Cited by 261 · see citing works
Evolution and functional classification of vertebrate gene desertsPreprint
Ovcharenko, I., Loots, G. G., Nóbrega, M. A., Hardison, R. C., Miller, W., & Stubbs, L. J. (2004) · Genome Research · doi:10.1101/gr.3015505 · Cited by 235 · see citing works
Upregulation of miR‐23a∼27a∼24 decreases transforming growth factor‐beta‐induced tumor‐suppressive activities in human hepatocellular carcinoma cells
Huang, S., He, X., Ding, J., Liang, L., Zhao, Y., Zhang, Z., Xiao, Y., Pan, Z., Zhang, P., Li, J., et al. (2008) · International Journal of Cancer · doi:10.1002/ijc.23580 · Cited by 204 · see citing works
Translational Suppression of Atrophic Regulators by MicroRNA-23a Integrates Resistance to Skeletal Muscle Atrophy
Wada, S., Kato, Y., Okutsu, M., Miyaki, S., Suzuki, K., Yan, Z., Schiaffino, S., Asahara, H., Ushida, T., & Akimoto, T. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.271270 · Cited by 200 · see citing works
Targeted Deletion of MicroRNA-22 Promotes Stress-Induced Cardiac Dilation and Contractile Dysfunction
Gurha, P., Abreu‐Goodger, C., Wang, T., Ramirez, M. O., Drumond‐Bock, A. L., van Dongen, S., Chen, Y., Bartoniček, N., Enright, A. J., Lee, B., et al. (2012) · Circulation · doi:10.1161/circulationaha.111.044354 · Cited by 185 · see citing works
Angiotensin II stimulates sis-inducing factor-like DNA binding activity. Evidence that the AT1A receptor activates transcription factor-Stat91 and/or a related protein.
Bhat, G. J., Thekkumkara, T., Thomas, W. G., Conrad, K., & Baker, K. M. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)31714-9 · Cited by 184 · see citing works
MEF2 is upregulated during cardiac hypertrophy and is required for normal post-natal growth of the myocardium
Kolodziejczyk, S. M., Wang, L., Balazsi, K., DeRepentigny, Y., Kothary, R., & Megeney, L. A. (1999) · Current Biology · doi:10.1016/s0960-9822(00)80027-5 · Cited by 168 · see citing works
TheMef2cgene is a direct transcriptional target of myogenic bHLH and MEF2 proteins during skeletal muscle development
Wang, D., Valdez, M. R., McAnally, J., Richardson, J. A., & Olson, E. N. (2001) · Development · doi:10.1242/dev.128.22.4623 · Cited by 162 · see citing works
Cardiomyopathy in transgenic mice with cardiac-specific overexpression of serum response factor
Zhang, X., Azhar, G., Chai, J., Sheridan, P. L., Nagano, K., Brown, T., Yang, J., Khrapko, K., Borras, A. M., Lawitts, J. A., et al. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.280.4.h1782 · Cited by 147 · see citing works
MicroRNAs in Skeletal and Cardiac Muscle Development
Callis, T. E., Chen, J.-F., & Wang, D.-Z. (2007) · DNA and Cell Biology · doi:10.1089/dna.2006.0556 · Cited by 138 · see citing works
miR-23a is decreased during muscle atrophy by a mechanism that includes calcineurin signaling and exosome-mediated export
Hudson, M. B., Woodworth-Hobbs, M. E., Zheng, B., Rahnert, J. A., Blount, M. A., Gooch, J. L., Searles, C. D., & Price, S. R. (2014) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00266.2013 · Cited by 137 · see citing works
Upregulation of miR-23a∼27a∼24-2 Cluster Induces Caspase-Dependent and -Independent Apoptosis in Human Embryonic Kidney Cells
Chhabra, R., Adlakha, Y. K., Hariharan, M., Scaria, V., & Saini, N. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005848 · Cited by 134 · see citing works
The Transcription Factor MEF2C Is Required for Craniofacial Development
Verzi, M. P., Agarwal, P., Brown, C., McCulley, D. J., Schwarz, J. J., & Black, B. L. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.03.007 · Cited by 129 · see citing works
MicroRNA-27a promotes myoblast proliferation by targeting myostatin
Huang, Z., Chen, X., Yu, B., He, J., & Chen, D. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.05.106 · Cited by 118 · see citing works
Signal transduction and activator of transcription (STAT) protein-dependent activation of angiotensinogen promoter: A cellular signal for hypertrophy in cardiac muscle
Mascareno, E. J., Dhar, M., & Siddiqui, M. A. Q. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.10.5590 · Cited by 117 · see citing works
Taking microRNAs to heart
Callis, T. E., & Wang, D. (2008) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2008.03.006 · Cited by 114 · see citing works
Cardiac Hypertrophy Is Positively Regulated by MicroRNA miR-23a
Wang, K., Lin, Z., Long, B., Li, J.-H., Zhou, J., & Li, P. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.266940 · Cited by 113 · see citing works
A phenotypic screen to identify hypertrophy-modulating microRNAs in primary cardiomyocytes
Jentzsch, C., Leierseder, S., Loyer, X., Flohrschütz, I., Sassi, Y., Hartmann, D., Thum, T., Laggerbauer, B., & Engelhardt, S. H. (2011) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2011.07.010 · Cited by 113 · see citing works
MicroRNA profiling during mouse ventricular maturation: a role for miR-27 modulating Mef2c expression
Chinchilla, A., Lozano-Velasco, E., Daimi, H., Esteban, F. J., Crist, C. G., Aránega, A. E., & Franco, D. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq264 · Cited by 111 · see citing works
Self-citation
MicroRNAs in the cardiovascular system
Han, M., Toli, J., & Abdellatif, M. (2011) · Current Opinion in Cardiology · doi:10.1097/hco.0b013e328345983d · Cited by 103 · see citing works
In Vivo Suppression of MicroRNA-24 Prevents the Transition Toward Decompensated Hypertrophy in Aortic-Constricted Mice
Li, R.-C., Tao, J., Guo, Y., Wu, H., Liu, R., Bai, Y., Lv, Z., Luo, G., Li, L., Wang, M., et al. (2013) · Circulation Research · doi:10.1161/circresaha.112.300806 · Cited by 97 · see citing works
Modulation of adverse cardiac remodeling by STARS, a mediator of MEF2 signaling and SRF activity
Kuwahara, K., Pipes, G. C. T., McAnally, J., Richardson, J. A., Hill, J. A., Bassel‐Duby, R., & Olson, E. N. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31240 · Cited by 94 · see citing works
The Mef2 Transcription Network Is Disrupted in Myotonic Dystrophy Heart Tissue, Dramatically Altering miRNA and mRNA Expression
Kalsotra, A., Singh, R. K., Gurha, P., Ward, A. J., Creighton, C. J., & Cooper, T. A. (2014) · Cell Reports · doi:10.1016/j.celrep.2013.12.025 · Cited by 93 · see citing works
Down-Regulation of Myogenin Can Reverse Terminal Muscle Cell Differentiation
Mastroyiannopoulos, N. P., Nicolaou, P., Anayasa, M., Uney, J. B., & Phylactou, L. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029896 · Cited by 90 · see citing works
MicroRNA-27a Regulates Beta Cardiac Myosin Heavy Chain Gene Expression by Targeting Thyroid Hormone Receptor β1 in Neonatal Rat Ventricular Myocytes
Nishi, H., Ono, K., Horie, T., Nagao, K., Kinoshita, M., Kuwabara, Y., Watanabe, S., Takaya, T., Tamaki, Y., Takanabe‐Mori, R., et al. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00581-10 · Cited by 82 · see citing works
Regulation of miRNA biogenesis as an integrated component of growth factor signaling
Blahna, M. T., & Hata, A. (2013) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2012.12.005 · Cited by 77 · see citing works
Nuclear networking fashions pre-messenger RNA and primary microRNA transcripts for function
Pawlicki, J. M., & STEITZ, J. A. (2009) · Trends in Cell Biology · doi:10.1016/j.tcb.2009.10.004 · Cited by 77 · see citing works
Functional activity of the two promoters of the myosin alkali light chain gene in primary muscle cell cultures: comparison with other muscle gene promoters and other culture systems
Daubas, P., Klarsfeld, A., Garner, I., Pinset, C., Cox, R., & BUCKINGHAM, M. E. (1988) · Nucleic Acids Research · doi:10.1093/nar/16.4.1251 · Cited by 70 · see citing works
Pathophysiologic role of the renin-angiotensin-aldosterone and sympathetic nervous systems in heart failure
Adams, K. F. (2004) · American Journal of Health-System Pharmacy · doi:10.1093/ajhp/61.suppl_2.s4 · Cited by 68 · see citing works
microRNA expression profiling of the developing mouse heart
Cao, L. H., Kong, L., Yu, Z., Han, S., Bai, Y., Zhu, J., Hu, X., Zhu, C., Zhu, S., & Guo, X. (2012) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2012.1092 · Cited by 53 · see citing works
MicroRNA: Novel Regulators Involved in the Remodeling and Reverse Remodeling of the Heart
Wang, J., Xu, R., Lin, F., Zhang, S., Zhang, G., Hu, S., & Zhe, Z. (2008) · Cardiology · doi:10.1159/000172616 · Cited by 46 · see citing works
Pitx2c modulates Pax3+/Pax7+ cell populations and regulates Pax3 expression by repressing miR27 expression during myogenesis
Lozano-Velasco, E., Contreras‐Ramos, A., Crist, C. G., Hernández‐Torres, F., Franco, D., & Aránega, A. E. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.06.039 · Cited by 44 · see citing works
Self-citation
Gli2 and MEF2C activate each other's expression and function synergistically during cardiomyogenesis in vitro
Voronova, A., Madhoun, A. S. A., Anna, F., Shelton, M., Karamboulas, C., & Skerjanc, I. S. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1232 · Cited by 42 · see citing works
Angiotensin II and norepinephrine activate specific calcineurin-dependent NFAT transcription factor isoforms in cardiomyocytes
Lunde, I. G., Kvaløy, H., Austbø, B., Christensen, G., & Carlson, C. R. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01383.2010 · Cited by 40 · see citing works
Molecular mechanisms controlling the coupled development of myocardium and coronary vasculature
Bhattacharya, S., MacDonald, S. T., & Farthing, C. R. (2006) · Clinical Science · doi:10.1042/cs20060003 · Cited by 37 · see citing works
miR-24 Regulates Intrinsic Apoptosis Pathway in Mouse Cardiomyocytes
Wang, L., & Li, Q. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085389 · Cited by 35 · see citing works
Conservation and Evolution in and among SRF- and MEF2-Type MADS Domains and Their Binding Sites
Wu, W., Huang, X., Cheng, J., Li, Z., de Folter, S., Huang, Z., Jiang, X., Pang, H.-L., & Tao, S. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq214 · Cited by 35 · see citing works
Transcription factor binding sites are highly enriched within microRNA precursor sequences
Piriyapongsa, J., Jordan, I. K., Conley, A. B., Ronan, T., & Smalheiser, N. R. (2011) · Biology Direct · doi:10.1186/1745-6150-6-61 · Cited by 35 · see citing works
Correct Assembly of RNA Polymerase II Depends on the Foot Domain and Is Required for Multiple Steps of Transcription in Saccharomyces cerevisiae
Garrido-Godino, A. I., García-López, M. C., & Navarro, F. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.00262-13 · Cited by 34 · see citing works
β-MyHC and Cardiac Hypertrophy
Pandya, K., & Smithies, O. (2011) · Circulation Research · doi:10.1161/circresaha.111.252619 · Cited by 34 · see citing works
Regulatory conservation of protein coding and microRNA genes in vertebrates: lessons from the opossum genome
Mahony, S., Corcoran, D. L., Feingold, E., & Benos, P. V. (2007) · Genome biology · doi:10.1186/gb-2007-8-5-r84 · Cited by 31 · see citing works
Pitx2c Modulates Cardiac-Specific Transcription Factors Networks in Differentiating Cardiomyocytes from Murine Embryonic Stem Cells
Lozano-Velasco, E., Chinchilla, A., Martínez-Fernández, S., Hernández‐Torres, F., Navarro, F., Lyons, G. E., Franco, D., & Aránega, A. E. (2011) · Cells Tissues Organs · doi:10.1159/000323533 · Cited by 31 · see citing works
Self-citation
Reciprocal regulation of miR-23a and lysophosphatidic acid receptor signaling in cardiomyocyte hypertrophy
Yang, J., Nie, Y., Wang, F., Hou, J., Cong, X., Hu, S., & Chen, X. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2013.05.005 · Cited by 30 · see citing works
Role of micro RNA ‐27a in myoblast differentiation
Chen, X., Huang, Z., Chen, D., Yang, T., & Liu, G. (2013) · Cell Biology International · doi:10.1002/cbin.10192 · Cited by 28 · see citing works
Identification of novel microRNAs negatively regulating cardiac hypertrophy
Jeong, M. H., Lee, J., Kim, D. H., Park, W. J., & Yang, D. K. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.10.040 · Cited by 17 · see citing works
Brief report: SRF-dependent MiR-210 silences the sonic hedgehog signaling during cardiopoesis
Zheng, G., Tao, Y., Yu, W., & Schwartz, R. J. (2013) · Stem Cells · doi:10.1002/stem.1464 · Cited by 17 · see citing works
An Intragenic SRF-Dependent Regulatory Motif Directs Cardiac-Specific microRNA-1-1/133a-2 Expression
Li, Q., Guo, J., Lin, X., Yang, X., Ma, Y., Fan, G., & Chang, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075470 · Cited by 15 · see citing works
Synergistic up-regulation of muscle LIM protein expression in C2C12 and NIH3T3 cells by myogenin and MEF2C
Ji, Z.-X., Du, C., Wu, G., Li, S., An, G., Yang, Y., Jia, R., Jia, H., & Ni, J. (2008) · Molecular Genetics and Genomics · doi:10.1007/s00438-008-0393-7 · Cited by 13 · see citing works
Intron retention and transcript chimerism conserved across mammals: Ly6g5b and Csnk2b-Ly6g5b as examples
Hernández‐Torres, F., Rastrojo, A., & Aguado, B. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-199 · Cited by 10 · see citing works
Interplay between two myogenesis-related proteins: TBP-interacting protein 120B and MyoD
Suzuki, H., Suzuki, A., Maekawa, Y., Shiraishi, S., & Tamura, T. (2012) · Gene · doi:10.1016/j.gene.2012.05.022 · Cited by 6 · see citing works

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1 of the 73 references couldn’t be matched to a known paper.

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Xu, Q., Cui, Y., Luan, J. Y., Zhou, X., Li, H., & Han, J. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.02.144 · Cited by 109 · see citing works
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Reynolds, J. O., Quick, A. P., Wang, Q., Beavers, D. L., Philippen, L. E., Showell, J., Barreto‐Torres, G., Thuerauf, D. J., Doroudgar, S., Glembotski, C. C., et al. (2016) · International Journal of Cardiology · doi:10.1016/j.ijcard.2016.10.021 · Cited by 99 · see citing works
The HDAC3–SMARCA4–miR-27a axis promotes expression of the PAX3:FOXO1 fusion oncogene in rhabdomyosarcoma
Bharathy, N., Berlow, N., Wang, E., Abraham, J., Settelmeyer, T. P., Hooper, J. E., Svalina, M. N., Ishikawa, Y., Zientek, K. D., Bajwa, Z., et al. (2018) · Science Signaling · doi:10.1126/scisignal.aau7632 · Cited by 75 · see citing works
MicroRNAs in Skeletal Muscle and Hints on Their Potential Role in Muscle Wasting During Cancer Cachexia
Marceca, G. P., Nigita, G., Calore, F., & Croce, C. M. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.607196 · Cited by 44 · see citing works
Therapeutic Implications of miRNAs for Muscle-Wasting Conditions
Yedigaryan, L., & Sampaolesi, M. (2021) · Cells · doi:10.3390/cells10113035 · Cited by 43 · see citing works
MiR-23a transcriptional activated by Runx2 increases metastatic potential of mouse hepatoma cell via directly targeting Mgat3
Huang, H., Liu, Y., Yu, P., Qu, J., Guo, Y., Li, W., Wang, S., & Zhang, J. (2018) · Scientific Reports · doi:10.1038/s41598-018-25768-z · Cited by 34 · see citing works
Assessment and Distribution of Runs of Homozygosity in Horse Breeds Representing Different Utility Types
Szmatoła, T., Gurgul, A., Jasielczuk, I., Oclon, E., Ropka-Molik, K., Stefaniuk-Szmukier, M., Polak, G., Tomczyk-Wrona, I., & Bugno-Poniewierska, M. (2022) · Animals · doi:10.3390/ani12233293 · Cited by 33 · see citing works
MiR‐27 alleviates myocardial cell damage induced by hypoxia/reoxygenation via targeting TGFBR1 and inhibiting NF‐κB pathway
Zhang, X., An, B., & Zhang, G. (2019) · The Kaohsiung Journal of Medical Sciences · doi:10.1002/kjm2.12092 · Cited by 32 · see citing works
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Liu, X., Trakooljul, N., Hadlich, F., Muráni, E., Wimmers, K., & Ponsuksili, S. (2016) · BMC Genomics · doi:10.1186/s12864-016-2850-8 · Cited by 27 · see citing works
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Mukherjee, S., Shelar, B., & Krishna, S. (2022) · PubMed Central · Cited by 26 · see citing works
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Zahedi, F., Nazari-Jahantigh, M., Zhou, Z., Subramanian, P., Wei, Y., Grommes, J., Offermanns, S., Steffens, S., Weber, C., & Schober, A. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2349-0 · Cited by 25 · see citing works
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Zhang, X., Cai, S., Chen, L., Yuan, R., Nie, Y., Ding, S., Fang, Y., Zhu, Q., Chen, K., Wei, H., et al. (2019) · Journal of Animal Science · doi:10.1093/jas/skz091 · Cited by 24 · see citing works
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Yang, Y., Song, S., Meng, Q., Wang, L., Li, X., Xie, S., Chen, Y., Jiang, X., Wang, C., Lu, Y., et al. (2020) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.15030 · Cited by 24 · see citing works
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Sun, L., Liu, X., & Zuo, Z. (2021) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2021.10912 · Cited by 23 · see citing works
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Tang, Y., Wang, H., Wei, B., Guo, Y., Gu, L., Yang, Z., Zhang, Q., Wu, Y., Yuan, Q., Zhao, G., et al. (2015) · Scientific Reports · doi:10.1038/srep16083 · Cited by 21 · see citing works
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Lee, M., Wada, S., Oikawa, S., Suzuki, K., Ushida, T., & Akimoto, T. (2019) · Scientific Reports · doi:10.1038/s41598-018-37765-3 · Cited by 20 · see citing works
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Huang, X., LI, Z., BAI, B., Li, X., & Li, Z. (2015) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2015.2645 · Cited by 15 · see citing works
MicroRNA-27a participates in the pathological process of depression in rats by regulating VEGFA
Cui, J., Gong, C., Cao, B., & Li, L. (2018) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2018.5942 · Cited by 14 · see citing works
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Haybar, H., Shahrabi, S., Rezaeeyan, H., Shirzad, R., & Saki, N. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27639 · Cited by 14 · see citing works
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Pasławska, M., Grodzka, A., Peczyńska, J., Sawicka, B., & Bossowski, A. T. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25020956 · Cited by 10 · see citing works
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Pan, C., Chien, S., Chen, C.-J., Shih, C., HSIEH, M., Huang, C., Bi, W., Chan, C., Kao, Y., Hsiao, C., et al. (2021) · BMC Cardiovascular Disorders · doi:10.1186/s12872-021-01893-y · Cited by 10 · see citing works
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Chen, Y., Sun, F., Zhang, Y., Song, G., Qiao, W., Zhou, K., Ren, S., Zhao, Q., & Ren, W. (2020) · Annals of Translational Medicine · doi:10.21037/atm-20-2912 · Cited by 7 · see citing works
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Loss of miR-23a cluster in skeletal muscle can suppress bone remodeling
Zhang, H., Luan, J. Y., Cui, Y., & Han, J. (2021) · Intractable & Rare Diseases Research · doi:10.5582/irdr.2021.01054 · Cited by 6 · see citing works
Recent advances of miR-23 in human diseases and growth development
Qian, X., Jiang, Y., Yang, Y., Zhang, Y., Xu, N., Xu, B., Pei, K., Yu, Z., & Wu, W. (2025) · Non-coding RNA Research · doi:10.1016/j.ncrna.2024.12.010 · Cited by 5 · see citing works
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Khudayberdiev, S., Weiß, K., Heinze, A., Colombaretti, D., Trausch, N., Linne, U., & Rust, M. B. (2024) · Science Signaling · doi:10.1126/scisignal.adj0032 · Cited by 3 · see citing works
MEF2C Directly Interacts with Pre-miRNAs and Distinct RNPs to Post-Transcriptionally Regulate miR-23a-miR-27a-miR-24-2 microRNA Cluster Member Expression
Lozano-Velasco, E., García‐Padilla, C., Carmona-García, M., Gonzalez-Diaz, A., Arequipa-Rendon, A., Aránega, A. E., & Franco, D. (2024) · Non-Coding RNA · doi:10.3390/ncrna10030032 · Cited by 3 · see citing works
Self-citation
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Manenti, I., Viola, I., Canto, F., Accornero, P., Toschi, P., Versace, C., Macchi, E., Martignani, E., Abecia, J., & Miretti, S. (2025) · Journal of Animal Science · doi:10.1093/jas/skaf123 · Cited by 2 · see citing works
Supplement astaxanthin affects PPAR-γ/miR-27a axis and metabolic profile
Taghiyar, S., Aarabi, M. H., Pourrajab, F., Rad, N. R., & Sharifi-Rigi, A. (2023) · Gene Reports · doi:10.1016/j.genrep.2023.101838 · Cited by 2 · see citing works
Correlação Entre Micrornas Circulantes E Parâmetros Clínicos Na Cardiomiopatia Hipertrófica: Uma Revisão Sistemática E Meta-AnálisePreprint
de Oliveira, H. L., de Lima, K. B. A., dos Santos, C. C., Miranda, M. C. R., Barbosa, G. A., Silva, D. D. M. E., Scolari, F. L., & Menezes, A. (2025) · SSRN Electronic Journal · doi:10.2139/ssrn.5365245
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Ohara, M., Mikami, E., Inohana, W., Kurosawa, T., Nakame, A., Sakakibara, A., Ichinose, Y., Fujimoto, A., Nukui, A., Asano, A., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.07.674683
Circulating MicroRNAs and Clinical Parameters in Hypertrophic Cardiomyopathy: A Systematic Review and Correlation Meta-Analysis
Menezes, A. D. S., de Oliveira, H. L., & de Lima, K. B. A. (2026) · Frontiers in Bioscience-Scholar · doi:10.31083/fbs47633
Delphinidin induces the upregulation of miR-23a-3p expression in skeletal muscle and miR-23a-3p release from intestinal cells
Marugamea, Y., Murata, M., Migihashi, R., Goto, M., Morozumi, M., Kumazoe, M., Fujimura, Y., & Tachibana, H. (2026) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2026.154724

miR-23a functions downstream of NFATc3 to regulate cardiac hypertrophy
Lin, Z., Murtaza, I., Wang, K., Jiao, J., Gao, J., & Li, P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811371106 · Cited by 360 · see citing works
Cardiac Hypertrophy Is Positively Regulated by MicroRNA miR-23a
Wang, K., Lin, Z., Long, B., Li, J.-H., Zhou, J., & Li, P. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.266940 · Cited by 113 · see citing works
MEF2C Directly Interacts with Pre-miRNAs and Distinct RNPs to Post-Transcriptionally Regulate miR-23a-miR-27a-miR-24-2 microRNA Cluster Member Expression
Lozano-Velasco, E., García‐Padilla, C., Carmona-García, M., Gonzalez-Diaz, A., Arequipa-Rendon, A., Aránega, A. E., & Franco, D. (2024) · Non-Coding RNA · doi:10.3390/ncrna10030032 · Cited by 3 · see citing works
Self-citation
miR-27 and miR-125 Distinctly Regulate Muscle-Enriched Transcription Factors in Cardiac and Skeletal Myocytes
Lozano-Velasco, E., Galiano-Torres, J., Jódar-García, Á., Aránega, A. E., & Franco, D. (2015) · BioMed Research International · doi:10.1155/2015/391306 · Cited by 36 · see citing works
Self-citation
Overexpression of miR-223 Tips the Balance of Pro- and Anti-hypertrophic Signaling Cascades toward Physiologic Cardiac Hypertrophy
Yang, L., Li, Y., Wang, X., Mu, X., Qin, D., Huang, W. C., Alshahrani, S., Nieman, M. L., Peng, J., Essandoh, K., et al. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.715805 · Cited by 48 · see citing works

Authors: Hernandez-Torres, F., Aranega, A. E., & Franco, D.
Affiliations: Universidad de Jaén (ES)
Corresponding author: Franco, Diego
ORCID: Franco, Diego
Venue: Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms
Publisher: Elsevier BV
Published: 2014-09
Volume: 1839
Issue: 9
Pages: 885-897
ISSN: 1874-9399 (ISSN-L)
DOI: 10.1016/j.bbagrm.2014.07.009
OpenAlex: W1987534159
Cited by: 36
References: 73
Citations by year: 2026: 2 · 2025: 3 · 2024: 4 · 2023: 1 · 2022: 2 · 2021: 5 · 2020: 3 · 2019: 4 · 2018: 5 · 2017: 1 · 2016: 3 · 2015: 3
FWCI: 0.75
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms (publishedVersion)
PubMed (publishedVersion)
Funders: Junta de Andalucía Regional Council (CVI-6556)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords: miR-23a, miR-27a, miR-24-2, miRNA clusters, transcriptional regulation, SRF, serum response factor, proximal promoter, muscle hypertrophy, angiotensin II, norepinephrine, myocardium, skeletal muscle, hypertrophic cardiomyopathy, muscle atrophy, regulatory elements
MeSH terms: Angiotensin II, Animals, Gene Expression Regulation, Genes, Regulator, Cardiomegaly, Hypertrophy, Norepinephrine, Promoter Regions, Genetic, Transcription, Genetic, 3T3 Cells, Muscle, Skeletal, Myocytes, Cardiac, MicroRNAs, Mice

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Identification of regulatory elements directing miR-23a–miR-27a–miR-24-2 transcriptional regulation in response to muscle hypertrophic stimuli

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