miR-96 regulates the progression of differentiation in mammalian cochlear inner and outer hair cells
Open accessAbstract
MicroRNAs (miRNAs) are small noncoding RNAs able to regulate a broad range of protein-coding genes involved in many biological processes. miR-96 is a sensory organ-specific miRNA expressed in the mammalian cochlea during development. Mutations in miR-96 cause nonsyndromic progressive hearing loss in humans and mice. The mouse mutant diminuendo has a single base change in the seed region of the Mir96 gene leading to widespread changes in the expression of many genes. We have used this mutant to explore the role of miR-96 in the maturation of the auditory organ. We found that the physiological development of mutant sensory hair cells is arrested at around the day of birth, before their biophysical differentiation into inner and outer hair cells. Moreover, maturation of the hair cell stereocilia bundle and remodelling of auditory nerve connections within the cochlea fail to occur in miR-96 mutants. We conclude that miR-96 regulates the progression of the physiological and morphological differentiation of cochlear hair cells and, as such, coordinates one of the most distinctive functional refinements of the mammalian auditory system.
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Point mutations within the seed region of miR-96 cause autosomal dominant non-syndromic sensorineural hearing loss in two Spanish families and in a mouse model of NSHL.
“Recently, point mutations within the seed region of miR-96 were reported in two Spanish families with autosomal dominant non-syndromic sensorineural hearing loss (NSHL) and in a mouse model of NSHL.”
From A novel mutation within the MIR96 gene causes non-syndromic inherited hearing loss in an Italian family by altering pre-miRNA processing (2012) · cites this paper as [16]
Tight regulation of miR-96 levels within the vertebrate inner ear is crucial for the correct function and development of hair cells.
“Indeed, tight regulation of miR-96 levels within the vertebrate inner ear seems to be crucial for the correct function and development of hair cells, as demonstrated by knockdown experiments in zebrafish (11) and by the phenotypic differences between the heterozygous and the homozygous diminuendo mice (15,16).”
From A novel mutation within the MIR96 gene causes non-syndromic inherited hearing loss in an Italian family by altering pre-miRNA processing (2012) · cites this paper as [16]
Cites
Down-Regulation of Na+/K+ATPase Activity by Human Parvovirus B19 Capsid Protein VP1
Almilaji, A., Szteyn, K., Fein, E., Pakladok, T., Muñoz, C., Elvira, B., Towhid, S. T., Alesutan, I., Shumilina, E. V., Bock, C. –., et al. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350083 · Cited by 8,675 · see citing works
MicroRNAs: small RNAs with a big role in gene regulation
He, L., & Hannon, G. J. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1379 · Cited by 5,910 · see citing works
The versatility and universality of calcium signalling
Berridge, M. J., Lipp, P., & Bootman, M. D. (2000) · Nature Reviews Molecular Cell Biology · doi:10.1038/35036035 · Cited by 5,701 · see citing works
Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs
Lim, L. P., Lau, N. C., Garrett-Engele, P., Grimson, A., Schelter, J. M., Castle, J., Bartel, D. P., Linsley, P. S., & Johnson, J. M. (2005) · Nature · doi:10.1038/nature03315 · Cited by 4,755 · see citing works
Mammalian microRNAs predominantly act to decrease target mRNA levels
Guo, H., Ingolia, N. T., Weissman, J. S., & Bartel, D. P. (2010) · Nature · doi:10.1038/nature09267 · Cited by 3,886 · see citing works
Widespread changes in protein synthesis induced by microRNAs
Selbach, M., Schwanhäusser, B., Thierfelder, N., Fang, Z., Khanin, R., & Rajewsky, N. (2008) · Nature · doi:10.1038/nature07228 · Cited by 3,429 · cited 1× · see citing works
“Although they can repress hundreds of proteins, this repression appears to be relatively mild (42).”
BackgroundMicroRNA Expression in Zebrafish Embryonic Development
Wienholds, E., Kloosterman, W. P., Miska, E., Alvarez-Saavedra, E., Berezikov, E., de Bruijn, E., Horvitz, H. R., Kauppinen, S., & Plasterk, R. H. A. (2005) · Science · doi:10.1126/science.1114519 · Cited by 1,551 · see citing works
Dysregulation of Cardiogenesis, Cardiac Conduction, and Cell Cycle in Mice Lacking miRNA-1-2
Zhao, Y. B., Ransom, J. F., Li, A., Vedantham, V., von Drehle, M., Muth, A. N., Tsuchihashi, T., McManus, M. T., Schwartz, R. J., & Srivastava, D. (2007) · Cell · doi:10.1016/j.cell.2007.03.030 · Cited by 1,418 · see citing works
Small non-coding RNAs in animal development
Stefani, G., & Slack, F. J. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2347 · Cited by 1,361 · see citing works
Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier
Liberman, M. C., Gao, J., He, D. Z. Z., Wu, X., Jia, S., & Zuo, J. (2002) · Nature · doi:10.1038/nature01059 · Cited by 931 · see citing works
Kubisch, C., Schroeder, B. C., Friedrich, T., Lütjohann, B., El-Amraoui, A., Marlin, S., Petit, C., & Jentsch, T. J. (1999) · Cell · doi:10.1016/s0092-8674(00)80556-5 · Cited by 866 · see citing works
Mechanisms underlying spontaneous patterned activity in developing neural circuits
Blankenship, A. G., & Feller, M. B. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2759 · Cited by 851 · see citing works
Development of the inner ear of the mouse: a radioautographic study of terminal mitoses.
Ruben, R. J. (1967) · PubMed · Cited by 683 · see citing works
The origin of spontaneous activity in the developing auditory system
Tritsch, N. X., Yi, E., Gale, J. E., Glowatzki, E., & Bergles, D. E. (2007) · Nature · doi:10.1038/nature06233 · Cited by 569 · see citing works
Mencía, Á., Modamio-Høybjør, S., Redshaw, N., Morín, M., Mayo-Merino, F., Olavarrieta, L., Aguirre, L. A., del Castillo, I., Steel, K. P., Dalmay, T., et al. (2009) · Nature Genetics · doi:10.1038/ng.355 · Cited by 550 · see citing works
Self-citationXu, S., Witmer, P. D., Lumayag, S., Kovacs, B., & Valle, D. L. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m700501200 · Cited by 474 · see citing works
Schratt, G. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2763 · Cited by 455 · see citing works
CaV1.3 Channels Are Essential for Development and Presynaptic Activity of Cochlear Inner Hair Cells
Brandt, A., Striessnig, J., & Moser, T. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-34-10832.2003 · Cited by 415 · see citing works
Pietrzykowski, A. Z., Friesen, R. M., Martin, G. E., Puig, S. I., Nowak, C. L., Wynne, P. M., Siegelmann, H. T., & Treistman, S. N. (2008) · Neuron · doi:10.1016/j.neuron.2008.05.032 · Cited by 344 · see citing works
An instructive role for retinal waves in the development of retinogeniculate connectivity
Stellwagen, D., & Shatz, C. J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00577-9 · Cited by 342 · see citing works
The diverse roles of ribbon synapses in sensory neurotransmission
Matthews, G., & Fuchs, P. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2924 · Cited by 334 · see citing works
Physiology of Olivocochlear Efferents
Guinan, J. J. (1996) · Springer handbook of auditory research · doi:10.1007/978-1-4612-0757-3_8 · Cited by 323 · see citing works
An ENU-induced mutation of miR-96 associated with progressive hearing loss in mice
Lewis, M. A., Quint, E., Glazier, A. M., Fuchs, H., De Angelis, M. H., Langford, C., van Dongen, S., Abreu-Goodger, C., Piipari, M., Redshaw, N., et al. (2009) · Nature Genetics · doi:10.1038/ng.369 · Cited by 302 · see citing works
Self-citationUnderstanding microRNAs in neurodegeneration
Eacker, S. M., Dawson, T. M., & Dawson, V. L. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2726 · Cited by 275 · see citing works
WALLIS, D. E., Hamblen, M. J., Zhou, Y., Venken, K. J. T., Schumacher, A., Grimes, H. L., Zoghbi, H. Y., Orkin, S. H., & Bellen, H. J. (2002) · Development · doi:10.1242/dev.00190 · Cited by 263 · see citing works
Marcotti, W., Johnson, S. L., Holley, M. C., & Kros, C. J. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.034801 · Cited by 262 · see citing works
Self-citationMembers of the miRNA-200 Family Regulate Olfactory Neurogenesis
Choi, P. S., Zakhary, L., Choi, W.-Y., Caron, S. J. C., Alvarez-Saavedra, E., Miska, E. A., McManus, M. T., Harfe, B. D., Giráldez, A. J., Horvitz, H. R., et al. (2008) · Neuron · doi:10.1016/j.neuron.2007.11.018 · Cited by 245 · see citing works
Marcotti, W., & Kros, C. J. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.00653.x · Cited by 212 · see citing works
Self-citationRibbon synapses in the developing intact and cultured organ of Corti in the mouse
Sobkowicz, H. M., Rose, J., Scott, G., & Slapnick, S. M. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-07-00942.1982 · Cited by 212 · see citing works
Hearing Loss: Mechanisms Revealed by Genetics and Cell Biology
Dror, A. A., & Avraham, K. B. (2009) · Annual Review of Genetics · doi:10.1146/annurev-genet-102108-134135 · Cited by 210 · see citing works
MicroRNA gene expression in the mouse inner ear
Weston, M. D., Pierce, M. L., Rocha-Sanchez, S. M., Beisel, K. W., & Soukup, G. A. (2006) · Brain Research · doi:10.1016/j.brainres.2006.07.006 · Cited by 202 · see citing works
Johnson, S. L., Marcotti, W., & Kros, C. J. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.074740 · Cited by 193 · see citing works
Self-citationDevelopment of Sensory and Neural Structures in the Mammalian Cochlea
Pujol, R., Rebillard, M., & Lenoir, M. (1998) · Springer handbook of auditory research · doi:10.1007/978-1-4612-2186-9_4 · Cited by 180 · see citing works
MicroRNA‐183 family conservation and ciliated neurosensory organ expression
Pierce, M. L., Weston, M. D., Fritzsch, B., Gabel, H. W., Ruvkun, G., & Soukup, G. A. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2007.00217.x · Cited by 177 · see citing works
MicroRNAs are essential for development and function of inner ear hair cells in vertebrates
Friedman, L. M., Dror, A. A., Mor, E., Tenne, T., Toren-Haritan, G., Satoh, T., Biesemeier, D. J., Shomron, N., Fekete, D. M., Hornstein, E., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812446106 · Cited by 170 · see citing works
Goodyear, R. J., Legan, P. K., Wright, M. B., Marcotti, W., Oganesian, A., Coats, S. A., Booth, C. J., Kros, C. J., Seifert, R. A., Bowen‐Pope, D. F., et al. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-27-09208.2003 · Cited by 150 · see citing works
Self-citationRüsch, A., Ng, L., Goodyear, R. J., Oliver, D., Lisoukov, I., Vennström, B., Richardson, G. P., Kelley, M. W., & Forrest, D. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-24-09792.2001 · Cited by 143 · see citing works
MicroRNA-183 family members regulate sensorineural fates in the inner ear
Li, H., Kloosterman, W., & Fekete, D. M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4948-09.2010 · Cited by 140 · see citing works
Marcotti, W., Johnson, S. L., & Kros, C. J. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.072868 · Cited by 137 · see citing works
Self-citationSynaptotagmin IV determines the linear Ca2+ dependence of vesicle fusion at auditory ribbon synapses
Johnson, S. L., Franz, C., Kuhn, S. A. C., Furness, D. N., Rüttiger, L., Münkner, S., Rivolta, M. N., Seward, E. P., Herschman, H. R., Engel, J., et al. (2009) · Nature Neuroscience · doi:10.1038/nn.2456 · Cited by 128 · see citing works
Self-citationMarcotti, W., Erven, A., Johnson, S. L., Steel, K. P., & Kros, C. J. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2005.095661 · Cited by 122 · see citing works
Self-citationHeidrych, P., Zimmermann, U., Kuhn, S. A. C., Franz, C., Engel, J., Duncker, S. V., Hirt, B., Pusch, C. M., Ruth, P., Pfister, M., et al. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp213 · Cited by 115 · see citing works
Self-citationMarcotti, W., Johnson, S. L., & Kros, C. J. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2003.060137 · Cited by 98 · see citing works
Self-citationCalcium- and Otoferlin-Dependent Exocytosis by Immature Outer Hair Cells
Beurg, M., Safieddine, S., Roux, I., Bouleau, Y., Petit, C., & Dulon, D. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4653-07.2008 · Cited by 95 · see citing works
Expression patterns of miR-96, miR-182 and miR-183 in the developing inner ear
Sacheli, R., Nguyen, L., Borgs, L., Vandenbosch, R., Bodson, M., Lefebvre, P. P., & Malgrange, B. (2009) · Gene Expression Patterns · doi:10.1016/j.gep.2009.01.003 · Cited by 92 · see citing works
Hair cell fate decisions in cochlear development and regeneration
Cotanche, D. A., & Kaiser, C. L. (2010) · Hearing Research · doi:10.1016/j.heares.2010.04.012 · Cited by 91 · see citing works
Hair Cells – Beyond the Transducer
Housley, G. D., Marcotti, W., Navaratnam, D. S., & Yamoah, E. N. (2006) · The Journal of Membrane Biology · doi:10.1007/s00232-005-0835-7 · Cited by 86 · see citing works
Self-citationMarcotti, W., Géléoc, G. S. G., Lennan, G. W. T., & Kros, C. J. (1999) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004249900157 · Cited by 85 · see citing works
Self-citationGlowatzki, E., Grant, L. M., & Fuchs, P. A. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.09.006 · Cited by 82 · see citing works
Functional maturation of the exocytotic machinery at gerbil hair cell ribbon synapses
Johnson, S. L., Franz, C., Knipper, M., & Marcotti, W. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.168542 · Cited by 59 · see citing works
Self-citationJohnson, S. L., Adelman, J. P., & Marcotti, W. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.136630 · Cited by 55 · see citing works
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MicroRNAs in Stress Signaling and Human Disease
Mendell, J. T., & Olson, E. N. (2012) · Cell · doi:10.1016/j.cell.2012.02.005 · Cited by 1,673 · see citing works
The role of microRNAs in human diseases
Tüfekci, K. U., Öner, M. G., Meuwissen, R. L. J., & Genç, Ş. (2014) · Methods in molecular biology · doi:10.1007/978-1-62703-748-8_3 · Cited by 566 · see citing works
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Xiao, M.-F., Xu, D., Craig, M. T., Pelkey, K. A., Chien, C.-C., Shi, Y., Zhang, J., Resnick, S., Pletnikova, O., Salmon, D., et al. (2017) · eLife · doi:10.7554/elife.23798 · Cited by 316 · see citing works
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Ambros, V. (2011) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2011.04.003 · Cited by 314 · see citing works
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Wu, D. K., & Kelley, M. W. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008409 · Cited by 212 · see citing works
The microRNA-183 cluster: the family that plays together stays together
Dambal, S., Shah, M., Mihelich, B. L., & Nonn, L. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv703 · Cited by 213 · see citing works
Inactivation of the microRNA -183/96/182 cluster results in syndromic retinal degeneration
Lumayag, S., Haldin, C. E., Corbett, N. J., Wahlin, K. J., Cowan, C. E., Turturro, S. B., Larsen, P. E., Kovacs, B., Witmer, P. D., Valle, D. L., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1212655110 · Cited by 182 · see citing works
Position-dependent patterning of spontaneous action potentials in immature cochlear inner hair cells
Johnson, S. L., Eckrich, T., Kuhn, S. A. C., Zampini, V., Franz, C., Ranatunga, K. M., Roberts, T., Masetto, S., Knipper, M., Kros, C. J., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2803 · Cited by 165 · see citing works
Self-citationWang, L., Jia, X., Jiang, H.-J., Du, Y., Yang, F., Si, S., & Hong, B. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01580-12 · Cited by 161 · see citing works
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Groves, A. K., Zhang, K. D., & Fekete, D. M. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170309 · Cited by 100 · see citing works
Soldà, G., Robusto, M., Primignani, P., Castorina, P., Benzoni, E., Cesarani, A., Ambrosetti, U., Asselta, R., & Duga, S. (2012) · Human Molecular Genetics · doi:10.1093/hmg/ddr493 · Cited by 102 · see citing works
Gambari, R., Fabbri, E., Borgatti, M., Lampronti, I., Finotti, A., Brognara, E., Bianchi, N., Manicardi, A., Marchelli, R., & Corradini, R. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2011.08.007 · Cited by 101 · see citing works
Identifying MicroRNAs Involved in Degeneration of the Organ of Corti during Age-Related Hearing Loss
Zhang, Q. Y., Liu, H., McGee, J., Walsh, E. J., Soukup, G. A., & He, D. Z. Z. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062786 · Cited by 91 · see citing works
An Integrated Analysis of miRNA and mRNA Expressions in Non-Small Cell Lung Cancers
Ma, L., Huang, Y., Zhu, W., Zhou, S., Zhou, J., Fang, Z., Liu, X., Zhang, Y., & Yu, J. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026502 · Cited by 90 · see citing works
Nakano, Y., Jahan, I., Bonde, G., Sun, X., Hildebrand, M. S., Engelhardt, J. F., Smith, R. J., Cornell, R. A., Fritzsch, B., & Bánfi, B. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002966 · Cited by 89 · see citing works
Johnson, S. L., Kuhn, S. A. C., Franz, C., Ingham, N. J., Furness, D. N., Knipper, M., Steel, K. P., Adelman, J. P., Holley, M. C., & Marcotti, W. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219578110 · Cited by 80 · see citing works
Self-citationmiR-183/96 plays a pivotal regulatory role in mouse photoreceptor maturation and maintenance
Xiang, L., Chen, X., Wu, K., Zhang, C.-J., Zhou, G.-H., Lv, J., Sun, L., Cheng, F., Cai, X., & Jin, Z. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1618757114 · Cited by 78 · see citing works
Sensory hair cell death and regeneration in fishes
Monroe, J. D., Rajadinakaran, G., & Smith, M. E. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00131 · Cited by 74 · see citing works
Burns, J. C., & Corwin, J. T. (2013) · Hearing Research · doi:10.1016/j.heares.2013.01.005 · Cited by 61 · see citing works
Hereditary hearing loss: From human mutation to mechanism
Lenz, D. R., & Avraham, K. B. (2011) · Hearing Research · doi:10.1016/j.heares.2011.05.021 · Cited by 60 · see citing works
Zhou, L., Miller, C. L., Miraglia, L. J., Romero, A., Xu, S., Mure, L. S., Panda, S., & Kay, S. A. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2020454118 · Cited by 54 · see citing works
Functional assembly of mammalian cochlear hair cells
Marcotti, W. (2011) · Experimental Physiology · doi:10.1113/expphysiol.2011.059303 · Cited by 51 · see citing works
Self-citationDiverse Functions of MicroRNAs in Nervous System Development
Cochella, L., & Hobert, O. (2012) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-387038-4.00005-7 · Cited by 51 · see citing works
microRNAs: the art of silencing in the ear
Rudnicki, A., & Avraham, K. B. (2012) · EMBO Molecular Medicine · doi:10.1002/emmm.201100922 · Cited by 49 · see citing works
miR‐96 promotes osteogenic differentiation by suppressing HBEGF–EGFR signaling in osteoblastic cells
Mingfu, Y., Pan, Y., & Zhou, Y. (2014) · FEBS Letters · doi:10.1016/j.febslet.2014.11.008 · Cited by 48 · see citing works
Beyond generalized hair cells: Molecular cues for hair cell types
Jahan, I., Pan, N., Kersigo, J., & Fritzsch, B. (2012) · Hearing Research · doi:10.1016/j.heares.2012.11.008 · Cited by 46 · see citing works
MiR-182-5p protects inner ear hair cells from cisplatin-induced apoptosis by inhibiting FOXO3a
Li, Y., Li, A., Wu, J., He, Y., Yu, H., Chai, R., & Li, H. (2016) · Cell Death & Disease · doi:10.1038/cddis.2016.246 · Cited by 46 · see citing works
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Michalski, N., & Petit, C. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070918-050428 · Cited by 45 · see citing works
Rudnicki, A., Isakov, O., Ushakov, K., Shivatzki, S., Weiss, I., Friedman, L. M., Shomron, N., & Avraham, K. B. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-484 · Cited by 45 · see citing works
MicroRNAs: effective elements in ear-related diseases and hearing loss
Mahmoudian‐Sani, M., Ghahfarrokhi, A. M., Ahmadinejad, F., Chaleshtori, M. H., Saidijam, M., & Jami, M. (2017) · European Archives of Oto-Rhino-Laryngology · doi:10.1007/s00405-017-4470-6 · Cited by 45 · see citing works
Geng, R., Furness, D. N., Muraleedharan, C. K., Zhang, J., Dabdoub, A., Lin, V., & Xu, S. (2018) · Scientific Reports · doi:10.1038/s41598-018-36894-z · Cited by 45 · see citing works
Self-citationmiR-96-5p prevents hepatic stellate cell activation by inhibiting autophagy via ATG7
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Zhang, C.-J., Xiang, L., Chen, X., Wang, X.-Y., Wu, K., Zhang, B., Chen, D., Jin, G.-H., Zhang, H., Chen, Y., et al. (2020) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.61.3.12 · Cited by 36 · see citing works
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Jahan, I., Pan, N., Kersigo, J., & Fritzsch, B. (2015) · Development · doi:10.1242/dev.123091 · Cited by 35 · see citing works
MicroRNAs in Hearing Disorders: Their Regulation by Oxidative Stress, Inflammation and Antioxidants
Prasad, K. N., & Bondy, S. C. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00276 · Cited by 34 · see citing works
MicroRNA-183 Family in Inner Ear: Hair Cell Development and Deafness
Sani, M. R. M., Chaleshtori, M. H., Saidijam, M., Jami, M., & Ghasemi-Dehkordi, P. (2016) · Journal of Audiology & Otology · doi:10.7874/jao.2016.20.3.131 · Cited by 34 · see citing works
Zhu, W., Du, W., Rameshbabu, A. P., Armstrong, A. M., Silver, S., Kim, Y., Wei, W., Shu, Y., Liu, X., Lewis, M. A., et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.adn0689 · Cited by 33 · see citing works
Self-citationMicroRNAs in inner ear biology and pathogenesis
Patel, M. B., & Hu, B. (2012) · Hearing Research · doi:10.1016/j.heares.2012.03.008 · Cited by 31 · see citing works
Pathogenic variants in non‐protein‐coding sequences
Makrythanasis, P., & Antonarakis, S. E. (2013) · Clinical Genetics · doi:10.1111/cge.12272 · Cited by 30 · see citing works
Doetzlhofer, A., & Avraham, K. B. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.11.002 · Cited by 30 · see citing works
Kumar, V., Sethi, B., Staller, D. W., Xin, X., Ma, J., Dong, Y., Talmon, G. A., & Mahato, R. I. (2023) · Biomaterials · doi:10.1016/j.biomaterials.2023.122049 · Cited by 29 · see citing works
High throughput gene expression analysis of the inner ear
Hertzano, R. P., & Elkon, R. (2012) · Hearing Research · doi:10.1016/j.heares.2012.01.002 · Cited by 28 · see citing works
Lewis, M. A., Domenico, F. D., Ingham, N. J., Prosser, H. M., & Steel, K. P. (2020) · Disease Models & Mechanisms · doi:10.1242/dmm.047225 · Cited by 28 · see citing works
Self-citationOutcomes of Gene Panel Testing for Sensorineural Hearing Loss in a Diverse Patient Cohort
Liao, E. N., Taketa, E., Mohamad, N. I., & Chan, D. K. (2022) · JAMA Network Open · doi:10.1001/jamanetworkopen.2022.33441 · Cited by 28 · see citing works
MicroRNA-124 Regulates Cell Specification in the Cochlea through Modulation of Sfrp4/5
Huyghe, A., den Ackerveken, P. V., Sacheli, R., Prévôt, P.-P., Thelen, N., Renauld, J. M., Thiry, M., Delacroix, L., Nguyen, L., & Malgrange, B. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.08.054 · Cited by 27 · see citing works
Sensational MicroRNAs: Neurosensory Roles of the MicroRNA-183 Family
Banks, S. A., Pierce, M. L., & Soukup, G. A. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-01717-3 · Cited by 27 · see citing works
Lai, R., Cai, C., Wu, W., Hu, P., & Wang, Q. (2020) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.3089 · Cited by 26 · see citing works
MicroRNA-182 regulates otocyst-derived cell differentiation and targets T-box1 gene
Wang, X., Zhang, X., Du, J., & Jiang, H. (2012) · Hearing Research · doi:10.1016/j.heares.2012.02.005 · Cited by 26 · see citing works
Schimmang, T. (2012) · Hearing Research · doi:10.1016/j.heares.2012.11.001 · Cited by 26 · see citing works
Li, J., Liu, J., Zhang, Y., Wang, X., Li, W., Zhang, H., & Wang, H. (2016) · Aquatic Toxicology · doi:10.1016/j.aquatox.2016.07.009 · Cited by 26 · see citing works
Role of microRNAs in inner ear development and hearing loss
Mittal, R., Liu, C., Polineni, S. P., Bencie, N., Yan, D. L. S., & Liu, X. Z. (2018) · Gene · doi:10.1016/j.gene.2018.10.075 · Cited by 25 · see citing works
Chen, J., Johnson, S. L., Lewis, M. A., Hilton, J. M., Huma, A. C., Marcotti, W., & Steel, K. P. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12484 · Cited by 23 · see citing works
Self-citationRosengauer, E., Hartwich, H., Hartmann, A. M., Rudnicki, A., Satheesh, S. V., Avraham, K. B., & Nothwang, H. G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049503 · Cited by 23 · see citing works
MicroRNA-96 Promotes Schistosomiasis Hepatic Fibrosis in Mice by Suppressing Smad7
Luo, X., Zhang, D., Xie, J., Su, Q., He, X., Bai, R., Gao, G., & Pan, W. (2018) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2018.10.002 · Cited by 22 · see citing works
Identification and expression profiling of microRNAs in Hymenolepis
Macchiaroli, N., Cucher, M. A., Kamenetzky, L., Yones, C., Bugnon, L. A., Berriman, M., Olson, P. D., & Rosenzvit, M. C. (2019) · International Journal for Parasitology · doi:10.1016/j.ijpara.2018.07.005 · Cited by 20 · see citing works
Seitz, H. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae694 · Cited by 19 · see citing works
Exploring regulatory networks of miR-96 in the developing inner ear
Lewis, M. A., Buniello, A., Hilton, J. M., Zhu, F., Zhang, W. I., Evans, S. K., van Dongen, S., Enright, A. J., & Steel, K. P. (2016) · Scientific Reports · doi:10.1038/srep23363 · Cited by 18 · see citing works
Self-citationWeston, M. D., Tarang, S., Pierce, M. L., Pyakurel, U., Rocha-Sanchez, S. M., McGee, J., Walsh, E. J., & Soukup, G. A. (2018) · Scientific Reports · doi:10.1038/s41598-018-21811-1 · Cited by 18 · see citing works
Carlton, A. J., Jeng, J., Grandi, F. C., Faveri, F. D., Ceriani, F., Tomasi, L. D., Underhill, A., Johnson, S. L., Legan, P. K., Kros, C. J., et al. (2023) · The EMBO Journal · doi:10.15252/embj.2022112118 · Cited by 16 · see citing works
Self-citationThe long and short: Non-coding RNAs in the mammalian inner ear
Koffler-Brill, T., Noy, Y., & Avraham, K. B. (2022) · Hearing Research · doi:10.1016/j.heares.2022.108666 · Cited by 16 · see citing works
Cai, T., Long, J., Wang, H., Liu, W., & Zhang, Y. (2017) · Oncology Reports · doi:10.3892/or.2017.5754 · Cited by 16 · see citing works
Ebeid, M., Sripal, P., Pecka, J. L., Beisel, K. W., Kwan, K. Y., & Soukup, G. A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0180855 · Cited by 15 · see citing works
Functional Development of Hair Cells in the Mammalian Inner Ear
Corns, L. F., Bardhan, T., Houston, O., Olt, J., Holley, M. C., Masetto, S., Johnson, S. L., & Marcotti, W. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-408088-1.00006-3 · Cited by 14 · see citing works
Self-citationKrohs, C., Körber, C., Ebbers, L., Altaf, F., Hollje, G., Hoppe, S., Dörflinger, Y., Prosser, H. M., & Nothwang, H. G. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0139-20.2021 · Cited by 15 · see citing works
The miR-183/ItgA3 axis is a key regulator of prosensory area during early inner ear development
den Ackerveken, P. V., Mounier, A., Huyghe, A., Sacheli, R., Vanlerberghe, P.-B., Volvert, M.-L., Delacroix, L., Nguyen, L., & Malgrange, B. (2017) · Cell Death and Differentiation · doi:10.1038/cdd.2017.127 · Cited by 13 · see citing works
Ingham, N. J. (2019) · BIO-PROTOCOL · doi:10.21769/bioprotoc.3447 · Cited by 12 · see citing works
Self-citationPitpnm1 is expressed in hair cells during development but is not required for hearing
Carlisle, F. A., Pearson, S. A., Steel, K. P., & Lewis, M. A. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.06.045 · Cited by 12 · see citing works
Self-citationLi, W., Zhang, Y., Xu, J., Chen, J., & Gao, X. (2021) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2021.10965 · Cited by 11 · see citing works
Self-citationLight-regulated microRNAs shape dynamic gene expression in the zebrafish circadian clock
Wang, Z., Wang, S., Bi, Y., Boiti, A., Zhang, S., Vallone, D., Lan, X., Foulkes, N. S., & Zhao, H. (2025) · PLoS Genetics · doi:10.1371/journal.pgen.1011545 · Cited by 11 · see citing works
Expression and Misexpression of the miR-183 Family in the Developing Hearing Organ of the Chicken
Zhang, K. D., Stoller, M. L., & Fekete, D. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132796 · Cited by 11 · see citing works
Kuhn, S. A. C., Ingham, N. J., Pearson, S. A., Gribble, S. M., Clayton, S., Steel, K. P., & Marcotti, W. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031433 · Cited by 11 · see citing works
Self-citationmiRNA Long-Term Response to Early Metabolic Environmental Challenge in Hypothalamic Arcuate Nucleus
Benoit, C., Doubi-Kadmiri, S., Benigni, X., Crépin, D., Riffault, L., Poizat, G., Vacher, C., Taouis, M., Baroin‐Tourancheau, A., & Amar, L. S. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00090 · Cited by 11 · see citing works
Li, J., Ling, Y., Huang, W., Sun, L., Li, Y., Wang, C., Zhang, Y., Wang, X., Dahlgren, R. A., & Wang, H. (2018) · Chemosphere · doi:10.1016/j.chemosphere.2018.09.118 · Cited by 11 · see citing works
Dallol, A., Daghistani, K. J., Elaimi, A., Alwazani, W. A., Bamanie, A., Safiah, M., Sagaty, S., Taha, L., Zahed, R., Bajouh, O. S., et al. (2016) · BMC Medical Genetics · doi:10.1186/s12881-016-0329-8 · Cited by 10 · see citing works
Gupta, N., Somayajulu, M., Gurdziel, K., LoGrasso, G., Aziz, H., Rosati, R., McClellan, S. A., Pitchaikannu, A., Santra, M., Shukkur, M. F. A., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-58403-1 · Cited by 8 · see citing works
Sani, M. R. M., & Ghahfarrokhi, A. M. (2017) · Journal of Otology · doi:10.1016/j.joto.2017.03.003 · Cited by 8 · see citing works
Mutation Screening in the miR-183/96/182 Cluster in Patients With Inherited Retinal Dystrophy
Xu, S., Coku, A., Muraleedharan, C. K., Harajli, A., Mishulin, E., Dahabra, C., Choi, J. J., Garcia, W. J., Webb-Jones, K., Birch, D. G., et al. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.619641 · Cited by 8 · see citing works
Two new mouse alleles of Ocm and Slc26a5
Lachgar-Ruiz, M., Ingham, N. J., Martelletti, E., Chen, J., James, E., Panganiban, C. H., Lewis, M. A., & Steel, K. P. (2024) · Hearing Research · doi:10.1016/j.heares.2024.109109 · Cited by 7 · see citing works
Self-citationGenotype Characterization and MiRNA Expression Profiling in Usher Syndrome Cell Lines
Tom, W. A., Chandel, D. S., Jiang, C. Q., Krzyzanowski, G. D., Fernando, N., Olou, A. A., & Fernando, M. R. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25189993 · Cited by 7 · see citing works
Bicistronic Gene Transfer Tools for Delivery of miRNAs and Protein Coding Sequences
Stoller, M. L., Chang, H. C., & Fekete, D. M. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms140918239 · Cited by 7 · see citing works
MicroRNA Maintenance of Cone Outer Segments
Moore, K. B., & Vetter, M. L. (2014) · Neuron · doi:10.1016/j.neuron.2014.07.031 · Cited by 6 · see citing works
NcRNA: key and potential in hearing loss
Zhu, K., Wang, T., Li, S., Liu, Z., Zhan, Y., & Zhang, Q. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1333131 · Cited by 6 · see citing works
Xia, R., Jin, C., Fei, S., Dong, T., Wen, T., Zhu, F., Shi, Y., Zhou, Q., Yong, T., & Peng, C. (2025) · iScience · doi:10.1016/j.isci.2025.112355 · Cited by 4 · see citing works
Mechanisms driving the functional maturation of the developing mammalian auditory pathway
Ceriani, F., Wood, K. C., Johnson, S. L., Kros, C. J., & Marcotti, W. (2025) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2025.03.005 · Cited by 4 · see citing works
Self-citationHuang, G., & Eckrich, S. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.643517 · Cited by 4 · see citing works
Ernsberger, U. (2014) · Cell and Tissue Research · doi:10.1007/s00441-014-2049-8 · Cited by 4 · see citing works
eRNAkit: Expanding the Functional Atlas of human Enhancer RNAs Beyond the NucleusPreprint
Benova, N., Kuklinkova, R., Eldahshoury, M. K., & Anene, C. A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.25.650683 · Cited by 4 · see citing works
MicroRNAs as potential biomarkers for monitoring of acquired sensorineural hearing loss
Hu, Y., Chen, H., Zhou, X., Luo, X., Tu, Z., Ke, J., & Yuan, W. (2024) · Pediatric Discovery · doi:10.1002/pdi3.51 · Cited by 3 · see citing works
Zeng, T., Liu, L., Lv, J., Xie, H., Shi, Q., Tao, G., Zheng, X., Zhu, L., Xiong, L., & Xie, H. (2025) · Biomolecules · doi:10.3390/biom15101434 · Cited by 3 · see citing works
Lewis, M. A., Lachgar-Ruiz, M., Domenico, F. D., Duddy, G., Chen, J., Fernández, S., Morin, M., Williams, G. H., Moreno-Pelayo, M. Á., & Steel, K. P. (2024) · Genome Medicine · doi:10.1186/s13073-024-01394-5 · Cited by 3 · see citing works
Self-citationNew Insight Into the Neuroimmune Interplay In Pseudomonas aeruginosa Keratitis
Gupta, N., LoGrasso, G., Hazlett, L. D., & Xu, S. (2025) · The Ocular Surface · doi:10.1016/j.jtos.2025.07.008 · Cited by 2 · see citing works
Xie, Y., Ding, N., Sun, J., Jin, X., Zhang, X., Sun, J., Xu, H., Bing, H., Guan, L., Li, Y., et al. (2025) · Journal of Functional Foods · doi:10.1016/j.jff.2025.107060 · Cited by 2 · see citing works
A cell type–specific approach to elucidate the role of miR-96 in inner ear hair cells
Gwilliam, K., Sperber, M., Perry, K., Rose, K. P., Ginsberg, L., Paladugu, N., Song, Y., Milon, B. C., Elkon, R., & Hertzano, R. P. (2024) · Frontiers in Audiology and Otology · doi:10.3389/fauot.2024.1400576 · Cited by 2 · see citing works
- Authors
- Kuhn, S., Johnson, S. L., Furness, D. N., Chen, J., Ingham, N., Hilton, J. M., Steffes, G., Lewis, M. A., Zampini, V., Hackney, C. M., Masetto, S., Holley, M. C., Steel, K. P., & Marcotti, W.
- Affiliations
- University of Sheffield (GB)
- Keele University (GB)
- Wellcome Sanger Institute (GB)
- University of Pavia (IT)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2011-01-18
- Volume
- 108
- Issue
- 6
- Pages
- 2355-2360
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3038748
- OpenAlex
- W2027444951
- Cited by
- 114
- References
- 51
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 10 · 2023: 3 · 2022: 4 · 2021: 3 · 2020: 7 · 2019: 4 · 2018: 8 · 2017: 9 · 2016: 7 · 2015: 6 · 2014: 6 · 2013: 14 · 2012: 15
- FWCI
- 7.24
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Research Portal (King's College London) (submittedVersion)
- Funders
- Wellcome Trust (077189, 088719)
- Deafness Research UK
- Henry Smith Charity
- University of Sheffield
- Medical Research Council (MC_qA137918)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
- Health Sciences › Medicine › Genetics › Congenital Ear and Nasal Anomalies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Hearing Loss and Rehabilitation
- Keywords
- miR-96, microRNA, cochlear hair cells, inner hair cells, outer hair cells, hair cell differentiation, progressive hearing loss
- MeSH terms
- Animals, Cell Differentiation, Hair Cells, Auditory, Inner, Mice, Mutant Strains, Mutation, Organ Specificity, Hair Cells, Auditory, Outer, MicroRNAs, Mice
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