MicroRNA-124 Regulates Cell Specification in the Cochlea through Modulation of Sfrp4/5

Cell Reports

Volumn 13, Issue 1, 2015, Pages 31-42

  Huyghe, Aurélia ^a   Van den Ackerveken, Priscilla ^a   Sacheli, Rosalie ^a   Prévot, Pierre Paul ^a   Thelen, Nicolas ^a   Renauld, Justine ^a   Thiry, Marc ^a   Delacroix, Laurence ^a   Nguyen, Laurent ^a   Malgrange, Brigitte ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; DICER; MICRORNA 124; SECRETED FRIZZLED RELATED PROTEIN 4; SECRETED FRIZZLED RELATED PROTEIN 5; WNT PROTEIN; 3' UNTRANSLATED REGION; CTNNB1 PROTEIN, MOUSE; DEAD BOX PROTEIN; DICER1 PROTEIN, MOUSE; MICRORNA; MIRN124 MICRORNA, MOUSE; ONCOPROTEIN; RIBONUCLEASE III; SFRP4 PROTEIN, MOUSE; SFRP5 PROTEIN, MOUSE; SIGNAL PEPTIDE; SMALL INTERFERING RNA; SOX2 PROTEIN, MOUSE; TRANSCRIPTION FACTOR SOX;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FATE; CELL POLARITY; CONTROLLED STUDY; CORTI ORGAN; DICER GENE; EPIGENETICS; FEMALE; GENE DELETION; GENE EXPRESSION; INNER EAR; INNER HAIR CELL; MICROARRAY ANALYSIS; MORPHOGENESIS; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN RNA BINDING; PROTEIN TARGETING; REGULATORY MECHANISM; 3' UNTRANSLATED REGION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL DIFFERENTIATION; COCHLEAR HAIR CELL; CYTOLOGY; DEFICIENCY; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; LABYRINTH SUPPORTING CELLS; MAMMALIAN EMBRYO; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; WNT SIGNALING PATHWAY;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; BETA CATENIN; CELL DIFFERENTIATION; CELL POLARITY; DEAD-BOX RNA HELICASES; EMBRYO, MAMMALIAN; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAIR CELLS, AUDITORY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LABYRINTH SUPPORTING CELLS; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; ORGANOGENESIS; PROTO-ONCOGENE PROTEINS; RIBONUCLEASE III; RNA, SMALL INTERFERING; SOXB1 TRANSCRIPTION FACTORS; WNT SIGNALING PATHWAY;

EID: 84943363267     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.08.054     Document Type: Article

References (53)

1. Arnold K., Sarkar A., Yram M.A., Polo J.M., Bronson R., Sengupta S., Seandel M., Geijsen N., Hochedlinger K. Sox2(+) adult stem and progenitor cells are important for tissue regeneration and survival of mice. Cell Stem Cell 2011, 9:317-329.
2. Aulicino F., Theka I., Ombrato L., Lluis F., Cosma M.P. Temporal perturbation of the Wnt signaling pathway in the control of cell reprogramming is modulated by TCF1. Stem Cell Reports 2014, 2:707-720.
3. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
4. Bermingham N.A., Hassan B.A., Price S.D., Vollrath M.A., Ben-Arie N., Eatock R.A., Bellen H.J., Lysakowski A., Zoghbi H.Y. Math1: an essential gene for the generation of inner ear hair cells. Science 1999, 284:1837-1841.
5. Bermingham-McDonogh O., Oesterle E.C., Stone J.S., Hume C.R., Huynh H.M., Hayashi T. Expression of Prox1 during mouse cochlear development. J. Comp. Neurol. 2006, 496:172-186.
6. Borovina A., Ciruna B. IFT88 plays a cilia- and PCP-independent role in controlling oriented cell divisions during vertebrate embryonic development. Cell Rep. 2013, 5:37-43.
7. Chai R., Xia A., Wang T., Jan T.A., Hayashi T., Bermingham-McDonogh O., Cheng A.G. Dynamic expression of Lgr5, a Wnt target gene, in the developing and mature mouse cochlea. J. Assoc. Res. Otolaryngol. 2011, 12:455-469.
8. Chamorro M.N., Schwartz D.R., Vonica A., Brivanlou A.H., Cho K.R., Varmus H.E. FGF-20 and DKK1 are transcriptional targets of beta-catenin and FGF-20 is implicated in cancer and development. EMBO J. 2005, 24:73-84.
9. Cheng L.C., Pastrana E., Tavazoie M., Doetsch F. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat. Neurosci. 2009, 12:399-408.
10. Cobb B.S., Nesterova T.B., Thompson E., Hertweck A., O'Connor E., Godwin J., Wilson C.B., Brockdorff N., Fisher A.G., Smale S.T., Merkenschlager M. T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J. Exp. Med. 2005, 201:1367-1373.
11. Curtin J.A., Quint E., Tsipouri V., Arkell R.M., Cattanach B., Copp A.J., Henderson D.J., Spurr N., Stanier P., Fisher E.M., et al. Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr. Biol. 2003, 13:1129-1133.
12. Dabdoub A., Donohue M.J., Brennan A., Wolf V., Montcouquiol M., Sassoon D.A., Hseih J.C., Rubin J.S., Salinas P.C., Kelley M.W. Wnt signaling mediates reorientation of outer hair cell stereociliary bundles in the mammalian cochlea. Development 2003, 130:2375-2384.
13. Dabdoub A., Puligilla C., Jones J.M., Fritzsch B., Cheah K.S., Pevny L.H., Kelley M.W. Sox2 signaling in prosensory domain specification and subsequent hair cell differentiation in the developing cochlea. Proc. Natl. Acad. Sci. USA 2008, 105:18396-18401.
14. Ezan J., Montcouquiol M. Revisiting planar cell polarity in the inner ear. Semin. Cell Dev. Biol. 2013, 24:499-506.
15. Freyer L., Morrow B.E. Canonical Wnt signaling modulates Tbx1, Eya1, and Six1 expression, restricting neurogenesis in the otic vesicle. Dev. Dyn. 2010, 239:1708-1722.
16. Friedman L.M., Dror A.A., Mor E., Tenne T., Toren G., Satoh T., Biesemeier D.J., Shomron N., Fekete D.M., Hornstein E., Avraham K.B. MicroRNAs are essential for development and function of inner ear hair cells in vertebrates. Proc. Natl. Acad. Sci. USA 2009, 106:7915-7920.
17. Groves A.K., Zhang K.D., Fekete D.M. The genetics of hair cell development and regeneration. Annu. Rev. Neurosci. 2013, 36:361-381.
18. Hayashi T., Ray C.A., Bermingham-McDonogh O. Fgf20 is required for sensory epithelial specification in the developing cochlea. J. Neurosci. 2008, 28:5991-5999.
19. Hébert J.M., McConnell S.K. Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev. Biol. 2000, 222:296-306.
20. Heydeck W., Zeng H., Liu A. Planar cell polarity effector gene Fuzzy regulates cilia formation and Hedgehog signal transduction in mouse. Dev. Dyn. 2009, 238:3035-3042.
21. Huh S.H., Jones J., Warchol M.E., Ornitz D.M. Differentiation of the lateral compartment of the cochlea requires a temporally restricted FGF20 signal. PLoS Biol. 2012, 10:e1001231.
22. Jacques B.E., Puligilla C., Weichert R.M., Ferrer-Vaquer A., Hadjantonakis A.K., Kelley M.W., Dabdoub A. A dual function for canonical Wnt/β-catenin signaling in the developing mammalian cochlea. Development 2012, 139:4395-4404.
23. Jansson L., Kim G.S., Cheng A.G. Making sense of Wnt signaling-linking hair cell regeneration to development. Front. Cell. Neurosci. 2015, 9:66.
24. Jones C., Roper V.C., Foucher I., Qian D., Banizs B., Petit C., Yoder B.K., Chen P. Ciliary proteins link basal body polarization to planar cell polarity regulation. Nat. Genet. 2008, 40:69-77.
25. Kersigo J., D'Angelo A., Gray B.D., Soukup G.A., Fritzsch B. The role of sensory organs and the forebrain for the development of the craniofacial shape as revealed by Foxg1-cre-mediated microRNA loss. Genesis 2011, 49:326-341.
26. 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., et al. miR-96 regulates the progression of differentiation in mammalian cochlear inner and outer hair cells. Proc. Natl. Acad. Sci. USA 2011, 108:2355-2360.
27. 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. An ENU-induced mutation of miR-96 associated with progressive hearing loss in mice. Nat. Genet. 2009, 41:614-618.
28. Li H., Fekete D.M. MicroRNAs in hair cell development and deafness. Curr. Opin. Otolaryngol. Head Neck Surg. 2010, 18:459-465.
29. Lim D.J., Anniko M. Developmental morphology of the mouse inner ear. A scanning electron microscopic observation. Acta Otolaryngol. Suppl. 1985, 422:1-69.
30. Löwenheim H., Furness D.N., Kil J., Zinn C., Gültig K., Fero M.L., Frost D., Gummer A.W., Roberts J.M., Rubel E.W., et al. Gene disruption of p27(Kip1) allows cell proliferation in the postnatal and adult organ of corti. Proc. Natl. Acad. Sci. USA 1999, 96:4084-4088.
31. Mak A.C., Szeto I.Y., Fritzsch B., Cheah K.S. Differential and overlapping expression pattern of SOX2 and SOX9 in inner ear development. Gene Expr. Patterns 2009, 9:444-453.
32. Makeyev E.V., Zhang J., Carrasco M.A., Maniatis T. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 2007, 27:435-448.
33. Meijer L., Flajolet M., Greengard P. Pharmacological inhibitors of glycogen synthase kinase 3. Trends Pharmacol. Sci. 2004, 25:471-480.
34. Mencía A., 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. Mutations in the seed region of human miR-96 are responsible for nonsyndromic progressive hearing loss. Nat. Genet. 2009, 41:609-613.
35. Montcouquiol M., Rachel R.A., Lanford P.J., Copeland N.G., Jenkins N.A., Kelley M.W. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 2003, 423:173-177.
36. Morrison A., Hodgetts C., Gossler A., Hrabé de Angelis M., Lewis J. Expression of Delta1 and Serrate1 (Jagged1) in the mouse inner ear. Mech. Dev. 1999, 84:169-172.
37. Moser J.J., Fritzler M.J., Rattner J.B. Repression of GW/P body components and the RNAi microprocessor impacts primary ciliogenesis in human astrocytes. BMC Cell Biol. 2011, 12:37.
38. Mueller K.L., Jacques B.E., Kelley M.W. Fibroblast growth factor signaling regulates pillar cell development in the organ of corti. J. Neurosci. 2002, 22:9368-9377.
39. Mulvaney J.F., Yatteau A., Sun W.W., Jacques B., Takubo K., Suda T., Yamada W., Dabdoub A. Secreted factor R-Spondin 2 is involved in refinement of patterning of the mammalian cochlea. Dev. Dyn. 2013, 242:179-188.
40. Qian D., Jones C., Rzadzinska A., Mark S., Zhang X., Steel K.P., Dai X., Chen P. Wnt5a functions in planar cell polarity regulation in mice. Dev. Biol. 2007, 306:121-133.
41. Ruben R.J. Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol. 1967, 220:220. 1-44.
42. Sacheli R., Nguyen L., Borgs L., Vandenbosch R., Bodson M., Lefebvre P., Malgrange B. Expression patterns of miR-96, miR-182 and miR-183 in the development inner ear. Gene Expr. Patterns 2009, 9:364-370.
43. Shi F., Kempfle J.S., Edge A.S. Wnt-responsive Lgr5-expressing stem cells are hair cell progenitors in the cochlea. J. Neurosci. 2012, 32:9639-9648.
44. Shi F., Hu L., Jacques B.E., Mulvaney J.F., Dabdoub A., Edge A.S. β-Catenin is required for hair-cell differentiation in the cochlea. J. Neurosci. 2014, 34:6470-6479.
45. Sinkkonen S.T., Chai R., Jan T.A., Hartman B.H., Laske R.D., Gahlen F., Sinkkonen W., Cheng A.G., Oshima K., Heller S. Intrinsic regenerative potential of murine cochlear supporting cells. Sci. Rep. 2011, 1:26.
46. Soukup G.A., Fritzsch B., Pierce M.L., Weston M.D., Jahan I., McManus M.T., Harfe B.D. Residual microRNA expression dictates the extent of inner ear development in conditional Dicer knockout mice. Dev. Biol. 2009, 328:328-341.
47. Tissir F., Qu Y., Montcouquiol M., Zhou L., Komatsu K., Shi D., Fujimori T., Labeau J., Tyteca D., Courtoy P., et al. Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nat. Neurosci. 2010, 13:700-707.
48. Volvert M.L., Prévot P.P., Close P., Laguesse S., Pirotte S., Hemphill J., Rogister F., Kruzy N., Sacheli R., Moonen G., et al. MicroRNA targeting of CoREST controls polarization of migrating cortical neurons. Cell Rep. 2014, 7:1168-1183.
49. Walentek P., Song R., He L. microRNAs and cilia. An ancient connection. Cell Cycle 2014, 13:2315-2316.
50. Wallingford J.B. Planar cell polarity and the developmental control of cell behavior in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 2012, 28:627-653.
51. Weston M.D., Pierce M.L., Rocha-Sanchez S., Beisel K.W., Soukup G.A. MicroRNA gene expression in the mouse inner ear. Brain Res. 2006, 1111:95-104.
52. Weston M.D., Pierce M.L., Jensen-Smith H.C., Fritzsch B., Rocha-Sanchez S., Beisel K.W., Soukup G.A. MicroRNA-183 family expression in hair cell development and requirement of microRNAs for hair cell maintenance and survival. Dev. Dyn. 2011, 240:808-819.
53. Zine A., Van De Water T.R., de Ribaupierre F. Notch signaling regulates the pattern of auditory hair cell differentiation in mammals. Development 2000, 127:3373-3383.