Atoh1 directs hair cell differentiation and survival in the late embryonic mouse inner ear

Developmental Biology

Volumn 381, Issue 2, 2013, Pages 401-410

  Chonko, Kurt T ^a   Jahan, Israt ^b   Stone, Jennifer ^c   Wright, Margaret C ^d   Fujiyama, Tomoyuki ^e   Hoshino, Mikio ^e   Fritzsch, Bernd ^b   Maricich, Stephen M ^f  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^f UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Cochlea; Development; Differentiation; Hearing; Vestibular system

Indexed keywords

ATOH1 PROTEIN; CELL MARKER; CELL PROTEIN; MYOSIN VIIA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BARHL1; TRANSCRIPTION FACTOR GFI1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ATOH1 GENE; CELL DEATH; CELL DIFFERENTIATION; CELL MATURATION; CELL SPECIFICITY; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE DELETION; GENE EXPRESSION; HAIR CELL; INNER EAR; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STEREOCILIUM; UTRICLE;

EID: 84882847293     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.06.022     Document Type: Article

References (47)

1. Ahmed M., Wong E.Y., Sun J., Xu J., Wang F., Xu P.X. Eya1-Six1 interaction is sufficient to induce hair cell fate in the cochlea by activating Atoh1 expression in cooperation with Sox2. Dev. Cell 2012, 22:377-390.
2. Barald K.F., Kelley M.W. From placode to polarization: new tunes in inner ear development. Development 2004, 131:4119-4130.
3. Basch M.L., Ohyama T., Segil N., Groves A.K. Canonical Notch signaling is not necessary for prosensory induction in the mouse cochlea: insights from a conditional mutant of RBPjkappa. J. Neurosci. 2011, 31:8046-8058.
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. Burns J.C., On D., Baker W., Collado M.S., Corwin J.T. Over half the hair cells in the mouse utricle first appear after birth, with significant numbers originating from early postnatal mitotic production in peripheral and striolar growth zones. J. Assoc. Res. Otolaryngol. 2012, 13:609-627.
6. Chellappa R., Li S., Pauley S., Jahan I., Jin K., Xiang M. Barhl1 regulatory sequences required for cell-specific gene expression and autoregulation in the inner ear and central nervous system. Mol. Cell Biol. 2008, 28:1905-1914.
7. Chen P., Johnson J.E., Zoghbi H.Y., Segil N. The role of Math1 in inner ear development: uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 2002, 129:2495-2505.
8. 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.
9. Du X., Jensen P., Goldowitz D., Hamre K.M. Wild-type cells rescue genotypically Math1-null hair cells in the inner ears of chimeric mice. Dev. Biol. 2007, 305:430-438.
10. Fritzsch B., Matei V.A., Nichols D.H., Bermingham N., Jones K., Beisel K.W., Wang V.Y. Atoh1 null mice show directed afferent fiber growth to undifferentiated ear sensory epithelia followed by incomplete fiber retention. Dev. Dyn. 2005, 233:570-583.
11. Fritzsch, B., Jahan, I., Pan, N., Kersigo, J., Duncan, J., Kopecky, B., 2011. Dissecting the molecular basis of organ of Corti development: where are we now? Hear. Res. 76, 2011, 16-26.
12. Fujiyama T., Yamada M., Terao M., Terashima T., Hioki H., Inoue Y.U., Inoue T., Masuyama N., Obata K., Yanagawa Y., Kawaguchi Y., Nabeshima Y., Hoshino M. Inhibitory and excitatory subtypes of cochlear nucleus neurons are defined by distinct bHLH transcription factors, Ptf1a and Atoh1. Development 2009, 136:2049-2058.
13. Groves A.K., Fekete D.M. Shaping sound in space: the regulation of inner ear patterning. Development 2012, 139:245-257.
14. Hertzano R., Montcouquiol M., Rashi-Elkeles S., Elkon R., Yucel R., Frankel W.N., Rechavi G., Moroy T., Friedman T.B., Kelley M.W., Avraham K.B. Transcription profiling of inner ears from Pou4f3(ddl/ddl) identifies Gfi1 as a target of the Pou4f3 deafness gene. Hum. Mol. Genet. 2004, 13:2143-2153.
15. Hertzano R., Dror A.A., Montcouquiol M., Ahmed Z.M., Ellsworth B., Camper S., Friedman T.B., Kelley M.W., Avraham K.B Lhx3, a LIM domain transcription factor, is regulated by Pou4f3 in the auditory but not in the vestibular system. Eur. J. Neurosci. 2007, 25:999-1005.
16. Jahan I., Pan N., Kersigo J., Fritzsch B. Neurod1 suppresses hair cell differentiation in ear ganglia and regulates hair cell subtype development in the cochlea. PLoS One 2010, 5:e11661.
17. Jahan I., Pan N., Kersigo J., Calisto L.E., Morris K.A., Kopecky B., Duncan J.S., Beisel K.W., Fritzsch B. Expression of neurog1 instead of atoh1 can partially rescue organ of corti cell survival. PLoS One 2012, 7:e30853.
18. Jahan I., Pan N., Kersigo J., Fritzsch B. Beyond generalized hair cells: molecular cues for hair cell types. Hear. Res. 2013, 297:30-41.
19. Kawamoto K., Ishimoto S., Minoda R., Brough D.E., Raphael Y. Math1 gene transfer generates new cochlear hair cells in mature guinea pigs in vivo. J. Neurosci. 2003, 23:4395-4400.
20. Kelley M.W. Regulation of cell fate in the sensory epithelia of the inner ear. Nature reviews. Neuroscience 2006, 7:837-849.
21. Kim W.Y., Fritzsch B., Serls A., Bakel L.A., Huang E.J., Reichardt L.F., Barth D.S., Lee J.E. NeuroD-null mice are deaf due to a severe loss of the inner ear sensory neurons during development. Development 2001, 128:417-426.
22. Kirjavainen A., Sulg M., Heyd F., Alitalo K., Yla-Herttuala S., Moroy T., Petrova T.V., Pirvola U. Prox1 interacts with Atoh1 and Gfi1, and regulates cellular differentiation in the inner ear sensory epithelia. Dev. Biol. 2008, 322:33-45.
23. Lagziel A., Ahmed Z.M., Schultz J.M., Morell R.J., Belyantseva I.A., Friedman T.B. Spatiotemporal pattern and isoforms of cadherin 23 in wild type and waltzer mice during inner ear hair cell development. Dev. Biol. 2005, 280:295-306.
24. Lanford P.J., Shailam R., Norton C.R., Gridley T., Kelley M.W. Expression of Math1 and HES5 in the cochleae of wildtype and Jag2 mutant mice. J. Assoc. Res. Otolaryngol. 2000, 1:161-171.
25. Li S., Price S.M., Cahill H., Ryugo D.K., Shen M.M., Xiang M. Hearing loss caused by progressive degeneration of cochlear hair cells in mice deficient for the Barhl1 homeobox gene. Development 2002, 129:3523-3532.
26. Lumpkin E.A., Collisson T., Parab P., Omer-Abdalla A., Haeberle H., Chen P., Doetzlhofer A., White P., Groves A., Segil N., Johnson J.E. Math1-driven GFP expression in the developing nervous system of transgenic mice. Gene Expression Patterns 2003, 3:389-395.
27. Masuda M., Dulon D., Pak K., Mullen L.M., Li Y., Erkman L., Ryan A.F. Regulation of POU4F3 gene expression in hair cells by 5' DNA in mice. Neuroscience 2011, 197:48-64.
28. Masuda M., Pak K., Chavez E., Ryan A.F. TFE2 and GATA3 enhance induction of POU4F3 and myosin VIIa positive cells in nonsensory cochlear epithelium by ATOH1. Dev. Biol. 2012, 372:68-80.
29. Matei V., Pauley S., Kaing S., Rowitch D., Beisel K.W., Morris K., Feng F., Jones K., Lee J., Fritzsch B. Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Dev. Dyn. 2005, 234:633-650.
30. Pan N., Jahan I., Kersigo J., Kopecky B., Santi P., Johnson S., Schmitz H., Fritzsch B. Conditional deletion of Atoh1 using Pax2-Cre results in viable mice without differentiated cochlear hair cells that have lost most of the organ of Corti. Hear. Res. 2011, 275:66-80.
31. Pan N., Jahan I., Kersigo J., Duncan J.S., Kopecky B., Fritzsch B. A novel atoh1 "self-terminating" mouse model reveals the necessity of proper atoh1 level and duration for hair cell differentiation and viability. PLoS One 2012, 7:e30358.
32. Pauley S., Kopecky B., Beisel K., Soukup G., Fritzsch B. Stem cells and molecular strategies to restore hearing. Panminerva Med. 2008, 50:41-53.
33. Qian D., Radde-Gallwitz K., Kelly M., Tyrberg B., Kim J., Gao W.Q., Chen P. Basic helix-loop-helix gene Hes6 delineates the sensory hair cell lineage in the inner ear. Dev. Dyn. 2006, 235:1689-1700.
34. Rubel E.W. Ontogeny of Structure and Function in the Vertebrate Auditory System 1978, Springer, New York.
35. Ruben R.J. Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol. 1967, (220):221-244.
36. Sans A., Chat M. Analysis of temporal and spatial patterns of rat vestibular hair cell differentiation by tritiated thymidine radioautography. J. Comp. Neurol. 1982, 206:1-8.
37. Scheffer D., Sage C., Corey D.P., Pingault V. Gene expression profiling identifies Hes6 as a transcriptional target of ATOH1 in cochlear hair cells. FEBS Lett. 2007, 581:4651-4656.
38. Shailam R., Lanford P.J., Dolinsky C.M., Norton C.R., Gridley T., Kelley M.W. Expression of proneural and neurogenic genes in the embryonic mammalian vestibular system. J. Neurocytol. 1999, 28:809-819.
39. Shroyer N.F., Wallis D., Venken K.J., Bellen H.J., Zoghbi H.Y. Gfi1 functions downstream of Math1 to control intestinal secretory cell subtype allocation and differentiation. Genes Dev. 2005, 19:2412-2417.
40. Shroyer N.F., Helmrath M.A., Wang V.Y., Antalffy B., Henning S.J., Zoghbi H.Y. Intestine-specific ablation of mouse atonal homolog 1 (Math1) reveals a role in cellular homeostasis. Gastroenterology 2007, 132:2478-2488.
41. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
42. 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.
43. Takumida M., Harada Y. Development of the utricular macula in the mouse. Arch. Oto-Rhino-Laryngology 1984, 241:9-15.
44. Wallis D., Hamblen M., Zhou Y., Venken K.J., Schumacher A., Grimes H.L., Zoghbi H.Y., Orkin S.H., Bellen H.J. The zinc finger transcription factor Gfi1, implicated in lymphomagenesis, is required for inner ear hair cell differentiation and survival. Development 2003, 130:221-232.
45. Woods C., Montcouquiol M., Kelley M.W. Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat. Neurosci. 2004, 7:1310-1318.
46. Xiang M., Gao W.Q., Hasson T., Shin J.J. Requirement for Brn-3c in maturation and survival, but not in fate determination of inner ear hair cells. Development 1998, 125:3935-3946.
47. Zheng J.L., Gao W.Q. Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat. Neurosci. 2000, 3:580-586.