Atoh1-lineal neurons are required for hearing and for the survival of neurons in the spiral ganglion and brainstem accessory auditory nuclei

Journal of Neuroscience

Volumn 29, Issue 36, 2009, Pages 11123-11133

  Maricich, Stephen M ^a   Xia, Anping ^b   Mathes, Erin L ^a   Wang, Vincent Y ^c   Oghalai, John S ^e   Fritzsch, Bernd ^f   Zoghbi, Huda Y ^d,e  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATOH1 PROTIEN; CRE RECOMBINASE; EARLY GROWTH RESPONSE FACTOR 2; HELIX LOOP HELIX PROTEIN; HOMEODOMAIN PROTEIN; UNCLASSIFIED DRUG;

ACOUSTIC NERVE FIBER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CELL STRUCTURE; CELL SURVIVAL; COCHLEA; COCHLEAR NUCLEUS; CONTROLLED STUDY; DISEASE MODEL; EMBRYO; EVOKED BRAIN STEM AUDITORY RESPONSE; GENE DELETION; HEARING; HEARING IMPAIRMENT; KNOCKOUT MOUSE; LOXP SITE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SPIRAL GANGLION;

ACOUSTIC STIMULATION; ANIMALS; ANIMALS, NEWBORN; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN STEM; CELL SURVIVAL; COCHLEAR NUCLEUS; FEMALE; HEARING; MICE; MICE, CONGENIC; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONS; PREGNANCY; SPIRAL GANGLION;

EID: 70349089328     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2232-09.2009     Document Type: Article

References (55)

1. Agrawal Y, Platz EA, Niparko JK (2008) Prevalence of hearing loss and differences by demographic characteristics among US adults: data from the National Health and Nutrition Examination Survey, 1999-2004. Arch Intern Med 168:1522-1530.
2. Akazawa C, Ishibashi M, Shimizu C, Nakanishi S, Kageyama R (1995) A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J Biol Chem 270:8730-8738.
3. Arenkiel BR, Gaufo GO, Capecchi MR (2003) Hoxb1 neural crest preferentially form glia of the PNS. Dev Dyn 227:379-386.
4. Ben-Arie N, McCall AE, Berkman S, Eichele G, Bellen HJ, Zoghbi HY (1996) Evolutionary conservation of sequence and expression of the bHLH protein Atonal suggests a conserved role in neurogenesis. Hum Mol Genet 5:1207-1216. (Pubitemid 26335837)
5. Bermingham NA, Hassan BA, Price SD, Vollrath MA, Ben-Arie N, Eatock RA, Bellen HJ, Lysakowski A, Zoghbi HY (1999) Math1: an essential gene for the generation of inner ear hair cells. Science 284:1837-1841. (Pubitemid 29275624)
6. Butowt R, von Bartheld CS (2005) Anterograde axonal transport of BDNF and NT-3 by retinal ganglion cells: roles of neurotrophin receptors. Mol Cell Neurosci 29:11-25. (Pubitemid 40603878)
7. Cambronero F, Puelles L (2000) Rostrocaudal nuclear relationships in the avian medulla oblongata: a fate map with quail chick chimeras. J Comp Neurol 427:522-545. (Pubitemid 30818924)
8. Carson JP, Thaller C, Eichele G (2002) A transcriptome atlas of the mouse brain at cellular resolution. Curr Opin Neurobiol 12:562-565. (Pubitemid 35284092)
9. Carson JP, Eichele G, Chiu W (2005) A method for automated detection of gene expression required for the establishment of a digital transcriptome-wide gene expression atlas. J Microsc 217:275-281. (Pubitemid 40333328)
10. Cramer KS, Fraser SE, Rubel EW (2000) Embryonic origins of auditory brain-stem nuclei in the chick hindbrain. Dev Biol 224:138-151.
11. Ernfors P, Van De Water T, Loring J, Jaenisch R (1995) Complementary roles of BDNF and NT-3 in vestibular and auditory development. Neuron 14:1153-1164.
12. Farago AF, Awatramani RB, Dymecki SM (2006) Assembly of the brainstem cochlear nuclear complex is revealed by intersectional and subtractive genetic fate maps. Neuron 50:205-218.
13. Friauf E, Lohmann C (1999) Development of auditory brainstem circuitry. Activity-dependent and activity-independent processes. Cell Tissue Res 297:187-195.
14. Fritzsch B, Barbacid M, Silos-Santiago I (1998) The combined effects of trkB and trkC mutations on the innervation of the inner ear. Int J Dev Neurosci 16:493-505. (Pubitemid 28555717)
15. Fritzsch B, Muirhead KA, Feng F, Gray BD, Ohlsson-Wilhelm BM (2005) Diffusion and imaging properties of three new lipophilic tracers, NeuroVue Maroon, NeuroVue Red and NeuroVue Green and their use for double and triple labeling of neuronal profile. Brain Res Bull 66:249-258. (Pubitemid 40981026)
16. Griffiths TD (2002) Central auditory pathologies. Br Med Bull 63:107-120.
17. Hafidi A, Moore T, Sanes DH (1996) Regional distribution of neurotrophin receptors in the developing auditory brainstem. J Comp Neurol 367:454-464. (Pubitemid 26107131)
18. Hanson MG, Landmesser LT (2004) Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron 43:687-701.
19. Harrison JM, Irving R (1966) Ascending connections of the anterior ventral cochlear nucleus in the rat. J Comp Neurol 126:51-63.
20. Hendry IA (1976) A method to correct adequately for the change in neuronal size when estimating neuronal numbers after nerve growth factor treatment. J Neurocytol 5:337-349.
21. Ino H (2004) Immunohistochemical characterization of the orphan nuclear receptor ROR alpha in the mouse nervous system. J Histochem Cytochem 52:311-323.
22. Jarman AP, Grau Y, Jan LY, Jan YN (1993) atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73:1307-1321.
23. Jones KR, Fariñas I, Backus C, Reichardt LF (1994) Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76:989-999. (Pubitemid 24106380)
24. Jones TA, Jones SM, Paggett KC (2001) Primordial rhythmic bursting in embryonic cochlear ganglion cells. J Neurosci 21:8129-8135.
25. Leake PA, Snyder RL, Merzenich MM (1992) Topographic organization of the cochlear spiral ganglion demonstrated by restricted lesions of the anteroventral cochlear nucleus. J Comp Neurol 320:468-478.
26. Lippe WR (1994) Rhythmic spontaneous activity in the developing avian auditory system. J Neurosci 14:1486-1495.
27. Lurie DI, Pasic TR, Hockfield SJ, Rubel EW (1997) Development of Cat-301 immunoreactivity in auditory brainstem nuclei of the gerbil. J Comp Neurol 380:319-334. (Pubitemid 27161324)
28. Machold R, Fishell G (2005) Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48:17-24.
29. Marín F, Puelles L (1995) Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur J Neurosci 7:1714-1738.
30. Matei V, Pauley S, Kaing S, Rowitch D, Beisel KW, Morris K, Feng F, Jones K, Lee J, Fritzsch B (2005) Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Dev Dyn 234:633-650. (Pubitemid 41532984)
31. Moore DR (1990) Auditory brainstem of the ferret: early cessation of developmental sensitivity of neurons in the cochlear nucleus to removal of the cochlea. J Comp Neurol 302:810-823.
32. Moore DR (1992) Trophic influences of excitatory and inhibitory synapses on neurones in the auditory brain stem. Neuroreport 3:269-272.
33. Pasic TR, Moore DR, Rubel EW (1994) Effect of altered neuronal activity on cell size in the medial nucleus of the trapezoid body and ventral cochlear nucleus of the gerbil. J Comp Neurol 348:111-120.
34. Pirvola U, Hallböök F, Xing-Qun L, Virkkala J, Saarma M, Ylikoski J (1997) Expression of neurotrophins and Trk receptors in the developing, adult, and regenerating avian cochlea. J Neurobiol 33:1019-1033. (Pubitemid 27513689)
35. Postigo A, Calella AM, Fritzsch B, Knipper M, Katz D, Eilers A, Schimmang T, Lewin GR, Klein R, Minichiello L (2002) Distinct requirements for TrkB and TrkC signaling in target innervation by sensory neurons. Genes Dev 16:633-645. (Pubitemid 34212495)
36. Powell TP, Erulkar SD (1962) Transneuronal cell degeneration in the auditory relay nuclei of the cat. J Anat 96:249-268.
37. Rubel EW, Fritzsch B (2002) Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci 25:51-101.
38. Schecterson LC, Bothwell M (1994) Neurotrophin and neurotrophin receptor mRNA expression in developing inner ear. Hear Res 73:92-100. (Pubitemid 24061122)
39. Sekiya T, Yagihashi A, Shimamura N, Asano K, Suzuki S, Matsubara A, Namba A, Shinkawa H (2003) Apoptosis of auditory neurons following central process injury. Exp Neurol 184:648-658. (Pubitemid 38182794)
40. Shroyer NF, Helmrath MA, Wang VY, Antalffy B, Henning SJ, Zoghbi HY (2007) Intestine-specific ablation of mouse atonal homolog 1 (Math1) reveals a role in cellular homeostasis. Gastroenterology 132:2478-2488. (Pubitemid 46890862)
41. Silos-Santiago I, Fagan AM, Garber M, Fritzsch B, Barbacid M (1997) Severe sensory deficits but normal CNS development in newborn mice lacking TrkB and TrkC tyrosine protein kinase receptors. Eur J Neurosci 9:2045-2056. (Pubitemid 27485237)
42. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70-71.
43. Spoendlin H (1971) Degeneration behaviour of the cochlear nerve. Arch Klin Exp Ohren Nasen Kehlkopfheilkd 200:275-291.
44. Trune DR (1982) Influence of neonatal cochlear removal on the development of mouse cochlear nucleus. I. Number, size, and density of its neurons. J Comp Neurol 209:409-424. (Pubitemid 12015149)
45. Visel A, Thaller C, Eichele G (2004) GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res 32:D552-D556. (Pubitemid 38081719)
46. Voiculescu O, Charnay P, Schneider-Maunoury S (2000) Expression pattern of a Krox-20/Cre knock-in allele in the developing hindbrain, bones, and peripheral nervous system. Genesis 26:123-126. (Pubitemid 30158095)
47. von Bartheld CS, Fritzsch B (2006) Comparative analysis of neurotrophin receptors and ligands in vertebrate neurons: tools for evolutionary stability or changes in neural circuits? Brain Behav Evol 68:157-172.
48. von Bartheld CS, Byers MR, Williams R, Bothwell M (1996) Anterograde transport of neurotrophins and axodendritic transfer in the developing visual system. Nature 379:830-833. (Pubitemid 26067725)
49. Wang VY, Rose MF, Zoghbi HY (2005) Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48:31-43.
50. Wang X, Butowt R, Vasko MR, von Bartheld CS (2002) Mechanisms of the release of anterogradely transported neurotrophin-3 from axon terminals. J Neurosci 22:931-945. (Pubitemid 34141773)
51. Willott J, ed (2001) Handbook of mouse auditory research: from behavior to molecular biology. Boca Raton, FL: CRC.
52. Xia A, Visosky AM, Cho JH, Tsai MJ, Pereira FA, Oghalai JS (2007) Altered traveling wave propagation and reduced endocochlear potential associated with cochlear dysplasia in the BETA2/NeuroD1 null mouse. J Assoc Res Otolaryngol 8:447-463. (Pubitemid 350059931)
53. Yao W, Godfrey DA (1998) Immunohistochemical evaluation of cholinergic neurons in the rat superior olivary complex. Microsc Res Tech 41:270-283. (Pubitemid 28208633)
54. Yaylaoglu MB, Titmus A, Visel A, Alvarez-Bolado G, Thaller C, Eichele G (2005) Comprehensive expression atlas of fibroblast growth factors and their receptors generated by a novel robotic in situ hybridization platform. Dev Dyn 234:371-386. (Pubitemid 41369147)
55. Ylikoski J, Pirvola U, Moshnyakov M, Palgi J, Arumäe U, Saarma M (1993) Expression patterns of neurotrophin and their receptor mRNAs in the rat inner ear. Hear Res 65:69-78. (Pubitemid 23054416)