Autonomous functions of murine thyroid hormone receptor TRα and TRβ in cochlear hair cells

Molecular and Cellular Endocrinology

Volumn 382, Issue 1, 2014, Pages 26-37

  Dettling, Juliane ^a   Franz, Christoph ^a   Zimmermann, Ulrike ^a   Lee, Sze Chim ^a   Bress, Andreas ^b   Brandt, Niels ^c   Feil, Robert ^b   Pfister, Markus ^b   Engel, Jutta ^c   Flamant, Frédéric ^d   Rüttiger, Lukas ^a   Knipper, Marlies ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

^d UNIVERSITÉ DE LYON   (France)

Author keywords

ABR amplitudes; BK channel; Cochlear hair cells; Conditional mutant mice; Hypothyroidism; Thyroid hormone receptor ,

Indexed keywords

LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDIOMETRY; AUDITORY THRESHOLD; CELL FUNCTION; COCHLEA; CONTROLLED STUDY; EMBRYO; EVOKED BRAIN STEM AUDITORY RESPONSE; FEMALE; GENOTYPE; HAIR CELL; IMMUNOHISTOCHEMISTRY; MOUSE; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ABR AMPLITUDES; BK CHANNEL; COCHLEAR HAIR CELLS; CONDITIONAL MUTANT MICE; HYPOTHYROIDISM; THYROID HORMONE RECEPTOR Α, Β;

AFFERENT PATHWAYS; ANIMALS; AUDITORY PERCEPTION; BRAIN STEM; GENE EXPRESSION REGULATION; HAIR CELLS, AUDITORY; KCNQ POTASSIUM CHANNELS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MICE; MICE, KNOCKOUT; MOLECULAR MOTOR PROTEINS; ORGAN SPECIFICITY; OTOACOUSTIC EMISSIONS, SPONTANEOUS; PHENOTYPE; RECOMBINATION, GENETIC; SIGNAL TRANSDUCTION; TECTORIAL MEMBRANE; THYROID HORMONE RECEPTORS ALPHA; THYROID HORMONE RECEPTORS BETA;

EID: 84884547269     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.08.025     Document Type: Article

References (71)

1. Alzoubi K.H., Aleisa A.M., Alkadhi K.A. Adult-onset hypothyroidism facilitates and enhances LTD: reversal by chronic nicotine treatment. Neurobiol. Dis. 2007, 26:264-272.
2. Ben-Arie N., Bellen H.J., Armstrong D.L., McCall A.E., Gordadze P.R., Guo Q., Matzuk M.M., Zoghbi H.Y. Math1 is essential for genesis of cerebellar granule neurons. Nature 1997, 390:169-172.
3. 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.
4. Bernal J., Guadano-Ferraz A., Morte B. Perspectives in the study of thyroid hormone action on brain development and function. Thyroid 2003, 13:1005-1012.
5. Bradley D.J., Towle H.C., Young W.S. A and b thyroid hormone receptor (TR) gene expression during auditory neurogenesis: evidence for TR isoform-specific transcriptional regulation in vivo. Proc. Natl. Acad. Sci. USA 1994, 91:439-443.
6. + channels in rodent inner hair cells. J. Neurosci. 2007, 27:3174-3186.
7. Chatonnet F., Picou F., Fauquier T., Flamant F. Thyroid hormone action in cerebellum and cerebral cortex development. J. Thyroid Res. 2011, 2011:145762.
8. Chow L.M., Tian Y., Weber T., Corbett M., Zuo J., Baker S.J. Inducible Cre recombinase activity in mouse cerebellar granule cell precursors and inner ear hair cells. Dev. Dyn. 2006, 235:2991-2998.
9. Christ S., Biebel U.W., Hoidis S., Friedrichsen S., Bauer K., Smolders J.W. Hearing loss in athyroid pax8 knockout mice and effects of thyroxine substitution. Audiol. Neurootol. 2004, 9:88-106.
10. Cimerman J., Waldhaus J., Harasztosi C., Duncker S.V., Dettling J., Heidrych P., Bress A., Gampe-Braig C., Frank G., Gummer A.W., Oliver D., Knipper M., Zimmermann U. Generation of somatic electromechanical force by outer hair cells may be influenced by prestin-CASK interaction at the basal junction with the Deiter's cell. Histochem. Cell. Biol. 2013, 140:119-135.
11. Cordas E.A., Ng L., Hernandez A., Kaneshige M., Cheng S.Y., Forrest D. Thyroid hormone receptors control developmental maturation of the middle ear and the size of the ossicular bones. Endocrinology 2012, 153:1548-1560.
12. Dallos P. The active cochlea. J. Neurosci. 1992, 12:4575-4585.
13. Deol M.S. Inherited diseases of the inner ear in man in the light of studies on the mouse. J. Med. Genet. 1968, 5:137-158.
14. Deol M.S. An experimental approach to the understanding and treatment of hereditary syndromes with congenital deafness and hypothyroidism. J. Med. Genet. 1973, 10:235-242.
15. Dolan D.F., Nuttall A.L. Masked cochlear whole-nerve response intensity functions altered by electrical stimulation of the crossed olivocochlear bundle. J. Acoust. Soc. Am. 1988, 83:1081-1086.
16. Duncker S.V., Franz C., Kuhn S., Schulte W., Campanelli D., Brandt N., Hirt B., Fakler B., Blin N., Ruth P., Engel J., Marcotti W., Zimmermann U., Knipper M. The adaptor protein AP-2 (CLAP) interacts with otoferlin and myosin IV to mediate endocytosis in cochlear inner hair cells. J. Neurosci. 2013, 33:9508-9519.
17. Engel J., Braig C., Rüttiger L., Kuhn S., Zimmermann U., Blin N., Sausbier M., Kalbacher H., Münkner S., Rohbock K., Ruth P., Winter H., Knipper M. Two classes of outer hair cells along the tonotopic axis of the cochlea. Neuroscience 2006, 143:837-849.
18. -/- mutant mice can be rescued by inactivating the TRal gene. Mol. Endocrinol. 2002, 16:24-32.
19. Forrest D. Deafness and goiter: molecular genetic considerations. J. Clin. Endocrinol. Metab. 1996, 81:2764-2767.
20. Forrest D., Erway L.C., Ng L., Altschuler R., Curran T. Thyroid hormone receptor b is essential for development of auditory function. Nat. Genet. 1996, 13:354-357.
21. Forrest D., Hanebuth E., Smeyne R.J., Everds N., Stewart C.L., Wehner J.M., Curran T. Recessive resistance to thyroid hormone in mice lacking thyroid hormone receptor b: evidence for tissue-specific modulation of receptor function. Embo J. 1996, 15:3006-3015.
22. Forrest D., Reh T.A., Rüsch A. Neurodevelopmental control by thyroid hormone receptors. Curr. Opin. Neurobiol. 2002, 12:49-56.
23. Fuchs P.A., Murrow B.W. Cholinergic inhibition of short (outer) hair cells of the chick's cochlea. J. Neurosci. 1992, 12:800-809.
24. Fuchs P.A., Murrow B.W. A novel cholinergic receptor mediates inhibition of chick cochlear hair cells. Proc. Biol. Sci. 1992, 248:35-40.
25. Hashimoto K., Curty F.H., Borges P.P., Lee C.E., Abel E.D., Elmquist J.K., Cohen R.N., Wondisford F.E. An unliganded thyroid hormone receptor causes severe neurological dysfunction. Proc. Natl. Acad. Sci. USA 2001, 98:3998-4003.
26. He D.Z., Jia S., Feng F. Thyroid hormone is not necessary for the development of outer hair cell electromotility. Hear. Res. 2003, 175:183-189.
27. Housley G.D., Ashmore J.F. Direct measurement of the action of acetylcholine on isolated outer hair cells of the guinea pig cochlea. Proc. Biol. Sci. 1991, 244:161-167.
28. Janssen T., Niedermeyer H.P., Arnold W. Diagnostics of the cochlear amplifier by means of distortion product otoacoustic emissions. ORL J. Otorhinolaryngol. Relat. Spec. 2006, 68:334-339.
29. Johnson D.H., Kiang N.Y. Analysis of discharges recorded simultaneously from pairs of auditory nerve fibers. Biophys. J. 1976, 16:719-734.
30. 2+ dependence of vesicle fusion at auditory ribbon synapses. Nat. Neurosci. 2010, 13:45-52.
31. NGFR in nonneuronal cells during the critical TH-dependent period of the cochlea. J. Neurobiol. 1999, 38:338-356.
32. Knipper M., Zinn C., Maier H., Praetorius M., Rohbock K., Köpschall I., Zimmermann U. Thyroid hormone deficiency before the onset of hearing causes irreversible damage to peripheral and central auditory systems. J. Neurophysiol. 2000, 83:3101-3112.
33. Knipper M., Richardson G., Mack A., Müller M., Goodyear R., Limberger A., Rohbock K., Köpschall I., Zenner H.P., Zimmermann U. Thyroid hormone-deficient period prior to the onset of hearing is associated with reduced levels of b-tectorin protein in the tectorial membrane: implication for hearing loss. J. Biol. Chem. 2001, 276:39046-39052.
34. Kurt S., Sausbier M., Rüttiger L., Brandt N., Moeller C.K., Kindler J., Sausbier U., Zimmermann U., van Straaten H., Neuhuber W., Engel J., Knipper M., Ruth P., Schulze H. Critical role for cochlear hair cell BK channels for coding the temporal structure and dynamic range of auditory information for central auditory processing. FASEB J. 2012, 26:3834-3843.
35. Lautermann J., ten Cate W.J. Postnatal expression of the a-thyroid hormone receptor in the rat cochlea. Hear. Res. 1997, 107:23-28.
36. Legan P.K., Lukashkina V.A., Goodyear R.J., Kossi M., Russell I.J., Richardson G.P. A targeted deletion in a-tectorin reveals that the tectorial membrane is required for the gain and timing of cochlear feedback. Neuron 2000, 28:273-285.
37. Li M., Tian Y., Fritzsch B., Gao J., Wu X., Zuo J. Inner hair cell Cre-expressing transgenic mouse. Genesis 2004, 39:173-177.
38. Maison S.F., Pyott S.J., Meredith A.L., Liberman M.C. Olivocochlear suppression of outer hair cells in vivo: evidence for combined action of BK and SK2 channels throughout the cochlea. J. Neurophysiol. 2013, 109:1525-1534.
39. Marcotti W., Kros C.J. Developmental expression of the potassium current IK, n contributes to maturation of mouse outer hair cells. J. Physiol. 1999, 520(3):653-660.
40. Murugasu E., Russell I.J. The effect of efferent stimulation on basilar membrane displacement in the basal turn of the guinea pig cochlea. J. Neurosci. 1996, 16:325-332.
41. dw mutants. J. Neurosci. 2009, 29:1212-1223.
42. Ng L., Rüsch A., Amma L.L., Nordstrom K., Erway L.C., Vennström B., Forrest D. Suppression of the deafness and thyroid dysfunction in Thrb-null mice by an independent mutation in the Thra thyroid hormone receptor a gene. Hum. Mol. Genet. 2001, 10:2701-2708.
43. Ng L., Goodyear R.J., Woods C.A., Schneider M.J., Diamond E., Richardson G.P., Kelley M.W., Germain D.L., Galton V.A., Forrest D. Hearing loss and retarded cochlear development in mice lacking type 2 iodothyronine deiodinase. Proc. Natl. Acad. Sci. USA 2004, 101:3474-3479.
44. Ng L., Kelley M.W., Forrest D. Making sense with thyroid hormone-the role of T3 in auditory development. Nat. Rev. Endocrinol. 2013, 9:296-307.
45. Nouvian R., Ruel J., Wang J., Guitton M.J., Pujol R., Puel J.L. Degeneration of sensory outer hair cells following pharmacological blockade of cochlear KCNQ channels in the adult guinea pig. Eur. J. Neurosci. 2003, 17:2553-2562.
46. Pangršič T., Lasarow L., Reuter K., Takago H., Schwander M., Riedel D., Frank T., Tarantino L.M., Bailey J.S., Strenzke N., Brose N., Muller U., Reisinger E., Moser T. Hearing requires otoferlin-dependent efficient replenishment of synaptic vesicles in hair cells. Nat. Neurosci. 2010, 13:869-876.
47. Picou F., Fauquier T., Chatonnet F., Flamant F. A bimodal influence of thyroid hormone on cerebellum oligodendrocyte differentiation. Mol. Endocrinol. 2012, 26:608-618.
48. Quignodon L., Vincent S., Winter H., Samarut J., Flamant F. A point mutation in the activation function 2 domain of thyroid hormone receptor a1 expressed after CRE-mediated recombination partially recapitulates hypothyroidism. Mol. Endocrinol. 2007, 21:2350-2360.
49. Refetoff S., Weiss R.E., Usala S.J. The syndromes of resistance to thyroid hormone. Endocr. Rev. 1993, 14:348-399.
50. Ritter F.N. The effects of hypothyroidism upon the ear, nose and throat. A clinical and experimental study. Laryngoscope 1967, 77:1427-1479.
51. Rüsch A., Erway L.C., Oliver D., Vennström B., Forrest D. Thyroid hormone receptor b-dependent expression of a potassium conductance in inner hair cells at the onset of hearing. Proc. Natl. Acad. Sci. USA 1998, 95:15758-15762.
52. Rüsch A., Ng L., Goodyear R., Oliver D., Lisoukov I., Vennström B., Richardson G., Kelley M.W., Forrest D. Retardation of cochlear maturation and impaired hair cell function caused by deletion of all known thyroid hormone receptors. J. Neurosci. 2001, 21:9792-9800.
53. 2+-activated potassium (BK) a-subunit but not the BKb1-subunit leads to progressive hearing loss. Proc. Natl. Acad. Sci. USA 2004, 101:12922-12927.
54. Sap J., Munoz A., Damm K., Goldberg Y., Ghysdael J., Leutz A., Beug H., Vennström B. The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature 1986, 324:635-640.
55. Schimmang T., Tan J., Müller M., Zimmermann U., Rohbock K., Köpschall I., Limberger A., Minichiello L., Knipper M. Lack of Bdnf and TrkB signalling in the postnatal cochlea leads to a spatial reshaping of innervation along the tonotopic axis and hearing loss. Development 2003, 130:4741-4750.
56. Simmons D.D. Development of the inner ear efferent system across vertebrate species. J. Neurobiol. 2002, 53:228-250.
57. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
58. Tinnikov A., Nordstrom K., Thoren P., Kindblom J.M., Malin S., Rozell B., Adams M., Rajanayagam O., Pettersson S., Ohlsson C., Chatterjee K., Vennstrom B. Retardation of post-natal development caused by a negatively acting thyroid hormone receptor a1. Embo J. 2002, 21:5079-5087.
59. Uziel A. Periods of sensitivity to thyroid hormone during the development of the organ of Corti. Acta Otolaryngol. 1986, 429(Suppl.):23-27.
60. Uziel A., Legrand C., Rabie A. Corrective effects of thyroxine on cochlear abnormalities induced by congenital hypothyroidism in the rat. I. Morphological study. Brain Res. 1985, 351:111-122.
61. Walsh, E.J., McGee, J., Dallos, P., He, D.Z.Z., Knipper, M., Jia, S., Zheng, J., 2003. Prestin expression and electromotility in genetically-induced hypothyroidism. In: Santi, P.A. (Ed.), 26th Annual Midwinter Research Meeting of the Association for Research in Otolaryngology, Daytona Beach, Florida, USA, pp. 127, ARO Abstr. No. 499.
62. Warr W.B., Boche J.B., Neely S.T. Efferent innervation of the inner hair cell region: origins and terminations of two lateral olivocochlear systems. Hear. Res. 1997, 108:89-111.
63. Weber T., Zimmermann U., Winter H., Mack A., Köpschall I., Rohbock K., Zenner H.P., Knipper M. Thyroid hormone is a critical determinant for the regulation of the cochlear motor protein prestin. Proc. Natl. Acad. Sci. USA 2002, 99:2901-2906.
64. Weinberger C., Thompson C.C., Ong E.S., Lebo R., Gruol D.J., Evans R.M. The c-erb-A gene encodes a thyroid hormone receptor. Nature 1986, 324:641-646.
65. Wiederhold M.L., Kiang N.Y. Effects of electric stimulation of the crossed olivocochlear bundle on single auditory-nerve fibers in the cat. J. Acoust. Soc. Am. 1970, 48:950-965.
66. Winter H., Braig C., Zimmermann U., Geisler H.S., Fraenzer J.T., Weber T., Ley M., Engel J., Knirsch M., Bauer K., Christ S., Walsh E.J., McGee J., Köpschall I., Rohbock K., Knipper M. Thyroid hormone receptors TRa1 and TRb differentially regulate gene expression of Kcnq4 and prestin during final differentiation of outer hair cells. J. Cell Sci. 2006, 119:2975-2984.
67. Winter H., Braig C., Zimmermann U., Engel J., Rohbock K., Knipper M. Thyroid hormone receptor a1 is a critical regulator for the expression of ion channels during final differentiation of outer hair cells. Histochem. Cell. Biol. 2007, 128:65-75.
68. Winter H., Rüttiger L., Müller M., Kuhn S., Brandt N., Zimmermann U., Hirt B., Bress A., Sausbier M., Conscience A., Flamant F., Tian Y., Zuo J., Pfister M., Ruth P., Löwenheim H., Samarut J., Engel J., Knipper M. Deafness in TRb mutants is caused by malformation of the tectorial membrane. J. Neurosci. 2009, 29:2581-2587.
69. 2+ entry regulates sound transduction and auditory neurotransmission. Eur. J. Neurosci. 2013, 37:1478-1486.
70. Woods C., Montcouquiol M., Kelley M.W. Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat. Neurosci. 2004, 7:1310-1318.
71. Zheng J., Shen W., He D.Z., Long K.B., Madison L.D., Dallos P. Prestin is the motor protein of cochlear outer hair cells. Nature 2000, 405:149-155.