Thyroid hormone receptor α1 is a critical regulator for the expression of ion channels during final differentiation of outer hair cells

Histochemistry and Cell Biology

Volumn 128, Issue 1, 2007, Pages 65-75

  Winter, Harald ^a   Braig, Claudia ^a   Zimmermann, Ulrike ^a   Engel, Jutta ^b   Rohbock, Karin ^a   Knipper, Marlies ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

BK; CaV1.3; Repression; SK2; TR aporeceptors

Indexed keywords

ION CHANNEL; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; POTASSIUM CHANNEL; POTASSIUM CHANNEL KCNQ4; PRISTINAMYCIN; REGULATOR PROTEIN; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; THYROID HORMONE; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR ALPHA1; THYROID HORMONE RECEPTOR BETA; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DISEASE MODEL; GENE REPRESSION; HAIR CELL; HYPOTHESIS; HYPOTHYROIDISM; MOUSE; MUTANT; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REGULATORY MECHANISM; RODENT; THYROID DISEASE; VESTIBULAR SYSTEM;

RODENTIA;

EID: 34250886943     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-007-0294-6     Document Type: Article

References (68)

1. Beisel KW, Rocha-Sanchez SM, Morris KA, Nie L, Feng F, Kachar B, Yamoah EN, Fritzsch B (2005) Differential expression of KCNQ4 in inner hair cells and sensory neurons is the basis of progressive high-frequency hearing loss. J Neurosci 25:9285-9293
2. Belyantseva IA, Adler HJ, Curi R, Frolenkov GI, Kachar B (2000) Expression and localization of prestin and the sugar transporter GLUT-5 during development of electromotility in cochlear outer hair cells. J Neurosci 20:RC116
3. Bianchi LM, Conover JC, Fritzsch B, DeChiara T, Lindsay RM, Yancopoulos GD (1996) Degeneration of vestibular neurons in late embryogenesis of both heterozygous and homozygous BDNF null mutant mice. Development 122:1965-1973
4. Callery EM, Elinson RP (2000) Thyroid hormone-dependent metamorphosis in a direct developing frog. Proc Natl Acad Sci USA 97:2615-2620
5. Campos-Barros A, Amma LL, Faris JS, Shailam R, Kelley MW, Forrest D (2000) Type 2 iodothyronine deiodinase expression in the cochlea before the onset of hearing. Proc Natl Acad Sci USA 97:1287-1292
6. Chassande O (2003) Do unliganded thyroid hormone receptors have physiological functions? J Mol Endocrinol 31:9-20
7. Christ S, Biebel UW, Hoidis S, Friedrichsen S, Bauer K, Smolders JW (2004) Hearing loss in a thyroid pax8 knockout mice and effects of thyroxine substitution. Audiol Neurootol 9:88-106
8. Deol MS (1968) Inherited diseases of the inner ear in man in the light of studies on the mouse. J Med Genet 5:137-158
9. Deol MS (1973) An experimental approach to the understanding and treatment of hereditary syndromes with congenital deafness and hypothyroidism. J Med Genet 10:235-242
10. 2+ channel gene results in deafness but no vestibular defect in mice. J Assoc Res Otolaryngol 5:215-226
11. Dulon D, Lenoir M (1996) Cholinergic responses in developing outer hair cells of the rat cochlea. Eur J Neurosci 8:1945-1952
12. Eayrs JT (1971) Thyroid and developing brain: anatomical, behavioral effects. In: Hamburgh M, Barrington EJW (eds) In hormones and development. Appleton Centruy Crofts, New York, pp 345-355
13. Elgoyhen AB, Johnson DS, Boulter J, Vetter DE, Heinemann S (1994) Alpha 9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell 79:705-715
14. Elgoyhen AB, Vetter DE, Katz E, Rothlin CV, Heinemann SF, Boulter J (2001) Alpha10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Proc Natl Acad Sci USA 98:3501-3506
15. Engel J, Braig C, Ruttiger L, Kuhn S, Zimmermann U, Blin N, Sausbier M, Kalbacher H, Munkner S, Rohbock K, Ruth P, Winter H, Knipper M (2006) Two classes of outer hair cells along the tonotopic axis of the cochlea. Neuroscience 143:837-849
16. Flamant F, Poguet AL, Plateroti M, Chassande O, Gauthier K, Streichenberger N, Mansouri A, Samarut J (2002) Congenital hypothyroid Pax8(-/-) mutant mice can be rescued by inactivating the TR alpha gene. Mol Endocrinol 16:24-32
17. Forrest D, Erway LC, Ng L, Altschuler R, Curran T (1996a) Thyroid hormone receptor beta is essential for development of auditory function. Nat Genet 13:354-357
18. Forrest D, Hanebuth E, Smeyne RJ, Everds N, Stewart CL, Wehner JM, Curran T (1996b) Recessive resistance to thyroid hormone in mice lacking thyroid hormone receptor beta: evidence for tissue-specific modulation of receptor function. Embo J 15:3006-3015
19. Forrest D, Reh TA, Rusch A (2002) Neurodevelopmental control by thyroid hormone receptors. Curr Opin Neurobiol 12:49-56
20. Fritzsch B, Barald KF, Lomax MI (1998) Early embryology of the vertebrate ear. In: Rubel EW, Popper AN, Fay RR (eds) Development of the auditory system, vol 9. Springer, New York, Berlin, Heidelberg, pp 80-146
21. Geleoc GS, Risner JR, Holt JR (2004) Developmental acquisition of voltage-dependent conductances and sensory signaling in hair cells of the embryonic mouse inner ear. J Neurosci 24:11148-11159
22. 2+ channels for cochlear morphology. Hear Res 178:95-105
23. Hermanson O, Glass CK, Rosenfeld MG (2002) Nuclear receptor coregulators: multiple modes of modification. Trends Endocrinol Metab 13:55-60
24. Kharkovets T, Dedek K, Maier H, Schweizer M, Khimich D, Nouvian R, Vardanyan V, Leuwer R, Moser T, Jentsch TJ (2006) Mice with altered KCNQ4 K(+) channels implicate sensory outer hair cells in human progressive deafness. Embo J 25:642-652
25. + channel mutated in a form of dominant deafness, is expressed in the inner ear and the central auditory pathway. Proc Natl Acad Sci USA 97:4333-4338
26. Knipper M, Bandtlow C, Gestwa L, Kopschall I, Rohbock K, Wiechers B, Zenner HP, Zimmermann U (1998) Thyroid hormone affects Schwann cell and oligodendrocyte gene expression at the glial transition zone of the VIIIth nerve prior to cochlea function. Development 125:3709-3718
27. Knipper M, Gestwa L, Ten Cate WJ, Lautermann J, Brugger H, Maier H, Zimmermann U, Rohbock K, Kopschall I, Wiechers B, Zenner HP (1999) Distinct thyroid hormone-dependent expression of TrKB and p75NGFR in nonneuronal cells during the critical TH-dependent period of the cochlea. J Neurobiol 38:338-356
28. Knipper M, Richardson G, Mack A, Muller M, Goodyear R, Limberger A, Rohbock K, Kopschall I, Zenner HP, Zimmermann U (2001) Thyroid hormone-deficient period prior to the onset of hearing is associated with reduced levels of beta-tectorin protein in the tectorial membrane: implication for hearing loss. J Biol Chem 276:39046-39052
29. Knipper M, Zinn C, Maier H, Praetorius M, Rohbock K, Kopschall I, Zimmermann U (2000) Thyroid hormone deficiency before the onset of hearing causes irreversible damage to peripheral and central auditory systems. J Neurophysiol 83:3101-3112
30. Kros CJ, Ruppersberg JP, Rusch A (1998) Expression of a potassium current in inner hair cells during development of hearing in mice. Nature 394:281-284
31. Kubisch C, Schroeder BC, Friedrich T, Lutjohann B, El-Amraoui A, Marlin S, Petit C, Jentsch TJ (1999) KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness. Cell 96:437-446
32. Lautermann J, ten Cate WJ (1997) Postnatal expression of the alpha-thyroid hormone receptor in the rat cochlea. Hear Res 107:23-28
33. Liberman MC, Gao J, He DZ, Wu X, Jia S, Zuo J (2002) Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419:300-304
34. Macchia PE (2000) Recent advances in understanding the molecular basis of primary congenital hypothyroidism. Mol Med Today 6:36-42
35. Mai W, Janier MF, Allioli N, Quignodon L, Chuzel T, Flamant F, Samarut J (2004) Thyroid hormone receptor alpha is a molecular switch of cardiac function between fetal and postnatal life. Proc Natl Acad Sci USA 101:10332-10337
36. Mansouri A, Chowdhury K, Gruss P (1998) Follicular cells of the thyroid gland require Pax8 gene function. Nat Genet 19:87-90
37. Marcotti W, Kros CJ (1999) Developmental expression of the potassium current IK,n contributes to maturation of mouse outer hair cells. J Physiol 520.3:653-660
38. McNabb FMA (1988) Peripheral thyroid hormone dynamics in precocial and altrcial avian development. Am Zool 28:427-440
39. Meyerhoff WL (1979) Hypothyroidism and the ear: electrophysiological, morphological, and chemical considerations. Laryngoscope 89:1-25
40. Meza G, Acuna D, Escobar C (1996) Development of vestibular and auditory function: effects of hypothyroidism and thyroxine replacement therapy on nystagmus and auditory evoked potentials in the pigmented rat. Int J Dev Neurosci 14:515-522
41. 2+ currents in neonatal outer hair cells of mice. J Physiol 553:747-758
42. Moehren U, Eckey M, Baniahmad A (2004) Gene repression by nuclear hormone receptors. Essays Biochem 40:89-104
43. Morte B, Manzano J, Scanlan T, Vennstrom B, Bernal J (2002) Deletion of the thyroid hormone receptor alpha 1 prevents the structural alterations of the cerebellum induced by hypothyroidism. Proc Natl Acad Sci USA 99:3985-3989
44. Ng L, Rusch A, Amma LL, Nordstrom K, Erway LC, Vennstrom B, Forrest D (2001) Suppression of the deafness and thyroid dysfunction in Thrb-null mice by an independent mutation in the Thra thyroid hormone receptor alpha gene. Hum Mol Genet 10:2701-2708
45. + channels controls fast inhibitory synaptic transmission at auditory outer hair cells. Neuron 26:595-601
46. Paul BD, Buchholz DR, Fu L, Shi YB (2005) Tissue- and gene-specific recruitment of steroid receptor coactivator-3 by thyroid hormone receptor during development. J Biol Chem 280:27165-27172
47. 2+ channels. Cell 102:89-97
48. Quignodon L, Legrand C, Allioli N, Guadano-Ferraz A, Bernal J, Samarut J, Flamant F (2004) Thyroid hormone signaling is highly heterogeneous during pre- and postnatal brain development. J Mol Endocrinol 33:467-476
49. Ritter FN (1967) The effects of hypothyroidism upon the ear, nose and throat. A clinical and experimental study. Laryngoscope 77:1427-1479
50. Rocha-Sanchez SM, Morris KA, Kachar B, Nichols D, Fritzsch B, Beisel KW (2007) Developmental expression of Kcnq4 in vestibular neurons and neurosensory epithelia. Brain Res 1139:117-125
51. Rusch A, Erway LC, Oliver D, Vennstrom B, Forrest D (1998) Thyroid hormone receptor beta-dependent expression of a potassium conductance in inner hair cells at the onset of hearing. Proc Natl Acad Sci USA 95:15758-15762
52. 2+-activated potassium (BK) {alpha}-subunit but not the BK{beta}1-subunit leads to progressive hearing loss. Proc Natl Acad Sci USA 101:12922-12927
53. Simmons DD (2002) Development of the inner ear efferent system across vertebrate species. J Neurobiol 53:228-250
54. Solntseva GN (2001) Comparative analysis of vestibular system development in various groups of mammals living under different environmental conditions. Ontogenez 32:212-224
55. Spreadbury IC, Kros CJ, Meech RW (2004) Effects of trypsin on large-conductance Ca(2+)-activated K(+) channels of guinea-pig outer hair cells. Hear Res 190:115-127
56. Tell G, Pellizzari L, Esposito G, Pucillo C, Macchia PE, Di Lauro R, Damante G (1999) Structural defects of a Pax8 mutant that give rise to congenital hypothyroidism. Biochem J 341:89-93
57. Tinnikov A, Nordstrom K, Thoren P, Kindblom JM, Malin S, Rozell B, Adams M, Rajanayagam O, Pettersson S, Ohlsson C, Chatterjee K, Vennstrom B (2002) Retardation of post-natal development caused by a negatively acting thyroid hormone receptor alpha1. Embo J 21:5079-5087
58. Uziel A, Legrand C, Rabie A (1985) Corrective effects of thyroxine on cochlear abnormalities induced by congenital hypothyroidism in the rat. I. Morphological study. Brain Res 351:111-122
59. Uziel A, Pujol R, Legrand C, Legrand J (1983) Cochlear synaptogenesis in the hypothyroid rat. Brain Res 283:295-301
60. Vetter DE, Liberman MC, Mann J, Barhanin J, Boulter J, Brown MC, Saffiote-Kolman J, Heinemann SF, Elgoyhen AB (1999) Role of alpha9 nicotinic ACh receptor subunits in the development and function of cochlear efferent innervation. Neuron 23:93-103
61. Weber T, Zimmermann U, Winter H, Mack A, Kopschall I, Rohbock K, Zenner HP, Knipper M (2002) Thyroid hormone is a critical determinant for the regulation of the cochlear motor protein prestin. Proc Natl Acad Sci USA 99:2901-2906
62. Weiss RE, Refetoff S (2000) Resistance to thyroid hormone. Rev Endocr Metab Disord 1:97-108
63. Wikstrom L, Johansson C, Salto C, Barlow C, Campos Barros A, Baas F, Forrest D, Thoren P, Vennstrom B (1998) Abnormal heart rate and body temperature in mice lacking thyroid hormone receptor alpha 1. Embo J 17:455-461
64. Winter H, Braig C, Zimmermann U, Geisler HS, Franzer JT, Weber T, Ley M, Engel J, Knirsch M, Bauer K, Christ S, Walsh EJ, McGee J, Kopschall I, Rohbock K, Knipper M (2006) Thyroid hormone receptors TR{alpha}1 and TR{beta} differentially regulate gene expression of Kcnq4 and prestin during final differentiation of outer hair cells. J Cell Sci 119:2975-2984
65. Wooltorton JR, Gaboyard S, Hurley KM, Price SD, Garcia JL, Zhong M, Lysakowski A, Eatock RA (2007) Developmental changes in two voltage-dependent sodium currents in utricular hair cells. J Neurophysiol 97:1684-1704
66. Wu Y, Koenig RJ (2000) Gene regulation by thyroid hormone. Trends Endocrinol Metab 11:207-211
67. Yamano K (2005) The role of thyroid hormone in fish development with reference to aquaculture. JARQ 39:161-168
68. Zheng J, Shen W, He DZ, Long KB, Madison LD, Dallos P (2000) Prestin is the motor protein of cochlear outer hair cells. Nature 405:149-155