A protective role for type 3 deiodinase, a thyroid hormone-inactivating enzyme, in cochlear development and auditory function

Endocrinology

Volumn 150, Issue 4, 2009, Pages 1952-1960

  Ng, Lily ^a   Hernandez, Arturo ^b   He, Wenxuan ^c   Ren, Tianying ^c   Srinivas, Maya ^d   Michelle, Ma ^a   Galton, Valerie A ^b   St Germain, Donald L ^b   Forrest, Douglas ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEIODINASE 2; DEIODINASE 3; LIOTHYRONINE RECEPTOR; MESSENGER RNA; OXIDOREDUCTASE; THYROID HORMONE RECEPTOR BETA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COCHLEA; CONTROLLED STUDY; EMBRYO; HEARING; HEARING DISORDER; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPIRAL GANGLION; STRIA VASCULARIS;

ANIMALS; BLOTTING, NORTHERN; COCHLEA; IN SITU HYBRIDIZATION; IODIDE PEROXIDASE; MICE; MICE, MUTANT STRAINS; RADIOIMMUNOASSAY; THYROID HORMONE RECEPTORS BETA; THYROID HORMONES;

EID: 63849159901     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-1419     Document Type: Article

References (50)

1. DeLong GR, Stanbury JB, Fierro-Benitez R 1985 Neurological signs in congenital iodine-deficiency disorder (endemic cretinism). Dev Med Child Neurol 27:317-324
2. Rovet J, Walker W, Bliss B, Buchanan L, Ehrlich R 1996 Long-term sequelae of hearing impairment in congenital hypothyroidism. J Pediatr 128:776-783
3. Deol MS 1976 The role of thyroxine in the differentiation of the organ of Corti. Acta Otolaryngol 81:429-435
4. Hebert R, Langlois JM, Dussault JH 1985 Permanent defects in rat peripheral auditory function following perinatal hypothyroidism: determination of a critical period. Brain Res 23:161-170
5. Uziel A 1986 Periods of sensitivity to thyroid hormone during the development of the organ of Corti. Acta Otolaryngol Suppl 429:23-27
6. R̈sch A, Ng L, Goodyear R, Oliver D, Lisoukov I, Vennstrom B, Richardson G, Kelley MW, Forrest D 2001 Retardation of cochlear maturation and impaired hair cell function caused by deletion of all known thyroid hormone receptors. J Neurosci 21:9792-9800
7. 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
8. Sendin G, Bulankina AV, Riedel D, Moser T 2007 Maturation of ribbon synapses in hair cells is driven by thyroid hormone. J Neurosci 27:3163-3173
9. Refetoff S, DeWind LT, DeGroot LJ 1967 Familial syndrome combining deafmutism,stippledepiphyses,goiter,andabnormallyhighPBI:possibletargetorgan refractoriness to thyroid hormone. J Clin Endocrinol Metab 27:279 -294
10. Brucker-Davis F, Skarulis MC, Pikus A, Ishizawar D, Mastroianni M-A, Koby M,WeintraubBD1996Prevalenceandmechanismsofhearinglossinpatients with resistance to thyroid hormone. J Clin Endocrinol Metab 81:2768 -2772
11. Phillips SA, Rotman-Pikielny P, Lazar J, Ando S, Hauser P, Skarulis MC, Brucker- Davis F, Yen PM 2001 Extreme thyroid hormone resistance in a patient with a novel truncated TR mutant. J Clin Endocrinol Metab 86:5142-5147
12. Forrest D, Erway LC, Ng L, Altschuler R, Curran T 1996 Thyroid hormone receptor β is essential for development of auditory function. Nat Genet 13: 354-357
13. Griffith AJ, Szymko YM, Kaneshige M, Quinonez RE, Kaneshige K, Heintz KA, Mastroianni MA, Kelley MW, Cheng SY 2002 Knock-inmousemodelfor resistance to thyroid hormone (RTH): an RTH mutation in the thyroid hormone receptor β gene disrupts cochlear morphogenesis. J Assoc Res Otolaryngol 3:279-288
14. Bradley DJ, Towle HC, Young 3rd WS 1994 α and β thyroid hormone receptor (TR) gene expression during auditory neurogenesis: evidence for TR isoform- specific transcriptional regulation in vivo. Proc Natl Acad Sci USA 91:439-443
15. Bianco AC, Salvatore D, GerebenB, Berry MJ, LarsenPR 2002 Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr Rev 23:38 -89
16. St Germain DL, Hernandez A, Schneider MJ, Galton VA 2005 Insights into the role of deiodinases from studies of genetically modified animals. Thyroid 15: 905-916
17. 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
18. Ng L, Goodyear RJ, Woods CA, Schneider MJ, Diamond E, Richardson GP, Kelley MW, Germain DL, Galton VA, Forrest D 2004 Hearing loss and retarded cochlear development in mice lacking type 2 iodothyronine deiodinase. Proc Natl Acad Sci USA 101:3474-3479
19. Hernandez A, Martinez ME, Fiering S, Galton VA, St Germain D 2006 Type 3 deiodinase is critical for the maturation and function of the thyroid axis. JClin Invest 116:476-484
20. Ren T 2002 Longitudinal pattern of basilar membrane vibration in the sensitive cochlea. Proc Natl Acad Sci USA 99:17101-17106
21. Cheatham MA, Huynh KH, Gao J, Zuo J, Dallos P 2004 Cochlear function in Prestin knockout mice. J Physiol 560(Pt 3):821-830
22. 4. Mol Endocrinol 15:2137-2148
23. Hernandez A 2005 Structureand function of the type 3 deiodinase gene. Thyroid 15:865-874
24. Dentice M, Luongo C, Huang S, Ambrosio R, Elefante A, Mirebeau-Prunier D, Zavacki AM, Fenzi G, Grachtchouk M, Hutchin M, Dlugosz AA, Bianco AC, Missero C, Larsen PR, Salvatore D 2007 Sonic hedgehog-induced type 3 deiodinase blocks thyroid hormone action enhancing proliferation of normal and malignant keratinocytes. Proc Natl Acad Sci USA 104:14466-14471
25. Nakashima T, Naganawa S, Sone M, Tominaga M, Hayashi H, Yamamoto H, Liu X, Nuttall AL 2003 Disorders of cochlear blood flow. Brain Res Brain Res Rev 43:17-28
26. Hernandez A, Fiering S, Martinez E, Galton VA, St Germain D 2002 The gene locus encoding iodothyronine deiodinasetype 3 (Dio3) is imprinted in the fetus and expresses antisense transcripts. Endocrinology 143:4483-4486
27. Parham K, SunX-M, Kim D 2001 Noninvasive assessment of auditory function in mice: auditory brainstem response and distortion product otoacoustic emissions. In: Willott J, ed. Handbook of mouse auditory research. Boca Raton, FL: CRC Press; 37-58
28. Karolyi IJ, Dootz GA, Halsey K, Beyer L, Probst FJ, Johnson KR, Parlow AF, Raphael Y, Dolan DF, Camper SA 2007 Dietary thyroid hormone replacement ameliorates hearing deficits in hypothyroid mice. Mamm Genome 18:596-608
29. Kikuchi K, Hilding DA 1967 The spiral vessel and stria vascularis in Shaker-1 mice. Electron microscopic and histochemical observations. Acta Otolaryngol 63:395-410
30. Dallos P, Popper A, Fay R 1996 The cochlea. New York: Springer
31. Dumitrescu AM, Liao XH, Best TB, BrockmannK, Refetoff S 2004 Anovel syndrome combining thyroid and neurological abnormalities is associated with mutations in a monocarboxylate transporter gene. Am J Hum Genet 74:168-175
32. Friesema EC, Grueters A, Biebermann H, Krude H, von Moers A, Reeser M, Barrett TG, Mancilla EE, Svensson J, Kester MH, Kuiper GG, Balkassmi S, Uitterlinden AG, Koehrle J, Rodien P, Halestrap AP, Visser TJ 2004 Association between mutations in a thyroid hormone transporter and severe X-linked psychomotor retardation. Lancet 364:1435-1437
33. Katz LC, Shatz CJ 1996 Synaptic activity and the construction of cortical circuits. Science 274:1133-1138
34. Ruben RJ, Rapin I 1980 Plasticity of the developing auditory system. Ann Otol Rhinol Laryngol 89:303-311
35. Inui Y, Miwa S 1985 Thyroid hormone induces metamorphosis of flounder larvae. Gen Comp Endocrinol 60:450 -454
36. Takahashi K, Kamiya K, Urase K, Suga M, Takizawa T, Mori H, Yoshikawa Y, IchimuraK, KuidaK, MomoiT2001 Caspase-3-deficiencyinduces hyper- plasia of supporting cells and degeneration of sensory cells resulting in the hearing loss. Brain Res 894:359-367
37. Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE 2007 The origin of spontaneous activity in the developing auditory system. Nature 450:50 -55
38. Dow-Edwards D, Crane AM, Rosloff B, Kennedy C, Sokoloff L 1986 Local cerebral glucose utilization in the adult cretinous rat. Brain Res 373:139-145
39. Guadaño-Ferraz A, Escámez M, Rausell E, Bernal J 1999 Expression of type 2 iodothyronine deiodinase in hypothyroid rat brain indicates an important role of thyroid hormone in the development of specific primary sensory neurons. J Neurosci 19:3430 -3439
40. Sprenkle PM, McGee J, Bertoni JM, Walsh EJ 2001 Prevention of auditory dysfunction in hypothyroid Tshr mutant mice by thyroxin treatment during development. J Assoc Res Otolaryngol 2:348 -361
41. Bernard PA, Hebert R, Coulombe P 1982 Influence of tetraiodothyronine on hearing maturation in rats. Arch Otorhinolaryngol 234:181-186
42. Freeman S, Cherny L, Sohmer H 1996 Thyroxine affects physiological and morphological development of the ear. Hear Res 97:19 -29
43. Marsh-Armstrong N, Huang H, Remo BF, Liu TT, Brown DD 1999 Asymmetric growth and development of the Xenopus laevis retina during metamorphosis is controlled by type III deiodinase. Neuron 24:871-878
44. Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, Hirunagi K, Ebihara S 2003 Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 426:178 -181
45. Galton VA, Martinez E, Hernandez A, St Germain EA, Bates JM, St Germain DL 1999 Pregnant rat uterus expresses high levels of the type 3 iodothyronine deiodinase. J Clin Invest 103:979-987
46. Huang SA, Dorfman DM, Genest DR, Salvatore D, Larsen PR 2003 Type 3 iodothyronine deiodinase is highly expressed in the human uteroplacental unit and in fetal epithelium. J Clin Endocrinol Metab 88:1384-1388
47. Hernandez A, Martinez ME, Liao XH, Van Sande J, Refetoff S, Galton VA, St Germain DL 2007 Type 3 deiodinase deficiency results in functional abnormalities at multiple levels of the thyroid axis. Endocrinology 148:5680 -5687
48. Trigueiros-Cunha N, Leao P, Renard N, Tavares MA, Eybalin M 2006 Prenatal cocaine exposure accelerates morphological changes and transient expression of tyrosine hydroxylase in the cochlea of developing rats. Brain Res 1086:55-64
49. Church MW, Crossland WJ, Holmes PA, Overbeck GW, Tilak JP 1998 Effects of prenatal cocaine on hearing, vision, growth, and behavior. Ann NY Acad Sci 846:12-28
50. Lester BM, Lagasse L, Seifer R, Tronick EZ, Bauer CR, Shankaran S, Bada HS, Wright LL, Smeriglio VL, Liu J, Finnegan LP, Maza PL 2003 The Maternal Lifestyle Study (MLS): effects of prenatal cocaine and/or opiate exposure on auditory brain response at one month. JPediatr 142:279-285