Developmental and cell-specific expression of thyroid hormone transporters in the mouse cochlea

Endocrinology

Volumn 152, Issue 12, 2011, Pages 5053-5064

  Sharlin, David S ^a   Visser, Theo J ^b   Forrest, Douglas ^a  

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

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSPORTER; CARRIER PROTEIN; CD31 ANTIGEN; L TYPE AMINO ACID TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 10; MONOCARBOXYLATE TRANSPORTER 8; ORGANIC ANION TRANSPORTER 1; THYROID HORMONE; THYROID HORMONE RECEPTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; BLOOD VESSEL; CELLULAR DISTRIBUTION; COCHLEA; COCHLEAR BLOOD VESSEL; CONTROLLED STUDY; FEMALE; HAIR CELL; HYPOTHYROIDISM; IMMUNOFLUORESCENCE TEST; IN SITU HYBRIDIZATION; MOUSE; NEUROEPITHELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SENSORY NERVE CELL; SPIRAL GANGLION; SPIRAL GANGLION NEURON; SPIRAL LIGAMENT; SPIRAL LIGAMENT FIBROCYTE; TYMPANIC BORDER CELL;

AMINO ACID TRANSPORT SYSTEMS, NEUTRAL; ANIMALS; BIOLOGICAL TRANSPORT; COCHLEA; MEMBRANE TRANSPORT PROTEINS; MICE; ORGAN SPECIFICITY; ORGANIC ANION TRANSPORT PROTEIN 1; ORGANIC CATION TRANSPORT PROTEINS; THYROID HORMONES;

EID: 82355188204     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1372     Document Type: Article

References (56)

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. Hébert R, Dussault JH 1984 Permanent peripheral hearing system alteration following transient neonatal hyperthyroidism in rats. Brain Res 316:159-164
5. Knipper M, Bandtlow C, Gestwa L, Köpschall 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
6. Uziel A, Rabie A, Marot M 1980 The effect of hypothyroidism on the onset of cochlear potentials in developing rats. Brain Res 182: 172-175
7. 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
8. Bradley DJ, Towle HC, Young 3rd WS 1992 Spatial and temporal expression of α- and β-thyroid hormone receptor mRNAs, including the β 2-subtype, in the developing mammalian nervous system. J Neurosci 12:2288-2302
9. 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
10. Ng L, Hernandez A, He W, Ren T, Srinivas M, Ma M, Galton VA, St Germain DL, Forrest D 2009 A protective role for type 3 deiodinase, a thyroid hormone-inactivating enzyme, in cochlear development and auditory function. Endocrinology 150:1952-1960
11. Rusch 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
12. Winter H, Braig C, Zimmermann U, Geisler HS, Fränzer JT, Weber T, Ley M, Engel J, Knirsch M, Bauer K, Christ S, Walsh EJ, McGee J, Köpschall I, Rohbock K, Knipper M 2006 Thyroid hormone receptors TRα1 and TRβ differentially regulate gene expression of Kcnq4 and prestin during final differentiation of outer hair cells. J Cell Sci 119:2975-2984
13. Axelsson A 1988 Comparative anatomy of cochlear blood vessels. Am J Otolaryngol 9:278-290
14. 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
15. 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
16. Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR 2002 Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr Rev 23:38-89
17. Friesema EC, Jansen J, Milici C, Visser TJ 2005 Thyroid hormone transporters. Vitam Horm 70:137-167
18. Dumitrescu AM, Liao XH, Best TB, Brockmann K, Refetoff S 2004 A novel syndrome combining thyroid and neurological abnormalities is associated with mutations in a monocarboxylate transporter gene. Am J Hum Genet 74:168-175
19. 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
20. Marians RC, Ng L, Blair HC, Unger P, Graves PN, Davies TF 2002 Defining thyrotropin-dependent and -independent steps of thyroid hormone synthesis by using thyrotropin receptor-null mice. Proc Natl Acad Sci USA 99:15776-15781
21. Wangemann P, Kim HM, Billings S, Nakaya K, Li X, Singh R, Sharlin DS, Forrest D, Marcus DC, Fong P 2009 Developmental delays consistent with cochlear hypothyroidism contribute to failure to develop hearing in mice lacking Slc26a4/pendrin expression. Am J Physiol Renal Physiol 297:F1435-F1447
22. Livak KJ, Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method. Methods 25:402-408
23. Roberts LM, Woodford K, Zhou M, Black DS, Haggerty JE, Tate EH, Grindstaff KK, Mengesha W, Raman C, Zerangue N 2008 Expression of the thyroid hormone transporters monocarboxylate transporter-8 (SLC16A2) and organic ion transporter-14 (SLCO1C1) at the blood-brain barrier. Endocrinology 149: 6251-6261
24. Trajkovic M, Visser TJ, Mittag J, Horn S, Lukas J, Darras VM, Raivich G, Bauer K, Heuer H 2007 Abnormal thyroid hormone metabolism in mice lacking the monocarboxylate transporter 8. J Clin Invest 117:627-635
25. Skvorak AB, Weng Z, Yee AJ, Robertson NG, Morton CC 1999 Human cochlear expressed sequence tags provide insight into cochlear gene expression and identify candidate genes for deafness. Hum Mol Genet 8:439-452
26. Spicer SS, Schulte BA 1996 The fine structure of spiral ligament cells relates to ion return to the stria and varies with place-frequency. Hear Res 100:80-100
27. Bernal J 2005 The significance of thyroid hormone transporters in the brain. Endocrinology 146:1698-1700
28. Freitas BC, Gereben B, Castillo M, Kalló I, Zeöld A, Egri P, Liposits Z, Zavacki AM, Maciel RM, Jo S, Singru P, Sanchez E, Lechan RM, Bianco AC 2010 Paracrine signaling by glial cell-derived triiodothyronine activates neuronal gene expression in the rodent brain and human cells. J Clin Invest 120:2206-2217
29. Guadaño-Ferraz A, Obregón MJ, St Germain DL, Bernal J 1997 The type 2 iodothyronine deiodinase is expressed primarily in glial cells in the neonatal rat brain. Proc Natl Acad Sci USA 94:10391-10396
30. Robbins J, Goncalves E, Lakshmanan M, Foti D 1989 Thyroid hormone transport from blood into brain cells. In: DeLong GR, Robbins J, Condliffe PG, eds. Iodine and the brain. New York: Plenum Press; 39-50
31. Verrey F 2003 System L: heteromeric exchangers of large, neutral amino acids involved in directional transport. Pflugers Arch 445: 529-533
32. Friesema EC, Docter R, Moerings EP, Verrey F, Krenning EP, Hennemann G, Visser TJ 2001 Thyroid hormone transport by the heterodimeric human system L amino acid transporter. Endocrinology 142:4339-4348
33. Kageyama T, Imura T, Matsuo A, Minato N, Shimohama S 2000 Distribution of the 4F2 light chain, LAT1, in the mouse brain. Neuroreport 11:3663-3666
34. Matsuo H, Tsukada S, Nakata T, Chairoungdua A, Kim DK, Cha SH, Inatomi J, Yorifuji H, Fukuda J, Endou H, Kanai Y 2000 Expression of a system L neutral amino acid transporter at the bloodbrain barrier. Neuroreport 11:3507-3511
35. Sugiyama D, Kusuhara H, Taniguchi H, Ishikawa S, Nozaki Y, Aburatani H, Sugiyama Y 2003 Functional characterization of rat brain-specific organic anion transporter (Oatp14) at the bloodbrain barrier: high affinity transporter for thyroxine. J Biol Chem 278:43489-43495
36. Tohyama K, Kusuhara H, Sugiyama Y 2004 Involvement of multispecific organic anion transporter, Oatp14 (Slc21a14), in the transport of thyroxine across the blood-brain barrier. Endocrinology 145:4384-4391
37. Friesema EC, Jansen J, Jachtenberg JW, Visser WE, Kester MH, Visser TJ 2008 Effective cellular uptake and efflux of thyroid hormone by human monocarboxylate transporter 10. Mol Endocrinol 22:1357-1369
38. Kim DK, Kanai Y, Chairoungdua A, Matsuo H, Cha SH, Endou H 2001 Expression cloning of a Na+-independent aromatic amino acid transporter with structural similarity to H+/monocarboxylate transporters. J Biol Chem 276:17221-17228
39. Chiba T, Marcus DC 2000 Nonselective cation and BK channels in apical membrane of outer sulcus epithelial cells. J Membr Biol 174: 167-179
40. Marcus DC, Chiba T 1999K+ and Na+absorption by outer sulcus epithelial cells. Hear Res 134:48-56
41. Ramadan T, Camargo SM, Summa V, Hunziker P, Chesnov S, Pos KM, Verrey F 2006 Basolateral aromatic amino acid transporter TAT1 (Slc16a10) functions as an efflux pathway. J Cell Physiol 206:771-779
42. Mustapha M, Fang Q, Gong TW, Dolan DF, Raphael Y, Camper SA, Duncan RK 2009 Deafness and permanently reduced potassium channel gene expression and function in hypothyroid Pit1dw mutants. J Neurosci 29:1212-1223
43. Schwartz CE, Stevenson RE 2007 The MCT8 thyroid hormone transporter and Allan-Herndon-Dudley syndrome. Best Pract Res Clin Endocrinol Metab 21:307-321
44. Wirth EK, Roth S, Blechschmidt C, Hölter SM, Becker L, Racz I, Zimmer A, Klopstock T, Gailus-Durner V, Fuchs H, Wurst W, Naumann T, Bräuer A, de Angelis MH, Köhrle J, Grüters A, Schweizer U 2009 Neuronal 3′,3,5-triiodothyronine (T3) uptake and behavioral phenotype of mice deficient in Mct8, the neuronal T3 transporter mutated in Allan-Herndon-Dudley syndrome. J Neurosci 29: 9439-9449
45. Braun D, Kinne A, Bräuer AU, Sapin R, Klein MO, Köhrle J, Wirth EK, Schweizer U 2011 Developmental and cell type-specific expression of thyroid hormone transporters in the mouse brain and in primary brain cells. Glia 59:463-471
46. Friesema EC, Ganguly S, Abdalla A, Manning Fox JE, Halestrap AP, Visser TJ 2003 Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. J Biol Chem 278:40128-40135
47. Flock A, Flock B, Fridberger A, Scarfone E, Ulfendahl M 1999 Supporting cells contribute to control of hearing sensitivity. J Neurosci 19:4498-4507
48. Brandt N, Kuhn S, Münkner S, Braig C, Winter H, Blin N, Vonthein R, Knipper M, Engel J 2007 Thyroid hormone deficiency affects postnatal spiking activity and expression of Ca2+ and K+channels in rodent inner hair cells. J Neurosci 27:3174-3186
49. Ali G, Santos RL, John P, Wambangco MA, Lee K, Ahmad W, Leal S 2006 The mapping of DFNB62, a new locus for autosomal recessive non-syndromic hearing impairment, to chromosome 12p13.2- p11.23. Clin Genet 69:429-433
50. Liang VC, Sedgwick T, Shi YB 1997 Characterization of the Xenopus homolog of an immediate early gene associated with cell activation: sequence analysis and regulation of its expression by thyroid hormone during amphibian metamorphosis. Cell Res 7:179-193
51. Ritchie JW, Peter GJ, Shi YB, Taylor PM 1999 Thyroid hormone transport by 4F2hc-IU12 heterodimers expressed in Xenopus oocytes. J Endocrinol 163:R5-R9
52. Meier C, Ristic Z, Klauser S, Verrey F 2002 Activation of system L heterodimeric amino acid exchangers by intracellular substrates. EMBO J 21:580-589
53. Westholm DE, Salo DR, Viken KJ, Rumbley JN, Anderson GW 2009 The blood-brain barrier thyroxine transporter organic anion-transporting polypeptide 1c1 displays atypical transport kinetics. Endocrinology 150:5153-5162
54. Westholm DE, Stenehjem DD, Rumbley JN, Drewes LR, Anderson GW 2009 Competitive inhibition of organic anion transporting polypeptide 1c1-mediated thyroxine transport by the fenamate class of nonsteroidal antiinflammatory drugs. Endocrinology 150:1025-1032
55. Murillo-Cuesta S, Contreras J, Zurita E, Cediel R, Cantero M, Varela- Nieto I, Montoliu L 2010 Melanin precursors prevent premature age-related and noise-induced hearing loss in albino mice. Pigment Cell Melanoma Res 23:72-83
56. Bombardier C, Peloso PM, Goldsmith CH 1995 Salsalate, a non-acetylated salicylate, is as efficacious as diclofenac in patients with rheumatoid arthritis. Salsalate-Diclofenac study group. J Rheumatol 22:617-624