Advertisement

Mammalian Genome

, Volume 30, Issue 1–2, pp 5–22 | Cite as

Genetic variation in thyroid folliculogenesis influences susceptibility to hypothyroidism-induced hearing impairment

  • Amanda H. Mortensen
  • Qing Fang
  • Michelle T. Fleming
  • Thomas J. Jones
  • Alexandre Z. Daly
  • Kenneth R. Johnson
  • Sally A. CamperEmail author
Article
  • 126 Downloads

Abstract

Maternal and fetal sources of thyroid hormone are important for the development of many organ systems. Thyroid hormone deficiency causes variable intellectual disability and hearing impairment in mouse and man, but the basis for this variation is not clear. To explore this variation, we studied two thyroid hormone-deficient mouse mutants with mutations in pituitary-specific transcription factors, POU1F1 and PROP1, that render them unable to produce thyroid stimulating hormone. DW/J-Pou1f1dw/dw mice have profound deafness and both neurosensory and conductive hearing impairment, while DF/B-Prop1df/df mice have modest elevations in hearing thresholds consistent with developmental delay, eventually achieving normal hearing ability. The thyroid glands of Pou1f1 mutants are more severely affected than those of Prop1df/df mice, and they produce less thyroglobulin during the neonatal period critical for establishing hearing. We previously crossed DW/J-Pou1f1dw/+ and Cast/Ei mice and mapped a major locus on Chromosome 2 that protects against hypothyroidism-induced hearing impairment in Pou1f1dw/dw mice: modifier of dw hearing (Mdwh). Here we refine the location of Mdwh by genotyping 196 animals with 876 informative SNPs, and we conduct novel mapping with a DW/J-Pou1f1dw/+ and 129/P2 cross that reveals 129/P2 mice also have a protective Mdwh locus. Using DNA sequencing of DW/J and DF/B strains, we determined that the genes important for thyroid gland function within Mdwh vary in amino acid sequence between strains that are susceptible or resistant to hypothyroidism-induced hearing impairment. These results suggest that the variable effects of congenital hypothyroidism on the development of hearing ability are attributable to genetic variation in postnatal thyroid gland folliculogenesis and function.

Notes

Acknowledgements

We thank the March of Dimes for funding (Grant N018020 to SAC), the NIH (T32GM00754 and T32HG000040 to AZD), Stephen H. Hinshaw for access to the dermestid beetle colony at the University of Michigan Ruthven Museum, Dr. Robert H. Lyons, Jr. and members of the University of Michigan DNA Sequencing Core Facility for sequencing and genotyping, members of the Kresge Hearing Research Institute including Jennifer Benson, Lisa Kabala, and David F. Dolan for auditory brainstem response testing, and Jun Z. Li, David T. Burke, Ronald J. Koenig, and Miriam H. Meisler for helpful discussions.

Funding

March of Dimes Foundation (N018020) Sally A. Camper. National Institutes of Health (T32GM007544) Alexandre Z. Daly. National Institutes of Health (T32HG000040) Alexandre Z. Daly.

Compliance with ethical standards

Conflict of interest

The authors have nothing to disclose.

Ethical Approval

Guidelines of the Care and Use of Experimental Animals are approved by our Institutional Animal Care and Use Committee.

Supplementary material

335_2019_9792_MOESM1_ESM.tif (13 mb)
Supplementary material 1 (TIF 13335 KB)
335_2019_9792_MOESM2_ESM.tif (22 mb)
Supplementary material 2 (TIF 22528 KB)
335_2019_9792_MOESM3_ESM.docx (15 kb)
Supplementary material 3 (DOCX 15 KB)

References

  1. Abu-Khudir R, Larrivee-Vanier S, Wasserman JD, Deladoey J (2017) Disorders of thyroid morphogenesis. Best Pract Res Clin Endocrinol Metab 31:143–159CrossRefGoogle Scholar
  2. Amendola E, De Luca P, Macchia PE, Terracciano D, Rosica A, Chiappetta G, Kimura S, Mansouri A, Affuso A, Arra C, Macchia V, Di Lauro R, De Felice M (2005) A mouse model demonstrates a multigenic origin of congenital hypothyroidism. Endocrinology 146:5038–5047CrossRefGoogle Scholar
  3. Amendola E, Sanges R, Galvan A, Dathan N, Manenti G, Ferrandino G, Alvino FM, Di Palma T, Scarfo M, Zannini M, Dragani TA, De Felice M, Di Lauro R (2010) A locus on mouse chromosome 2 is involved in susceptibility to congenital hypothyroidism and contains an essential gene expressed in thyroid. Endocrinology 151:1948–1958CrossRefGoogle Scholar
  4. Beamer WJ, Eicher EM, Maltais LJ, Southard JL (1981) Inherited primary hypothyroidism in mice. Science 212:61–63CrossRefGoogle Scholar
  5. Bellman SC, Davies A, Fuggle PW, Grant DB, Smith I (1996) Mild impairment of neuro-otological function in early treated congenital hypothyroidism. Arch Dis Child 74:215–218CrossRefGoogle Scholar
  6. Berbel P, Obregon MJ, Bernal J, Escobar del Rey F, Morreale de Escobar G (2007) Iodine supplementation during pregnancy: a public health challenge. Trends Endocrinol Metab 18:338–343CrossRefGoogle Scholar
  7. Bernal J, Guadano-Ferraz A, Morte B (2015) Thyroid hormone transporters–functions and clinical implications. Nat Rev Endocrinol 11:506CrossRefGoogle Scholar
  8. Brent GA (2012) Mechanisms of thyroid hormone action. J Clin Invest 122:3035–3043CrossRefGoogle Scholar
  9. Brinkmeier ML, Davis SW, Carninci P, MacDonald JW, Kawai J, Ghosh D, Hayashizaki Y, Lyons RH, Camper SA (2009) Discovery of transcriptional regulators and signaling pathways in the developing pituitary gland by bioinformatic and genomic approaches. Genomics 93:449–460CrossRefGoogle Scholar
  10. Brucker-Davis F, Skarulis MC, Pikus A, Ishizawar D, Mastroianni MA, Koby M, Weintraub BD (1996) Prevalence and mechanisms of hearing loss in patients with resistance to thyroid hormone. J Clin Endocrinol Metab 81:2768–2772Google Scholar
  11. Buchner DA, Nadeau JH (2015) Contrasting genetic architectures in different mouse reference populations used for studying complex traits. Genome Res 25:775–791CrossRefGoogle Scholar
  12. Christ S, Biebel UW, Hoidis S, Friedrichsen S, Bauer K, Smolders JW (2004) Hearing loss in athyroid pax8 knockout mice and effects of thyroxine substitution. Audiol Neurootol 9:88–106CrossRefGoogle Scholar
  13. Cooper GM, Stone EA, Asimenos G, Program NCS, Green ED, Batzoglou S, Sidow A (2005) Distribution and intensity of constraint in mammalian genomic sequence. Genome Res 15:901–913CrossRefGoogle Scholar
  14. Cordas EA, Ng L, Hernandez A, Kaneshige M, Cheng SY, Forrest D (2012) Thyroid hormone receptors control developmental maturation of the middle ear and the size of the ossicular bones. Endocrinology 153:1548–1560CrossRefGoogle Scholar
  15. Corvol H, Blackman SM, Boelle PY, Gallins PJ, Pace RG, Stonebraker JR, Accurso FJ, Clement A, Collaco JM, Dang H, Dang AT, Franca A, Gong J, Guillot L, Keenan K, Li W, Lin F, Patrone MV, Raraigh KS, Sun L, Zhou YH, O’Neal WK, Sontag MK, Levy H, Durie PR, Rommens JM, Drumm ML, Wright FA, Strug LJ, Cutting GR, Knowles MR (2015) Genome-wide association meta-analysis identifies five modifier loci of lung disease severity in cystic fibrosis. Nat Commun 6:8382CrossRefGoogle Scholar
  16. Cuevas E, Auso E, Telefont M, Morreale de Escobar G, Sotelo C, Berbel P (2005) Transient maternal hypothyroxinemia at onset of corticogenesis alters tangential migration of medial ganglionic eminence-derived neurons. Eur J Neurosci 22:541–551CrossRefGoogle Scholar
  17. Di Jeso B, Arvan P (2016) Thyroglobulin from molecular and cellular biology to clinical endocrinology. Endocr Rev 37:2–36CrossRefGoogle Scholar
  18. Douglas KR, Brinkmeier ML, Kennell JA, Eswara P, Harrison TA, Patrianakos AI, Sprecher BS, Potok MA, Lyons RH Jr, MacDougald OA, Camper SA (2001) Identification of members of the Wnt signaling pathway in the embryonic pituitary gland. Mamm Genome 12:843–851CrossRefGoogle Scholar
  19. Dumont BL, Payseur BA (2011) Genetic analysis of genome-scale recombination rate evolution in house mice. PLoS Genet 7:e1002116CrossRefGoogle Scholar
  20. Engels K, Rakov H, Zwanziger D, Moeller LC, Homuth G, Kohrle J, Brix K, Fuhrer D (2015) Differences in mouse hepatic thyroid hormone transporter expression with age and hyperthyroidism. Eur Thyroid J 4:81–86CrossRefGoogle Scholar
  21. Fang Q, Longo-Guess C, Gagnon LH, Mortensen AH, Dolan DF, Camper SA, Johnson KR (2011) A modifier gene alleviates hypothyroidism-induced hearing impairment in Pou1f1 dw dwarf mice. Genetics 189:665–673CrossRefGoogle Scholar
  22. Fang Q, Giordimaina AM, Dolan DF, Camper SA, Mustapha M (2012) Genetic background of Prop1(df) mutants provides remarkable protection against hypothyroidism-induced hearing impairment. J Assoc Res Otolaryngol 13:173–184CrossRefGoogle Scholar
  23. Forrest D, Reh TA, Rusch A (2002) Neurodevelopmental control by thyroid hormone receptors. Curr Opin Neurobiol 12:49–56CrossRefGoogle Scholar
  24. Fugazzola L, Muzza M, Weber G, Beck-Peccoz P, Persani L (2011) DUOXS defects: genotype-phenotype correlations. Ann Endocrinol (Paris) 72:82–86CrossRefGoogle Scholar
  25. Furlan LL, Marson FA, Ribeiro JD, Bertuzzo CS, Salomao Junior JB, Souza DR (2016) IL8 gene as modifier of cystic fibrosis: unraveling the factors which influence clinical variability. Hum Genet 135:881–894CrossRefGoogle Scholar
  26. Gage PJ, Brinkmeier ML, Scarlett LM, Knapp LT, Camper SA, Mahon KA (1996) The Ames dwarf gene, df, is required early in pituitary ontogeny for the extinction of Rpx transcription and initiation of lineage-specific cell proliferation. Mol Endocrinol 10:1570–1581Google Scholar
  27. Geister KA, Brinkmeier ML, Cheung LY, Wendt J, Oatley MJ, Burgess DL, Kozloff KM, Cavalcoli JD, Oatley JM, Camper SA (2015) LINE-1 mediated insertion into Poc1a (Protein of Centriole 1 A) causes growth insufficiency and male infertility in mice. PLoS Genet 11:e1005569CrossRefGoogle Scholar
  28. Glinoer D, Delange F (2000) The potential repercussions of maternal, fetal, and neonatal hypothyroxinemia on the progeny. Thyroid 10:871–887CrossRefGoogle Scholar
  29. Grasberger H, Refetoff S (2006) Identification of the maturation factor for dual oxidase. Evolution of an eukaryotic operon equivalent. J Biol Chem 281:18269–18272CrossRefGoogle Scholar
  30. Grasberger H, De Deken X, Mayo OB, Raad H, Weiss M, Liao XH, Refetoff S (2012) Mice deficient in dual oxidase maturation factors are severely hypothyroid. Mol Endocrinol 26:481–492CrossRefGoogle Scholar
  31. Grubb SC, Maddatu TP, Bult CJ, Bogue MA (2009) Mouse phenome database. Nucleic Acids Res 37:D720–D730CrossRefGoogle Scholar
  32. Haddow JE, Palomaki GE, Allan WC, Williams JR, Knight GJ, Gagnon J, O’Heir CE, Mitchell ML, Hermos RJ, Waisbren SE, Faix JD, Klein RZ (1999) Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N Engl J Med 341:549–555CrossRefGoogle Scholar
  33. Hamilton BA, Yu BD (2012) Modifier genes and the plasticity of genetic networks in mice. PLoS Genet 8:e1002644CrossRefGoogle Scholar
  34. Hanken J, Thorogood P (1993) Evolution and development of the vertebrate skull: the role of pattern formation. Trends Ecol Evol 8:9–15CrossRefGoogle Scholar
  35. Hardisty RE, Erven A, Logan K, Morse S, Guionaud S, Sancho-Oliver S, Hunter AJ, Brown SD, Steel KP (2003) The deaf mouse mutant Jeff (Jf) is a single gene model of otitis media. J Assoc Res Otolaryngol 4:130–138CrossRefGoogle Scholar
  36. Hosoda Y, Sasaki N, Kameda Y, Torigoe D, Agui T (2012) Identifying quantitative trait loci affecting resistance to congenital hypothyroidism in 129/SvJcl strain mice. PLoS ONE 7:e31035CrossRefGoogle Scholar
  37. Huangfu M, Saunders JC (1983) Auditory development in the mouse: structural maturation of the middle ear. J Morphol 176:249–259CrossRefGoogle Scholar
  38. Ikeda A, Zheng QY, Zuberi AR, Johnson KR, Naggert JK, Nishina PM (2002) Microtubule-associated protein 1A is a modifier of tubby hearing (moth1). Nat Genet 30:401–405CrossRefGoogle Scholar
  39. Jaskoll TF, Maderson PF (1978) A histological study of the development of the avian middle ear and tympanum. Anat Rec 190:177–199CrossRefGoogle Scholar
  40. Johnson KR, Zheng QY, Weston MD, Ptacek LJ, Noben-Trauth K (2005) The Mass1frings mutation underlies early onset hearing impairment in BUB/BnJ mice, a model for the auditory pathology of Usher syndrome IIC. Genomics 85:582–590CrossRefGoogle Scholar
  41. Johnson KR, Zheng QY, Noben-Trauth K (2006) Strain background effects and genetic modifiers of hearing in mice. Brain Res 1091:79–88CrossRefGoogle Scholar
  42. Johnson KR, Marden CC, Ward-Bailey P, Gagnon LH, Bronson RT, Donahue LR (2007) Congenital hypothyroidism, dwarfism, and hearing impairment caused by a missense mutation in the mouse dual oxidase 2 gene, Duox2. Mol Endocrinol 21:1593–1602CrossRefGoogle Scholar
  43. Jump DB, Narayan P, Towle H, Oppenheimer JH (1984) Rapid effects of triiodothyronine on hepatic gene expression. Hybridization analysis of tissue-specific triiodothyronine regulation of mRNAS14. J Biol Chem 259:2789–2797Google Scholar
  44. Kallman JC, Phillips JO, Bramhall NF, Kelly JP, Street VA (2008) In search of the DFNA11 myosin VIIA low- and mid-frequency auditory genetic modifier. Otol Neurotol 29:860–867CrossRefGoogle Scholar
  45. 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 18:596–608CrossRefGoogle Scholar
  46. Keane TM, Goodstadt L, Danecek P, White MA, Wong K, Yalcin B, Heger A, Agam A, Slater G, Goodson M, Furlotte NA, Eskin E, Nellaker C, Whitley H, Cleak J, Janowitz D, Hernandez-Pliego P, Edwards A, Belgard TG, Oliver PL, McIntyre RE, Bhomra A, Nicod J, Gan X, Yuan W, van der Weyden L, Steward CA, Bala S, Stalker J, Mott R, Durbin R, Jackson IJ, Czechanski A, Guerra-Assuncao JA, Donahue LR, Reinholdt LG, Payseur BA, Ponting CP, Birney E, Flint J, Adams DJ (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477:289–294CrossRefGoogle Scholar
  47. 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 83:3101–3112CrossRefGoogle Scholar
  48. Kousi M, Katsanis N (2015) Genetic modifiers and oligogenic inheritance. Cold Spring Harb Perspect Med 5:a017145CrossRefGoogle Scholar
  49. Kumar P, Henikoff S, Ng PC (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4:1073–1081CrossRefGoogle Scholar
  50. Lavado-Autric R, Auso E, Garcia-Velasco JV, Arufe Mdel C, Escobar del Rey F, Berbel P, Morreale de Escobar G (2003) Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J Clin Invest 111:1073–1082CrossRefGoogle Scholar
  51. Lazarus JH, Bestwick JP, Channon S, Paradice R, Maina A, Rees R, Chiusano E, John R, Guaraldo V, George LM, Perona M, Dall’Amico D, Parkes AB, Joomun M, Wald NJ (2012) Antenatal thyroid screening and childhood cognitive function. N Engl J Med 366:493–501CrossRefGoogle Scholar
  52. Li S, Crenshaw EB 3rd, Rawson EJ, Simmons DM, Swanson LW, Rosenfeld MG (1990) Dwarf locus mutants lacking three pituitary cell types result from mutations in the POU-domain gene Pit-1. Nature 347:528–533CrossRefGoogle Scholar
  53. Li D, Henley CM, O’Malley BW Jr (1999) Distortion product otoacoustic emissions and outer hair cell defects in the hyt/hyt mutant mouse. Hear Res 138:65–72CrossRefGoogle Scholar
  54. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408CrossRefGoogle Scholar
  55. Marovitz WF, Berryhill BH, Peterson RR (1968) Disruptions of bony labyrinth, ossicular chain and tympanic bullae in dwarf mice. Laryngoscope 78:863–872CrossRefGoogle Scholar
  56. Moore JK, Linthicum FH Jr (2007) The human auditory system: a timeline of development. Int J Audiol 46:460–478CrossRefGoogle Scholar
  57. Mortensen AH, Schade V, Lamonerie T, Camper SA (2015) Deletion of OTX2 in neural ectoderm delays anterior pituitary development. Hum Mol Genet 24:939–953CrossRefGoogle Scholar
  58. 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 Pit1 dw mutants. J Neurosci 29:1212–1223CrossRefGoogle Scholar
  59. Napiontek U, Borck G, Muller-Forell W, Pfarr N, Bohnert A, Keilmann A, Pohlenz J (2004) Intrafamilial variability of the deafness and goiter phenotype in Pendred syndrome caused by a T416P mutation in the SLC26A4 gene. J Clin Endocrinol Metab 89:5347–5351CrossRefGoogle Scholar
  60. Ng L, Kelley MW, Forrest D (2013) Making sense with thyroid hormone-the role of T3 in auditory development. Nat Rev Endocrinol 9:296–307CrossRefGoogle Scholar
  61. Nicholas AK, Serra EG, Cangul H, Alyaarubi S, Ullah I, Schoenmakers E, Deeb A, Habeb AM, Almaghamsi M, Peters C, Nathwani N, Aycan Z, Saglam H, Bober E, Dattani M, Shenoy S, Murray PG, Babiker A, Willemsen R, Thankamony A, Lyons G, Irwin R, Padidela R, Tharian K, Davies JH, Puthi V, Park SM, Massoud AF, Gregory JW, Albanese A, Pease-Gevers E, Martin H, Brugger K, Maher ER, Chatterjee VK, Anderson CA, Schoenmakers N (2016) Comprehensive screening of eight known causative genes in congenital hypothyroidism with gland-in-situ. J Clin Endocrinol Metab 101:4521–4531CrossRefGoogle Scholar
  62. Niu H, Li X, Makmura L, Friedman RA (2008) Mapping of genetic modifiers of Eya1 (bor/bor) in CAST/EiJ and BALB/cJ that suppress cochlear aplasia and associated deafness. Mamm Genome 19:634–639CrossRefGoogle Scholar
  63. Noben-Trauth K, Zheng QY, Johnson KR, Nishina PM (1997) mdfw: a deafness susceptibility locus that interacts with deaf waddler (dfw). Genomics 44:266–272CrossRefGoogle Scholar
  64. Noben-Trauth K, Zheng QY, Johnson KR (2003) Association of cadherin 23 with polygenic inheritance and genetic modification of sensorineural hearing loss. Nat Genet 35:21–23CrossRefGoogle Scholar
  65. Pascarella A, Ferrandino G, Credendino SC, Moccia C, D’Angelo F, Miranda B, D’Ambrosio C, Bielli P, Spadaro O, Ceccarelli M, Scaloni A, Sette C, De Felice M, De Vita G, Amendola E (2018) DNAJC17 is localized in nuclear speckles and interacts with splicing machinery components. Sci Rep 8:7794CrossRefGoogle Scholar
  66. Pine-Twaddell E, Romero CJ, Radovick S (2013) Vertical transmission of hypopituitarism: critical importance of appropriate interpretation of thyroid function tests and levothyroxine therapy during pregnancy. Thyroid 23:892–897CrossRefGoogle Scholar
  67. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A (2010) Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res 20:110–121CrossRefGoogle Scholar
  68. Postiglione MP, Parlato R, Rodriguez-Mallon A, Rosica A, Mithbaokar P, Maresca M, Marians RC, Davies TF, Zannini MS, De Felice M, Di Lauro R (2002) Role of the thyroid-stimulating hormone receptor signaling in development and differentiation of the thyroid gland. Proc Natl Acad Sci USA 99:15462–15467CrossRefGoogle Scholar
  69. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575CrossRefGoogle Scholar
  70. Richter CA, Amin S, Linden J, Dixon J, Dixon MJ, Tucker AS (2010) Defects in middle ear cavitation cause conductive hearing loss in the Tcof1 mutant mouse. Hum Mol Genet 19:1551–1560CrossRefGoogle Scholar
  71. Rovet J, Daneman D (2003) Congenital hypothyroidism: a review of current diagnostic and treatment practices in relation to neuropsychologic outcome. Paediatr Drugs 5:141–149CrossRefGoogle Scholar
  72. Rovet JF, Ehrlich R (2000) Psychoeducational outcome in children with early-treated congenital hypothyroidism. Pediatrics 105:515–522CrossRefGoogle Scholar
  73. 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 21:9792–9800CrossRefGoogle Scholar
  74. Rye MS, Bhutta MF, Cheeseman MT, Burgner D, Blackwell JM, Brown SD, Jamieson SE (2011) Unraveling the genetics of otitis media: from mouse to human and back again. Mamm Genome 22:66–82CrossRefGoogle Scholar
  75. Salvatore G, Edelhoch H (1973) Chemistry and biosynthesis of thyroid Iodoproteins. In: Li CH (ed) Hormonal proteins and pepetides. Academic Press, New York, pp 201–244CrossRefGoogle Scholar
  76. Sasaki N, Hosoda Y, Nagata A, Ding M, Cheng JM, Miyamoto T, Okano S, Asano A, Miyoshi I, Agui T (2007) A mutation in Tpst2 encoding tyrosylprotein sulfotransferase causes dwarfism associated with hypothyroidism. Mol Endocrinol 21:1713–1721CrossRefGoogle Scholar
  77. Schultz JM, Yang Y, Caride AJ, Filoteo AG, Penheiter AR, Lagziel A, Morell RJ, Mohiddin SA, Fananapazir L, Madeo AC, Penniston JT, Griffith AJ (2005) Modification of human hearing loss by plasma-membrane calcium pump PMCA2. N Engl J Med 352:1557–1564CrossRefGoogle Scholar
  78. Seelig S, Liaw C, Towle HC, Oppenheimer JH (1981) Thyroid hormone attenuates and augments hepatic gene expression at a pretranslational level. Proc Natl Acad Sci USA 78:4733–4737CrossRefGoogle Scholar
  79. Sofia VM, Da Sacco L, Surace C, Tomaiuolo AC, Genovese S, Grotta S, Gnazzo M, Petrocchi S, Ciocca L, Alghisi F, Montemitro E, Martemucci L, Elce A, Lucidi V, Castaldo G, Angioni A (2016) Extensive molecular analysis suggested the strong genetic heterogeneity of idiopathic chronic pancreatitis. Mol Med 22:300CrossRefGoogle Scholar
  80. Sornson MW, Wu W, Dasen JS, Flynn SE, Norman DJ, O’Connell SM, Gukovsky I, Carriere C, Ryan AK, Miller AP, Zuo L, Gleiberman AS, Andersen B, Beamer WG, Rosenfeld MG (1996) Pituitary lineage determination by the Prophet of Pit-1 homeodomain factor defective in Ames dwarfism. Nature 384:327–333CrossRefGoogle Scholar
  81. Sprenkle PM, McGee J, Bertoni JM, Walsh EJ (2001) Consequences of hypothyroidism on auditory system function in Tshr mutant (hyt) mice. J Assoc Res Otolaryngol 2:312–329CrossRefGoogle Scholar
  82. Stoppa-Vaucher S, Van Vliet G, Deladoey J (2011) Variation by ethnicity in the prevalence of congenital hypothyroidism due to thyroid dysgenesis. Thyroid 21:13–18CrossRefGoogle Scholar
  83. Strug LJ, Gonska T, He G, Keenan K, Ip W, Boelle PY, Lin F, Panjwani N, Gong J, Li W, Soave D, Xiao B, Tullis E, Rabin H, Parkins MD, Price A, Zuberbuhler PC, Corvol H, Ratjen F, Sun L, Bear CE, Rommens JM (2016) Cystic fibrosis gene modifier SLC26A9 modulates airway response to CFTR-directed therapeutics. Hum Mol Genet 25:4590–4600Google Scholar
  84. Sundaresan S, Kong JH, Fang Q, Salles FT, Wangsawihardja F, Ricci AJ, Mustapha M (2016) Thyroid hormone is required for pruning, functioning and long-term maintenance of afferent inner hair cell synapses. Eur J Neurosci 43:148–161CrossRefGoogle Scholar
  85. Uziel A (1986) Periods of sensitivity to thyroid hormone during the development of the organ of Corti. Acta Otolaryngol Suppl 429:23–27CrossRefGoogle Scholar
  86. Uziel A, Legrand C, Ohresser M, Marot M (1983) Maturational and degenerative processes in the organ of Corti after neonatal hypothyroidism. Hear Res 11:203–218CrossRefGoogle Scholar
  87. van der Spek AH, Fliers E, Boelen A (2017) The classic pathways of thyroid hormone metabolism. Mol Cell Endocrinol 458:29–38CrossRefGoogle Scholar
  88. Vanderschueren-Lodeweyckx M, Debruyne F, Dooms L, Eggermont E, Eeckels R (1983) Sensorineural hearing loss in sporadic congenital hypothyroidism. Arch Dis Child 58:419–422CrossRefGoogle Scholar
  89. Vesper AH, Raetzman LT, Camper SA (2006) Role of prophet of Pit1 (PROP1) in gonadotrope differentiation and puberty. Endocrinology 147:1654–1663CrossRefGoogle Scholar
  90. Vigone MC, Fugazzola L, Zamproni I, Passoni A, Di Candia S, Chiumello G, Persani L, Weber G (2005) Persistent mild hypothyroidism associated with novel sequence variants of the DUOX2 gene in two siblings. Hum Mutat 26:395CrossRefGoogle Scholar
  91. Weber G, Rabbiosi S, Zamproni I, Fugazzola L (2013) Genetic defects of hydrogen peroxide generation in the thyroid gland. J Endocrinol Invest 36:261–266Google Scholar
  92. White KR (2004) Early hearing detection and intervention programs: opportunities for genetic services. Am J Med Genet A 130A:29–36CrossRefGoogle Scholar
  93. Yan D, Liu XZ (2010) Modifiers of hearing impairment in humans and mice. Curr Genom 11:269–278CrossRefGoogle Scholar
  94. Zheng X, Ma SG, Guo ML, Qiu YL, Yang LX (2017) Compound Heterozygous mutations in the DUOX2/DUOXA2 genes cause congenital hypothyroidism. Yonsei Med J 58:888–890CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Amanda H. Mortensen
    • 1
  • Qing Fang
    • 1
  • Michelle T. Fleming
    • 1
  • Thomas J. Jones
    • 1
  • Alexandre Z. Daly
    • 1
  • Kenneth R. Johnson
    • 2
  • Sally A. Camper
    • 1
    Email author
  1. 1.Department of Human GeneticsUniversity of MichiganAnn ArborUSA
  2. 2.The Jackson LaboratoryBar HarborUSA

Personalised recommendations