Clinical and molecular characteristics of Pendred syndrome;Caractéristiques cliniques et moléculaires du syndrome de Pendred

Annales d'Endocrinologie

Volumn 72, Issue 2, 2011, Pages 88-94

  Kopp, P ^a   Bizhanova, A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Deafness; Goiter; Pendred syndrome; Pendrin; SLC26A4; Thyroid hormone

Indexed keywords

IODIDE; PENDRIN;

ARTICLE; DIETARY INTAKE; GENE; GENE MUTATION; GOITER; HUMAN; HYPOTHYROIDISM; LOSS OF FUNCTION MUTATION; MISSENSE MUTATION; NONHUMAN; NONSENSE MUTATION; PATHOPHYSIOLOGY; PENDRED SYNDROME; PHENOTYPE; PROTEIN EXPRESSION; SLC26A4 GENE; THYROID FOLLICLE CELL;

ANIMALS; CHLORIDE-BICARBONATE ANTIPORTERS; EAR, INNER; ENDOLYMPH; GOITER; GOITER, NODULAR; HEARING LOSS, SENSORINEURAL; HUMANS; HYPOTHYROIDISM; IODIDES; KIDNEY; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, KNOCKOUT; MUTATION; THYROID GLAND; THYROID HORMONES;

EID: 79955709196     PISSN: 00034266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ando.2011.03.010     Document Type: Article

References (90)

1. Pendred V. Deaf-mutism and goitre. Lancet 1896, ii:532.
2. Morgans M.E., Trotter W.R. Association of congenital deafness with goitre; the nature of the thyroid defect. Lancet 1958, 1:607-609.
3. Everett L.A., Glaser B., Beck J.C., Idol J.R., Buchs A., Heyman M., et al. Pendred syndrome is caused by mutations in a putative sulphate transporter gene (PDS). Nat Genet 1997, 17:411-422.
4. Reardon W., Coffey R., Phelps P.D., Luxon L.M., Stephens D., Kendall-Taylor P., et al. Pendred syndrome--100 years of underascertainment?. QJM 1997, 90:443-447.
5. Fraser G.R. Association of congenital deafness with goitre (Pendred's Syndrome) a study of 207 families. Ann Hum Genet 1965, 28:201-249.
6. Kopp P., Pesce L., Solis S.J. Pendred syndrome and iodide transport in the thyroid. Trends Endocrinol Metab 2008, 19:260-268.
7. Cremers W.R., Bolder C., Admiraal R.J., Everett L.A., Joosten F.B., van Hauwe P., et al. Progressive sensorineural hearing loss and a widened vestibular aqueduct in Pendred syndrome. Arch Otolaryngol Head Neck Surg 1998, 124:501-505.
8. Fugazzola L., Mannavola D., Cerutti N., Maghnie M., Pagella F., Bianchi P., et al. Molecular analysis of the Pendred's syndrome gene and magnetic resonance imaging studies of the inner ear are essential for the diagnosis of true Pendred's syndrome. J Clin Endocrinol Metab 2000, 85:2469-2475.
9. Phelps P.D., Coffey R.A., Trembath R.C., Luxon L.M., Grossman A.B., Britton K.E., et al. Radiological malformations of the ear in Pendred syndrome. Clin Radiol 1998, 53:268-273.
10. Hartley G.J., Phelps P.D. The anatomical section of a boy born deaf (Mondini translation). Am J Otol 1997, 18:288-293.
11. Pryor S.P., Madeo A.C., Reynolds J.C., Sarlis N.J., Arnos K.S., Nance W.E., et al. SLC26A4/PDS genotype-phenotype correlation in hearing loss with enlargement of the vestibular aqueduct (EVA): evidence that Pendred syndrome and non-syndromic EVA are distinct clinical and genetic entities. J Med Genet 2005, 42:159-165.
12. Azaiez H., Yang T., Prasad S., Sorensen J.L., Nishimura C.J., Kimberling W.J., et al. Genotype-phenotype correlations for SLC26A4-related deafness. Hum Genet 2007, 122:451-457.
13. Pera A., Villamar M., Vinuela A., Gandia M., Meda C., Moreno F., et al. A mutational analysis of the SLC26A4 gene in Spanish hearing-impaired families provides new insights into the genetic causes of Pendred syndrome and DFNB4 hearing loss. Eur J Hum Genet 2008, 16:888-896.
14. Yang T., Vidarsson H., Rodrigo-Blomqvist S., Rosengren S.S., Enerback S., Smith R.J. Transcriptional control of SLC26A4 is involved in Pendred syndrome and nonsyndromic enlargement of vestibular aqueduct (DFNB4). Am J Hum Genet 2007, 80:1055-1063.
15. Yang T., Gurrola J.G., 2nd, Wu H., Chiu S.M., Wangemann P., et al. Mutations of KCNJ10 together with mutations of SLC26A4 cause digenic nonsyndromic hearing loss associated with enlarged vestibular aqueduct syndrome. Am J Hum Genet 2009, 84:651-657.
16. Fraser G.R., Morgans M.E., Trotter W.R. The syndrome of sporadic goitre and congenital deafness. Q J Med 1960, 29:279-295.
17. Baschieri L., Benedetti G., Deluca F., Negri M. Evaluation and limitations of the perchlorate test in the study of thyroid function. J Clin Endocrinol Metab 1963, 23:786-791.
18. Kopp P. Thyroid hormone synthesis: thyroid iodine metabolism. Wegner and Ingbar's the thyroid: a fundamental and clinical text 2005, 52-76. Lippincott, Williams & Wilkins, Philadelphia. L. Braverman, R. Utiger (Eds.).
19. Gillam M.P., Sidhaye A.R., Lee E.J., Rutishauser J., Stephan C.W., Kopp P. Functional characterization of pendrin in a polarized cell system. Evidence for pendrin-mediated apical iodide efflux. J Biol Chem 2004, 279:13004-13010.
20. Nilsson L.R., Borgfors N., Gamstorp I., Holst H.E., Liden G. Nonendemic Goitre and Deafness. Acta Paediatr 1964, 53:117-131.
21. Trotter W.R. The association of deafness with thyroid dysfunction. Br Med Bull 1960, 16:92-98.
22. Gausden E., Coyle B., Armour J.A., Coffey R., Grossman A., Fraser G.R., et al. Pendred syndrome: evidence for genetic homogeneity and further refinement of linkage. J Med Genet 1997, 34:126-129.
23. Sato E., Nakashima T., Miura Y., Furuhashi A., Nakayama A., Mori N., et al. Phenotypes associated with replacement of His by Arg in the Pendred syndrome gene. Eur J Endocrinol 2001, 145:697-703.
24. Park H.J., Lee S.J., Jin H.S., Lee J.O., Go S.H., Jang H.S., et al. Genetic basis of hearing loss associated with enlarged vestibular aqueducts in Koreans. Clin Genet 2005, 67:160-165.
25. Park H.J., Shaukat S., Liu X.Z., Hahn S.H., Naz S., Ghosh M., et al. Origins and frequencies of SLC26A4 (PDS) mutations in east and south Asians: global implications for the epidemiology of deafness. J Med Genet 2003, 40:242-248.
26. Tsukamoto K., Suzuki H., Harada D., Namba A., Abe S., Usami S. Distribution and frequencies of PDS (SLC26A4) mutations in Pendred syndrome and nonsyndromic hearing loss associated with enlarged vestibular aqueduct: a unique spectrum of mutations in Japanese. Eur J Hum Genet 2003, 11:916-922.
27. Gonzalez Trevino O., Karamanoglu Arseven O., Ceballos C.J., Vives V.I., Ramirez R.C., Gomez V.V., et al. Clinical and molecular analysis of three Mexican families with Pendred's syndrome. Eur J Endocrinol 2001, 144:585-593.
28. Sheffield V.C., Kraiem Z., Beck J.C., Nishimura D., Stone E.M., Salameh M., et al. Pendred syndrome maps to chromosome 7q21-34 and is caused by an intrinsic defect in thyroid iodine organification. Nat Genet 1996, 12:424-426.
29. Medeiros-Neto G., Stanbury J.B. Pendred's syndrome: association of congenital deafness with sporadic goiter. Inherited disorders of the thyroid system 1994, 81-105. CRC Press, Boca Raton. G. Medeiros-Neto, J.B. Stanbury (Eds.).
30. Royaux I.E., Wall S.M., Karniski L.P., Everett L.A., Suzuki K., Knepper M.A., et al. Pendrin, encoded by the Pendred syndrome gene, resides in the apical region of renal intercalated cells and mediates bicarbonate secretion. Proc Natl Acad Sci U S A 2001, 98:4221-4226.
31. Soleimani M., Greeley T., Petrovic S., Wang Z., Amlal H., Kopp P., et al. Pendrin: an apical Cl-/OH-/HCO3- exchanger in the kidney cortex. Am J Physiol Renal Physiol 2001, 280:F356-F364.
32. Verlander J.W., Hassell K.A., Royaux I.E., Glapion D.M., Wang M.E., Everett L.A., et al. Deoxycorticosterone upregulates PDS (Slc26a4) in mouse kidney: role of pendrin in mineralocorticoid-induced hypertension. Hypertension 2003, 42:356-362.
33. Wall S.M., Kim Y.H., Stanley L., Glapion D.M., Everett L.A., Green E.D., et al. NaCl restriction upregulates renal Slc26a4 through subcellular redistribution: role in Cl- conservation. Hypertension 2004, 44:982-987.
34. Wall S.M. Recent advances in our understanding of intercalated cells. Curr Opin Nephrol Hypertens 2005, 14:480-484.
35. Everett L.A., Green E.D. A family of mammalian anion transporters and their involvement in human genetic diseases. Hum Mol Genet 1999, 8:1883-1891.
36. Dawson P.A., Markovich D. Pathogenetics of the human SLC26 transporters. Curr Med Chem 2005, 12:385-396.
37. 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.
38. Hastbacka J., de la Chapelle A., Mahtani M.M., Clines G., Reeve-Daly M.P., Daly M., et al. The diastrophic dysplasia gene encodes a novel sulfate transporter: positional cloning by fine-structure linkage disequilibrium mapping. Cell 1994, 78:1073-1087.
39. Hoglund P., Haila S., Socha J., Tomaszewski L., Saarialho-Kere U., Karjalainen-Lindsberg M.L., et al. Mutations of the Down-regulated in adenoma (DRA) gene cause congenital chloride diarrhoea. Nat Genet 1996, 14:316-319.
40. Silberg D.G., Wang W., Moseley R.H., Traber P.G. The Down regulated in Adenoma (dra) gene encodes an intestine-specific membrane sulfate transport protein. J Biol Chem 1995, 270:11897-11902.
41. Kopp P. Pendred's syndrome: identification of the genetic defect a century after its recognition. Thyroid 1999, 9:65-69.
42. Satoh H., Susaki M., Shukunami C., Iyama K., Negoro T., Hiraki Y. Functional analysis of diastrophic dysplasia sulfate transporter. Its involvement in growth regulation of chondrocytes mediated by sulfated proteoglycans. J Biol Chem 1998, 273:12307-12315.
43. Scott D.A., Karniski L.P. Human pendrin expressed in Xenopus laevis oocytes mediates chloride/formate exchange. Am J Physiol Cell Physiol 2000, 278:C207-C211.
44. Royaux I.E., Suzuki K., Mori A., Katoh R., Everett L.A., Kohn L.D., et al. Pendrin, the protein encoded by the Pendred syndrome gene (PDS), is an apical porter of iodide in the thyroid and is regulated by thyroglobulin in FRTL-5 cells. Endocrinology 2000, 141:839-845.
45. Rotman-Pikielny P., Hirschberg K., Maruvada P., Suzuki K., Royaux I.E., Green E.D., et al. Retention of pendrin in the endoplasmic reticulum is a major mechanism for Pendred syndrome. Hum Mol Genet 2002, 11:2625-2633.
46. Aravind L., Koonin E.V. The STAS domain - a link between anion transporters and antisigma-factor antagonists. Curr Biol 2000, 10:R53-R55.
47. Shcheynikov N., Ko S.B., Zeng W., Choi J.Y., Dorwart M.R., Thomas P.J., et al. Regulatory interaction between CFTR and the SLC26 transporters. Novartis Found Symp 2006, 273:177-186. [discussion 186-92, 261-174].
48. Ko S.B., Zeng W., Dorwart M.R., Luo X., Kim K.H., Millen L., et al. Gating of CFTR by the STAS domain of SLC26 transporters. Nat Cell Biol 2004, 6:343-350.
49. Ko S.B., Shcheynikov N., Choi J.Y., Luo X., Ishibashi K., Thomas P.J., et al. A molecular mechanism for aberrant CFTR-dependent HCO(3)(-) transport in cystic fibrosis. EMBO J 2002, 21:5662-5672.
50. Everett L.A. New insights into the role of pendrin (SLC26A4) in inner ear fluid homeostasis. Novartis Found Symp 2006, 273:213-225. [discussion 225-30, 261-14].
51. Scott D.A., Wang R., Kreman T.M., Sheffield V.C., Karniski L.P. The Pendred syndrome gene encodes a chloride-iodide transport protein. Nat Genet 1999, 21:440-443.
52. Everett L.A., Morsli H., Wu D.K., Green E.D. Expression pattern of the mouse ortholog of the Pendred's syndrome gene (Pds) suggests a key role for pendrin in the inner ear. Proc Natl Acad Sci U S A 1999, 96:9727-9732.
53. Nakaya K., Harbidge D.G., Wangemann P., Schultz B.D., Green E.D., Wall S.M., et al. Lack of pendrin HCO3- transport elevates vestibular endolymphatic [Ca2+] by inhibition of acid-sensitive TRPV5 and TRPV6 channels. Am J Physiol Renal Physiol 2007, 292:F1314-F1321.
54. Wangemann P., Nakaya K., Wu T., Maganti R.J., Itza E.M., Sanneman J.D., et al. Loss of cochlear HCO3- secretion causes deafness via endolymphatic acidification and inhibition of Ca2+ reabsorption in a Pendred syndrome mouse model. Am J Physiol Renal Physiol 2007, 292:F1345-F1353.
55. Wangemann P., Itza E.M., Albrecht B., Wu T., Jabba S.V., Maganti R.J., et al. Loss of KCNJ10 protein expression abolishes endocochlear potential and causes deafness in Pendred syndrome mouse model. BMC Med 2004, 2:30.
56. Everett L.A., Belyantseva I.A., Noben-Trauth K., Cantos R., Chen A., Thakkar S.I., et al. Targeted disruption of mouse Pds provides insight about the inner-ear defects encountered in Pendred syndrome. Hum Mol Genet 2001, 10:153-161.
57. Hulander M., Kiernan A.E., Blomqvist S.R., Carlsson P., Samuelsson E.J., Johansson B.R., et al. Lack of pendrin expression leads to deafness and expansion of the endolymphatic compartment in inner ears of Foxi1 null mutant mice. Development 2003, 130:2013-2025.
58. Dohan O., De la Vieja A., Paroder V., Riedel C., Artani M., Reed M., et al. The sodium/iodide Symporter (NIS): characterization, regulation, and medical significance. Endocr Rev 2003, 24:48-77.
59. Wolff J. Transport of iodide and other anions in the thyroid gland. Physiol Rev 1964, 44:45-90.
60. Golstein P., Abramow M., Dumont J.E., Beauwens R. The iodide channel of the thyroid: a plasma membrane vesicle study. Am J Physiol 1992, 263:C590-C597.
61. Di Cosmo C., Liao X.H., Dumitrescu A.M., Philp N.J., Weiss R.E., Refetoff S. Mice deficient in MCT8 reveal a mechanism regulating thyroid hormone secretion. J Clin Invest 2010, 120:3377-3388.
62. Moreno J.C. Identification of novel genes involved in congenital hypothyroidism using serial analysis of gene expression. Horm Res 2003, 60(Suppl. 3):96-102.
63. Moreno J.C., Klootwijk W., van Toor H., Pinto G., D'Alessandro M., Leger A., et al. Mutations in the iodotyrosine deiodinase gene and hypothyroidism. N Engl J Med 2008, 358:1811-1818.
64. Taylor J.P., Metcalfe R.A., Watson P.F., Weetman A.P., Trembath R.C. Mutations of the PDS gene, encoding pendrin, are associated with protein mislocalization and loss of iodide efflux: implications for thyroid dysfunction in Pendred syndrome. J Clin Endocrinol Metab 2002, 87:1778-1784.
65. Yoshida A., Taniguchi S., Hisatome I., Royaux I.E., Green E.D., Kohn L.D., et al. Pendrin is an iodide-specific apical porter responsible for iodide efflux from thyroid cells. J Clin Endocrinol Metab 2002, 87:3356-3361.
66. Yoshida A., Hisatome I., Taniguchi S., Sasaki N., Yamamoto Y., Miake J., et al. Mechanism of iodide/chloride exchange by pendrin. Endocrinology 2004, 145:4301-4308.
67. Calebiro D., Porazzi P., Bonomi M., Lisi S., Grindati A., De Nittis D., et al. Absence of primary hypothyroidism and goiter in Slc26a4(-/-) mice fed on a low iodine diet. J Endocrinol Invest 2010, [Epub ahead of print].
68. Paroder V., Spencer S.R., Paroder M., Arango D., Schwartz S., Mariadason J.M., et al. Na(+)/monocarboxylate transport (SMCT) protein expression correlates with survival in colon cancer: molecular characterization of SMCT. Proc Natl Acad Sci U S A 2006, 103:7270-7275.
69. Rodriguez A.M., Perron B., Lacroix L., Caillou B., Leblanc G., Schlumberger M., et al. Identification and characterization of a putative human iodide transporter located at the apical membrane of thyrocytes. J Clin Endocrinol Metab 2002, 87:3500-3503.
70. van den Hove M.F., Croizet-Berger K., Jouret F., Guggino S.E., Guggino W.B., Devuyst O., et al. The loss of the chloride channel, ClC-5, delays apical iodide efflux and induces a euthyroid goiter in the mouse thyroid gland. Endocrinology 2006, 147:1287-1296.
71. Nilsson M., Bjorkman U., Ekholm R., Ericson L.E. Iodide transport in primary cultured thyroid follicle cells: evidence of a TSH-regulated channel mediating iodide efflux selectively across the apical domain of the plasma membrane. Eur J Cell Biol 1990, 52:270-281.
72. Weiss S.J., Philp N.J., Grollman E.F. Effect of thyrotropin on iodide efflux in FRTL-5 cells mediated by Ca2+. Endocrinology 1984, 114:1108-1113.
73. Nilsson M., Bjorkman U., Ekholm R., Ericson L.E. Polarized efflux of iodide in porcine thyrocytes occurs via a cAMP-regulated iodide channel in the apical plasma membrane. Acta Endocrinol (Copenh) 1992, 126:67-74.
74. Muscella A., Marsigliante S., Verri T., Urso L., Dimitri C., Botta G., et al. PKC-epsilon-dependent cytosol-to-membrane translocation of pendrin in rat thyroid PC Cl3 cells. J Cell Physiol 2008, 217:103-112.
75. Pesce L., Kopp P. Thyrotropin rapidly regulates pendrin membrane abundance via PKA dependent and PKC dependent pathways in rat thyroid cells 2007, 78th Annual Meeting of the American Thyroid Association, New York, NY.
76. Suzuki K., Kohn L.D. Differential regulation of apical and basal iodide transporters in the thyroid by thyroglobulin. J Endocrinol 2006, 189:247-255.
77. Suzuki K., Lavaroni S., Mori A., Ohta M., Saito J., Pietrarelli M., et al. Autoregulation of thyroid-specific gene transcription by thyroglobulin. Proc Natl Acad Sci U S A 1998, 95:8251-8256.
78. Quentin F., Chambrey R., Trinh-Trang-Tan M.M., Fysekidis M., Cambillau M., Paillard M., et al. The Cl-/HCO3- exchanger pendrin in the rat kidney is regulated in response to chronic alterations in chloride balance. Am J Physiol Renal Physiol 2004, 287:F1179-F1188.
79. Wagner C.A., Finberg K.E., Stehberger P.A., Lifton R.P., Giebisch G.H., Aronson P.S., et al. Regulation of the expression of the Cl-/anion exchanger pendrin in mouse kidney by acid-base status. Kidney Int 2002, 62:2109-2117.
80. Verlander J.W., Kim Y.H., Shin W., Pham T.D., Hassell K.A., Beierwaltes W.H., et al. Dietary Cl(-) restriction upregulates pendrin expression within the apical plasma membrane of type B intercalated cells. Am J Physiol Renal Physiol 2006, 291:F833-F839.
81. Kim Y.H., Pech V., Spencer K.B., Beierwaltes W.H., Everett L.A., Green E.D., et al. Reduced ENaC protein abundance contributes to the lower blood pressure observed in pendrin-null mice. Am J Physiol Renal Physiol 2007, 293:F1314-F1324.
82. Kopp P. Pendred syndrome: clinical characteristics and molecular basis. Curr Opin Endocrinol Diabetes 1999, 6:261-269.
83. Kopp P. Pendred's syndrome and genetic defects in thyroid hormone synthesis. Rev Endocr Metab Disord 2000, 1:109-121.
84. Campbell C., Cucci R.A., Prasad S., Green G.E., Edeal J.B., Galer C.E., et al. Pendred syndrome, DFNB4, and PDS/SLC26A4 identification of eight novel mutations and possible genotype-phenotype correlations. Hum Mutat 2001, 17:403-411.
85. Yoon J.S., Park H.J., Yoo S.Y., Namkung W., Jo M.J., Koo S.K., et al. Heterogeneity in the processing defect of SLC26A4 mutants. J Med Genet 2008, 45:411-419.
86. Ishihara K., Okuyama S., Kumano S., Iida K., Hamana H., Murakoshi M., et al. Salicylate restores transport function and anion exchanger activity of missense pendrin mutations. Hear Res 2010, 270:110-118.
87. Bidart J.M., Lacroix L., Evain-Brion D., Caillou B., Lazar V., Frydman R., et al. Expression of Na+/I- symporter and Pendred syndrome genes in trophoblast cells. J Clin Endocrinol Metab 2000, 85:4367-4372.
88. Rillema J.A., Hill M.A. Prolactin regulation of the pendrin-iodide transporter in the mammary gland. Am J Physiol Endocrinol Metab 2003, 284:E25-E28.
89. Lacroix L., Pourcher T., Magnon C., Bellon N., Talbot M., Intaraphairot T., et al. Expression of the apical iodide transporter in human thyroid tissues: a comparison study with other iodide transporters. J Clin Endocrinol Metab 2004, 89:1423-1428.
90. Pedemonte N., Caci E., Sondo E., Caputo A., Rhoden K., Pfeffer U., et al. Thiocyanate transport in resting and IL-4-stimulated human bronchial epithelial cells: role of pendrin and anion channels. J Immunol 2007, 178:5144-5153.