Identification of allelic variants of pendrin (SLC26A4) with loss and gain of function

Cellular Physiology and Biochemistry

Volumn 28, Issue 3, 2011, Pages 467-476

  Dossena, Silvia ^a   Bizhanova, Aigerim ^b   Nofziger, Charity ^a   Bernardinelli, Emanuele ^a   Ramsauer, Josef ^a   Kopp, Peter ^b   Paulmichl, Markus ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Asthma; Functional tests; Hypertension; Inherited hearing loss; Pendred syndrome; Pendrin

Indexed keywords

CHLORIDE ION; COMPLEMENTARY DNA; IODIDE; IODINE 125; PENDRIN; SODIUM IODIDE SYMPORTER;

AIRWAY; ALLELE; ARTICLE; ASTHMA; CELL PH; CELL STRAIN HEK293; CHRONIC OBSTRUCTIVE LUNG DISEASE; COHORT ANALYSIS; CONTROLLED STUDY; FLUOROMETRY; FUNCTION TEST; GENE MUTATION; HEARING LOSS; HUMAN; HUMAN CELL; HYPERTENSION; INNER EAR; ION TRANSPORT; ISOTOPE LABELING; KIDNEY; MAJOR CLINICAL STUDY; PATHOGENESIS; PENDRED SYNDROME; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; VESTIBULE AQUEDUCT;

EID: 82255167145     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000335108     Document Type: Article

References (51)

1. Soleimani M, Greeley T, Petrovic S, Wang Z, Amlal H, Kopp P, Burnham CE: Pendrin: an apical Cl-/OH-/HCO3-exchanger in the kidney cortex. Am J Physiol Renal Physiol 2001;280:F356-F364.
2. Shcheynikov N, Yang D, Wang Y, Zeng W, Karniski LP, So I, Wall SM, Muallem S: The Slc26a4 transporter functions as an electroneutral Cl-/I-/HCO3-exchanger: role of Slc26a4 and Slc26a6 in I-and HCO3-secretion and in regulation of CFTR in the parotid duct. J Physiol 2008;586:3813-3824.
3. Royaux IE, Suzuki K, Mori A, Katoh R, Everett LA, Kohn LD, Green ED: 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. (Pubitemid 32250509)
4. Yoshida A, Hisatome I, Taniguchi S, Sasaki N, Yamamoto Y, Miake J, Fukui H, Shimizu H, Okamura T, Okura T, Igawa O, Shigemasa C, Green ED, Kohn LD, Suzuki K: Mechanism of iodide/chloride exchange by pendrin. Endocrinology 2004;145:4301-4308. (Pubitemid 39120580)
5. Yoshida A, Taniguchi S, Hisatome I, Royaux IE, Green ED, Kohn LD, Suzuki K: Pendrin is an iodide-specific apical porter responsible for iodide efflux from thyroid cells. J Clin Endocrinol Metab 2002;87:3356-3361. (Pubitemid 34816389)
6. Kopp P, Bizhanova A: Clinical and molecular characteristics of Pendred syndrome. Ann Endocrinol (Paris) 2011;72:88-94.
7. Kim HM, Wangemann P: Epithelial cell stretching and luminal acidification lead to a retarded development of stria vascularis and deafness in mice lacking pendrin. PLoS One 2011;6:e17949.
8. Nakaya K, Harbidge DG, Wangemann P, Schultz BD, Green ED, Wall SM, Marcus DC: 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. (Pubitemid 46701858)
9. Wangemann P, Nakaya K, Wu T, Maganti RJ, Itza EM, Sanneman JD, Harbidge DG, Billings S, Marcus DC: 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. (Pubitemid 46701861)
10. Everett LA, Glaser B, Beck JC, Idol JR, Buchs A, Heyman M, Adawi F, Hazani E, Nassir E, Baxevanis AD, Sheffield VC, Green ED: Pendred syndrome is caused by mutations in a putative sulphate transporter gene (PDS). Nat Genet 1997;17:411-422. (Pubitemid 27518389)
11. Bizhanova A, Kopp P: Genetics and phenomics of Pendred syndrome. Mol Cell Endocrinol 2010;322:83-90.
12. Kopp P, Pesce L, Solis-S JC: Pendred syndrome and iodide transport in the thyroid. Trends Endocrinol Metab 2008;19:260-268.
13. Fugazzola L, Mannavola D, Cerutti N, Maghnie M, Pagella F, Bianchi P, Weber G, Persani L, Beck-Peccoz P: 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. (Pubitemid 32269202)
14. Choi BY, Stewart AK, Madeo AC, Pryor SP, Lenhard S, Kittles R, Eisenman D, Kim HJ, Niparko J, Thomsen J, Arnos KS, Nance WE, King KA, Zalewski CK, Brewer CC, Shawker T, Reynolds JC, Butman JA, Karniski LP, Alper SL, Griffith AJ: Hypo-functional SLC26A4 variants associated with nonsyndromic hearing loss and enlargement of the vestibular aqueduct: genotype-phenotype correlation or coincidental polymorphisms? Hum Mutat 2009;30:599-608.
15. Pryor SP, Madeo AC, Reynolds JC, Sarlis NJ, Arnos KS, Nance WE, Yang Y, Zalewski CK, Brewer CC, Butman JA, Griffith AJ: SLC26A4/PDS genotypephenotype 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. (Pubitemid 40204371)
16. Albert S, Blons H, Jonard L, Feldmann D, Chauvin P, Loundon N, Sergent-Allaoui A, Houang M, Joannard A, Schmerber S, Delobel B, Leman J, Journel H, Catros H, Dollfus H, Eliot MM, David A, Calais C, Drouin-Garraud V, Obstoy MF, Tran Ba HP, Lacombe D, Duriez F, Francannet C, Bitoun P, Petit C, Garabedian EN, Couderc R, Marlin S, Denoyelle F: SLC26A4 gene is frequently involved in nonsyndromic hearing impairment with enlarged vestibular aqueduct in Caucasian populations. Eur J Hum Genet 2006;14:773-779. (Pubitemid 43797276)
17. Royaux IE, Wall SM, Karniski LP, Everett LA, Suzuki K, Knepper MA, Green ED: Pendrin, encoded by the Pendred syndrome gene, resides in the apical region of renal intercalated cells and mediates bicarbonate secretion. Proc Natl Acad Sci USA 2001;98:4221-4226. (Pubitemid 32249925)
18. Wall SM, Hassell KA, Royaux IE, Green ED, Chang JY, Shipley GL, Verlander JW: Localization of pendrin in mouse kidney. Am J Physiol Renal Physiol 2003;284:F229-F241. (Pubitemid 35471303)
19. Amlal H, Petrovic S, Xu J, Wang Z, Sun X, Barone S, Soleimani M: Deletion of the anion exchanger Slc26a4 (pendrin) decreases apical Cl-/HCO3-exchanger activity and impairs bicarbonate secretion in kidney collecting duct. Am J Physiol Cell Physiol 2010;299:C33-C41.
20. Wall SM, Pech V: Pendrin and sodium channels: relevance to hypertension. J Nephrol 2010;23:S118-S123.
21. Verlander JW, Hassell KA, Royaux IE, Glapion DM, Wang ME, Everett LA, Green ED, Wall SM: Deoxycorticosterone upregulates PDS (Slc26a4) in mouse kidney: role of pendrin in mineralocorticoid-induced hypertension. Hypertension 2003;42:356-362. (Pubitemid 37093485)
22. Pech V, Kim YH, Weinstein AM, Everett LA, Pham TD, Wall SM: Angiotensin II increases chloride absorption in the cortical collecting duct in mice through a pendrin-dependent mechanism. Am J Physiol Renal Physiol 2007;292:F914-F920. (Pubitemid 46393416)
23. Kim YH, Pech V, Spencer KB, Beierwaltes WH, Everett LA, Green ED, Shin W, Verlander JW, Sutliff RL, Wall SM: Reduced ENaC protein abundance contributes to the lower blood pressure observed in pendrin-null mice. Am J Physiol Renal Physiol 2007;293:F1314-F1324. (Pubitemid 47583967)
24. Eladari D, Chambrey R, Frische S, Vallet M, Edwards A: Pendrin as a regulator of ECF and blood pressure. Curr Opin Nephrol Hypertens 2009;18:356-362.
25. Kuperman DA, Lewis CC, Woodruff PG, Rodriguez MW, Yang YH, Dolganov GM, Fahy JV, Erle DJ: Dissecting asthma using focused transgenic modeling and functional genomics. J Allergy Clin Immunol 2005;116:305-311. (Pubitemid 41096536)
26. Nakao I, Kanaji S, Ohta S, Matsushita H, Arima K, Yuyama N, Yamaya M, Nakayama K, Kubo H, Watanabe M, Sagara H, Sugiyama K, Tanaka H, Toda S, Hayashi H, Inoue H, Hoshino T, Shiraki A, Inoue M, Suzuki K, Aizawa H, Okinami S, Nagai H, Hasegawa M, Fukuda T, Green ED, Izuhara K: Identification of pendrin as a common mediator for mucus production in bronchial asthma and chronic obstructive pulmonary disease. J Immunol 2008;180:6262-6269.
27. Nakagami Y, Favoreto S Jr, Zhen G, Park SW, Nguyenvu LT, Kuperman DA, Dolganov GM, Huang X, Boushey HA, Avila PC, Erle DJ: The epithelial anion transporter pendrin is induced by allergy and rhinovirus infection, regulates airway surface liquid, and increases airway reactivity and inflammation in an asthma model. J Immunol 2008;181:2203-2210.
28. Di Valentin E, Crahay C, Garbacki N, Hennuy B, Gueders M, Noel A, Foidart JM, Grooten J, Colige A, Piette J, Cataldo D: New asthma biomarkers: lessons from murine models of acute and chronic asthma. Am J Physiol Lung Cell Mol Physiol 2009;296:L185-L197.
29. Pedemonte N, Caci E, Sondo E, Caputo A, Rhoden K, Pfeffer U, Di CM, Bandettini R, Ravazzolo R, Zegarra-Moran O, Galietta LJ: Thiocyanate transport in resting and IL-4-stimulated human bronchial epithelial cells: role of pendrin and anion channels. J Immunol 2007;178:5144-5153. (Pubitemid 46595298)
30. Nofziger C, Vezzoli V, Dossena S, Schonherr T, Studnicka J, Nofziger J, Vanoni S, Stephan S, Silva M, Meyer G, Paulmichl M: STAT6 Links IL-4/IL-13 Stimulation With Pendrin Expression in Asthma and Chronic Obstructive Pulmonary Disease. Clin Pharmacol Ther 2011;90:399-405.
31. Taylor JP, Metcalfe RA, Watson PF, Weetman AP, Trembath RC: 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. (Pubitemid 34615268)
32. Dossena S, Nofziger C, Tamma G, Bernardinelli E, Vanoni S, Nowak C, Grabmayer E, Koessler S, Stephan S, Patsch W, Paulmichl M: Molecular and functional characterization of human pendrin and its allelic variants. Cell Physiol Biochem 2011;28:451-466.
33. Fugazzola L, Cerutti N, Mannavola D, Crino A, Cassio A, Gasparoni P, Vannucchi G, Beck-Peccoz P: Differential diagnosis between Pendred and pseudo-Pendred syndromes: clinical, radiologic, and molecular studies. Pediatr Res 2002;51:479-484. (Pubitemid 34267319)
34. Kara C, Kilic M, Ucakturk A, Aydin M: Congenital goitrous hypothyroidism, deafness and iodide organification defect in four siblings: pendred or pseudo-pendred syndrome? J Clin Res Pediatr Endocrinol 2010;2:81-84.
35. Davis N, Lunardi C, Shield JP: Sensorineural deafness and hypothyroidism: autoimmunity causing 'pseudo-Pendred syndrome'. Horm Res 2006;65:267-268. (Pubitemid 43876728)
36. Pfarr N, Borck G, Turk A, Napiontek U, Keilmann A, Muller-Forell W, Kopp P, Pohlenz J: Goitrous congenital hypothyroidism and hearing impairment associated with mutations in the TPO and SLC26A4/PDS genes. J Clin Endocrinol Metab 2006;91:2678-2681. (Pubitemid 44024636)
37. Pera A, Dossena S, Rodighiero S, Gandia M, Botta G, Meyer G, Moreno F, Nofziger C, Hernandez-Chico C, Paulmichl M: Functional assessment of allelic variants in the SLC26A4 gene involved in Pendred syndrome and nonsyndromic EVA. Proc Natl Acad Sci USA 2008;105:18608-18613.
38. Galietta LJ, Haggie PM, Verkman AS: Green fluorescent protein-based halide indicators with improved chloride and iodide affinities. FEBS Lett 2001;499:220-224. (Pubitemid 32553868)
39. DiCiommo DP, Duckett A, Burcescu I, Bremner R, Gallie BL: Retinoblastoma protein purification and transduction of retina and retinoblastoma cells using improved alphavirus vectors. Invest Ophthalmol Vis Sci 2004;45:3320-3329. (Pubitemid 39121872)
40. Dossena S, Rodighiero S, Vezzoli V, Nofziger C, Salvioni E, Boccazzi M, Grabmayer E, Botta G, Meyer G, Fugazzola L, Beck-Peccoz P, Paulmichl M: Functional characterization of wild-type and mutated pendrin (SLC26A4), the anion transporter involved in Pendred syndrome. J Mol Endocrinol 2009;43:93-103.
41. Dossena S, Rodighiero S, Vezzoli V, Bazzini C, Sironi C, Meyer G, Furst J, Ritter M, Garavaglia ML, Fugazzola L, Persani L, Zorowka P, Storelli C, Beck-Peccoz P, Botta G, Paulmichl M: Fast fluorometric method for measuring pendrin (SLC26A4) Cl-/I-transport activity. Cell Physiol Biochem 2006;18:67-74.
42. Dror AA, Politi Y, Shahin H, Lenz DR, Dossena S, Nofziger C, Fuchs H, Hrabe de AM, Paulmichl M, Weiner S, Avraham KB: Calcium oxalate stone formation in the inner ear as a result of an Slc26a4 mutation. J Biol Chem 2010;285:21724-21735.
43. Fugazzola L, Cirello V, Dossena S, Rodighiero S, Muzza M, Castorina P, Lalatta F, Ambrosetti U, Beck-Peccoz P, Botta G, Paulmichl M: High phenotypic intrafamilial variability in patients with Pendred syndrome and a novel duplication in the SLC26A4 gene: clinical characterization and functional studies of the mutated SLC26A4 protein. Eur J Endocrinol 2007;157:331-338. (Pubitemid 47603538)
44. Scott DA, Wang R, Kreman TM, Sheffield VC, Karniski LP: The Pendred syndrome gene encodes a chloride-iodide transport protein. Nat Genet 1999;21:440-443. (Pubitemid 29159585)
45. Gillam MP, Sidhaye AR, Lee EJ, Rutishauser J, Stephan CW, 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. (Pubitemid 38445877)
46. Gillam MP, Bartolone L, Kopp P, Benvenga S: Molecular analysis of the PDS gene in a nonconsanguineous Sicilian family with Pendred's syndrome. Thyroid 2005;15:734-741. (Pubitemid 41117528)
47. Coyle B, Reardon W, Herbrick JA, Tsui LC, Gausden E, Lee J, Coffey R, Grueters A, Grossman4 A, Phelps PD, Luxon L, Kendall-Taylor P, Scherer SW, Trembath RC: Molecular analysis of the PDS gene in Pendred syndrome. Hum Mol Genet 1998;7:1105-1112.
48. Blons H, Feldmann D, Duval V, Messaz O, Denoyelle F, Loundon N, Sergout-Allaoui A, Houang M, Duriez F, Lacombe D, Delobel B, Leman J, Catros H, Journel H, Drouin-Garraud V, Obstoy MF, Toutain A, Oden S, Toublanc JE, Couderc R, Petit C, Garabedian EN, Marlin S: Screening of SLC26A4 (PDS) gene in Pendred's syndrome: a large spectrum of mutations in France and phenotypic heterogeneity. Clin Genet 2004;66:333-340. (Pubitemid 39317635)
49. Dai P, Stewart AK, Chebib F, Hsu A, Rozenfeld J, Huang D, Kang D, Lip V, Fang H, Shao H, Liu X, Yu F, Yuan H, Kenna M, Miller DT, Shen Y, Yang W, Zelikovic I, Platt OS, Han D, Alper SL, Wu BL: Distinct and novel SLC26A4/Pendrin mutations in Chinese and U.S. patients with nonsyndromic hearing loss. Physiol Genomics 2009;38:281-290.
50. Yang T, Vidarsson H, Rodrigo-Blomqvist S, Rosengren SS, Enerback S, Smith RJ: Transcriptional control of SLC26A4 is involved in Pendred syndrome and nonsyndromic enlargement of vestibular aqueduct (DFNB4). Am J Hum Genet 2007;80:1055-1063. (Pubitemid 47579342)
51. Prasad S, Kolln KA, Cucci RA, Trembath RC, Van CG, Smith RJ: Pendred syndrome and DFNB4-mutation screening of SLC26A4 by denaturing highperformance liquid chromatography and the identification of eleven novel mutations. Am J Med Genet A 2004;124A:1-9. (Pubitemid 38139809)