Functional characterization of wild-type and mutated pendrin (SLC26A4), the anion transporter involved in Pendred syndrome

Journal of Molecular Endocrinology

Volumn 43, Issue 3, 2009, Pages 93-103

  Dossena, Silvia ^a   Rodighiero, Simona ^b   Vezzoli, Valeria ^a,b   Nofziger, Charity ^a   Salvioni, Elisabetta ^a,b   Boccazzi, Marta ^a,b   Grabmayer, Elisabeth ^a   Bottà, Guido ^b   Meyer, Giuliano ^b   Fugazzola, Laura ^b,c   Beck Peccoz, Paolo ^b,c   Paulmichl, Markus ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF MILAN   (Italy)

^c IRCCS   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PRESTIN; CARRIER PROTEIN; MUTANT PROTEIN; SLC26A4 PROTEIN, HUMAN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANION TRANSPORT; BODY REGIONS; EAR; GENE FREQUENCY; GENETIC VARIABILITY; GENOTYPE; HUMAN; KIDNEY; MUTATION; NUCLEOTIDE SEQUENCE; PENDRED SYNDROME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; THYROID GLAND; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIPLE MALFORMATION SYNDROME; SYNDROME;

ABNORMALITIES, MULTIPLE; AMINO ACID SEQUENCE; GENOTYPE; HUMANS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; SYNDROME;

EID: 70350733385     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1677/JME-08-0175     Document Type: Review

References (62)

1. Aravind L & Koonin EV 2000 The STAS domain - a link between anion transporters and antisigma-factor antagonists. Current Biology 10 R53-R55.
2. Batsakis JG & Nishiyama RH 1962 Deafness with sporadic goiter. Pendred's syndrome. Archives of Otolaryngology 76 401-406.
3. Blons H, Feldmann D, Duval V, Messaz O, Denoyelle F, Loundon N, Sergout-Allaoui A, Houang M, Duriez F, Lacombe D et al. 2004 Screening of SLC26A4 (PDS) gene in Pendred's syndrome: a large spectrum of mutations in France and phenotypic heterogeneity. Clinical Genetics 66 333-340.
4. Bogazzi F, Bartalena L, Raggi F, Ultimieri F & Martino E 2000 Pendrin does not increase sulfate uptake in mammalian COS-7 cells. Journal of Endocrinological Investigation 23 170-172. (Pubitemid 30218786)
5. Campbell C, Cucci RA, Prasad S, Green GE, Edeal JB, Galer CE, Karniski LP, Sheffield VC & Smith RJ 2001 Pendred syndrome, DFNB4, and PDS/SLC26A4 identification of eight novel mutations and possible genotype-phenotype correlations. Human Mutation 17 403-411.
6. Cantone A, Wang T, Pica A, Simeoni M & Capasso G 2006 Use of transgenic mice in acid-base balance studies. Journal of Nephrology 19 S121-S127. (Pubitemid 44420097)
7. Choi B, Stewart A, Madeo A, Yang Y, Pryor S, Lenhard S, Kittles R, Eisenman D, Kim H, Niparko J et al. 2008 SLC26A4 variants associated with nonsyndromic hearing loss and enlargement of the vestibular aqueduct: genotype-phenotype correlation or coincidental polymorphisms? Human Mutation 30 599-608.
8. Dossena S, Maccagni A, Vezzoli V, Bazzini C, Garavaglia ML, Meyer G, Furst J, Ritter M, Fugazzola L, Persani L et al. 2005 The expression of wild-type pendrin (SLC26A4) in human embryonic kidney (HEK 293 Phoenix) cells leads to the activation of cationic currents. European Journal of Endocrinology 153 693-699. (Pubitemid 41672416)
9. Dossena S, Rodighiero S, Vezzoli V, Bazzini C, Sironi C, Meyer G, Furst J, Ritter M, Garavaglia ML, Fugazzola L et al. 2006a Fast fluorometric method for measuring pendrin (SLC26A4) ClK/IK transport activity. Cellular Physiology and Biochemistry 18 67-74.
10. Dossena S, Vezzoli V, Cerutti N, Bazzini C, Tosco M, Sironi C, Rodighiero S, Meyer G, Fascio U, Fürst J et al. 2006b Functional characterization of wild-type and a mutated form of SLC26A4 identified in a patient with Pendred syndrome. Cellular Physiology and Biochemistry 17 245-256. (Pubitemid 43946280)
11. Everett LA, Glaser B, Beck JC, Idol JR, Buchs A, Heyman M, Adawi F, Hazani E, Nassir E, Baxevanis AD et al. 1997 Pendred syndrome is caused by mutations in a putative sulphate transporter gene (PDS). Nature Genetics 17 411-422. (Pubitemid 27518389)
12. Everett LA, Morsli H, Wu DK & Green ED 1999 Expression pattern of the mouse ortholog of the Pendred's syndrome gene (Pds) suggests a key role for pendrin in the inner ear. PNAS 96 9727-9732. (Pubitemid 29398800)
13. Everett LA, Belyantseva IA, Noben-Trauth K, Cantos R, Chen A, Thakkar SI, Hoogstraten-Miller SL, Kachar B, Wu DK & Green ED 2001 Targeted disruption of mouse Pds provides insight about the inner-ear defects encountered in Pendred syndrome. Human Molecular Genetics 10 153-161. (Pubitemid 32098125)
14. Fraser GR 1965 Association of congenital deafness with goitre (Pendred's syndrome) a study of 207 families. Annals of Human Genetics 28 201-249.
15. Fugazzola L, Mannavola D, Cerutti N, Maghnie M, Pagella F, Bianchi P, Weber G, Persani L & Beck-Peccoz P 2000 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. Journal of Clinical Endocrinology and Metabolism 85 2469-2475. (Pubitemid 32269202)
16. Fugazzola L, Cerutti N, Mannavola D, Vannucchi G & Beck-Peccoz P 2001 The role of pendrin in iodide regulation. Experimental and Clinical Endocrinology and Diabetes 109 18-22.
17. Fugazzola L, Cirello V, Dossena S, Rodighiero S, Muzza M, Castorina P, Lalatta F, Ambrosetti U, Beck-Peccoz P, Botta G et al. 2007 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. European Journal of Endocrinology 157 331-338. (Pubitemid 47603538)
18. Gillam MP, Sidhaye AR, Lee EJ, Rutishauser J, Stephan CW & Kopp P 2004 Functional characterization of pendrin in a polarized cell system. Evidence for pendrin-mediated apical iodide efflux. Journal of Biological Chemistry 279 13004-13010. (Pubitemid 38445877)
19. Gillam MP, Bartolone L, Kopp P & Bevenga S 2005 Molecular analysis of the PDS gene in a nonconsanguineous Sicilian family with Pendred's syndrome. Thyroid 15 734-741. (Pubitemid 41117528)
20. Golstein P, Abramow M, Dumont JE & Beauwens R 1992 The iodide channel of the thyroid: a plasma membrane vesicle study. American Journal of Physiology 263 C590-C597.
21. Grimaldi R, Capuano P, Miranda N, Wagner C & Capasso G 2007 Pendrin: physiology, molecular biology and clinical importance. Giornale Italiano di Nefrologia 24 288-294.
22. Hughey RP & Kleyman TR 2007 Functional cross talk between ENaC and pendrin. American Journal of Physiology. Renal Physiology 293 F1439-F1440.
23. Illum P, Kiaer HW, Hvidberg-Hansen J & Sondergaard G 1972 Fifteen cases of Pendred's syndrome. Congenital deafness and sporadic goiter. Archives of Otolaryngology 96 297-304.
24. Kim YH, Kwon TH, Frische S, Kim J, Tisher CC, Madsen KM & Nielsen S 2002 Immunocytochemical localization of pendrin in intercalated cell subtypes in rat and mouse kidney. American Journal of Physiology. Renal Physiology 283 F744-F754.
25. Kim YH, Verlander JW, Matthews SW, Kurtz I, Shin W, Weiner ID, Everett LA, Green ED, Nielsen S & Wall SM 2005 Intercalated cell HC/OHK transporter expression is reduced in Slc26a4 null mice. American Journal of Physiology. Renal Physiology 289 F1262-F1272.
26. Ko SB, Shcheynikov N, Choi JY, Luo X, Ishibashi K, Thomas PJ, Kim JY, Kim KH, Lee MG, Naruse S et al. 2002 A molecular mechanism for aberrant CFTR-dependent HCO(3)(K) transport in cystic fibrosis. EMBO Journal 21 5662-5672.
27. KoSB,ZengW,DorwartMR,Luo X, KimKH,Millen L,Goto H,Naruse S, SoyomboA,ThomasPJ et al. 2004GatingofCFTRby the STASdomain of SLC26 transporters. Nature Cell Biology 6 343-350.
28. Kopp P, Pesce L & Solis SJ 2008 Pendred syndrome and iodide transport in the thyroid. Trends in Endocrinology and Metabolism 19 260-268.
29. Lopez-Bigas N, Rabionet R, de Cid R, Govea N, Gasparini P, Zelante L, Arbones ML & Estivill X 1999 Splice-site mutation in the PDS gene may result in intrafamilial variability for deafness in Pendred syndrome. Human Mutation 14 520-526.
30. Masmoudi S, Charfedine I, Hmani M, Grati M, Ghorbel AM, Elgaied- Boulila A, Drira M, Hardelin JP & Ayadi H 2000 Pendred syndrome: phenotypic variability in two families carrying the same PDS missense mutation. American Journal of Medical Genetics 90 38-44.
31. Mount DB & Romero MF 2004 The SLC26 gene family of multifunctional anion exchangers. Pflügers Archiv 447 710-721.
32. 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. Journal of Clinical Endocrinology and Metabolism 89 5347-5351. (Pubitemid 39518407)
33. Palos F, Garcia-Rendueles ME, Araujo-Vilar D, Obregon MJ, Calvo RM, Cameselle-Teijeiro J, Bravo SB, Perez-Guerra O, Loidi L, Czarnocka B et al. 2008 Pendred syndrome in two Galician families: insights into clinical phenotypes through cellular, genetic, and molecular studies. Journal of Clinical Endocrinology and Metabolism 93 267-277.
34. Pendred V 1896 Deaf-mutism and goiter. Lancet 148 532.
35. Pera A, Dossena S, Rodighiero S, Gandia M, Botta G, Meyer G, Moreno F, Nofziger C, Hernandez-Chico C & Paulmichl M 2008 Functional assessment of allelic variants in the SLC26A4 gene involved in Pendred syndrome and nonsyndromic EVA. PNAS 105 18608-18613.
36. Pfarr N, Borck G, Turk A, Napiontek U, Keilmann A, Muller-Forell W, Kopp P & Pohlenz J 2006 Goitrous congenital hypothyroidism and hearing impairment associated with mutations in the TPO and SLC26A4/PDS genes. Journal of Clinical Endocrinology and Metabolism 91 2678-2681. (Pubitemid 44024636)
37. Phelps PD, Coffey RA, Trembath RC, Luxon LM, Grossman AB, Britton KE, Kendall-Taylor P, Graham JM, Cadge BC, Stephens SG et al. 1998 Radiological malformations of the ear in Pendred syndrome. Clinical Radiology 53 268-273. (Pubitemid 28171170)
38. Pryor SP, Madeo AC, Reynolds JC, Sarlis NJ, Arnos KS, Nance WE, Yang Y, Zalewski CK, Brewer CC, Butman JA et al. 2005 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. Journal of Medical Genetics 42 159-165. (Pubitemid 40204371)
39. Reardon W, Coffey R, Phelps PD, Luxon LM, Stephens D, Kendall- Taylor P, Britton KE, Grossman A & Trembath R 1997 Pendred syndrome - 100 years of underascertainment? Quarterly Journal of Medicine 90 443-447.
40. Rotman-Pikielny P, Hirschberg K, Maruvada P, Suzuki K, Royaux IE, Green ED, Kohn LD, Lippincott-Schwartz J & Yen PM2002 Retention of pendrin in the endoplasmic reticulum is a major mechanism for Pendred syndrome. Human Molecular Genetics 11 2625-2633.
41. Royaux IE, Suzuki K,Mori A, Katoh R, Everett LA, Kohn LD& Green ED 2000 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 141 839-845. (Pubitemid 32250509)
42. Royaux IE, Wall SM, Karniski LP, Everett LA, Suzuki K, Knepper MA & Green ED 2001 Pendrin, encoded by the Pendred syndrome gene, resides in the apical region of renal intercalated cells and mediates bicarbonate secretion. PNAS 98 4221-4226. (Pubitemid 32249925)
43. Scott DA & Karniski LP 2000 Human pendrin expressed in Xenopus laevis oocytes mediates chloride/formate exchange. American Journal of Physiology. Cell Physiology 278 C207-C211.
44. Scott DA, Wang R, Kreman TM, Sheffield VC & Karniski LP 1999 The Pendred syndrome gene encodes a chloride-iodide transport protein. Nature Genetics 21 440-443. (Pubitemid 29159585)
45. Scott DA, Wang R, Kreman TM, Andrews M, McDonald JM, Bishop JR, Smith RJ, Karniski LP & Sheffield VC 2000 Functional differences of the PDS gene product are associated with phenotypic variation in patients with Pendred syndrome and non-syndromic hearing loss (DFNB4). Human Molecular Genetics 9 1709-1715. (Pubitemid 30427008)
46. Shafrir Y & Guy HR 2004 STAM: simple transmembrane alignment method. Bioinformatics 20 758-769. (Pubitemid 38443832)
47. Sindic A, Chang MH, Mount DB & Romero MF 2007 Renal physiology of SLC26 anion exchangers. Current Opinion in Nephrology and Hypertension 16 484-490. (Pubitemid 47254701)
48. Soleimani M & Xu J 2006 SLC26 chloride/base exchangers in the kidney in health and disease. Seminars in Nephrology 26 375-385.
49. 3 exchanger in the kidney cortex. American Journal of Physiology. Renal Physiology 280 F356-F364.
50. Sweet RM & Eisenberg D 1983 Correlation of sequence hydrophobicities measures similarity in three-dimensional protein structure. Journal of Molecular Biology 171 479-488.
51. Taylor JP, Metcalfe RA, Watson PF, Weetman AP & Trembath RC 2002 Mutations of the PDS gene, encoding pendrin, are associated with protein mislocalization and loss of iodide efflux: implications for thyroid dysfunction in Pendred syndrome. Journal of Clinical Endocrinology and Metabolism 87 1778-1784.
52. Wall SM 2005 Recent advances in our understanding of intercalated cells. Current Opinion in Nephrology and Hypertension 14 480-484. (Pubitemid 41152712)
53. Wall SM 2006 The renal physiology of pendrin (SLC26A4) and its role in hypertension. Novartis Foundation Symposium 273 231-239.
54. Wall SM & Pech V 2008 The interaction of pendrin and the epithelial sodium channel in blood pressure regulation. Current Opinion in Nephrology and Hypertension 17 18-24.
55. 2+ reabsorption in a Pendred syndrome mouse model. American Journal of Physiology. Renal Physiology 292 F1345-F1353.
56. Yang JJ, Tsai CC, Hsu HM, Shiao JY, Su CC & Li SY 2005 Hearing loss associated with enlarged vestibular aqueduct and Mondini dysplasia is caused by splice-site mutation in the PDS gene. Hearing Research 199 22-30.
57. Yang T, Vidarsson H, Rodrigo-Blomqvist S, Rosengren SS, Enerback S & Smith RJ 2007 Transcriptional control of SLC26A4 is involved in Pendred syndrome and nonsyndromic enlargement of vestibular aqueduct (DFNB4). American Journal of Human Genetics 80 1055-1063. (Pubitemid 47579342)
58. Yoon JS, Park HJ, Yoo SY, NamkungW, JoMJ, Koo SK, Park HY, Lee WS, Kim KH & Lee MG 2008 Heterogeneity in the processing defect of SLC26A4 mutants. Journal of Medical Genetics 45 411-419.
59. - channel in FRTL-5 cells. Biochemical and Biophysical Research Communications 259 631-635.
60. Yoshida A, Taniguchi S, Hisatome I, Royaux IE, Green ED, Kohn LD & Suzuki K 2002 Pendrin is an iodide-specific apical porter responsible for iodide efflux from thyroid cells. Journal of Clinical Endocrinology and Metabolism 87 3356-3361. (Pubitemid 34816389)
61. YoshidaA,Hisatome I,Taniguchi S, Sasaki N, Yamamoto Y, Miake J, Fukui H, Shimizu H, Okamura T, Okura Tet al. 2004 Mechanism of iodide/chloride exchange by pendrin. Endocrinology 145 4301-4308.
62. Zhai Y & Saier MH Jr 2001 A web-based program (WHAT) for the simultaneous prediction of hydropathy, amphipathicity, secondary structure and transmembrane topology for a single protein sequence. Journal of Molecular Microbiology and Biotechnology 3 501-502.