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Properties and Function of the Solute Carrier 26 Family of Anion Transporters

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Ion Channels and Transporters of Epithelia in Health and Disease

Part of the book series: Physiology in Health and Disease ((PIHD))

Abstract

The SLC26 family of anion transporters consists of 10 members that display remarkable functional and substrate diversity. Mutations in several members of the family have been identified as causing a variety of human diseases and mouse phenotype when deleted. The family drew the attention and strong interest of epithelial biologist with the identification of the first elusive luminal Cl−/HCO3 − exchange, which turned to be the third member of the family SLC26A3. Fairly quick, progress since revealed that members of the family transport all halides, NO3 −, SO4 2−, oxalate, and formate, among others. Members of the family can be grouped into three subgroups based on substrate selectivity and transport mode: the SO4 2− transporters SLC26A1 and SLC26A2; the anion exchangers 2Cl−/1HCO3 − SLC26A3, 1Cl−/1HCO3 − SLC26A4, and 1Cl−/2HCO3 − SLC26A6; and the Cl− channels SLC26A7, SLC26A9, and SLC26A11. This chapter discusses structural features, transport properties, and regulation of the transporters that are essential to understand their functions and roles in human diseases.

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References

  • Ahuja M, Jha A, Maleth J, Park S, Muallem S (2014) cAMP and Ca(2)(+) signaling in secretory epithelia: crosstalk and synergism. Cell Calcium 55:385–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alper SL, Stewart AK, Vandorpe DH, Clark JS, Horack RZ, Simpson JE, Walker NM, Clarke LL (2011) Native and recombinant Slc26a3 (downregulated in adenoma, Dra) do not exhibit properties of 2Cl-/1HCO3- exchange. Am J Physiol Cell Physiol 300:C276–86

    Article  CAS  PubMed  Google Scholar 

  • Amlal H, Xu J, Barone S, Zahedi K, Soleimani M (2013) The chloride channel/transporter Slc26a9 regulates the systemic arterial pressure and renal chloride excretion. J Mol Med 91:561–72

    Article  CAS  PubMed  Google Scholar 

  • Anagnostopoulou P, Riederer B, Duerr J, Michel S, Binia A, Agrawal R, Liu X, Kalitzki K, Xiao F, Chen M, Schatterny J, Hartmann D, Thum T, Kabesch M, Soleimani M, Seidler U, Mall MA (2012) SLC26A9-mediated chloride secretion prevents mucus obstruction in airway inflammation. J Clin Invest 122:3629–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ando H, Mizutani A, Matsu-ura T, Mikoshiba K (2003) IRBIT, a novel inositol 1,4,5-trisphosphate (IP3) receptor-binding protein, is released from the IP3 receptor upon IP3 binding to the receptor. J Biol Chem 278:10602–12

    Article  CAS  PubMed  Google Scholar 

  • Ando H, Mizutani A, Kiefer H, Tsuzurugi D, Michikawa T, Mikoshiba K (2006) IRBIT suppresses IP3 receptor activity by competing with IP3 for the common binding site on the IP3 receptor. Mol Cell 22:795–806

    Article  CAS  PubMed  Google Scholar 

  • Aravind L, Koonin EV (2000) The STAS domain - a link between anion transporters and antisigma-factor antagonists. Curr Biol 10:R53–5

    Article  CAS  PubMed  Google Scholar 

  • Asano K, Matsushita T, Umeno J, Hosono N, Takahashi A, Kawaguchi T, Matsumoto T, Matsui T, Kakuta Y, Kinouchi Y, Shimosegawa T, Hosokawa M, Arimura Y, Shinomura Y, Kiyohara Y, Tsunoda T, Kamatani N, Iida M, Nakamura Y, Kubo M (2009) A genome-wide association study identifies three new susceptibility loci for ulcerative colitis in the Japanese population. Nat Genet 41:1325–9

    Article  CAS  PubMed  Google Scholar 

  • Babu M, Greenblatt JF, Emili A, Strynadka NC, Reithmeier RA, Moraes TF (2010) Structure of a SLC26 anion transporter STAS domain in complex with acyl carrier protein: implications for E. coli YchM in fatty acid metabolism. Structure 18:1450–62

    Article  CAS  PubMed  Google Scholar 

  • Bachmann O, Reichelt D, Tuo B, Manns MP, Seidler U (2006) Carbachol increases Na+−HCO3- cotransport activity in murine colonic crypts in a M3-, Ca2+/calmodulin-, and PKC-dependent manner. Am J Physiol Gastrointest Liver Physiol 291:G650–7

    Article  CAS  PubMed  Google Scholar 

  • Bai JP, Surguchev A, Ogando Y, Song L, Bian S, Santos-Sacchi J, Navaratnam D (2010) Prestin surface expression and activity are augmented by interaction with MAP1S, a microtubule-associated protein. J Biol Chem 285:20834–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker JM, Hudson RP, Kanelis V, Choy WY, Thibodeau PH, Thomas PJ, Forman-Kay JD (2007) CFTR regulatory region interacts with NBD1 predominantly via multiple transient helices. Nat Struct Mol Biol 14:738–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bakouh N, Bienvenu T, Thomas A, Ehrenfeld J, Liote H, Roussel D, Duquesnoy P, Farman N, Viel M, Cherif-Zahar B, Amselem S, Taam RA, Edelman A, Planelles G, Sermet-Gaudelus I (2013) Characterization of SLC26A9 in patients with CF-like lung disease. Hum Mutat 34:1404–14

    Article  CAS  PubMed  Google Scholar 

  • Bertrand CA, Zhang R, Pilewski JM, Frizzell RA (2009) SLC26A9 is a constitutively active, CFTR-regulated anion conductance in human bronchial epithelia. J Gen Physiol 133:421–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bissig M, Hagenbuch B, Stieger B, Koller T, Meier PJ (1994) Functional expression cloning of the canalicular sulfate transport system of rat hepatocytes. J Biol Chem 269:3017–21

    CAS  PubMed  Google Scholar 

  • Blackman SM, Commander CW, Watson C, Arcara KM, Strug LJ, Stonebraker JR, Wright FA, Rommens JM, Sun L, Pace RG, Norris SA, Durie PR, Drumm ML, Knowles MR, Cutting GR (2013) Genetic modifiers of cystic fibrosis-related diabetes. Diabetes 62:3627–35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blouquit-Laye S, Chinet T (2007) Ion and liquid transport across the bronchiolar epithelium. Respir Physiol Neurobiol 159:278–82

    Article  CAS  PubMed  Google Scholar 

  • Bozoky Z, Krzeminski M, Chong PA, Forman-Kay JD (2013a) Structural changes of CFTR R region upon phosphorylation: a plastic platform for intramolecular and intermolecular interactions. FEBS J 280:4407–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bozoky Z, Krzeminski M, Muhandiram R, Birtley JR, Al-Zahrani A, Thomas PJ, Frizzell RA, Ford RC, Forman-Kay JD (2013b) Regulatory R region of the CFTR chloride channel is a dynamic integrator of phospho-dependent intra- and intermolecular interactions. Proc Natl Acad Sci USA 110:E4427–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Hum Mutat 17:403–11

    Article  CAS  PubMed  Google Scholar 

  • Chapman JM, Karniski LP (2010) Protein localization of SLC26A2 (DTDST) in rat kidney. Histochem Cell Biol 133:541–7

    Article  CAS  PubMed  Google Scholar 

  • Chen AP, Chang MH, Romero MF (2012) Functional analysis of nonsynonymous single nucleotide polymorphisms in human SLC26A9. Hum Mutat 33:1275–84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chernova MN, Jiang L, Friedman DJ, Darman RB, Lohi H, Kere J, Vandorpe DH, Alper SL (2005) Functional comparison of mouse slc26a6 anion exchanger with human SLC26A6 polypeptide variants: differences in anion selectivity, regulation, and electrogenicity. J Biol Chem 280:8564–80

    Article  CAS  PubMed  Google Scholar 

  • Choi BY, Kim HM, Ito T, Lee KY, Li X, Monahan K, Wen Y, Wilson E, Kurima K, Saunders TL, Petralia RS, Wangemann P, Friedman TB, Griffith AJ (2011) Mouse model of enlarged vestibular aqueducts defines temporal requirement of Slc26a4 expression for hearing acquisition. J Clin Invest 121:4516–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Compton EL, Karinou E, Naismith JH, Gabel F, Javelle A (2011) Low resolution structure of a bacterial SLC26 transporter reveals dimeric stoichiometry and mobile intracellular domains. J Biol Chem 286:27058–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Compton EL, Page K, Findlay HE, Haertlein M, Moulin M, Zachariae U, Norman DG, Gabel F, Javelle A (2014) Conserved structure and domain organisation amongst bacterial Slc26 transporters. Biochem J 463(2):297–307

    Article  CAS  PubMed  Google Scholar 

  • Coyle B, Coffey R, Armour JA, Gausden E, Hochberg Z, Grossman A, Britton K, Pembrey M, Reardon W, Trembath R (1996) Pendred syndrome (goitre and sensorineural hearing loss) maps to chromosome 7 in the region containing the nonsyndromic deafness gene DFNB4. Nat Genet 12:421–3

    Article  CAS  PubMed  Google Scholar 

  • Dawson PA, Russell CS, Lee S, McLeay SC, van Dongen JM, Cowley DM, Clarke LA, Markovich D (2010) Urolithiasis and hepatotoxicity are linked to the anion transporter Sat1 in mice. J Clin Invest 120:706–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Della Valle MC, Sleat DE, Zheng H, Moore DF, Jadot M, Lobel P (2011) Classification of subcellular location by comparative proteomic analysis of native and density-shifted lysosomes. Mol Cell Proteomics 10(M110):006403

    PubMed  Google Scholar 

  • Detro-Dassen S, Schanzler M, Lauks H, Martin I, Meyer Zu Berstenhorst S, Nothmann D, Torres-Salazar D, Hidalgo P, Schmalzing G, Fahlke C (2007) Conserved dimeric subunit stoichiometry of SLC26 multifunctional anion exchangers. J Biol Chem 283(7):4177–88

    Article  PubMed  CAS  Google Scholar 

  • Detro-Dassen S, Schanzler M, Lauks H, Martin I, zu Berstenhorst SM, Nothmann D, Torres-Salazar D, Hidalgo P, Schmalzing G, Fahlke C (2008) Conserved dimeric subunit stoichiometry of SLC26 multifunctional anion exchangers. J Biol Chem 283:4177–88

    Article  CAS  PubMed  Google Scholar 

  • Dorwart MR, Shcheynikov N, Wang Y, Stippec S, Muallem S (2007) SLC26A9 is a Cl(−) channel regulated by the WNK kinases. J Physiol 584:333–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorwart MR, Shcheynikov N, Yang D, Muallem S (2008) The solute carrier 26 family of proteins in epithelial ion transport. Physiology (Bethesda) 23:104–14

    Article  CAS  Google Scholar 

  • Dudas PL, Mentone S, Greineder CF, Biemesderfer D, Aronson PS (2006) Immunolocalization of anion transporter Slc26a7 in mouse kidney. Am J Physiol Renal Physiol 290:F937–45

    Article  CAS  PubMed  Google Scholar 

  • Everett LA, Glaser B, Beck JC, Idol JR, Buchs A, Heyman M, Adawi F, Hazani E, Nassir E, Baxevanis AD, Sheffield VC, Green ED (1997) Pendred syndrome is caused by mutations in a putative sulphate transporter gene (PDS). Nat Genet 17:411–22

    Article  CAS  PubMed  Google Scholar 

  • Farkas K, Yeruva S, Rakonczay Z Jr, Ludolph L, Molnar T, Nagy F, Szepes Z, Schnur A, Wittmann T, Hubricht J, Riederer B, Venglovecz V, Lazar G, Kiraly M, Zsembery A, Varga G, Seidler U, Hegyi P (2011) New therapeutic targets in ulcerative colitis: the importance of ion transporters in the human colon. Inflamm Bowel Dis 17:884–98

    Article  PubMed  Google Scholar 

  • Forlino A, Piazza R, Tiveron C, Della Torre S, Tatangelo L, Bonafe L, Gualeni B, Romano A, Pecora F, Superti-Furga A, Cetta G, Rossi A (2005) A diastrophic dysplasia sulfate transporter (SLC26A2) mutant mouse: morphological and biochemical characterization of the resulting chondrodysplasia phenotype. Hum Mol Genet 14:859–71

    Article  CAS  PubMed  Google Scholar 

  • Garnett JP, Hickman E, Burrows R, Hegyi P, Tiszlavicz L, Cuthbert AW, Fong P, Gray MA (2011) Novel role for pendrin in orchestrating bicarbonate secretion in cystic fibrosis transmembrane conductance regulator (CFTR)-expressing airway serous cells. J Biol Chem 286:41069–82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gorbunov D, Sturlese M, Nies F, Kluge M, Bellanda M, Battistutta R, Oliver D (2014) Molecular architecture and the structural basis for anion interaction in prestin and SLC26 transporters. Nat Commun 5:3622

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gualeni B, de Vernejoul MC, Marty-Morieux C, De Leonardis F, Franchi M, Monti L, Forlino A, Houillier P, Rossi A, Geoffroy V (2013) Alteration of proteoglycan sulfation affects bone growth and remodeling. Bone 54:83–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haila S, Saarialho-Kere U, Karjalainen-Lindsberg ML, Lohi H, Airola K, Holmberg C, Hastbacka J, Kere J, Hoglund P (2000) The congenital chloride diarrhea gene is expressed in seminal vesicle, sweat gland, inflammatory colon epithelium, and in some dysplastic colon cells. Histochem Cell Biol 113:279–86

    Article  CAS  PubMed  Google Scholar 

  • Haila S, Hastbacka J, Bohling T, Karjalainen-Lindsberg ML, Kere J, Saarialho-Kere U (2001) SLC26A2 (diastrophic dysplasia sulfate transporter) is expressed in developing and mature cartilage but also in other tissues and cell types. J Histochem Cytochem 49:973–82

    Article  CAS  PubMed  Google Scholar 

  • Hastbacka J, de la Chapelle A, Mahtani MM, Clines G, Reeve-Daly MP, Daly M, Hamilton BA, Kusumi K, Trivedi B, Weaver A et al (1994) The diastrophic dysplasia gene encodes a novel sulfate transporter: positional cloning by fine-structure linkage disequilibrium mapping. Cell 78:1073–87

    Article  CAS  PubMed  Google Scholar 

  • Heneghan JF, Akhavein A, Salas MJ, Shmukler BE, Karniski LP, Vandorpe DH, Alper SL (2010) Regulated transport of sulfate and oxalate by SLC26A2/DTDST. Am J Physiol Cell Physiol 298:C1363–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoglund P, Haila S, Socha J, Tomaszewski L, Saarialho-Kere U, Karjalainen-Lindsberg ML, Airola K, Holmberg C, de la Chapelle A, Kere J (1996) Mutations of the Down-regulated in adenoma (DRA) gene cause congenital chloride diarrhoea. Nat Genet 14:316–9

    Article  CAS  PubMed  Google Scholar 

  • Hoglund P, Sormaala M, Haila S, Socha J, Rajaram U, Scheurlen W, Sinaasappel M, de Jonge H, Holmberg C, Yoshikawa H, Kere J (2001) Identification of seven novel mutations including the first two genomic rearrangements in SLC26A3 mutated in congenital chloride diarrhea. Hum Mutat 18:233–42

    Article  CAS  PubMed  Google Scholar 

  • Homma K, Miller KK, Anderson CT, Sengupta S, Du GG, Aguinaga S, Cheatham M, Dallos P, Zheng J (2010) Interaction between CFTR and prestin (SLC26A5). Biochim Biophys Acta 1798:1029–40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong JH, Yang D, Shcheynikov N, Ohana E, Shin DM, Muallem S (2013) Convergence of IRBIT, phosphatidylinositol (4,5) bisphosphate, and WNK/SPAK kinases in regulation of the Na+−HCO3- cotransporters family. Proc Natl Acad Sci USA 110:4105–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang J, Shan J, Kim D, Liao J, Evagelidis A, Alper SL, Hanrahan JW (2012) Basolateral chloride loading by the anion exchanger type 2: role in fluid secretion by the human airway epithelial cell line Calu-3. J Physiol 590:5299–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson GC, Mittaz-Crettol L, Taylor JA, Mortier GR, Spranger J, Zabel B, Le Merrer M, Cormier-Daire V, Hall CM, Offiah A, Wright MJ, Savarirayan R, Nishimura G, Ramsden SC, Elles R, Bonafe L, Superti-Furga A, Unger S, Zankl A, Briggs MD (2012) Pseudoachondroplasia and multiple epiphyseal dysplasia: a 7-year comprehensive analysis of the known disease genes identify novel and recurrent mutations and provides an accurate assessment of their relative contribution. Hum Mutat 33:144–57

    Article  CAS  PubMed  Google Scholar 

  • Jacob P, Rossmann H, Lamprecht G, Kretz A, Neff C, Lin-Wu E, Gregor M, Groneberg DA, Kere J, Seidler U (2002) Down-regulated in adenoma mediates apical Cl-/HCO3- exchange in rabbit, rat, and human duodenum. Gastroenterology 122:709–24

    Article  CAS  PubMed  Google Scholar 

  • Jiang Z, Grichtchenko II, Boron WF, Aronson PS (2002) Specificity of anion exchange mediated by mouse Slc26a6. J Biol Chem 277:33963–7

    Article  CAS  PubMed  Google Scholar 

  • Jiang Z, Asplin JR, Evan AP, Rajendran VM, Velazquez H, Nottoli TP, Binder HJ, Aronson PS (2006) Calcium oxalate urolithiasis in mice lacking anion transporter Slc26a6. Nat Genet 38:474–8

    Article  CAS  PubMed  Google Scholar 

  • Karniski LP, Lotscher M, Fucentese M, Hilfiker H, Biber J, Murer H (1998) Immunolocalization of sat-1 sulfate/oxalate/bicarbonate anion exchanger in the rat kidney. Am J Physiol 275:F79–87

    CAS  PubMed  Google Scholar 

  • Keller JP, Homma K, Duan C, Zheng J, Cheatham MA, Dallos P (2014) Functional regulation of the SLC26-family protein prestin by calcium/calmodulin. J Neurosci 34:1325–32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim KH, Shcheynikov N, Wang Y, Muallem S (2005) SLC26A7 is a Cl- channel regulated by intracellular pH. J Biol Chem 280:6463–70

    Article  CAS  PubMed  Google Scholar 

  • Kim HJ, Myers R, Sihn CR, Rafizadeh S, Zhang XD (2013) Slc26a6 functions as an electrogenic Cl-/HCO3- exchanger in cardiac myocytes. Cardiovasc Res 100:383–91

    Article  CAS  PubMed  Google Scholar 

  • Kim KX, Sanneman JD, Kim HM, Harbidge DG, Xu J, Soleimani M, Wangemann P, Marcus DC (2014) Slc26a7 chloride channel activity and localization in mouse Reissner’s membrane epithelium. PLoS ONE 9, e97191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Knauf F, Yang CL, Thomson RB, Mentone SA, Giebisch G, Aronson PS (2001) Identification of a chloride-formate exchanger expressed on the brush border membrane of renal proximal tubule cells. Proc Natl Acad Sci USA 98:9425–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ko SB, Shcheynikov N, Choi JY, Luo X, Ishibashi K, Thomas PJ, Kim JY, Kim KH, Lee MG, Naruse S, Muallem S (2002) A molecular mechanism for aberrant CFTR-dependent HCO(3)(−) transport in cystic fibrosis. EMBO J 21:5662–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ko SB, Zeng W, Dorwart MR, Luo X, Kim KH, Millen L, Goto H, Naruse S, Soyombo A, Thomas PJ, Muallem S (2004) Gating of CFTR by the STAS domain of SLC26 transporters. Nat Cell Biol 6:343–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosiek O, Busque SM, Foller M, Shcheynikov N, Kirchhoff P, Bleich M, Muallem S, Geibel JP (2007) SLC26A7 can function as a chloride-loading mechanism in parietal cells. Pflugers Arch 454:989–98

    Article  CAS  PubMed  Google Scholar 

  • Lamprecht G, Seidler U (2006) The emerging role of PDZ adapter proteins for regulation of intestinal ion transport. Am J Physiol Gastrointest Liver Physiol 291:G766–77

    Article  CAS  PubMed  Google Scholar 

  • Lee JH, Nam JH, Park J, Kang DW, Kim JY, Lee MG, Yoon JS (2012a) Regulation of SLC26A3 activity by NHERF4 PDZ-mediated interaction. Cell Signal 24:1821–30

    Article  CAS  PubMed  Google Scholar 

  • Lee MG, Ohana E, Park HW, Yang D, Muallem S (2012b) Molecular mechanism of pancreatic and salivary gland fluid and HCO3 secretion. Physiol Rev 92:39–74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Sanneman JD, Harbidge DG, Zhou F, Ito T, Nelson R, Picard N, Chambrey R, Eladari D, Miesner T, Griffith AJ, Marcus DC, Wangemann P (2013a) SLC26A4 targeted to the endolymphatic sac rescues hearing and balance in Slc26a4 mutant mice. PLoS Genet 9, e1003641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Zhou F, Marcus DC, Wangemann P (2013b) Endolymphatic Na(+) and K(+) concentrations during cochlear growth and enlargement in mice lacking Slc26a4/pendrin. PLoS ONE 8, e65977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Soave D, Miller MR, Keenan K, Lin F, Gong J, Chiang T, Stephenson AL, Durie P, Rommens J, Sun L, Strug LJ (2014) Unraveling the complex genetic model for cystic fibrosis: pleiotropic effects of modifier genes on early cystic fibrosis-related morbidities. Hum Genet 133:151–61

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Li T, Riederer B, Lenzen H, Ludolph L, Yeruva S, Tuo B, Soleimani M, Seidler U (2014) Loss of Slc26a9 anion transporter alters intestinal electrolyte and HCO transport and reduces survival in CFTR-deficient mice. Pflugers Arch 467(6):1261–75

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lohi H, Kujala M, Makela S, Lehtonen E, Kestila M, Saarialho-Kere U, Markovich D, Kere J (2002) Functional characterization of three novel tissue-specific anion exchangers SLC26A7, −A8, and -A9. J Biol Chem 277:14246–54

    Article  CAS  PubMed  Google Scholar 

  • Lohi H, Lamprecht G, Markovich D, Heil A, Kujala M, Seidler U, Kere J (2003) Isoforms of SLC26A6 mediate anion transport and have functional PDZ interaction domains. Am J Physiol 284:C769–79

    Article  CAS  Google Scholar 

  • Loriol C, Dulong S, Avella M, Gabillat N, Boulukos K, Borgese F, Ehrenfeld J (2008) Characterization of SLC26A9, facilitation of Cl(−) transport by bicarbonate. Cell Physiol Biochem 22:15–30

    Article  CAS  PubMed  Google Scholar 

  • Malakooti J, Saksena S, Gill RK, Dudeja PK (2011) Transcriptional regulation of the intestinal luminal Na(+) and Cl(−) transporters. Biochem J 435:313–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melvin JE, Park K, Richardson L, Schultheis PJ, Shull GE (1999) Mouse down-regulated in adenoma (DRA) is an intestinal Cl(−)/HCO(3)(−) exchanger and is up-regulated in colon of mice lacking the NHE3 Na(+)/H(+) exchanger. J Biol Chem 274:22855–61

    Article  CAS  PubMed  Google Scholar 

  • Melvin JE, Yule D, Shuttleworth T, Begenisich T (2005) Regulation of fluid and electrolyte secretion in salivary gland acinar cells. Annu Rev Physiol 67:445–69

    Article  CAS  PubMed  Google Scholar 

  • Moseley RH, Hoglund P, Wu GD, Silberg DG, Haila S, de la Chapelle A, Holmberg C, Kere J (1999) Downregulated in adenoma gene encodes a chloride transporter defective in congenital chloride diarrhea. Am J Physiol 276:G185–92

    CAS  PubMed  Google Scholar 

  • Nakagami Y, Favoreto S Jr, Zhen G, Park SW, Nguyenvu LT, Kuperman DA, Dolganov GM, Huang X, Boushey HA, Avila PC, Erle DJ (2008) 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 181:2203–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 (2008) Identification of pendrin as a common mediator for mucus production in bronchial asthma and chronic obstructive pulmonary disease. J Immunol 180:6262–9

    Article  CAS  PubMed  Google Scholar 

  • Ohana E, Yang D, Shcheynikov N, Muallem S (2009) Diverse transport modes by the solute carrier 26 family of anion transporters. J Physiol 587:2179–85

    Article  CAS  PubMed  Google Scholar 

  • Ohana E, Shcheynikov N, Yang D, So I, Muallem S (2011) Determinants of coupled transport and uncoupled current by the electrogenic SLC26 transporters. J Gen Physiol 137:239–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohana E, Shcheynikov N, Park M, Muallem S (2012) Solute carrier family 26 member a2 (Slc26a2) protein functions as an electroneutral SOFormula/OH-/Cl- exchanger regulated by extracellular Cl. J Biol Chem 287:5122–32

    Article  CAS  PubMed  Google Scholar 

  • Ohana E, Shcheynikov N, Moe OW, Muallem S (2013) SLC26A6 and NaDC-1 transporters interact to regulate oxalate and citrate homeostasis. J Am Soc Nephrol 24(10):1617–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmieri M, Impey S, Kang H, di Ronza A, Pelz C, Sardiello M, Ballabio A (2011) Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum Mol Genet 20:3852–66

    Article  CAS  PubMed  Google Scholar 

  • Park HW, Nam JH, Kim JY, Namkung W, Yoon JS, Lee JS, Kim KS, Venglovecz V, Gray MA, Kim KH, Lee MG (2010) Dynamic regulation of CFTR bicarbonate permeability by [Cl-]i and its role in pancreatic bicarbonate secretion. Gastroenterology 139:620–31

    Article  CAS  PubMed  Google Scholar 

  • Park S, Hong JH, Ohana E, Muallem S (2012) The WNK/SPAK and IRBIT/PP1 pathways in epithelial fluid and electrolyte transport. Physiology (Bethesda) 27:291–9

    Article  CAS  Google Scholar 

  • Park S, Shcheynikov N, Hong JH, Zheng C, Suh SH, Kawaai K, Ando H, Mizutani A, Abe T, Kiyonari H, Seki G, Yule D, Mikoshiba K, Muallem S (2013) Irbit mediates synergy between ca(2+) and cAMP signaling pathways during epithelial transport in mice. Gastroenterology 145:232–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park M, Ohana E, Choi SY, Lee MS, Park JH, Muallem S (2014) Multiple roles of the SO4(2-)/Cl-/OH- exchanger protein Slc26a2 in chondrocyte functions. J Biol Chem 289:1993–2001

    Article  CAS  PubMed  Google Scholar 

  • Pasqualetto E, Aiello R, Gesiot L, Bonetto G, Bellanda M, Battistutta R (2010) Structure of the cytosolic portion of the motor protein prestin and functional role of the STAS domain in SLC26/SulP anion transporters. J Mol Biol 400:448–62

    Article  CAS  PubMed  Google Scholar 

  • Pech V, Pham TD, Hong S, Weinstein AM, Spencer KB, Duke BJ, Walp E, Kim YH, Sutliff RL, Bao HF, Eaton DC, Wall SM (2010) Pendrin modulates ENaC function by changing luminal HCO3. J Am Soc Nephrol 21:1928–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedemonte N, Caci E, Sondo E, Caputo A, Rhoden K, Pfeffer U, Di Candia M, Bandettini R, Ravazzolo R, Zegarra-Moran O, Galietta LJ (2007) Thiocyanate transport in resting and IL-4-stimulated human bronchial epithelial cells: role of pendrin and anion channels. J Immunol 178:5144–53

    Article  CAS  PubMed  Google Scholar 

  • Pesce L, Bizhanova A, Caraballo JC, Westphal W, Butti ML, Comellas A, Kopp P (2012) TSH regulates pendrin membrane abundance and enhances iodide efflux in thyroid cells. Endocrinology 153:512–21

    Article  CAS  PubMed  Google Scholar 

  • Petrovic S, Ju X, Barone S, Seidler U, Alper SL, Lohi H, Kere J, Soleimani M (2003) Identification of a basolateral Cl-/HCO3- exchanger specific to gastric parietal cells. Am J Physiol Gastrointest Liver Physiol 284:G1093–103

    Article  CAS  PubMed  Google Scholar 

  • Rahmati N, Kunzelmann K, Xu J, Barone S, Sirianant L, De Zeeuw CI, Soleimani M (2013) Slc26a11 is prominently expressed in the brain and functions as a chloride channel: expression in Purkinje cells and stimulation of V H(+)-ATPase. Pflugers Arch 465:1583–97

    Article  CAS  PubMed  Google Scholar 

  • Regeer RR, Lee A, Markovich D (2003) Characterization of the human sulfate anion transporter (hsat-1) protein and gene (SAT1; SLC26A1). DNA Cell Biol 22:107–17

    Article  CAS  PubMed  Google Scholar 

  • Rode B, Dirami T, Bakouh N, Rizk-Rabin M, Norez C, Lhuillier P, Lores P, Jollivet M, Melin P, Zvetkova I, Bienvenu T, Becq F, Planelles G, Edelman A, Gacon G, Toure A (2012) The testis anion transporter TAT1 (SLC26A8) physically and functionally interacts with the cystic fibrosis transmembrane conductance regulator channel: a potential role during sperm capacitation. Hum Mol Genet 21:1287–98

    Article  CAS  PubMed  Google Scholar 

  • 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 141:839–45

    Article  CAS  PubMed  Google Scholar 

  • 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. Proc Natl Acad Sci U S A 98:4221–6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sardiello M, Palmieri M, di Ronza A, Medina DL, Valenza M, Gennarino VA, Di Malta C, Donaudy F, Embrione V, Polishchuk RS, Banfi S, Parenti G, Cattaneo E, Ballabio A (2009) A gene network regulating lysosomal biogenesis and function. Science 325:473–7

    CAS  PubMed  Google Scholar 

  • Schaechinger TJ, Oliver D (2007) Nonmammalian orthologs of prestin (SLC26A5) are electrogenic divalent/chloride anion exchangers. Proc Natl Acad Sci USA 104:7693–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schroder BA, Wrocklage C, Hasilik A, Saftig P (2010) The proteome of lysosomes. Proteomics 10:4053–76

    Article  PubMed  CAS  Google Scholar 

  • Schweinfest CW, Spyropoulos DD, Henderson KW, Kim JH, Chapman JM, Barone S, Worrell RT, Wang Z, Soleimani M (2006) slc26a3 (dra)-deficient mice display chloride-losing diarrhea, enhanced colonic proliferation, and distinct up-regulation of ion transporters in the colon. J Biol Chem 281:37962–71

    Article  CAS  PubMed  Google Scholar 

  • Shan J, Liao J, Huang J, Robert R, Palmer ML, Fahrenkrug SC, O’Grady SM, Hanrahan JW (2012) Bicarbonate-dependent chloride transport drives fluid secretion by the human airway epithelial cell line Calu-3. J Physiol 590:5273–97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma AK, Ye L, Baer CE, Shanmugasundaram K, Alber T, Alper SL, Rigby AC (2011) Solution structure of the guanine nucleotide-binding STAS domain of SLC26-related SulP protein Rv1739c from Mycobacterium tuberculosis. J Biol Chem 286:8534–44

    Article  CAS  PubMed  Google Scholar 

  • Shcheynikov N, Ko SB, Zeng W, Choi JY, Dorwart MR, Thomas PJ, Muallem S (2006a) Regulatory interaction between CFTR and the SLC26 transporters. Novartis Found Symp 273:177–86; discussion 186–92, 261–74

    Article  PubMed  Google Scholar 

  • Shcheynikov N, Wang Y, Park M, Ko SB, Dorwart M, Naruse S, Thomas PJ, Muallem S (2006b) Coupling modes and stoichiometry of Cl-/HCO3- exchange by slc26a3 and slc26a6. J Gen Physiol 127:511–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shcheynikov N, Yang D, Wang Y, Zeng W, Karniski LP, So I, Wall SM, Muallem S (2008) 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 586:3813–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shelden MC, Howitt SM, Price GD (2010) Membrane topology of the cyanobacterial bicarbonate transporter, BicA, a member of the SulP (SLC26A) family. Mol Membr Biol 27:12–22

    Article  PubMed  CAS  Google Scholar 

  • Simpson JE, Schweinfest CW, Shull GE, Gawenis LR, Walker NM, Boyle KT, Soleimani M, Clarke LL (2007) PAT-1 (Slc26a6) is the predominant apical membrane Cl-/HCO3- exchanger in the upper villous epithelium of the murine duodenum. Am J Physiol Gastrointest Liver Physiol 292:G1079–88

    Article  CAS  PubMed  Google Scholar 

  • Singla A, Dwivedi A, Saksena S, Gill RK, Alrefai WA, Ramaswamy K, Dudeja PK (2010) Mechanisms of lysophosphatidic acid (LPA) mediated stimulation of intestinal apical Cl-/OH- exchange. Am J Physiol Gastrointest Liver Physiol 298:G182–9

    Article  CAS  PubMed  Google Scholar 

  • Soave D, Miller MR, Keenan K, Li W, Gong J, Ip W, Accurso F, Sun L, Rommens JM, Sontag M, Durie PR, Strug LJ (2014) Evidence for a causal relationship between early exocrine pancreatic disease and cystic fibrosis-related diabetes: a Mendelian randomization study. Diabetes 63:2114–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soleimani M, Greeley T, Petrovic S, Wang Z, Amlal H, Kopp P, Burnham CE (2001) Pendrin: an apical Cl-/OH-/HCO3- exchanger in the kidney cortex. Am J Physiol Renal Physiol 280:F356–64

    CAS  PubMed  Google Scholar 

  • Song Y, Yamamoto A, Steward MC, Ko SB, Stewart AK, Soleimani M, Liu BC, Kondo T, Jin CX, Ishiguro H (2012) Deletion of Slc26a6 alters the stoichiometry of apical Cl-/HCO-3 exchange in mouse pancreatic duct. Am J Physiol Cell Physiol 303:C815–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spyroglou A, Bozoglu T, Rawal R, De Leonardis F, Sterner C, Boulkroun S, Benecke AG, Monti L, Zennaro MC, Petersen AK, Doring A, Rossi A, Bidlingmaier M, Warth R, Gieger C, Reincke M, Beuschlein F (2014) Diastrophic dysplasia sulfate transporter (SLC26A2) is expressed in the adrenal cortex and regulates aldosterone secretion. Hypertension 63:1102–9

    Article  CAS  PubMed  Google Scholar 

  • Steward MC, Ishiguro H, Case RM (2005) Mechanisms of bicarbonate secretion in the pancreatic duct. Annu Rev Physiol 67:377–409

    Article  CAS  PubMed  Google Scholar 

  • Stewart AK, Yamamoto A, Nakakuki M, Kondo T, Alper SL, Ishiguro H (2009) Functional coupling of apical Cl-/HCO3- exchange with CFTR in stimulated HCO3- secretion by guinea pig interlobular pancreatic duct. Am J Physiol Gastrointest Liver Physiol 296:G1307–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stewart AK, Shmukler BE, Vandorpe DH, Reimold F, Heneghan JF, Nakakuki M, Akhavein A, Ko S, Ishiguro H, Alper SL (2011) SLC26 anion exchangers of guinea pig pancreatic duct: molecular cloning and functional characterization. Am J Physiol Cell Physiol 301:C289–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun L, Rommens JM, Corvol H, Li W, Li X, Chiang TA, Lin F, Dorfman R, Busson PF, Parekh RV, Zelenika D, Blackman SM, Corey M, Doshi VK, Henderson L, Naughton KM, O’Neal WK, Pace RG, Stonebraker JR, Wood SD, Wright FA, Zielenski J, Clement A, Drumm ML, Boelle PY, Cutting GR, Knowles MR, Durie PR, Strug LJ (2012) Multiple apical plasma membrane constituents are associated with susceptibility to meconium ileus in individuals with cystic fibrosis. Nat Genet 44:562–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verlander JW, Hassell KA, Royaux IE, Glapion DM, Wang ME, Everett LA, Green ED, Wall SM (2003) Deoxycorticosterone upregulates PDS (Slc26a4) in mouse kidney: role of pendrin in mineralocorticoid-induced hypertension. Hypertension 42:356–62

    Article  CAS  PubMed  Google Scholar 

  • Verlander JW, Hong S, Pech V, Bailey JL, Agazatian D, Matthews SW, Coffman TM, Le T, Inagami T, Whitehill FM, Weiner ID, Farley DB, Kim YH, Wall SM (2011) Angiotensin II acts through the angiotensin 1a receptor to upregulate pendrin. Am J Physiol Renal Physiol 301:F1314–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wall SM (2005) Recent advances in our understanding of intercalated cells. Curr Opin Nephrol Hypertens 14:480–4

    Article  CAS  PubMed  Google Scholar 

  • Wall SM, Kim YH, Stanley L, Glapion DM, Everett LA, Green ED, Verlander JW (2004) NaCl restriction upregulates renal Slc26a4 through subcellular redistribution: role in Cl- conservation. Hypertension 44:982–7

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Soyombo AA, Shcheynikov N, Zeng W, Dorwart M, Marino CR, Thomas PJ, Muallem S (2006) Slc26a6 regulates CFTR activity in vivo to determine pancreatic duct HCO3- secretion: relevance to cystic fibrosis. EMBO J 25:5049–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wangemann P, Nakaya K, Wu T, Maganti RJ, Itza EM, Sanneman JD, Harbidge DG, Billings S, Marcus DC (2007) 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 292:F1345–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wedenoja S, Pekansaari E, Hoglund P, Makela S, Holmberg C, Kere J (2011) Update on SLC26A3 mutations in congenital chloride diarrhea. Hum Mutat 32:715–22

    Article  CAS  PubMed  Google Scholar 

  • Xia W, Yu Q, Riederer B, Singh AK, Engelhardt R, Yeruva S, Song P, Tian DA, Soleimani M, Seidler U (2013) The distinct roles of anion transporters Slc26a3 (DRA) and Slc26a6 (PAT-1) in fluid and electrolyte absorption in the murine small intestine. Pflugers Arch 466(8):1541–56

    Article  PubMed Central  CAS  Google Scholar 

  • Xiao F, Juric M, Li J, Riederer B, Yeruva S, Singh AK, Zheng L, Glage S, Kollias G, Dudeja P, Tian DA, Xu G, Zhu J, Bachmann O, Seidler U (2012) Loss of downregulated in adenoma (DRA) impairs mucosal HCO3(−) secretion in murine ileocolonic inflammation. Inflamm Bowel Dis 18:101–11

    Article  PubMed  Google Scholar 

  • Xiao F, Yu Q, Li J, Johansson ME, Singh AK, Xia W, Riederer B, Engelhardt R, Montrose M, Soleimani M, Tian DA, Xu G, Hansson GC, Seidler U (2014) Slc26a3 deficiency is associated with loss of colonic HCO3 (−) secretion, absence of a firm mucus layer and barrier impairment in mice. Acta Physiol 211:161–75

    Article  CAS  Google Scholar 

  • Xie Q, Welch R, Mercado A, Romero MF, Mount DB (2002) Molecular characterization of the murine Slc26a6 anion exchanger: functional comparison with Slc26a1. Am J Physiol Renal Physiol 283:F826–38

    Article  PubMed  Google Scholar 

  • Xie R, Nguyen S, McKeehan K, Wang F, McKeehan WL, Liu L (2011) Microtubule-associated protein 1S (MAP1S) bridges autophagic components with microtubules and mitochondria to affect autophagosomal biogenesis and degradation. J Biol Chem 286:10367–77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Henriksnas J, Barone S, Witte D, Shull GE, Forte JG, Holm L, Soleimani M (2005) SLC26A9 is expressed in gastric surface epithelial cells, mediates Cl-/HCO3- exchange, and is inhibited by NH4+. Am J Physiol Cell Physiol 289:C493–505

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Song P, Miller ML, Borgese F, Barone S, Riederer B, Wang Z, Alper SL, Forte JG, Shull GE, Ehrenfeld J, Seidler U, Soleimani M (2008) Deletion of the chloride transporter Slc26a9 causes loss of tubulovesicles in parietal cells and impairs acid secretion in the stomach. Proc Natl Acad Sci USA 105:17955–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Song P, Nakamura S, Miller M, Barone S, Alper SL, Riederer B, Bonhagen J, Arend LJ, Amlal H, Seidler U, Soleimani M (2009) Deletion of the chloride transporter slc26a7 causes distal renal tubular acidosis and impairs gastric acid secretion. J Biol Chem 284:29470–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Barone S, Li H, Holiday S, Zahedi K, Soleimani M (2011) Slc26a11, a chloride transporter, localizes with the vacuolar H(+)-ATPase of A-intercalated cells of the kidney. Kidney Int 80:926–37

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Jiang W, Furth EE, Wen X, Katz JP, Sellon RK, Silberg DG, Antalis TM, Schweinfest CW, Wu GD (1998) Intestinal inflammation reduces expression of DRA, a transporter responsible for congenital chloride diarrhea. Am J Physiol 275:G1445–53

    CAS  PubMed  Google Scholar 

  • Yang D, Shcheynikov N, Zeng W, Ohana E, So I, Ando H, Mizutani A, Mikoshiba K, Muallem S (2009) IRBIT coordinates epithelial fluid and HCO3- secretion by stimulating the transporters pNBC1 and CFTR in the murine pancreatic duct. J Clin Invest 119:193–202

    CAS  PubMed  Google Scholar 

  • Yang D, Li Q, So I, Huang CL, Ando H, Mizutani A, Seki G, Mikoshiba K, Thomas PJ, Muallem S (2011a) IRBIT governs epithelial secretion in mice by antagonizing the WNK/SPAK kinase pathway. J Clin Invest 121:956–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SK, Jung Y, Kim H, Hong M, Ye BD, Song K (2011b) Association of FCGR2A, JAK2 or HNF4A variants with ulcerative colitis in Koreans. Dig Liver Dis 43:856–61

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Star RA, Muallem S (1994) Membrane localization of H+ and HCO3- transporters in the rat pancreatic duct. J Gen Physiol 104:57–85

    Article  CAS  PubMed  Google Scholar 

  • Zheng J, Shen W, He DZ, Long KB, Madison LD, Dallos P (2000) Prestin is the motor protein of cochlear outer hair cells. Nature 405:149–55

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Epithelial Signaling and Transport Section, Molecular Physiology and Therapeutics Branch, National Institute of Dental and Craniofacial Research, National Institute of Health, NIH, NIDCR, Building 10, Room 1N-112, Bethesda, MD, 20892, USA

    Nikolay Shcheynikov & Shmuel Muallem

  2. Department of Clinical Biochemistry and Pharmacology, Ben Gurion University of the Negev, Beer Sheva, Israel

    Ehud Ohana

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  1. Nikolay Shcheynikov
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  2. Ehud Ohana
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  3. Shmuel Muallem
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Correspondence to Shmuel Muallem .

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  1. Department of Physiology, University of Otago , Dunedin, Otago, New Zealand

    Kirk L. Hamilton

  2. Department of Cell Biology, University of Pittsburgh, Pittsburgh, Pennsylvania, USA

    Daniel C Devor

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Shcheynikov, N., Ohana, E., Muallem, S. (2016). Properties and Function of the Solute Carrier 26 Family of Anion Transporters. In: Hamilton, K., Devor, D. (eds) Ion Channels and Transporters of Epithelia in Health and Disease. Physiology in Health and Disease. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-3366-2_14

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