Slc26a11 is prominently expressed in the brain and functions as a chloride channel: Expression in Purkinje cells and stimulation of v H+-ATPase

Pflugers Archiv European Journal of Physiology

Volumn 465, Issue 11, 2013, Pages 1583-1597

  Rahmati, Negah ^a   Kunzelmann, Karl ^b   Xu, Jie ^c   Barone, Sharon ^c   Sirianant, Lalida ^b   De Zeeuw, Chris I ^a,c,d   Soleimani, Manoocher ^c,e,f  

^a ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^d NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^e UNIVERSITY OF CINCINNATI   (United States)

^f Veterans Administration   (United States)

Author keywords

Cerebellum; Chloride channel; Hippocampus; Olfactory bulb; SLC26 isoforms

Indexed keywords

CALCIUM; CARRIER PROTEIN; CHLORIDE CHANNEL; COMPLEMENTARY DNA; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FORSKOLIN; PROTEIN SLC26A11; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL STIMULATION; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; GENETIC TRANSFECTION; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY BULB; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; PURKINJE CELL; SUBCORTEX;

ANIMALS; ANION TRANSPORT PROTEINS; CALCIUM; CELL MEMBRANE; CEREBRAL CORTEX; COLFORSIN; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MICE; MICE, INBRED C57BL; OLFACTORY BULB; ORGAN SPECIFICITY; PROTEIN TRANSPORT; PROTON-TRANSLOCATING ATPASES; PURKINJE CELLS; RNA, MESSENGER;

EID: 84887161012     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-013-1300-6     Document Type: Article

References (57)

1. +-ATPase. Proc Natl Acad Sci U S A 86(14):5429-5433 (Pubitemid 19185562)
2. + secretion in IMCD cells. Am J Physiol 275(4 Pt 2):F487-F501
3. Bellemer A, Hirata T, Romero MF, Koelle MR (2011) Two types of chloride transporters are required for GABA(A) receptor-mediated inhibition in C. elegans. EMBO J 30(9):1852-1863
4. Berend K, van Hulsteijn LH, Gans RO (2012) Chloride: the queen of electrolytes? Eur J Intern Med 23(3):203-211
5. + ATPase. Curr Opin Nephrol Hypertens 18(5):433-438, Review
6. Brown D, Hirsch S, Gluck S (1988) Localization of a proton-pumping ATPase in rat kidney. J Clin Invest 82(6):2114-2126 (Pubitemid 19054961)
7. Burge JA, Hanna MG (2012) Novel insights into the pathomechanisms of skeletal muscle channelopathies. Curr Neurol Neurosci Rep 12(1):62-69, Review
8. Chang MH, Plata C, Zandi-Nejad K, Sindić A, Sussman CR, Mercado A, Broumand V, Raghuram V, Mount DB, Romero MF (2009) Slc26a9 - anion exchanger, channel and Na+ transporter. J Membr Biol 228(3):125-140
9. De Zeeuw C, Hoebeek F, Bosman L et al (2011) Spatiotemporal firing patterns in the cerebellum. Nat Rev Neurosci 12:327-344
10. - channel regulated by the WNK kinases. J Physiol 584:333-345 (Pubitemid 47504877)
11. 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 17:411-422 (Pubitemid 27518389)
12. Hoglund P, Haila S, Socha J, Tomaszewski L, Saarialho-Kere U, Karjalainen-Lindsberg M-L, Airola K, Holmberg C, de la Chapelle A, Kere J (1996) Mutations of the down-regulated in adenoma (DRA) gene cause congenital chloride diarrhea. Nat Genet 14:316-319
13. Jentsch TJ, Stein V, Weinreich F, Zdebik AA (2002) Molecular structure and physiological function of chloride channels. Physiol Rev 82(2):503-568 (Pubitemid 34654460)
14. A and glycine receptors. J Gen Physiol 138:609-626
15. Kasper D, Planells-Cases R, Fuhrmann JC, Olaf S, Oliver Z, Klaus R, Schmitt A, Mallorie P, Robert S, Michaela S, Uwe K, Jentsch TJ (2005) Loss of the chloride channel ClC-7 leads to lysosomal storage disease and neurodegeneration. EMBO J 24(5):1079-1091 (Pubitemid 40470155)
16. - channel regulated by intracellular pH. J Biol Chem 280:6463-6470 (Pubitemid 40341194)
17. Lohi H, Kujala M, Kerkela E, Saarialho-Kere U, Kestila M, Kere J (2000) Mapping of five new putative anion transporter genes in human and characterization of SLC26A6, a candidate gene for pancreatic anion exchanger. Genomics 70:102-112
18. 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 277:14246-14254 (Pubitemid 34968039)
19. Lynch J (2003) Molecular structure and function of the glycine receptor chloride channel. J Physiol Rev 84:1051-1095
20. +-ATPase in vesicular trafficking: targeting, regulation and function. Curr Opin Cell Biol 20(4):415-426, Review
21. Martins JR, Faria D, Kongsuphol P, Reisch B, Schreiber R, Kunzelmann K (2011) Anoctamin 6 is an essential component of the outwardly rectifying chloride channel. Proc Natl Acad Sci U S A 108(44):18168-18172
22. Moriyama Y, Maeda M, Futai M (1992) The role of V-ATPase in neuronal and endocrine systems. J Exp Biol 172:171-178
23. Moriyama Y, Tsai HL, Futai M (1993) Energy-dependent accumulation of neuron blockers causes selective inhibition of neurotransmitter uptake by brain synaptic vesicles. Arch Biochem Biophys 305:278-281 (Pubitemid 23282908)
24. Mulberg A, Resta L, Windner E et al (1994) Expression and localization of the cystic fibrosis transmembrane conductance regulator mRNA and its protein in rat brain. J Clin Invest 96:646-652
25. Murata Y, Sun-Wada GH, Yoshimizu T, Yamamoto A, Wada Y, Futai M (2002) Differential localization of the vacuolar H+ pump with G subunit isoforms (G1 and G2) in mouse neurons. J Biol Chem 277(39):36296-36303
26. Nelson N, Perzov N, Cohen A, Hagai K, Padler V, Nelson H (2000) The cellular biology of proton-motive force generation by V-ATPases. J Exp Biol 203(Pt 1):89-95, Review (Pubitemid 30079073)
27. Ohana E, Yang D, Shcheynikov N, Muallem S (2009) Diverse transport modes by the solute carrier 26 family of anion transporters. J Physiol 587(Pt 10):2179-2185, Review
28. Okada Y, Sato K, Numata T (2009) Pathophysiology and puzzles of the volume-sensitive outwardly rectifying anion channel. J Physiol 587(Pt 10):2141-2149, Review
29. 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(6):G1093-G1103
30. Plans V, Rickheit G, Jentsch TJ (2009) Physiological roles of CLC Cl(-)/H (+) exchangers in renal proximal tubules. Pflugers Arch 458(1):23-37, Review
31. Poëa-Guyon S, Amar M, Fossier P, Morel N (2006) Alternative splicing controls neuronal expression of v-ATPase subunit a1 and sorting to nerve terminals. J Biol Chem 281(25):17164-17172
32. Pouille F, Scanziani M (2001) Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:1159-1163 (Pubitemid 32758100)
33. Ratte' S, Prescott S (2011) ClC-2 channels regulate neuronal excitability, not intracellular chloride levels. J Neurosci 31(44):15838-15843
34. - cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol 562(1):27-36 (Pubitemid 40207781)
35. Romero MF, Chang MH, Plata C, Zandi-Nejad K, Mercado A, Broumand V, Sussman CR, Mount DB (2006) Physiology of electrogenic SLC26 paralogues. Novartis Found Symp 273:126-138
36. Saroussi S, Nelson N (2009) Vacuolar H(+)-ATPase-an enzyme for all seasons. Pflugers Arch 457(3):581-587, Review
37. Saroussi S, Nelson N (2009) The little we know on the structure and machinery of V-ATPase. J Exp Biol 12:1604-1610, Review
38. 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 281:37962-37971 (Pubitemid 46042100)
39. - in cerebellar granule cells affects their excitability and vestibulo-ocular learning. EMBO I 31:1217-1230
40. 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 Ren Physiol 280:F356-F364
41. Soleimani M, Xu J (2006) SLC26 chloride/base exchangers in the kidney in health and disease. Semin Nephrol 26(5):375-385 (Pubitemid 44634902)
42. Stadler H, Tsukita S (1984) Synaptic vesicles contain an ATP-dependent proton pump and show 'knob-like' protrusions on their surface. EMBO J 3:3333-3337
43. Strauss O, Neussert R, Müller C, Milenkovic VM (2012) A potential cytosolic function of bestrophin-1. Adv Exp Med Biol 723:603-610, Review
44. Takahashi KI, Copenhagen DR (1996) Modulation of neuronal function by intracellular pH. Neurosci Res 24(2):109-116 (Pubitemid 26048186)
45. Tornberg J, Voikar V, Savilahti H et al (2005) Behavioral phenotype of hypomorphic KCC2-deficient mice. J Eur J NeuroSci 21:1327-1337 (Pubitemid 40516631)
46. Vincourt JB, Jullien D, Amalric F, Girard JP (2003) Molecular and functional characterization of SLC26A11, a sodium-independent sulfate transporter from high endothelial venules. FASEB J 17:890-892
47. Walcott BP, Kahle KT, Simard JM (2012) Novel treatment targets for cerebral edema. Neurotherapeutics 9(1):65-72, Review
48. Wellhauser L, D'Antonio C, Bear CE (2010) ClC transporters: discoveries and challenges in defining the mechanisms underlying function and regulation of ClC-5. Pflugers Arch 460(2):543-557, Review
49. Weyler R, Yurko-Mauro K, Rubenstein R et al (1999) CFTR is functionally active in GnRH-expressing GT1-7 hypothalamic neurons. Am J Physiol Cell Physiol 277:C563-C571
50. Wulff P, Schonewille M, Renzi M, Viltono L, Sassoè-Pognetto M, Badura A, Gao Z, Hoebeek FE, van Dorp S, Wisden W, Farrant M, De Zeeuw CI (2009) Synaptic inhibition of Purkinje cells mediates consolidation of vestibulo-cerebellar motor learning. Nat Neurosci 12(8):1042-1049
51. 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(43):29470-29479
52. 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(9):926-937
53. Xu J, Song P, Miller ML, Borgese F, Barone S, Riederer B, Wang Z, Alper SL, Forte JG, Shull GE, Ehrenfeld J, Seideler 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 U S A 105(46):17955-17960
54. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, Park SP, Lee J, Lee B, Kim BM, Raouf R, Shin YK, Oh U (2008) TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455(7217):1210-1215
55. Yao G, Feng H, Cai Y, Qi W, Kong K (2007) Characterization of vacuolar-ATPase and selective inhibition of vacuolar-H(+)-ATPase in osteoclasts. Biochem Biophys Res Commun 357(4):821-827, Review (Pubitemid 46693667)
56. B receptors in mammalian brain: potential targets for drug development. J Drug Dev Res 21:161-167
57. Zhang Z, Nguyen KT, Barrett EF, David G (2010) Vesicular ATPase inserted into the plasma membrane of motor terminals by exocytosis alkalinizes cytosolic pH and facilitates endocytosis. Neuron 68(6):1097-1108