Substrate specificity of the electrogenic sodium/bicarbonate cotransporter NBCe1-A (SLC4A4, variant A) from humans and rabbits

American Journal of Physiology - Renal Physiology

Volumn 304, Issue 7, 2013, Pages

  Lee, Seong Ki ^a   Boron, Walter F ^a   Parker, Mark D ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Benzamil; Carbonate; Harmaline; NBC1; Nitrate

Indexed keywords

BICARBONATE; BICARBONATE SODIUM COTRANSPORTER; HARMALINE; LITHIUM ION; NBCE1 A PROTEIN; OXALIC ACID; SODIUM ION; SULFITE; UNCLASSIFIED DRUG; 4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; AMILORIDE; BENZAMIL; DRUG DERIVATIVE; NITRATE; OXALIC ACID DERIVATIVE; SLC4A4 PROTEIN, HUMAN; SODIUM;

ANIMAL CELL; ARTICLE; CLONING; CONTROLLED STUDY; ENZYME SPECIFICITY; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; SODIUM TRANSPORT; STOICHIOMETRY; THERMODYNAMICS; XENOPUS; ANIMAL; DRUG EFFECT; HUMAN; KIDNEY; METABOLISM; RABBIT;

4,4'-DIISOTHIOCYANOSTILBENE-2,2'-DISULFONIC ACID; AMILORIDE; ANIMALS; BICARBONATES; HARMALINE; HUMANS; KIDNEY; NITRATES; OXALATES; RABBITS; SODIUM; SODIUM-BICARBONATE SYMPORTERS; SUBSTRATE SPECIFICITY; SULFITES;

MLCS; MLOWN;

EID: 84878252077     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00612.2012     Document Type: Article

References (58)

1. Abuladze N, Lee I, Newman D, Hwang J, Boorer K, Pushkin A, Kurtz I. Molecular cloning, chromosomal localization, tissue distribution, and functional expression of the human pancreatic sodium bicarbonate cotransporter. J Biol Chem 273: 17689-17695, 1998.
2. +/carbonate cotransport in rabbit renal cortical basolateral membrane-vesicles (BLMV). Clin Res 35: A633-A633, 1987.
3. Alvarado F, Brot-Laroche E, L'Herminier M, Murer H, Stange G. The effect of harmaline on intestinal sodium transport and on sodium-dependent D-glucose transport in brush-border membrane vesicles from rabbit jejunum. Pflügers Arch 382: 35-41, 1979.
4. +:HCO3 cotransporter. J Biol Chem 273: 16810-16815, 1998.
5. Aronson PS, Bounds SE. Harmaline inhibition of Na-dependent transport in renal microvillus membrane vesicles. Am J Physiol Renal Fluid Electrolyte Physiol 238: F210-F217, 1980.
6. Bevensee MO, Schmitt BM Choi I, Romero MF, Boron WF. An electrogenic Na/HCO3 cotransporter (NBC) with a novel C terminus, cloned from rat brain. Am J Physiol Cell Physiol 278: C1200-C1211, 2000.
7. Boron WF, Boulpaep EL. Intracellular pH regulation in the renal proximal tubule of the salamander: basolateral HCO3 transport. J Gen Physiol 81: 53-94, 1983.
8. Boron WF, Chen L, Parker MD. Modular structure of sodium-coupled bicarbonate transporters. J Exp Biol 212: 1697-1706, 2009.
9. + and HCO3 dependences. J Gen Physiol 85: 325-345, 1985.
10. +:HCO3 cotransporter. J Biol Chem272: 19111-19114, 1997.
11. Capewell S, Hefter G, Sipos P, May P. Protonation and sodium ion-pairing of the sulfite ion in concentrated aqueous electrolyte solutions. J Solution Chem 26: 957-972, 1997.
12. Choi I, Aalkjær C, Boulpaep EL, Boron WF. An electroneutral sodium/ bicarbonate cotransporter NBCn1 and associated sodium channel. Nature 405: 571-575, 2000.
13. +-HCO3 cotransporter (NBCe1). Am J Physiol Renal Physiol 284: F1199-F1206, 2003.
14. Ducoudret O, Diakov A, Muller-Berger S, Romero MF, Frömter E. The renal Na-HCO3 cotransporter expressed in Xenopus laevis oocytes: inhibition by tenidap and benzamil and effect of temperature on transport rate and stoichiometry. Pflügers Arch 442: 709-717, 2001.
15. +/HCO3 co-transport in basolateral membrane vesicles isolated from rabbit renal cortex. J Biol Chem 261: 8778-8783, 1986.
16. Grassl SM, Holohan PD, Ross CR. HCO3 transport in basolateral membrane vesicles isolated from rat renal cortex. J Biol Chem 262: 2682-2687, 1987.
17. = transport (Abstract). FASEB J 16: A795, 2002.
18. +-driven Cl-HCO3 exchanger. J Biol Chem 276: 8358-8363, 2001.
19. Grichtchenko II, Romero MF, Boron WF. Extracellular HCO3 dependence of electrogenic Na/HCO3 cotransporters cloned from salamander and rat kidney. J Gen Physiol 115: 533-545, 2000.
20. Gross E, Hawkins K, Abuladze N, Pushkin A, Cotton CU, Hopfer U, Kurtz I. The stoichiometry of the electrogenic sodium bicarbonate cotransporter NBC1 is cell-type dependent. J Physiol 531: 597-603, 2001.
21. +-HCO3 cotransporter expressed in Xenopus laevis oocytes. Pflügers Arch 438: 322-329, 1999.
22. Horita S, Yamada H, Inatomi J, Moriyama N, Sekine T, Igarashi T, Endo Y, Dasouki M, Ekim M, Al Gazali L, Shimadzu M, Seki G, Fujita T. Functional analysis of NBC1 mutants associated with proximal renal tubular acidosis and ocular abnormalities. J Am Soc Nephrol 16: 2270-2278, 2005.
23. Humphreys BD, Jiang L, Chernova MN, Alper SL. Functional characterization and regulation by pH of murine AE2 anion exchanger expressed in Xenopus oocytes. Am J Physiol Cell Physiol 267: C1295-C1307, 1994.
24. Igarashi T, Inatomi J, Sekine T, Cha SH, Kanai Y, Kunimi M, Tsukamoto K, Satoh H, Shimadzu M, Tozawa F, Mori T, Shiobara M, Seki G, Endou H. Mutations in SLC4A4 cause permanent isolated proximal renal tubular acidosis with ocular abnormalities. Nat Genet 23: 264-266, 1999.
25. Kao L, Sassani P, Azimov R, Pushkin A, Abuladze N, Peti-Peterdi J, Liu W, Newman D, Kurtz I. Oligomeric structure and minimal functional unit of the electrogenic sodium bicarbonate cotransporter NBCe1-A. J Biol Chem 283: 26782-26794, 2008.
26. Karniski LP, Lotscher M Fucentese M, Hilfiker H, Biber H, Murer H. Immunolocalization of sat-1 sulfate/oxalate/bicarbonate anion exchanger in the rat kidney. Am J Physiol Renal Physiol 275: F79-F87, 1998.
27. Krick W, Schnedler N, Burckhardt G, Burckhardt BC. Ability of sat-1 to transport sulfate, bicarbonate, or oxalate under physiological conditions. Am J Physiol Renal Physiol 297: F145-F154, 2009.
28. Lee SK, Boron WF, Parker MD. Relief of autoinhibition of the electrogenic Na/HCO3 cotransporter NBCe1-B: role of IRBIT versus amino-terminal truncation. Am J Physiol Cell Physiol 302: C518-C526, 2012.
29. = transport by NBCe1-A (Abstract). FASEB J 25: 656.9, 2011.
30. Liu Y, Xu JY, Wang DK, Wang L, Chen LM. Cloning and identification of two novel NBCe1 splice variants from mouse reproductive tract tissues: a comparative study of NCBT genes. Genomics 98: 112-119, 2011.
31. Lu J, Boron WF. Reversible and irreversible interactions of DIDS with the human electrogenic Na/HCO3 cotransporter NBCe1-A: role of lysines in the KKMIK motif of TM5. Am J Physiol Cell Physiol 292: C1787-C1798, 2007.
32. Maunsbach AB, Vorum H, Kwon TH, Nielsen S, Simonsen B, Choi I, Schmitt BM, Boron WF, Aalkjær C. Immunoelectron microscopic localization of the electrogenic Na/HCO3 cotransporter in rat and Amby-stoma kidney. J Am Soc Nephrol 11: 2179-2189, 2000.
33. McAlear SD, Liu X, Williams JB, McNicholas-Bevensee CM, Bevensee MO. Electrogenic Na/HCO3 cotransporter (NBCe1) variants expressed in Xenopus oocytes: functional comparison and roles of the amino and carboxy termini. J Gen Physiol 127: 639-658, 2006.
34. Musa-Aziz R, Boron WF, Parker MD. Using fluorometry and ion-sensitive microelectrodes to study the functional expression of heterolo-gously-expressed ion channels and transporters in Xenopus oocytes. Methods 51: 134-145, 2010.
35. Parker MD, Boron WF. The divergence, actions, roles, and relatives of sodium-coupled bicarbonate transporters. Physiol Rev. In press.
36. Parker MD, Musa-Aziz R, Rojas JD, Choi I, Daly CM, Boron WF. Characterization of human SLC4A10 as an electroneutral Na/HCO3 cotransporter (NBCn2) with Cl~ self-exchange activity. J Biol Chem 283: 12777-12788, 2008.
37. +/HCO3 cotransporter (SLC4A4) in a case of proximal renal tubular acidosis with hypokalemic paralysis. J Physiol 590: 2009-2034, 2012.
38. Perry DL, Phillips SL. Handbook of Inorganic Compounds. Boca Raton, FL: CRC, 1995.
39. Rawn JD. Proteins, energy, metabolism. Burlington, NC: N. Patterson, 1989.
40. +-HCO3 cotransporter from rat kidney. Am J Physiol Renal Physiol 274: F425-F432, 1998.
41. Romero MF, Fulton CM, Boron WF. The SLC4 family of HCO3 transporters. Pflügers Arch 447: 495-509, 2004.
42. +/HCO3 cotransporter. Nature 387: 409-413, 1997.
43. Ruiz OS, Qiu YY, Arruda JA. The renal cortical Na-HCO3 cotransporter: V. Expression in Xenopus oocytes. Proc Soc Exp Biol Med 211: 199-204, 1996.
44. Samarzija I, Kinne-Saffran E, Baumann K, Frömter E. The mechanism of action of harmaline on renal solute transport. Pflügers Arch 368: 83-88, 1977.
45. Sassani P, Pushkin A, Abuladze N, Azimov R Kao L, Peti-Peterdi J, Liu W, Newman D, Kurtz I. Role of S-S bond formation in the oligomerization of kNBC1 (NBCe1-A) (Abstract). FASEB J 21: 916.3, 2007.
46. Schmitt BM, Biemesderfer D, Romero MF, Boulpaep EL, Boron WF. Immunolocalization of the electrogenic Na+/HCO cotransporter in mammalian and amphibian kidney. Am J Physiol Renal Physiol 276: F27-F36, 1999.
47. Sciortino CM. Characterization and Localization of the Sodium Mediated Bicarbonate Transporters NBC and NDAE1 (PhD thesis). Cleveland, OH: Case Western Reserve University, 2001.
48. +-HCO3 cotransporter, rkNBC, expressed in oocytes. Am J Physiol Renal Physiol 277: F611-F623, 1999.
49. + in isolated rabbit renal proximal tubule. Pflügers Arch 425: 409-416, 1993.
50. Sepulveda FV, Robinson JW. Harmaline, a potent inhibitor of sodium-dependent transport. Biochim Biophys Acta 373: 527-531, 1974.
51. Skelton LA, Boron WF, Zhou Y. Acid-base transport by the renal proximal tubule. J Nephrol 23: 4-18, 2010.
52. Soleimani M, Aronson PS. Ionic mechanism of sodium bicarbonate cotransport in rabbit renal basolateral membrane vesicles. J Biol Chem 264:31: 18302-18308, 1989.
53. +-HCO3~-cotransport in basolateral membrane vesicles isolated from rabbit renal cortex. J Clin Invest 79: 1276-1280, 1987.
54. 23~:HCO3 cotransporter in renal basolateral membrane vesicles. J Biol Chem 266: 8706-8710, 1991.
55. Toye AM, Parker MD, Daly CM, Lu J, Virkki LV, Pelletier MF, Boron WF. The human NBCe1-A mutant R881C, associated with proximal renal tubular acidosis, retains function but is mistargeted in polarized renal epithelia. Am J Physiol Cell Physiol 291: C788-C801, 2006.
56. Trudeau MC, Warmke JW, Ganetzky B, Robertson GA. HERG, a human inward rectifier on the voltage-gated potassium channel family. Science 269: 92-95, 1995.
57. +-driven Cl/HCO3 exchanger from squid giant fiber lobe. Am J Physiol Cell Physiol 285: C771-C780, 2003.
58. Yoshitomi K, Burckhardt BC, Frömter E. Rheogenic sodium-bicarbonate cotransport in the peritubular cell membrane of rat renal proximal tubule. Pflügers Arch 405: 360-366, 1985.