Evidence that SLC26 anion transporters mediate branchial chloride uptake in adult zebrafish (Danio rerio)

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 4, 2009, Pages

  Perry, S F ^a   Vulesevic, B ^a   Grosell, M ^b   Bayaa, M ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF MIAMI   (United States)

Author keywords

Acid base balance; Gill; Ionic regulation; Mitochondrion rich cell; Pendrin; SLC26a3; SLC26a4; SLC26a6

Indexed keywords

MESSENGER RNA;

ANION TRANSPORT; ARTICLE; CONTROLLED STUDY; GENE; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SLC26 GENE; ZEBRA FISH;

ACID-BASE EQUILIBRIUM; ADAPTATION, PHYSIOLOGICAL; AGE FACTORS; ANIMALS; BICARBONATES; BIOLOGICAL TRANSPORT; BRANCHIAL REGION; CHLORIDE-BICARBONATE ANTIPORTERS; CHLORIDES; GILLS; MITOCHONDRIA; RNA, MESSENGER; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 70349630424     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00327.2009     Document Type: Article

References (73)

1. Alper SL. Molecular physiology of SLC4 anion exchangers. Exp Physiol 91: 153-161, 2006.
2. - exchangers. J Nephrol 15, Suppl 5: S41-S53, 2002.
3. - exchange in zebrafish (Danio rerio) larvae. J Exp Biol. In Press.
4. Boisen AM, Amstrup J, Novak I, Grosell M. Sodium and chloride transport in soft water and hard water acclimated zebrafish (Danio rerio). Biochim Biophys Acta 1618: 207-218, 2003. (Pubitemid 38077145)
5. Cameron BA, Perry SF, Wu CB, Ko K, Tufts BL. Bicarbonate permeability and immunological evidence for an anion exchanger-like protein in the red blood cells of the sea lamprey, Petromyzon marinus. J Comp Physiol B 166: 197-204, 1996. (Pubitemid 26309630)
6. - uptake mechanism in freshwater-adapted tilapia (Oreochromis mossambicus). Physiol Biochem Zool 77: 406-414, 2004.
7. - channel regulated by the WNK kinases. J Physiol 584: 333-345, 2007.
8. Dorwart MR, Shcheynikov N, Yang D, Muallem S. The solute carrier 26 family of proteins in epithelial ion transport. Physiology 23: 104-114, 2008.
9. Epstein FH, Maetz J, DeRenzis G. Active transport of chloride by the teleost gill: inhibition by thiocyanate. Am J Physiol 224: 1295-1299, 1973.
10. Evans DH. Teleost fish osmoregulation: what have we learned since August Krogh, Homer Smith, and Ancel Keys. Am J Physiol Regul Integr Comp Physiol 295: R704-R713, 2008.
11. Galvez F, Reid SD, Hawkings G, Goss GG. Isolation and characterization of mitochondria-rich cell types from the gill of freshwater rainbow trout. Am J Physiol Regul Integr Comp Physiol 282: R658-R668, 2002. (Pubitemid 34665638)
12. Goss GG, Adamia S, Galvez F. Peanut lectin binds to a subpopulation of mitochondria-rich cells in the rainbow trout gill epithelium. Am J Physiol Regul Integr Comp Physiol 281: R1718-R1725, 2001. (Pubitemid 33116230)
13. Goss GG, Laurent P, Perry SF. Evidence for a morphological component in the regulation of acid-base balance in hypercapnic catfish (Ictalurus nebulosus). Cell Tiss Res 268: 539-552, 1992.
14. 3) and acid (HCl) infusions. Fish Physiol Biochem 12: 465-477, 1994.
15. +-pump metabolon? J Exp Biol 212: 1684-1696, 2009.
16. - cotransporter and CFTR anion channel. J Exp Biol 208: 2023-2036, 2005.
17. Hiroi J, Yasumasu S, McCormick SD, Hwang PP, Kaneko T. Evidence for an apical Na-Cl cotransporter involved in ion uptake in a teleost fish. J Exp Biol 211: 2584-2599, 2008.
18. Hwang PP. Ion uptake and acid secretion in zebrafish (Danio rerio). J Exp Biol 212: 1745-1752, 2009.
19. Hwang PP, Lee TH. New insights into fish ion regulation and mitochondrion-rich cells. Comp Biochem Physiol A 148: 479-497, 2007.
20. Inokuchi M, Hiroi J, Watanabe S, Hwang PP, Kaneko T. Morphological and functional classification of ion-absorbing mitochondria-rich cells in the gills of Mozambique tilapia. J Exp Biol 212: 1003-1010, 2009.
21. Ivanis G, Esbaugh AJ, Perry SF. Branchial expression and localization of SLC9A2 and SLC9A3 sodium hydrogen exchangers and their possible role in acid-base regulation in freshwater rainbow trout (Oncorhynchus mykiss). J Exp Biol 211: 2467-2477, 2008.
22. Katoh F, Tresguerres M, Lee KM, Kaneko T, Aida K, Goss GG. Cloning of rainbow trout SLC26A1: involvement in renal sulfate secretion. Am J Physiol Regul Integr Comp Physiol 290: R1468-R1478, 2006.
23. Kessel RG, Beams HW. Electron microscope studies on the gill filaments of Fundulus heteroclitus from sea water and fresh water with special reference to the ultrastructural organization of the "chloride cell". J Ultrastruct Res 6: 77-87, 1962.
24. - channel regulated by intracellular pH. J Biol Chem 280: 6463-6470, 2005.
25. Krogh A. Osmotic regulation in freshwater fishes by active absorption of chloride ions. Z Vergl Physiol 24: 656-666, 1937.
26. Krogh A. The active absorption of ions in some freshwater animals. Z Vergl Physiol 25: 335-350, 1938.
27. Kudrycki KE, Shull GE. Primary structure of the rat kidney band 3 anion exchange protein deduced from a cDNA. J Biol Chem 264: 8185-8192, 1989. (Pubitemid 19137306)
28. Kurita Y, Nakada T, Kato A, Doi H, Mistry AC, Chang MH, Romero MF, Hirose S. Identification of intestinal bicarbonate transporters involved in formation of carbonate precipitates to stimulate water absorption in marine teleost fish. Am J Physiol Regul Integr Comp Physiol 294: R1402-R1412, 2008.
29. - uptake in freshwater. Cell Tissue Res 325: 481-492, 2006.
30. Laurent P, Perry SF. Effects of cortisol on gill chloride cell morphology and ionic uptake on the freshwater trout, Salmo gairdneri. Cell Tiss Res 259: 429-442, 1990. (Pubitemid 20084081)
31. Lin LY, Hwang PP. Modification of morphology and function of integument mitochondria-rich cells in tilapia larvae (Oreochromis mossambicus) acclimated to ambient chloride levels. Physiol Biochem Zool 74: 469-476, 2001.
32. +-ATPase-rich cells. Am J Physiol Cell Physiol 294: C1250-C1260, 2008.
33. 2+ transport by fish gills: retrospective review and prospective synthesis. J Exp Zool 293: 264-283, 2002.
34. McDonald DG, Wood CM. Branchial and renal acid and ion fluxes in the rainbow trout, Salmo gairdneri, at low environmental pH. J Exp Biol 93: 101-118, 1981.
35. Morgan IJ, Potts WTW. The effects of thiocyanate on the intracellular ion concentrations in branchial epithelial cells of brown trout. J Exp Biol 198: 1229-1232, 1995.
36. Morgan I I, Potts W, Oates K. Intracellular ion concentrations in branchial epithelial cells of brown trout (Salmo trutta l) determined by X-ray microanalysis. J Exp Biol 194: 139-151, 1994. (Pubitemid 2135715)
37. Mount DB, Romero MF. The SLC26 gene family of multifunctional anion exchangers. Pflügers Arch 447: 710-721, 2004.
38. Nakada T, Zandi-Nejad K, Kurita Y, Kudo H, Broumand V, Kwon CY, Mercado A, Mount DB, Hirose S. Roles of Slc13a1 and Slc26a1 sulfate transporters of eel kidney in sulfate homeostasis and osmoregulation in freshwater. Am J Physiol Regul Integr Comp Physiol 289: R575-R585, 2005. (Pubitemid 41060513)
39. Ohana E, Yang D, Shcheynikov N, Muallem S. Diverse transport modes by the Solute Carrier 26 family of anion transporters. J Physiol 587: 2179-2185, 2009.
40. - transport in trout gill mitochondrion-rich cells. Am J Physiol Regul Integr Comp Physiol 296: R1161-R1169, 2009.
41. Perry SF. The chloride cell: structure and function in the gill of freshwater fishes. Annu Rev Physiol 59: 325-347, 1997.
42. 2 excretion in fish: unanswered questions and emerging models. Respir Physiol Neurobiol 154: 199-215, 2006.
43. Perry SF, Goss GG. The effects of experimentally altered gill chloride cell surface area on acid-base regulation in rainbow trout during metabolic alkalosis. J Comp Physiol A 164: 327-336, 1994.
44. Perry SF, Goss GG, Laurent P. The interrelationships between gill chloride cell morphology and ionic uptake in four freshwater teleosts. Can J Zool 70: 1737-1742, 1992.
45. Perry SF, Haswell MS, Randall DJ, Farrell AP. Branchial ionic uptake and acid-base regulation in the rainbow trout, Salmo gairdneri. J Exp Biol 92: 289-303, 1981.
46. Perry SF, Laurent P. Adaptational responses of rainbow trout to lowered external NaCl concentration: contribution of the branchial chloride cell. J Exp Biol 147: 147-168, 1989. (Pubitemid 20049034)
47. Perry SF, Randall DJ. Effects of amiloride and SITS on branchial ion fluxes in rainbow trout, Salmo gairdneri. J Exp Zool 215: 225-228, 1981.
48. Perry SF, Shahsavarani A, Georgalis T, Bayaa M, Furimsky M, Thomas SLY. Channels, pumps and exchangers in the gill and kidney of freshwater fishes: their role in ionic and acid-base regulation. J Exp Zool 300: 53-62, 2003. (Pubitemid 37529029)
49. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29: 2002-2007, 2001.
50. Piermarini PM, Verlander JW, Royaux IE, Evans DH. Pendrin immunoreactivity in the gill epithelium of a euryhaline elasmobranch. Am J Physiol Regul Integr Comp Physiol 283: R983-R992, 2002.
51. Pisam M, Auperin B, Prunet P, Rentierdelrue F, Martial J, Rambourg A. Effects of prolactin on α-chloride and β-chloride cells in the gill epithelium of the saltwater adapted tilapia Oreochromis niloticus. Anat Rec 235: 275-284, 1993. (Pubitemid 23015301)
52. Pisam M, Moal Le C, Auperin B, Prunet P, Rambourg A. Apical structures of mitochondria-rich α and β cells in euryhaline fish gill: their behaviour in various living conditions. Anat Rec 241: 13-24, 1995.
53. - transport in two species of freshwater fish. Physiol Biochem Zool 78: 259-272, 2005.
54. 2-) transporters: classification, function, structure, genetic diseases, and knockout models. Am J Physiol Renal Physiol 290: F580-F599, 2006.
55. + influx in isolated rainbow trout gill epithelial cells. J Exp Biol 206: 551-559, 2003.
56. Romero MF, Chang MH, Plata C, Zandi-Nejad K, Mercado A, Broumand V, Sussman CR, Mount DB. Physiology of electrogenic SLC26 paralogues. Novartis Found Symp 273: 126-138, 2006.
57. - transporters. Pflügers Arch 447: 495-509, 2004.
58. 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 98: 4221-4226, 2001.
59. - exchange by SLC26A3 and SLC26A6. J Gen Physiol 127: 511-524, 2006.
60. Shmukler BE, Clark JS, Hsu A, Vandorpe DH, Stewart AK, Kurschat CE, Choe SK, Zhou Y, Amigo J, Paw BH, Alper SL. Zebrafish ae2.2 encodes a second slc4a2 anion exchanger. Am J Physiol Regul Integr Comp Physiol 294: R1081-R1091, 2008. (Pubitemid 351346988)
61. Shmukler BE, Kurschat CE, Ackermann GE, Jiang L, Zhou Y, Barut B, Stuart-Tilley AK, Zhao J, Zon LI, Drummond IA, Vandorpe DH, Paw BH, Alper SL. Zebrafish slc4a2/ae2 anion exchanger: cDNA cloning, mapping, functional characterization, and localization. Am J Physiol Renal Physiol 289: F835-F849, 2005. (Pubitemid 41324205)
62. Sindic A, Chang MH, Mount DB, Romero MF. Renal physiology of SLC26 anion exchangers. Curr Opin Nephrol Hypertens 16: 484-490, 2007. (Pubitemid 47254701)
63. - exchangers in kidney and gastrointestinal tract. Novartis Found Symp 273: 91-102, 2006.
64. - exchanger in the kidney cortex. Am J Physiol Renal Physiol 280: F356-F364, 2001.
65. - exchanger in rainbow trout gill. Can J Zool 74: 2095-2103, 1996.
66. - cotransporter, cystic fibrosis transmembrane conductance regulator, anion, exchanger 1, and chloride channel 3 in gills of a euryhaline teleost, Tetraodon nigroviridis. Comp Biochem Physiol A 147: 521-528, 2007.
67. Tang CH, Lee TH. The novel correlation of carbonic anhydrase II and anion exchanger 1 in gills of the spotted green pufferfish, Tetraodon nigrovirids. J Exp Zool Part A Ecol Genet Physiol 307: 411-418, 2007.
68. Tresguerres M, Katoh F, Orr E, Parks SK, Goss GG. Chloride uptake and base secretion in freshwater fish: a transepithelial ion-transport metabolon? Physiol Biochem Zool 79: 981-996, 2006. (Pubitemid 44728730)
69. Verdouw H, van Echteld CJA, Dekkers EMJ. Ammonia determinations based on indophenol formation with sodium salicylate. Water Res 12: 399-402, 1978. (Pubitemid 8369301)
70. Wang YF, Tseng YC, Yan JJ, Hiroi J, Hwang PP. Role of SLC12A10.2, a Na-Cl cotransporter-like protein, in a Cl uptake mechanism in zebrafish (Danio rerio). Am J Physiol Regul Integr Comp Physiol 296: R1650-R1660, 2009.
71. Westerfield M. The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio). Eugene OR: University of Oregon Press, 2007.
72. Wilson JM, Laurent P, Tufts BL, Benos DJ, Donowitz M, Vogl AW, Randall DJ. NaCl uptake by the branchial epithelium in freshwater teleost fish: an immunological approach to ion-transport protein localization. J Exp Biol 203: 2279-2296, 2000. (Pubitemid 30656241)
73. Zall DM, Fisher MD, Garner QM. Photometric determination of chloride in water. Anal Chem 28: 1665-1678, 1956.