Sex-independent expression of chloride/formate exchanger Cfex (Slc26a6) in rat pancreas, small intestine, and liver, and male-dominant expression in kidneys

Karaica, Dean; Breljak, Davorka; Lončar, Jovica; Lovrić, Mila; Micek, Vedran; Vrhovac Madunić, Ivana; Brzica, Hrvoje; Herak-Kramberger, Carol M.; Dupor, Jana Ivković; Ljubojević, Marija; Smital, Tvrtko; Vogrinc, Željka; Burckhardt, Gerhard; Burckhardt, Birgitta C.; Sabolić, Ivan

doi:10.2478/aiht-2018-69-3157

References

1. Alper SL, Sharma AK. The SLC26 gene family of anion transporters and channels. Mol Aspects Med 2013;34:494-515. doi: 10.1016/j.mam.2012.07.009
Open DOI Search in Google Scholar Back to article
2. Brzica H, Breljak D, Burckhardt BC, Burckhardt G, Sabolić I. Oxalate: from the environment to kidney stones. Arh Hig Rada Toksikol 2013;64:609-30. doi: 10.2478/10004-1254-64-2013-2428
Open DOI Search in Google Scholar Back to article
3. Mount DB, Romero MF. The SLC26 gene family of multifunctional anion exchangers. Pflug Arch Eur J Phy 2004;447:710-21. doi: 10.1007/s00424-003-1090-3
Open DOI Search in Google Scholar Back to article
4. Steward MC, Ishiguro H. Molecular and cellular regulation of pancreatic duct cell function. Curr Opin Gastroen 2009;25:447-53. doi: 10.1097/MOG.0b013e32832e06ce
Open DOI Search in Google Scholar Back to article
5. Chernova MN, Jiang L, Friedman DJ, Darman RB, Lohi H, Kere J, Vandorpe DH, Alper SL. Functional comparison of mouse slc26a6 anion exchanger with human SLC26A6 polypeptide variants: differences in anion selectivity, regulation, and electrogenicity. J Biol Chem 2005;280:8564-80. doi: 10.1074/jbc.M411703200
Open DOI Search in Google Scholar Back to article
6. Ishiguro H, Namkung W, Yamamoto A, Wang Z, Worrell RT, Xu J, Lee MG, Soleimani M. Effect of Slc26a6 deletion on apical Cl-/HCO³- exchanger activity and cAMP-stimulated bicarbonate secretion in pancreatic duct. Am J Physiol-Gastr L 2007;292:G447-55. doi: 10.1152/ajpgi.00286.2006
Open DOI Search in Google Scholar Back to article
7. Simpson JE, Schweinfest CW, Shull GE, Gawenis LR, Walker NM, Boyle KT, Soleimani M, Clarke LL. PAT-1 (Slc26a6) is the predominant apical membrane Cl-/HCO3- exchanger in the upper villous epithelium of the murine duodenum. Am J Physiol-Gastr L 2007;292:G1079-88. doi: 10.1152/ajpgi.00354.2006
Open DOI Search in Google Scholar Back to article
8. Stewart AK, Shmukler BE, Vandorpe DH, Reimold F, Heneghan JF, Nakakuki M, Akhavein A, Ko S, Ishiguro H, Alper SL. SLC26 anion exchangers of guinea pig pancreatic duct: molecular cloning and functional characterization. Am J Physiol-Cell Ph 2011;301:C289-303. doi: 10.1152/ajpcell.00089.2011
Open DOI Search in Google Scholar Back to article
9. Stewart AK, Yamamoto A, Nakakuki M, Kondo T, Alper SL, Ishiguro H. Functional coupling of apical Cl-/HCO3- exchange with CFTR in stimulated HCO3- secretion by guinea pig interlobular pancreatic duct. Am J Physiol-Gastr L 2009;296:G1307-17. doi: 10.1152/ajpgi.90697.2008
Open DOI Search in Google Scholar Back to article
10. Petrović S, Ma L, Wang Z, Soleimani M. Identification of an apical Cl-/HCO3- exchanger in rat kidney proximal tubule. Am J Physiol-Cell Ph 2003;285:C608-17. doi: 0.1152/ajpcell.00084.2003
Open DOI Search in Google Scholar Back to article
11. Thomson RB, Wang T, Thomson BR, Tarrats L, Girardi A, Mentone S, Soleimani M, Kocher O, Aronson PS. Role of PDZK1 in membrane expression of renal brush border ion exchangers. P Natl Acad Sci USA 2005;102:13331-6. doi: 10.1073/pnas.0506578102
Open DOI Search in Google Scholar Back to article
12. Kujala M, Tienari J, Lohi H, Elomaa O, Sariola H, Lehtonen E, Kere J. SLC26A6 and SLC26A7 anion exchangers have a distinct distribution in human kidney. Nephron Exp Nephrol 2005;101:e50-8. doi: 10.1159/000086345
Open DOI Search in Google Scholar Back to article
13. Lohi H, Kujala M, Kerkelä E, Saarialho-Kere U, Kestilä M, Kere J. Mapping of five new putative anion transporter genes in human and characterization of SLC26A6, a candidate gene for pancreatic anion exchanger. Genomics 2000;70:102-12. doi: 10.1006/geno.2000.6355
Open DOI Search in Google Scholar Back to article
14. Lohi H, Lamprecht G, Markovich D, Heil A, Kujala M, Seidler U, Kere J. Isoforms of SLC26A6 mediate anion transport and have functional PDZ interaction domains. Am J Physiol-Cell Ph 2003;284:C769-79. doi: 10.1152/ajpcell.00270.2002
Open DOI Search in Google Scholar Back to article
15. Waldegger S, Moschen I, Ramirez A, Smith RJ, Ayadi H, Lang F, Kubisch C. Cloning and characterization of SLC26A6, a novel member of the solute carrier 26 gene family. Genomics 2001;72:43-50. doi: 10.1006/geno.2000.6445
Open DOI Search in Google Scholar Back to article
16. Knauf F, Yang CL, Thomson RB, Mentone SA, Giebisch G, Aronson PS. Identification of a chloride-formate exchanger expressed on the brush border membrane of renal proximal tubule cells. P Natl Acad Sci USA 2001;98:9425-30. doi: 10.1073/pnas.141241098
Open DOI Search in Google Scholar Back to article
17. Xie Q, Welch R, Mercado A, Romero MF, Mount DB, Michael F. Molecular characterization of the murine Slc26a6 anion exchanger: functional comparison with Slc26a1. Am J Physiol-Renal 2002;283:F826-38. doi: 10.1152/ajprenal.00079.2002
Open DOI Search in Google Scholar Back to article
18. Wang Z, Petrović S, Mann E, Soleimani M. Identification of an apical Cl-/HCO3- exchanger in the small intestine. Am J Physiol-Gastr L 2002;282:G573-9. doi: 10.1152/ajpgi.00338.2001
Open DOI Search in Google Scholar Back to article
19. Gholami K, Muniandy S, Salleh N. Progesterone downregulates oestrogen-induced expression of CFTR and SLC26A6 proteins and mRNA in rats’ uteri. J Biomed Biotechnol 2012;2012:596084. doi: 10.1155/2012/596084
Open DOI Search in Google Scholar Back to article
20. García M, Hernández-Lorenzo P, San Román JI, Calvo JJ. Pancreatic duct secretion: experimental methods, ion transport mechanisms and regulation. J Physiol Biochem 2008;64:243-57. doi: 10.1007/BF03178846
Open DOI Search in Google Scholar Back to article
21. Saint-Criq V, Gray MA. Role of CFTR in epithelial physiology. Cell Mol Life Sci 2016;74:93-115. doi: 10.1007/s00018-016-2391-y
Open DOI Search in Google Scholar Back to article
22. Petrović S, Wang Z, Ma L, Seidler U, Forte JG, Shull GE, Soleimani M. Colocalization of the apical Cl-/HCO3- exchanger PAT1 and gastric H-K-ATPase in stomach parietal cells. Am J Physiol-Gastr L 2002;283:G1207-16. doi: 0.1152/ajpgi.00137.2002
Open DOI Search in Google Scholar Back to article
23. Alvarez BV, Kieller DM, Quon AL, Markovich D, Casey JR. Slc26a6: a cardiac chloride-hydroxyl exchanger and predominant chloride-bicarbonate exchanger of the mouse heart. J Physiol 2004;561:721-34. doi: 10.1113/jphysiol.2004.077339
Open DOI Search in Google Scholar Back to article
24. Kim HJ, Myers R, Sihn C-R, Rafizadeh S, Zhang X-D. Slc26a6 functions as an electrogenic Cl-/HCO3- exchanger in cardiac myocytes. Cardiovasc Res 2013;100:383-91. doi: 10.1093/cvr/cvt195
Open DOI Search in Google Scholar Back to article
25. Aronson PS. Essential roles of CFEX-mediated Cl--oxalate exchange in proximal tubule NaCl transport and prevention of urolithiasis. Kidney Int 2006;70:1207-13. doi: 10.1038/sj.ki.5001741
Open DOI Search in Google Scholar Back to article
26. Freel RW, Hatch M, Green M, Soleimani M. Ileal oxalate absorption and urinary oxalate excretion are enhanced in Slc26a6 null mice. Am J Physiol-Gastr L 2006;290:G719-28. doi: 10.1152/ajpgi.00481.2005
Open DOI Search in Google Scholar Back to article
27. Greeley T, Shumaker H, Wang Z, Schweinfest CW, Soleimani M. Downregulated in adenoma and putative anion transporter are regulated by CFTR in cultured pancreatic duct cells. Am J Physiol-Gastr L 2001;281:G1301-8. doi: 10.1152/ajpgi.2001.281.5.G1301
Open DOI Search in Google Scholar Back to article
28. Knauf F, Ko N, Jiang Z, Robertson WG, Van Itallie CM, Anderson JM, Aronson PS. Net intestinal transport of oxalate reflects passive absorption and SLC26A6-mediated secretion. J Am Soc Nephrol 2011;22:2247-55. doi: 10.1681/ASN.2011040433
Open DOI Search in Google Scholar Back to article
29. Wang Z, Wang T, Petrović S, Tuo B, Riederer B, Barone SL, Lorenz JN, Seidler U, Aronson PS, Soleimani M. Renal and intestinal transport defects in Slc26a6-null mice. Am J Physiol-Cell Ph 2005;288:C957-65. doi: 10.1152/ajpcell.00505.2004
Open DOI Search in Google Scholar Back to article
30. Thomson RB, Thomson CL, Aronson PS. N-glycosylation critically regulates function of oxalate transporter SLC26A6. Am J Physiol-Cell Ph 2016;311:C866-73. doi: 10.1152/ajpcell.00171.2016
Open DOI Search in Google Scholar Back to article
31. Hassan HA, Mentone S, Karniski LP, Rajendran VM, Aronson PS. Regulation of anion exchanger Slc26a6 by protein kinase C. Am J Physiol-Cell Ph 2007;292:C1485-92. doi: 10.1152/ajpcell.00447.2006
Open DOI Search in Google Scholar Back to article
32. Ohana E, Shcheynikov N, Moe OW, Muallem S. SLC26A6 and NaDC-1 transporters interact to regulate oxalate and citrate homeostasis. J Am Soc Nephrol 2013;24:1617-26. doi: 10.1681/ASN.2013010080
Open DOI Search in Google Scholar Back to article
33. Dawson PA, Russell CS, Lee S, McLeay SC, van Dongen JM, Cowley DM, Clarke LA, Markovich D. Urolithiasis and hepatotoxicity are linked to the anion transporter Sat1 in mice. J Clin Invest 2010;120:706-12. doi: 10.1172/JCI31474
Open DOI Search in Google Scholar Back to article
34. Jiang Z, Asplin JR, Evan AP, Rajendran VM, Velazquez H, Nottoli TP, Binder HJ, Aronson PS. Calcium oxalate urolithiasis in mice lacking anion transporter Slc26a6. Nat Genet 2006;38:474-8. doi: 10.1038/ng1762
Open DOI Search in Google Scholar Back to article
35. Robijn S, Hoppe B, Vervaet BA, D’Haese PC, Verhulst A. Hyperoxaluria: a gut-kidney axis? Kidney Int 2011;80:1146-58. doi: 10.1038/ki.2011.287
Open DOI Search in Google Scholar Back to article
36. Romero V, Akpinar H, Assimos DG. Kidney stones: a global picture of prevalence, incidence, and associated risk factors. Rev Urol 2010:12:e86-96. doi: 10.3909/riu0459
Open DOI Search in Google Scholar Back to article
37. Brzica H, Breljak D, Krick W, Lovrić M, Burckhardt G, Burckhardt BC, Sabolić I. The liver and kidney expression of sulfate anion transporter sat-1 in rats exhibits maledominant gender differences. Pflug Arch Eur J Phy 2009;457:1381-92. doi: 10.1007/s00424-008-0611-5
Open DOI Search in Google Scholar Back to article
38. Ko N, Knauf F, Jiang Z, Markovich D, Aronson PS. Sat1 is dispensable for active oxalate secretion in mouse duodenum. Am J Physiol-Cell Ph 2012;303:C52-7. doi: 10.1152/ajpcell.00385.2011
Open DOI Search in Google Scholar Back to article
39. Freel RW, Hatch M. Hyperoxaluric rats do not exhibit alterations in renal expression patterns of Slc26a1 (SAT1) mRNA or protein. Urol Res 2012;40:647-54. doi: 10.1007/s00240-012-0480-4
Open DOI Search in Google Scholar Back to article
40. Breljak D, Brzica H, Vrhovac I, Micek V, Karaica D, Ljubojević M, Sekovanić A, Jurasović J, Rašić D, Peraica M, Lovrić M, Schnedler N, Henjakovic M, Wegner W, Burckhardt G, Burckhardt BC, Sabolić. In female rats, ethylene glycol treatment elevates protein expression of hepatic and renal oxalate transporter sat-1 (Slc26a1) without inducing hyperoxaluria. Croat Med J 2015;56:447-59. doi: 10.3325/cmj.2015.56.447
Open DOI Search in Google Scholar Back to article
41. Koressaar T, Remm M. Enhancements and modifications of primer design program Primer3. Bioinformatics 2007;23:1289-1291. doi: 10.1093/bioinformatics/btm09117379693
Open DOI Search in Google Scholar Back to article
42. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. Primer3--new capabilities and interfaces. Nucleic Acids Res 2012;40:e115. doi: 10.1093/nar/gks596
Open DOI Search in Google Scholar Back to article
43. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC T method. Methods 2001;25:402-8. doi: 10.1006/meth.2001.126211846609
Open DOI Search in Google Scholar Back to article
44. Sambrook JF, Fritsch EF, Maniatis T. Molecular Cloning - A Laboratory Manual. 3rd ed. New York: Cold Spring Harb Lab Press; 1989. ISBN 978-1-936113-41-5
Search in Google Scholar Back to article
45. Tom R, Bisson L, Durocher Y. Transfection of adherent HEK293-EBNA1 cells in a six-well plate with branched PEI for production of recombinant proteins. CSH Protoc 2008;2008:pdb.prot4978. doi: 10.1101/pdb.prot4978
Open DOI Search in Google Scholar Back to article
46. Popović M, Žaja R, Fent K, Smital T. Molecular characterization of zebrafish Oatp1d1 (Slco1d1), a novel organic anion-transporting polypeptide. J Biol Chem 2013;288:33894-911. doi: 10.1074/jbc.M113.518506
Open DOI Search in Google Scholar Back to article
47. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54. doi: 10.1016/0003-2697(76)90527-3
Open DOI Search in Google Scholar Back to article
48. Brzica H, Breljak D, Vrhovac I, Sabolić I. Role of microwave heating in antigen retrieval in cryosections of formalin-fixed tissues. In: Chandra U, editor. Microwave heating. Rijeka: IN-TECH Open; 2011. p. 41-62. doi: 10.5772/20319
Open DOI Search in Google Scholar Back to article
49. Lee MG, Ohana E, Park HW, Yang D, Muallem S. Molecular mechanism of pancreatic and salivary gland fluid and HCO3 - secretion. Physiol Rev 2012;92:39-74. doi: 10.1152/physrev.00011.2011
Open DOI Search in Google Scholar Back to article
50. Clark JS, Vandorpe DH, Chernova MN, Heneghan JF, Stewart AK, Alper SL. Species differences in Cl- affinity and in electrogenicity of SLC26A6-mediated oxalate/Cl- exchange correlate with the distinct human and mouse susceptibilities to nephrolithiasis. J Physiol 2008;586:1291-306. doi: 10.1113/jphysiol.2007.143222
Open DOI Search in Google Scholar Back to article
51. Garcia-Perez I, Villaseñor A, Wijeyesekera A, Posma JM, Stamler J, Aronson P, Unwin R, Barbas C, Elliott P, Nicholson J, Holmes E. Urinary metabolic phenotyping the slc26a6 (chloride-oxalate exchanger) null mouse model. J Proteome Res 2012;11:4425-35. doi: 10.1021/pr2012544
Open DOI Search in Google Scholar Back to article
52. Jiang Z, Grichtchenko II, Boron WF, Aronson PS. Specificity of anion exchange mediated by mouse Slc26a6. J Biol Chem 2002;277:33963-7. doi: 10.1074/jbc.M202660200
Open DOI Search in Google Scholar Back to article
53. Karniski LP, Lötscher M, Fucentese M, Hilfiker H, Biber J, Murer H. Immunolocalization of sat-1 sulfate/oxalate/ bicarbonate anion exchanger in the rat kidney. Am J Physiol- Renal 1998;275:F79-87. doi: 10.1152/ajprenal.1998.275.1.F79
Open DOI Search in Google Scholar Back to article
54. Costello JF, Smith M, Stolarski C, Sadovnic MJ. Extrarenal clearance of oxalate increases with progression of renal failure in the rat. J Am Soc Nephrol 1992;3:1098-104. PMID: 1482750148275010.1681/ASN.V351098
Search in Google Scholar Back to article
55. Hatch M, Freel RW, Vaziri ND. Intestinal excretion of oxalate in chronic renal failure. J Am Soc Nephrol 1994;5:1339-43. PMID: 789399910.1681/ASN.V561339
Search in Google Scholar Back to article
56. Green ML, Hatch M, Freel RW. Ethylene glycol induces hyperoxaluria without metabolic acidosis in rats. Am J Physiol-Renal 2005;289:F536-43. doi: 10.1152/ajprenal.00025.2005
Open DOI Search in Google Scholar Back to article
57. Iguchi M, Takamura C, Umekawa T, Kurita T, Kohri K. Inhibitory effects of female sex hormones on urinary stone formation in rats. Kidney Int 1999;56:479-85. doi: 10.1046/j.1523-1755.1999.00586.x10432386
Open DOI Search in Google Scholar Back to article
58. Lee YH, Huang WC, Huang JK, Chang LS. Testosterone enhances whereas estrogen inhibits calcium oxalate stone formation in ethylene glycol treated rats. J Urology 1996;156:502-5. PMID: 868372510.1016/S0022-5347(01)65914-7
Search in Google Scholar Back to article
59. Farinelli MP, Richardson KE. Oxalate synthesis from [14C1] glycollate and [14C1]glycoxylate in the hepatectomized rat. Biochim Biophys Acta 1983;757:8-14. doi: 10.1016/0304-4165(83)90146-0
Open DOI Search in Google Scholar Back to article
60. Meier PJ, Valantinas J, Hugentobler G, Rahm I. Bicarbonate/ sulfate (electroneutral), bicarbonate/oxalate or sulfate/oxalate exchange in canalicular rat liver plasma mebrane vesicles. Am J Physiol-Gastr L 1987;253:G461-8. doi: 10.1152/ajpgi.1987.253.4.G461
Open DOI Search in Google Scholar Back to article
61. Boyer JL. Bile formation and secretion. Compr Physiol 2013;3:1035-78. doi: 10.1002/cphy.c120027
Open DOI Search in Google Scholar Back to article
62. Sugimoto T, Osswald H, Yamamoto K, Kanazawa T, Iimori H, Funae Y, Kamokawa S, Kishimoto T. Fate of circulating oxalate in rats. Eur Urol 1993;23:485-9. doi: 10.1159/000474659.8335055
Open DOI Search in Google Scholar Back to article

Sex-independent expression of chloride/formate exchanger Cfex (Slc26a6) in rat pancreas, small intestine, and liver, and male-dominant expression in kidneys

References

Paradigm

My account