Clinical and Experimental Nephrology

, Volume 10, Issue 2, pp 102–110 | Cite as

Mechanism of iodide transport in the rabbit cortical collecting duct

  • Yohkazu Matsushima
  • Shigeaki Muto
  • Junichi Taniguchi
  • Masashi Imai
ORIGINAL ARTICLE

Abstract

Background

Pendrin, an anion exchanger known to participate in iodide transport in the apical membrane of follicular cells of the thyroid gland, has recently been shown to exist in the apical membrane of the β- and γ-intercalated (β/γ-IC) cells of the cortical collecting duct (CCD). We examined mechanisms of iodide transport in the CCD.

Methods

Rabbit CCD was perfused in vitro, and lumen-to-bath flux coefficients for both 125I (KI (lb)) and 36Cl (KCl (lb)) were measured simultaneously. The intracellular pH (pHi) of β/γ-IC cells in the perfused CCD was measured by microscopic fluorometory, by loading 2′,7′-bis-(2-carboxyethyl)-5(6)-carboxyfluorescein tetraacetoxy methylester (BCECF-AM), a fluorescent marker for pHi. The effects on pHi of the replacement of NaCl with Na cyclamate, NaI, or NaBr in the lumen or bath were observed.

Results

KI (lb) was comparable to or slightly higher than KCl (lb). Both iodide and chloride in the lumen caused self- and cross-inhibitions to both fluxes. The addition of 5-nitro-2-(-3-phenylpropylamino)-benzoate (NPPB), a Cl channel inhibitor, to the bath significantly reduced KCl (lb), but not KI (lb). Replacement of luminal fluid NaCl with Na cyclamate, NaI, or NaBr caused alkalization of pHi, no change in pHi, and slight acidification of pHi, respectively. Replacement of bath NaCl with Na cyclamate, NaI, or NaBr caused alkalization, alkalization, and acidification of pHi, respectively. Luminal NaI prevented the acidification of pHi caused by bath Na cyclamate.

Conclusions

The data are consistent with the model that iodide is transported via the Cl/HCO3 exchanger in the apical membrane of β/γ-IC cells and exits the basolateral membrane via an electroneutral transporter that is distinct from the Cl channel. We could not, however, identify which type of β/γ-IC cell was mainly responsible.

Key words

Iodide transport Pendrin β-/γ-Intercalated cells Cortical collecting duct Cl/HCO3 exchanger Cl channel 

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References

  1. 1.
    Halmi, NS 1961Thyroidal iodide transportVitam Horm1913363CrossRefGoogle Scholar
  2. 2.
    Dohan, O, DeLa Vieja, A, Paroder, V, Riedel, C, Artani, M, Reed, M,  et al. 2003The sodium/iodide symporter (NIS): characterization, regulation, and medical significanceEndocr Rev244877PubMedCrossRefGoogle Scholar
  3. 3.
    Katz, AI, Emmanouel, DS, Lindheimer, MD 1975Thyroid hormone and the kidneyNephron1522349PubMedCrossRefGoogle Scholar
  4. 4.
    US National Research Council1989Recommended dietary allowances. 10th ed. Iodine Food and Nutrition BoardNational Academy Press PublicationWashington DC2137Google Scholar
  5. 5.
    Park, YK, Harland, BF, Vanderveen, JE, Shank, FR, Prosky, L 1981Estimation of dietary iodine intake of Americans in recent yearsJ Am Diet Assoc791724PubMedGoogle Scholar
  6. 6.
    Everett, LA, Glaser, B, Beck, JC, Idol, JR, Buchs, A, Heyman, M,  et al. 1997Pendred syndrome is caused by mutations in a putative sulfate transporter gene (PDS)Nat Genet1741122PubMedCrossRefGoogle Scholar
  7. 7.
    Scott, DA, Wang, R, Kreman, TM, Schefield, VC, Karniski, LP 1999The Pendred syndrome gene encodes a chloride-iodide transport proteinNat Genet214403PubMedCrossRefGoogle Scholar
  8. 8.
    Gillam, MP, Sidhaye, AR, Lee, EJ, Rutishauser, J, Stephan, CW, Kopp, P 2004Functional characterization of pendrin in a polarized cell system. Evidence for pendrin-mediated apical iodine fluxJ Biol Chem2791300410PubMedCrossRefGoogle Scholar
  9. 9.
    Mitsuma, T, Rhue, N, Hirooka, Y, Kayama, M, Yokoi, Y, Mori, Y,  et al. 1997Organ distribution of iodide transporter (symporter) in the rat: immunohistochemical studyEndocr Regul31158PubMedGoogle Scholar
  10. 10.
    Spitzweg, C, Dutton, CM, Castro, MR, Bergert, ER, Goellner, JR, Heufelder, AE,  et al. 2001Expression of the sodium iodide symporter in human kidneyKidney Int59101323PubMedCrossRefGoogle Scholar
  11. 11.
    Vayre, L, Sabourin, JC, Caillou, B, Ducreux, M, Schlumberger, M, Bidart, JM 1999Immunohistochemical analysis of Na+/I symporter distribution in human extra-thyroidal tissuesEur J Endocrinol1413826PubMedCrossRefGoogle Scholar
  12. 12.
    Lacoix, L, Mian, M, Caillou, BT, Yalbot, M, Filetti, M, Schlunberger, ER,  et al. 2001Na+/I symporter and Pendred syndrome gene and protein expression in human extra-thyroidal tissuesEur J Endocrinol144279302Google Scholar
  13. 13.
    Soleimani, M, Greenley, T, Petrovic, S, Wang, Z, Amlal, H, Kopp, P,  et al. 2001Pendrin: an apical Cl/OH/HCO3 exchanger in the kidney cortexAm J Physiol Renal Physiol280F35664PubMedGoogle Scholar
  14. 14.
    Royaux, IE, Wall SMÅCKarniski, LP, Everett, LA, Suzuki, K, Knepper, MA,  et al. 2001Pendrin, encoded by the Pendred syndrome gene, resides in the apical region of renal intercalated cells and mediates bicarbonate secretionProc Natl Acad Sci USA9842216PubMedCrossRefGoogle Scholar
  15. 15.
    Kim Y-H, Kwon T-H, Frische, S, Kim, J, Tisher, CJ, Madsen, KM,  et al. 2002Immunocytochemical localization of pendrin in intercalated cell subtypes in rat and mouse kidneyAm J Physiol Renal Physiol283F74454PubMedGoogle Scholar
  16. 16.
    Frische, S, Kwon, T-H, Frakiaer, J, Madsen, KM, Nielsen, S 2003Regulated expression of pendrin in rat kidney in response to chronic NH4Cl or NaHCO3 loadingAm J Physiol Renal Physiol284F58493PubMedGoogle Scholar
  17. 17.
    Petrovic, S, Wang, Z, Ma, L, Soleiman, M 2003Regulation of the apical Cl/HCO3 exchanger pendrin in rat cortical collecting duct in metabolic acidosisAm J Physiol Renal Physiol284F10312PubMedGoogle Scholar
  18. 18.
    Wall, SM, Hassel, KA, Royaux, IE, Green, ED, Chang, JY, Shipley, GL,  et al. 2003Localization of pendrin in mouse kidneyAm J Physiol Renal Physiol284F22941PubMedGoogle Scholar
  19. 19.
    Quentin, S, Chambrey, R, Trinn-Tran-Tan, MM, Fysekidis, M, Cambillau, M, Paillard, M,  et al. 2004The Cl/HCO3 exchanger pendrin in the rat kidney is regulated in response to chronic alterations in chloride balanceAm J Physiol Renal Physiol287F117988PubMedCrossRefGoogle Scholar
  20. 20.
    Wall, SM, Kim, YH, Stanley, L, Glapion, DM, Everett, LA, Green, ED,  et al. 2004NaCl restriction upregulates renal Slc26a4 through subcellular redistribution: role in Cl conservationHypertension449827PubMedCrossRefGoogle Scholar
  21. 21.
    Yoshida, A, Hisatome, I, Taniguchi, S, Sasaki, N, Yamamoto, Y, Miake, J,  et al. 2004Mechanism of iodide/chloride exchange by pendrinEndocrinology14543018PubMedCrossRefGoogle Scholar
  22. 22.
    Muto, S, Yasoshima, K, Yoshitomi, K, Imai, M, Asano, Y 1990Electro-physiological identification of α- and β-intercalated cells and their distribution along the rabbit distal nephron segmentsJ Clin Invest86182939PubMedGoogle Scholar
  23. 23.
    Emmons, C, Kurzt, I 1994Functional characterization of three intercalated cell subtypes in the rabbit outer cortical collecting ductJ Clin Invest9341723PubMedCrossRefGoogle Scholar
  24. 24.
    Shuster, VL 1993Function and regulation of collecting duct intercalated cellsAnnu Rev Physiol5526788CrossRefGoogle Scholar
  25. 25.
    Muto, S, Matsushima, Y, Imai, M, Interaction, Asano Y. 1991between Cl and I in the rabbit β-intercalated cell (β-IC) in the rabbit CCD (abstract)J Am Soc Nephrol2707Google Scholar
  26. 26.
    Imai, M, Muto, S, Matsushima, Y 1995Axial and segmental heterogeneity of intercalated cellsDe Santo, NGCapasso, G eds. Symposium on acid-base and electrolyte balance. Molecular, cellular, and clinical aspectInstitut Italiano per gli Studi FilosoliciNaples10110Google Scholar
  27. 27.
    Burg, M, Grantham, Abramow M, Orloff, J 1966Preparation and study of fragments of single rabbit nephronsAm J Physiol21012938PubMedGoogle Scholar
  28. 28.
    Matsushima, Y, Yoshitomi, K, Koseki, C, Kawamura, M, Akabane, S, Imanishi, M,  et al. 1990Mechanisms of intracellular pH regulation in the hamster inner medullary collecting duct perfused in vitroPflugers Arch41671521PubMedCrossRefGoogle Scholar
  29. 29.
    Isozaki, T, Yoshitomi, K, Imai, M 1989Effects of Cl transport inhibitors on Cl permeability across the hamster ascending thin limbAm J Physiol257F928PubMedGoogle Scholar
  30. 30.
    Isozaki, T, Yoshitomi, K, Imai, M 1991Selectivity of ion permeability across ascending thin limb of Henle's loop: interaction of Cl and other halogens with anion transport systemKidney Int40S1139Google Scholar
  31. 31.
    Rink, TJ, Tsien, RY, Cytoplasmic, Pozann T. 1982pH and free Mg in lymphocytesJ Cell Biol9518996PubMedCrossRefGoogle Scholar
  32. 32.
    Wangemann, P, Witter, M, DiStefano, A, Englert, HC, Lang, HJ, Schlatter, E,  et al. 1986Cl channel blockers in the thick ascending limb of the loop of Henle. Structure activity relationshipPflugers Arch407S12841PubMedCrossRefGoogle Scholar
  33. 33.
    Vadstrup, S 1989Renal iodide clearance in rabbitsActa Endocrinol (Copenh)12124650Google Scholar
  34. 34.
    Vadstrup, S, Bojsen, J 1983The glomerular filtration rate in unrestrained rabbits determined by means of an implanted telemetrical deviceActa Physiol Scand11717782PubMedCrossRefGoogle Scholar
  35. 35.
    Tsuganezawa, H, Kobayashi, K, Iyori, M, Araki, T, Koizumi, A, Watanabe, S,  et al. 2001A new member of the HCO3 transporter superfamily is an apical anion exchanger of b-intercalated cells in the kidneyJ Biol Chem27681809PubMedCrossRefGoogle Scholar
  36. 36.
    Furuya, H, Breyer, MD, Jacobson, HR 1991Functional characterization of α- and β-intercalated cell types in rabbit cortical collecting ductAm J Physiol261F37785PubMedGoogle Scholar
  37. 37.
    Sackin, H, Palmer, LC 2000Electrophysiological analysis of transepithelial transportSeldin, DWGiebisch, G eds. The kidney: physiology and pathophysiology. Third edLippincott Williams & WilkinsPhiladelphia50132Google Scholar
  38. 38.
    Muto, S, Imai, M, Asano, Y 1992Interaction of Cl and other halogens with Cl transport systems in the rabbit cortical collecting ductAm J Physiol263F8707PubMedGoogle Scholar
  39. 39.
    Emmons, C 1996Halide transport patterns of apical anion exchange in rabbit cortical collecting duct intercalated cellsAm J Physiol271F799805PubMedGoogle Scholar

Copyright information

© Japanese Society of Nephrology 2006

Authors and Affiliations

  • Yohkazu Matsushima
    • 1
  • Shigeaki Muto
    • 2
  • Junichi Taniguchi
    • 3
  • Masashi Imai
    • 3
  1. 1.Department of Cardiovascular Dynamics, Research InstituteNational Cardiovascular CenterOsakaJapan
  2. 2.Department of Internal Medicine, Division of NephrologyJichi Medical UniversityTochigiJapan
  3. 3.Department of Pharmacology, Division of Molecular PharmacologyJichi Medical UniversityTochigiJapan

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