Corticomedullary difference in the effects of dietary Ca2+ on tight junction properties in thick ascending limbs of Henle’s loop

Pflugers Archiv European Journal of Physiology

Volumn 468, Issue 2, 2016, Pages 293-303

  Plain, Allein ^a   Wulfmeyer, Vera C ^a   Milatz, Susanne ^a   Klietz, Adrian ^a   Hou, Jianghui ^b   Bleich, Markus ^a   Himmerkus, Nina ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium; Claudin; Ion transport; Microperfusion; Nephron; Paracellular permeability

Indexed keywords

CLAUDIN; CLAUDIN 10; CLAUDIN 14; CLAUDIN 16; CLAUDIN 19; DIVALENT CATION; MAGNESIUM; SODIUM CHLORIDE; UNCLASSIFIED DRUG; CALCIUM; CALCIUM INTAKE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM BLOOD LEVEL; CALCIUM INTAKE; CALCIUM TRANSPORT; CATION TRANSPORT; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; FEMALE; HENLE LOOP; IMMUNOHISTOCHEMISTRY; KIDNEY CORTEX; KIDNEY MEDULLA; KIDNEY OUTER MEDULLA; KIDNEY PERFUSION; KIDNEY TUBULE ABSORPTION; MICRODISSECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ASSAY; REAL TIME POLYMERASE CHAIN REACTION; TIGHT JUNCTION; TRANSCYTOSIS; TRANSEPITHELIAL RESISTANCE; UPREGULATION; ACTION POTENTIAL; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GENETICS; METABOLISM; PHARMACOLOGY;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM, DIETARY; CLAUDINS; FEMALE; KIDNEY CORTEX; KIDNEY MEDULLA; LOOP OF HENLE; MAGNESIUM; MICE; MICE, INBRED C57BL; RENAL REABSORPTION; SODIUM CHLORIDE; TIGHT JUNCTIONS; UP-REGULATION;

EID: 84954362968     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-015-1748-7     Document Type: Article

References (42)

1. Bailly C, Imbert-Teboul M, Roinel N, Amiel C (1990) Isoproterenol increases Ca, Mg, and NaCl reabsorption in mouse thick ascending limb. Am J Physiol 258:F1224–1231
2. Barry PH, Lynch JW (1991) Liquid junction potentials and small cell effects in patch-clamp analysis. J Membr Biol 121:101–117
3. Ben-Yosef T, Belyantseva IA, Saunders TL, Hughes ED, Kawamoto K, Van Itallie CM, Beyer LA, Halsey K, Gardner DJ, Wilcox ER, Rasmussen J, Anderson JM, Dolan DF, Forge A, Raphael Y, Camper SA, Friedman TB (2003) Claudin 14 knockout mice, a model for autosomal recessive deafness DFNB29, are deaf due to cochlear hair cell degeneration. Hum Mol Genet 12:2049–2061
4. Bleich M, Shan Q, Himmerkus N (2012) Calcium regulation of tight junction permeability. Ann N Y Acad Sci 1258:93–99
5. Borschewski A, Himmerkus N, Boldt C, Blankenstein KI, McCormick JA, Lazelle R, Willnow TE, Jankowski V, Plain A, Bleich M, Ellison DH, Bachmann S, Mutig K (2015) Calcineurin and Sorting-Related Receptor with A-Type Repeats Interact to Regulate the Renal Na+−K+−2Cl- Cotransporter. J Am Soc Nephrol. doi:10.1681/ASN.2014070728
6. Breiderhoff T, Himmerkus N, Stuiver M, Mutig K, Will C, Meij IC, Bachmann S, Bleich M, Willnow TE, Müller D (2012) Deletion of claudin-10 (Cldn10) in the thick ascending limb impairs paracellular sodium permeability and leads to hypermagnesemia and nephrocalcinosis. Proc Natl Acad Sci U S A 109:14241–14246
7. de Rouffignac C, Quamme G (1994) Renal magnesium handling and its hormonal control. Physiol Rev 74:305–322
8. Di Stefano A, Roinel N, de Rouffignac C, Wittner M (1993) Transepithelial Ca2+ and Mg2+ transport in the cortical thick ascending limb of Henle's loop of the mouse is a voltage-dependent process. Ren Physiol Biochem 16:157–166
9. Di Stefano A, Wittner M, Nitschke R, Braitsch R, Greger R, Bailly C, Amiel C, Elalouf JM, Roinel N, de Rouffignac C (1989) Effects of glucagon on Na+, Cl-, K+, Mg2+ and Ca2+ transports in cortical and medullary thick ascending limbs of mouse kidney. Pflugers Arch 414:640–646
10. Di Stefano A, Wittner M, Nitschke R, Braitsch R, Greger R, Bailly C, Amiel C, Roinel N, de Rouffignac C (1990) Effects of parathyroid hormone and calcitonin on Na+, Cl-, K+, Mg2+ and Ca2+ transport in cortical and medullary thick ascending limbs of mouse kidney. Pflugers Arch 417:161–167
11. Dimke H, Desai P, Borovac J, Lau A, Pan W, Alexander RT (2013) Activation of the Ca(2+)-sensing receptor increases renal claudin-14 expression and urinary Ca(2+) excretion. Am J Physiol Renal Physiol 304:F761–769
12. Elkouby-Naor L, Abassi Z, Lagziel A, Gow A, Ben-Yosef T (2008) Double gene deletion reveals lack of cooperation between claudin 11 and claudin 14 tight junction proteins. Cell Tissue Res 333:427–438
13. Gamba G, Friedman PA (2009) Thick ascending limb: the Na(+):K (+):2Cl (−) co-transporter, NKCC2, and the calcium-sensing receptor, CaSR. Pflugers Arch 458:61–76
14. Gong Y, Himmerkus N, Plain A, Bleich M, Hou J (2015) Epigenetic regulation of microRNAs controlling CLDN14 expression as a mechanism for renal calcium handling. J Am Soc Nephrol 26:663–676
15. Gong Y, Hou J (2014) Claudin-14 underlies Ca(+)(+)-sensing receptor-mediated Ca(+)(+) metabolism via NFAT-microRNA-based mechanisms. J Am Soc Nephrol 25:745–760
16. Gong Y, Renigunta V, Himmerkus N, Zhang J, Renigunta A, Bleich M, Hou J (2012) Claudin-14 regulates renal Ca(+)(+) transport in response to CaSR signalling via a novel microRNA pathway. EMBO J 31:1999–2012
17. Greger R (1981) Cation selectivity of the isolated perfused cortical thick ascending limb of Henle's loop of rabbit kidney. Pflugers Arch 390:30–37
18. Günzel D, Stuiver M, Kausalya PJ, Haisch L, Krug SM, Rosenthal R, Meij IC, Hunziker W, Fromm M, Muller D (2009) Claudin-10 exists in six alternatively spliced isoforms that exhibit distinct localization and function. J Cell Sci 122:1507–1517
19. Günzel D, Yu AS (2013) Claudins and the modulation of tight junction permeability. Physiol Rev 93:525–569
20. Hannan FM, Thakker RV (2013) Calcium-sensing receptor (CaSR) mutations and disorders of calcium, electrolyte and water metabolism. Best Pract Res Clin Endocrinol Metab 27:359–371
21. Hebert SC, Andreoli TE (1986) Ionic conductance pathways in the mouse medullary thick ascending limb of Henle. The paracellular pathway and electrogenic Cl- absorption. J Gen Physiol 87:567–590
22. Himmerkus N, Shan Q, Goerke B, Hou J, Goodenough DA, Bleich M (2008) Salt and acid–base metabolism in claudin-16 knockdown mice: impact for the pathophysiology of FHHNC patients. Am J Physiol Renal Physiol 295:F1641–1647
23. Hoek AC, Lemmens AG, Mullink JW, Beynen AC (1988) Influence of dietary calcium:phosphorus ratio on mineral excretion and nephrocalcinosis in female rats. J Nutr 118:1210–1216
24. Hou J, Renigunta A, Gomes AS, Hou M, Paul DL, Waldegger S, Goodenough DA (2009) Claudin-16 and claudin-19 interaction is required for their assembly into tight junctions and for renal reabsorption of magnesium. Proc Natl Acad Sci U S A 106:15350–15355
25. Hou J, Shan Q, Wang T, Gomes AS, Yan Q, Paul DL, Bleich M, Goodenough DA (2007) Transgenic RNAi depletion of claudin-16 and the renal handling of magnesium. J Biol Chem 282:17114–17122
26. Kimizuka H, Koketsu K (1964) Ion transport through cell membrane. J Theor Biol 6:290–305
27. Kirk A, Campbell S, Bass P, Mason J, Collins J (2010) Differential expression of claudin tight junction proteins in the human cortical nephron. Nephrol Dial Transplant 25:2107–2119
28. Kiuchi-Saishin Y, Gotoh S, Furuse M, Takasuga A, Tano Y, Tsukita S (2002) Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J Am Soc Nephrol 13:875–886
29. Konrad M, Schaller A, Seelow D, Pandey AV, Waldegger S, Lesslauer A, Vitzthum H, Suzuki Y, Luk JM, Becker C, Schlingmann KP, Schmid M, Rodriguez-Soriano J, Ariceta G, Cano F, Enriquez R, Juppner H, Bakkaloglu SA, Hediger MA, Gallati S, Neuhauss SC, Nurnberg P, Weber S (2006) Mutations in the tight-junction gene claudin 19 (CLDN19) are associated with renal magnesium wasting, renal failure, and severe ocular involvement. Am J Hum Genet 79:949–957
30. Loupy A, Ramakrishnan SK, Wootla B, Chambrey R, de la Faille R, Bourgeois S, Bruneval P, Mandet C, Christensen EI, Faure H, Cheval L, Laghmani K, Collet C, Eladari D, Dodd RH, Ruat M, Houillier P (2012) PTH-independent regulation of blood calcium concentration by the calcium-sensing receptor. J Clin Invest 122:3355–3367
31. Matsubara M (2004) Renal sodium handling for body fluid maintenance and blood pressure regulation. Yakugaku Zasshi 124:301–309
32. Ng B, Barry PH (1995) The measurement of ionic conductivities and mobilities of certain less common organic ions needed for junction potential corrections in electrophysiology. J Neurosci Methods 56:37–41
33. Ohta H, Adachi H, Takiguchi M, Inaba M (2006) Restricted localization of claudin-16 at the tight junction in the thick ascending limb of Henle's loop together with claudins 3, 4, and 10 in bovine nephrons. J Vet Med Sci 68:453–463
34. Peterson CA, Baker DH, Erdman JW Jr (1996) Diet-induced nephrocalcinosis in female rats is irreversible and is induced primarily before the completion of adolescence. J Nutr 126:259–265
35. Schaafsma G, Duursma SA, Visser WJ, Dekker PR (1985) The influence of dietary calcium on kidney calcification and renal function in rats fed high-phosphate diets. Bone 6:155–163
36. Shan Q, Himmerkus N, Hou J, Goodenough DA, Bleich M (2009) Insights into driving forces and paracellular permeability from claudin-16 knockdown mouse. Ann N Y Acad Sci 1165:148–151
37. Simon DB, Lu Y, Choate KA, Velazquez H, Al-Sabban E, Praga M, Casari G, Bettinelli A, Colussi G, Rodriguez-Soriano J, McCredie D, Milford D, Sanjad S, Lifton RP (1999) Paracellin-1, a renal tight junction protein required for paracellular Mg2+ resorption. Science 285:103–106
38. Thorleifsson G, Holm H, Edvardsson V, Walters GB, Styrkarsdottir U, Gudbjartsson DF, Sulem P, Halldorsson BV, de Vegt F, d'Ancona FC, den Heijer M, Franzson L, Christiansen C, Alexandersen P, Rafnar T, Kristjansson K, Sigurdsson G, Kiemeney LA, Bodvarsson M, Indridason OS, Palsson R, Kong A, Thorsteinsdottir U, Stefansson K (2009) Sequence variants in the CLDN14 gene associate with kidney stones and bone mineral density. Nat Genet 41:926–930
39. Toka HR, Pollak MR, Houillier P (2015) Calcium Sensing in the Renal Tubule. Physiology (Bethesda) 30:317–326
40. Van Itallie CM, Rogan S, Yu A, Vidal LS, Holmes J, Anderson JM (2006) Two splice variants of claudin-10 in the kidney create paracellular pores with different ion selectivities. Am J Physiol Renal Physiol 291:F1288–1299
41. Will C, Breiderhoff T, Thumfart J, Stuiver M, Kopplin K, Sommer K, Günzel D, Querfeld U, Meij IC, Shan Q, Bleich M, Willnow TE, Müller D (2010) Targeted deletion of murine Cldn16 identifies extra- and intrarenal compensatory mechanisms of Ca2+ and Mg2+ wasting. Am J Physiol Renal Physiol 298:F1152–1161
42. Wittner M, di Stefano A, Wangemann P, Nitschke R, Greger R, Bailly C, Amiel C, Roinel N, de Rouffignac C (1988) Differential effects of ADH on sodium, chloride, potassium, calcium and magnesium transport in cortical and medullary thick ascending limbs of mouse nephron. Pflugers Arch 412:516–523