Claudin-14 regulates renal Ca ++ transport in response to CaSR signalling via a novel microRNA pathway

EMBO Journal

Volumn 31, Issue 8, 2012, Pages 1999-2012

  Gong, Yongfeng ^a,b   Renigunta, Vijayaram ^c   Himmerkus, Nina ^d   Zhang, Jiaqi ^a   Renigunta, Aparna ^c   Bleich, Markus ^d   Hou, Jianghui ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BINZHOU MEDICAL UNIVERSITY   (China)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d UNIVERSITY OF KIEL   (Germany)

Author keywords

bone mineral loss; hypercalciuria; kidney stone; tight junction

Indexed keywords

CALCIUM; CALCIUM SENSING RECEPTOR; CLAUDIN; CLAUDIN 14; CLAUDIN 16; CLAUDIN 19; MEMBRANE PROTEIN; MICRORNA; MICRORNA 374; MICRORNA 9; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM HOMEOSTASIS; CONTROLLED STUDY; DIET; DISEASE COURSE; DOWN REGULATION; FEMALE; HENLE LOOP; HYPERMAGNESEMIA; HYPOCALCIURIA; HYPOMAGNESEMIA; KIDNEY; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; CALCIUM; CLAUDINS; KIDNEY; MICE; MICE, KNOCKOUT; MICRORNAS; RECEPTORS, CALCIUM-SENSING;

ANIMALIA;

EID: 84862804787     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.49     Document Type: Article

References (46)

1. 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 (Pubitemid 37038814)
2. Bourgeois S, Rossignol P, Grelac F, Chalumeau C, Klein C, Laghmani K, Chambrey R, Bruneval P, Duong JP, Poggioli J, Houillier P, Paillard M, Kellermann O, Froissart M (2003) Differentiated thick ascending limb (TAL) cultured cells derived from SV40 transgenic mice express functional apical NHE2 isoform: effect of nitric oxide. Pflugers Arch 446: 672-683 (Pubitemid 37215003)
3. Buchert M, Papin M, Bonnans C, Darido C, Raye WS, Garambois V, Peaposlegrin A, Bourgaux JF, Pannequin J, Joubert D, Hollande F (2010) Symplekin promotes tumorigenicity by up-regulating claudin-2 expression. Proc Natl Acad Sci USA 107: 2628-2633
4. Desfleurs E, Wittner M, Simeone S, Pajaud S, Moine G, Rajerison R, Di Stefano A (1998) CaSR: regulation of electrolyte transport in the thick ascending limb of Henle's loop. Kidney Blood Press Res 21: 401-412 (Pubitemid 29078035)
5. 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
6. Furuse M, Sasaki H, Tsukita S (1999) Manner of interaction of heterogeneous claudin species within and between tight junction strands. J Cell Biol 147: 891-903
7. 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
8. Greger R (1985) Ion transport mechanisms in thick ascending limb of Henle's loop of mammalian nephron. Physiol Rev 65: 760-797
9. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10: 593-601 (Pubitemid 351627379)
10. Harvey SJ, Jarad G, Cunningham J, Goldberg S, Schermer B, Harfe BD, McManus MT, Benzing T, Miner JH (2008) Podocytespecific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J Am Soc Nephrol 19: 2150-2158
11. 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 (Pubitemid 16117195)
12. Hebert SC, Riccardi D, Geibel J (2007) The calcium-sensing receptor. In The Kidney: Physiology and Pathophysiology, Alpern RJ, Hebert SC (eds), 4th edn, pp 1785-1882. Amsterdam: Elsevier
13. 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-F1647
14. Hou J, Paul DL, Goodenough DA (2005) Paracellin-1 and the modulation of ion selectivity of tight junctions. J Cell Sci 118: 5109-5118 (Pubitemid 41672441)
15. 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 USA 106: 15350-15355
16. Hou J, Renigunta A, Konrad M, Gomes AS, Schneeberger EE, Paul DL, Waldegger S, Goodenough DA (2008) Claudin-16 and claudin-19 interact and form a cation-selective tight junction complex. J Clin Invest 118: 619-628 (Pubitemid 351206551)
17. 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 (Pubitemid 47093227)
18. Hu H, Du L, Nagabayashi G, Seeger RC, Gatti RA (2010) ATM is down-regulated by N-Myc-regulated microRNA-421. Proc Natl Acad Sci USA 107: 1506-1511
19. Huntzinger E, Izaurralde E (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12: 99-110
20. 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 (Pubitemid 34274083)
21. 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 et al (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 (Pubitemid 44763409)
22. Krol J, Loedige I, Filipowicz W (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11: 597-610
23. Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, Stoffel M (2005) Silencing of microRNAs in vivo with 'antagomirs'. Nature 438: 685-689
24. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, Teruya- Feldstein J, Reinhardt F, Onder TT, Valastyan S, Westermann F, Speleman F, Vandesompele J, Weinberg RA (2010) miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 12: 247-256
25. Mineta K, Yamamoto Y, Yamazaki Y, Tanaka H, Tada Y, Saito K, Tamura A, Igarashi M, Endo T, Takeuchi K, Tsukita S (2011) Predicted expansion of the claudin multigene family. FEBS Lett 585: 606-612
26. Motoyama HI, Friedman PA (2002) CaSR regulation of PTH dependent calcium absorption by mouse cortical ascending limbs. Am J Physiol Renal Physiol 283: F399-F406
27. Nübel T, Preobraschenski J, Tuncay H, Weiss T, Kuhn S, Ladwein M, Langbein L, Zöller M (2009) Claudin-7 regulates EpCAM-mediated functions in tumor progression. Mol Cancer Res 7: 285-299
28. Pietrzykowski AZ, Friesen RM, Martin GE, Puig SI, Nowak CL, Wynne PM, Siegelmann HT, Treistman SN (2008) Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron 59: 274-287 (Pubitemid 352033687)
29. Riccardi D, Brown EM (2010) Physiology and pathophysiology of the calcium-sensing receptor in the kidney. Am J Physiol Renal Physiol 298: F485-F499
30. 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 (Pubitemid 29307575)
31. Stevenson BR, Goodenough DA (1984) Zonulae occludentes in junctional complex enriched fractions from mouse liver: preliminary morphological and biochemical characterization. J Cell Biol 98: 1209-1221 (Pubitemid 14128904)
32. 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 et al (2009) Sequence variants in the CLDN14 gene associate with kidney stones and bone mineral density. Nat Genet 41: 926-930
33. Tsukita S, Furuse M, Itoh M (2001) Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2: 285-293 (Pubitemid 33676971)
34. Van Itallie CM, Gambling TM, Carson JL, Anderson JM (2005) Palmitoylation of claudins is required for efficient tight-junction localization. J Cell Sci 118: 1427-1436 (Pubitemid 40585123)
35. Vargas-Poussou R, Huang C, Hulin P, Houillier P, Jeunemaître X, Paillard M, Planelles G, Déchaux M, Miller RT, Antignac C (2002) Functional characterization of a calcium-sensing receptor mutation in severe autosomal dominant hypocalcemia with a Bartter-like syndrome. J Am Soc Nephrol 13: 2259-2266 (Pubitemid 34925236)
36. Wang K, Long B, Zhou J, Li PF (2010) miR-9 and NFATc3 regulate myocardin in cardiac hypertrophy. J Biol Chem 285: 11903-11912
37. + channels in rat TAL. Am J Physiol Renal Physiol 273: F421-F429
38. + channels in the TAL. Am J Physiol Cell Physiol 271: C103-C111
39. Weber S, Schneider L, Peters M, Misselwitz J, Rönnefarth G, Böswald M, Bonzel KE, Seeman T, Sulaaposkova T, Kuwertz- Bröking E, Gregoric A, Palcoux JB, Tasic V, Manz F, Schärer K, Seyberth HW, Konrad M (2001) Novel paracellin-1 mutations in 25 families with familial hypomagnesemia with hypercalciuria and nephrocalcinosis. J Am Soc Nephrol 12: 1872-1881 (Pubitemid 32801362)
40. Wei Q, Bhatt K, He HZ, Mi QS, Haase VH, Dong Z (2010) Targeted deletion of Dicer from proximal tubules protects against renal ischemia-reperfusion injury. J Am Soc Nephrol 21: 756-761
41. Wilcox ER, Burton QL, Naz S, Riazuddin S, Smith TN, Ploplis B, Belyantseva I, Ben-Yosef T, Liburd NA, Morell RJ, Kachar B, Wu DK, Griffith AJ, Riazuddin S, Friedman TB (2001) Mutations in the gene encoding tight junction claudin-14 cause autosomal recessive deafness DFNB29. Cell 104: 165-172 (Pubitemid 32144981)
42. Wong V (1997) Phosphorylation of occludin correlates with occludin localization and function at the tight junction. Am J Physiol 273: C1859-C1867
43. Yan H, Yuan W, Velculescu VE, Vogelstein B, Kinzler KW (2002) Allelic variation in human gene expression. Science 297: 1143 (Pubitemid 36193340)
44. Yoo AS, Staahl BT, Chen L, Crabtree GR (2009) MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 460: 642-646
45. Yu AS, Cheng MH, Angelow S, Günzel D, Kanzawa SA, Schneeberger EE, Fromm M, Coalson RD (2009) Molecular basis for cation selectivity in claudin-2-based paracellular pores: identification of an electrostatic interaction site. J Gen Physiol 133: 111-127
46. Zheng B, Cantley LC (2007) Regulation of epithelial tight junction assembly and disassembly by AMP-activated protein kinase. Proc Natl Acad Sci USA 104: 819-822 (Pubitemid 46154694)