FGF23 promotes renal calcium reabsorption through the TRPV5 channel

EMBO Journal

Volumn 33, Issue 3, 2014, Pages 229-246

  Andrukhova, Olena ^a   Smorodchenko, Alina ^a   Egerbacher, Monika ^a   Streicher, Carmen ^a   Zeitz, Ute ^a   Goetz, Regina ^b   Shalhoub, Victoria ^c   Mohammadi, Moosa ^b   Pohl, Elena E ^a   Lanske, Beate ^d   Erben, Reinhold G ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AMGEN INC   (United States)

^d HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

Calcium homeostasis; Fibroblast growth factor 23; Klotho; Renal calcium reabsorption; Transient receptor potential vanilloid 5

Indexed keywords

ALPHA KLOTHO PROTEIN; CALBINDIN; CALBINDIN 1; CALCIUM; CYTOPLASM PROTEIN; FIBROBLAST GROWTH FACTOR 23; FIBROBLAST GROWTH FACTOR RECEPTOR; KLOTHO PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROTEIN KINASE P60; PROTEIN KINASE WNK4; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 5; VITAMIN D;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; CALCIUM ABSORPTION; CALCIUM BLOOD LEVEL; CALCIUM CELL LEVEL; CALCIUM EXCRETION; CALCIUM TRANSPORT; CALCIUM URINE LEVEL; CELL MIGRATION; CELLULAR DISTRIBUTION; GENOTYPE; GLYCOSYLATION; GOLGI COMPLEX; IMMUNOBLOTTING; IN VITRO STUDY; KIDNEY DISTAL TUBULE; KIDNEY FUNCTION; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE ABSORPTION; LIMIT OF DETECTION; MALE; MOUSE; NONHUMAN; PARATHYROID HORMONE BLOOD LEVEL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; CALCIUM; CELL MEMBRANE; FIBROBLAST GROWTH FACTORS; IMMEDIATE-EARLY PROTEINS; KIDNEY; MALE; MICE; MICE, KNOCKOUT; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TRPV CATION CHANNELS;

EID: 84897838979     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1002/embj.20128418     Document Type: Article

References (55)

1. Alexander RT, Woudenberg-Vrenken TE, Buurman J, Dijkman H, van der Eerden BC, van Leeuwen JP, Bindels RJ, Hoenderop JG (2009) Klotho prevents renal calcium loss. J Am Soc Nephrol 20: 2371 - 2379
2. Andrukhova O, Zeitz U, Goetz R, Mohammadi M, Lanske B, Erben RG (2012) FGF23 acts directly on renal proximal tubules to induce phosphaturia through activation of the ERK1/2-SGK1 signaling pathway. Bone 51: 621 - 628
3. Anour R, Andrukhova O, Ritter E, Zeitz U, Erben RG (2012) Klotho lacks a vitamin D independent physiological role in glucose homeostasis, bone turnover, and steady-state PTH secretion in vivo. PLoS ONE 7: e31376
4. Burg MB, Grantham J, Abramow M, Orloff J, Schafer JA (1997) Preparation and study of fragments of single rabbit nephrons. J Am Soc Nephrol 8: 675 - 683
5. Cai H, Cebotaru V, Wang YH, Zhang XM, Cebotaru L, Guggino SE, Guggino WB (2006) WNK4 kinase regulates surface expression of the human sodium chloride cotransporter in mammalian cells. Kidney Int 69: 2162 - 2170
6. Cha SK, Huang CL (2010) WNK4 kinase stimulates caveola-mediated endocytosis of TRPV5 amplifying the dynamic range of regulation of the channel by protein kinase C. J Biol Chem 285: 6604 - 6611
7. Cha SK, Ortega B, Kurosu H, Rosenblatt KP, Kuro O, Huang CL (2008) Removal of sialic acid involving Klotho causes cell-surface retention of TRPV5 channel via binding to galectin-1. Proc Natl Acad Sci USA 105: 9805 - 9810
8. Chang Q, Hoefs S, Van Der Kemp AW, Topala CN, Bindels RJ, Hoenderop JG (2005) The beta-glucuronidase klotho hydrolyzes and activates the TRPV5 channel. Science 310: 490 - 493
9. Erben RG, Soegiarto DW, Weber K, Zeitz U, Lieberherr M, Gniadecki R, Möller G, Adamski J, Balling R (2002) Deletion of deoxyribonucleic acid binding domain of the vitamin D receptor abrogates genomic and nongenomic functions of vitamin D. Mol Endocrinol 16: 1524 - 1537
10. Farrow EG, Davis SI, Summers LJ, White KE (2009) Initial FGF23-mediated signaling occurs in the distal convoluted tubule. J Am Soc Nephrol 20: 955 - 960
11. Farrow EG, Summers LJ, Schiavi SC, McCormick JA, Ellison DH, White KE (2010) Altered renal FGF23-mediated activity involving MAPK and Wnt: effects of the Hyp mutation. J Endocrinol 207: 67 - 75
12. Fischer SS, Kempe DS, Leibrock CB, Rexhepaj R, Siraskar B, Boini KM, Ackermann TF, Foller M, Hocher B, Rosenblatt KP, Kuro O, Lang F (2010) Hyperaldosteronism in Klotho-deficient mice. Am J Physiol Renal Physiol 299: F1171 - F1177
13. Goetz R, Beenken A, Ibrahimi OA, Kalinina J, Olsen SK, Eliseenkova AV, Xu C, Neubert TA, Zhang F, Linhardt RJ, Yu X, White KE, Inagaki T, Kliewer SA, Yamamoto M, Kurosu H, Ogawa Y, Kuro-o M, Lanske B, Razzaque MS et al (2007) Molecular insights into the klotho-dependent, endocrine mode of action of fibroblast growth factor 19 subfamily members. Mol Cell Biol 27: 3417 - 3428
14. Gonzalez-Mariscal L, Namorado MC, Martin D, Luna J, Alarcon L, Islas S, Valencia L, Muriel P, Ponce L, Reyes JL (2000) Tight junction proteins ZO-1, ZO-2, and occludin along isolated renal tubules. Kidney Int 57: 2386 - 2402
15. de Groot T, Lee K, Langeslag M, Xi Q, Jalink K, Bindels RJ, Hoenderop JG (2009) Parathyroid hormone activates TRPV5 via PKA-dependent phosphorylation. J Am Soc Nephrol 20: 1693 - 1704
16. He G, Wang HR, Huang SK, Huang CL (2007) Intersectin links WNK kinases to endocytosis of ROMK1. J Clin Invest 117: 1078 - 1087
17. Hellwig N, Albrecht N, Harteneck C, Schultz G, Schaefer M (2005) Homo- and heteromeric assembly of TRPV channel subunits. J Cell Sci 118: 917 - 928
18. Hesse M, Frohlich LF, Zeitz U, Lanske B, Erben RG (2007) Ablation of vitamin D signaling rescues bone, mineral, and glucose homeostasis in Fgf-23 deficient mice. Matrix Biol 26: 75 - 84
19. Hoenderop JG, Vennekens R, Muller D, Prenen J, Droogmans G, Bindels RJ, Nilius B (2001) Function and expression of the epithelial Ca(2+) channel family: comparison of mammalian ECaC1 and 2. J Physiol 537: 747 - 761
20. Hu MC, Shi M, Zhang J, Pastor J, Nakatani T, Lanske B, Razzaque MS, Rosenblatt KP, Baum MG, Kuro-o M, Moe OW (2010) Klotho: a novel phosphaturic substance acting as an autocrine enzyme in the renal proximal tubule. FASEB J 24: 3438 - 3450
21. Imura A, Tsuji Y, Murata M, Maeda R, Kubota K, Iwano A, Obuse C, Togashi K, Tominaga M, Kita N, Tomiyama K, Iijima J, Nabeshima Y, Fujioka M, Asato R, Tanaka S, Kojima K, Ito J, Nozaki K, Hashimoto N et al (2007) alpha-Klotho as a regulator of calcium homeostasis. Science 316: 1615 - 1618
22. Jiang Y, Cong P, Williams SR, Zhang W, Na T, Ma HP, Peng JB (2008) WNK4 regulates the secretory pathway via which TRPV5 is targeted to the plasma membrane. Biochem Biophys Res Commun 375: 225 - 229
23. Jiang Y, Ferguson WB, Peng JB (2007) WNK4 enhances TRPV5-mediated calcium transport: potential role in hypercalciuria of familial hyperkalemic hypertension caused by gene mutation of WNK4. Am J Physiol Renal Physiol 292: F545 - F554
24. Juppner H, Wolf M, Salusky IB (2010) FGF-23: more than a regulator of renal phosphate handling? J Bone Miner Res 25: 2091 - 2097
25. Kessler W, Budde T, Gekle M, Fabian A, Schwab A (2008) Activation of cell migration with fibroblast growth factor-2 requires calcium-sensitive potassium channels. Pflugers Arch 456: 813 - 823
26. Kuro-o M, Matsumura Y, Aizawa H, Kawaguchi H, Suga T, Utsugi T, Ohyama Y, Kurabayashi M, Kaname T, Kume E, Iwasaki H, Iida A, Shiraki-Iida T, Nishikawa S, Nagai R, Nabeshima YI (1997) Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390: 45 - 51
27. Kurosu H, Ogawa Y, Miyoshi M, Yamamoto M, Nandi A, Rosenblatt KP, Baum MG, Schiavi S, Hu MC, Moe OW, Kuro O (2006) Regulation of fibroblast growth factor-23 signaling by Klotho. J Biol Chem 281: 6120 - 6123
28. Kurosu H, Yamamoto M, Clark JD, Pastor JV, Nandi A, Gurnani P, McGuinness OP, Chikuda H, Yamaguchi M, Kawaguchi H, Shimomura I, Takayama Y, Herz J, Kahn CR, Rosenblatt KP, Kuro-o M (2005) Suppression of aging in mice by the hormone Klotho. Science 309: 1829 - 1833
29. Lambers TT, Bindels RJ, Hoenderop JG (2006) Coordinated control of renal Ca2 + handling. Kidney Int 69: 650 - 654
30. Li H, Martin A, David V, Quarles LD (2011) Compound deletion of Fgfr3 and Fgfr4 partially rescues the Hyp mouse phenotype. Am J Physiol Endocrinol Metab 300: E508 - E517
31. Li YC, Amling M, Pirro AE, Priemel M, Meuse J, Baron R, Delling G, Demay MB (1998) Normalization of mineral ion homeostasis by dietary means prevents hyperparathyroidism, rickets, and osteomalacia, but not alopecia in vitamin D receptor-ablated mice. Endocrinology 139: 4391 - 4396
32. Martin A, David V, Quarles LD (2012) Regulation and function of the FGF23/klotho endocrine pathways. Physiol Rev 92: 131 - 155
33. Matsumura Y, Aizawa H, Shiraki-Iida T, Nagai R, Kuro-o M, Nabeshima Y (1998) Identification of the human klotho gene and its two transcripts encoding membrane and secreted klotho protein. Biochem Biophys Res Commun 242: 626 - 630
34. Mayan H, Vered I, Mouallem M, Tzadok-Witkon M, Pauzner R, Farfel Z (2002) Pseudohypoaldosteronism type II: marked sensitivity to thiazides, hypercalciuria, normomagnesemia, and low bone mineral density. J Clin Endocrinol Metab 87: 3248 - 3254
35. McCormick JA, Yang CL, Ellison DH (2008) WNK kinases and renal sodium transport in health and disease: an integrated view. Hypertension 51: 588 - 596
36. Michlig S, Mercier A, Doucet A, Schild L, Horisberger JD, Rossier BC, Firsov D (2004) ERK1/2 controls Na, K-ATPase activity and transepithelial sodium transport in the principal cell of the cortical collecting duct of the mouse kidney. J Biol Chem 279: 51002 - 51012
37. Nakatani T, Sarraj B, Ohnishi M, Densmore MJ, Taguchi T, Goetz R, Mohammadi M, Lanske B, Razzaque MS (2009) In vivo genetic evidence for klotho-dependent, fibroblast growth factor 23 (Fgf23) -mediated regulation of systemic phosphate homeostasis. FASEB J 23: 433 - 441
38. Okano T, Tsugawa N, Morishita A, Kato S (2004) Regulation of gene expression of epithelial calcium channels in intestine and kidney of mice by 1alpha,25-dihydroxyvitamin D3. J Steroid Biochem Mol Biol 89-90: 335 - 338
39. Ring AM, Leng Q, Rinehart J, Wilson FH, Kahle KT, Hebert SC, Lifton RP (2007) An SGK1 site in WNK4 regulates Na+ channel and K+ channel activity and has implications for aldosterone signaling and K+ homeostasis. Proc Natl Acad Sci USA 104: 4025 - 4029
40. Sandulache D, Grahammer F, Artunc F, Henke G, Hussain A, Nasir O, Mack A, Friedrich B, Vallon V, Wulff P, Kuhl D, Palmada M, Lang F (2006) Renal Ca2 + handling in sgk1 knockout mice. Pflugers Arch 452: 444 - 452
41. Schafer JA, Watkins ML, Li L, Herter P, Haxelmans S, Schlatter E (1997) A simplified method for isolation of large numbers of defined nephron segments. Am J Physiol 273: F650 - F657
42. Segawa H, Yamanaka S, Ohno Y, Onitsuka A, Shiozawa K, Aranami F, Furutani J, Tomoe Y, Ito M, Kuwahata M, Imura A, Nabeshima Y, Miyamoto K (2007) Correlation between hyperphosphatemia and type II Na-Pi cotransporter activity in klotho mice. Am J Physiol Renal Physiol 292: F769 - F779
43. Shimada T, Hasegawa H, Yamazaki Y, Muto T, Hino R, Takeuchi Y, Fujita T, Nakahara K, Fukumoto S, Yamashita T (2004) FGF-23 is a potent regulator of vitamin D metabolism and phosphate homeostasis. J Bone Miner Res 19: 429 - 435
44. Shimada T, Mizutani S, Muto T, Yoneya T, Hino R, Takeda S, Takeuchi Y, Fujita T, Fukumoto S, Yamashita T (2001) Cloning and characterization of FGF23 as a causative factor of tumor-induced osteomalacia. Proc Natl Acad Sci USA 98: 6500 - 6505
45. Shiraki-Iida T, Aizawa H, Matsumura Y, Sekine S, Iida A, Anazawa H, Nagai R, Kuro-o M, Nabeshima Y (1998) Structure of the mouse klotho gene and its two transcripts encoding membrane and secreted protein. FEBS Lett 424: 6 - 10
46. Sitara D, Razzaque MS, Hesse M, Yoganathan S, Taguchi T, Erben RG, Juppner H, Lanske B (2004) Homozygous ablation of fibroblast growth factor-23 results in hyperphosphatemia and impaired skeletogenesis, and reverses hypophosphatemia in Phex-deficient mice. Matrix Biol 23: 421 - 432
47. Streicher C, Zeitz U, Andrukhova O, Rupprecht A, Pohl E, Larsson TE, Windisch W, Lanske B, Erben RG (2012) Long-term Fgf23 deficiency does not influence aging, glucose homeostasis, or fat metabolism in mice with a nonfunctioning vitamin D receptor. Endocrinology 153: 1795 - 1805
48. Tohyama O, Imura A, Iwano A, Freund JN, Henrissat B, Fujimori T, Nabeshima Y (2004) Klotho is a novel beta-glucuronidase capable of hydrolyzing steroid beta-glucuronides. J Biol Chem 279: 9777 - 9784
49. Tsujikawa H, Kurotaki Y, Fujimori T, Fukuda K, Nabeshima Y (2003) Klotho, a gene related to a syndrome resembling human premature aging, functions in a negative regulatory circuit of vitamin D endocrine system. Mol Endocrinol 17: 2393 - 2403
50. Urakawa I, Yamazaki Y, Shimada T, Iijima K, Hasegawa H, Okawa K, Fujita T, Fukumoto S, Yamashita T (2006) Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 444: 770 - 774
51. Weber K, Erben RG, Rump A, Adamski J (2001) Gene structure and regulation of the murine epithelial calcium channels ECaC1 and 2. Biochem Biophys Res Commun 289: 1287 - 1294
52. Weinman EJ, Steplock D, Shenolikar S, Biswas R (2011) FGF-23-mediated inhibition of renal phosphate transport in mice requires NHERF-1 and synergizes with PTH. J Biol Chem 286: 37216 - 37221
53. White KE, Econs MJ (2008) Fibroblast Growth Factor-23. In Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism, Rosen CJ (ed), pp 112 - 116. Washington, DC: Society of Bone and Mineral Research
54. Woudenberg-Vrenken TE, Bindels RJ, Hoenderop JG (2009) The role of transient receptor potential channels in kidney disease. Nat Rev Nephrol 5: 441 - 449
55. Zeitz U, Weber K, Soegiarto DW, Wolf E, Balling R, Erben RG (2003) Impaired insulin secretory capacity in mice lacking a functional vitamin D receptor. FASEB J 17: 509 - 511