Shedding of klotho by ADAMs in the kidney

American Journal of Physiology - Renal Physiology

Volumn 309, Issue 4, 2015, Pages F359-F368

  Van Loon, Ellen P M ^a   Pulskens, Wilco P ^a   Van Der Hagen, Eline A E ^a   Lavrijsen, Marla ^a   Vervloet, Marc G ^b   Van Goor, Harry ^c   Bindels, René J M ^a   Hoenderop, Joost G J ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

A disintegrin and metalloproteinase 10; A disintegrin and metalloproteinase 17; A disintegrin and metalloproteinase matrix metalloproteinase inhibitor; Klotho; Klotho shedding

Indexed keywords

ADAM PROTEIN; ADAM10 ENDOPEPTIDASE; CALCIUM; FIBROBLAST GROWTH FACTOR 23; KLOTHO PROTEIN; MATRIX METALLOPROTEINASE; MESSENGER RNA; PHOSPHATE TRANSPORTER; PROTEIN ADAM17; TAMM HORSFALL GLYCOPROTEIN; UNCLASSIFIED DRUG; ADAM10 PROTEIN, MOUSE; BETA GLUCURONIDASE; CULTURE MEDIUM; MEMBRANE PROTEIN; PHOSPHATE; PROTEINASE INHIBITOR; SECRETASE; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME INHIBITION; GENE EXPRESSION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CELL; MALE; MDCK CELL LINE; MOUSE; NONHUMAN; PHOSPHATE BLOOD LEVEL; PHOSPHATE URINE LEVEL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN URINE LEVEL; UPREGULATION; URINARY EXCRETION; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; C57BL MOUSE; CELL MEMBRANE; CULTURE MEDIUM; DOG; DOSE RESPONSE; DRUG EFFECTS; DUODENUM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; KIDNEY; METABOLISM; PROTEIN PROCESSING;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CELL MEMBRANE; CULTURE MEDIA, CONDITIONED; DOGS; DOSE-RESPONSE RELATIONSHIP, DRUG; DUODENUM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCURONIDASE; HEK293 CELLS; HUMANS; KIDNEY; MADIN DARBY CANINE KIDNEY CELLS; MALE; MEMBRANE PROTEINS; MICE, INBRED C57BL; PHOSPHATE TRANSPORT PROTEINS; PHOSPHATES; PROTEASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; TRANSFECTION;

EID: 84939561232     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00240.2014     Document Type: Article

References (51)

1. Alexander RT, Woudenberg-Vrenken TE, Buurman J, Dijkman H, van der Eerden BC, van Leeuwen JP, Bindels RJ, Hoenderop JG. Klotho prevents renal calcium loss. J Am Soc Nephrol 20: 2371-2379, 2009.
2. Bai X, Miao D, Li J, Goltzman D, Karaplis AC. Transgenic mice overexpressing human fibroblast growth factor 23 (R176Q) delineate a putative role for parathyroid hormone in renal phosphate wasting disorders. Endocrinology 145: 5269-5279, 2004.
3. Bzowska M, Jura N, Lassak A, Black RA, Bereta J. Tumour necrosis factor-β stimulates expression of TNF-β converting enzyme in endothelial cells. Eur J Biochem 271: 2808-2820, 2004.
4. Cha SK, Hu MC, Kurosu H, Kuro-o M, Moe O, Huang CL. Regulation of renal outer medullary potassium channel and renal K+ excretion by Klotho. Mol Pharmacol 76: 38-46, 2009.
5. Chang Q, Hoefs S, van der Kemp AW, Topala CN, Bindels RJ, Hoenderop JG. The β-glucuronidase klotho hydrolyzes and activates the TRPV5 channel. Science 310: 490-493, 2005.
6. Chen CD, Podvin S, Gillespie E, Leeman SE, Abraham CR. Insulin stimulates the cleavage and release of the extracellular domain of Klotho by ADAM10 and ADAM17. Proc Natl Acad Sci USA 104: 19796-19801, 2007.
7. Chen CD, Tung TY, Liang J, Zeldich E, Tucker Zhou TB, Turk BE, Abraham CR. Identification of cleavage sites leading to the shed form of the anti-aging protein klotho. Biochemistry 53: 5579-5587, 2014.
8. Cuppen E, van Ham M, Wansink DG, de Leeuw A, Wieringa B, Hendriks W. The zyxin-related protein TRIP6 interacts with PDZ motifs in the adaptor protein RIL and the protein tyrosine phosphatase PTP-BL. Eur J Cell Biol 79: 283-293, 2000.
9. de Baaij JH, Stuiver M, Meij IC, Lainez S, Kopplin K, Venselaar H, Muller D, Bindels RJ, Hoenderop JG. Membrane topology and intracellular processing of cyclin M2 (CNNM2). J Biol Chem 287: 13644-13655, 2012.
10. Edwards DR, Handsley MM, Pennington CJ. The ADAM metalloproteinases. Mol Aspects Med 29: 258-289, 2008.
11. Erraji-Benchekroun L, Couton D, Postic C, Borde I, Gaston J, Guillet JG, Andre C. Overexpression of β2-adrenergic receptors in mouse liver alters the expression of gluconeogenic and glycolytic enzymes. Am J Physiol Endocrinol Metab 288: E715-E722, 2005.
12. Gattineni J, Bates C, Twombley K, Dwarakanath V, Robinson ML, Goetz R, Mohammadi M, Baum M. FGF23 decreases renal NaPi-2a and NaPi-2c expression and induces hypophosphatemia in vivo predominantly via FGF receptor 1. Am J Physiol Renal Physiol 297: F282-F291, 2009.
13. Green WN, Millar NS. Ion-channel assembly. Trends Neurosci 18: 280-287, 1995.
14. Heijboer AC, Blankenstein MA, Hoenderop J, de Borst MH, Vervloet MG. Laboratory aspects of circulating β-Klotho. Nephrol Dial Transplant 28: 2283-2287, 2013.
15. Hoenderop JG, Muller D, Van Der Kemp AW, Hartog A, Suzuki M, Ishibashi K, Imai M, Sweep F, Willems PH, Van Os CH, Bindels RJ. Calcitriol controls the epithelial calcium channel in kidney. J Am Soc Nephrol 12: 1342-1349, 2001.
16. Hofmeister MV, Fenton RA, Praetorius J. Fluorescence isolation of mouse late distal convoluted tubules and connecting tubules: effects of vasopressin and vitamin D3 on Ca2+ signaling. Am J Physiol Renal Physiol 296: F194-F203, 2009.
17. Hu MC, Shi M, Zhang J, Addo T, Cho HJ, Barker SL, Ravikumar P, Gillings N, Bian A, Sidhu SS, Kuro OM, Moe OW. Renal production, uptake, and handling of circulating βKlotho. J Am Soc Nephrol; doi: 10.1681/ASN.2014101030.
18. Hu MC, Shi M, Zhang J, Pastor J, Nakatani T, Lanske B, Razzaque MS, Rosenblatt KP, Baum MG, Kuro-o M, Moe OW. Klotho: A novel phosphaturic substance acting as an autocrine enzyme in the renal proximal tubule. FASEB J 24: 3438-3450, 2010.
19. Hu MC, Shi M, Zhang J, Quinones H, Griffith C, Kuro-o M, Moe OW. Klotho deficiency causes vascular calcification in chronic kidney disease. J Am Soc Nephrol 22: 124-136, 2011.
20. Hundhausen C, Misztela D, Berkhout TA, Broadway N, Saftig P, Reiss K, Hartmann D, Fahrenholz F, Postina R, Matthews V, Kallen KJ, Rose-John S, Ludwig A. The disintegrin-like metalloproteinase ADAM10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion. Blood 102: 1186-1195, 2003.
21. Huybers S, Apostolaki M, van der Eerden BC, Kollias G, Naber TH, Bindels RJ, Hoenderop JG. Murine TNF(deltaARE) Crohn’s disease model displays diminished expression of intestinal Ca2+ transporters. Inflam Bowel Dis 14: 803-811, 2008.
22. Imura A, Iwano A, Tohyama O, Tsuji Y, Nozaki K, Hashimoto N, Fujimori T, Nabeshima Y. Secreted Klotho protein in sera and CSF: implication for post-translational cleavage in release of Klotho protein from cell membrane. FEBS Lett 565: 143-147, 2004.
23. Kawaguchi H, Manabe N, Miyaura C, Chikuda H, Nakamura K, Kuro-o M. Independent impairment of osteoblast and osteoclast differentiation in klotho mouse exhibiting low-turnover osteopenia. J Clin Invest 104: 229-237, 1999.
24. Koenderink JB, Geibel S, Grabsch E, De Pont JJ, Bamberg E, Friedrich T. Electrophysiological analysis of the mutated Na,K-ATPase cation binding pocket. J Biol Chem 278: 51213-51222, 2003.
25. Kottirsch G, Koch G, Feifel R, Neumann U. β-Aryl-succinic acid hydroxamates as dual inhibitors of matrix metalloproteinases and tumor necrosis factor β converting enzyme. J Med Chem 45: 2289-2293, 2002.
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. Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390: 45-51, 1997.
27. Kurosu H, Ogawa Y, Miyoshi M, Yamamoto M, Nandi A, Rosenblatt KP, Baum MG, Schiavi S, Hu MC, Moe OW, Kuro-o M. Regulation of fibroblast growth factor-23 signaling by klotho. J Biol Chem 281: 6120-6123, 2006.
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. Suppression of aging in mice by the hormone Klotho. Science 309: 1829-1833, 2005.
29. Lee WS, Ngo-Anh TJ, Bruening-Wright A, Maylie J, Adelman JP. Small conductance Ca2+-activated K+ channels and calmodulin: cell surface expression and gating. J Biol Chem 278: 25940-25946, 2003.
30. Leunissen EH, Nair AV, Bull C, Lefeber DJ, van Delft FL, Bindels RJ, Hoenderop JG. The epithelial calcium channel TRPV5 is regulated differentially by klotho and sialidase. J Biol Chem 288: 29238-29246, 2013.
31. Li SA, Watanabe M, Yamada H, Nagai A, Kinuta M, Takei K. Immunohistochemical localization of Klotho protein in brain, kidney, and reproductive organs of mice. Cell Struct Funct 29: 91-99, 2004.
32. Loffing J, Vallon V, Loffing-Cueni D, Aregger F, Richter K, Pietri L, Bloch-Faure M, Hoenderop JG, Shull GE, Meneton P, Kaissling B. Altered renal distal tubule structure and renal Na+ and Ca2+ handling in a mouse model for Gitelman’s syndrome. J Am Soc Nephrol 15: 2276-2288, 2004.
33. Lu P, Boros S, Chang Q, Bindels RJ, Hoenderop JG. The β-glucuronidase klotho exclusively activates the epithelial Ca2+ channels TRPV5 and TRPV6. Nephrol Dial Transplant 23: 3397-3402, 2008.
34. Maretzky T, Scholz F, Koten B, Proksch E, Saftig P, Reiss K. ADAM10-mediated E-cadherin release is regulated by proinflammatory cytokines and modulates keratinocyte cohesion in eczematous dermatitis. J Invest Dermatol 128: 1737-1746, 2008.
35. Markadieu N, San-Cristobal P, Nair AV, Verkaart S, Lenssen E, Tudpor K, van Zeeland F, Loffing J, Bindels RJ, Hoenderop JG. A primary culture of distal convoluted tubules expressing functional thiazide-sensitive NaCl transport. Am J Physiol Renal Physiol 303: F886-F892, 2012.
36. Meli DN, Loeffler JM, Baumann P, Neumann U, Buhl T, Leppert D, Leib SL. In Pneumococcal meningitis a novel water-soluble inhibitor of matrix metalloproteinases and TNF-β converting enzyme attenuates seizures and injury of the cerebral cortex. J Neuroimmunol 151: 6-11, 2004.
37. Meyer AH, Katona I, Blatow M, Rozov A, Monyer H. In Vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J Neurosci 22: 7055-7064, 2002.
38. Mulder GM, Melenhorst WB, Celie JW, Kloosterhuis NJ, Hillebrands JL, Ploeg RJ, Seelen MA, Visser L, van Dijk MC, van Goor H. ADAM17 up-regulation in renal transplant dysfunction and non-transplant-related renal fibrosis. Nephrol Dial Transplant 27: 2114-2122, 2012.
39. Murphy G. Regulation of the proteolytic disintegrin metalloproteinases, the “sheddases”. Semin Cell Dev Biol 20: 138-145, 2009.
40. Nijenhuis T, Hoenderop JG, Loffing J, van der Kemp AW, van Os CH, Bindels RJ. Thiazide-induced hypocalciuria is accompanied by a decreased expression of Ca2+ transport proteins in kidney. Kidney Int 64: 555-564, 2003.
41. Pearce LR, Sommer EM, Sakamoto K, Wullschleger S, Alessi DR. Protor-1 is required for efficient mTORC2-mediated activation of SGK1 in the kidney. Biochem J 436: 169-179, 2011.
42. Reddy P, Slack JL, Davis R, Cerretti DP, Kozlosky CJ, Blanton RA, Shows D, Peschon JJ, Black RA. Functional analysis of the domain structure of tumor necrosis factor-β converting enzyme. J Biol Chem 275: 14608-14614, 2000.
43. Sahin U, Weskamp G, Kelly K, Zhou HM, Higashiyama S, Peschon J, Hartmann D, Saftig P, Blobel CP. Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J Cell Biol 164: 769-779, 2004.
44. Satoh M, Nagasu H, Morita Y, Yamaguchi TP, Kanwar YS, Kashihara N. Klotho protects against mouse renal fibrosis by inhibiting Wnt signaling. Am J Physiol Renal Physiol 303: F1641-F1651, 2012.
45. Schramme A, Abdel-Bakky MS, Gutwein P, Obermuller N, Baer PC, Hauser IA, Ludwig A, Gauer S, Schafer L, Sobkowiak E, Altevogt P, Koziolek M, Kiss E, Grone HJ, Tikkanen R, Goren I, Radeke H, Pfeilschifter J. Characterization of CXCL16 and ADAM10 in the normal and transplanted kidney. Kidney Int 74: 328-338, 2008.
46. Shimada T, Mizutani S, Muto T, Yoneya T, Hino R, Takeda S, Takeuchi Y, Fujita T, Fukumoto S, Yamashita T. Cloning and characterization of FGF23 as a causative factor of tumor-induced osteomalacia. Proc Natl Acad Sci USA 98: 6500-6505, 2001.
47. Shiraki-Iida T, Iida A, Nabeshima Y, Anazawa H, Nishikawa S, Noda M, Kuro-o M, Nabeshima Y. Improvement of multiple pathophysiological phenotypes of klotho (kl/kl) mice by adenovirus-mediated expression of the klotho gene. J Gene Med 2: 233-242, 2000.
48. Souza DG, Ferreira FL, Fagundes CT, Amaral FA, Vieira AT, Lisboa RA, Andrade MV, Trifilieff A, Teixeira MM. Effects of PKF242-484 and PKF241-466, novel dual inhibitors of TNF-β converting enzyme and matrix metalloproteinases, in a model of intestinal reperfusion injury in mice. Eur J Pharmacol 571: 72-80, 2007.
49. Tohyama O, Imura A, Iwano A, Freund JN, Henrissat B, Fujimori T, Nabeshima Y. Klotho is a novel β-glucuronidase capable of hydrolyzing steroid β-glucuronides. J Biol Chem 279: 9777-9784, 2004.
50. Trifilieff A, Walker C, Keller T, Kottirsch G, Neumann U. Pharmacological profile of PKF242-484 and PKF241-466, novel dual inhibitors of TNF-β converting enzyme and matrix metalloproteinases, in models of airway inflammation. Br J Pharmacol 135: 1655-1664, 2002.
51. Urakawa I, Yamazaki Y, Shimada T, Iijima K, Hasegawa H, Okawa K, Fujita T, Fukumoto S, Yamashita T. Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 444: 770-774, 2006.