α-Klotho mice demonstrate increased expression of the non-sulfated N-glycan form of the HNK-1 glyco-epitope in kidney tissue

Journal of Biochemistry

Volumn 156, Issue 2, 2014, Pages 107-113

  Akasaka Manya, Keiko ^a   Manya, Hiroshi ^a   Kizuka, Yasuhiko ^b   Oka, Shogo ^b   Endo, Tamao ^a  

^a Tokyo Metropolitan Institute of Gerontology   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Glucuronyltransferase; Kidney; Non sulfated HNK 1 epitope; Klotho; Glucuronidase

Indexed keywords

ALPHA KLOTHO PROTEIN; BETA GLUCURONIDASE; GLUCURONIC ACID; GLUCURONOSYLTRANSFERASE; GLUCURONOSYLTRANSFERASE S; GLYCAN; HUMAN NATURAL KILLER 1 GLYCO EPITOPE; KLOTHO PROTEIN; MICROSOMAL AMINOPEPTIDASE; UNCLASSIFIED DRUG; ALPHAKLOTHO PROTEIN, MOUSE; CD57 ANTIGEN; CELL SURFACE RECEPTOR; POLYSACCHARIDE;

AGING; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; KIDNEY CORTEX; KIDNEY PARENCHYMA; MALE; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; ANIMAL; ANTIBODY SPECIFICITY; BRAIN; C57BL MOUSE; ENZYMOLOGY; GENETICS; GLYCOSYLATION; KIDNEY; KNOCKOUT MOUSE; METABOLISM; PROTEIN PROCESSING;

ANIMALS; ANTIGENS, CD57; BRAIN; GLUCURONIDASE; GLYCOSYLATION; KIDNEY; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN SPECIFICITY; POLYSACCHARIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, CELL SURFACE;

EID: 84905662107     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvu024     Document Type: Article

References (35)

1. 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., and Nabeshima, Y.I. (1997) Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390, 45-51
2. Kurosu, H., Yamamoto, M., Clark, J.D., Pastor, J.V., Nandi, A., Gurnani, P., McGuinness, O.P., Chikuda, H., Yamaguchi, M., Kawaguchi, H., Shimomura, I., Takayama, Y., Herz, J., Kahn, C.R., Rosenblatt, K.P., and Kuro-o, M. (2005) Suppression of aging in mice by the hormone Klotho. Science 309, 1829-1833
3. Tohyama, O., Imura, A., Iwano, A., Freund, J.N., Henrissat, B., Fujimori, T., and Nabeshima, Y. (2004) Klotho is a novel beta-glucuronidase capable of hydrolyzing steroid beta-glucuronides. J. Biol. Chem. 279, 9777-9784
4. Cha, S.K., Ortega, B., Kurosu, H., Rosenblatt, K.P., Kuro-o, M., and Huang, C.L. (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
5. Cha, S.K., Hu, M.C., Kurosu, H., Kuro-o, M., Moe, O., and Huang, C.L. (2009) Regulation of renal outer medullary potassium channel and renal K+ excretion by Klotho. Mol. Pharmacol. 76, 38-46
6. Chang, Q., Hoefs, S., van der Kemp, A.W., Topala, C.N., Bindels, R.J., and Hoenderop, J.G. (2005) The beta-glucuronidase klotho hydrolyzes and activates the TRPV5 channel. Science 310, 490-493
7. Lu, P., Boros, S., Chang, Q., Bindels, R.J., and Hoenderop, J.G. (2008) The beta-glucuronidase klotho exclusively activates the epithelial Ca2+ channels TRPV5 and TRPV6. Nephrol. Dial. Transplant. 23, 3397-3402
8. Leunissen, E.H., Nair, A.V., Bull, C., Lefeber, D.J., van Delft, F.L., Bindels, R.J., and Hoenderop, J.G. (2013) The epithelial calcium channel TRPV5 is regulated differentially by klotho and sialidase. J. Biol. Chem. 288, 29238-29246
9. Hu, M.C., Shi, M., Zhang, J., Pastor, J., Nakatani, T., Lanske, B., Razzaque, M.S., Rosenblatt, K.P., Baum, M.G., Kuro-o, M., and Moe, O.W. (2010) Klotho: a novel phosphaturic substance acting as an autocrineenzyme in the renal proximal tubule. FASEB J. 24, 3438-3450
10. Manya, H., Akasaka-Manya, K., and Endo, T. (2010) Klotho protein deficiency and aging. Geriatr. Gerontol. Int. 10 (Suppl. 1), S80-S87
11. Terayama, K., Oka, S., Seiki, T., Miki, Y., Nakamura, A., Kozutsumi, Y., Takio, K., and Kawasaki, T. (1997) Cloning and functional expression of a novel glucuronyltransferase involved in the biosynthesis of the carbohydrate epitope HNK-1. Proc. Natl. Acad. Sci. USA 94, 6093-6098
12. Tagawa, H., Kizuka, Y., Ikeda, T., Itoh, S., Kawasaki, N., Kurihara, H., Onozato, M.L., Tojo, A., Sakai, T., Kawasaki, T., and Oka, S. (2005) A non-sulfated form of the HNK-1 carbohydrate is expressed in mouse kidney. J. Biol. Chem. 280, 23876-23883
13. Allory, Y., Commo, F., Boccon-Gibod, L., Sibony, M., Callard, P., Ronco, P., and Debiec, H. (2006) Sulfated HNK-1 epitope in developing and mature kidney: a new marker for thin ascending loop of Henle and tubular injury in acute tubular necrosis. J. Histochem. Cytochem. 54, 575-584
14. Kruse, J., Mailhammer, R., Wernecke, H., Faissner, A., Sommer, I., Goridis, C., and Schachner, M. (1984) Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature 311, 153-155
15. Becker, T., Becker, C.G., Schachner, M., and Bernhardt, R.R. (2001) Antibody to the HNK-1 glycoepitope affects fasciculation and axonal pathfinding in the developing posterior lateral line nerve of embryonic zebrafish. Mech. Dev. 109, 37-49
16. Nagase, T., Sanai, Y., Nakamura, S., Asato, H., Harii, K., and Osumi, N. (2003) Roles of HNK-1 carbohydrate epitope and its synthetic glucuronyltransferase genes on migration of rat neural crest cells. J. Anat. 203, 77-88
17. Manya, H., Inomata, M., Fujimori, T., Dohmae, N., Sato, Y., Takio, K., Nabeshima, Y., and Endo, T. (2002) Klotho protein deficiency leads to overactivation of mu-calpain. J. Biol. Chem. 277, 35503-35508
18. Jiang, W., Gorbea, C.M., Flannery, A.V., Beynon, R.J., Grant, G.A., and Bond, J.S. (1992) The alpha subunit of meprin A. Molecular cloning and sequencing, differential expression in inbred mouse strains, and evidence for divergent evolution of the alpha and beta subunits. J. Biol. Chem. 267, 9185-9193
19. Takeshita, K., Fujimori, T., Kurotaki, Y., Honjo, H., Tsujikawa, H., Yasui, K., Lee, J.K., Kamiya, K., Kitaichi, K., Yamamoto, K., Ito, M., Kondo, T., Iino, S., Inden, Y., Hirai, M., Murohara, T., Kodama, I., and Nabeshima, Y. (2004) Sinoatrial node dysfunction and early unexpected death of mice with a defect of klotho gene expression. Circulation 109, 1776-1782
20. Kato, Y., Arakawa, E., Kinoshita, S., Shirai, A., Furuya, A., Yamano, K., Nakamura, K., Iida, A., Anazawa, H., Koh, N., Iwano, A., Imura, A., Fujimori, T., Kuro-o, M., Hanai, N., Takeshige, K., and Nabeshima, Y. (2000) Establishment of the anti-Klotho monoclonal antibodies and detection of Klotho protein in kidneys. Biochem. Biophys. Res. Commun. 267, 597-602
21. Li, S.A., Watanabe, M., Yamada, H., Nagai, A., Kinuta, M., and Takei, K. (2004) Immunohistochemical localization of Klotho protein in brain, kidney, and reproductive organs of mice. Cell Struct. Funct. 29, 91-99
22. Kakuda, S., Sato, Y., Tonoyama, Y., Oka, S., and Kawasaki, T. (2005) Different acceptor specificities of two glucuronyltransferases involved in the biosynthesis of HNK-1 carbohydrate. Glycobiology 15, 203-210
23. Kakuda, S., Shiba, T., Ishiguro, M., Tagawa, H., Oka, S., Kajihara, Y., Kawasaki, T., Wakatsuki, S., and Kato, R. (2004) Structural basis for acceptor substrate recognition of a human glucuronyltransferase, GlcAT-P, an enzyme critical in the biosynthesis of the carbohydrate epitope HNK-1. J. Biol. Chem. 279, 22693-22703
24. Ito, S., Kinoshita, S., Shiraishi, N., Nakagawa, S., Sekine, S., Fujimori, T., and Nabeshima, Y.I. (2000) Molecular cloning and expression analyses of mouse betaklotho, which encodes a novel Klotho family protein. Mech. Dev. 98, 115-119
25. Ito, S., Fujimori, T., Hayashizaki, Y., and Nabeshima, Y. (2002) Identification of a novel mouse membranebound family 1 glycosidase-like protein, which carries an atypical active site structure. Biochim. Biophys. Acta 1576, 341-345
26. Yahata, K., Mori, K., Arai, H., Koide, S., Ogawa, Y., Mukoyama, M., Sugawara, A., Ozaki, S., Tanaka, I., Nabeshima, Y., and Nakao, K. (2000) Molecular cloning and expression of a novel klotho-related protein. J. Mol. Med. (Berl) 78, 389-394
27. Hayashi, Y., Okino, N., Kakuta, Y., Shikanai, T., Tani, M., Narimatsu, H., and Ito, M. (2007) Klotho-related protein is a novel cytosolic neutral beta-glycosylceramidase. J. Biol. Chem. 282, 30889-30900
28. Mina-Osorio, P. (2008) The moonlighting enzyme CD13: old and new functions to target. Trends Mol. Med. 14, 361-371
29. Broder, C. and Becker-Pauly, C. (2013) The metalloproteases meprin alpha and meprin beta: unique enzymes in inflammation, neurodegeneration, cancer and fibrosis. Biochem. J. 450, 253-264
30. Sterchi, E.E., Stocker, W., and Bond, J.S. (2008) Meprins, membrane-bound and secreted astacin metalloproteinases. Mol. Aspects Med. 29, 309-328
31. Kadowaki, T., Tsukuba, T., Bertenshaw, G.P., and Bond, J.S. (2000) N-Linked oligosaccharides on the meprin A metalloprotease are important for secretion and enzymatic activity, but not for apical targeting. J. Biol. Chem. 275, 25577-25584
32. Bostrom, M.A., Hicks, P.J., Lu, L., Langefeld, C.D., Freedman, B.I., and Bowden, D.W. (2010) Association of polymorphisms in the klotho gene with severity of non-diabetic ESRD in African Americans. Nephrol. Dial. Transplant. 25, 3348-3355
33. Friedman, D.J., Afkarian, M., Tamez, H., Bhan, I., Isakova, T., Wolf, M., Ankers, E., Ye, J., Tonelli, M., Zoccali, C., Kuro-o, M., Moe, O., Karumanchi, S.A., and Thadhani, R. (2009) Klotho variants and chronic hemodialysis mortality. J. Bone Miner. Res. 24, 1847-1855
34. Ko, G.J., Lee, E.A., Jeon, U.S., Pyo, H.J., Chin, H.J., Chae, D.W., Kim, S., and Kwon, Y.J. (2012) The association of Klotho polymorphism with disease progression and mortality in IgA nephropathy. Kidney Blood Press. Res. 36, 191-199
35. Ichikawa, S., Imel, E.A., Kreiter,M.L., Yu, X., Mackenzie, D.S., Sorenson, A.H., Goetz, R., Mohammadi, M., White, K.E., and Econs, M.J. (2007) A homozygous missense mutation in human KLOTHO causes severe tumoral calcinosis. J. Clin. Invest. 117, 2684-2691