Biochemical and functional characterization of the klotho-VS polymorphism implicated in aging and disease risk

Journal of Biological Chemistry

Volumn 288, Issue 51, 2013, Pages 36302-36311

  Zhou, Tracey B Tucker ^a   King, Gwendalyn D ^a   Chen, CiDi ^a   Abraham, Carmela R ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-AGING; DISEASE RISKS; FUNCTIONAL CHARACTERIZATION; HETERODIMERIZATION; HOMODIMERIZATION; IN-VITRO; LIFE SPAN;

BIOCHEMISTRY; BIOLOGY;

DIMERIZATION;

FIBROBLAST GROWTH FACTOR RECEPTOR 1; KLOTHO PROTEIN;

AGING; ARTICLE; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HUMAN; HUMAN CELL; KLVS GENE; LIFE EXPECTANCY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN POLYMORPHISM; PROTEIN PROTEIN INTERACTION; RISK FACTOR; WILD TYPE;

AGING; CELL SIGNALING; DIMERIZAION; FIBROBLAST GROWTH FACTOR RECEPTOR (FGFR); GENETIC POLYMORPHISM; PROTEIN COMPLEXES; SHEDDING;

AGING; AGING, PREMATURE; GENETIC PREDISPOSITION TO DISEASE; GLUCURONIDASE; HEK293 CELLS; HUMANS; MUTATION, MISSENSE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1;

EID: 84890893910     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.490052     Document Type: Article

References (62)

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. Duce, J. A., Podvin, S., Hollander, W., Kipling, D., Rosene, D. L., and Abraham, C. R. (2008) Gene profile analysis implicates Klotho as an important contributor to aging changes in brain white matter of the rhesus monkey. Glia 56, 106-117
3. King, G. D., Rosene, D. L., and Abraham, C. R. (2012) Promoter methylation and age-related downregulation of Klotho in rhesus monkey. Age 34, 1405-1419
4. 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
5. Yamamoto, M., Clark, J. D., Pastor, J. V., Gurnani, P., Nandi, A., Kurosu, H., Miyoshi, M., Ogawa, Y., Castrillon, D. H., Rosenblatt, K. P., and Kuro-o, M. (2005) Regulation of oxidative stress by the anti-aging hormone klotho. J. Biol. Chem. 280, 38029-38034
6. Haruna, Y., Kashihara, N., Satoh, M., Tomita, N., Namikoshi, T., Sasaki, T., Fujimori, T., Xie, P., and Kanwar, Y. S. (2007) Amelioration of progressive renal injury by genetic manipulation of Klotho gene. Proc. Natl. Acad. Sci. U.S.A. 104, 2331-2336
7. Chen, C. D., Podvin, S., Gillespie, E., Leeman, S. E., and Abraham, C. R. (2007) Insulin stimulates the cleavage and release of the extracellular domain of Klotho by ADAM10 and ADAM17. Proc. Natl. Acad. Sci. U.S.A. 104, 19796-19801
8. Imura, A., Iwano, A., Tohyama, O., Tsuji, Y., Nozaki, K., Hashimoto, N., Fujimori, T., and Nabeshima, Y. (2004) 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
9. Lin, B. C., Wang, M., Blackmore, C., and Desnoyers, L. R. (2007) Liverspecific activities of FGF19 require Klotho β. J. Biol. Chem. 282, 27277-27284
10. Ogawa, Y., Kurosu, H., Yamamoto, M., Nandi, A., Rosenblatt, K. P., Goetz, R., Eliseenkova, A. V., Mohammadi, M., and Kuro-o, M. (2007) βKlotho is required for metabolic activity of fibroblast growth factor 21. Proc. Natl. Acad. Sci. U.S.A. 104, 7432-7437
11. Kharitonenkov, A., Dunbar, J. D., Bina, H. A., Bright, S., Moyers, J. S., Zhang, C., Ding, L., Micanovic, R., Mehrbod, S. F., Knierman, M. D., Hale, J. E., Coskun, T., and Shanafelt, A. B. (2008) FGF-21/FGF-21 receptor interaction and activation is determined by betaKlotho. J. Cell. Physiol. 215, 1-7
12. Liu, H., Fergusson, M. M., Castilho, R. M., Liu, J., Cao, L., Chen, J., Malide, D., Rovira, II, Schimel, D., Kuo, C. J., Gutkind, J. S., Hwang, P. M., and Finkel, T. (2007) Augmented Wnt signaling in a mammalian model of accelerated aging. Science 317, 803-806
13. Chang, Q., Hoefs, S., van der Kemp, A. W., Topala, C. N., Bindels, R. J., and Hoenderop, J. G. (2005) The β-glucuronidase klotho hydrolyzes and activates the TRPV5 channel. Science 310, 490-493
14. 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 cellsurface retention of TRPV5 channel via binding to galectin-1. Proc. Natl Acad. Sci. U.S.A. 105, 9805-9810
15. Lu, L., Katsaros, D., Wiley, A., de la Longrais, I. A., Puopolo, M., and Yu, H. (2008) Klotho expression in epithelial ovarian cancer and its association with insulin-like growth factors and disease progression. Cancer Invest.26, 185-192
16. 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
17. Kusaba, T., Okigaki, M., Matui, A., Murakami, M., Ishikawa, K., Kimura, T., Sonomura, K., Adachi, Y., Shibuya, M., Shirayama, T., Tanda, S., Hatta, T., Sasaki, S., Mori, Y., and Matsubara, H. (2010) Klotho is associated with VEGF receptor-2 and the transient receptor potential canonical-1 Ca2+channel to maintain endothelial integrity. Proc. Natl. Acad. Sci. U.S.A. 107, 19308-19313
18. Sopjani, M., Alesutan, I., Dërmaku-Sopjani, M., Gu, S., Zelenak, C., Munoz, C., Velic, A., Föller, M., Rosenblatt, K. P., Kuro-o, M., and Lang, F. (2011) Regulation of the Na+/K+ ATPase by Klotho. FEBS Lett. 585, 1759-1764
19. Maekawa, Y., Ishikawa, K., Yasuda, O., Oguro, R., Hanasaki, H., Kida, I., Takemura, Y., Ohishi, M., Katsuya, T., and Rakugi, H. (2009) Klotho suppresses TNF-α-induced expression of adhesion molecules in the endothelium and attenuates NF-κB activation. Endocrine 35, 341-346
20. Invidia, L., Salvioli, S., Altilia, S., Pierini, M., Panourgia, M. P., Monti, D., De Rango, F., Passarino, G., and Franceschi, C. (2010) The frequency of Klotho KL-VS polymorphism in a large Italian population, from young subjects to centenarians, suggests the presence of specific time windows for its effect. Biogerontology 11, 67-73
21. Arking, D. E., Atzmon, G., Arking, A., Barzilai, N., and Dietz, H. C. (2005) Association between a functional variant of the KLOTHO gene and highdensity lipoprotein cholesterol, blood pressure, stroke, and longevity. Circ. Res. 96, 412-418
22. Arking, D. E., Krebsova, A., Macek, M., Sr., Macek, M., Jr., Arking, A., Mian, I. S., Fried, L., Hamosh, A., Dey, S., McIntosh, I., and Dietz, H. C. (2002) Association of human aging with a functional variant of klotho. Proc. Natl. Acad. Sci. U.S.A. 99, 856-861
23. Arking, D. E., Becker, D. M., Yanek, L. R., Fallin, D., Judge, D. P., Moy, T. F., Becker, L. C., and Dietz, H. C. (2003) KLOTHO allele status and the risk of early-onset occult coronary artery disease. Am. J. Hum. Genet. 72, 1154-1161
24. Majumdar, V., Nagaraja, D., and Christopher, R. (2010) Association of the functional KL-VS variant of Klotho gene with early-onset ischemic stroke. Biochem. Biophys. Res. Commun. 403, 412-416
25. Majumdar, V., and Christopher, R. (2011) Association of exonic variants of Klotho with metabolic syndrome in Asian Indians. Clin. Chim. Acta 412, 1116-1121
26. Riancho, J. A., Valero, C., Hernández, J. L., Ortiz, F., Zarrabeitia, A., Alonso, M. A., Peña, N., Pascual, M. A., González-Macías, J., and Zarrabeitia, M. T. (2007) Association of the F352V variant of the Klotho gene with bone mineral density. Biogerontology 8, 121-127
27. Zarrabeitia, M. T., Hernández, J. L., Valero, C., Zarrabeitia, A. L., Ortiz, F., Gonzalez-Macias, J., and Riancho, J. A. (2007) Klotho gene polymorphism and male bone mass. Calcif Tissue Int. 80, 10-14
28. Wolf, I., Laitman, Y., Rubinek, T., Abramovitz, L., Novikov, I., Beeri, R., Kuro-O, M., Koeffler, H. P., Catane, R., Freedman, L. S., Levy-Lahad, E., Karlan, B. Y., Friedman, E., and Kaufman, B. (2010) Functional variant o of KLOTHO: a breast cancer risk modifier among BRCA1 mutation carriers of Ashkenazi origin. Oncogene 29, 26-33
29. Laitman, Y., Kuchenbaecker, K. B., Rantala, J., Hogervorst, F., Peock, S., Godwin, A. K., Arason, A., Kirchhoff, T., Offit, K., Isaacs, C., Schmutzler, R. K., Wappenschmidt, B., Nevanlinna, H., Chen, X., Chenevix-Trench, G., Healey, S., Couch, F., Peterlongo, P., Radice, P., Nathanson, K. L., Caligo, M. A., Neuhausen, S. L., Ganz, P., Sinilnikova, O. M., McGuffog, L., Easton, D. F., Antoniou, A. C., Wolf, I., and Friedman, E. (2012) The KL-VS sequence variant of Klotho and cancer risk in BRCA1 and BRCA2 mutation carriers. Breast Cancer Res. Treat. 132, 1119-1126
30. Fimbel, S., Déchaud, H., Grenot, C., Tabard, L., Claustrat, F., Bador, R., and Pugeat, M. (1995) Use of non-radioactive labels for half-life measurement of sex hormone-binding globulin in the rabbit. Steroids 60, 686-692
31. Hurtley, S. M., and Helenius, A. (1989) Protein oligomerization in the endoplasmic reticulum. Annu. Rev. Cell Biol. 5, 277-307
32. Pelham, H. R. (1989) Control of protein exit from the endoplasmic reticulum. Annu. Rev. Cell Biol. 5, 1-23
33. Li, W., and Stanley, E. R. (1991) Role of dimerization and modification of the CSF-1 receptor in its activation and internalization during the CSF-1 response. EMBO J. 10, 277-288
34. Wang, Q., Villeneuve, G., and Wang, Z. (2005) Control of epidermal growth factor receptor endocytosis by receptor dimerization, rather than receptor kinase activation. EMBO Rep. 6, 942-948
35. Kurosu, H., Ogawa, Y., Miyoshi, M., Yamamoto, M., Nandi, A., Rosenblatt, K. P., Baum, M. G., Schiavi, S., Hu, M. C., Moe, O. W., and Kuro-o, M. (2006) Regulation of fibroblast growth factor-23 signaling by klotho. J. Biol. Chem. 281, 6120-6123
36. Urakawa, I., Yamazaki, Y., Shimada, T., Iijima, K., Hasegawa, H., Okawa, K., Fujita, T., Fukumoto, S., and Yamashita, T. (2006) Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 444, 770-774
37. Goetz, R., Beenken, A., Ibrahimi, O. A., Kalinina, J., Olsen, S. K., Eliseenkova, A. V., Xu, C., Neubert, T. A., Zhang, F., Linhardt, R. J., Yu, X., White, K. E., Inagaki, T., Kliewer, S. A., Yamamoto, M., Kurosu, H., Ogawa, Y., Kuro-o, M., Lanske, B., Razzaque, M. S., and Mohammadi, M. (2007) Molecular insights into the klotho-dependent, endocrine mode of action of fibroblast growth factor 19 subfamily members. Mol. Cell. Biol. 27, 3417-3428
38. Wu, X., Lemon, B., Li, X., Gupte, J., Weiszmann, J., Stevens, J., Hawkins, N., Shen, W., Lindberg, R., Chen, J. L., Tian, H., and Li, Y. (2008) C-terminal tail of FGF19 determines its specificity toward Klotho co-receptors. J. Biol. Chem. 283, 33304-33309
39. 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. Musculoskelet. Neuronal Interact. 7, 318-319
40. Brownstein, C. A., Adler, F., Nelson-Williams, C., Iijima, J., Li, P., Imura, A., Nabeshima, Y., Reyes-Mugica, M., Carpenter, T. O., and Lifton, R. P. (2008) A translocation causing increased α-klotho level results in hypophosphatemic ickets and hyperparathyroidism. Proc. Natl. Acad. Sci. U.S.A. 105, 3455-3460
41. Rhee, E. J., Oh, K. W., Yun, E. J., Jung, C. H., Lee, W. Y., Kim, S. W., Baek, K. H., Kang, M. I., and Park, S. W. (2006) Relationship between polymorphisms G395A in promoter and C1818T in exon 4 of the KLOTHO gene with glucose metabolism and cardiovascular risk factors in Korean women. J. Endocrinol. Invest. 29, 613-618
42. Kawano, K., Ogata, N., Chiano, M., Molloy, H., Kleyn, P., Spector, T. D., Uchida, M., Hosoi, T., Suzuki, T., Orimo, H., Inoue, S., Nabeshima, Y., Nakamura, K., Kuro-o, M., and Kawaguchi, H. (2002) Klotho gene polymorphisms associated with bone density of aged postmenopausal women. J. Bone Miner Res. 17, 1744-1751
43. Rhee, E. J., Oh, K. W., Lee, W. Y., Kim, S. Y., Jung, C. H., Kim, B. J., Sung, K. C., Kim, B. S., Kang, J. H., Lee, M. H., Kim, S. W., and Park, J. R. (2006) The differential effects of age on the association of KLOTHO gene polymorphisms with coronary artery disease. Metabolism 55, 1344-1351
44. Ogata, N., Matsumura, Y., Shiraki, M., Kawano, K., Koshizuka, Y., Hosoi, T., Nakamura, K., Kuro-O, M., and Kawaguchi, H. (2002) Association of klotho gene polymorphism with bone density and spondylosis of the lumbar spine in postmenopausal women. Bone 31, 37-42
45. Mullin, B. H., Wilson, S. G., Islam, F. M., Calautti, M., Dick, I. M., Devine, A., and Prince, R. L. (2005) Klotho gene polymorphisms are associated with osteocalcin levels but not bone density of aged postmenopausal women. Calcif. Tissue Int. 77, 145-151
46. Shimoyama, Y., Nishio, K., Hamajima, N., and Niwa, T. (2009) KLOTHO gene polymorphisms G-395A and C1818T are associated with lipid and glucose metabolism, bone mineral density and systolic blood pressure in Japanese healthy subjects. Clin. Chim. Acta 406, 134-138
47. Nolan, V. G., Baldwin, C., Ma, Q., Wyszynski, D. F., Amirault, Y., Farrell, J. J., Bisbee, A., Embury, S. H., Farrer, L. A., and Steinberg, M. H. (2005) Association of single nucleotide polymorphisms in klotho with priapism in sickle cell anaemia. Br. J. Haematol. 128, 266-272
48. Shimoyama, Y., Taki, K., Mitsuda, Y., Tsuruta, Y., Hamajima, N., and Niwa, T. (2009) KLOTHO gene polymorphisms G-395A and C1818T are associated with low-density lipoprotein cholesterol and uric acid in Japanese hemodialysis patients. Am. J. Nephrol. 30, 383-388
49. 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
50. Freathy, R. M., Weedon, M. N., Melzer, D., Shields, B., Hitman, G. A., Walker, M., McCarthy, M. I., Hattersley, A. T., and Frayling, T. M. (2006) The functional "KL-VS" variant of KLOTHO is not associated with type 2 diabetes in 5028 UK Caucasians. BMC Med. Genet. 7, 51
51. Low, A. F., O'Donnell, C. J., Kathiresan, S., Everett, B., Chae, C. U., Shaw, S. Y., Ellinor, P. T., and MacRae, C. A. (2005) Aging syndrome genes and premature coronary artery disease. BMC Med. Genet. 6, 38
52. Tangri, N., Alam, A., Wooten, E. C., and Huggins, G. S. (2011) Lack of association of Klotho gene variants with valvular and vascular calcification in Caucasians: a candidate gene study of the Framingham Offspring Cohort. Nephrol. Dial Transplant 26, 3998-4002
53. Brunelli, S. M., and Goldfarb, S. (2007) Hypophosphatemia: clinical consequences and management. J. Am. Soc. Nephrol. 18, 1999-2003
54. Creighton, T. E. (1978) Experimental studies of protein folding and unfolding. Prog. Biophys. Mol. Biol. 33, 231-297
55. Banerjee, R. R., and Lazar, M. A. (2001) Dimerization of resistin and resistin- like molecules is determined by a single cysteine. J. Biol. Chem. 276, 25970-25973
56. Romano, C., Yang, W. L., and O'Malley, K. L. (1996) Metabotropic glutamate receptor 5 is a disulfide-linked dimer. J. Biol. Chem. 271, 28612-28616
57. Boyson, J. E., Erskine, R., Whitman, M. C., Chiu, M., Lau, J. M., Koopman, L. A., Valter, M. M., Angelisova, P., Horejsi, V., and Strominger, J. L. (2002) Disulfide bond-mediated dimerization of HLA-G on the cell surface. Proc. Natl. Acad. Sci. U.S.A. 99, 16180-16185
58. Scheuermann, S., Hambsch, B., Hesse, L., Stumm, J., Schmidt, C., Beher, D., Bayer, T. A., Beyreuther, K., and Multhaup, G. (2001) Homodimerization of amyloid precursor protein and its implication in the amyloidogenic pathway of Alzheimer's disease. J. Biol. Chem. 276, 33923-33929
59. Ferrè, F., and Clote, P. (2005) DiANNA: a web server for disulfide connectivity prediction. Nucleic Acids Res. 33, W230-232
60. Hu, M. C., Kuro-O, M., and Moe, O. W. (2013) Klotho and chronic kidney disease. Contrib. Nephrol. 180, 47-63
61. Olauson, H., and Larsson, T. E. (2013) FGF23 and Klotho in chronic kidney disease. Curr. Opin Nephrol Hypertens. 22, 397-404
62. Martin, A., David, V., and Quarles, L. D. (2012) Regulation and function of the FGF23/klotho endocrine pathways. Physiol. Rev. 92, 131-155