Klotho as a regulator of oxidative stress and senescence

Biological Chemistry

Volumn 389, Issue 3, 2008, Pages 233-241

  Kuro o, Makoto ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Fibroblast growth factor (FGF); IGF; Phosphate; Vitamin D; Wnt

Indexed keywords

FIBROBLAST GROWTH FACTOR 23; FIBROBLAST GROWTH FACTOR RECEPTOR; FOLLITROPIN; INSULIN; KLOTHO PROTEIN; LUTEINIZING HORMONE; NITRIC OXIDE; SOMATOMEDIN C; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR FKHR; VANILLOID RECEPTOR 5; WNT PROTEIN;

AGING; AMYOTROPHIC LATERAL SCLEROSIS; CALCIFICATION; CELL DIFFERENTIATION; CELL MATURATION; COGNITIVE DEFECT; GENE FUNCTION; GENE OVEREXPRESSION; HEARING LOSS; HYPOGONADISM; LIFESPAN; LUNG EMPHYSEMA; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SENESCENCE; SKIN ATROPHY; THYMUS; VITAMIN D METABOLISM;

AGING; ANIMALS; ATROPHY; BONE DENSITY; CALCINOSIS; COGNITION DISORDERS; FEMALE; FIBROBLAST GROWTH FACTORS; GLUCURONIDASE; HEARING LOSS; HYPOGONADISM; INSULIN; INSULIN-LIKE GROWTH FACTOR I; ION CHANNELS; MALE; MICE; MICE, TRANSGENIC; NITRIC OXIDE; OSTEOPOROSIS; OXIDATIVE STRESS; PULMONARY EMPHYSEMA; SIGNAL TRANSDUCTION; SKIN; SPINAL CORD DISEASES; WNT PROTEINS;

MUS;

EID: 40149102029     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2008.028     Document Type: Review

References (74)

1. Anamizu, Y., Kawaguchi, H., Seichi, A., Yamaguchi, S., Kawakami, E., Kanda, N., Matsubara, S., Kuro-o, M., Nabeshima, Y., Nakamura, K., et al. (2005). Klotho insufficiency causes decrease of ribosomal RNA gene transcription activity, cytoplasmic RNA and rough ER in the spinal anterior horn cells. Acta Neuropathol. (Berl.) 109, 457-466.
2. Badman, M.K., Pissios, P., Kennedy, A.R., Koukos, G., Flier, J.S., and Maratos-Flier, E. (2007). Hepatic fibroblast growth factor 21 is regulated by PPARa and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metab. 5, 426-437.
3. Bartke, A., Brown-Borg, H., Mattison, J., Kinney, B., Hauck, S., and Wright, C. (2001). Prolonged longevity of hypopituitary dwarf mice. Exp. Gerontol. 36, 21-28.
4. Bluher, M., Kahn, B.B., and Kahn, C.R. (2003). Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299, 572-574.
5. Brunet, A., Bonni, A., Zigmond, M.J., Lin, M.Z., Juo, P., Hu, L.S., Anderson, M.J., Arden, K.C., Blenis, J., and Greenberg, M.E. (1999). Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868.
6. 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.
7. Clancy, D.J., Gems, D., Harshman, L.G., Oldham, S., Stocker, H., Hafen, E., Leevers, S.J., and Partridge, L. (2001). Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292, 104-106.
8. Essers, M.A., de Vries-Smits, L.M., Barker, N., Polderman, P.E., Burgering, B.M., and Korswagen, H.C. (2005). Functional interaction between β-catenin and FOXO in oxidative stress signaling. Science 308, 1181-1184.
9. Goetz, R., Beenken, A., Ibrahimi, O.A., Kalinina, J., Olsen, S.K., Eliseenkova, A.V., Xu, C., Neubert, T., Zhang, F., Linhardt, R.J., et al. (2007). Molecular insights into the Klotho-dependent, endocrine mode of action of FGF19 subfamily members. Mol. Cell Biol. 27, 3417-3428.
10. 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. USA 104, 2331-2336.
11. Hesse, M., Frohlich, L.F., Zeitz, U., Lanske, B., and Erben, R.G. (2007). Ablation of vitamin D signaling rescues bone, mineral, and glucose homeostasis in Fgf-23 deficient mice. Matrix Biol. 26, 75-84.
12. Hoenderop, J.G., Nilius, B., and Bindels, R.J. (2005). Calcium absorption across epithelia. Physiol. Rev. 85, 373-422.
13. Holzenberger, M., Dupont, J., Ducos, B., Leneuve, P., Geloen, A., Even, P.C., Cervera, P., and Le Bouc, Y. (2003). IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421, 182-187.
14. 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, 2692-2701.
15. Ikushima, M., Rakugi, H., Ishikawa, K., Maekawa, Y., Yamamoto, K., Ohta, J., Chihara, Y., Kida, I., and Ogihara, T. (2006). Anti-apoptotic and anti-senescence effects of Klotho on vascular endothelial cells. Biochem. Biophys. Res. Commun. 339, 827-832.
16. 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.
17. Imura, A., Tsuji, Y., Murata, M., Maeda, R., Kubota, K., Iwano, A., Obuse, C., Togashi, K., Tominaga, M., Kita, N., et al. (2007). a-Klotho as a regulator of calcium homeostasis. Science 316, 1615-1618.
18. Inagaki, T., Choi, M., Moschetta, A., Peng, L., Cummins, C.L., McDonald, J.G., Luo, G., Jones, S.A., Goodwin, B., Richardson, J.A., et al. (2005). Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab. 2, 217-225.
19. Inagaki, T., Dutchak, P., Zhao, G., Ding, X., Gautron, L., Parameswara, V., Li, Y., Goetz, R., Mohammadi, M., Esser, V., et al. (2007). Endocrine regulation of the fasting response by PPARa-mediated induction of fibroblast growth factor 21. Cell Metab. 5, 415-425.
20. Ito, S., Kinoshita, S., Shiraishi, N., Nakagawa, S., Sekine, S., Fujimori, T., and Nabeshima, Y. (2000). Molecular cloning and expression analyses of mouse beta-klotho, which encodes a novel Klotho family protein. Mech. Dev. 98, 115-119.
21. Ito, S., Fujimori, T., Furuya, A., Satoh, J., Nabeshima, Y., and Nabeshima, Y. (2005). Impaired negative feedback suppression of bile acid synthesis in mice lacking bKlotho. J. Clin. Invest. 115, 2202-2208.
22. Itoh, N. and Ornitz, D.M. (2004). Evolution of the Fgf and Fgfr gene families. Trends Genet. 20, 563-569.
23. Kamemori, M., Ohyama, Y., Kurabayashi, M., Takahashi, K., Nagai, R., and Furuya, N. (2002). Expression of Klotho protein in the inner ear. Hear. Res. 171, 103-110.
24. Kawaguchi, H., Manabe, N., Miyaura, C., Chikuda, H., Nakamura, K., and Kuro-o, M. (1999). Independent impairment of osteoblast and osteoclast differentiation in klotho mouse exhibiting low-turnover osteopenia. J. Clin. Invest. 104, 229-237.
25. Kenyon, C., Chang, J., Gensch, E., Rudner, A., and Tabtiang, R. (1993). A C. elegans mutant that lives twice as long as wild type. Nature 366, 461-464.
26. Kharitonenkov, A., Shiyanova, T.L., Koester, A., Ford, A.M., Micanovic, R., Galbreath, E.J., Sandusky, G.E., Hammond, L.J., Moyers, J.S., Owens, R.A., et al. (2005). FGF-21 as a novel metabolic regulator. J. Clin. Invest. 115, 1627-1635.
27. Kirstetter, P., Anderson, K., Porse, B.T., Jacobsen, S.E., and Nerlov, C. (2006). Activation of the canonical Wnt pathway leads to loss of hematopoietic stem cell repopulation and multi-lineage differentiation block. Nat. Immunol. 7, 1048-1056.
28. Kops, G.J., Dansen, T.B., Polderman, P.E., Saarloos, I., Wirtz, K.W., Coffer, P.J., Huang, T.T., Bos, J.L., Medema, R.H., and Burgering, B.M. (2002a). Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419, 316-321.
29. Kops, G.J., Medema, R.H., Glassford, J., Essers, M.A., Dijkers, P.F., Coffer, P.J., Lam, E.W., and Burgering, B.M. (2002b). Control of cell cycle exit and entry by protein kinase B-regulated forkhead transcription factors. Mol. Cell. Biol. 22, 2025-2036.
30. Kuro-o, M., Hanaoka, K., Hiroi, Y., Noguchi, T., Fujimori, Y., Takewaki, S., Hayasaka, M., Katoh, H., Miyagishi, A., Nagai, R., et al. (1995). Salt-sensitive hypertension in transgenic mice overexpressing Naq-proton exchanger. Circ. Res. 76, 148-153.
31. Kuro-o, M., Matsumura, Y., Aizawa, H., Kawaguchi, H., Suga, T., Utsugi, T., Ohyama, Y., Kurabayashi, M., Kaname, T., Kume, E., et al. (1997). Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390, 45-51.
32. Kurosu, H., Yamamoto, M., Clark, J.D., Pastor, J.V., Nandi, A., Gurnani, P., McGuinness, O.P., Chikuda, H., Yamaguchi, M., Kawaguchi, H., et al. (2005). Suppression of aging in mice by the hormone Klotho. Science 309, 1829-1833.
33. Kurosu, H., Ogawa, Y., Miyoshi, M., Yamamoto, M., Nandi, A., Rosenblatt, K.P., Baum, M.G., Schiavi, S., Hu, M.C., Moe, O.W., et al. (2006). Regulation of fibroblast growth factor-23 signaling by Klotho. J. Biol. Chem. 281, 6120-6123.
34. Kurosu, H., Choi, M., Ogawa, Y., Dickson, A.S., Goetz, R., Eliseenkova, A.V., Mohammadi, M., Rosenblatt, K.P., Kliewer, S.A., and Kuro-o, M. (2007). Tissue-specific expression of bKlotho and fibroblast growth factor (FGF) receptor isoforms determines metabolic activity of FGF19 and FGF21. J. Biol. Chem. 282, 26687-26695.
35. Li, G. and Iyengar, R. (2002). Calpain as an effector of the Gq signaling pathway for inhibition of Wnt/beta-catenin-regulated cell proliferation. Proc. Natl. Acad. Sci. USA 99, 13254-13259.
36. Lin, B.C., Wang, M., Blackmore, C., and Desnoyers, L.R. (2007). Liver specific activities of FGF19 require KLOTHOβ. J. Biol. Chem. 282, 27277-27284.
37. Liu, H., Fergusson, M.M., Castilho, R.M., Liu, J., Cao, L., Chen, J., Malide, D., Rovira, I.I., Schimel, D., Kuo, C.J., et al. (2007a). Augmented Wnt signaling in a mammalian model of accelerated aging. Science 317, 803-806.
38. Liu, S., Gupta, A., and Quarles, L.D. (2007b). Emerging role of fibroblast growth factor 23 in a bone-kidney axis regulating systemic phosphate homeostasis and extracellular matrix mineralization. Curr. Opin. Nephrol. Hypertens. 16, 329-335.
39. 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.
40. Masuda, H., Chikuda, H., Suga, T., Kawaguchi, H., and Kuro-o, M. (2005). Regulation of multiple ageing-like phenotypes by inducible klotho gene expression in klotho mutant mice. Mech. Ageing Dev. 126, 1274-1283.
41. Matsumura, Y., Aizawa, H., Shiraki-Iida, T., Nagai, R., Kuro-o, M., and 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.
42. Min, D., Panoskaltsis-Mortari, A., Kuro-o, M., Hollander, G.A., Blazar, B.R., and Weinberg, K.I. (2007). Sustained thymopoiesis and improvement in functional immunity induced by exogenous KGF administration in murine models of aging. Blood 109, 2529-2537.
43. Mohammadi, M., Olsen, S.K., and Ibrahimi, O.A. (2005). Structural basis for fibroblast growth factor receptor activation. Cytok. Growth Factor Rev. 16, 107-137.
44. Morishita, K., Shirai, A., Kubota, M., Katakura, Y., Nabeshima, Y., Takeshige, K., and Kamiya, T. (2001). The progression of aging in klotho mutant mice can be modified by dietary phosphorus and zinc. J. Nutr. 131, 3182-3188.
45. Morris, J.Z., Tissenbaum, H.A., and Ruvkun, G. (1996). A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382, 536-539.
46. Nagai, T., Yamada, K., Kim, H.C., Kim, Y.S., Noda, Y., Imura, A., Nabeshima, Y., and Nabeshima, T. (2003). Cognition impairment in the genetic model of aging klotho gene mutant mice: a role of oxidative stress. FASEB J. 17, 50-52.
47. Ogawa, Y., Kurosu, H., Yamamoto, M., Nandi, A., Rosenblatt, K.P., Goetz, R., Eliseenkova, A.V., Mohammadi, M., and Kuro-o, M. (2007). bKlotho is required for metabolic activity of fibroblast growth factor 21. Proc. Natl. Acad. Sci. USA 104, 7432-7437.
48. Ogg, S., Paradis, S., Gottlieb, S., Patterson, G.I., Lee, L., Tissenbaum, H.A., and Ruvkun, G. (1997). The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389, 994-999.
49. Razzaque, M.S., Sitara, D., Taguchi, T., St-Arnaud, R., and Lanske, B. (2006). Premature aging-like phenotype in fibroblast growth factor 23 null mice is a vitamin D-mediated process. FASEB J. 20, 720-722.
50. Saito, Y., Yamagishi, T., Nakamura, T., Ohyama, Y., Aizawa, H., Suga, T., Matsumura, Y., Masuda, H., Kurabayashi, M., Kuro-o, M., et al. (1998). Klotho protein protects against endothelial dysfunction. Biochem. Biophys. Res. Commun. 248, 324-329.
51. Saito, Y., Nakamura, T., Ohyama, Y., Suzuki, T., Iida, A., Shiraki-Iida, T., Kuro-o, M., Nabeshima, Y., Kurabayashi, M., and Nagai, R. (2000). In vivo klotho gene delivery protects against endothelial dysfunction in multiple risk factor syndrome. Biochem. Biophys. Res. Commun. 276, 767-772.
52. Scheller, M., Huelsken, J., Rosenbauer, F., Taketo, M.M., Birchmeier, W., Tenen, D.G., and Leutz, A. (2006). Hematopoietic stem cell and multilineage defects generated by constitutive β-catenin activation. Nat. Immunol. 7, 1037-1047.
53. Segawa, H., Yamanaka, S., Ohno, Y., Onitsuka, A., Shiozawa, K., Aranami, F., Furutani, J., Tomoe, Y., Ito, M., Kuwahata, M., et al. (2007). Correlation between hyperphosphatemia and type II Na-Pi cotransporter activity in klotho mice. Am. J. Physiol. Renal Physiol. 292, F769-779.
54. Shimada, T., Kakitani, M., Yamazaki, Y., Hasegawa, H., Takeuchi, Y., Fujita, T., Fukumoto, S., Tomizuka, K., and Yamashita, T. (2004a). Targeted ablation of Fgf23 demonstrates an essential physiological role of FGF23 in phosphate and vitamin D metabolism. J. Clin. Invest. 113, 561-568.
55. Shimada, T., Takeshita, Y., Murohara, T., Sasaki, K., Egami, K., Shintani, S., Katsuda, Y., Ikeda, H., Nabeshima, Y., and Imaizumi, T. (2004b). Angiogenesis and vasculogenesis are impaired in the precocious-aging klotho mouse. Circulation 110, 1148-1155.
56. Shiraki-Iida, T., Aizawa, H., Matsumura, Y., Sekine, S., Iida, A., Anazawa, H., Nagai, R., Kuro-o, M., and Nabeshima, Y. (1998). Structure of the mouse klotho gene and its two transcripts encoding membrane and secreted protein. FEBS Lett. 424, 6-10.
57. Stubbs, J.R., Liu, S., Tang, W., Zhou, J., Wang, Y., Yao, X., and Quarles, L.D. (2007). Role of hyperphosphatemia and 1,25-dihydroxyvitamin D in vascular calcification and mortality in fibroblastic growth factor 23 null mice. J. Am. Soc. Nephrol. 18, 2116-2124.
58. Suga, T., Kurabayashi, M., Sando, Y., Ohyama, Y., Maeno, T., Maeno, Y., Aizawa, H., Matsumura, Y., Kuwaki, T., Kuro-o, M., et al. (2000). Disruption of the klotho gene causes pulmonary emphysema in mice. Defect in maintenance of pulmonary integrity during postnatal life. Am. J. Respir. Cell Mol. Biol. 22, 26-33.
59. Sugiura, H., Yoshida, T., Tsuchiya, K., Mitobe, M., Nishimura, S., Shirota, S., Akiba, T., and Nihei, H. (2005). Klotho reduces apoptosis in experimental ischaemic acute renal failure. Nephrol. Dial. Transplant. 20, 2636-2645.
60. Taguchi, A., Wartschow, L.M., and White, M.F. (2007). Brain IRS2 signaling coordinates life span and nutrient homeostasis. Science 317, 369-372.
61. Tatar, M., Kopelman, A., Epstein, D., Tu, M.-P., Yin, C.-M., and Garofalo, R.S. (2001). A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292, 107-110.
62. Tatar, M., Bartke, A., and Antebi, A. (2003). The endocrine regulation of aging by insulin-like signals. Science 299, 1346-1351.
63. Tohyama, O., Imura, A., Iwano, A., Freund, J.N., Henrissat, B., Fujimori, T., and Nabeshima, Y. (2004). Klotho is a novel β-glucuronidase capable of hydrolyzing steroid β-glucuronides. J. Biol. Chem. 279, 9777-9784.
64. Toyama, R., Fujimori, T., Nabeshima, Y., Itoh, Y., Tsuji, Y., and Osamura, R.Y. (2006). Impaired regulation of gonadotropins leads to the atrophy of the female reproductive system in klotho-deficient mice. Endocrinology 147, 120-129.
65. Tsujikawa, H., Kurotaki, Y., Fujimori, T., Fukuda, K., and 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.
66. 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.
67. Utsugi, T., Ohno, T., Ohyama, Y., Uchiyama, T., Saito, Y., Matsumura, Y., Aizawa, H., Itoh, H., Kurabayashi, M., Kawazu, S., et al. (2000). Decreased insulin production and increased insulin sensitivity in the klotho mutant mouse, a novel animal model for human aging. Metabolism 49, 1118-1123.
68. White, K.E., Evans, W.E., O'Riordan, J.L.H., Speer, M.C., Econs, M.J., Lorenz-Deplereux, B., Grabowski, M., Meitinger, T., and Storm, T.M. (2000). Autosomal dominant hypophosphataemic rickets is associated with mutations in FGF23. Nat. Genet. 26, 345-348.
69. Wu, X., Ge, H., Gupte, J., Weiszmann, J., Shimamoto, G., Stevens, J., Hawkins, N., Lemon, B., Shen, W., Xu, J., et al. (2007). Co-receptor requirements for fibroblast growth factor-19 signaling. J. Biol. Chem. 282, 29069-29072.
70. Yamamoto, M., Clark, J.D., Pastor, J.V., Gurnani, P., Nandi, A., Kurosu, H., Miyoshi, M., Ogawa, Y., Castrillon, D.H., Rosenblatt, K.P., et al. (2005). Regulation of oxidative stress by the anti-aging hormone Klotho. J. Biol. Chem. 280, 38029-38034.
71. Yamashita, T., Nifuji, A., Furuya, K., Nabeshima, Y., and Noda, M. (1998). Elongation of the epiphyseal trabecular bone in transgenic mice carrying a klotho gene locus mutation that leads to a syndrome resembling aging. J. Endocrinol. 159, 1-8.
72. Yoshida, T., Fujimori, T., and Nabeshima, Y. (2002). Mediation of unusually high concentrations of 1,25-dihydroxyvitamin D in homozygous klotho mutant mice by increased expression of renal 1a-hydroxylase gene. Endocrinology 143, 683-689.
73. Yu, C., Wang, F., Kan, M., Jin, C., Jones, R.B., Weinstein, M., Deng, C.X., and McKeehan, W.L. (2000). Elevated cholesterol metabolism and bile acid synthesis in mice lacking membrane tyrosine kinase receptor FGFR4. J. Biol. Chem. 275, 15482-15489.
74. Zhang, X., Ibrahimi, O.A., Olsen, S.K., Umemori, H., Mohammadi, M., and Ornitz, D.M. (2006). Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J. Biol. Chem. 281, 15694-15700.