Altered distribution of bone matrix proteins and defective bone mineralization in klotho-deficient mice

Bone

Volumn 57, Issue 1, 2013, Pages 206-219

  Sasaki, Muneteru ^a   Hasegawa, Tomoka ^a   Yamada, Tamaki ^a   Hongo, Hiromi ^a   de Freitas, Paulo Henrique Luiz ^c   Suzuki, Reiko ^a   Yamamoto, Tomomaya ^a   Tabata, Chihiro ^a   Toyosawa, Satoru ^b   Yamamoto, Tsuneyuki ^a   Oda, Kimimitsu ^d   Li, Minqi ^e   Inoue, Nobuo ^a   Amizuka, Norio ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c FEDERAL UNIVERSITY OF SERGIPE   (Brazil)

^d NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^e SHANDONG UNIVERSITY   (China)

Author keywords

DMP 1; Klotho deficient mice; MGP; Osteocalcin; Osteocyte

Indexed keywords

CALCIUM BINDING PROTEIN; DENTIN MATRIX PROTEIN 1; KLOTHO PROTEIN; MATRIX GLA PROTEIN; OSTEOCALCIN; OSTEOPONTIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MATRIX; BONE MINERALIZATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOPLASM; EPIPHYSEAL CARTILAGE; EPIPHYSIS; KNEE CRUCIATE LIGAMENT; MALE; METAPHYSIS; MOUSE; NONHUMAN; OSTEOCYTE; PROTEIN LOCALIZATION; TIBIA; TRABECULAR BONE; WILD TYPE;

DMP-1; KLOTHO DEFICIENT MICE; MGP; OSTEOCALCIN; OSTEOCYTE;

ACID PHOSPHATASE; ALKALINE PHOSPHATASE; ANIMALS; EXTRACELLULAR MATRIX PROTEINS; GLUCURONIDASE; IMMUNOHISTOCHEMISTRY; ISOENZYMES; MALE; MICE; MICROSCOPY, IMMUNOELECTRON; OSTEOCALCIN; OSTEOCYTES; OSTEOPONTIN;

EID: 84883311907     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.08.008     Document Type: Article

References (50)

1. Nabeshima Y., Imura H. Alpha-klotho: a regulator that integrates calcium homeostasis. Am J Nephrol 2008, 28:455-464.
2. Ito S., Fujimori T., Furuya A., Satoh J., Nabeshima Y., Nabeshima Y. Impaired negative feedback suppression of bile acid synthesis in mice lacking βklotho. J Clin Invest 2005, 112:2202-2208.
3. Kurosu H., Ogawa Y., Miyoshi M., Yamamoto M., Nandi A., Rosenblatt K.P., et al. Regulation of fibroblast growth factor-23 signaling by klotho. J Biol Chem 2006, 281:6120-6123.
4. Nabeshima Y. Toward a better understanding of Klotho. Sci Aging Knowledge Environ 2006, 2006:pe11.
5. Urakawa I., Yamazaki Y., Shimada T., Iijima K., Hasegawa H., Okawa K., et al. Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 2006, 444:770-777.
6. Nakatani T., Sarraj B., Ohnishi M., Densmore M.J., Taguchi T., Goetz R., et al. In vivo genetic evidence for klotho-dependent, fibroblast growth factor 23 (Fgf23)-mediated regulation of systemic phosphate homeostasis. FASEB J 2009, 23:433-441.
7. Fukumoto S. The role of bone in phosphate metabolism. Mol Cell Endocrinol 2008, 310:63-70.
8. Razzaque M.S. The FGF23-Klotho axis: endocrine regulation of phosphate homeostasis. Nat Rev Endocrinol 2009, 5:611-619.
9. Kuro-o M. Overview of the FGF23-Klotho axis. Pediatr Nephrol 2010, 25:583-590.
10. Kuro-o M., Matsumura H., Aizawa H., Kawaguchi H., Suga T., Utsugi T., et al. Mutation of the mouse klotho gene leads to a syndrome resembling aging. Nature 1997, 390:45-51.
11. 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 1999, 104:229-237.
12. Yamashita T., Yoshitake H., Tsuji K., Kawaguchi N., Nabeshima Y., Noda M. Retardation in bone resorption after bone marrow ablation in klotho mutant mice. Endocrinology 2000, 141:438-445.
13. Yamashita T., Sekiya I., Kawaguchi N., Kashimada K., Nifuji A., Nabeshima Y., et al. Klotho-deficient mice are resistance to bone loss induced by unloading due to sciatic neurectomy. J Endocrinol 2001, 168:347-351.
14. Shimada T., Kakitani M., Yamazaki Y., Hasegawa H., Takeuchi Y., Fujita T., et al. Targeted ablation of Fgf23 demonstrates an essential physiological role of FGF23 in phosphate and vitamin D metabolism. J Clin Invest 2004, 113:561-568.
15. Sitara D., Razzaque M.S., Hesse M., Yoganathan S., Taguchi T., Erben R.G., et al. Homozygous ablation of fibroblast growth factor-23 results in hyperphosphatemia and impaired skeletogenesis, and reverses hypophosphatemia in Phex-deficient mice. Matrix Biol 2004, 23:421-432.
16. Yamashita T., Nifuji A., Furuya K., Nabeshima Y., Noda M. Elongation of the epiphyseal trabecular bone in transgenic mice carrying a klotho gene locus mutation that leads to a syndrome resembling aging. J Endocrinol 1998, 159:1-8.
17. Yamashita T., Nabeshima Y., Noda M. High-resolution micro-computed tomography analyses of the abnormal trabecular bone structures in klotho gene mutant mice. J Endocrinol 2000, 164:239-245.
18. Toyosawa S., Shintani S., Fujiwara T., Ooshima T., Sato A., Ijuhin N., et al. Dentin matrix protein 1 is predominantly expressed in chicken and rat osteocytes but not in osteoblasts. J Bone Miner Res 2001, 16:2017-2026.
19. Feng J.Q., Ward L.M., Liu S., Lu Y., Xie Y., Yuan B., et al. Loss of DMP1 causes rickets and osteomalacia and identifies a role for osteocytes in mineral metabolism. Nat Genet 2006, 38:1310-1315.
20. Hauschika P.V., Lian J.B., Gallop P.M. Direct identification of the calcium-binding amino acids, γ-carboxyglutamate, in mineralized tissue. Proc Natl Acad Sci U S A 1975, 72:3925-3929.
21. Price P.A., Otsuka A.S., Poser J.W., Kristaponis J., Raman N. Characterization of a γ-carboxyglutamic acid containing protein from bone. Proc Natl Acad Sci U S A 1976, 73:1447-1451.
22. Price P.A., Williamson M.K. Primary structure of bovine MGP, a new vitamin K-dependent bone protein. J Biol Chem 1985, 260:14971-14975.
23. Price P.A., Nishimoto S.K. Radioimmunoassay for the vitamin K-dependent protein of bone and its discovery in plasma. Proc Natl Acad Sci U S A 1980, 77:2234-2238.
24. Hauschka P.V., Carr S.A. Calcium-dependent alpha-helical structure in osteocalcin. Biochemistry 1982, 21:2538-2547.
25. Amizuka N., Ozawa H. Intracellular localization and translocation of 1 alpha, 25-dihydroxyvitamin D3 receptor in osteoblasts. Arch Histol Cytol 1992, 55:77-88.
26. Hunter G.K., Hauschka P.V., Poole A.R., Rosenberg L.C., Goldberg H.A. Nucleation and inhibition of hydroxyapatite formation by mineralized tissue proteins. Biochem J 1996, 317:59-64.
27. Luo G., Ducy P., McKee M.D., Pinero G.J., Loyer E., Behringer R.R., et al. Spontaneous calcification of arteries and cartilage in mice lacking MGP. Nature 1997, 386:78-81.
28. Murshed M., Schinke T., McKee M.D., Karsenty G. Extracellular matrix mineralization is regulated locally; different roles of two gla-containing proteins. J Cell Biol 2004, 165:625-630.
29. Kaipatur N.R., Murshed M., McKee M.D. MGP inhibition of tooth mineralization. J Dent Res 2008, 87:839-844.
30. Hirose S., Li M., Kojima T., de Freitas P.H., Ubaidus S., Oda K., et al. A histological assessment on the distribution of the osteocytic lacunar canalicular system using silver staining. J Bone Miner Metab 2007, 25:374-382.
31. Ubaidus S., Li M., Sultana S., de Freitas P.H., Oda K., Maeda T., et al. FGF23 is mainly synthesized by osteocytes in the regularly distributed osteocytic lacunar canalicular system established after physiological bone remodeling. J Electron Microsc (Tokyo) 2009, 58:381-392.
32. Burger E.H., Klein-Nulend J. Mechanotransduction in bone role of the lacuno-canalicular network. FASEB J 1999, 13:101-112.
33. Kamioka H., Honjo T., Takano-Yamamoto T. A three dimensional distribution of osteocyte processes revealed by the combination of confocal laser scanning microscopy and differential interference contrast microscopy. Bone 2001, 28:145-149.
34. Knothe Tate M.L., Adamson J.R., Tami A.E., Bauer T.W. The osteocyte. Int J Biochem Cell Biol 2004, 36:1-8.
35. Tatsumi S., Ishii K., Amizuka N., Li M., Kobayashi T., Kohno K., et al. Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab 2007, 5:464-475.
36. Oda K., Amaya Y., Fukushi-Irie M., Kinameri Y., Ohsuye K., Kubota I., et al. A general method for rapid purification of soluble versions of glycosylphosphatidylinositol-anchored proteins expressed in insect cells: an application for human tissue-nonspecific alkaline phosphatase. J Biochem 1999, 126:694-699.
37. Hoshi K., Amizuka N., Oda K., Ikehara Y., Ozawa H. Immunolocalization of tissue non-specific alkaline phosphatase in mice. Histochem Cell Biol 1997, 107(3):183-191.
38. Amizuka N., Li M., Kobayashi M., Hara K., Akahane S., Takeuchi K., et al. Vitamin K2, a gamma-carboxylating factor of gla-proteins, normalizes the bone crystal nucleation impaired by Mg-insufficiency. Histol Histopathol 2008, 23:1353-1366.
39. Amizuka N., Li M., Hara K., Kobayashi M., de Freitas P.H., Ubaidus S., et al. Warfarin administration disrupts the assembly of mineralized nodules in the osteoid. J Electron Microsc (Tokyo) 2009, 58:55-65.
40. Masuki H., Li M., Hasegawa T., Suzuki R., Ying G., Zhusheng L., et al. Immunolocalization of DMP1 and sclerostin in the epiphyseal trabeculae and diaphyseal cortical bone of osteoprotegerin deficient mice. Biomed Res 2010, 31:307-318.
41. Zhang K., Barragan-Adjemian C., Ye L., Kotha S., Dallas M., Lu Y., et al. E11/gp38 selective expression in osteocytes: regulation by mechanical strain and role in dendrite elongation. Mol Cell Biol 2006, 26:4539-4552.
42. Sakagami N., Amizuka N., Li M., Takeuchi K., Hoshino M., Nakamura N., et al. Reduced osteoblastic population and defective mineralization in osteopetrotic (op/op) mice. Micron 2005, 36:688-695.
43. Gu G., Nars M., Hentunen T.A., Metsikkö K., Väänänen H.K. Isolated primary osteocytes express functional gap junctions in vitro. Cell Tissue Res 2006, 323:263-271.
44. Suzuki H., Amizuka N., Oda K., Li M., Yoshie H., Ohshima H., et al. Histological evidence of the altered distribution of osteocytes and bone matrix synthesis in klotho-deficient mice. Arch Histol Cytol 2005, 68:371-381.
45. Rhee Y., Bivi N., Farrow E., Lezcano V., Plotkin L.I., White K.E., et al. Parathyroid hormone receptor signaling in osteocytes increases the expression of fibroblast growth factor-23 in vitro and in vivo. Bone 2011, 49:636-643.
46. Lu Y., Yuan B., Qin C., Cao Z., Xie Y., Dallas S.L., et al. The biological function of DMP-1 in osteocyte maturation is mediated by its 57-kDa C-terminal fragment. J Bone Miner Res 2011, 26:331-340.
47. Shimada T., Hasegawa H., Yamazaki Y., Muto T., Hino R., Takeuchi Y., et al. FGF-23 is a potent regulator of vitamin D metabolism and phosphate homeostasis. J Bone Miner Res 2004, 19:429-435.
48. Saito H., Maeda A., Ohtomo S., Hirata M., Kusano K., Kato S., et al. FGF-23 is a potent regulator of vitamin D metabolism and phosphate homeostasis. J Biol Chem 2005, 280:2543-2549.
49. Hesse M., Fröhlich L.F., Zeitz U., Lanske B., Erben R.G. Ablation of vitamin D signaling rescues bone, mineral, and glucose homeostasis in Fgf-23 deficient mice. Matrix Biol 2007, 26:75-84.
50. Rangiani A., Cao Z., Sun Y., Lu Y., Gao T., Yuan B., et al. Protective roles of DMP1 in high phosphate homeostasis. PLoS One 2012, 7:e42329.