Modulation of bone resorption by phosphorylation state of bone sialoprotein

Biochemistry

Volumn 48, Issue 29, 2009, Pages 6876-6886

  Curtin, Paul ^a   McHugh, Kevin P ^d   Zhou, Hai Yan ^a   Fluckiger, Rudolf ^a   Goldhaber, Paul ^c   Oppenheim, Frank G ^b   Salih, Erdjan ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b BOSTON UNIVERSITY   (United States)

^c HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE REMODELING; BONE RESORPTION; BONE SIALOPROTEIN; CALVARIAL BONES; COVALENTLY BOUND; DIFFERENTIALLY EXPRESSED GENE; DOWN-REGULATION; IN-VIVO; INHIBITORY EFFECT; INTEGRIN RECEPTORS; MC3T3-E1; MINIMAL EFFECTS; ORGAN CULTURE; ORGAN CULTURE SYSTEM; OSTEOBLAST CELLS; PARATHYROID HORMONES; PARTIAL REDUCTION; TRANS-MEMBRANE PROTEINS; TRANSMEMBRANE; TYPE I COLLAGEN; TYROSINE PHOSPHORYLATION;

AMINES; AMINO ACIDS; BIOACTIVITY; CELL CULTURE; CELL MEMBRANES; GENE EXPRESSION; MACROPHAGES; PHOSPHORYLATION; SIGNALING;

BONE;

BONE SIALOPROTEIN; COLLAGEN TYPE 1; GLYCYLARGINYLGLYCYLASPARTYLSERINE; OSTEOCLAST DIFFERENTIATION FACTOR; PARATHYROID HORMONE; PHOSPHATE;

ANIMAL TISSUE; ARTICLE; CALVARIA; CELL STRAIN 3T3; CONCENTRATION RESPONSE; CONTROLLED STUDY; COVALENT BOND; DOWN REGULATION; GENE EXPRESSION; HORMONAL REGULATION; MACROPHAGE; MALE; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION;

3T3 CELLS; ANIMALS; ANIMALS, NEWBORN; BONE RESORPTION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; MICE; PHOSPHORYLATION; RANK LIGAND; SIALOGLYCOPROTEINS;

EID: 67651211839     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900066b     Document Type: Article

References (62)

1. Ingber, D. E. (1993) The riddle of morphogenesis: a question of solution chemistry or molecular cell engeneering. Cell 75, 1249-1252.
2. Mizuno, M., Imai, T., Fujisawa, R., Tani, H., and Kuboki, Y. (2000) Bone sialoprotein (BSP) is a crucial factor for the expression of osteoblastic phenotypes of bone marrow cells cultured on type I collagen matrix. Calcif. Tissue Int. 66, 388-396.
3. Decup, F., Six, N., Palmier, B., Buch, D., Lasfargues, J. J., Salih, E., and Goldberg, M. (2000) Bone sialoprotein-induced reparative dentinogenesis in the pulp of a rat's molar. Clin. Oral Investig. 4, 110-119.
4. Six, N., Decup, F., Lasfargues, J. J., Salih, E., and Goldberg, M. (2002) Osteogenic proteins, bone sialoprotein and bone morphogenetic protein 7 (OP-1), and pulp mineralization. J. Mater. Sci. (Mater. Med.) 13, 225-232.
5. Wang, J., Zhou, H.-Y., Salih, E., Xu, L., Wunderlich, L., Gu, X., Hofstaetter, J. G., Torres, M., and Glimcher, M. J. (2006) Site-specific in vivo calcification and osteogenesis stimulated by bone sialoprotein. Calcif. Tissue Int. 79, 179-189.
6. Gordon, J. A. R., Tye, C. E., Sampaio, A. V., Underhill, T. M., Hunter, G. K., and Goldberg, H. A. (2007) Bone sialoprotein expression enhances osteoblast differentiation and matrix mineralization in vitro. Bone 41, 462-473.
7. Hynes, R. O. (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.
8. Albelda, S. M., and Buck, C. A. (1990) Integrins and other cell adhesion molecules. FASEB J. 4, 2868-2880.
9. Blobel, C. P., and White, J. M. (1992) Structure, function and evolutionary relationship of proteins containing a disintegrin domain. Curr. Opin. Cell Biol. 4, 760-765.
10. Fisher, L. W., Whitson, S. W., Avioli, L. V., and Termine, J. D. (1983) Matrix sialoprotein of developing bone. J. Biol. Chem. 258, 12723-12727.
11. Franzen, A., and Heinegard, D. (1985) Isolation and charachterization of two sialoproteins present only in bone calcified matrix. Biochem. J. 232, 715-724.
12. Salih, E., Ashkar, S., Gerstenfeld, L. C., and Glimcher, M. J. (1996) Protein kinases of cultured chicken osteoblasts: Selectivity for extracellular matrix proteins of bone and their catalytic competence for osteopontin. J. Bone Miner. Res. 11, 1461-1473.
13. Salih, E., Zhou, H. Y., and Glimcher, M. J. (1996) Phosphorylation of purified bovine bone sialoprotein and osteopontin by protein kinases. J. Biol .Chem. 271, 16897-16905.
14. 32P-labeled osteopontin from cultured chicken osteoblasts. J. Biol. Chem. 272, 13966-13973.
15. Salih, E., Wang, J., Mah, J., and Fluckiger, R. (2002) Natural variation in the extent of phosphorylation of bone phosphoproteins as a function of in vivo new bone formation induced by demineralized bone matrix in soft tissue and bony environments. Biochem. J. 364, 465-474.
16. Salih, E., and Fluckiger, R. (2004) Complete topographical distribution of both the in vivo and in vitro phosphorylation sites of bone sialoprotein and their biological implications. J. Biol. Chem. 279, 19808-19815.
17. Glimcher, M. J., Kossiva, D., and Rouosse, A. (1979) Identification of phosphopeptides and γ-carboxyglutamic acid-containing peptides in epiphysealgroth plate cartilage. Calcif. Tissue Int. 27, 1871.
18. Boskey, A. L., Doty, S. B., Kudryashov, V., Mayer-Kuckuk, P., Roy, R., and Binderman, I. (2008) Modulation of extracellular matrix protein phosphorylation alters mineralization in differentiating chich limb-bud mesencymal cell micromass cultures. Bone 42, 1061-1071.
19. Gorski, J. P., Wang, A., Lovitch, D., Powell, K., and Midura, R. J. (2004) Extracellular bone acidic glycoprotein-75 condensed mesenchyme regions to be mineralized and localized with bone sialoprotein during intramembranous bone formation. J. Biol. Chem. 279, 25455-25461.
20. Veis, A., Spector, A. R., and Zamonscanyk, H. (1972) Isolation of an EDTA-soluble phosphoprotein from mineralizing bovine dentin. Biochim. Biophys. Acta 257, 404-413.
21. Veis, A. (1985) Phosphoproteins of dentin and bone: Do they have a role in matrix mineralization? The Chemistry and Biology of Mineralized Tissues (Butler, W. T., Ed.), 170-176, Ebsco Media, Inc., Birmingham, AL.
22. He, G., Ramachandran, A., Dahl, T., George, S., Schultz, D., Cookson, D., Veis, A., and George, A. (2005) Phosphorylation of phosphophoryn is crucial for its function as a mediator of biomineralization. J. Biol. Chem. 280, 33109-33114.
23. Jadlowiec, J. A., Zhang, X., Li, J., Campbell, P. G., and Sfeir, C. (2006) Extracellular matrix-mediated signaling by dentin phosphophoryn involves activation of the smad pathway independent of bone morphogenetic protein. J. Biol. Chem. 281, 5341-5348.
24. Giachelli, C. M., Bae, N., Almeida, M., Denhard, D. T., Alpers, C. E., and Schwartz, S. M. (1993) Osteopontin is elevated during neoitima formation in rat arteries and in novel component of human atherosclerotic plaque. J. Clin. Invest. 92, 1686-1696.
25. Okada, A., Nomura, S., Sacki, Y., Higashiba, Y., Hamamoto, S., Hirose, M., Itoh, Y., Yasui, T., Tozawa, K., and Kohri, K. (2008) Morphological conversion of calcium oxalate crystals into stones is regulated by osteopontin in mouse kidney. J. Bone Miner. Res. 23, 1629-1637.
26. Kido, J., Kasahara, C., Ohishi, K., Nishikawa, S., Ishida, H., Yamashita, K., Kitamura, S., Kohri, K., and Nakata, T. (1995) Identification of osteopontin in human dental calculus matrix. Arch. Oral Biol. 40, 967-972.
27. Bellahcene, A., and Castronovo, V. (1997) Expression of bone matrix proteins in human breast cancer: potential roles in microcalcification formation and in the genesis of bone metastases. Bull Cancer 84, 17-24.
28. Midura, K. J., McQuilan, D. J., Benhan, K. J., Fisher, L. W., and Hascall, V. C. (1990) A rat osteogenic cell line (UMR 106-01) synthesises a highly sulphated form of bone sialoprotein. J. Biol. Chem. 265, 2347-2351.
29. Wang, J., Glimcher, M. J., Mah, J., Zhou, H. Y., and Salih, E. (1998) Expression of bone microsomal casein kinase II, bone sialoprotein, and osteopontin during the repair of calvarial defects. Bone 22, 621-628.
30. Endo, A., and Glimcher, M. J. (1989) The effect of complexing phosphoproteins to decalcified collaged on in vitro calcification. Connect. Tissue Res. 21, 179-190.
31. Hunter, G. K., and Goldberg, H. A. (1993) Nucleation of hydroxyappatite by bone sialoprotein. Proc. Natl. Acad. Sci. U.S.A. 90, 8562-8565.
32. Boskey, A. L., Maresca, M., Ullrich, W., Doty, S. B., Butler, W. T., and Prince, C. W. (1993) Osteopontin-hydroxyapitite interactions in vitro: inhibition of hydrxyapatite formation and growth in a gelatin. Bone Miner. 22, 147-159.
33. Stubbs, J. T.III, Mintz, K. P., Eanes, E. D., Torchia, D. A., and Fisher, L. W. (1997) Characterization of native and recombinant bone sialoprotein: delineation of the mineral-binding and cell adhesion domains and structural analysis of the RGD domains. J. Bone Miner. Res. 12, 1210-1222.
34. Buttler, W. T., Ridall, A. L., McKee, M. D. (1996) Osteopontin, in Bilezikian, J. P., Raisz, L. G., Rodan, G. A., Eds. Principles of Bone Biology , pp 167-181, Academic Press, San Diego, CA.
35. Denhardt, D. T., and Noda, M. (1998) Osteopontin expression and function: role in bone remodeling. J. Cell Biochem. Suppl. 30-31, 92-102.
36. Chambers, T. J., Fuller, K., Darby, J. A., Pringle, J. A., and Horton, M. A. (1986) Monoclonal antibodies against osteoclasts inhibit bone resorption in vitro. Bone Miner. 1, 127-135.
37. Davies, J., Warwick, J., Totty, N., Philip, R., Helfrich, M., and Horton, M. A. (1989) The osteoclast functional antigen, implicated in the regulation of bone resorption, is biochemically related to the vitronectin receptor. J. Cell Biol. 109, 1817-1826.
38. Reinholt, F. P., Hultenby, K., Oldberg, A., and Heinegard, D. (1990) Osteopontin- a possible anchor of osteoclasts to bone. Proc. Natl. Acad. Sci. U. S. A. 87, 4473-4475.
39. 3 integrin potentiate bone resorption. J. Biol. Chem. 268, 9901-9907.
40. Senger, D. R., and Perruzzi, C. A. (1996) Cell migration promoted by a potent GRGDS-containing thrombin-cleavage fragment of osteopontin. Biochim. Biophys. Acta 1314, 13-24.
41. O'Regal, A. W., Chupp, G. L., Lowry, J. A., Goetschkes, M., Mulligan, N., and Berman, J. S. (1999) Osteopontin is associated with T cells in sarcoid granulomas and has T cell adhesive and cytokine-like properties in vitro. J. Immunol. 162, 1024-1031.
42. Fedarko, N. S., Fohr, B., Robey, P. G., Young, M. F., and Fisher, L. W. (2000) Factor H binding to bone sialoprotein and osteopontin enables molecular cloaking of tumor cells from complement-mediated attack. J. Biol. Chem. 275, 16666-16672.
43. Helfrich, M. H., Nesbitt, S. A., Dorey, E. L., and Horton, M. A. (1992) Rat osteoclasts adhere to a wide range of RGD (Arg-Gly-Asp) peptide containing proteins including the bone sialoproteins and fibronectin. J. Bone Miner. Res. 7, 335-343.
44. Horton, M. A., Nesbit, M. A., and Helfrich, M. H. (1995) Interaction of osteopontin with osteoclast integrins. Ann. N. Y. Acad. Sci. 760, 190-200.
45. Bayliss, K. J., Meininger, G. A., Scholtz, J. M., and Davis, G. E. (1998) Osteopontin is a ligand for the alpha4beta1 integrin. J. Cell Sci. 111, 1165-1174.
46. Yokosaki, Y., Matsura, N., Sasaki, T., Murakami, I., Schneider, H., Higashiyama, S., Saitoh, Y., Yamakido, M., Taooka, Y., and Sheppard, D. (1999) The integrin alpha(9)beta(1) binds to a novel recognition sequence (SVVYGLR) in the thrombin-cleaved amino-terminal fragment of osteopontin. J. Biol. Chem. 274, 36328-36334.
47. Harris, N. L., Rattray, K. R., Tye, C. E., Underhill, T. M., Somerman, M. J., D'Errico, J. A., Chambers, A. F., Hunter, G. K., and Goldberg, H. A. (2000) Functional analysis of bone sialoprotein: identification of hydroxyapatite-nucleating and cell-binding domains by recombinant peptide expression and site-directed mutagenesis. Bone 27, 795-802.
48. Zhou, H. Y., Takita, H., Fujisawa, R., Mizuno, M., and Kuboki, Y. (1995) Stimulation by bone sialoprotein of calcification in osteoblast-like MC3T3-E1. Calcif. Tissue Int. 56, 403-407.
49. Gericke, A., Qin, C., Spevak, L., Fujimoto, Y., Butler, W. T., Sorensen, E. S., and Boskey, A. L. (2005) Importance of phosphorylation for osteopontin regulation of mineralization. Calcif. Tissue Int. 77, 45-54.
50. Oldberg, A., Jirskog-Hed, B., Axelsson, S., and Heinegard, D. (1989) Regulation of bone sialoprotein mRNA by steroid hormones. J. Cell Biol. 109, 3183-3186.
51. Razzouk, S., Brunn, J. C., Qin, C., Tye, C. E., Goldberg, H. A., and Butler, W. T. (2002) Osteopontin posttranslational modification, possibly phosphorylation, are required for in vitro bone resorption but not osteoclast adhesion. Bone 30, 40-47.
52. Ek-Rylander, B., Flores, M., Wendel, M., Heinegard, D., and Andersson, G. (1994) Dephosphorylation of osteopontin and bone sialoprotein by osteoclast tartrate-resistant acid phosphatase: modulation of osteoclast adhesion in vitro. J. Biol. Chem. 269, 14853-14856.
53. Katayama, Y., House, C. M., Udagawa, N., Kazama, J. J., McFarland, R. J., Martin, T. J., and Findlay, D. M. (1998) Casein kinase 2 phosphorylation of recombinant rat osteopontin enhances adhesion of osteoclasts but not osteoblasts. J. Cell Physiol. 176, 179-187.
54. Andersson, G., Ek-Rylander, B., Hollberg, K., Ljusberg-Sjolander, J., Lang, P., Norgard, M., Wang, Y., and Zhang, S. J. (2003) TRACP as an osteopontin phosphatase. J. Bone Miner. Res. 18, 1912-1915.
55. McHugh, K. P., Kitazawa, S, Teitelbaum, S. L., and Ross, F. P. (2001) Cloning and characterization of the murine beta(3) integrin gene promoter: identification of an interleukin element and regulation by STAT-6. J. Cell Biochem. 81, 320-332.
56. +-stimulation of cell mediated bone resorption in tissue culture. Am. J. Physiol. (Endocrinol. Metab.) 16, E90-E98.
57. +-stimulated release of prostoglandin E2 and cyclic adenosine 3′,5′-monophosphoric acid and their relationship to bone resorption in neonatal mouse calvaria cultures. Bone Miner. 11, 295-304.
58. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with folin phenol reagent. J. Biol. Chem. 193, 265-275.
59. Cooper, L. F., Yliheikkila, P. K., Felton, D. A., and Whitson, S. W. (1998) Spatiotemporal assessment of fetal bovine osteoblast culture differentiation indicates a role for BSP in promoting differentiation. J. Bone Miner. Res. 13, 620-632.
60. Malaval, L., Wade-Gueye, N. M., Boudiffa, M, Fei, J., Zirngibl, R., Chen, F., Laroche, N., Roux, J.-P., Burt-Pichat, B., Duboeuf, F., Boivin, G., Jurdic, P., Lafage-Proust, M.-H., Amedee, J., Vico, L., Rossant, J., and Aubin, J. E. (2008) Bone sialoprotein plays a functional role in bone formation and osteoclastogenesis. J. Exp. Med. 205, 1145-1153.
61. Raynal, C., Delmas, P. D., and Chenu, C. (1996) Bone sialoprotein stimulates in vitro bone resorption. Endocrinology 137, 2347-2354.
62. Valverde, P., Tu, Q., and Chen, J. (2005) BSP and RANKL induce osteoclastogenesis and bone resorption synergistically. J. Bone Miner. Res. 20, 1669-1679.