Phosphate ions in bone: Identification of a calcium-organic phosphate complex by 31P solid-state NMR spectroscopy at early stages of mineralization

Calcified Tissue International

Volumn 72, Issue 5, 2003, Pages 610-626

  Wu, Y ^a   Ackerman, J L ^a,b   Strawich, E S ^a   Rey, C ^c   Kim, H M ^d   Glimcher, M J ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d Seoul National University   (South Korea)

Author keywords

31P NMR; Apatite; Bone; Calcification; Phosphoproteins

Indexed keywords

APATITE; CALCIUM; NANOPARTICLE; PHOSPHATE; PHOSPHOAMINO ACID; PHOSPHOPROTEIN; PHOSPHORUS 31;

ANIMAL TISSUE; BONE MINERALIZATION; CALCIFICATION; COMPLEX FORMATION; CONFERENCE PAPER; CRYSTAL; ELECTRON MICROSCOPY; MINERALIZATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL;

ANIMALS; CALCIFICATION, PHYSIOLOGIC; CALCIUM PHOSPHATES; CHICK EMBRYO; CHICKENS; CRYSTALLIZATION; FEMUR; MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHOPROTEINS; PHOSPHORUS ISOTOPES; TIBIA;

EID: 0042659482     PISSN: 0171967X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00223-002-1068-8     Document Type: Conference Paper

References (69)

1. Wu Y, Glimcher MJ, Rey C, Ackerman JL (1994) A unique protonated phosphate group in bone mineral not present in synthetic calcium phosphates. Identification by phosphorus-31 solid state NMR spectroscopy. J Mol Biol 244:423-435
2. Kuhn LT, Wu Y, Rey C, Gerstenfeld LC, Grynpas MD, Ackerman JL, Kim HM, Glimcher MJ (2000) Structure, composition, and maturation of newly deposited calcium-phosphate crystals in chicken osteoblast cell cultures. J Bone Miner Res 15:1301-1309
3. Glimcher MJ (1979) Phosphopeptides of enamel matrix. J Dent Res 58:790-809
4. Glimcher MJ (1976) Composition, structure and organization of bone and other mineralized tissues and the mechanism of calcification. In: Greep RO, Astwood EB (eds) Handbook of Physiology 7: Endocrinology, vol VII. American Physiological Society, Washington, pp 25-116
5. Glimcher MJ, Krane SM (1968) The organization and structure of bone, and the mechanism of calcification. In: Ramachandran GN, Gould BS (eds) Treatise on collagen, vol HB. Academic Press, New York, pp 68-251
6. 31P nuclear magnetic resonance spectroscopic evidence for ternary complex formation of fetal dentin phosphoprotein with calcium and inorganic orthophosphate ions. Calcif Tissue Int 35:815-818
7. Glimcher MJ (1984) Recent studies of the mineral phase in bone and its possible linkage to the organic matrix by protein-bound phosphate bonds. Philos Trans R Soc Lond B Biol Sci 304:479-508
8. Glimcher MJ (1989) Mechanism of calcification: role of collagen fibrils and collagen-phosphoprotein complexes in vitro and in vivo. Anat Rec 244:139-153
9. Veis A (1985) Phosphoroproteins of dentin and bone. Do they have a role in matrix mineralization? In: Butler WT (ed) The Chemistry and Biology of Mineralized Tissues. Ebsco Media, Birmingham, AL, pp 170-176
10. Veis A (1989) Studies of vertebrate tooth mineralization. Insights from studies of dentinogenesis imperfecta type II. Northwest Dent Res 1:3-5
11. Veis A, Anesey J, Mussell S (1967) The phosphoprotein of the dentin matrix. Biochemistry 6:2409-2416
12. Lee SL, Veis A (1980) Cooperativity in calcium ion binding to repetitive, carboxylate-serylphosphopolypeptides and the relationship of this property to dentin mineralization. Int J Pept Protein Res 16:231-240
13. George A, Sabsay B, Simonian PAL, Veis A (1993) Characterization of a novel dentin matrix acidic phosphoprotein. Implications for induction of biomineralization. J Biol Chem 268:12624-12630
14. Veis A (1993) Mineral-matrix interactions in bone and dentin. J Bone Miner Res 8(Suppl 2):S493-S497
15. Suga T, Okabe N (1996) Aqua (L-O-serine phosphato)calcium (II). Acta Crystallogr 52:1894-1896
16. Boskey AL, Posner AS (1982) Optimal conditions for Ca-acidic phospholipid-PO4 formation. Calcif Tisse Int 34:S1-7
17. Bradbury MWB, Kleeman CR, Bagdoyan H, Berberian A (1968) The calcium and magnesium content of skeletal muscle, brain, and cerebrospinal fluid as determined by atomic absorption flame photometry. J Lab Clin Med 71:884
18. Fernandez FJ, Kahn HL (1971) Clinical methods for atomic absorption spectroscopy. Clin Chem Newslett 3:24
19. Kirkpatrick D, Bishop S (1971) Simplified wet ash procedure for total phosphorus analysis of organophosphonates in biological samples. Anal Chem 43:1707-1709
20. Cohen-Solal L, Lian JB, Kossiva D, Glimcher MJ (1978) The identification of O-phosphothreonine in the soluble non-collagenous phosphoproteins of bone matrix. FEBS Lett 89:107-110
21. Cohen-Solal L, Lian JB, Kossiva D, Glimcher MJ (1979) Identification of organic phosphorus covalently bound to collagen and non-collagenous proteins of chicken-bone matrix. The presence of O-phosphoserine and O-phosphothreonine in non-collagenous proteins, and their absence from phosphorylated collagen. Biochem J 177:81-98
22. Gotoh Y, Salih E, Glimcher MJ, Gerstenfeld LC (1995) Characterization of the major non-collagenous proteins of chicken bone: identification of a novel 60 kDa non-collagenous phosphoprotein. Biochem Biophys Res Commun 208:863-870
23. Toyosawa S, Sato A, O'h Uigin C, Tichy H, Klein J (2000) Expression of the dentin matrix protein 1 gene in birds. J Mol Evol 50:31-38
24. Toyosawa S, Shintani S, Fujiwara T, Ooshima T, Sato A, Ijuhin N, Komori T (2001) Dentin matrix protein 1 is predominantly expressed in chicken and rat osteocytes but not in osteoblasts. J Bone Miner Res 16:2017-2026
25. Kim HM, Rey C, Glimcher MJ (1995) Isolation of calcium-phosphate crystals of bone by nonaqueous methods at low temperature. J Bone Miner Res 10:1589-1601
26. Rothwell WP, Waugh JS, Yesinowski JP (1980) High-resolution variable-temperature phosphorus-31 NMR of solid calcium phosphates. J Am Chem Soc 102:2637-2643
27. Herzfeld J, Roufosse A, Haberkorn RA, Griffin RG, Glimcher MJ (1980) Magic angle sample spinning in inhomogeneously broadened systems. Phil Trans R Soc Lond B Biol Sci 289:459-469
28. 31P NMR spectra of hydroxyapatite and diphosphonates. J Am Chem Soc 103:666-6267
29. Aue WP, Rôufosse AH, Glimcher MK, Griffin RG (1984) Solid state phosphorus-31 nuclear magnetic resonance studies of synthetic solid phases of calcium phosphate: potential models of bone mineral. Biochemistry 23:6110-6114
30. Rôufosse AH, Aue WP, Roberts JE, Glimcher MJ, Griffin RG (1984) Investigation of the mineral phases of bone by solid-state phosphorus-31 magic angle spinning nuclear magnetic resonance. Biochemistry 23:6115-6120
31. 31P and proton nuclear magnetic resonance study. J Bone Miner Res 6:1167-1176
32. Yesinowski JP (1998) Nuclear magnetic resonance spectroscopy of calcium phosphates. In: Amjad Z (ed) Calcium phosphates in biological and industrial systems. Kluwer, Amsterdam, pp 103-143
33. 31P cross-polarization in human trabecular bone. Solid State Nucl Magn Reson 10:191-195
34. Kaflak-Hachulska A, Slosarczyk A, Kolodziejski W (2000) Kinetics of NMR cross-polarization from protons to phosphorus-31 in natural brushite. Solid-State Nucl Magn Reson 15:237-238
35. Wu Y, Ackerman JL, Kim H-M, Rey C, Barroug A, Glimcher MJ (2002) Nuclear magnetic resonance spinspin relaxation of the crystals of bone, dental enamel and synthetic hydroxyapatites. J Bone Miner Res 17:472-480
36. Legrand AP, Bresson B, Guidoin R, Famery R (2002) Mineralization follow-up with the use of NMR spectroscopy and others. J Biomed Mater Res 63:390-395
37. Herzfeld J, Berger SE (1980) Sideband intensities in NMR spectra of sample spinning at the magic angle. J Chem Phys 73:6021-6030
38. Mason J (1993) Conventions for the reporting of nuclear magnetic shielding (or shift) tensors suggested by participants in the NATO ARW on NMR Shielding Constants at the University of Maryland, College Park, July 1992. Solid State Nucl Magn Reson 2:285-288
39. 31P magnetic resonance. J Biol Chem 248:7276-7278
40. Lian JB, Roufosse AH, Reit B, Glimcher MJ (1982) Concentrations of osteocalcin and phosphoprotein as a function of mineral content and age in cortical bone. Calcif Tissue Int 34:S82-S87
41. Glimcher MJ (1959) Molecular biology of mineralized tissues with particular reference to bone. Rev Mod Phys 31:359-393
42. Lee DD, Glimcher MJ (1991) The three-dimensional spatial relationship between the collagen fibrils and the inorganic calcium-phosphate crystals of pickerel (Americanus americanus) and herring (Clupea harengus) bone. J Mol Biol 217:487-501
43. Glimcher MJ (1968) A basic architectural principle in the organization of mineralized tissues. Clin Orthop 61:16-36
44. Glimcher MJ (1984) Recent studies of the mineral phase in bone and its possible linkage to the organic matrix by protein-bound phosphate bonds. Philos Trans R Soc Lond B Biol Sci 304:479-508
45. White SW, Hulmes DJS, Miller A, Timmins PA (1977) Collagen-mineral axial relationship in calcified turkey leg tendon by x-ray and neutron diffraction. Nature 266
46. Burger C, Liu L-Z, Hsiao BS, Chu B, Hanson J, Hori T, Glimcher MJ (2001) Synchrotron SAXS/WAXS study of the composite nature of bone. Am Chem Soc PMSE Preprint [abstr] 85:169-170
47. Berthet-Colominas C, Miller A, White SW (1979) Structural study of the calcifying collagen in turkey leg tendons. J Mol Biol 134:431-435
48. Katz EP, Wachtel E, Yamauchi M, Mechanic GL (1989) The structure of mineralized collagen fibrils. Connect Tissue Res 21:149-158
49. Katz EP, Li S-T (1973) Structure and function of bone collagen fibrils. J Mol Biol 80:1-15
50. Katz EP, Li S-T (1972) The molecular packing of collagen in mineralized and non-mineralized tissues. Biochem Biophys Res Commun 46:1-15
51. Landis WJ, Hodgens KJ, Arena J (1996) Structural relations between collagen and mineral in bone as determined by high voltage electron microscopic tomography. Microsc Res Tech 33:192-202
52. Landis WJ, Song MJ, Leith A, McEwen L, McEwen B (1992) Mineral and organic matrix interaction in normally calcifying tendon visualized in three dimensions by high-voltage electron microscopic tomography and graphic image reconstruction. J Struct Biol 110:39-54
53. Landis WJ, Song MJ (1991) Early mineral deposition in calcifying tendon characterized by high voltage electron microscopy and three-dimensional graphic imaging. J Struct Biol 107:116-127
54. Landis WJ, Moradian-Oldak J, Weiner S (1991) Topographic imaging of mineral and collagen in the calcifying turkey tendon. Connect Tissue Res 25:181-196
55. Glimcher MJ (1998) The nature of the mineral phase in bone: Biological and clinical implications. In: Avioli LV, Krane SM (eds) Metabolic bone disease and clinically related disorders, 3rd ed. Academic Press, San Diego, pp 23-50
56. Hohling H, Hall T, Boothroyd B, Cooke C, Duncumb P, Fitton-Jackson S (1967) Studies on the early stages of bone formation, using ordinary and electron microscopic electron probe x-ray microanalysis. Naturwissenschaften 54:142-143
57. Katz EP (1969) The kinetics of mineralization in vitro. Biochim Biophys Acta 194:121-129
58. Glimcher MJ, Hodge AJ, Schmitt FO (1957) Macromolecular aggregation states in relation to mineralization: the collagen hydroxyapatite system as studied in vitro. Proc Natl Acad Sci USA 43:860-867
59. Mergenhagen SE, Martin GR, Rizzo AA, Wright DN, Scott DB (1960) Calcification in vivo of implanted collagens. Biochim Biophys Acta 43:563-565
60. Hunter GK, Goldberg HA (1993) Nucleation of hydroxyapatite by bone sialoprotein. Proc Natl Acad Sci USA 90:8562-8565
61. Hunter GK, Goldberg HA (1994) Modulation of crystal formation by bone phosphoproteins: Role of glutamic acid-rich sequences in the nucleation of hydroxyapatite by bone sialoprotein. Biochem J 302:175-179
62. Hunter GK, Kyle CL, Goldberg HA (1994) Modulation of crystal formation by bone phosphoproteins; Structural specificity of the osteopontin-mediated inhibition of hydroxyapatite formation. Biochem J 300:723-728
63. Hunter GK, Hauschka PV, Poole AR, Rosenberg LC, Goldberg HA (1996) Nucleation and inhibition of hydroxyapatite formation by mineralized tissue proteins. Biochem J 317:59-64
64. Goldberg HA, Warner KJ, Stillman MJ, Hunter GK (1996) Determination of the hydroxyapatite-nucleating region of bone sialoprotein. Connect Tissue Res 35:385-392
65. Goldberg HA, Hunter GK (1995) The inhibitory activity of osteopontin on hydroxyapatite formation in vitro. Ann NY Acad Sci 760:305-308
66. Stanford CM, Jacobson PA, Eanes ED, Lembke LA, Midura RJ (1995) Rapidly forming apatitic mineral in an osteoblastic cell line (UMR 106-01 BSP). J Biol Chem 270:9420-9428
67. Wang A, Martin JA, Lemke LA, Midura RJ (2000) Reversible suppression of in vitro biomineralization by activation of protein kinase A. J Biol Chem 275:11082-11091
68. Kohler SJ, Klein MP (1977) Phosphorus-31 nuclear magnetic resonance chemical shielding tensors of L-O-serine phosphate and 3′-cytidine monophosphate. J Am Chem Soc 99:8290-8293
69. 31 P chemical shielding tensor in phospholipids. J Am Chem Soc 110:1054-1058