Mechanism of cell-mediated mineralization

Current Opinion in Orthopaedics

Volumn 18, Issue 5, 2007, Pages 434-443

  Van De Lest, Chris H A ^a,b   Vaandrager, Arie B ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Bone development; Chondrocytes; Endochondral ossification; Lipid; Mineralization; Osteoblasts

Indexed keywords

ALKALINE PHOSPHATASE; BONE ACIDIC GLYCOPROTEIN 75; BONE MORPHOGENETIC PROTEIN 2; BONE SIALOPROTEIN; CALCIUM; CALCIUM PHOSPHATE; CASPASE INHIBITOR; COLLAGEN TYPE 10; COLLAGEN TYPE 2; COLLAGENASE 3; DENTIN MATRIX PROTEIN 1; DENTIN SIALOPHOSPHOPROTEIN; GELATINASE B; GLYCOPROTEIN; HYDROXYAPATITE; MATRIX EXTRACELLULAR PHOSPHORGLYCOPROTEIN; MATRIX GAMMA CARBOXYGLUTAMIC ACID RICH PROTEIN; MATRIX METALLOPROTEINASE; MATRIX PROTEIN; OSTEOCALCIN; OSTEOPONTIN; PHOSPHATE; PHOSPHODIESTERASE I; PYROPHOSPHATE; UNCLASSIFIED DRUG;

BONE CELL; BONE MASS; BONE MATRIX; BONE MINERALIZATION; CALCIFICATION; CALCIUM BLOOD LEVEL; CARTILAGE CELL; FRACTURE; HUMAN; ODONTOBLAST; OSTEOBLAST; PHOSPHATE BLOOD LEVEL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVIEW;

EID: 34547912844     PISSN: 10419918     EISSN: None     Source Type: Journal    
DOI: 10.1097/BCO.0b013e3282742022     Document Type: Review

References (84)

1. Giachelli CM. Inducers and inhibitors of biomineralization: lessons from pathological calcification. Orthod Craniofac Res 2005; 8:229-231.
2. Lian JB. Biology of bone mineralization. Curr Opin Endocrinol Diab 2006; 13:1-9.
3. Taylor D, Hazenberg J, Lee TC. The cellular transducer in bone: What is it? Technol Healthcare 2006; 14:367-377.
4. Martin TJ, Sims NA. Osteoclast-derived activity in the coupling of bone formation to resorption. Trends Mol Med 2005; 11:76-81.
5. Butler WT, Brunn JC, Qin C. Dentin extracellular matrix (ECM) proteins: comparison to bone ECM and contribution to dynamics of dentinogenesis. Connect Tissue Res 2003; 44 (Suppl 1):171-178.
6. Goldring MB, Tsuchimochi K, Ijiri K. The control of chondrogenesis. J Cell Biochem 2006; 97:33-44.
7. Behonick DJ, Werb Z. A bit of give and take: the relationship between the extracellular matrix and the developing chondrocyte. Mech Dev 2003; 120:1327-1336.
8. Stickens D, Behonick DJ, Ortega N, et al. Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development 2004; 131:5883-5895.
9. Liu Z, Lavine KJ, Hung IH, Ornitz DM. FGF18 is required for early chondrocyte proliferation, hypertrophy and vascular invasion of the growth plate. Dev Biol 2007; 302:80-91. Delayed mineralization in FGF18(-/-) mice was found to be associated with delayed initiation of chondrocyte hypertrophy, decreased proliferation at early stages of chondrogenesis, delayed skeletal vascularization and delayed osteoclast and osteoblast recruitment to the growth plate. Furthermore, FGF18 was shown to be necessary for vascular endothelial growth factor expression in hypertrophic chondrocytes and the perichondrium, indicating the role of FGF18 in skeletal vascularization and recruitment of osteoblasts and osteoclasts.
10. Shapiro IM, Adams CS, Freeman T, Srinivas V. Fate of the hypertrophic chondrocyte: microenvironmental perspectives on apoptosis and survival in the epiphyseal growth plate. Birth Defects Res C Embryo Today 2005; 75:330-339.
11. Bianco P, Cancedda FD, Riminucci M, Cancedda R. Bone formation via cartilage models: the 'borderline' chondrocyte. Matrix Biol 1998; 17:185-192.
12. Kirsch T. Determinants of pathological mineralization. Curr Opin Rheumatol 2006; 18:174-180.
13. Bobryshev YV. Transdifferentiation of smooth muscle cells into chondrocytes in atherosclerotic arteries in situ: implications for diffuse intimal calcification. J Pathol 2005; 205:641-650.
14. Tyson KL, Reynolds JL, McNair R, et al. Osteo/chondrocytic transcription factors and their target genes exhibit distinct patterns of expression in human arterial calcification. Arterioscler Thromb Vasc Biol 2003; 23:489-494.
15. Magne D, Julien M, Vinatier C, et al. Cartilage formation in growth plate and arteries: from physiology to pathology. Bioessays 2005; 27:708-716.
16. Giachelli CM. Vascular calcification: in vitro evidence for the role of inorganic phosphate. J Am Soc Nephrol 2003; 14:S300-S304.
17. Deneke T, Langner K, Grewe PH, et al. Ossification in atherosclerotic carotid arteries. Z Kardiol 2001; 90 (Suppl 3):106-115.
18. Zhang Y, Brown MA, Peach C, et al. Investigation of the role of ENPP1 and TNAP genes in chondrocalcinosis. Rheumatology 2007; 46:586-589.
19. Johnson K, Goding J, Van ED, et al. Linked deficiencies in extracellular PP(i) and osteopontin mediate pathologic calcification associated with defective PC-1 and ANK expression. J Bone Miner Res 2003; 18:994-1004.
20. Beck GR Jr. Inorganic phosphate as a signaling molecule in osteoblast differentiation. J Cell Biochem 2003; 90:234-243.
21. Lundquist P, Ritchie HH, Moore K, et al. Phosphate and calcium uptake by rat odontoblast-like MRPC-1 cells concomitant with mineralization. J Bone Miner Res 2002; 17:1801-1813.
22. Narisawa S, Frohlander N, Millan JL. Inactivation of two mouse alkaline phosphatase genes and establishment of a model of infantile hypophosphatasia. Dev Dyn 1997; 208:432-446.
23. Magne D, Bluteau G, Faucheux C, et al. Phosphate is a specific signal for ATDC5 chondrocyte maturation and apoptosis-associated mineralization: possible implication of apoptosis in the regulation of endochondral ossification. J Bone Miner Res 2003; 18:1430-1442.
24. Zhang W, Pantschenko AG, McCarthy MB, Gronowicz G. Bone-targeted overexpression of bcl-2 increases osteoblast adhesion and differentiation and inhibits mineralization in vitro. Calcif Tissue Int 2007; 80:111-122. Additional effects on bcl-2 on osteoblasts and mineralization. Overexpression of Bcl-2 promoted the differentiation of osteoblasts, i.e. increased message levels of TNAP, type I collagen, bone sialoprotein, and osteocalcin. Also the two transcription factors essential for osteoblast differentiation, Runx2 and osterix, had significantly higher expression levels.
25. Lundquist P, Murer H, Biber J. Type II Na+-Pi cotransporters in osteoblast mineral formation: regulation by inorganic phosphate. Cell Physiol Biochem 2007; 19:43-56. Studied the 'cotransporters' regulation by inorganic phosphate and during mineralization in vitro. The authors demonstrated that, besides the less phosphonoformic acid sensitive sodium/phosphate type III transporter, the phosphonoformic acid sensitive sodium/phosphate type II transporter was upregulated in osteoblasts by increasing inorganic phosphate.
26. Wang W, Xu J, Du B, Kirsch T. Role of the progressive ankylosis gene (ank) in cartilage mineralization. Mol Cell Biol 2005; 25:312-323.
27. Addison WN, Azari F, Sorensen ES, et al. Pyrophosphate inhibits mineralization of osteoblast cultures by binding to mineral, upregulating osteopontin and inhibiting alkaline phosphatase activity. J Biol Chem 2007. [Epub ahead of print] Mineralization is dose-dependently inhibited by PPi. This inhibition could be reversed by TNAP, but not if PPi was bound to mineral. PPi also led to osteopontin upregulation, which did not result from changes in inorganic phosphate. Exogenous osteopontin inhibited mineralization but dephosphorylation by TNAP reversed this effect. Enzyme kinetic studies indicate that PPi inhibits TNAP-mediated inorganic phosphate release from β-glycerophosphate in an uncompetitive way.
28. Hoshi K, Ozawa H. Matrix vesicle calcification in bones of adult rats. Calcif Tissue Int 2000; 66:430-434.
29. Reynolds JL, Joannides AJ, Skepper JN, et al. Human vascular smooth muscle cells undergo vesicle-mediated calcification in response to changes in extracellular calcium and phosphate concentrations: a potential mechanism for accelerated vascular calcification in ESRD. J Am Soc Nephrol 2004; 15:2857-2867.
30. Borg TK, Runyan R, Wuthier RE. A freeze-fracture study of avian epiphyseal cartilage differentiation. Anat Rec 1981; 199:449-457.
31. Anderson HC. Molecular biology of matrix vesicles. Clin Orthop Relat Res 1995; (314):266-280.
32. Anderson HC, Sipe JB, Hessle L, et al. Impaired calcification around matrix vesicles of growth plate and bone in alkaline phosphatase- deficient mice. Am J Pathol 2004; 164:841-847.
33. Montessuit C, Bonjour JP, Caverzasio J. Expression and regulation of Na-dependent P(i) transport in matrix vesicles produced by osteoblast-like cells. J Bone Miner Res 1995; 10:625-631.
34. Majeska RJ, Holwerda DL, Wuthier RE. Localization of phosphatidylserine in isolated chick epiphyseal cartilage matrix vesicles with trinitrobenzenesulfonate. Calcif Tissue Int 1979; 27:41-46.
35. Kirsch T, Harrison G, Golub EE, Nah HD. The roles of annexins and types II and X collagen in matrix vesicle-mediated mineralization of growth plate cartilage. J Biol Chem 2000; 275:35577-35583.
36. Brachvogel B, Dikschas J, Moch H, et al. Annexin A5 is not essential for skeletal development. Mol Cell Biol 2003; 23:2907-2913.
37. Xiao Z, Camalier CE, Nagashima K, et al. Analysis of the extracellular matrix vesicle proteome in mineralizing osteoblasts. J Cell Physiol 2007; 210:325-335.
38. Bobryshev YV, Killingsworth MC, Huynh TG, et al. Are calcifying matrix vesicles in atherosclerotic lesions of cellular origin? Basic Res Cardiol 2007; 102:133-143.
39. Xu S, Yu JJ. Beneath the minerals, a layer of round lipid particles was identified to mediate collagen calcification in compact bone formation. Biophys J 2006; 91:4221-4229.
40. Speer MY, Giachelli CM. Regulation of cardiovascular calcification. Cardiovasc Pathol 2004; 13:63-70.
41. Mansfield K, Teixeira CC, Adams CS, Shapiro IM. Phosphate ions mediate chondrocyte apoptosis through a plasma membrane transporter mechanism. Bone 2001; 28:1-8.
42. Mansfield K, Pucci B, Adams CS, Shapiro IM. Induction of apoptosis in skeletal tissues: phosphate-mediated chick chondrocyte apoptosis is calcium dependent. Calcif Tissue Int 2003; 73:161-172.
43. Sabbagh Y, Carpenter TO, Demay MB. Hypophosphatemia leads to rickets by impairing caspase-mediated apoptosis of hypertrophic chondrocytes. Proc Natl Acad Sci U S A 2005; 102:9637-9642.
44. Ketteler M, Brandenburg V, Jahnen-Dechent W, et al. Do not be misguided by guidelines: the calcium x phosphate product can be a Trojan horse. Nephrol Dial Transplant 2005; 20:673-677.
45. Takeda E, Yamamoto H, Nashiki K, et al. Inorganic phosphate homeostasis and the role of dietary phosphorus. J Cell Mol Med 2004; 8:191-200.
46. Lomashvili KA, Cobbs S, Hennigar RA, et al. Phosphate-induced vascular calcification: role of pyrophosphate and osteopontin. J Am Soc Nephrol 2004; 15:1392-1401.
47. Bratton DL, Fadok VA, Richter DA, et al. Appearance of phosphatidylserine on apoptotic cells requires calcium-mediated nonspecific flip-flop and is enhanced by loss of the aminophospholipid translocase. J Biol Chem 1997; 272:26159-26165.
48. Boskey AL, Dick BL. The effect of phosphatidylserine on in vitro hydroxyapatite growth and proliferation. Calcif Tissue Int 1991; 49:193-196.
49. Kirsch T, Wang W, Pfander D. Functional differences between growth plate apoptotic bodies and matrix vesicles. J Bone Miner Res 2003; 18:1872-1881.
50. Rohde M, Mayer H. Exocytotic process as a novel model for mineralization by osteoblasts in vitro and in vivo determined by electron microscopic analysis. Calcif Tissue Int 2007. [Epub ahead of print] A novel model for mineralization by osteoblasts is described, in which amorphous calcium/phosphate material is directly secreted via an exocytotic process from vacuoles of the osteoblast, deposited extracellularly, propagated into the collagen fibril matrix, and matured to hydroxyapatite. This process was shown to be present in vitro as well as in vivo.
51. Stanford CM, Jacobson PA, Eanes ED, et al. Rapidly forming apatitic mineral in an osteoblastic cell line (UMR 106-01 BSP). J Biol Chem 1995; 270:9420-9428.
52. Midura RJ, Wang A, Lovitch D, et al. Bone acidic glycoprotein-75 delineates the extracellular sites of future bone sialoprotein accumulation and apatite nucleation in osteoblastic cultures. J Biol Chem 2004; 279:25464-25473.
53. Gorski JP, Wang A, Lovitch D, et al. Extracellular bone acidic glycoprotein-75 defines condensed mesenchyme regions to be mineralized and localizes with bone sialoprotein during intramembranous bone formation. J Biol Chem 2004; 279:25455-25463.
54. He G, Gajjeraman S, Schultz D, et al. Spatially and temporally controlled biomineralization is facilitated by interaction between self-assembled dentin matrix protein 1 and calcium phosphate nuclei in solution. Biochemistry 2005; 44:16140-16148.
55. Hunter GK, Poitras MS, Underhill TM, et al. Induction of collagen mineralization by a bone sialoprotein-decorin chimeric protein. J Biomed Mater Res 2001; 55:496-502.
56. Tye CE, Hunter GK, Goldberg HA. Identification of the type I collagen-binding domain of bone sialoprotein and characterization of the mechanism of interaction. J Biol Chem 2005; 280:13487-13492.
57. Tye CE, Rattray KR, Warner KJ, et al. Delineation of the hydroxyapatitenucleating domains of bone sialoprotein. J Biol Chem 2003; 278:7949-7955.
58. Wang A, Martin JA, Lembke LA, Midura RJ. Reversible suppression of in vitro biomineralization by activation of protein kinase A. J Biol Chem 2000; 275:11082-11091.
59. Gorski JP, Kremer EA, Chen Y, et al. Bone acidic glycoprotein-75 selfassociates to form macromolecular complexes in vitro and in vivo with the potential to sequester phosphate ions. J Cell Biochem 1997; 64:547-564.
60. Gowen LC, Petersen DN, Mansolf AL, et al. Targeted disruption of the osteoblast/osteocyte factor 45 gene (OF45) results in increased bone formation and bone mass. J Biol Chem 2003; 278:1998-2007.
61. Liu S, Rowe PS, Vierthaler L, et al. Phosphorylated acidic serine-aspartate-rich MEPE-associated motif peptide from matrix extracellular phosphoglycoprotein inhibits phosphate regulating gene with homologies to endopeptidases on the X-chromosome enzyme activity. J Endocrinol 2007; 192:261-267. This study indicates that MEPE inhibits mineralization and PHEX activity and leads to increased FGF23 production. The resulting coordination of mineralization and release of a phosphaturic factor by MEPE may serve a physiological role in regulating systemic phosphate homeostasis to meet the needs for bone mineralization.
62. Qin C, Baba O, Butler WT. Posttranslational modifications of sibling proteins and their roles in osteogenesis and dentinogenesis. Crit Rev Oral Biol Med 2004; 15:126-136.
63. Yang W, Lu Y, Kalajzic I, et al. Dentin matrix protein 1 gene cis-regulation: use in osteocytes to characterize local responses to mechanical loading in vitro and in vivo. J Biol Chem 2005; 280:20680-20690.
64. Ling Y, Rios HF, Myers ER, et al. DMP1 depletion decreases bone mineralization in vivo: an FTIR imaging analysis. J Bone Miner Res 2005; 20:2169-2177.
65. Ye L, MacDougall M, Zhang S, et al. Deletion of dentin matrix protein-1 leads to a partial failure of maturation of predentin into dentin, hypomineralization, and expanded cavities of pulp and root canal during postnatal tooth development. J Biol Chem 2004; 279:19141-19148.
66. Tartaix PH, Doulaverakis M, George A, et al. In vitro effects of dentin matrix protein-1 on hydroxyapatite formation provide insights into in vivo functions. J Biol Chem 2004; 279:18115-18120.
67. Sreenath T, Thyagarajan T, Hall B, et al. Dentin sialophosphoprotein knockout mouse teeth display widened predentin zone and develop defective dentin mineralization similar to human dentinogenesis imperfecta type III. J Biol Chem 2003; 278:24874-24880.
68. Alford AI, Hankenson KD. Matricellular proteins: extracellular modulators of bone development, remodeling, and regeneration. Bone 2006; 38:749-757.
69. Gericke A, Qin C, Spevak L, et al. Importance of phosphorylation for osteopontin regulation of biomineralization. Calcif Tissue Int 2005; 77:45-54.
70. Shapses SA, Cifuentes M, Spevak L, et al. Osteopontin facilitates bone resorption, decreasing bone mineral crystallinity and content during calcium deficiency. Calcif Tissue Int 2003; 73:86-92.
71. Ducy P, Desbois C, Boyce B, et al. Increased bone formation in osteocalcindeficient mice. Nature 1996; 382:448-452.
72. Rammelt S, Neumann M, Hanisch U, et al. Osteocalcin enhances bone remodeling around hydroxyapatite/collagen composites. J Biomed Mater Res A 2005; 73:284-294.
73. Glowacki J, Rey C, Glimcher MJ, et al. A role for osteocalcin in osteoclast differentiation. J Cell Biochem 1991; 45:292-302.
74. Doi Y, Horiguchi T, Kim SH, et al. Effects of noncollagenous proteins on the formation of apatite in calcium beta-glycerophosphate solutions. Arch Oral Biol 1992; 37:15-21.
75. Ketteler M, Vermeer C, Wanner C, et al. Novel insights into uremic vascular calcification: role of matrix Gla protein and alpha-2-Heremans Schmid glycoprotein/ fetuin. Blood Purif 2002; 20:473-476.
76. Merx MW, Schafer C, Westenfeld R, et al. Myocardial stiffness, cardiac remodeling, and diastolic dysfunction in calcification-prone fetuin-A-deficient mice. J Am Soc Nephrol 2005; 16:3357-3364.
77. Ketteler M. Fetuin-A and extraosseous calcification in uremia. Curr Opin Nephrol Hypertens 2005; 14:337-342.
78. Schinke T, Amendt C, Trindl A, et al. The serum protein alpha2-HSglycoprotein/ fetuin inhibits apatite formation in vitro and in mineralizing calvaria cells. A possible role in mineralization and calcium homeostasis. J Biol Chem 1996; 271:20789-20796.
79. Price PA, Lim JE. The inhibition of calcium phosphate precipitation by fetuin is accompanied by the formation of a fetuin-mineral complex. J Biol Chem 2003; 278:22144-22152.
80. Suttamanatwong S, Franceschi RT, Carlson AE, Gopalakrishnan R. Regulation of matrix Gla protein by parathyroid hormone in MC3T3-E1 osteoblast-like cells involves protein kinase A and extracellular signal-regulated kinase pathways. J Cell Biochem 2007. [Epub ahead of print]
81. Luo G, Ducy P, McKee MD, et al. Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 1997; 386:78-81.
82. Reynolds JL, Skepper JN, McNair R, et al. Multifunctional roles for serum protein fetuin-a in inhibition of human vascular smooth muscle cell calcification. J Am Soc Nephrol 2005; 16:2920-2930.
83. Chen NX, O'Neill KD, Chen X, et al. Fetuin-A uptake in bovine vascular smooth muscle cells is calcium dependent and mediated by annexins. Am J Physiol Renal Physiol 2007; 292:F599-F606. This study demonstrates a calcium and annexin-dependent uptake of fetuin by vascular smooth muscle cells that leads to a sustained rise in intracellular calcium. This regulated uptake may be a mechanism by which fetuin-A inhibits VSMC calcification in the presence of excess calcium.
84. 2+ moiety of the vasodilating NO-donor sodium nitroprusside effectively inhibits mineralization, implying that sodium nitroprusside is not only a vasodilating drug, but may also prevent vascular calcification.