Intracellular precipitation of hydroxyapatite mineral and implications for pathologic calcification

Journal of Structural Biology

Volumn 162, Issue 3, 2008, Pages 468-479

  Azari, Fereshteh ^a   Vali, Hojatollah ^a,b   Guerquin Kern, Jean Luc ^c,d   Wu, Ting Di ^c,d   Croisy, Alain ^c,d   Sears, S Kelly ^b   Tabrizian, Maryam ^a,b   McKee, Marc D ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c INSERM   (France)

^d INSTITUT CURIE   (France)

Author keywords

Autophagosomes; Biomineralization; Decorin; Ectopic calcification; Electron microscopy; Hydroxyapatite; Intracellular calcification; NanoSIMS; Pathologic calcification

Indexed keywords

DECORIN; GLYCEROL 2 PHOSPHATE; HYDROXYAPATITE; MINERAL;

ANIMAL CELL; ARTICLE; BIOMINERALIZATION; CALCIFICATION; CELL CULTURE; CONTROLLED STUDY; ELECTRON MICROSCOPY; HISTOCHEMISTRY; MASS SPECTROMETRY; NONHUMAN; PRECIPITATION; PRIORITY JOURNAL;

ANIMALS; AUTOPHAGY; BIOCHEMISTRY; BIOPHYSICS; CALCIUM; CELL MEMBRANE; DOGS; DURAPATITE; EXTRACELLULAR MATRIX PROTEINS; GLYCEROPHOSPHATES; LEUCINE; MICROSCOPY, ELECTRON; MICROSCOPY, ELECTRON, TRANSMISSION; NANOTECHNOLOGY; PROTEOGLYCANS;

VERTEBRATA;

EID: 44649174978     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2008.03.003     Document Type: Article

References (90)

1. Addadi L., and Weiner S. Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Proc. Natl. Acad. Sci. USA 82 (1985) 4110-4114
2. Addison W.N., Azari F., Sorensen E.S., Kaartinen M.T., and McKee M.D. Pyrophosphate inhibits mineralization of osteoblast cultures by binding to mineral, up-regulating osteopontin, and inhibiting alkaline phosphatase activity. J. Biol. Chem. 282 (2007) 15872-15883
3. Anderson H.C. Vesicles associated with calcification in the matrix of epiphyseal cartilage. J. Cell Biol. 41 (1969) 59-72
4. Anderson H.C. Mechanisms of pathologic calcification. Rheum. Dis. Clin. North Am. 14 (1988) 303-319
5. Anderson H.C. Biology of disease-mechanism of mineral formation in bone. In: Rubin E., and Damjanov I. (Eds). In Pathology Reviews (1990), The Human Press Inc., Clifton, NJ
6. Anderson H.C. Molecular biology of matrix vesicles. Clin. Orthop. Relat. Res. (1995) 266-280
7. Anderson H.C. Matrix vesicles and calcification. Curr. Rheumatol. Rep. 5 (2003) 222-226
8. Anderson H.C., Sipe J.B., Hessle L., Dhanyamraju R., Atti E., Camacho N.P., and Millan J.L. Impaired calcification around matrix vesicles of growth plate and bone in alkaline phosphatase-deficient mice. Am. J. Pathol. 164 (2004) 841-847
9. Ando Y., Ichihara N., Takeshita S., Saito Y., Kikuchi T., and Wakasugi N. Histological and ultrastructural features in the early stage of Purkinje cell degeneration in the cerebellar calcification (CC) rat. Exp. Anim. 53 (2004) 81-88
10. Bellows C.G., Aubin J.E., Heersche J.N., and Antosz M.E. Mineralized bone nodules formed in vitro from enzymatically released rat calvaria cell populations. Calcif. Tissue Int. 38 (1986) 143-154
11. Bonewald L.F., Harris S.E., Rosser J., Dallas M.R., Dallas S.L., Camacho N.P., Boyan B., and Boskey A. von Kossa staining alone is not sufficient to confirm that mineralization in vitro represents bone formation. Calcif. Tissue Int. 72 (2003) 537-547
12. Bonucci E. Fine structure and histochemistry of "calcifying globules" in epiphyseal cartilage. Z. Zellforsch. Mikrosk. Anat. 103 (1970) 192-217
13. Bordat C., Guerquin-Kern J.L., Lieberherr M., and Cournot G. Direct visualization of intracellular calcium in rat osteoblasts by energy-filtering transmission electron microscopy. Histochem. Cell Biol. 121 (2004) 31-38
14. Boskey A.L. Noncollagenous matrix proteins and their role in mineralization. Bone Miner. 6 (1989) 111-123
15. Boskey A.L., Spevak L., Doty S.B., and Rosenberg L. Effects of bone CS-proteoglycans, DS-decorin, and DS-biglycan on hydroxyapatite formation in a gelatin gel. Calcif. Tissue Int. 61 (1997) 298-305
16. Boskey A.L., Stiner D., Binderman I., and Doty S.B. Effects of proteoglycan modification on mineral formation in a differentiating chick limb-bud mesenchymal cell culture system. J. Cell. Biochem. 64 (1997) 632-643
17. Campo R.D., and Betz R.R. Loss of proteoglycans during decalcification of fresh metaphyses with disodium ethylenediaminetetraacetate (EDTA). Calcif. Tissue Int. 41 (1987) 52-55
18. Cash D.E., Bock C.B., Schughart K., Linney E., and Underhill T.M. Retinoic acid receptor alpha function in vertebrate limb skeletogenesis: a modulator of chondrogenesis. J. Cell Biol. 136 (1997) 445-457
19. Chau H., El-Maadawy S., McKee M.D., and Tenenhouse H.S. Renal calcification in mice homozygous for the disrupted type IIa Na/Pi cotransporter gene Npt2. J. Bone Miner. Res. 18 (2003) 644-657
20. Chen C.C., and Boskey A.L. Mechanisms of proteoglycan inhibition of hydroxyapatite growth. Calcif. Tissue Int. 37 (1985) 395-400
21. Corsi A., Xu T., Chen X.D., Boyde A., Liang J., Mankani M., Sommer B., Iozzo R.V., Eichstetter I., Robey P.G., Bianco P., and Young M.F. Phenotypic effects of biglycan deficiency are linked to collagen fibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers-Danlos-like changes in bone and other connective tissues. J. Bone Miner. Res. 17 (2002) 1180-1189
22. Donley G.E., and Fitzpatrick L.A. Noncollagenous matrix proteins controlling mineralization; possible role in pathologic calcification of vascular tissue. Trends Cardiovasc. Med. 8 (1998) 199-206
23. Drut R., Drut R.M., and Greco M.A. Massive myocardial calcification in the perinatal period. Pediatr. Dev. Pathol. 1 (1998) 366-374
24. Ecarot-Charrier B., Glorieux F.H., van der Rest M., and Pereira G. Osteoblasts isolated from mouse calvaria initiate matrix mineralization in culture. J. Cell Biol. 96 (1983) 639-643
25. Fischer J.W., Steitz S.A., Johnson P.Y., Burke A., Kolodgie F., Virmani R., Giachelli C., and Wight T.N. Decorin promotes aortic smooth muscle cell calcification and colocalizes to calcified regions in human atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 2391-2396
26. Gajjeraman S., Narayanan K., Hao J., Qin C., and George A. Matrix macromolecules in hard tissues control the nucleation and hierarchical assembly of hydroxyapatite. J. Biol. Chem. 282 (2007) 1193-1204
27. Garimella R., Bi X., Camacho N., Sipe J.B., and Anderson H.C. Primary culture of rat growth plate chondrocytes: an in vitro model of growth plate histotype, matrix vesicle biogenesis and mineralization. Bone 34 (2004) 961-970
28. Ghadially F.N. As you like it, Part 3: a critique and historical review of calcification as seen with the electron microscope. Ultrastruct. Pathol. 25 (2001) 243-267
29. Giachelli C.M. Ectopic calcification: gathering hard facts about soft tissue mineralization. Am. J. Pathol. 154 (1999) 671-675
30. Giachelli C.M. Vascular calcification: in vitro evidence for the role of inorganic phosphate. J. Am. Soc. Nephrol. 14 (2003) S300-S304
31. Giachelli C.M. Vascular calcification mechanisms. J. Am. Soc. Nephrol. 15 (2004) 2959-2964
32. Giachelli C.M. Inducers and inhibitors of biomineralization: lessons from pathological calcification. Orthod. Craniofac. Res. 8 (2005) 229-231
33. Guerquin-Kern J.L., Wu T.D., Quintana C., and Croisy A. Progress in analytical imaging of the cell by dynamic secondary ion mass spectrometry (SIMS microscopy). Biochim. Biophys. Acta 1724 (2005) 228-238
34. He G., Dahl T., Veis A., and George A. Nucleation of apatite crystals in vitro by self-assembled dentin matrix protein 1. Nat. Mater. 2 (2003) 552-558
35. Hollander A.P., Atkins R.M., Eastwood D.M., Dieppe P.A., and Elson C.J. Human cartilage is degraded by rheumatoid arthritis synovial fluid but not by recombinant cytokines in vitro. Clin. Exp. Immunol. 83 (1991) 52-57
36. Hoshi K., Ejiri S., and Ozawa H. Localizational alterations of calcium, phosphorus, and calcification-related organics such as proteoglycans and alkaline phosphatase during bone calcification. J. Bone Miner. Res. 16 (2001) 289-298
37. Hsu H.H., and Anderson H.C. Calcification of isolated matrix vesicles and reconstituted vesicles from fetal bovine cartilage. Proc. Natl. Acad. Sci. USA 75 (1978) 3805-3808
38. Hunter G.K., and Goldberg H.A. Nucleation of hydroxyapatite by bone sialoprotein. Proc. Natl. Acad. Sci. USA 90 (1993) 8562-8565
39. Iyemere V.P., Proudfoot D., Weissberg P.L., and Shanahan C.M. Vascular smooth muscle cell phenotypic plasticity and the regulation of vascular calcification. J. Intern. Med. 260 (2006) 192-210
40. Jahnen-Dechent W., Schafer C., Ketteler M., and McKee M.D. Mineral chaperones: a role for fetuin-A and osteopontin in the inhibition and regression of pathologic calcification. J. Mol. Med. (2008) 10.1007/s00109-007-0294-y
41. Kalantari F., Miao D., Emadali A., Tzimas G.N., Goltzman D., Vali H., Chevet E., and Auguste P. Cellular and molecular mechanisms of abnormal calcification following ischemia-reperfusion injury in human liver transplantation. Mod. Pathol. 20 (2007) 357-366
42. Kim H.M., Himeno T., Kokubo T., and Nakamura T. Process and kinetics of bonelike apatite formation on sintered hydroxyapatite in a simulated body fluid. Biomaterials 26 (2005) 4366-4373
43. Kimmel C.A., and Trammell C. A rapid procedure for routine double staining of cartilage and bone in fetal and adult animals. Stain Technol. 56 (1981) 271-273
44. Kirsch T., Nah H.D., Shapiro I.M., and Pacifici M. Regulated production of mineralization-competent matrix vesicles in hypertrophic chondrocytes. J. Cell Biol. 137 (1997) 1149-1160
45. Kolset S.O., and Gallagher J.T. Proteoglycans in haemopoietic cells. Biochim. Biophys. Acta 1032 (1990) 191-211
46. Kolset S.O., Prydz K., and Pejler G. Intracellular proteoglycans. Biochem. J. 379 (2004) 217-227
47. Lander A.D., and Selleck S.B. The elusive functions of proteoglycans: in vivo veritas. J. Cell Biol. 148 (2000) 227-232
48. Landis W.J., Hodgens K.J., Arena J., Song M.J., and McEwen B.F. Structural relations between collagen and mineral in bone as determined by high voltage electron microscopic tomography. Microsc. Res. Tech. 33 (1996) 192-202
49. Li X., and Giachelli C.M. Sodium-dependent phosphate cotransporters and vascular calcification. Curr. Opin. Nephrol. Hypertens. 16 (2007) 325-328
50. Lieske J.C., and Toback F.G. Renal cell-urinary crystal interactions. Curr. Opin. Nephrol. Hypertens. 9 (2000) 349-355
51. Luo G., Ducy P., McKee M.D., Pinero G.J., Loyer E., Behringer R.R., and Karsenty G. Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386 (1997) 78-81
52. Magne D., Julien M., Vinatier C., Merhi-Soussi F., Weiss P., and Guicheux J. Cartilage formation in growth plate and arteries: from physiology to pathology. Bioessays 27 (2005) 708-716
53. Martin R.I., and Brown P.W. Formation of hydroxyapatite in serum. J. Mater. Sci. Mater. Med. 5 (1994) 96-102
54. McKee M.D., Addison W.N., and Kaartinen M.T. Hierarchies of extracellular matrix and mineral organization in bone of the craniofacial complex and skeleton. Cells Tissues Organs 181 (2005) 176-188
55. Millane T., Wilson A.J., Patel M.K., Jennison S.H., Holt D.W., Murday A.J., and Camm A.J. Mitochondrial calcium deposition in association with cyclosporine therapy and myocardial magnesium depletion: a serial histologic study in heart transplant recipients. J. Heart Lung Transplant. 13 (1994) 473-480
56. Mody N., Tintut Y., Radcliff K., and Demer L.L. Vascular calcification and its relation to bone calcification: possible underlying mechanisms. J. Nucl. Cardiol. 10 (2003) 177-183
57. Mogyorosi A., and Ziyadeh F.N. Increased decorin mRNA in diabetic mouse kidney and in mesangial and tubular cells cultured in high glucose. Am. J. Physiol. Renal Physiol. 275 (1998) 827-832
58. Moriguchi M., Yamada M., and Yanagisawa T. Immunocytochemistry of keratan sulfate proteoglycan and dermatan sulfate proteoglycan in porcine tooth-germ dentin. Anat. Sci. Int. 79 (2004) 145-151
59. Murshed M., Harmey D., Millan J.L., McKee M.D., and Karsenty G. Unique coexpression in osteoblasts of broadly expressed genes accounts for the spatial restriction of ECM mineralization to bone. Genes Dev. 19 (2005) 1093-1104
60. Nakano Y., Addison W.N., and Kaartinen M.T. ATP-mediated mineralization of MC3T3-E1 osteoblast cultures. Bone 41 (2007) 549-561
61. Nancollas G.H., Tsortos A., and Zieba A. The nucleation and growth of calcium phosphate crystals at protein and phosphatidylserine liposome surfaces. Scanning Microsc. 10 (1996) 499-507 discussion 508
62. Pampena D.A., Robertson K.A., Litvinova O., Lajoie G., Goldberg H.A., and Hunter G.K. Inhibition of hydroxyapatite formation by osteopontin phosphopeptides. Biochem. J. 378 (2004) 1083-1087
63. Plate U., Tkotz T., Wiesmann H.P., Stratmann U., Joos U., and Hohling H.J. Early mineralization of matrix vesicles in the epiphyseal growth plate. J. Microsc. 183 (1996) 102-107
64. Proudfoot D., Skepper J.N., Hegyi L., Bennett M.R., Shanahan C.M., and Weissberg P.L. Apoptosis regulates human vascular calcification in vitro: evidence for initiation of vascular calcification by apoptotic bodies. Circ. Res. 87 (2000) 1055-1062
65. Rasband, W.S., 1997-2006. ImageJ, http://rsb.info.nih.gov/ij/, US National Institutes of Health, Bethesda, MD, USA.
66. Rees S.G., Hughes Wassell D.T., Waddington R.J., and Embery G. Interaction of bone proteoglycans and proteoglycan components with hydroxyapatite. Biochim. Biophys. Acta 1568 (2001) 118-128
67. Rees S.G., Wassell D.T., Shellis R.P., and Embery G. Effect of serum albumin on glycosaminoglycan inhibition of hydroxyapatite formation. Biomaterials 25 (2004) 971-977
68. Reynolds J.L., Joannides A.J., Skepper J.N., McNair R., Schurgers L.J., Proudfoot D., Jahnen-Dechent W., Weissberg P.L., and Shanahan C.M. 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. 15 (2004) 2857-2867
69. Rohde M., and 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. 80 (2007) 323-336
70. Roughley P.J., White R.J., and Mort J.S. Presence of pro-forms of decorin and biglycan in human articular cartilage. Biochem. J. 318 Pt 3 (1996) 779-784
71. Saito T., Arsenault A.L., Yamauchi M., Kuboki Y., and Crenshaw M.A. Mineral induction by immobilized phosphoproteins. Bone 21 (1997) 305-311
72. Schoen F.J., and Levy R.J. Calcification of tissue heart valve substitutes: progress toward understanding and prevention. Ann. Thorac. Surg. 79 (2005) 1072-1080
73. Shanahan C.M. Vascular calcification. Curr. Opin. Nephrol. Hypertens. 14 (2005) 361-367
74. Shanahan C.M., Cary N.R., Salisbury J.R., Proudfoot D., Weissberg P.L., and Edmonds M.E. Medial localization of mineralization-regulating proteins in association with Monckeberg's sclerosis: evidence for smooth muscle cell-mediated vascular calcification. Circulation 100 (1999) 2168-2176
75. Shioi A., Nishizawa Y., Jono S., Koyama H., Hosoi M., and Morii H. Beta-glycerophosphate accelerates calcification in cultured bovine vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 15 (1995) 2003-2009
76. Siegel G., Malmsten M., Pietzsch J., Schmidt A., Buddecke E., Michel F., Ploch M., and Schneider W. The effect of garlic on arteriosclerotic nanoplaque formation and size. Phytomedicine 11 (2004) 24-35
77. Stanford C.M., Jacobson P.A., Eanes E.D., Lembke L.A., and Midura R.J. Rapidly forming apatitic mineral in an osteoblastic cell line (UMR 106-01 BSP). J. Biol. Chem. 270 (1995) 9420-9428
78. Steitz S.A., Speer M.Y., Curinga G., Yang H.Y., Haynes P., Aebersold R., Schinke T., Karsenty G., and Giachelli C.M. Smooth muscle cell phenotypic transition associated with calcification: upregulation of Cbfa1 and downregulation of smooth muscle lineage markers. Circ. Res. 89 (2001) 1147-1154
79. Tartaix P.H., Doulaverakis M., George A., Fisher L.W., Butler W.T., Qin C., Salih E., Tan M., Fujimoto Y., Spevak L., and Boskey A.L. In vitro effects of dentin matrix protein-1 on hydroxyapatite formation provide insights into in vivo functions. J. Biol. Chem. 279 (2004) 18115-18120
80. Tweedie E.P., Coblentz F.E., and Shafer T.H. Purification of a soluble glycoprotein from the uncalcified ecdysial cuticle of the blue crab Callinectes sapidus and its possible role in initial mineralization. J. Exp. Biol. 207 (2004) 2589-2598
81. Tyson K.L., Reynolds J.L., McNair R., Zhang Q., Weissberg P.L., and Shanahan C.M. Osteo/chondrocytic transcription factors and their target genes exhibit distinct patterns of expression in human arterial calcification. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 489-494
82. Vali H., and Bachmann L. Ultrastructure and flow behavior of colloidal smectile dispersions. J. Colloid Interface Sci. 126 (1988) 273-291
83. Vali H., McKee M.D., Sears K., Plows F.L., Chevet E., Ghiabi P., Plavsic M., Kajander E.O., and Zare R.N. Nanoforms: a new type of protein-associated mineralization. Geochem Cosmochim Acta 65 (2001) 63-74
84. Veis A. Mineral-matrix interactions in bone and dentin. J. Bone Miner. Res. 8 Suppl 2 (1993) S493-S497
85. Wada T., McKee M.D., Steitz S., and Giachelli C.M. Calcification of vascular smooth muscle cell cultures: inhibition by osteopontin. Circ. Res. 84 (1999) 166-178
86. Waddington R.J., and Langley M.S. Structural analysis of proteoglycans synthesized by mineralizing bone cells in vitro in the presence of fluoride. Matrix Biol. 17 (1998) 255-268
87. Waddington R.J., Roberts H.C., Sugars R.V., and Schonherr E. Differential roles for small leucine-rich proteoglycans in bone formation. Eur. Cell Mater. 6 (2003) 12-21 discussion 21
88. Wahab N.A., Harper K., and Mason R.M. Expression of extracellular matrix molecules in human mesangial cells in response to prolonged hyperglycemia. Biochem. J. 316 (1996) 985-992
89. Wang D., Christensen K., Chawla K., Xiao G., Krebsbach P.H., and Franceschi R.T. Isolation and characterization of MC3T3-E1 preosteoblast subclones with distinct in vitro and in vivo differentiation/mineralization potential. J. Bone Miner. Res. 14 (1999) 893-903
90. Young M.F., Bi Y., Ameye L., Xu T., Wadhwa S., Heegaard A., Kilts T., and Chen X.D. Small leucine-rich proteoglycans in the aging skeleton. J. Musculoskelet. Neuronal Interact. 6 (2006) 364-365