Morphological and immunocytochemical characterization of primary osteogenic cell cultures derived from fetal rat cranial tissue

Anatomical Record

Volumn 252, Issue 4, 1998, Pages 554-567

  Irie, K ^a,b   Zalzal, S ^a   Ozawa, H ^b   McKee, M D ^a   Nanci, A ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b NIIGATA UNIVERSITY   (Japan)

Author keywords

Bone sialoprotein; Cell differentiation; Mineralization; Osteoblast; Osteocalcin; Osteopontin

Indexed keywords

OSTEOPONTIN; SIALOPROTEIN;

ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; CELL CULTURE; CELL DIFFERENTIATION; FETUS; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; CALCIUM; CELL SEPARATION; CELLS, CULTURED; ELECTRON PROBE MICROANALYSIS; FETUS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; OSTEOBLASTS; OSTEOCALCIN; OSTEOPONTIN; PHOSPHORUS; RATS; RATS, WISTAR; SIALOGLYCOPROTEINS; SKULL;

ANIMALIA;

EID: 0031754667     PISSN: 0003276X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0185(199812)252:4<554::AID-AR6>3.0.CO;2-2     Document Type: Article

References (97)

1. Aronow MA, Gerstenfeld LC, Owen TA, Tassinari MS, Stein GS, Lian JB. Factors that promote progressive development of the osteoblast phenotype in cultured fetal rat calvaria cells. J. Cell. Physiol. 1990;143:213-221.
2. Asahina I, Sampath TK, Nishimura I, Hauschka PV. Human osteogenic protein-1 induces both chondroblastic and osteoblastic differentiation of osteoprogenitor cells derived from newborn rat calvaria. J. Cell. Biol. 1993;123:921-933.
3. Aubin JE, Turksen K, Heersche JNM. Osteoblastic cell lineage. In: Noda M, ed. Cellular and Molecular Biology of Bone. San Diego, CA: Academic Press, 1993: 1-45.
4. Aubin JE, Liu F. The osteoblast lineage. In: Bilezikian JP, Raisz LG, Rodan GA, eds. Principles of Bone Biology. San Diego, CA: Academic Press, 1996: 51-67.
5. Bellows CG, Aubin JE, Heersche JNM, Antosz ME. Mineralized bone nodules formed in vitro from enzymatically released rat calvaria cell populations. Calcif. Tissue Int. 1986;38:143-154.
6. Bellows CG, Aubin JE. Determination of numbers of osteoprogenitors present in isolated fetal rat calvaria cells in vitro. Dev. Biol. 1989;133:8-13.
7. Bellows CG, Heersche JNM, Aubin JE. Effects of dexamethasone on expression and maintenance of cartilage in serum-containing cultures of calvaria cells. Cell. Tissue Res. 1989;256:145-151.
8. Bellows CG, Heersche JNM, Aubin JE. Determination of the capacity for proliferation and differentiation of osteoprogenitor cells in the presence and absence of dexamethasone. Dev. Biol. 1990;140:132-138.
9. Bendayan M. Colloidal gold post-embedding immunocytochemistry. Progr. Histochem. Cytochem. 1995;29:1-159.
10. Benhamou N. Preparation and application of lectin-gold complexes. In: Hayat MA, ed. Colloidal Gold: Principles, Methods, and Applications, Vol. 1. San Diego, CA: Academic Press, 1989: 95-143.
11. Bhargava U, Bar-Lev M, Bellows CG, Aubin JE. Ultrastructural analysis of bone nodules formed in vitro by isolated fetal rat calvaria cells. Bone 1988;9:155-163.
12. Bianco P, Hayashi Y, Silvestrini G, Termine JD, Bonucci E. Osteonectin and GLA-protein in calf bone: ultrastructural immunohistochemical localization using the protein A-gold method. Calcif. Tissue Int. 1985;37:684-686.
13. Bianco P, Riminucci M, Bonucci E, Termine JD, Gehron Robey P. Bone sialoprotein (BSP) secretion and osteoblast differentiation: relationship to bromodeoxyuridine incorporation, alkaline phosphatase, and matrix deposition. J. Histochem. Cytochem. 1993a;41:183-191.
14. Bianco P, Riminucci M, Silvestrini G, Bonucci E, Termine JD, Fisher LW, Gehron Robey P. Localization of bone sialoprotein (BSP) to Golgi and post-Golgi secretory structures in osteoblasts and to discrete sites in early bone matrix. J. Histochem. Cytochem. 1993b;41:193-203.
15. Binderman I, Duksin D, Harell A, Katzir E, Sachs L. Formation of bone tissue in culture from isolated bone cells. J. Cell. Biol. 1974;61:427-439.
16. Boskey AL, Maresca M, Ullrich W, Doty SB, Butler WT, Prince CW. Osteopontin-hydroxyapatite interactions in vitro: inhibition of hydroxyapatite formation and growth in a gelatin-gel. Bone Miner. 1993;22:147-159.
17. Bosshardt DD, Nanci A. Immunodetection of enamel- and cementum-related (bone) proteins at the enamel-free area and cervical portion of the tooth in rat molars. J. Bone Miner. Res. 1997;12:367-379.
18. Bosshardt DD, Zalzal S, McKee MD, Nanci A. Developmental appearance and distribution of bone sialoprotein and osteopontin in human and rat cementum. Anat. Rec. 1998;250:13-33.
19. Bradbeer JN, Virdi AS, Serre CM, Beresford JN, Delmas PD, Reeve J, Triffitt JT. A number of osteocalcin antisera recognize epitopes on proteins other than osteocalcin in cultured skin fibroblasts: implications for the identification of cells of the osteoblastic lineage in vitro. J. Bone Miner. Res. 1994;9:1221-1228.
20. Butler WT. The nature and significance of osteopontin. Connect. Tissue Res. 1989;23:123-136.
21. Butler WT, Ridall AL, McKee MD (1996) Osteopontin. In: Bilezikian JP, Raisz LG, Rodan GA, eds. Principles of Bone Biology. San Diego, CA: Academic Press, 1996: 167-181.
22. Camarda AJ, Butler WT, Finkelman RD, Nanci A. Immunocytochemical localization of γ-carboxyglutamic acid-containing proteins (osteocalcin) in rat bone and dentin. Calcif. Tissue Int. 1987;40:349-355.
23. Chen J, McKee MD, Nanci A, Sodek J. Bone sialoprotein mRNA expression and ultrastructural localization in fetal porcine calvarial bone: comparisons with osteopontin. Histochem. J. 1994;26:67-78.
24. Davies JE, Chernecky R, Lowenberg B, Shiga A. Deposition and resorption of calcified matrix in vitro by rat marrow cells. Cells Materials 1991;1:3-15.
25. Davies JE. In vitro modeling of the bone/implant interface. Anat. Rec. 1996;245:426-445.
26. Denhardt DT, Guo X. Osteopontin: a protein with diverse functions. FASEB J. 1993;7:1475-1482.
27. Ejiri S. The preosteoclast and its cytodifferentiation into the osteoclast: ultrastructural and histochemical studies of rat fetal parietal bone. Arch. Histol. Jpn. 1983;46:533-557.
28. Finkelman RD, Butler WT. Appearance of dentin γ-carboxyglutamic acid-containing proteins in developing rat molars in vitro. J. Dent. Res. 1985;64:1008-1015.
29. Fisher LW, Whitson SW, Avioli LV, Termine JD. Matrix sialoprotein of developing bone. J. Biol. Chem. 1983;258:12723-12727.
30. 3 integrals. Exp Cell Res 1996;227:40-46.
31. Franzén A, Heinegård D. Isolation and characterization of two sialoproteins present only in bone calcified matrix. Biochem. J. 1985;232:715-724.
32. Frens G. Controlled nucleation for the regulation of particle size in monodispersed gold suspensions. Nature Phys. Sci. 1973;241:20-22.
33. Gehron Robey P. Cell-mediated calcification in vitro. In: Bonucci E, ed. Calcification in Biological Systems. Boca Raton, FL: CRC Press, 1992: 107-127.
34. Gehron Robey P. Bone matrix proteoglycans and glycoproteins. In: Bilezikian JP, Raisz LG, Rodan GA, eds. Principles of Bone Biology. San Diego, CA: Academic Press, 1996: 155-165.
35. Gerstenfeld LC, Chipman SD, Kelly CM, Hodgens KJ, Lee DD, Landis WJ. Collagen expression, ultrastructural assembly, and mineralization in cultures of chicken embryo osteoblasts. J. Cell. Biol. 1988;106: 979-989.
36. Gerstenfeld LC, Gotoh Y, McKee MD, Nanci A, Landis WJ, Glimcher MJ. Expression and ultrastructural immunolocalization of a major 66 kDa phosphoprotein synthesized by chicken osteoblasts during mineralization in vitro. Anat. Rec. 1990;228:93-103.
37. Gerstenfeld LC, Uporova T, Ashkar S, Salih E, Gotoh Y, McKee MD, Nanci A, Landis WJ, Glimcher MJ. Regulation of avian osteopontin pre- and posttranscriptional expression in skeletal tissues. Ann. NY Acad. Sci. 1995;760:67-82.
38. Gerstenfeld LC, Zurakowski D, Schaffer JL, Nichols DP, Toma CD, Broess M, Bruder SP, Caplan AI. Variable hormone responsiveness of osteoblast populations isolated at different stages of embryogenesis and its relationship to the osteogenic lineage. Endocrinology 1996;137:3957-3968.
39. Gorski JP. Is all bone the same? Distinctive distributions and properties of non-collagenous matrix proteins in lamellar vs. woven bone imply the existence of different underlying osteogenic mechanisms. Crit. Rev. Oral Biol. Med. 1998;9:201-223.
40. Groot CG, Danes JK, Blok J, Hoogendijk A, Hauschka PV. Light and electron microscopic demonstration of osteocalcin antigenicity in embryonic and adult rat bone. Bone 1986;7:379-385.
41. Hauschka PV, Frenkel J, DeMuth R, Gundberg CM. Presence of osteocalcin and related higher molecular weight 4-carboxyglutamic acid-containing proteins in developing bone. J. Biol. Chem. 1983;258: 176-182.
42. 3 integrin. J. Bone Miner. Res. 1992;7:335-343.
43. Hultenby K, Reinholt FP, Norgård M, Oldberg Å, Wendel M, Heinegård D. Distribution and synthesis of bone sialoprotein in metaphyseal bone of young rats show a distinctly different pattern from that of osteopontin. Eur. J. Cell. Biol. 1994;63:230-239.
44. Hunter GK, Goldberg HA. Nucleation of hydroxyapatite by bone sialoprotein. Proc. Natl. Acad. Sci. USA 1993;90:8562-8565.
45. Hunter GK, Hauschka PV, Poole AR, Rosenberg LC, Goldberg HA. Nucleation and inhibition of hydroxyapatite formation by mineralized tissue proteins. Biochem. J. 1996;317:59-64.
46. Ibaraki K, Termine JD, Whitson SW, Young MF. Bone matrix mRNA expression in differentiating fetal bovine osteoblasts. J. Bone Miner. Res. 1992;7:743-754.
47. Jamal HH, Aubin JE. CD44 expression in fetal rat bone: in vivo and in vitro analysis. Exp. Cell. Res. 1996;223:467-477.
48. Kasugai S, Nagata T, Sodek J. Temporal studies on the tissue compartmentalization of bone sialoprotein (BSP), osteopontin (OPN), and SPARC protein during bone formation in vitro. J. Cell. Physiol. 1992;152:467-477.
49. Kawaguchi H, McKee MD, Okamoto H, Nanci A. Immunocytochemical and lectin-gold characterization of the interface between alveolar bone and implanted hydroxyapatite in the rat. Cells Materials 1993;3:337-350.
50. Komaki M, Katagiri T, Suda T. Bone morphogenetic protein-2 does not alter the differentiation pathway of committed progenitors of osteoblasts and chondroblasts. Cell. Tissue Res. 1996;284:9-17.
51. Lian JB, Stein GS. Concepts of osteoblast growth and differentiation: basis for modulation of bone cell development and tissue formation. Crit. Rev. Oral Biol. Med. 1992;3:269-305.
52. Lian JB, McKee MD, Todd AM, Gerstenfeld LC. Induction of bone-related proteins, osteocalcin and osteopontin, and their matrix ultrastructural localization with development of chondrocyte hypertrophy in vitro. J. Cell. Biochem. 1993;52:206-219.
53. Majeska RJ. Culture of osteoblastic cells. In: Bilezikian JP, Raisz LG, Rodan GA, eds. Principles of Bone Biology. San Diego, CA: Academic Press, 1996: 1229-1237.
54. Mark MP, Prince CW, Gay S, Austin RL, Bhown M, Finkelman RD, Butler WT. A comparative immunocytochemical study on the subcellular distributions of 44 kDa bone phosphoprotein and bone γ-carboxyglutamic acid (Gla)-containing protein in osteoblasts. J. Bone Miner. Res. 1987;2:337-346.
55. Mark MP, Butler WT, Prince CW, Finkelman RD, Ruch J-V. Developmental expression of 44-kDa bone phosphoprotein (osteopontin) and bone y-carboxyglutamic acid (Gla)-containing protein (osteocalcin) in calcifying tissues of rat. Differentiation 1988;37:123-136.
56. McKee MD, Glimcher MJ, Nanci A. High-resolution immunolocalization of osteopontin and osteocalcin in bone and cartilage during endochondral ossification in the chicken tibia. Anat. Rec. 1992;234: 479-492.
57. McKee MD, Nanci A. Ultrastructural, cytochemical and immunocytochemical studies on bone and its interfaces. Cells Materials 1993;3: 219-243.
58. 2HS-glycoprotein) proteins in rat bone. J. Bone Miner. Res. 1993;8:485-496.
59. McKee MD, Nanci A. Osteopontin and the bone remodeling sequence, colloidal-gold immunocytochemistry of an interfacial extracellular matrix protein. Ann. NY Acad. Sci. 1995a;760:177-189
60. McKee MD, Nanci A. Postembedding colloidal-gold immunocytochemistry of noncollagenous extracellular matrix proteins in mineralized tissues. Microsc. Res. Tech. 1995b;31:44-62.
61. McKee MD, Nanci A. Osteopontin at mineralized tissue interfaces in bone, teeth, and osseointegrated implants: ultrastructural distribution and implications for mineralized tissue formation, turnover and repair. Microsc. Res. Tech. 1996a;33:141-164.
62. McKee MD, Nanci A. Osteopontin deposition in remodeling bone: an osteoblast mediated event [letter to the editor]. J. Bone Miner. Res. 1996b;11:873-874.
63. Midura RJ, McQuillan DJ, Benham KJ, Fisher LW, Hascall VC. A rat osteogenic cell line (UMR 106-01) synthesizes a highly sulfated form of bone sialoprotein. J. Biol. Chem. 1990;265:5285-5291.
64. Midura RJ, Hascall VC. Bone sialoprotein - A mucin in disguise? Glycobiology 1996;6:677-681.
65. Mintz KP, Grzesik WJ, Midura RJ, Gehron Robey P, Termine JD, Fisher LW. Purification and fragmentation of nondenatured bone sialoprotein: evidence for a cryptic, RGD-resistant cell attachment domain. J. Bone Miner. Res. 1993;8:985-995.
66. 3 integrin stimulates immediate cell signals in osteoclasts. J. Biol. Chem. 1991;266:20369-20374.
67. Nagata T, Bellows CG, Kasugai S, Butler WT, Sodek J. Biosynthesis of bone proteins [SPP-1 (secreted phosphoprotein-1, osteopontin), BSP (bone sialoprotein) and SPARC (osteonectin)] in association with mineralized-tissue formation by fetal-rat calvarial cells in culture. Biochem. J. 1991;274:513-520.
68. Nanci A, Ahluwalia JP, Zalzal S, Smith CE. Cytochemical and biochemical characterization of glycoproteins in forming and maturing enamel of the rat incisor. J. Histochem. Cytochem. 1989;37:1619-1633.
69. Nanci A, McCarthy GF, Zalzal S, Clokie CML, Warshawsky H, McKee MD. Tissue response to titanium implants in the rat tibia: ultrastructural, immunocytochemical and lectin-cytochemical characterization of the bone-titanium interface. Cells Materials 1994;4:1-30.
70. Nanci A, Zalzal S, Gotoh Y, McKee MD. Ultrastructural characterization and immunolocalization of osteopontin in rat calvarial osteoblast primary cultures. Microsc. Res. Tech. 1996;33:214-231.
71. Nefussi JR, Boy-Lefevre ML, Boulekbache H, Forest N. Mineralization in vitro of matrix formed by osteoblasts isolated by collagenase digestion. Differentiation 1985;29:160-168.
72. Nefussi JR, Brami G, Modrowski D, Oboeuf M, Forest N. Sequential expression of bone matrix proteins during rat calvaria osteoblast differentiation and bone nodule formation in vitro. J. Histochem. Cytochem. 1997;45:493-503.
73. Neiss WT. Electron staining of the cell surface coat by osmium-low ferrocyanide. Histochemistry 1984;80:231-242.
74. Nijweide PJ, Burger EH. Mechanisms of bone formation in vitro. In: Hall BK, ed. Bone: The Osteoblast and Osteocyte. Caldwell, NJ: The Telford Press, 1990: 303-326.
75. Oldberg Å, Franzén A, Heinegård D. Cloning and sequence analysis of rat bone sialoprotein (osteopontin) cDNA reveals an Arg-Gly-Asp cell-binding sequence. Proc. Natl. Acad. Sci. USA 1986;83:8819-8823.
76. Oldberg Å, Franzén A, Heinegård D. The primary structure of a cell-binding bone sialoprotein. J. Biol. Chem. 1988;263:19430-19432.
77. Owen TA, Aronow MA, Shalhoub V, Barone LM, Wilming LG, Tassinari MS, Kennedy MB, Pockwinse SM, Lian JB, Stein GS. Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J. Cell. Physiol. 1990;143:420-430.
78. Pockwinse SM, Wilming LG, Conlon DM, Stein GS, Lian JB. Expression of cell growth and bone specific genes at single cell resolution during development of bone tissue-like organization in primary osteoblast cultures. J. Cell. Biochem. 1992;49:310-323.
79. Prince CW, Oosawa T, Butler WT, Tomana M, Bhown AS, Bhown M, Schrohenloher RE. Isolation, characterization, and biosynthesis of a phosphorylated glycoprotein from rat bone. J. Biol. Chem. 1987;262: 2900-2907.
80. Ramakrishnan PR, Lin W-L, Sodek J, Cho M-I. Synthesis of noncollagenous extracellular matrix proteins during development of mineralized nodules by rat periodontal ligament cells in vitro. Calcif. Tissue Int. 1995;57:52-59.
81. Reinholt FP, Hultenby K, Oldberg Å, Heinegård D. Osteopontin-a possible anchor of osteoclasts to bone. Proc. Natl. Acad. Sci. USA 1990;87:4473-4475.
82. Rifas L, Uitto J, Memoli VA, Kuettner KE, Henry RW, Peck WA. Selective emergence of differentiated chondrocytes during serum-free culture of cells derived from fetal rat calvaria. J. Cell. Biol. 1982;92:493-504.
83. Riminucci M, Silvestrini G, Bonucci E, Fisher LW. Gehron Robey P, Bianco P. The anatomy of bone sialoprotein immunoreactive sites in bone as revealed by combined ultrastructural histochemistry and immunohistochemistry. Calcif. Tissue Int. 1995;57:277-284.
84. Ritter NM, Farach-Carson MC, Butler WT. Evidence for the formation of a complex between osteopontin and osteocalcin. J. Bone Miner. Res. 1992;7:877-885.
85. Roth J. Application of lectin-gold complexes for electron microscopic localization of glycoconjugates on thin sections. J. Histochem. Cytochem. 1983;31:987-999.
86. Scherft JP. The lamina limitans of the organic matrix of calcified cartilage and bone. J. Ultrastruct. Res. 1972;38:318-331.
87. Scherft JP. The lamina limitans of the organic bone matrix: formation in vitro. J. Ultrastruct. Res. 1978;64:173-181.
88. Shen X, Roberts E, Peel SAF, Davies JE. Organic extracellular matrix components at the bone cell/substratum interface. Cells Materials 1993;3:257-272.
89. Sodek J, Chen J, Kasugai S, Nagata T, Zhang Q, McKee MD, Nanci A. Elucidating the functions of bone sialoprotein and osteopontin in bone formation. In: Slavkin H, Price P, eds. Chemistry and Biology of Mineralized Tissues. Amsterdam: Excerpta Medica, 1992: 297-306.
90. Sodek J, Chen J, Nagata T, Kasugai S, Todescan R Jr., Li IWS, Kim RH. Regulation of osteopontin expression in osteoblasts. Ann. NY Acad. Sci. 1995;760:223-241.
91. Sorensen ES, Petersen TE. Identification of two phosphorylation motifs in bovine osteopontin. Biochem. Biophys. Res. Commun. 1994;198:200-205.
92. Sorensen ES, Petersen TE. Phosphorylation, glycosylation, and transglutaminase sites in bovine osteopontin. Ann. NY Acad. Sci. 1995;760: 363-366.
93. Stein GS, Lian JB. Stein JL, van Wijnen AJ, Frenkel B, Montecino M. Mechanisms regulating osteoblast proliferation and differentiation. In: Bilezikian JP, Raisz LG, Rodan GA, eds. Principles of Bone Biology. San Diego, CA: Academic Press, 1996: 69-86.
94. Triffit JT. The stem cell of the osteoblast. In: Bilezikian JP, Raisz LG, Rodan GA, eds. Principles of Bone Biology. San Diego, CA: Academic Press, 1996: 39-50.
95. van Dijk S, D'Errico JA, Somerman MJ, Farach-Carson MC, Butler WT. Evidence that a non-RGD domain in rat osteopontin is involved in cell attachment. J. Bone Miner. Res. 1993;8:1499-1506.
96. Wong G. Isolation and behavior of isolated bone-forming cells. In: Hall BK, ed. Bone: The Osteoblast and Osteocyte. Caldwell, NJ: The Telford Press, 1990: 171-192.
97. Zohar R, Lee W, Arora P, Cheifetz S, McCulloch C, Sodek J. Single cell analysis of intracellular osteopontin in osteogenic cultures of fetal rat calvarial cells. J. Cell. Physiol. 1997;170:88-100.