Summary
Diffusion chambers containing bone marrow cells from adult rats were implanted intraperitoneally into rat hosts and cultured in vivo for up to 64 days. Biochemical and histological analyses of the contents of the chambers demonstrate that a connective tissue consisting of bone, cartilage and fibrous tissues is formed by precursor cells present in marrow stroma. The amounts of osteogenic tissue and DNA are directly correlated with time of implantation and with number of cells inoculated. In the chambers there is initial formation of fibrous tissue which is strongly reactive to collagen type III, laminin and fibronectin. In areas of osteogenesis which appear later within this fibrous anlage, expression of collagen type III, laminin and fibronectin decrease and collagen types I and II increase in association with bone and cartilage respectively. Where osteogenesis does not develop, fibrous tissue continues to express collagen type III. The sequential expression of the different extracellular matrix components is similar to that previously observed during osteogenic differentiation in embryonic and adult developmental systems. It is concluded that the formation of fibrous and osteogenic tissues in diffusion chambers by precursor cells present in adult marrow, resembles the normal developmental process.
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References
Ashton BA, Allen TD, Howlett CR, Eaglesom CC, Hattori A, Owen M (1980) Formation of bone and cartilage by marrow stromal cells in diffusion chambers in vivo. Clin Orthop Rel Res 151:294–307
Ashton BA, Eaglesom CC, Bab I, Owen ME (1984) Distribution of fibroblastic colony-forming cells in rabbit bone marrow and assay of their osteogenic potential by an in vivo diffusion chamber method. Calcif Tissue Int 36:83–86
Bab I, Ashton BA, Syftestad GT, Owen ME (1984a) Assessment of an in vivo diffusion chamber method as a quantitative assay for osteogenesis. Calcif Tissue Int 36:77–82
Bab I, Howlett CR, Ashton BA, Owen ME (1984b) Ultrastructure of bone and cartilage formed in vivo in diffusion chambers. Clin Orthop Rel Res 187:243–254
Bab I, Ashton BA, Gazit D, Marx G, Williamson MC, Owen ME (1986) Kinetics and differentiation of marrow stromal cells in diffusion chambers in vivo. J Cell Sci 84:139–151
Bentley SA, Foidart J-M, Kleinman HK (1984) Connective tissue elements in rat bone marrow: Immunofluorescent visualization of the hematopoietic microenvironment. J Histochem Cytochem 32:114–116
Dessau W, Adelmann BC, Timpl R, Martin GR (1978) Identification of the sites in collagen α-chains that bind serum anti-gelatin factor (cold-insoluble globulin). Biochem J 169:55–59
Dessau W, von der Mark H, von der Mark K, Fischer S (1980) Changes in the patterns of collagens and fibronectin during limb-bud chondrogenesis. J Embryol Exp Morphol 57:51–60
Duthie RB, Mervin RM, Wolff J (1959) The functional activity of thyroid isografts within diffusion chambers in mice. Exp Cell Res 16:565–574
Friedenstein AJ (1976) Precursor cells of mechanocytes. Int Rev Cytol 47:327–355
Friedenstein AJ (1980) Stromal mechanisms of bone marrow: cloning in vitro and retransplantation in vivo. In: Thienfelder S (ed) Immunobiology of bone marrow transplantation. Springer, Berlin Heidelberg New York, pp 19–29
Friedenstein AJ, Chailakhjan RK, Lalykina KS (1970) The development of fibroblast colonies in monolayer cultures of guinea pig bone marrow and spleen cells. Cell Tissue Kinet 3:393–402
Friedenstein AJ, Ivanov-Smolenski AA, Chailakhjan RK, Gorskeja UF, Kuralesova AI, Latzinik NV, Gerasimov UF (1978) Origin of bone marrow stromal mechanocytes in radiochimeras and heterotopic transplants. Exp Hematol 6:440–444
Hotta T, Murate T, Utsumi M, Hirabayashi N, Yamada H (1983) Origins of hemopoietic and stromal cells in subcutaneous femur implants. Exp Hematol 11:107–113
Ksiazek T, Moskalewski S (1983) Studies of bone formation by cartilage reconstructed by isolated epiphyseal chondrocytes transplanted syngeneically or across known histocompatibility barriers in mice. Clin Orthop Rel Res 172:233–250
Mardon HJ, Triffitt JT (1987) A tissue-specific protein in rat osteogenic tissues. J Bone Miner Res 2 (3):191–199
Mark K von der (1981) Localization of collagen types in tissues. In: Hall DA, Jackson DS (eds) Int Rev Conn Tissue Res, vol 9. Academic Press, New York, pp 265–324
Mark K von der, Mark M von der (1977) Immunological and biochemical studies of collagen type transition during in vitro chondrogenesis of chick limb mesodermal cells. J Cell Biol 73:736–747
Mark H von der, Mark K von der, Gay S (1976a) Study of differential collagen synthesis during development of the chick embryo by immunofluorescence. I. Preparation of collagen type I and type II specific antibodies and their application to early stages of the chick embryo. Dev Biol 48:237–249
Mark K von der, Mark H von der, Gay S (1976b) Study of differential collagen synthesis during development of the chick embryo by immunofluorescence. II. Localization of type I and type II collagen during long bone development. Dev Biol 53:153–170
Owen ME (1985) Lineage of osteogenic cells and their relationship to the stromal system. In: Peck WA (ed) Bone and mineral research, vol 3. Elsvier, Amsterdam New York Oxford, pp 1–25
Reddi AH, Gay R, Gay S, Miller EJ (1977) Transitions in collagen types during matrix-induced cartilage, bone, and bone marrow formation. Proc Natl Acad Sci USA 74:5589–5592
Stenman S, Vaheri A (1978) Distribution of a major connective tissue protein, fibronectin, in normal human tissues. J Exp Med 147:1054–1064
Tavassoli M, Crosby WH (1968) Transplantation of marrow to extramedullary sites. Science 161:54–56
Timpl R, Rohde H, Robey PG, Rennard SI, Foidart J-M, Martin GR (1979) Laminin — A glycoprotein from basement membranes. J Biol Chem 254:9933–9937
Vuento M, Vaheri A (1979) Purification of fibronectin from human plasma by affinity chromatography under non-denaturing conditions. Biochem J 183:331–337
Weiss RE, Reddi AH (1980) Synthesis and localization of fibronectin during collagenous matrix-mesenchymal cell interaction and differentiation of cartilage and bone in vivo. Proc Natl Acad Sci USA 77:2074–2078
Weston H, Bainton DF (1979) Association of alkaline phosphatase-positive reticulum cells in bone marrow with granulocytic precursors. J Exp Med 150:919–937
Wick G, Glanville RW, Timpl R (1979) Characterisation of antibodies to basement membrane (type IV) collagen in immunohistological studies. Immunobiology 156:372–381
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Mardon, H.J., Bee, J., von der Mark, K. et al. Development of osteogenic tissue in diffusion chambers from early precursor cells in bone marrow of adult rats. Cell Tissue Res. 250, 157–165 (1987). https://doi.org/10.1007/BF00214667
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DOI: https://doi.org/10.1007/BF00214667