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Osteoblastic and osteoclastic differentiation of mononuclear cells facing the resorbing surface of uncalcified cartilage in the tibia of embryonic chick


The resorbing region of uncalcified cartilage in the tibia of embryonic chick was studied using 3H-proline autoradiography, histochemistry, and horseradish-peroxidase tracers.

At the cartilage-bone marrow interface, two kinds of cells (A and B) were identified. Type-A cells were elongated, contacted the matrix of the uncalcified cartilage directly, and possessed extensive rough endoplasmic reticulum, one or two juxtanuclear Golgi apparatus and cell membranes exhibiting prominent alkaline phosphatase activity. Type-B cells were round to oval, mononucleate (occasionally binucleate), and contained abundant mitochondria, vacuoles and vesicles, well-developed Golgi apparatus, and lysosomes. The lysosomes and the majority of vacuoles and Golgi lamellae of these cells showed prominent acid phosphatase activity. Type-B cells accumulated more horseradish-peroxidase reaction product in their vacuoles and vesicles than type-A cells. Thick, banded collagen fibrils were occasionally found in the matrix of the resorbing surface. 3H-proline autoradiography revealed small numbers of grains at the cartilage-bone marrow interface.

These findings suggest that type-A cells have osteoblastic and type-B cells osteoclastic properties and are precursor cells of osteoblasts and osteoclasts, respectively. The appearance of a mineral phase in the resorbing cartilage is probably important for the differentiation of these cells.

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  1. Dingle JT (1973) The role of lysosomal enzyme in skeletal tissues. J Bone Joint Surg 55B:87–95

  2. Fell HB (1925) The histogenesis of cartilage and bone in the long bones of embryonic fowl. J Morphol Physiol 40:417–459

  3. Göthlin G, Ericsson LE (1976) The osteoclast. Review of ultrastructure, origin, and structure-function relationship. Clin Orthop 120:201–231

  4. Graham RC, Karnovsky MJ (1964) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem 14:291–302

  5. Ham W, Cormack DH (1979) Histology. J.B. Lippincott Company, Philadelphia and Toronto

  6. Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92

  7. Higuchi S, Suga M, Dannergerg AM, Schofied BH (1979) Histochemical demonstration of enzyme activities in plastic and paraffin embedded tissue sections. Stain Technol 55:5–12

  8. Howlett CR (1980) The fine structure of the proximal growth plate and metaphysis of the avian tibia: endochondral osteogenesis. J Anat 130:745–768

  9. Jetereau FU, Le Douarin NM (1978) The developmental relationship between osteocytes and osteoclasts: a study using the quail-chick nuclear marker in endochondral ossification. Dev Biol 63:253–265

  10. Kahn AJ, Simmons DJ (1975) Investigation of cell lineage in bone using chimera of chicks and quail embryonic tissue. Nature (Lond) 258:325

  11. Krukowski M, Kahn AJ (1982) Inductive specificity of mineralized bone matrix in ectopic osteoclast differentiation. Calcif Tiss Int 34:474–479

  12. Lucht U (1972) Absorption by osteoclasts as studied by electron microscopic histochemistry. Histochemistry 29:274–286

  13. Mark K von der, Mark H von der, Gay S (1976) 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

  14. Rifkin BR, Brand JS, Cushing JE, Coleman S, Sanavi F (1980) Fine structure of fetal rat calvarium: provisional identification of preosteoclasts. Calcif Tiss Int 31:21–28

  15. Sakamoto M, Sakamoto S (1984) Immunocytochemical localization of collagenase in isolated mouse bone cells. Biomed Res 5:29–38

  16. Scott BL (1976) Thymidine-3H electron microscopic radioautography of osteogenic cells in the fetal rat. J Cell Biol 35:115–126

  17. Scott BL, Glimcher MJ (1971) Distribution of glycogen in osteoblasts of the fetal rat. J Ultrastruct Res 36:565–586

  18. Silverstrina GS, Ricordi ME, Bonucci E (1979) Resorption of uncalcified cartilage in the diaphysis of the chick embryo tibia. Cell Tissue Res 196:221–235

  19. Sorrell JM, Weiss LA (1980) A light and electron microscopic study of the region of cartilage resorption in the embryonic chick femur. Anat Rec 198:513–530

  20. Sorrell JM, Weiss L (1982) The cellular organization of fibroblastic cells and macrophages at regions of uncalcified cartilage resorption in the embryonic chick femur as revealed by alkaline and acid phosphatase histochemistry. Anat Rec 202:491–499

  21. Thyberg J, Nilsson S, Friberg U (1975) Electron microscopic and enzyme cytochemical studies on the guinea pig metaphysis with special reference to lysosomal system of different cell type. Cell Tissue Res 156:273–299

  22. Walker DG (1975) Bone resorption restored in osteopetrotic mice by transplants of normal bone marrow and spleen cells. Science (Wash DC) 190:784–785

  23. Wolbach SB, Hegsted DM (1952) Endochondral bone growth in the chick. Arch Pathol 54:1–12

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Correspondence to Dr. Akira Yamaguchi.

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Yamaguchi, A., Yamanouchi, M. & Yoshiki, S. Osteoblastic and osteoclastic differentiation of mononuclear cells facing the resorbing surface of uncalcified cartilage in the tibia of embryonic chick. Cell Tissue Res. 240, 425–431 (1985).

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Key words

  • Osteoblasts
  • Osteoclasts
  • Differentiation
  • Bone
  • Cartilage
  • Chicken