Skip to main content

Some NLM-NCBI services and products are experiencing heavy traffic, which may affect performance and availability. We apologize for the inconvenience and appreciate your patience. For assistance, please contact our Help Desk at info@ncbi.nlm.nih.gov.

The Journal of Biophysical and Biochemical Cytology logoLink to The Journal of Biophysical and Biochemical Cytology
. 1960 Dec 1;8(3):719–760. doi: 10.1083/jcb.8.3.719

CHONDROGENESIS, STUDIED WITH THE ELECTRON MICROSCOPE

Gabriel C Godman 1, Keith R Porter 1
PMCID: PMC2224963  PMID: 13706207

Abstract

The role of the cells in the fabrication of a connective tissue matrix, and the structural modifications which accompany cytodifferentiation have been investigated in developing epiphyseal cartilage of fetal rat by means of electron microscopy. Differentiation of the prechondral mesenchymal cells to chondroblasts is marked by the acquisition of an extensive endoplasmic reticulum, enlargement and concentration of the Golgi apparatus, the appearance of membrane-bounded cytoplasmic inclusions, and the formation of specialized foci of increased density in the cell cortex. These modifications are related to the secretion of the cartilage matrix. The matrix of young hyaline cartilage consists of groups of relatively short, straight, banded collagen fibrils of 10 to 20 mµ and a dense granular component embedded in an amorphous ground substance of moderate electron density. It is postulated that the first phase of fibrillogenesis takes place at the cell cortex in dense bands or striae within the ectoplasm subjacent to the cell membrane. These can be resolved into sheaves of "primary" fibrils of about 7 to 10 mµ. They are supposedly shed (by excortication) into the matrix space between the separating chondroblasts, where they may serve as "cores" of the definitive matrix fibrils. The diameter of the fibrils may subsequently increase up to threefold, presumably by incorporation of "soluble" or tropocollagen units from the ground substance. The chondroblast also discharges into the matrix the electrondense amorphous or granular contents of vesicles derived from the Golgi apparatus, and the mixed contents of large vacuoles or blebs bounded by distinctive double membranes. Small vesicles with amorphous homogeneous contents of moderate density are expelled in toto from the chondroblasts. In their subsequent evolution to chondrocytes, both nucleus and cytoplasm of the chondroblasts undergo striking condensation. Those moving toward the osteogenic plate accumulate increasingly large stores of glycogen. In the chondrocyte, the enlarged fused Golgi vesicles with dense contents, massed in the juxtanuclear zone, are the most prominent feature of the cytoplasm. Many of these make their way to the surface to discharge their contents. The hypertrophied chondrocytes of the epiphyseal plate ultimately yield up their entire contents to the matrix.

Full Text

The Full Text of this article is available as a PDF (4.2 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. BOSTROM H., ODEBLAD E. Autoradiographic observations on the incorporation of S35-labeled sodium sulfate in the rabbit fetus. Anat Rec. 1953 Mar;115(3):505–513. doi: 10.1002/ar.1091150305. [DOI] [PubMed] [Google Scholar]
  2. CAMERON D. A., ROBINSON R. A. Electron microscopy of cartilage and bone matrix at the distal epiphyseal line of the femur in the newborn infant. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):253–260. doi: 10.1083/jcb.2.4.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. CAMERON D. A., ROBINSON R. A. Electron microscopy of epiphyseal and articular cartilage matrix in the femur of the newborn infant. J Bone Joint Surg Am. 1958 Jan;40-A(1):163–170. [PubMed] [Google Scholar]
  4. DALTON A. J., FELIX M. D. A comparative study of the Golgi complex. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):79–84. doi: 10.1083/jcb.2.4.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. DALTON A. J., FELIX M. D. The electron microscopy of normal and malignant cells. Ann N Y Acad Sci. 1956 Mar 30;63(6):1117–1140. doi: 10.1111/j.1749-6632.1956.tb32127.x. [DOI] [PubMed] [Google Scholar]
  6. EICHELBERGER L., AKESON W. H., ROMA M. Biochemical studies of articular cartilage. I. Normal values. J Bone Joint Surg Am. 1958 Jan;40-A(1):142–152. [PubMed] [Google Scholar]
  7. EICHELBERGER L., ROMA M. Effects of age on the histochemical characterization of costal cartilage. Am J Physiol. 1954 Aug;178(2):296–304. doi: 10.1152/ajplegacy.1954.178.2.296. [DOI] [PubMed] [Google Scholar]
  8. EPSTEIN M. A. The fine structural organisation of Rous tumour cells. J Biophys Biochem Cytol. 1957 Nov 25;3(6):851–858. doi: 10.1083/jcb.3.6.851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. FOLLIS R. H., Jr, BERTHRONG M. Histochemical studies on cartilage and bone; the normal pattern. Bull Johns Hopkins Hosp. 1949 Oct;85(4):281–297. [PubMed] [Google Scholar]
  10. FOLLIS R. H., Jr, MELANOTTE P. L. Dehydrogenase activity of rat epiphyseal cartilage. Proc Soc Exp Biol Med. 1956 Nov;93(2):382–384. doi: 10.3181/00379727-93-22763. [DOI] [PubMed] [Google Scholar]
  11. FOLLIS R. H., Jr, TOUSIMIS A. J. Experimental lathyrism in the rat; nature of defect in epiphysial cartilage. Proc Soc Exp Biol Med. 1958 Aug-Sep;98(4):843–848. doi: 10.3181/00379727-98-24204. [DOI] [PubMed] [Google Scholar]
  12. GROSSFELD H., MEYER K., GODMAN G., LINKER A. Mucopolysaccharides produced in tissue culture. J Biophys Biochem Cytol. 1957 May 25;3(3):391–396. doi: 10.1083/jcb.3.3.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. GROSS J. The behavior of collagen units as a model in morphogenesis. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):261–274. doi: 10.1083/jcb.2.4.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. HAY E. D. The fine structure of blastema cells and differentiating cartilage cells in regenerating limbs of Amblystoma larvae. J Biophys Biochem Cytol. 1958 Sep 25;4(5):583–591. doi: 10.1083/jcb.4.5.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. HELLER-STEINBERG M. Ground substance, bone salts, and cellular activity in bone formation and destruction. Am J Anat. 1951 Nov;89(3):347–379. doi: 10.1002/aja.1000890302. [DOI] [PubMed] [Google Scholar]
  16. JACKSON D. S., WILLIAMS G. Two organic fixatives for acid mucopolysaccharides. Stain Technol. 1956 Sep;31(5):189–191. doi: 10.3109/10520295609113802. [DOI] [PubMed] [Google Scholar]
  17. JACKSON S. F., SMITH R. H. Studies on the biosynthesis of collagen. I. The growth of fowl osteoblasts and the formation of collagen in tissue culture. J Biophys Biochem Cytol. 1957 Nov 25;3(6):897–912. doi: 10.1083/jcb.3.6.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. JOEL W., MASTERS Y. F., SHETLAR M. R. Comparison of histochemical and biochemical methods for the polysaccharides of cartilage. J Histochem Cytochem. 1956 Sep;4(5):476–478. doi: 10.1177/4.5.476. [DOI] [PubMed] [Google Scholar]
  19. KAPLAN D., MEYER K. Ageing of human cartilage. Nature. 1959 May 2;183(4670):1267–1268. doi: 10.1038/1831267a0. [DOI] [PubMed] [Google Scholar]
  20. KLEMPERER P. The significance of the intermediate substances of the connective tissue in human disease. Harvey Lect. 1953;49:100–123. [PubMed] [Google Scholar]
  21. LEBLOND C. P., GLEGG R. E., EIDINGER D. Presence of carbohydrates with free 1,2-glycol groups in sites stained by the periodic acid-Schiff technique. J Histochem Cytochem. 1957 Sep;5(5):445–458. doi: 10.1177/5.5.445. [DOI] [PubMed] [Google Scholar]
  22. LOEWI G., MEYER K. The acid mucopolysaccharides of embryonic skin. Biochim Biophys Acta. 1958 Mar;27(3):453–456. doi: 10.1016/0006-3002(58)90371-8. [DOI] [PubMed] [Google Scholar]
  23. MEYER K., HOFFMAN P., LINKER A. Mucopolysaccharides of costal cartilage. Science. 1958 Oct 17;128(3329):896–896. doi: 10.1126/science.128.3329.896. [DOI] [PubMed] [Google Scholar]
  24. MONTAGNA W. Glycogen and lipids in human cartilage, with some cytochemical observations on the cartilage of the dog, cat, and rabbit. Anat Rec. 1949 Jan;103(1):77–92. doi: 10.1002/ar.1091030106. [DOI] [PubMed] [Google Scholar]
  25. McCLUSKEY R. T., THOMAS L. The removal of cartilage matrix, in vivo, by papain; identification of crystalline papain protease as the cause of the phenomenon. J Exp Med. 1958 Sep 1;108(3):371–384. doi: 10.1084/jem.108.3.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. PALADE G. E., PORTER K. R. Studies on the endoplasmic reticulum. I. Its identification in cells in situ. J Exp Med. 1954 Dec 1;100(6):641–656. doi: 10.1084/jem.100.6.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. PALADE G. E., SIEKEVITZ P. Pancreatic microsomes; an integrated morphological and biochemical study. J Biophys Biochem Cytol. 1956 Nov 25;2(6):671–690. doi: 10.1083/jcb.2.6.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. PALADE G. E. The endoplasmic reticulum. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):85–98. doi: 10.1083/jcb.2.4.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. PELC S. R., GLUCKSMANN A. Sulphate metabolism in the cartilage of the trachea, pinna and xiphoid process of the adult mouse as indicated by autoradiographs. Exp Cell Res. 1955 Apr;8(2):336–344. doi: 10.1016/0014-4827(55)90145-2. [DOI] [PubMed] [Google Scholar]
  30. PORTER K. R. Electron microscopy of basophilic components of cytoplasm. J Histochem Cytochem. 1954 Sep;2(5):346–375. doi: 10.1177/2.5.346. [DOI] [PubMed] [Google Scholar]
  31. PORTER K. R., PAPPAS G. D. Collagen formation by fibroblasts of the chick embryo dermis. J Biophys Biochem Cytol. 1959 Jan 25;5(1):153–166. doi: 10.1083/jcb.5.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. PRITCHARD J. J. A cytological and histochemical study of bone and cartilage formation in the rat. J Anat. 1952 Jul;86(3):259–277. [PMC free article] [PubMed] [Google Scholar]
  33. SCOTT B. L., PEASE D. C. Electron microscopy of the epiphyseal apparatus. Anat Rec. 1956 Dec;126(4):465–495. doi: 10.1002/ar.1091260405. [DOI] [PubMed] [Google Scholar]
  34. SHATTON J., SCHUBERT M. Isolation of a mucoprotein from cartilage. J Biol Chem. 1954 Dec;211(2):565–573. [PubMed] [Google Scholar]
  35. SHELDON H., ROBINSON R. A. Studies on cartilage: electron microscope observations on normal rabbit ear cartilage. J Biophys Biochem Cytol. 1958 Jul 25;4(4):401–406. doi: 10.1083/jcb.4.4.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. SIEKEVITZ P., WATSON M. L. The isolation and analysis of a mitochondrial membrane fraction. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):379–382. doi: 10.1083/jcb.2.4.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. STIDWORTHY G., MASTERS Y. F., SHETLAR M. R. The effect of aging on mucopolysaccharide composition of human costal cartilage as measured by hexosamine and uronic acid content. J Gerontol. 1958 Jan;13(1):10–13. doi: 10.1093/geronj/13.1.10. [DOI] [PubMed] [Google Scholar]
  38. TSALTAS T. T. Papain-induced changes in rabbit cartilage; alterations in the chemical structure of the cartilage matrix. J Exp Med. 1958 Oct 1;108(4):507–513. doi: 10.1084/jem.108.4.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. WASSERMANN F. Fibrillogenesis in the regenerating rat tendon with special reference to growth and composition of the collagenous fibril. Am J Anat. 1954 May;94(3):399–437. doi: 10.1002/aja.1000940304. [DOI] [PubMed] [Google Scholar]
  40. WATSON M. L. Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol. 1958 Jul 25;4(4):475–478. doi: 10.1083/jcb.4.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. ZELANDER T. Ultrastructure of articular cartilage. Z Zellforsch Mikrosk Anat. 1959;49(6):720–738. doi: 10.1007/BF00342718. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Biophysical and Biochemical Cytology are provided here courtesy of The Rockefeller University Press

RESOURCES