Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1984 Jul 1;99(1 Pt 1):208–216. doi: 10.1083/jcb.99.1.208

Synthesis of a low molecular weight collagen by chondrocytes from the presumptive calcification region of the embryonic chick sterna: the influence of culture with collagen gels

PMCID: PMC2275622  PMID: 6736128

Abstract

The mature chick sternum is divisible almost equally into cephalic calcified and caudal cartilagenous regions. Isolation and culture of cells derived from embryonic precursors of these regions has revealed two discrete populations of cells with distinct morphological features and synthetic capabilities. Both cell populations grew well in culture within or upon collagen gels or upon plastic and maintained morphologies similar to those observed in the parent tissue. Polyacrylamide gel electrophoresis of radiolabeled proteins synthesized by the cells in culture demonstrated large differences in the types of collagens synthesized. Both chondrocyte populations synthesized type II and minor cartilage collagens but only chondrocytes isolated from the presumptive calcification region synthesized the previously identified, low molecular weight collagen, termed G collagen. Synthesis of G collagen was stimulated by culture within or upon collagen gels such that it represented an average of 65% of the total collagen synthesized by presumptive calcification region chondrocytes after 7 d of culture within collagen gels. Light and scanning electron microscopy demonstrated that the two chondrocyte types exhibited distinct morphological features and accumulated different extracellular matrices in culture.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Ayad S., Abedin M. Z., Grundy S. M., Weiss J. B. Isolation and characterisation of an unusual collagen from hyaline cartilage and intervertebral disc. FEBS Lett. 1981 Jan 26;123(2):195–199. doi: 10.1016/0014-5793(81)80286-4. [DOI] [PubMed] [Google Scholar]
  2. BURTON K. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J. 1956 Feb;62(2):315–323. doi: 10.1042/bj0620315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  4. Brighton C. T., Heppenstall R. B. Oxygen tension in zones of the epiphyseal plate, the metaphysis and diaphysis. An in vitro and in vivo study in rats and rabbits. J Bone Joint Surg Am. 1971 Jun;53(4):719–728. [PubMed] [Google Scholar]
  5. Brighton C. T., Ray R. D., Soble L. W., Kuettner K. E. In vitro epiphyseal-plate growth in various oxygen tensions. J Bone Joint Surg Am. 1969 Oct;51(7):1383–1396. doi: 10.2106/00004623-196951070-00018. [DOI] [PubMed] [Google Scholar]
  6. Burgeson R. E., Hollister D. W. Collagen heterogeneity in human cartilage: identification of several new collagen chains. Biochem Biophys Res Commun. 1979 Apr 27;87(4):1124–1131. doi: 10.1016/s0006-291x(79)80024-8. [DOI] [PubMed] [Google Scholar]
  7. Duance V. C., Shimokomaki M., Bailey A. J. Immunofluorescence localization of type-M collagen in articular cartilage. Biosci Rep. 1982 Apr;2(4):223–227. doi: 10.1007/BF01136720. [DOI] [PubMed] [Google Scholar]
  8. Emerman J. T., Burwen S. J., Pitelka D. R. Substrate properties influencing ultrastructural differentiation of mammary epithelial cells in culture. Tissue Cell. 1979;11(1):109–119. doi: 10.1016/0040-8166(79)90011-9. [DOI] [PubMed] [Google Scholar]
  9. Flint M. Interrelationships of mucopolysaccharide and collagen in connective tissue remodelling. J Embryol Exp Morphol. 1972 Apr;27(2):481–495. [PubMed] [Google Scholar]
  10. Gibson G. J., Kielty C. M., Garner C., Schor S. L., Grant M. E. Identification and partial characterization of three low-molecular-weight collagenous polypeptides synthesized by chondrocytes cultured within collagen gels in the absence and in the presence of fibronectin. Biochem J. 1983 May 1;211(2):417–426. doi: 10.1042/bj2110417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gibson G. J., Schor S. L., Grant M. E. Effects of matrix macromolecules on chondrocyte gene expression: synthesis of a low molecular weight collagen species by cells cultured within collagen gels. J Cell Biol. 1982 Jun;93(3):767–774. doi: 10.1083/jcb.93.3.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Howlett C. R. The fine structure of the proximal growth plate of the avian tibia. J Anat. 1979 Mar;128(Pt 2):377–399. [PMC free article] [PubMed] [Google Scholar]
  13. Juva K., Prockop D. J. Modified procedure for the assay of H-3-or C-14-labeled hydroxyproline. Anal Biochem. 1966 Apr;15(1):77–83. doi: 10.1016/0003-2697(66)90249-1. [DOI] [PubMed] [Google Scholar]
  14. Kim J. J., Conrad H. E. Properties of cultured chondrocytes obtained from histologically distinct zones of the chick embryo tibiotarsus. J Biol Chem. 1977 Nov 25;252(22):8292–8299. [PubMed] [Google Scholar]
  15. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  16. Lutfi A. M. The ultrastructure of cartilage cells in the epiphyses of long bones in the domestic fowl. Acta Anat (Basel) 1974;87(1):12–21. doi: 10.1159/000144152. [DOI] [PubMed] [Google Scholar]
  17. Miller E. J. Biochemical characteristics and biological significance of the genetically-distinct collagens. Mol Cell Biochem. 1976 Dec 10;13(3):165–192. doi: 10.1007/BF01731779. [DOI] [PubMed] [Google Scholar]
  18. Ooira A., Kimata K., Suzuki S., Takata K., Suzuki I. A correlation between synthetic activities for matrix macromolecules and specific stages of cyto-differentiation in developing cartilage. J Biol Chem. 1974 Mar 10;249(5):1637–1645. [PubMed] [Google Scholar]
  19. Reese C. A., Mayne R. Minor collagens of chicken hyaline cartilage. Biochemistry. 1981 Sep 15;20(19):5443–5448. doi: 10.1021/bi00522a014. [DOI] [PubMed] [Google Scholar]
  20. Reese C. A., Wiedemann H., Kühn K., Mayne R. Characterization of a highly soluble collagenous molecule isolated from chicken hyaline cartilage. Biochemistry. 1982 Mar 2;21(5):826–830. doi: 10.1021/bi00534a002. [DOI] [PubMed] [Google Scholar]
  21. Remington M. C., Bashey R. I., Brighton C. T., Jimenez S. A. Biosynthesis of a low molecular weight collagen by rabbit growth plate cartilage organ cultures. Coll Relat Res. 1983 May;3(3):271–277. doi: 10.1016/s0174-173x(83)80009-0. [DOI] [PubMed] [Google Scholar]
  22. Ricard-Blum S., Hartmann D. J., Herbage D., Payen-Meyran C., Ville G. Biochemical properties and immunolocalization of minor collagens in foetal calf cartilage. FEBS Lett. 1982 Sep 20;146(2):343–347. doi: 10.1016/0014-5793(82)80949-6. [DOI] [PubMed] [Google Scholar]
  23. Sattler C. A., Michalopoulos G., Sattler G. L., Pitot H. C. Ultrastructure of adult rat hepatocytes cultured on floating collagen membranes. Cancer Res. 1978 Jun;38(6):1539–1549. [PubMed] [Google Scholar]
  24. Schmid T. M., Conrad H. E. A unique low molecular weight collagen secreted by cultured chick embryo chondrocytes. J Biol Chem. 1982 Oct 25;257(20):12444–12450. [PubMed] [Google Scholar]
  25. Schmid T. M., Conrad H. E. Metabolism of low molecular weight collagen by chondrocytes obtained from histologically distinct zones of the chick embryo tibiotarsus. J Biol Chem. 1982 Oct 25;257(20):12451–12457. [PubMed] [Google Scholar]
  26. Schmid T. M., Linsenmayer T. F. A short chain (pro)collagen from aged endochondral chondrocytes. Biochemical characterization. J Biol Chem. 1983 Aug 10;258(15):9504–9509. [PubMed] [Google Scholar]
  27. Shapiro I. M., Golub E. E., Kakuta S., Hazelgrove J., Havery J., Chance B., Frasca P. Initiation of endochondral calcification is related to changes in the redox state of hypertrophic chondrocytes. Science. 1982 Sep 3;217(4563):950–952. doi: 10.1126/science.7112108. [DOI] [PubMed] [Google Scholar]
  28. Shimokomaki M., Duance V. C., Bailey A. J. Identification of a new disulphide bonded collagen from cartilage. FEBS Lett. 1980 Nov 17;121(1):51–54. doi: 10.1016/0014-5793(80)81265-8. [DOI] [PubMed] [Google Scholar]
  29. Shimokomaki M., Duance V. C., Bailey A. J. Identification of two further collagenous fractions from articular cartilage. Biosci Rep. 1981 Jul;1(7):561–570. doi: 10.1007/BF01116305. [DOI] [PubMed] [Google Scholar]
  30. Solursh M., Linsenmayer T. F., Jensen K. L. Chondrogenesis from single limb mesenchyme cells. Dev Biol. 1982 Nov;94(1):259–264. doi: 10.1016/0012-1606(82)90090-2. [DOI] [PubMed] [Google Scholar]
  31. Yang J., Elias J. J., Petrakis N. L., Wellings S. R., Nandi S. Effects of hormones and growth factors on human mammary epithelial cells in collagen gel culture. Cancer Res. 1981 Mar;41(3):1021–1027. [PubMed] [Google Scholar]
  32. von der Mark K., van Menxel M., Wiedemann H. Isolation and characterization of new collagens from chick cartilage. Eur J Biochem. 1982 May;124(1):57–62. doi: 10.1111/j.1432-1033.1982.tb05905.x. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES