Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1986 Apr 1;102(4):1151–1156. doi: 10.1083/jcb.102.4.1151

Collagen gene expression during limb cartilage differentiation

PMCID: PMC2114156  PMID: 3754261

Abstract

As limb mesenchymal cells differentiate into chondrocytes, they initiate the synthesis of type II collagen and cease synthesizing type I collagen. Changes in the cytoplasmic levels of type I and type II collagen mRNAs during the course of limb chondrogenesis in vivo and in vitro were examined using cloned cDNA probes. A striking increase in cytoplasmic type II collagen mRNA occurs coincident with the crucial condensation stage of chondrogenesis in vitro, in which prechondrogenic mesenchymal cells become closely juxtaposed before depositing a cartilage matrix. Thereafter, a continuous and progressive increase in the accumulation of cytoplasmic type II collagen mRNA occurs which parallels the progressive accumulation of cartilage matrix by cells. The onset of overt chondrogenesis, however, does not involve activation of the transcription of the type II collagen gene. Low levels of type II collagen mRNA are present in the cytoplasm of prechondrogenic mesenchymal cells at the earliest stages of limb development, well before the accumulation of detectable levels of type II collagen. Type I collagen gene expression during chondrogenesis is regulated, at least in part, at the translational level. Type I collagen mRNAs are present in the cytoplasm of differentiated chondrocytes, which have ceased synthesizing detectable amounts of type I collagen.

Full Text

The Full Text of this article is available as a PDF (861.4 KB).

Selected References

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

  1. Allebach E. S., Boettiger D., Pacifici M., Adams S. L. Control of types I and II collagen and fibronectin gene expression in chondrocytes delineated by viral transformation. Mol Cell Biol. 1985 May;5(5):1002–1008. doi: 10.1128/mcb.5.5.1002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Archer C. W., Rooney P., Wolpert L. Cell shape and cartilage differentiation of early chick limb bud cells in culture. Cell Differ. 1982 Jun;11(4):245–251. doi: 10.1016/0045-6039(82)90072-0. [DOI] [PubMed] [Google Scholar]
  3. Biddulph D. M., Sawyer L. M., Smales W. P. Chondrogenesis of chick limb mesenchyme in vitro. Effects of prostaglandins on cyclic AMP. Exp Cell Res. 1984 Jul;153(1):270–274. doi: 10.1016/0014-4827(84)90471-3. [DOI] [PubMed] [Google Scholar]
  4. Brunk C. F., Jones K. C., James T. W. Assay for nanogram quantities of DNA in cellular homogenates. Anal Biochem. 1979 Jan 15;92(2):497–500. doi: 10.1016/0003-2697(79)90690-0. [DOI] [PubMed] [Google Scholar]
  5. Cheley S., Anderson R. A reproducible microanalytical method for the detection of specific RNA sequences by dot-blot hybridization. Anal Biochem. 1984 Feb;137(1):15–19. doi: 10.1016/0003-2697(84)90339-7. [DOI] [PubMed] [Google Scholar]
  6. Chepenik K. P., Ho W. C., Waite B. M., Parker C. L. Arachidonate metabolism during chondrogenesis in vitro. Calcif Tissue Int. 1984 Mar;36(2):175–181. doi: 10.1007/BF02405314. [DOI] [PubMed] [Google Scholar]
  7. Dessau W., von der Mark H., von der Mark K., Fischer S. Changes in the patterns of collagens and fibronectin during limb-bud chondrogenesis. J Embryol Exp Morphol. 1980 Jun;57:51–60. [PubMed] [Google Scholar]
  8. Duchêne M., Sobel M. E., Müller P. K. Levels of collagen mRNA in dedifferentiating chondrocytes. Exp Cell Res. 1982 Dec;142(2):317–324. doi: 10.1016/0014-4827(82)90373-1. [DOI] [PubMed] [Google Scholar]
  9. Focht R. J., Adams S. L. Tissue specificity of type I collagen gene expression is determined at both transcriptional and post-transcriptional levels. Mol Cell Biol. 1984 Sep;4(9):1843–1852. doi: 10.1128/mcb.4.9.1843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gay S. W., Kosher R. A. Prostaglandin synthesis during the course of limb cartilage differentiation in vitro. J Embryol Exp Morphol. 1985 Oct;89:367–382. [PubMed] [Google Scholar]
  11. Gay S. W., Kosher R. A. Uniform cartilage differentiation in micromass cultures prepared from a relatively homogeneous population of chondrogenic progenitor cells of the chick limb bud: effect of prostaglandins. J Exp Zool. 1984 Nov;232(2):317–326. doi: 10.1002/jez.1402320219. [DOI] [PubMed] [Google Scholar]
  12. Harpold M. M., Dobner P. R., Evans R. M., Bancroft F. C. Construction and identification by positive hybridization-translation of a bacterial plasmid containing a rat growth hormone structural gene sequence. Nucleic Acids Res. 1978 Jun;5(6):2039–2053. doi: 10.1093/nar/5.6.2039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ho W. C., Greene R. M., Shanfeld J., Davidovitch Z. Cyclic nucleotides during chondrogenesis: concentration and distribution in vivo and in vitro. J Exp Zool. 1982 Dec 30;224(3):321–330. doi: 10.1002/jez.1402240305. [DOI] [PubMed] [Google Scholar]
  14. Kosher R. A., Gay S. W. The effect of prostaglandins on the cyclic AMP content of limb mesenchymal cells. Cell Differ. 1985 Sep;17(3):159–167. doi: 10.1016/0045-6039(85)90483-x. [DOI] [PubMed] [Google Scholar]
  15. Kosher R. A., Savage M. P., Chan S. C. In vitro studies on the morphogenesis and differentiation of the mesoderm subjacent to the apical ectodermal ridge of the embryonic chick limb-bud. J Embryol Exp Morphol. 1979 Apr;50:75–97. [PubMed] [Google Scholar]
  16. Kosher R. A., Savage M. P. Studies on the possible role of cyclic AMP in limb morphogenesis and differentiation. J Embryol Exp Morphol. 1980 Apr;56:91–105. [PubMed] [Google Scholar]
  17. Kosher R. A., Savage M. P., Walker K. H. A gradation of hyaluronate accumulation along the proximodistal axis of the embryonic chick limb bud. J Embryol Exp Morphol. 1981 Jun;63:85–98. [PubMed] [Google Scholar]
  18. Kosher R. A., Walker K. H., Ledger P. W. Temporal and spatial distribution of fibronectin during development of the embryonic chick limb bud. Cell Differ. 1982 Jun;11(4):217–228. doi: 10.1016/0045-6039(82)90069-0. [DOI] [PubMed] [Google Scholar]
  19. Kosher R. A., Walker K. H. The effect of prostaglandins on in vitro limb cartilage differentiation. Exp Cell Res. 1983 Apr 15;145(1):145–153. doi: 10.1016/s0014-4827(83)80016-0. [DOI] [PubMed] [Google Scholar]
  20. Kravis D., Upholt W. B. Quantitation of type II procollagen mRNA levels during chick limb cartilage differentiation. Dev Biol. 1985 Mar;108(1):164–172. doi: 10.1016/0012-1606(85)90018-1. [DOI] [PubMed] [Google Scholar]
  21. Lehrach H., Frischauf A. M., Hanahan D., Wozney J., Fuller F., Crkvenjakov R., Boedtker H., Doty P. Construction and characterization of a 2.5-kilobase procollagen clone. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5417–5421. doi: 10.1073/pnas.75.11.5417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Linsenmayer T. F. Temporal and spatial transitions in collagen types during embryonic chick limb development. II. Comparison of the embryonic cartilage collagen molecule with that from adult cartilage. Dev Biol. 1974 Oct;40(2):372–377. doi: 10.1016/0012-1606(74)90138-9. [DOI] [PubMed] [Google Scholar]
  23. Merlino G. T., McKeon C., de Crombrugghe B., Pastan I. Regulation of the expression of genes encoding types I, II, and III collagen during chick embryonic development. J Biol Chem. 1983 Aug 25;258(16):10041–10048. [PubMed] [Google Scholar]
  24. Mohun T. J., Brennan S., Dathan N., Fairman S., Gurdon J. B. Cell type-specific activation of actin genes in the early amphibian embryo. Nature. 1984 Oct 25;311(5988):716–721. doi: 10.1038/311716a0. [DOI] [PubMed] [Google Scholar]
  25. Newman S. A., Pautou M. P., Kieny M. The distal boundary of myogenic primordia in chimeric avian limb buds and its relation to an accessible population of cartilage progenitor cells. Dev Biol. 1981 Jun;84(2):440–448. doi: 10.1016/0012-1606(81)90413-9. [DOI] [PubMed] [Google Scholar]
  26. Saxe S. A., Lukens L. N., Pawlowski P. J. Changes in the nuclear and cytoplasmic levels of type I and type II collagen RNAs during growth of chondrocytes in 5-bromo-2'-deoxyuridine. J Biol Chem. 1985 Mar 25;260(6):3812–3819. [PubMed] [Google Scholar]
  27. Solursh M., Reiter R. S., Ahrens P. B., Vertel B. M. Stage- and position-related changes in chondrogenic response of chick embryonic wing mesenchyme to treatment with dibutyryl cyclic AMP. Dev Biol. 1981 Apr 15;83(1):9–19. doi: 10.1016/s0012-1606(81)80003-6. [DOI] [PubMed] [Google Scholar]
  28. Solursh M., Reiter R., Ahrens P. B., Pratt R. M. Increase in levels of cyclic AMP during avian limb chondrogenesis in vitro. Differentiation. 1979;15(3):183–186. doi: 10.1111/j.1432-0436.1979.tb01049.x. [DOI] [PubMed] [Google Scholar]
  29. Tomasek J. J., Mazurkiewicz J. E., Newman S. A. Nonuniform distribution of fibronectin during avian limb development. Dev Biol. 1982 Mar;90(1):118–126. doi: 10.1016/0012-1606(82)90217-2. [DOI] [PubMed] [Google Scholar]
  30. Vuorio E. I., Schaefer I. M., Vuorio T. K., Dorfman A., Upholt W. B. Construction and partial characterization of recombinant cDNA clones for chicken type I collagen messenger RNAs. Acta Chem Scand B. 1984;38(3):237–241. doi: 10.3891/acta.chem.scand.38b-0237. [DOI] [PubMed] [Google Scholar]
  31. Vuorio E., Sandell L., Kravis D., Sheffield V. C., Vuorio T., Dorfman A., Upholt W. B. Construction and partial characterization of two recombinant cDNA clones for procollagen from chicken cartilage. Nucleic Acids Res. 1982 Feb 25;10(4):1175–1192. doi: 10.1093/nar/10.4.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. White B. A., Bancroft F. C. Cytoplasmic dot hybridization. Simple analysis of relative mRNA levels in multiple small cell or tissue samples. J Biol Chem. 1982 Aug 10;257(15):8569–8572. [PubMed] [Google Scholar]
  33. Zanetti N. C., Solursh M. Induction of chondrogenesis in limb mesenchymal cultures by disruption of the actin cytoskeleton. J Cell Biol. 1984 Jul;99(1 Pt 1):115–123. doi: 10.1083/jcb.99.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. von der Mark K. Immunological studies on collagen type transition in chondrogenesis. Curr Top Dev Biol. 1980;14(Pt 2):199–225. doi: 10.1016/s0070-2153(08)60195-7. [DOI] [PubMed] [Google Scholar]

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

RESOURCES