Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1986 May 1;102(5):1931–1939. doi: 10.1083/jcb.102.5.1931

On the role of type IX collagen in the extracellular matrix of cartilage: type IX collagen is localized to intersections of collagen fibrils

PMCID: PMC2114213  PMID: 3517011

Abstract

The tissue distribution of type II and type IX collagen in 17-d-old chicken embryo was studied by immunofluorescence using polyclonal antibodies against type II collagen and a peptic fragment of type IX collagen (HMW), respectively. Both proteins were found only in cartilage where they were co-distributed. They occurred uniformly throughout the extracellular matrix, i.e., without distinction between pericellular, territorial, and interterritorial matrices. Tissues that undergo endochondral bone formation contained type IX collagen, whereas periosteal and membranous bones were negative. The thin collagenous fibrils in cartilage consisted of type II collagen as determined by immunoelectron microscopy. Type IX collagen was associated with the fibrils but essentially was restricted to intersections of the fibrils. These observations suggested that type IX collagen contributes to the stabilization of the network of thin fibers of the extracellular matrix of cartilage by interactions of its triple helical domains with several fibrils at or close to their intersections.

Full Text

The Full Text of this article is available as a PDF (4.6 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. Bruckner P., Mayne R., Tuderman L. p-HMW-collagen, a minor collagen obtained from chick embryo cartilage without proteolytic treatment of the tissue. Eur J Biochem. 1983 Nov 2;136(2):333–339. doi: 10.1111/j.1432-1033.1983.tb07746.x. [DOI] [PubMed] [Google Scholar]
  3. Bruckner P., Vaughan L., Winterhalter K. H. Type IX collagen from sternal cartilage of chicken embryo contains covalently bound glycosaminoglycans. Proc Natl Acad Sci U S A. 1985 May;82(9):2608–2612. doi: 10.1073/pnas.82.9.2608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Capasso O., Tajana G., Cancedda R. Location of 64K collagen producer chondrocytes in developing chicken embryo tibiae. Mol Cell Biol. 1984 Jun;4(6):1163–1168. doi: 10.1128/mcb.4.6.1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Comper W. D., Laurent T. C. Physiological function of connective tissue polysaccharides. Physiol Rev. 1978 Jan;58(1):255–315. doi: 10.1152/physrev.1978.58.1.255. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Eggli P. S., Herrmann W., Hunziker E. B., Schenk R. K. Matrix compartments in the growth plate of the proximal tibia of rats. Anat Rec. 1985 Mar;211(3):246–257. doi: 10.1002/ar.1092110304. [DOI] [PubMed] [Google Scholar]
  8. Eikenberry E. F., Childs B., Sheren S. B., Parry D. A., Craig A. S., Brodsky B. Crystalline fibril structure of type II collagen in lamprey notochord sheath. J Mol Biol. 1984 Jun 25;176(2):261–277. doi: 10.1016/0022-2836(84)90424-8. [DOI] [PubMed] [Google Scholar]
  9. Evans H. B., Ayad S., Abedin M. Z., Hopkins S., Morgan K., Walton K. W., Weiss J. B., Holt P. J. Localisation of collagen types and fibronectin in cartilage by immunofluorescence. Ann Rheum Dis. 1983 Oct;42(5):575–581. doi: 10.1136/ard.42.5.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Franklin R. M. Immunohistochemistry on semi-thin sections of hydroxypropyl methacrylate embedded tissues. J Immunol Methods. 1984 Mar 30;68(1-2):61–72. doi: 10.1016/0022-1759(84)90137-6. [DOI] [PubMed] [Google Scholar]
  11. Gibson G. J., Flint M. H. Type X collagen synthesis by chick sternal cartilage and its relationship to endochondral development. J Cell Biol. 1985 Jul;101(1):277–284. doi: 10.1083/jcb.101.1.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Hartmann D. J., Magloire H., Ricard-Blum S., Joffre A., Couble M. L., Ville G., Herbage D. Light and electron immunoperoxidase localization of minor disulfide-bonded collagens in fetal calf epiphyseal cartilage. Coll Relat Res. 1983 Jul;3(4):349–357. doi: 10.1016/s0174-173x(83)80016-8. [DOI] [PubMed] [Google Scholar]
  14. Heinegård D., Björne-Persson A., Cöster L., Franzén A., Gardell S., Malmström A., Paulsson M., Sandfalk R., Vogel K. The core proteins of large and small interstitial proteoglycans from various connective tissues form distinct subgroups. Biochem J. 1985 Aug 15;230(1):181–194. doi: 10.1042/bj2300181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Horisberger M., Rosset J. Colloidal gold, a useful marker for transmission and scanning electron microscopy. J Histochem Cytochem. 1977 Apr;25(4):295–305. doi: 10.1177/25.4.323352. [DOI] [PubMed] [Google Scholar]
  16. Irwin M. H., Silvers S. H., Mayne R. Monoclonal antibody against chicken type IX collagen: preparation, characterization, and recognition of the intact form of type IX collagen secreted by chondrocytes. J Cell Biol. 1985 Sep;101(3):814–823. doi: 10.1083/jcb.101.3.814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lee S. L., Piez K. A. Type II collagen from lathyritic rat chondrosarcoma: preparation and in vitro fibril formation. Coll Relat Res. 1983 Mar;3(2):89–103. doi: 10.1016/s0174-173x(83)80036-3. [DOI] [PubMed] [Google Scholar]
  18. Lennette D. A. An improved mounting medium for immunofluorescence microscopy. Am J Clin Pathol. 1978 Jun;69(6):647–648. doi: 10.1093/ajcp/69.6.647. [DOI] [PubMed] [Google Scholar]
  19. Linsenmayer T. F., Fitch J. M., Schmid T. M., Zak N. B., Gibney E., Sanderson R. D., Mayne R. Monoclonal antibodies against chicken type V collagen: production, specificity, and use for immunocytochemical localization in embryonic cornea and other organs. J Cell Biol. 1983 Jan;96(1):124–132. doi: 10.1083/jcb.96.1.124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lozano G., Ninomiya Y., Thompson H., Olsen B. R. A distinct class of vertebrate collagen genes encodes chicken type IX collagen polypeptides. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4050–4054. doi: 10.1073/pnas.82.12.4050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mayne R., van der Rest M., Weaver D. C., Butler W. T. The structure of a small collagenous fragment isolated from chicken hyaline cartilage. J Cell Biochem. 1985;27(2):133–141. doi: 10.1002/jcb.240270207. [DOI] [PubMed] [Google Scholar]
  22. Ninomiya Y., Olsen B. R. Synthesis and characterization of cDNA encoding a cartilage-specific short collagen. Proc Natl Acad Sci U S A. 1984 May;81(10):3014–3018. doi: 10.1073/pnas.81.10.3014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ninomiya Y., van der Rest M., Mayne R., Lozano G., Olsen B. R. Construction and characterization of cDNA encoding the alpha 2 chain of chicken type IX collagen. Biochemistry. 1985 Jul 16;24(15):4223–4229. doi: 10.1021/bi00336a061. [DOI] [PubMed] [Google Scholar]
  24. Noro A., Kimata K., Oike Y., Shinomura T., Maeda N., Yano S., Takahashi N., Suzuki S. Isolation and characterization of a third proteoglycan (PG-Lt) from chick embryo cartilage which contains disulfide-bonded collagenous polypeptide. J Biol Chem. 1983 Aug 10;258(15):9323–9331. [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. 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]
  28. Schmid T. M., Linsenmayer T. F. Immunohistochemical localization of short chain cartilage collagen (type X) in avian tissues. J Cell Biol. 1985 Feb;100(2):598–605. doi: 10.1083/jcb.100.2.598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Smith G. N., Jr, Williams J. M., Brandt K. D. Interaction of proteoglycans with the pericellular (1 alpha, 2 alpha, 3 alpha) collagens of cartilage. J Biol Chem. 1985 Sep 5;260(19):10761–10767. [PubMed] [Google Scholar]
  31. Vaughan L., Winterhalter K. H., Bruckner P. Proteoglycan Lt from chicken embryo sternum identified as type IX collagen. J Biol Chem. 1985 Apr 25;260(8):4758–4763. [PubMed] [Google Scholar]
  32. Zeller R., Nyffenegger T., De Robertis E. M. Nucleocytoplasmic distribution of snRNPs and stockpiled snRNA-binding proteins during oogenesis and early development in Xenopus laevis. Cell. 1983 Feb;32(2):425–434. doi: 10.1016/0092-8674(83)90462-2. [DOI] [PubMed] [Google Scholar]
  33. van der Rest M., Mayne R., Ninomiya Y., Seidah N. G., Chretien M., Olsen B. R. The structure of type IX collagen. J Biol Chem. 1985 Jan 10;260(1):220–225. [PubMed] [Google Scholar]
  34. von der Mark K. Localization of collagen types in tissues. Int Rev Connect Tissue Res. 1981;9:265–324. doi: 10.1016/b978-0-12-363709-3.50012-7. [DOI] [PubMed] [Google Scholar]
  35. von der Mark K., van Menxel M., Wiedemann H. Isolation and characterization of a precursor form of M collagen from embryonic chicken cartilage. Eur J Biochem. 1984 Feb 1;138(3):629–633. doi: 10.1111/j.1432-1033.1984.tb07961.x. [DOI] [PubMed] [Google Scholar]
  36. 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