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. 1991 Jan 1;273(Pt 1):141–148. doi: 10.1042/bj2730141

Isolation of cDNAs encoding the complete sequence of bovine type X collagen. Evidence for the condensed nature of mammalian type X collagen genes.

J T Thomas 1, A P Kwan 1, M E Grant 1, R P Boot-Handford 1
PMCID: PMC1149890  PMID: 1703407

Abstract

The complete primary structure of the bovine alpha 1(X) collagen chain was determined by nucleotide sequencing of cDNA clones. The overlapping cDNA clones encode 3144 bp with a 5'-terminal untranslated region of 148 bp, a 2025 bp reading frame and a 3'-terminal untranslated region of 971 bp. This represents the first complete sequence of a mammalian type X collagen cDNA and has allowed a number of informative comparisons to be made with the previously published chick alpha 1(X) sequence. The primary translation products of both bovine and chick type X collagen are 674 amino acid residues in length and there is a 73.3% identity at the amino acid level (67.8% at the base level). Sequence analyses reveal that the greatest degree of identity between the two species occurs within the triple-helical domain and the C-terminal non-collagenous domain, whereas the identity within the N-terminal non-collagenous domain is markedly lower. The interchain disulphide-bonding observed previously within the triple helix of bovine type X collagen is explained by the presence of two cysteine residues within an imperfection of the triple-helical domain encoded by -Gly-Xaa-Cys-Xaa-Yaa-Cys-Xaa-Yaa-Gly-. Southern blot analyses of bovine genomic DNA demonstrate that the bovine type X collagen gene is likely to have a condensed structure, similar to that of the chick, with at least 1.3 kb of the coding sequence being contained within one exon.

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Selected References

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

  1. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ayad S., Kwan A. P., Grant M. E. Partial characterization of type X collagen from bovine growth-plate cartilage. Evidence that type X collagen is processed in vivo. FEBS Lett. 1987 Aug 10;220(1):181–186. doi: 10.1016/0014-5793(87)80899-2. [DOI] [PubMed] [Google Scholar]
  3. Baldwin C. T., Reginato A. M., Smith C., Jimenez S. A., Prockop D. J. Structure of cDNA clones coding for human type II procollagen. The alpha 1(II) chain is more similar to the alpha 1(I) chain than two other alpha chains of fibrillar collagens. Biochem J. 1989 Sep 1;262(2):521–528. doi: 10.1042/bj2620521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bird A. P. CpG-rich islands and the function of DNA methylation. Nature. 1986 May 15;321(6067):209–213. doi: 10.1038/321209a0. [DOI] [PubMed] [Google Scholar]
  5. Boot-Handford R. P., Kurkinen M., Prockop D. J. Steady-state levels of mRNAs coding for the type IV collagen and laminin polypeptide chains of basement membranes exhibit marked tissue-specific stoichiometric variations in the rat. J Biol Chem. 1987 Sep 15;262(26):12475–12478. [PubMed] [Google Scholar]
  6. Caplan A. I. Bone development. Ciba Found Symp. 1988;136:3–21. doi: 10.1002/9780470513637.ch2. [DOI] [PubMed] [Google Scholar]
  7. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  8. Gadher S. J., Eyre D. R., Duance V. C., Wotton S. F., Heck L. W., Schmid T. M., Woolley D. E. Susceptibility of cartilage collagens type II, IX, X, and XI to human synovial collagenase and neutrophil elastase. Eur J Biochem. 1988 Jul 15;175(1):1–7. doi: 10.1111/j.1432-1033.1988.tb14158.x. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Goblet C., Prost E., Whalen R. G. One-step amplification of transcripts in total RNA using the polymerase chain reaction. Nucleic Acids Res. 1989 Mar 11;17(5):2144–2144. doi: 10.1093/nar/17.5.2144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Grant W. T., Sussman M. D., Balian G. A disulfide-bonded short chain collagen synthesized by degenerative and calcifying zones of bovine growth plate cartilage. J Biol Chem. 1985 Mar 25;260(6):3798–3803. [PubMed] [Google Scholar]
  12. Kielty C. M., Hulmes D. J., Schor S. L., Grant M. E. Embryonic chick cartilage collagens. Differences in the low-Mr species present in sternal cartilage and tibiotarsal articular cartilage. FEBS Lett. 1984 Apr 24;169(2):179–184. doi: 10.1016/0014-5793(84)80314-2. [DOI] [PubMed] [Google Scholar]
  13. Kirsch T., von der Mark K. Isolation of bovine type X collagen and immunolocalization in growth-plate cartilage. Biochem J. 1990 Jan 15;265(2):453–459. doi: 10.1042/bj2650453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kwan A. P., Freemont A. J., Grant M. E. Immunoperoxidase localization of type X collagen in chick tibiae. Biosci Rep. 1986 Feb;6(2):155–162. doi: 10.1007/BF01115001. [DOI] [PubMed] [Google Scholar]
  15. Kwan A. P., Sear C. H., Grant M. E. Identification of disulphide-bonded type X procollagen polypeptides in embryonic chick chondrocyte cultures. FEBS Lett. 1986 Oct 6;206(2):267–272. doi: 10.1016/0014-5793(86)80994-2. [DOI] [PubMed] [Google Scholar]
  16. LuValle P., Ninomiya Y., Rosenblum N. D., Olsen B. R. The type X collagen gene. Intron sequences split the 5'-untranslated region and separate the coding regions for the non-collagenous amino-terminal and triple-helical domains. J Biol Chem. 1988 Dec 5;263(34):18378–18385. [PubMed] [Google Scholar]
  17. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  18. Ninomiya Y., Gordon M., van der Rest M., Schmid T., Linsenmayer T., Olsen B. R. The developmentally regulated type X collagen gene contains a long open reading frame without introns. J Biol Chem. 1986 Apr 15;261(11):5041–5050. [PubMed] [Google Scholar]
  19. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Schmid T. M., Mayne R., Jeffrey J. J., Linsenmayer T. F. Type X collagen contains two cleavage sites for a vertebrate collagenase. J Biol Chem. 1986 Mar 25;261(9):4184–4189. [PubMed] [Google Scholar]
  22. Thomas J. T., Boot-Handford R. P., Grant M. E. Modulation of type X collagen gene expression by calcium beta-glycerophosphate and levamisole: implications for a possible role for type X collagen in endochondral bone formation. J Cell Sci. 1990 Apr;95(Pt 4):639–648. doi: 10.1242/jcs.95.4.639. [DOI] [PubMed] [Google Scholar]
  23. Vänänen H. K. Immunohistochemical localization of alkaline phosphatase in the chicken epiphyseal growth cartilage. Histochemistry. 1980 Feb;65(2):143–148. doi: 10.1007/BF00493162. [DOI] [PubMed] [Google Scholar]
  24. Watson M. E. Compilation of published signal sequences. Nucleic Acids Res. 1984 Jul 11;12(13):5145–5164. doi: 10.1093/nar/12.13.5145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yamaguchi N., Benya P. D., van der Rest M., Ninomiya Y. The cloning and sequencing of alpha 1(VIII) collagen cDNAs demonstrate that type VIII collagen is a short chain collagen and contains triple-helical and carboxyl-terminal non-triple-helical domains similar to those of type X collagen. J Biol Chem. 1989 Sep 25;264(27):16022–16029. [PubMed] [Google Scholar]

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