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. 1984 Jun 1;220(2):385–394. doi: 10.1042/bj2200385

Collagen heterogeneity and quantification in developing bovine nuchal ligament.

C A Chambers, C A Shuttleworth, S Ayad, M E Grant
PMCID: PMC1153639  PMID: 6430281

Abstract

The collagenous components were investigated in peptic digests of developing bovine nuchal ligament. Types I and III collagen were the major species isolated, but the presence of types IV, V and VI was also shown. Changes in the pepsin-susceptibility of nuchal ligament during foetal development were observed. CNBr-cleavage peptide analysis indicated that type I collagen became cross-linked rapidly, as evidenced by the lack of alpha 1(I)CB6. At present it is not clear if this decrease in pepsin-susceptibility is due to cross-linking of collagen, to increased deposition of elastin, or to both. Quantification of collagen types I and III was shown to depend on the method used. When pepsin-solubilized material was examined an apparent increase in type III collagen with respect to foetal age was observed, whereas when CNBr digests of intact ligament were examined a relatively constant amount of type III collagen (approx. 24%) was found. The constant amount of type III collagen observed during foetal development changed at birth and increased in mature nuchal ligament to represent approx. 45% of the total collagen.

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Selected References

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

  1. Abedin M. Z., Ayad S., Weiss J. B. Isolation and native characterization of cysteine-rich collagens from bovine placental tissues and uterus and their relationship to types IV and V collagens. Biosci Rep. 1982 Jul;2(7):493–502. doi: 10.1007/BF01115247. [DOI] [PubMed] [Google Scholar]
  2. Birembaut P., Legrand Y. J., Bariety J., Bretton R., Fauvel F., Belair M. F., Pignaud G., Caen J. P. Histochemical and ultrastructural characterization of subendothelial glycoprotein microfibrils interacting with platelets. J Histochem Cytochem. 1982 Jan;30(1):75–80. doi: 10.1177/30.1.6274953. [DOI] [PubMed] [Google Scholar]
  3. Chung E., Miller E. J. Collagen polymorphism: characterization of molecules with the chain composition (alpha 1 (3)03 in human tissues. Science. 1974 Mar;183(130):1200–1201. doi: 10.1126/science.183.4130.1200. [DOI] [PubMed] [Google Scholar]
  4. Chung E., Rhodes K., Miller E. J. Isolation of three collagenous components of probable basement membrane origin from several tissues. Biochem Biophys Res Commun. 1976 Aug 23;71(4):1167–1174. doi: 10.1016/0006-291x(76)90776-2. [DOI] [PubMed] [Google Scholar]
  5. Cleary E. G., Sandberg L. B., Jackson D. S. The changes in chemical composition during development of the bovine nuchal ligament. J Cell Biol. 1967 Jun;33(3):469–479. doi: 10.1083/jcb.33.3.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Davidson J. M., Smith K., Shibahara S., Tolstoshev P., Crystal R. G. Regulation of elastin synthesis in developing sheep nuchal ligament by elastin mRNA levels. J Biol Chem. 1982 Jan 25;257(2):747–754. [PubMed] [Google Scholar]
  7. Epstein E. H., Jr (Alpha1(3))3 human skin collagen. Release by pepsin digestion and preponderance in fetal life. J Biol Chem. 1974 May 25;249(10):3225–3231. [PubMed] [Google Scholar]
  8. Epstein E. H., Jr, Munderloh N. H. Isolation and characterization of CNBr peptides of human (alpha 1 (III) )3 collagen and tissue distribution of (alpha 1 (I) )2 alpha 2 and (alpha 1 (III) )3 collagens. J Biol Chem. 1975 Dec 25;250(24):9304–9312. [PubMed] [Google Scholar]
  9. Fairbanks G., Steck T. L., Wallach D. F. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry. 1971 Jun 22;10(13):2606–2617. doi: 10.1021/bi00789a030. [DOI] [PubMed] [Google Scholar]
  10. Faris B., Moscaritolo R., Levine A., Snider R., Goldstein R., Franzblau C. Isolation of purified insoluble aortic collagen. Biochim Biophys Acta. 1978 May 24;534(1):64–72. doi: 10.1016/0005-2795(78)90476-2. [DOI] [PubMed] [Google Scholar]
  11. Furthmayr H., Wiedemann H., Timpl R., Odermatt E., Engel J. Electron-microscopical approach to a structural model of intima collagen. Biochem J. 1983 May 1;211(2):303–311. doi: 10.1042/bj2110303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hanson A. N., Bentley J. P. Quantitation of type I to type III collagen ratios in small samples of human tendon, blood vessels, and atherosclerotic plaque. Anal Biochem. 1983 Apr 1;130(1):32–40. doi: 10.1016/0003-2697(83)90646-2. [DOI] [PubMed] [Google Scholar]
  13. Jander R., Rauterberg J., Glanville R. W. Further characterization of the three polypeptide chains of bovine and human short-chain collagen (intima collagen). Eur J Biochem. 1983 Jun 1;133(1):39–46. doi: 10.1111/j.1432-1033.1983.tb07427.x. [DOI] [PubMed] [Google Scholar]
  14. Jimenez S. A., Yankowski R., Bashey R. I. Identification of two new collagen alpha-chains in extracts of lathyritic chick embryo tendons. Biochem Biophys Res Commun. 1978 Apr 28;81(4):1298–1306. doi: 10.1016/0006-291x(78)91277-9. [DOI] [PubMed] [Google Scholar]
  15. Knight K. R., Ayad S., Shuttleworth C. A., Grant M. E. A collagenous glycoprotein found in dissociative extracts of foetal bovine nuchal ligament. Evidence for a relationship with type VI collagen. Biochem J. 1984 Jun 1;220(2):395–403. doi: 10.1042/bj2200395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Laurent G. J., Cockerill P., McAnulty R. J., Hastings J. R. A simplified method for quantitation of the relative amounts of type I and type III collagen in small tissue samples. Anal Biochem. 1981 May 15;113(2):301–312. doi: 10.1016/0003-2697(81)90081-6. [DOI] [PubMed] [Google Scholar]
  18. Light N. D., Bailey A. J. Changes in crosslinking during aging in bovine tendon collagen. FEBS Lett. 1979 Jan 1;97(1):183–188. doi: 10.1016/0014-5793(79)80080-0. [DOI] [PubMed] [Google Scholar]
  19. Light N. D. Estimation of types I and III collagens in whole tissue by quantitation of CNBr peptides on SDS-polyacrylamide gels. Biochim Biophys Acta. 1982 Mar 18;702(1):30–36. doi: 10.1016/0167-4838(82)90024-3. [DOI] [PubMed] [Google Scholar]
  20. Limeback H. F., Sodek J., Brunette D. M. Nature of collagens synthesized by monkey periodontal-ligament fibroblasts in vitro. Biochem J. 1978 Jan 15;170(1):63–71. doi: 10.1042/bj1700063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Matsui T., Iijima K., Myokei Y., Hayakawa T. Collagen-like peptides in crystalline pepsin preparations. Coll Relat Res. 1982 Nov;2(6):565–566. doi: 10.1016/s0174-173x(82)80010-1. [DOI] [PubMed] [Google Scholar]
  22. McCullagh K. A., Balian G. Collagen characterisation and cell transformation in human atherosclerosis. Nature. 1975 Nov 6;258(5530):73–75. doi: 10.1038/258073a0. [DOI] [PubMed] [Google Scholar]
  23. Mecham R. P. Effects of extracellular matrix upon elastogenesis. Connect Tissue Res. 1981;8(3-4):241–244. doi: 10.3109/03008208109152382. [DOI] [PubMed] [Google Scholar]
  24. Mecham R. P., Lange G., Madaras J., Starcher B. Elastin synthesis by ligamentum nuchae fibroblasts: effects of culture conditions and extracellular matrix on elastin production. J Cell Biol. 1981 Aug;90(2):332–338. doi: 10.1083/jcb.90.2.332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Odermatt E., Risteli J., van Delden V., Timpl R. Structural diversity and domain composition of a unique collagenous fragment (intima collagen) obtained from human placenta. Biochem J. 1983 May 1;211(2):295–302. doi: 10.1042/bj2110295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ross R., Bornstein P. The elastic fiber. I. The separation and partial characterization of its macromolecular components. J Cell Biol. 1969 Feb;40(2):366–381. doi: 10.1083/jcb.40.2.366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sage H., Pritzl P., Bornstein P. A unique, pepsin-sensitive collagen synthesized by aortic endothelial cells in culture. Biochemistry. 1980 Dec 9;19(25):5747–5755. doi: 10.1021/bi00566a013. [DOI] [PubMed] [Google Scholar]
  29. Scott P. G., Veis A. The cyanogen bromide peptides of bovine soluble and insoluble collagens. II. Tissue specific cross-linked peptides of insoluble skin and dentin collagen. Connect Tissue Res. 1976;4(2):117–129. doi: 10.3109/03008207609152207. [DOI] [PubMed] [Google Scholar]
  30. Sear C. H., Grant M. E., Jackson D. S. The nature of the microfibrillar glycoproteins of elastic fibres. A biosynthetic study. Biochem J. 1981 Feb 15;194(2):587–598. doi: 10.1042/bj1940587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sear C. H., Jones C. J., Knight K. R., Grant M. E. Elastogenesis and microfibrillar glycoprotein synthesis by bovine ligamentum nuchae cells in culture. Connect Tissue Res. 1981;8(3-4):167–170. doi: 10.3109/03008208109152368. [DOI] [PubMed] [Google Scholar]
  32. Sear C. H., Kewley M. A., Jones C. J., Grant M. E., Jackson D. S. The identification of glycoproteins associated with elastic-tissue microfibrils. Biochem J. 1978 Mar 15;170(3):715–718. doi: 10.1042/bj1700715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Seyer J. M., Kang A. H., Rodnan G. Investigation of type I and type III collagens of the lung in progressive systemic sclerosis. Arthritis Rheum. 1981 Apr;24(4):625–631. doi: 10.1002/art.1780240410. [DOI] [PubMed] [Google Scholar]
  34. Shuttleworth C. A., Ward J. L., Hirschmann P. N. The presence of type III collagen in the developing tooth. Biochim Biophys Acta. 1978 Aug 21;535(2):348–355. doi: 10.1016/0005-2795(78)90101-0. [DOI] [PubMed] [Google Scholar]
  35. Stegemann H., Stalder K. Determination of hydroxyproline. Clin Chim Acta. 1967 Nov;18(2):267–273. doi: 10.1016/0009-8981(67)90167-2. [DOI] [PubMed] [Google Scholar]
  36. Sykes B., Puddle B., Francis M., Smith R. The estimation of two collagens from human dermis by interrupted gel electrophoresis. Biochem Biophys Res Commun. 1976 Oct 18;72(4):1472–1480. doi: 10.1016/s0006-291x(76)80180-5. [DOI] [PubMed] [Google Scholar]
  37. Trelstad R. L. Human aorta collagens: evidence for three distinct species. Biochem Biophys Res Commun. 1974 Apr 8;57(3):717–725. doi: 10.1016/0006-291x(74)90605-6. [DOI] [PubMed] [Google Scholar]
  38. Weber L., Meigel W. N., Rauterberg J. SDS-polyacrylamide gel electrophoretic determination of type I and type III collagen in small skin samples. Arch Dermatol Res. 1977 May 27;258(3):251–257. doi: 10.1007/BF00561127. [DOI] [PubMed] [Google Scholar]
  39. Wirtschafter Z. T., Cleary E. G., Jackson D. S., Sandberg L. B. Histological changes during the development of the bovine nuchal ligament. J Cell Biol. 1967 Jun;33(3):481–488. doi: 10.1083/jcb.33.3.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. van Amerongen J. P., Lemmens I. G., Tonino G. J. The concentration, extractability and characterization of collagen in human dental pulp. Arch Oral Biol. 1983;28(4):339–345. doi: 10.1016/0003-9969(83)90076-6. [DOI] [PubMed] [Google Scholar]

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