Skip to main content
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1974 Dec;54(6):1480–1487. doi: 10.1172/JCI107896

The Role of Collagen Quaternary Structure in the Platelet:Collagen Interaction

Lawrence F Brass 1, Howard B Bensusan 1
PMCID: PMC301704  PMID: 4215825

Abstract

We have investigated whether collagen queternary structure is required for the platelet: collagen interaction. Quaternary structure refers to the assembly of collagen monomers (tropocollagen) into polymers (native-type fibrils). Purified monomeric collagen was prepared from acetic acid extracts of fetal calfskin. Polymeric collagen was prepared by dispersion of bovine Achilles tendon collagen and by incubation of monomeric collagen at 37°C and pH 7.4. The state of polymerization was confirmed by electron microscopy. Release of platelet serotonin in the absence of platelet aggregation was used to determine the effectiveness of the platelet: collagen interaction. All forms of collagen produced serotonin release only after a lag period, but polymeric collagen gave a shorter lag period than did monomeric collagen. Monomeric collagen was also quanidinated selectively to convert collagen lysine groups to homoarginine, while leaving the arrangement of polar groups intact. Guanidination of monomeric collagen increased the rate of polymerization and reduced the lag time in serotonin release. Glucosamine (17 mM) retarded polymerization and inhibited the release of platelet serotonin by monomeric collagen but had little effect on release produced by thrombin or polymeric collagen. At the same concentration, glucosamine did not reduce the sensitivity of platelets to stimulation by collagen or block the platelet: collagen interaction. The only effect of glucosamine was on the collagen: collagen interaction. Galactosamine had a similar effect, but glucose, galactose, and N-acetylglycosamine had no effect. We conclude from this data that collagen monomers cannot effectively interact with platelets and that, therefore, collagen quaternary structure has a role in the recognition of collagen by platelets.

Full text

PDF
1487

Selected References

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

  1. Ardlie N. G., Perry D. W., Packham M. A., Mustard J. F. Influence of apyrase on stability of suspensions of washed rabbit platelets. Proc Soc Exp Biol Med. 1971 Apr;136(4):1021–1023. doi: 10.3181/00379727-136-35419. [DOI] [PubMed] [Google Scholar]
  2. BENSUSAN H. B., MUMAW V. R., SCANU A. W. Fiber formation from solutions of collagen. IV. On the role of the basic amino acid residues. Biochemistry. 1962 Mar;1:215–223. doi: 10.1021/bi00908a004. [DOI] [PubMed] [Google Scholar]
  3. Barber A. J., Jamieson G. A. Characterization of membrane-bound collagen galactosyltransferase of human blood platelets. Biochim Biophys Acta. 1971 Dec 21;252(3):546–552. doi: 10.1016/0304-4165(71)90157-7. [DOI] [PubMed] [Google Scholar]
  4. Bosmann H. B. Platelet adhesiveness and aggregation: the collagen:glycosyl, polypeptide:N-acetylgalactosaminyl and glycoprotein:galactosyl transferases of human platelets. Biochem Biophys Res Commun. 1971 Jun 4;43(5):1118–1124. doi: 10.1016/0006-291x(71)90578-x. [DOI] [PubMed] [Google Scholar]
  5. Chesney C. M., Harper E., Colman R. W. Critical role of the carbohydrate side chains of collagen in platelet aggregation. J Clin Invest. 1972 Oct;51(10):2693–2701. doi: 10.1172/JCI107088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gross J., Highberger J. H., Schmitt F. O. COLLAGEN STRUCTURES CONSIDERED AS STATES OF AGGREGATION OF A KINETIC UNIT. THE TROPOCOLLAGEN PARTICLE. Proc Natl Acad Sci U S A. 1954 Aug;40(8):679–688. doi: 10.1073/pnas.40.8.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hodge A. J., Schmitt F. O. THE CHARGE PROFILE OF THE TROPOCOLLAGEN MACROMOLECULE AND THE PACKING ARRANGEMENT IN NATIVE-TYPE COLLAGEN FIBRILS. Proc Natl Acad Sci U S A. 1960 Feb;46(2):186–197. doi: 10.1073/pnas.46.2.186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Holmsen H., Day H. J., Stormorken H. The blood platelet release reaction. Scand J Haematol Suppl. 1969;8:3–26. [PubMed] [Google Scholar]
  9. Holmsen H., Ostvold A. C., Day H. J. Behaviour of endogenous and newly absorbed serotonin in the platelet release reaction. Biochem Pharmacol. 1973 Oct 15;22(20):2599–2608. doi: 10.1016/0006-2952(73)90068-3. [DOI] [PubMed] [Google Scholar]
  10. Jaffe R., Deykin D. Evidence for a structural requirement for the aggregation of platelets by collagen. J Clin Invest. 1974 Mar;53(3):875–883. doi: 10.1172/JCI107628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jamieson G. A., Urban C. L., Barber A. J. Enzymatic basis for platelet: collagen adhesion as the primary step in haemostasis. Nat New Biol. 1971 Nov 3;234(44):5–7. doi: 10.1038/newbio234005a0. [DOI] [PubMed] [Google Scholar]
  12. Kang A. H., Beachey E. H., Katzman R. L. Interaction of an active glycopeptide from chick skin collagen (alpha 1-CB5) with human platelets. J Biol Chem. 1974 Feb 25;249(4):1054–1059. [PubMed] [Google Scholar]
  13. Katzman R. L., Kang A. H., Beachey E. H. Collagen-induced platelet aggregation: involement of an active glycopeptide fragment (alpha1-CB5). Science. 1973 Aug 17;181(4100):670–672. doi: 10.1126/science.181.4100.670. [DOI] [PubMed] [Google Scholar]
  14. Legrand Y., Caen J. P., Robert L. Effect of glucosamine on platelet-collagen reaction. Proc Soc Exp Biol Med. 1968 Mar;127(3):941–943. doi: 10.3181/00379727-127-32840. [DOI] [PubMed] [Google Scholar]
  15. Massini P., Lüscher E. F. The induction of the release reaction in human blood platelets by close cell contact. Thromb Diath Haemorrh. 1971;25(1):13–20. [PubMed] [Google Scholar]
  16. Mills D. C., Robb I. A., Roberts G. C. The release of nucleotides, 5-hydroxytryptamine and enzymes from human blood platelets during aggregation. J Physiol. 1968 Apr;195(3):715–729. doi: 10.1113/jphysiol.1968.sp008484. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mustard J. F., Packham M. A. Factors influencing platelet function: adhesion, release, and aggregation. Pharmacol Rev. 1970 Jun;22(2):97–187. [PubMed] [Google Scholar]
  18. Mustard J. F., Perry D. W., Ardlie N. G., Packham M. A. Preparation of suspensions of washed platelets from humans. Br J Haematol. 1972 Feb;22(2):193–204. doi: 10.1111/j.1365-2141.1972.tb08800.x. [DOI] [PubMed] [Google Scholar]
  19. Nossel H. L., Wilner G. D., LeRoy E. C. Importances of polar groups for initiating blood coagulation and aggregating platelets. Nature. 1969 Jan 4;221(5175):75–76. doi: 10.1038/221075a0. [DOI] [PubMed] [Google Scholar]
  20. Packham M. A., Guccione M. A., Chang P. L., Mustard J. F. Platelet aggregation and release: effects of low concentrations of thrombin or collagen. Am J Physiol. 1973 Jul;225(1):38–47. doi: 10.1152/ajplegacy.1973.225.1.38. [DOI] [PubMed] [Google Scholar]
  21. Puett D., Wasserman B. K., Ford J. D., Cunningham L. W. Collagen-mediated platelet aggregation. Effects of collagen modification involving the protein and carbohydrate moieties. J Clin Invest. 1973 Oct;52(10):2495–2506. doi: 10.1172/JCI107440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. WOOD G. C., KEECH M. K. The formation of fibrils from collagen solutions. 1. The effect of experimental conditions: kinetic and electron-microscope studies. Biochem J. 1960 Jun;75:588–598. doi: 10.1042/bj0750588. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. WOOD G. C. The formation of fibrils from collagen solutions. 2. A mechanism of collagen-fibril formation. Biochem J. 1960 Jun;75:598–605. doi: 10.1042/bj0750598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wilner G. D., Nossel H. L., LeRoy E. C. Aggregation of platelets by collagen. J Clin Invest. 1968 Dec;47(12):2616–2621. doi: 10.1172/JCI105944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wilner G. D., Nossel H. L., Procupez T. L. Aggregation of platelets by collagen: polar active sites of insoluble human collagen. Am J Physiol. 1971 Apr;220(4):1074–1079. doi: 10.1152/ajplegacy.1971.220.4.1074. [DOI] [PubMed] [Google Scholar]
  26. Wolfe S. M., Shulman N. R. Inhibition of platelet energy production and release reaction by PGE1, theophylline and cAMP. Biochem Biophys Res Commun. 1970 Oct 9;41(1):128–134. doi: 10.1016/0006-291x(70)90478-x. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES