Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 1992 May 15;284(Pt 1):103–108. doi: 10.1042/bj2840103

Binding of human plasminogen to basement-membrane (type IV) collagen.

M S Stack 1, T L Moser 1, S V Pizzo 1
PMCID: PMC1132703  PMID: 1599390

Abstract

Plasminogen, the zymogen form of the serine proteinase plasmin, has been implicated in numerous physiological and pathological processes involving extracellular-matrix remodelling. We have previously demonstrated that the activation of plasminogen catalysed by tissue plasminogen activator is dramatically stimulated in the presence of basement-membrane-specific type IV collagen [Stack, Gonzalez-Gronow & Pizzo (1990) Biochemistry 29, 4966-4970]. The present paper describes the binding of plasminogen to type IV collagen. Plasminogen binds to both the alpha 1(IV) and alpha 2(IV) chains of basement-membrane collagen, with binding to the alpha 2(IV) chain preferentially inhibited by 6-aminohexanoic acid. This binding is specific and saturable, with Kd,app. values of 11.5 and 12.7 nM for collagen and gelatin respectively. Although collagen also binds to immobilized plasminogen, this interaction is unaffected by 6-aminohexanoic acid. Limited elastase proteolysis of plasminogen generated distinct collagen-binding fragments, which were identified as the kringle 1-3 and kringle 4 domains. No binding of collagen to mini-plasminogen was observed. These studies demonstrate a specific interaction between plasminogen and type IV collagen and provide further evidence for regulation of plasminogen activation by protein components of the extracellular matrix.

Full text

PDF
108

Images in this article

104Fig. 1.
on p.104
105Fig. 2.
on p.105
105Fig. 3.
on p.105
105Fig. 4.
on p.105

Selected References

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

  1. Bányai L., Patthy L. Evidence for the involvement of type II domains in collagen binding by 72 kDa type IV procollagenase. FEBS Lett. 1991 Apr 22;282(1):23–25. doi: 10.1016/0014-5793(91)80436-7. [DOI] [PubMed] [Google Scholar]
  2. Christensen U. The AH-site of plasminogen and two C-terminal fragments. A weak lysine-binding site preferring ligands not carrying a free carboxylate function. Biochem J. 1984 Oct 15;223(2):413–421. doi: 10.1042/bj2230413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Collier I. E., Wilhelm S. M., Eisen A. Z., Marmer B. L., Grant G. A., Seltzer J. L., Kronberger A., He C. S., Bauer E. A., Goldberg G. I. H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloprotease capable of degrading basement membrane collagen. J Biol Chem. 1988 May 15;263(14):6579–6587. [PubMed] [Google Scholar]
  4. DePoli P., Bacon-Baguley T., Kendra-Franczak S., Cederholm M. T., Walz D. A. Thrombospondin interaction with plasminogen. Evidence for binding to a specific region of the kringle structure of plasminogen. Blood. 1989 Mar;73(4):976–982. [PubMed] [Google Scholar]
  5. Deutsch D. G., Mertz E. T. Plasminogen: purification from human plasma by affinity chromatography. Science. 1970 Dec 4;170(3962):1095–1096. doi: 10.1126/science.170.3962.1095. [DOI] [PubMed] [Google Scholar]
  6. Enghild J. J., Thøgersen I. B., Pizzo S. V., Salvesen G. Analysis of inter-alpha-trypsin inhibitor and a novel trypsin inhibitor, pre-alpha-trypsin inhibitor, from human plasma. Polypeptide chain stoichiometry and assembly by glycan. J Biol Chem. 1989 Sep 25;264(27):15975–15981. [PubMed] [Google Scholar]
  7. Gonzalez-Gronow M., Robbins K. C. In vitro biosynthesis of plasminogen in a cell-free system directed by mRNA fractions isolated from monkey liver. Biochemistry. 1984 Jan 17;23(2):190–196. doi: 10.1021/bi00297a003. [DOI] [PubMed] [Google Scholar]
  8. Highsmith R. F. Isolation and properties of a plasminogen activator derived from canine vascular tissue. J Biol Chem. 1981 Jul 10;256(13):6788–6795. [PubMed] [Google Scholar]
  9. Kefalides N. A. Structure and biosynthesis of basement membranes. Int Rev Connect Tissue Res. 1973;6:63–104. doi: 10.1016/b978-0-12-363706-2.50008-8. [DOI] [PubMed] [Google Scholar]
  10. Knudsen B. S., Silverstein R. L., Leung L. L., Harpel P. C., Nachman R. L. Binding of plasminogen to extracellular matrix. J Biol Chem. 1986 Aug 15;261(23):10765–10771. [PubMed] [Google Scholar]
  11. 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]
  12. Liotta L. A., Goldfarb R. H., Brundage R., Siegal G. P., Terranova V., Garbisa S. Effect of plasminogen activator (urokinase), plasmin, and thrombin on glycoprotein and collagenous components of basement membrane. Cancer Res. 1981 Nov;41(11 Pt 1):4629–4636. [PubMed] [Google Scholar]
  13. Mackay A. R., Corbitt R. H., Hartzler J. L., Thorgeirsson U. P. Basement membrane type IV collagen degradation: evidence for the involvement of a proteolytic cascade independent of metalloproteinases. Cancer Res. 1990 Sep 15;50(18):5997–6001. [PubMed] [Google Scholar]
  14. Matsudaira P. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem. 1987 Jul 25;262(21):10035–10038. [PubMed] [Google Scholar]
  15. Murphy G., McAlpine C. G., Poll C. T., Reynolds J. J. Purification and characterization of a bone metalloproteinase that degrades gelatin and types IV and V collagen. Biochim Biophys Acta. 1985 Sep 20;831(1):49–58. doi: 10.1016/0167-4838(85)90148-7. [DOI] [PubMed] [Google Scholar]
  16. Nagase H., Enghild J. J., Suzuki K., Salvesen G. Stepwise activation mechanisms of the precursor of matrix metalloproteinase 3 (stromelysin) by proteinases and (4-aminophenyl)mercuric acetate. Biochemistry. 1990 Jun 19;29(24):5783–5789. doi: 10.1021/bi00476a020. [DOI] [PubMed] [Google Scholar]
  17. Nieuwenhuizen W., Verheijen J. H., Vermond A., Chang G. T. Plasminogen activation by tissue activator is accelerated in the presence of fibrin(ogen) cyanogen bromide fragment FCB-2. Biochim Biophys Acta. 1983 Feb 22;755(3):531–533. doi: 10.1016/0304-4165(83)90261-1. [DOI] [PubMed] [Google Scholar]
  18. Okada Y., Morodomi T., Enghild J. J., Suzuki K., Yasui A., Nakanishi I., Salvesen G., Nagase H. Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties. Eur J Biochem. 1990 Dec 27;194(3):721–730. doi: 10.1111/j.1432-1033.1990.tb19462.x. [DOI] [PubMed] [Google Scholar]
  19. Okada Y., Nagase H., Harris E. D., Jr A metalloproteinase from human rheumatoid synovial fibroblasts that digests connective tissue matrix components. Purification and characterization. J Biol Chem. 1986 Oct 25;261(30):14245–14255. [PubMed] [Google Scholar]
  20. Patthy L., Trexler M., Váli Z., Bányai L., Váradi A. Kringles: modules specialized for protein binding. Homology of the gelatin-binding region of fibronectin with the kringle structures of proteases. FEBS Lett. 1984 Jun 4;171(1):131–136. doi: 10.1016/0014-5793(84)80473-1. [DOI] [PubMed] [Google Scholar]
  21. Preissner K. T. Specific binding of plasminogen to vitronectin. Evidence for a modulatory role of vitronectin on fibrin(ogen)-induced plasmin formation by tissue plasminogen activator. Biochem Biophys Res Commun. 1990 May 16;168(3):966–971. doi: 10.1016/0006-291x(90)91123-a. [DOI] [PubMed] [Google Scholar]
  22. Reich R., Thompson E. W., Iwamoto Y., Martin G. R., Deason J. R., Fuller G. C., Miskin R. Effects of inhibitors of plasminogen activator, serine proteinases, and collagenase IV on the invasion of basement membranes by metastatic cells. Cancer Res. 1988 Jun 15;48(12):3307–3312. [PubMed] [Google Scholar]
  23. Rånby M. Studies on the kinetics of plasminogen activation by tissue plasminogen activator. Biochim Biophys Acta. 1982 Jun 24;704(3):461–469. doi: 10.1016/0167-4838(82)90068-1. [DOI] [PubMed] [Google Scholar]
  24. Salonen E. M., Saksela O., Vartio T., Vaheri A., Nielsen L. S., Zeuthen J. Plasminogen and tissue-type plasminogen activator bind to immobilized fibronectin. J Biol Chem. 1985 Oct 5;260(22):12302–12307. [PubMed] [Google Scholar]
  25. Silverstein R. L., Nachman R. L., Leung L. L., Harpel P. C. Activation of immobilized plasminogen by tissue activator. Multimolecular complex formation. J Biol Chem. 1985 Aug 25;260(18):10346–10352. [PubMed] [Google Scholar]
  26. Stack S., Gonzalez-Gronow M., Pizzo S. V. Regulation of plasminogen activation by components of the extracellular matrix. Biochemistry. 1990 May 22;29(20):4966–4970. doi: 10.1021/bi00472a029. [DOI] [PubMed] [Google Scholar]
  27. Strickland S., Reich E., Sherman M. I. Plasminogen activator in early embryogenesis: enzyme production by trophoblast and parietal endoderm. Cell. 1976 Oct;9(2):231–240. doi: 10.1016/0092-8674(76)90114-8. [DOI] [PubMed] [Google Scholar]
  28. Thewes T., Constantine K., Byeon I. J., Llinás M. Ligand interactions with the kringle 5 domain of plasminogen. A study by 1H NMR spectroscopy. J Biol Chem. 1990 Mar 5;265(7):3906–3915. [PubMed] [Google Scholar]
  29. Váli Z., Patthy L. Location of the intermediate and high affinity omega-aminocarboxylic acid-binding sites in human plasminogen. J Biol Chem. 1982 Feb 25;257(4):2104–2110. [PubMed] [Google Scholar]
  30. Váradi A., Patthy L. Kringle 5 of human plasminogen carries a benzamidine-binding site. Biochem Biophys Res Commun. 1981 Nov 16;103(1):97–102. doi: 10.1016/0006-291x(81)91665-x. [DOI] [PubMed] [Google Scholar]
  31. Wilhelm S. M., Collier I. E., Marmer B. L., Eisen A. Z., Grant G. A., Goldberg G. I. SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase which is identical to that secreted by normal human macrophages. J Biol Chem. 1989 Oct 15;264(29):17213–17221. [PubMed] [Google Scholar]
  32. Yurchenco P. D., Schittny J. C. Molecular architecture of basement membranes. FASEB J. 1990 Apr 1;4(6):1577–1590. doi: 10.1096/fasebj.4.6.2180767. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES