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. 1993 Jan 2;120(2):557–567. doi: 10.1083/jcb.120.2.557

Structure and binding properties of collagen type XIV isolated from human placenta

PMCID: PMC2119504  PMID: 8421066

Abstract

Collagen XIV was isolated from neutral salt extracts of human placenta and purified by several chromatographic steps including affinity binding to heparin. The same procedures also led to the purification of a tissue form of fibronectin. Collagen XIV was demonstrated by partial sequence analysis of its Col1 and Col2 domains and by electron microscopy to be a disulphide-linked molecule with a characteristic cross-shape. The individual chains had a size of approximately 210 kD, which was reduced to approximately 180 kD (domain NC3) after treatment with bacterial collagenase. Specific antibodies mainly to NC3 epitopes were obtained by affinity chromatography and used in tissue and cell analyses by immunoblotting and radioimmunoassays. Two sequences from NC3 were identified on fragments obtained after trypsin cleavage. They were identical to cDNA-derived sequences of undulin, a noncollagenous extracellular matrix protein. This suggests that collagen XIV and undulin may be different splice variants from the same gene. Heparin binding was confirmed in ligand assays with a large basement membrane heparan sulphate proteoglycan. This binding could be inhibited by heparin and heparan sulphate but not by chondroitin sulphate. In addition, collagen XIV bound to the triple helical domain of collagen VI. The interactions with heparin sulphate proteoglycan and collagen VI were not shared by the NC3 domain, or by reduced and alkylated collagen XIV. No or only low binding was observed for collagens I-V, pN- collagens I and III, and several noncollagenous matrix proteins, including laminin, recombinant nidogen, BM-40/osteonectin, plasma and tissue fibronectin, vitronectin, and von Willebrand factor. Insignificant activity was also shown in cell attachment assays with nine established cell lines.

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Selected References

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  1. Aumailley M., Mann K., von der Mark H., Timpl R. Cell attachment properties of collagen type VI and Arg-Gly-Asp dependent binding to its alpha 2(VI) and alpha 3(VI) chains. Exp Cell Res. 1989 Apr;181(2):463–474. doi: 10.1016/0014-4827(89)90103-1. [DOI] [PubMed] [Google Scholar]
  2. Aumailley M., Wiedemann H., Mann K., Timpl R. Binding of nidogen and the laminin-nidogen complex to basement membrane collagen type IV. Eur J Biochem. 1989 Sep 1;184(1):241–248. doi: 10.1111/j.1432-1033.1989.tb15013.x. [DOI] [PubMed] [Google Scholar]
  3. Brown J. C., Spragg J. H., Wheeler G. N., Taylor P. W. Identification of the B1 and B2 subunits of human placental laminin and rat parietal-yolk-sac laminin using antisera specific for murine laminin-beta-galactosidase fusion proteins. Biochem J. 1990 Sep 1;270(2):463–468. doi: 10.1042/bj2700463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bruns R. R. Beaded filaments and long-spacing fibrils: relation to type VI collagen. J Ultrastruct Res. 1984 Nov;89(2):136–145. doi: 10.1016/s0022-5320(84)80010-6. [DOI] [PubMed] [Google Scholar]
  5. Bruns R. R., Press W., Engvall E., Timpl R., Gross J. Type VI collagen in extracellular, 100-nm periodic filaments and fibrils: identification by immunoelectron microscopy. J Cell Biol. 1986 Aug;103(2):393–404. doi: 10.1083/jcb.103.2.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carnemolla B., Balza E., Siri A., Zardi L., Nicotra M. R., Bigotti A., Natali P. G. A tumor-associated fibronectin isoform generated by alternative splicing of messenger RNA precursors. J Cell Biol. 1989 Mar;108(3):1139–1148. doi: 10.1083/jcb.108.3.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chu M. L., Conway D., Pan T. C., Baldwin C., Mann K., Deutzmann R., Timpl R. Amino acid sequence of the triple-helical domain of human collagen type VI. J Biol Chem. 1988 Dec 15;263(35):18601–18606. [PubMed] [Google Scholar]
  8. Chu M. L., Zhang R. Z., Pan T. C., Stokes D., Conway D., Kuo H. J., Glanville R., Mayer U., Mann K., Deutzmann R. Mosaic structure of globular domains in the human type VI collagen alpha 3 chain: similarity to von Willebrand factor, fibronectin, actin, salivary proteins and aprotinin type protease inhibitors. EMBO J. 1990 Feb;9(2):385–393. doi: 10.1002/j.1460-2075.1990.tb08122.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dublet B., Oh S., Sugrue S. P., Gordon M. K., Gerecke D. R., Olsen B. R., van der Rest M. The structure of avian type XII collagen. Alpha 1 (XII) chains contain 190-kDa non-triple helical amino-terminal domains and form homotrimeric molecules. J Biol Chem. 1989 Aug 5;264(22):13150–13156. [PubMed] [Google Scholar]
  10. Dublet B., van der Rest M. Type XII collagen is expressed in embryonic chick tendons. Isolation of pepsin-derived fragments. J Biol Chem. 1987 Dec 25;262(36):17724–17727. [PubMed] [Google Scholar]
  11. Dublet B., van der Rest M. Type XIV collagen, a new homotrimeric molecule extracted from fetal bovine skin and tendon, with a triple helical disulfide-bonded domain homologous to type IX and type XII collagens. J Biol Chem. 1991 Apr 15;266(11):6853–6858. [PubMed] [Google Scholar]
  12. Engel J., Hunter I., Schulthess T., Beck K., Dixon T. W., Parry D. A. Assembly of laminin isoforms by triple- and double-stranded coiled-coil structures. Biochem Soc Trans. 1991 Nov;19(4):839–843. doi: 10.1042/bst0190839. [DOI] [PubMed] [Google Scholar]
  13. Eyre D. R., Apon S., Wu J. J., Ericsson L. H., Walsh K. A. Collagen type IX: evidence for covalent linkages to type II collagen in cartilage. FEBS Lett. 1987 Aug 17;220(2):337–341. doi: 10.1016/0014-5793(87)80842-6. [DOI] [PubMed] [Google Scholar]
  14. Fleischmajer R., Perlish J. S., Burgeson R. E., Shaikh-Bahai F., Timpl R. Type I and type III collagen interactions during fibrillogenesis. Ann N Y Acad Sci. 1990;580:161–175. doi: 10.1111/j.1749-6632.1990.tb17927.x. [DOI] [PubMed] [Google Scholar]
  15. Fleischmajer R., Timpl R., Tuderman L., Raisher L., Wiestner M., Perlish J. S., Graves P. N. Ultrastructural identification of extension aminopropeptides of type I and III collagens in human skin. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7360–7364. doi: 10.1073/pnas.78.12.7360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fox J. W., Mayer U., Nischt R., Aumailley M., Reinhardt D., Wiedemann H., Mann K., Timpl R., Krieg T., Engel J. Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J. 1991 Nov;10(11):3137–3146. doi: 10.1002/j.1460-2075.1991.tb04875.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Gordon M. K., Castagnola P., Dublet B., Linsenmayer T. F., Van der Rest M., Mayne R., Olsen B. R. Cloning of a cDNA for a new member of the class of fibril-associated collagens with interrupted triple helices. Eur J Biochem. 1991 Oct 15;201(2):333–338. doi: 10.1111/j.1432-1033.1991.tb16290.x. [DOI] [PubMed] [Google Scholar]
  19. Gordon M. K., Gerecke D. R., Dublet B., van der Rest M., Olsen B. R. Type XII collagen. A large multidomain molecule with partial homology to type IX collagen. J Biol Chem. 1989 Nov 25;264(33):19772–19778. [PubMed] [Google Scholar]
  20. Gordon M. K., Gerecke D. R., Olsen B. R. Type XII collagen: distinct extracellular matrix component discovered by cDNA cloning. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6040–6044. doi: 10.1073/pnas.84.17.6040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Heremans A., van der Schueren B., de Cock B., Paulsson M., Cassiman J. J., van den Berghe H., David G. Matrix-associated heparan sulfate proteoglycan: core protein-specific monoclonal antibodies decorate the pericellular matrix of connective tissue cells and the stromal side of basement membranes. J Cell Biol. 1989 Dec;109(6 Pt 1):3199–3211. doi: 10.1083/jcb.109.6.3199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jilek F., Hörmann H. Cold-insoluble globulin, II. Plasminolysis of cold-insoluble globulin. Hoppe Seylers Z Physiol Chem. 1977 Jan;358(1):133–136. [PubMed] [Google Scholar]
  23. Just M., Herbst H., Hummel M., Dürkop H., Tripier D., Stein H., Schuppan D. Undulin is a novel member of the fibronectin-tenascin family of extracellular matrix glycoproteins. J Biol Chem. 1991 Sep 15;266(26):17326–17332. [PubMed] [Google Scholar]
  24. Keene D. R., Engvall E., Glanville R. W. Ultrastructure of type VI collagen in human skin and cartilage suggests an anchoring function for this filamentous network. J Cell Biol. 1988 Nov;107(5):1995–2006. doi: 10.1083/jcb.107.5.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Keene D. R., Lunstrum G. P., Morris N. P., Stoddard D. W., Burgeson R. E. Two type XII-like collagens localize to the surface of banded collagen fibrils. J Cell Biol. 1991 May;113(4):971–978. doi: 10.1083/jcb.113.4.971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lunstrum G. P., McDonough A. M., Marinkovich M. P., Keene D. R., Morris N. P., Burgeson R. E. Identification and partial purification of a large, variant form of type XII collagen. J Biol Chem. 1992 Oct 5;267(28):20087–20092. [PubMed] [Google Scholar]
  27. Lunstrum G. P., Morris N. P., McDonough A. M., Keene D. R., Burgeson R. E. Identification and partial characterization of two type XII-like collagen molecules. J Cell Biol. 1991 May;113(4):963–969. doi: 10.1083/jcb.113.4.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lunstrum G. P., Sakai L. Y., Keene D. R., Morris N. P., Burgeson R. E. Large complex globular domains of type VII procollagen contribute to the structure of anchoring fibrils. J Biol Chem. 1986 Jul 5;261(19):9042–9048. [PubMed] [Google Scholar]
  29. Mayer U., Aumailley M., Mann K., Timpl R., Engel J. Calcium-dependent binding of basement membrane protein BM-40 (osteonectin, SPARC) to basement membrane collagen type IV. Eur J Biochem. 1991 May 23;198(1):141–150. doi: 10.1111/j.1432-1033.1991.tb15996.x. [DOI] [PubMed] [Google Scholar]
  30. Miller E. J., Rhodes R. K. Preparation and characterization of the different types of collagen. Methods Enzymol. 1982;82(Pt A):33–64. doi: 10.1016/0076-6879(82)82059-4. [DOI] [PubMed] [Google Scholar]
  31. Mohri H., Yoshioka A., Zimmerman T. S., Ruggeri Z. M. Isolation of the von Willebrand factor domain interacting with platelet glycoprotein Ib, heparin, and collagen and characterization of its three distinct functional sites. J Biol Chem. 1989 Oct 15;264(29):17361–17367. [PubMed] [Google Scholar]
  32. Nischt R., Pottgiesser J., Krieg T., Mayer U., Aumailley M., Timpl R. Recombinant expression and properties of the human calcium-binding extracellular matrix protein BM-40. Eur J Biochem. 1991 Sep 1;200(2):529–536. doi: 10.1111/j.1432-1033.1991.tb16214.x. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Paulsson M., Aumailley M., Deutzmann R., Timpl R., Beck K., Engel J. Laminin-nidogen complex. Extraction with chelating agents and structural characterization. Eur J Biochem. 1987 Jul 1;166(1):11–19. doi: 10.1111/j.1432-1033.1987.tb13476.x. [DOI] [PubMed] [Google Scholar]
  35. Paulsson M., Yurchenco P. D., Ruben G. C., Engel J., Timpl R. Structure of low density heparan sulfate proteoglycan isolated from a mouse tumor basement membrane. J Mol Biol. 1987 Sep 20;197(2):297–313. doi: 10.1016/0022-2836(87)90125-2. [DOI] [PubMed] [Google Scholar]
  36. Pejler G., Bäckström G., Lindahl U., Paulsson M., Dziadek M., Fujiwara S., Timpl R. Structure and affinity for antithrombin of heparan sulfate chains derived from basement membrane proteoglycans. J Biol Chem. 1987 Apr 15;262(11):5036–5043. [PubMed] [Google Scholar]
  37. Risteli L., Risteli J. Analysis of extracellular matrix proteins in biological fluids. Methods Enzymol. 1987;145:391–411. doi: 10.1016/0076-6879(87)45022-2. [DOI] [PubMed] [Google Scholar]
  38. Schuppan D., Cantaluppi M. C., Becker J., Veit A., Bunte T., Troyer D., Schuppan F., Schmid M., Ackermann R., Hahn E. G. Undulin, an extracellular matrix glycoprotein associated with collagen fibrils. J Biol Chem. 1990 May 25;265(15):8823–8832. [PubMed] [Google Scholar]
  39. Shaw L. M., Olsen B. R. FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem Sci. 1991 May;16(5):191–194. doi: 10.1016/0968-0004(91)90074-6. [DOI] [PubMed] [Google Scholar]
  40. Sixma J. J., Schiphorst M. E., Verweij C. L., Pannekoek H. Effect of deletion of the A1 domain of von Willebrand factor on its binding to heparin, collagen and platelets in the presence of ristocetin. Eur J Biochem. 1991 Mar 14;196(2):369–375. doi: 10.1111/j.1432-1033.1991.tb15826.x. [DOI] [PubMed] [Google Scholar]
  41. Sonnenberg A., Linders C. J., Modderman P. W., Damsky C. H., Aumailley M., Timpl R. Integrin recognition of different cell-binding fragments of laminin (P1, E3, E8) and evidence that alpha 6 beta 1 but not alpha 6 beta 4 functions as a major receptor for fragment E8. J Cell Biol. 1990 Jun;110(6):2145–2155. doi: 10.1083/jcb.110.6.2145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Specks U., Mayer U., Nischt R., Spissinger T., Mann K., Timpl R., Engel J., Chu M. L. Structure of recombinant N-terminal globule of type VI collagen alpha 3 chain and its binding to heparin and hyaluronan. EMBO J. 1992 Dec;11(12):4281–4290. doi: 10.1002/j.1460-2075.1992.tb05527.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sugrue S. P., Gordon M. K., Seyer J., Dublet B., van der Rest M., Olsen B. R. Immunoidentification of type XII collagen in embryonic tissues. J Cell Biol. 1989 Aug;109(2):939–945. doi: 10.1083/jcb.109.2.939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Timpl R. Antibodies to collagens and procollagens. Methods Enzymol. 1982;82(Pt A):472–498. doi: 10.1016/0076-6879(82)82079-x. [DOI] [PubMed] [Google Scholar]
  45. Timpl R., Glanville R. W., Nowack H., Wiedemann H., Fietzek P. P., Kühn K. Isolation, chemical and electron microscopical characterization of neutral-salt-soluble type III collagen and procollagen from fetal bovine skin. Hoppe Seylers Z Physiol Chem. 1975 Nov;356(11):1783–1792. doi: 10.1515/bchm2.1975.356.2.1783. [DOI] [PubMed] [Google Scholar]
  46. Trueb J., Trueb B. Type XIV collagen is a variant of undulin. Eur J Biochem. 1992 Jul 15;207(2):549–557. doi: 10.1111/j.1432-1033.1992.tb17081.x. [DOI] [PubMed] [Google Scholar]
  47. Vaughan L., Mendler M., Huber S., Bruckner P., Winterhalter K. H., Irwin M. I., Mayne R. D-periodic distribution of collagen type IX along cartilage fibrils. J Cell Biol. 1988 Mar;106(3):991–997. doi: 10.1083/jcb.106.3.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Vuorio E., de Crombrugghe B. The family of collagen genes. Annu Rev Biochem. 1990;59:837–872. doi: 10.1146/annurev.bi.59.070190.004201. [DOI] [PubMed] [Google Scholar]
  49. Watt S. L., Lunstrum G. P., McDonough A. M., Keene D. R., Burgeson R. E., Morris N. P. Characterization of collagen types XII and XIV from fetal bovine cartilage. J Biol Chem. 1992 Oct 5;267(28):20093–20099. [PubMed] [Google Scholar]
  50. Yamagata M., Yamada K. M., Yamada S. S., Shinomura T., Tanaka H., Nishida Y., Obara M., Kimata K. The complete primary structure of type XII collagen shows a chimeric molecule with reiterated fibronectin type III motifs, von Willebrand factor A motifs, a domain homologous to a noncollagenous region of type IX collagen, and short collagenous domains with an Arg-Gly-Asp site. J Cell Biol. 1991 Oct;115(1):209–221. doi: 10.1083/jcb.115.1.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Yatohgo T., Izumi M., Kashiwagi H., Hayashi M. Novel purification of vitronectin from human plasma by heparin affinity chromatography. Cell Struct Funct. 1988 Aug;13(4):281–292. doi: 10.1247/csf.13.281. [DOI] [PubMed] [Google Scholar]
  52. Yurchenco P. D., Furthmayr H. Self-assembly of basement membrane collagen. Biochemistry. 1984 Apr 10;23(8):1839–1850. doi: 10.1021/bi00303a040. [DOI] [PubMed] [Google Scholar]
  53. van der Rest M., Aubert-Foucher E., Dublet B., Eichenberger D., Font B., Goldschmidt D. Structure and function of the fibril-associated collagens. Biochem Soc Trans. 1991 Nov;19(4):820–824. doi: 10.1042/bst0190820. [DOI] [PubMed] [Google Scholar]
  54. van der Rest M., Garrone R. Collagen family of proteins. FASEB J. 1991 Oct;5(13):2814–2823. [PubMed] [Google Scholar]
  55. van der Rest M., Mayne R. Type IX collagen proteoglycan from cartilage is covalently cross-linked to type II collagen. J Biol Chem. 1988 Feb 5;263(4):1615–1618. [PubMed] [Google Scholar]
  56. von der Mark H., Aumailley M., Wick G., Fleischmajer R., Timpl R. Immunochemistry, genuine size and tissue localization of collagen VI. Eur J Biochem. 1984 Aug 1;142(3):493–502. doi: 10.1111/j.1432-1033.1984.tb08313.x. [DOI] [PubMed] [Google Scholar]

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