Crystal structure of three consecutive laminin-type epidermal growth factor-like (LE) modules of laminin γ1 chain harboring the nidogen binding site

Journal of Molecular Biology

Volumn 257, Issue 3, 1996, Pages 644-657

  Stetefeld, Jörg ^a   Mayer, Ulrike ^a   Timpl, Rupert ^a   Huber, Robert ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Basement membranes; Extracellular module; Laminin nidogen interaction; X ray

Indexed keywords

ENTACTIN; EPIDERMAL GROWTH FACTOR; LAMININ;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; DISULFIDE BOND; HYDROGEN BOND; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION;

ANIMALIA;

EID: 0029967684     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0191     Document Type: Article

References (49)

1. Bairoch, A. (1995). Nomenclature of extracellular modules. SWISS-PROT Protein Sequence Data Bank, Release 31.0.
2. Baron, M., Norman, D. G. & Campbell, I. D. (1991). Protein modules. Trends Biochem. Sci. 16, 13-17.
3. Baumgartner, R., Czisch, M., Mayer, U., Pöschl, E., Huber, R., Timpl, R. & Holak, T. A. (1996). Structure of the nidogen binding LE module of the laminin γ1 chain in solution. J. Mol. Biol. 257, 658-668.
4. Beck, K., Hunter, I. & Engel, J. (1990). Structure and function of laminin: anatomy of a multidomain glycoprotein. FASEB J. 4, 148-160.
5. Brandstetter, H., Bauer, M., Huber, R., Lolla, P. & Bode, W. (1995). X-ray structure of clotting factor Ixa: active site and module structure related to Xase activity and hemophilia B. Proc. Natl Acad. Sci. USA, 92, 9796-9800.
6. Brown, J. C., Wiedemann, H. & Timpl, R. (1994). Protein binding and cell adhesion properties of two laminin isoforms (AmB1eB2e, AmB1sB2e) from human placenta. J. Cell Sci. 107, 329-338.
7. Brünger, A. T. (1992). XPLOR Version 3.1 A System for X-Ray Crystallography and NMR. Yale University Press, New Haven, CT.
8. Campbell, I. D. & Bork, P. (1993). Epidermal growth factor-like modules. Curr. Opin. Struct. Biol. 3, 385-392.
9. CCP4 (1979). The SERC (UK) Collaborative Computing Project No. 4, distributed from Daresbury Laboratory, Warrington, UK.
10. Cooke, R. M., Wilkinson, A. J., Baron, M., Pastore, A., Tappin, M. J., Campbell, I. D., Gregory H. & Sheard, B. (1987). The solution structure of human epidermal growth factor. Nature, 327, 339-341.
11. Cowtan, K. (1994). Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography, 31, 34-38.
12. Ekblom, P., Ekblom, M., Fecker, L., Klein, G., Zhang, H.-Y., Kadoya, Y., Chu, M.-L., Mayer, U. & Timpl, R. (1994). Role of mesenchymal nidogen for epithelial morphogenesis in vitro. Development, 120, 2003-2014.
13. Engel, J. (1989). EGF-like modules in extracellular matrix proteins: localized signals for growth and differentiation? FEBS Letters, 251, 1-7.
14. Engel, J., Odermatt, E., Engel, A., Madri, J. A., Furthmayr, H., Rohde, H. & Timpl, R. (1981). Shapes, domain organizations and flexibility of laminin and fibronectin, two multifunctional proteins of the extracellular matrix. J. Mol. Biol. 150, 97-120.
15. Engel, J., Efimov, V. P. & Maurer, P. (1994). Domain organizations of extracellular matrix proteins and their evolution. Development Suppl. 120, 35-42.
16. Engh, R. A. & Huber, R. (1991). Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A, 47, 392-400.
17. Fox, J. W., Mayer, U., Nischt, R., Aumailley M., Reinhardt, D., Wiedemann, H., Mann, K., Timpl, R., Krieg, T., Engel, J. & Chu, M.-L. (1991). Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J. 10, 3137-3146.
18. Gerl, M., Mann, K. H., Aumailley M. & Timpl, R. (1991). Localization of a major nidogen-binding site to module III of laminin B2 chain. Eur. J. Biochem. 202, 167-174.
19. Handford, P. A., Baron, M., Mayhew, M., Willis, A., Beesley T., Brownlee, G. G. & Campbell, I. D. (1990). The first EGF-like module from human factor IX contains a high-affinity calcium binding site. EMBO J. 9, 475-480.
20. Handford, P., Downing, A. K., Rao, Z., Hewett, D. R., Sykes, B. C. & Kielty C. M. (1995). The calcium binding properties and molecular organization of epidermal growth factor-like modules in human fibrillin-1. J. Biol. Chem. 270, 6751-6756.
21. Jones, T. A., Zou, J.-Y., Cowan, S. W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A, 47, 110-119.
22. Kabsch, W. & Sander, C. (1983). Dictionary of secondary structures: pattern recognition of hydrogen bonded and geometrical features. Biopolymers, 22, 2577-2637.
23. Kraulis, P, J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
24. Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. (1992). PROCHECK v.2: Programs to Check the Stereochemical Quality of Protein Structures, Oxford Molecular Ltd, Oxford, England.
25. Leslie, A. G. W. (1991). In Crystallographic Computing, vol. 5, pp. 50-61, Oxford University Press, Oxford.
26. Mackrell, A. J., Kusche-Gullberg, M., Garrison, K. & Fessler, J. H. (1993). Novel Drosophila laminin A chain reveals structural relationships between laminin subunits. FASEB J. 7, 375-381.
27. Mayer, U. & Timpl, R. (1994). Nidogen: a versatile binding protein of basement membranes. In Extracellular Matrix Assembly and Structure (Yurchenco, P. D., Birk, D. & Mecham, R. D., eds), pp. 389-416, Academic Press, Orlando, Fl.
28. Mayer, U., Nischt, R., Pöschl, E., Mann, K., Fukuda, K., Gerl, M., Yamada, Y. & Timpl, R. (1993). A single EGF-like motif of laminin is responsible for high affinity nidogen binding. EMBO J. 12, 1879-1885.
29. Mayer, U., Pöschl, E., Gerecke, D. R., Wagman, D. W., Burgeson, R. E. & Timpl, R. (1995). Low nidogen affinity of laminin-5 can be attributed to two serine residues in EGF-like motif γ2III4. FEBS Letters, 365, 129-132.
30. McMahan, U. J., Horton, S. E., Werle, M. J., Honig, L. S., Kröger, S., Ruegg, M. A. & Escher, G. (1992). Agrin isoforms and their role in synaptogenesis. Curr. Opin. Cell Biol. 4, 869-874.
31. Montelione, G. T., Wüthrich, K., Nice, E. C., Burgess, A. W. & Scheraga, H. A. (1987). Solution structure of murine epidermal growth factor: determination of the polypeptide backbone chain-fold by nuclear magnetic resonance and distance geometry Proc. Natl Acad. Sci. USA, 84, 5226-5230.
32. Paulsson, M., Aumailley M., Deutzmann, R., Timpl, R., Beck, K. & Engel, J. (1987). Laminin-nidogen complex: extraction with chelating agents and structural characterization. Eur. J. Biochem. 166, 11-19.
33. Pöschl, E., Fox, J. W., Block, D., Mayer, U. & Timpl, R. (1994). Two non-contiguous regions constribute to nidogen binding to a single EGF-like motif of the laminin γ1 chain. EMBO J. 13, 3741-3747.
34. Ramirez, F., Pereira, L., Zhang, H. & Lee, B. (1993). The fibrillin-marfan syndrome. BioEssays, 15, 589-594.
35. Reinhardt, D., Mann, K., Nischt, R., Fox, J. W., Chu, M.-L., Krieg, T. & Timpl, R. (1993). Mapping of nidogen binding sites for collagen type IV, heparan sulfate proteoglycan and zinc. J. Biol. Chem. 268, 10881-10887.
36. Rose, D., Gierasch, L. M. & Smith, J. A., (1985). Turns in peptids and proteins. Advan. Protein Chem. 37, 1-95.
37. Sasaki, M. & Yamada, Y. (1987). Structure of the laminin B2 chain shows multimodule structures homologues to the β1 chain. J. Biol. Chem. 262, 17111-17117.
38. Sasaki, M., Kato, S., Kohno, K., Martin, G. R. & Yamada, Y (1987). Sequence of cDNA encoding the laminin B1 chain reveals a multidomain protein containing cysteine-rich repeats. Proc. Natl Acad. Sci. USA, 84, 935-939.
39. Sasaki, M., Kleinman, H. K., Huber, H., Deutzmann, R. & Yamada, Y. (1988). Laminin, a multimodule protein: the A chain has a unique globular domain and homology with the basement membrane proteoglycan and the laminin B chains. J. Biol. Chem. 263, 16536-16544.
40. Sasaki, T., Kostka, G., Göhring, W., Wiedemann, H., Mann, K., Chu, M.-L. & Timpl, R. (1995). Structural characterization of two variants of fibulin-1 that differ in nidogen affinity J. Mol. Biol. 245, 241-250.
41. Schulze, B., Mann, K., Battistutta, R., Wiedemann, H. & Timpl, R. (1995). Structural properties of recombinant domain III-3 of perlecan containing a globular domain inserted into an epidermal-growth-factor-like motif. Eur. J. Biochem. 231, 551-556.
42. Selander-Sunnerhagen, M., Ullner, M., Persson, E., Teleman, O., Stenflo, J. & Drakenberg, T. (1992). How an epidermal growth factor (EGF)-like module binds calcium. High resolution NMR structure of the calcium form of the NH2-terminal EGF-like module in coagulation factor X. J. Biol. Chem. 267, 19642-19649.
43. Spring, J., Beck, K. & Chiquet-Ehrismann, R. (1989). Two contrary functions of tenascin: dissection of the active sites by recombinant tenascin fragment. Cell, 59, 325-314.
44. Steigemann, W. (1974). PhD thesis, Technische Universität München.
45. Timpl, R. (1993). Proteoglycans of basement membranes. Experientia, 49, 417-428.
46. Timpl, R. & Brown, J. C. (1996). Supramolecular assembly of basement membranes. BioEssays, in the press.
47. Turk, D. (1992). PhD thesis, Technische Universität München.
48. Yurchenco, P. D. (1994). Assembly of laminin and type IV collagen into basement membrane networks. In Extracellular Matrix Assembly and Structure (Yurchenco, P. D., Birk, D. & Mecham, R. D., eds), pp. 351-388, Academic Press, San Diego.
49. Yurchenco, P. D. & Cheng, Y.-S. (1993). Self-assembly and calcium-binding sites in laminin. A three-arm interaction model. J. Biol. Chem. 268, 17286-17299.