Structural basis of glycosaminoglycan modification and of heterotypic interactions of perlecan domain V

Journal of Molecular Biology

Volumn 294, Issue 1, 1999, Pages 259-270

  Friedrich, Martin V K ^a   Göhring, Walter ^a   Mörgelin, Matthias ^b   Brancaccio, Andrea ^c   David, Guido ^d   Timpl, Rupert ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b LUND UNIVERSITY   (Sweden)

^c CATHOLIC UNIVERSITY   (Italy)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Basement membranes; Carbohydrate ligands; Recombinant production; Site directed mutagenesis; dystroglycan

Indexed keywords

ASPARAGINE; ASPARTIC ACID; CELL RECEPTOR; DYSTROGLYCAN; ENTACTIN; FIBULIN; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; LAMININ; PERLECAN; SERINE; SULFATIDE;

ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CHEMICAL BOND; CONTROLLED STUDY; ELECTRON MICROSCOPY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MODIFICATION; RECEPTOR BINDING;

ANIMALIA; MAMMALIA;

EID: 0345148341     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3259     Document Type: Article

References (54)

1. Andac Z., Sasaki T., Mann K., Brancaccio A., Deutzmann R., Timpl R. Analysis of heparin, α-dystroglycan and sulfatide binding to the G domain of laminin α1 chain by site-directed mutagenesis. J. Mol. Biol. 287:1999;253-264.
2. Aviezer D., Hecht D., Safran M., Eisinger M., David G., Yayon A. Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis. Cell. 79:1994;1005-1013.
3. Battaglia G., Mayer U., Aumailley M., Timpl R. Basement membrane heparan sulfate proteoglycan binds to laminin by its heparan sulfate chains and to nidogen by sites in the protein core. Eur. J. Biochem. 208:1992;359-366.
4. Bork P., Downing A. K., Kieffer B., Campbell I. D. Structure and distribution of modules in extracellular proteins. Quart. Rev. Biophys. 29:1996;119-167.
5. Brancaccio A., Schulthess T., Gesemann M., Engel J. Electron microscopic evidence for a mucin-like region in chick muscle α-dystroglycan. FEBS Letters. 368:1995;139-142.
6. Brown J. C., Sasaki T., Göhring W., Yamada Y., Timpl R. The C-terminal domain V of perlecan promotes β1 integrin-mediated cell adhesion, binds heparin, nidogen and fibulin-2 and can be modified by glycosaminoglycans. Eur. J. Biochem. 250:1997;39-46.
7. Burgeson R. E. Laminins in epidermal structures. Ekblom P., Timpl R. The Laminins. 1996;65-96 Harwood Academic Publisher, Reading.
8. Campbell I. D., Bork P. Epidermal growth factor-like modules. Curr. Opin. Struct. Biol. 3:1993;385-392.
9. Chakravarti S., Horchar T., Jefferson B., Laurie G. W., Hassell J. R. Recombinant domain III of perlecan promotes cell attachment through its RGDS sequence. J. Biol. Chem. 270:1995;404-409.
10. Costell M., Sasaki T., Mann K., Yamada Y., Timpl R. Structural characterization of domain II of the basement membrane proteoglycan perlecan. FEBS Letters. 396:1996;127-131.
11. Costell M., Mann K., Yamada Y., Timpl R. Characterization of recombinant perlecan domain I and its substitution by glycosaminoglycans and oligosaccharides. Eur. J. Biochem. 243:1997;115-121.
12. Dolan M., Horchar T., Rigatti B., Hassell J. R. Identification of sites in domain I of perlecan that regulate heparan sulfate synthesis. J. Biol. Chem. 272:1997;4316-4322.
13. Engel J. Electron microscopy of extracellular matrix components. Methods Enzymol. 245:1994;469-488.
14. Engel J., Furthmayr H. Electron microscopy and other physical methods for the characterization of extracellular matrix components: laminin, fibronectin, collagen IV, collagen VI and proteoglycans. Methods Enzymol. 145:1987;3-78.
15. Fox J. W., Mayer U., Nischt R., Aumailley M., Reinhardt D., Wiedemann H., Mann K., Timpl R., Krieg T., Engel J., Chu M.-L. Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J. 10:1991;3137-3146.
16. Gesemann M. A., Denzer J., Rüegg M. A. Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site. J. Cell Biol. 128:1995;625-636.
17. Gesemann M., Cavalli V., Denzer A. J., Brancaccio A., Schumacher B., Rüegg M. A. Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor. Neuron. 16:1996;755-767.
18. Gesemann M., Brancaccio A., Schumacher B., Rüegg M. A. Agrin is a high-affinity binding protein of dystroglycan in non-muscle tissue. J. Biol. Chem. 273:1998;600-605.
19. Göhring W., Sasaki T., Heldin C.-H., Timpl R. Mapping of the binding of platelet-derived growth factor to distinct domains of the basement membrane proteins BM-40 and perlecan and distinction from the BM-40 collagen-binding epitope. Eur. J. Biochem. 255:1998;60-66.
20. Groffen A. J. A., Buskens C. A. F., Tryggvason K., Veerkamp J. A., Monnens L. A. H., van den Heuvel L. P. W. J. Expression and characterization of human perlecan domains I and II synthesized by baculovirus-infected insect cells. Eur. J. Biochem. 241:1996;827-834.
21. Henry M. D., Campbell K. P. Dystroglycan: an extracellular matrix receptor linked to the cytoskeleton. Curr. Opin. Cell Biol. 8:1996;625-631.
22. Heremans A., Cassiman J.-J., van den Berghe H., David G. Heparan sulfate proteoglycan from the extracellular matrix of human lung fibroblasts. Isolation, purification, and core protein characterization. J. Biol. Chem. 263:1998;4731-4739.
23. Hohenester E., Tisi D., Talts J. F., Timpl R. Crystal structure of a laminin G-like module reveals the molecular basis of calcium-dependent α-dystroglycan binding to laminins, perlecan and agrin. Mol. Cell. in the press:1999.
24. Hopf C., Hoch W. Agrin binding to α-dystroglycan. Domains of agrin necessary to induce acetylcholine receptor clustering are overlapping but not identical to the α-dystroglycan-binding region. J. Biol. Chem. 271:1996;5231-5236.
25. Hopf M., Göhring W., Kohfeldt E., Yamada Y., Timpl R. Recombinant domain IV of perlecan binds to nidogens, laminin-nidogen complex, fibronectin, fibulin-2 and heparin. Eur. J. Biochem. 259:1999;917-925.
26. Iozzo R., Cohen I. R., Grässel S., Murdoch A. D. The biology of perlecan: the multifaceted heparan sulphate proteoglycan of basement membranes and pericellular matrices. Biochem. J. 302:1994;625-639.
27. Kalb E., Engel J. Binding and calcium-induced aggregation of laminin onto lipid bilayers. J. Biol. Chem. 266:1991;19047-19052.
28. Kallunki P., Tryggvason K. Human basement membrane heparan sulfate proteoglycan core protein: a 467-KD protein containing multiple domains resembling elements of the low density lipoprotein receptor, laminin, neural cell adhesion molecules and epidermal growth factor. J. Cell Biol. 116:1992;559-571.
29. Kohfeldt E., Maurer P., Vannahme C., Timpl R. Properties of the extracellular calcium binding module of the proteoglycan testican. FEBS Letters. 414:1997;557-561.
30. Kokenyesi R., Silbert J. E. Formation of heparan sulfate or chondroitin/dermatan sulfate on recombinant domain I of mouse perlecan expressed in chinese hamster ovary cells. Biochem. Biophys. Res. Commun. 211:1995;262-267.
31. Lander A. D. Targeting the glycosaminoglycan-binding sites on proteins. Chem. Biol. 1:1994;73-78.
32. Murdoch A. D., Dodge G. R., Cohen I., Tuan R. S., Iozzo R. V. Primary structure of human heparan sulfate proteoglycan from basement membrane (HSPG2/Perlecan). A chimeric molecule with multiple domains homologous to the low density lipoprotein receptor, laminin, neural cell adhesion molecules, and epidermal growth factor. J. Biol. Chem. 267:1992;8544-8557.
33. Murphy G., Allan J. A., Willenbrock F., Cockett M. I., O'Conell J. P., Docherty A. J. P. The role of the C-terminal domain in collagenase and stromelysin specificity. J. Biol. Chem. 267:1992;9612-9618.
34. Noonan D. M., Fulle A., Valente P., Cai S., Horigan E., Sasaki M., Yamada Y., Hassell J. R. The complete sequence of perlecan, a basement membrane heparan sulfate proteoglycan, reveals extensive similarity with laminin A chain, LDL-receptor and N-CAM. J. Biol. Chem. 266:1991;22939-22947.
35. O'Toole J. J., Deyst K. A., Bowe M. A., Nastuk M. A., McKechnie B. A., Fallon J. R. Alternative splicing of agrin regulates its binding to heparin, α-dystroglycan, and the cell surface. Proc. Natl Acad. Sci. USA. 93:1996;7369-7374.
36. 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. 197:1987;297-313.
37. Pöschl E., Fox J. W., Block D., Mayer U., Timpl R. Two non-contiguous regions contribute to nidogen binding to a single EGF-like motif of the laminin γ1 chain. EMBO J. 13:1994;3741-3747.
38. Prockop D. J., Sieron A. L., Li S.-W. Procollagen N-proteinase and procollagen C-proteinase. Two unusual metalloproteinases that are essential for procollagen processing probably have important roles in development and cell signalling. Matrix Biol. 16:1998;399-408.
39. Roberts D. D., Ginsburg V. Sulfated glycolipids and cell adhesion. Arch. Biochem. Biophys. 267:1988;405-415.
40. Sasaki T., Göhring W., Pan T.-C., Chu M.-L., Timpl R. Binding of mouse and human fibulin-2 to extracellular matrix ligands. J. Mol. Biol. 254:1995;892-899.
41. Sasaki T., Wiedemann H., Matzner M., Chu M.-L., Timpl R. Expression of fibulin-2 by fibroblasts and deposition with fibronectin into a fibrillar matrix. J. Cell Sci. 109:1996;2895-2904.
42. Sasaki T., Costell M., Mann K., Timpl R. Inhibition of glycosaminoglycan modification of perlecan domain I by site-directed mutagenesis changes protease sensitivity and laminin-1 binding activity. FEBS Letters. 435:1998;169-172.
43. Schulze B., Mann K., Battistutta R., Wiedemann H., Timpl R. Structural properties of recombinant domain III-3 of perlecan containing a globular domain inserted into an epidermal-growth-factor-like motif. Eur. J. Biochem. 231:1995;551-556.
44. Schulze B., Sasaki T., Costell M., Mann K., Timpl R. Structural and cell-adhesive properties of three recombinant fragments derived from perlecan domain III. Matrix Biol. 15:1996;349-537.
45. Shipley J. M., Doyle G. A. R., Fliszar C. J., Ye Q.-Z., Johnson L. L., Shapiro S. D., Welgus H. G., Senior R. M. The structural basis for the elastolytic activity of the 92 kDa and 72 kDa gelatinases. Role of the fibronectin type II-like repeats. J. Biol. Chem. 271:1996;4335-4341.
46. Talts J. F., Mann K., Yamada Y., Timpl R. Structural analysis and proteolytic processing of recombinant G domain of mouse laminin α2 chain. FEBS Letters. 426:1998;71-76.
47. Talts J. F., Andac Z., Göhring W., Brancaccio A., Timpl R. Binding of the G domains of laminin α1 and α2 chains and perlecan to heparin, sulfatides, α-dystroglycan and several extracellular matrix proteins. EMBO J. 18:1999;863-870.
48. Timpl R. Proteoglycans of basement membranes. Experientia. 49:1993;417-428.
49. Timpl R. Macromolecular assembly of basement membranes. Curr. Opin. Cell Biol. 8:1996;618-624.
50. Timpl R., Paulsson M., Dziadek M., Fujiwara S. Basement membranes. Methods Enzymol. 145:1987;363-391.
51. Vallejo A. N., Pogulis R. J., Pease L. R. In vitro synthesis of novel genes: mutagenesis and recombination by PCR. PCR Methods Appl. 4:1994;123-130.
52. Whitelock J. M., Murdoch A. D., Iozzo R. V., Underwood P. A. The degradation of human endothelial cell-derived perlecan and release of bound basic fibroblast growth factor by stromelysin, collagenase, plasmin and heparanases. J. Biol. Chem. 271:1996;10079-10086.
53. Whitelock J. M., Graham L. D., Melrose J., Murdoch A. D., Iozzo R. V., Underwood P. A. Human perlecan immunopurified from different endothelial cell sources has different adhesive properties for vascular cells. Matrix Biol. 18:1999;163-178.
54. Yurchenco P. D., Cheng Y.-S., Ruben G. C. Self-assembly of a high molecular weight basement membrane heparan sulfate proteoglycan into dimers and oligomers. J. Biol. Chem. 262:1987;17668-17676.