Identification and structural analysis of type i collagen sites in complex with fibronectin fragments

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 11, 2009, Pages 4195-4200

  Erat, Michèle C ^a   Slatter, David A ^b   Lowe, Edward D ^c   Millard, Christopher J ^a   Farndale, Richard W ^b   Campbell, Iain D ^a   Vakonakis, Ioannis ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Collagen destabilization; Extracellular matrix; Protein structure

Indexed keywords

COLLAGEN TYPE 1; FIBRONECTIN; GELATIN; HELICASE; INTERSTITIAL COLLAGENASE;

ALPHA CHAIN; ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; EXPERIMENT; KINETICS; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

BINDING SITES; COLLAGEN TYPE I; CRYSTALLOGRAPHY, X-RAY; FIBRONECTINS; HUMANS; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DENATURATION;

VERTEBRATA;

EID: 63149115283     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0812516106     Document Type: Article

References (48)

1. Leitinger B, Hohenester E (2007) Mammalian collagen receptors. Matrix Biol 26:146-155.
2. Kadler KE, Hill A, Canty-Laird EG (2008) Collagen fibrillogenesis: Fibronectin, integrins, and minor collagens as organizers and nucleators. Curr Opin Cell Biol 20:495-501.
3. Vakonakis I, Campbell ID (2007) Extracellular matrix: From atomic resolution to ultra-structure. Curr Opin Cell Biol 19:578-583.
4. Pankov R, Yamada KM (2002) Fibronectin at a glance. J Cell Sci 115:3861-3863.
5. Mao Y, Schwarzbauer JE (2005) Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. Matrix Biol 24:389-399.
6. Dessau W, Adelmann BC, Timpl R (1978) Identification of the sites in collagen alpha-chains that bind serum anti-gelatin factor (cold-insoluble globulin). Biochem J 169:55-59.
7. Engvall E, Ruoslahti E (1977) Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int J Cancer 20:1-5.
8. Ingham KC, Brew SA, Isaacs BS (1988) Interaction of fibronectin and its gelatin-binding domains with fluorescent-labeled chains of type I collagen. J Biol Chem 263:4624-4628.
9. Ingham KC, Brew SA, Migliorini M (2002) Type I collagen contains at least 14 cryptic fibronectin binding sites of similar affinity. Arch Biochem Biophys 407:217-223.
10. Balian G, Click EM, Bornstein P (1980) Location of a collagen-binding domain in fibronectin. J Biol Chem 255:3234-3236.
11. Hynes R (1985) Molecular biology of fibronectin. Annu Rev Cell Biol 1:67-90.
12. McDonald JA, Kelley DG, Broekelmann TJ (1982) Role of fibronectin in collagen deposition: Fab' to the gelatin-binding domain of fibronectin inhibits both fibronectin and collagen organization in fibroblast extracellular matrix. J Cell Biol 92:485-492.
13. Iyer S, Visse R, Nagase H, Acharya KR (2006) Crystal structure of an active form of human MMP-1. J Mol Biol 362:78-88.
14. Kleinman HK, McGoodwin EB (1976) Localization of the cell attachment region in types I and II collagens. Biochem Biophys Res Commun 72:426-432.
15. Kleinman HK, et al. (1978) Localization of the binding site for cell attachment in the alpha1(I) chain of collagen. J Biol Chem 253:5642-5646.
16. Ingham KC, Brew SA, Migliorini MM (1989) Further localization of the gelatin-binding determinants within fibronectin. Active fragments devoid of type II homologous repeat modules. J Biol Chem 264:16977-16980.
17. Millard CJ, Campbell ID, Pickford AR (2005) Gelatin binding to the 8F19F1 module pair of human fibronectin requires site-specific N-glycosylation. FEBS Lett 579:4529-4534.
18. Katagiri Y, Brew SA, Ingham KC (2003) All six modules of the gelatin-binding domain of fibronectin are required for full affinity. J Biol Chem 278:11897-11902.
19. Baron M, Norman D, Willis A, Campbell ID (1990) Structure of the fibronectin type 1 module. Nature 345:642-646.
20. Pickford AR, Smith SP, Staunton D, Boyd J, Campbell ID (2001) The hairpin structure of the (6)F1(1)F2(2)F2 fragment from human fibronectin enhances gelatin binding. EMBO J 20:1519-1529.
21. Bingham RJ, et al. (2008) Crystal structures of fibronectin-binding sites from Staphylococcus aureus FnBPA in complex with fibronectin domains. Proc Natl Acad Sci USA 105:12254-12258.
22. Schwarz-Linek U, et al. (2003) Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423:177-181.
23. Wishart DS, Sykes BD, Richards FM (1992) The chemical shift index: A fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 31:1647-1651.
24. Remaut H, Waksman G (2006) Protein-protein interaction through beta-strand addition. Trends Biochem Sci 31:436-444.
25. Emsley J, Knight CG, Farndale RW, Barnes MJ, Liddington RC (2000) Structural basis of collagen recognition by integrin alpha2beta1. Cell 101:47-56.
26. Xu Y, et al. (2000) Multiple binding sites in collagen type I for the integrinsalpha1beta1 and alpha2beta1. J Biol Chem 275:38981-38989.
27. Siljander PR, et al. (2004) Integrin activation state determines selectivity for novel recognition sites in fibrillar collagens. J Biol Chem 279:47763-47772.
28. Perumal S, Antipova O, Orgel JP (2008) Collagen fibril architecture, domain organization, and triple-helical conformation govern its proteolysis. Proc Natl Acad Sci USA 105:2824-2829.
29. Orgel JP, Irving TC, Miller A, Wess TJ (2006) Microfibrillar structure of type I collagen in situ. Proc Natl Acad Sci USA 103:9001-9005.
30. Miles CA, Bailey AJ (2004) Studies of the collagen-like peptide (Pro-Pro-Gly)(10) confirm that the shape and position of the typeI collagen denaturation endotherm isgoverned by the rate of helix unfolding. J Mol Biol 337:917-931.
31. Litvinovich SV, Strickland DK, Medved LV, Ingham KC (1991) Domain structure and interactions of the type I and type II modules in the gelatin-binding region of fibronectin. All six modules are independently folded. J Mol Biol 217:563-575.
32. Ozeri V, et al. (1996) A two-domain mechanism for group A streptococcal adherence through protein F to the extracellular matrix. EMBO J 15:989-998.
33. Talay SR, et al. (2000) Co-operative binding of human fibronectin to Sfbl protein triggers streptococcal invasion into respiratory epithelial cells. Cell Microbiol 2:521-535.
34. Dinkla K, et al. (2003) Streptococcus pyogenes recruits collagen via surface-bound fibronectin: A novel colonization and immune evasion mechanism. Mol Microbiol 47:861-869.
35. Chung L, et al. (2004) Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J 23:3020-3030.
36. Muller JC, Ottl J, Moroder L (2000) Heterotrimeric collagen peptides as fluorogenic collagenase substrates: Synthesis, conformational properties, and enzymatic digestion. Biochemistry39:5111-5116.
37. Fiori S, Sacca B, Moroder L (2002) Structural properties of a collagenous heterotrimer that mimics the collagenase cleavage site of collagen type I. J Mol Biol 319:1235-1242.
38. Stultz CM (2002) Localized unfolding of collagen explains collagenase cleavage near imino-poor sites. J Mol Biol 319:997-1003.
39. Nerenberg PS, Salsas-Escat R, Stultz CM (2008) Do collagenases unwind triple-helical collagen before peptide bond hydrolysis? Reinterpreting experimental observations with mathematical models. Proteins 70:1154-1161.
40. Di Lullo GA, SweeneySM, Korkko J, Ala-Kokko L, San Antonio JD (2002) Mapping the ligand-binding sites and disease-associated mutations on the most abundant protein in the human, type I collagen. J Biol Chem 277:4223-4231.
41. Konitsiotis AD, et al. (2008) Characterization of high affinity binding motifs for the discoidin domain receptor DDR2 in collagen. J Biol Chem 283:6861-6868.
42. Friedl P, Wolf K (2008) Tube travel: The role of proteases in individual and collective cancer cell invasion. Cancer Res 68:7247-7249.
43. VakonakisI, Langenhan T, Promel S, RussA, Campbell ID (2008) Solution structure and sugar-binding mechanism ofmouselatrophilin-1 RBL: A7TM receptor-attached lectin-like domain. Structure (London) 16:944-953.
44. Slatter DA, Foley LA, Peachey AR, Nietlispach D, Farndale RW (2006) Rapid synthesis of a register-specific heterotrimeric type I collagen helix encompassing the integrin alpha2beta1 binding site. J Mol Biol 359:289-298.
45. Zwart PH, et al. (2008) Automated structure solution with the PHENIX suite. Methods Mol Biol 426:419-435.
46. Adams PD, et al. (2002) PHENIX: Building new software for automated crystallographic structure determination. Acta Crystallogr D 58:1948-1954.
47. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D 60:2126-2132.
48. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372:774-797.