Structural basis of sequence-specific collagen recognition by SPARC

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

Volumn 105, Issue 47, 2008, Pages 18273-18277

  Hohenester, Erhard ^a   Sasaki, Takako ^b,c   Giudici, Camilla ^b   Farndale, Richard W ^d   Bächinger, Hans Peter ^c,e  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e SHRINERS HOSPITAL FOR CHILDREN   (United States)

Author keywords

Extracellular matrix; X ray crystallography

Indexed keywords

ADHESIN; COLLAGEN; GLYCOPROTEIN; GLYCOPROTEIN 6; OSTEONECTIN; PHENYLALANINE; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; EMBRYO; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF;

AMINO ACID SEQUENCE; ANIMALS; COLLAGEN; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; OSTEONECTIN; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 57449115368     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0808452105     Document Type: Article

References (41)

1. Myllyharju J, Kivirikko KI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20:33-43.
2. Ameye L, Young MF Mice deficient in small leucine-rich proteoglycans: Novel in vivo models for osteoporosis, osteoarthritis, Ehlers-Danlos syndrome, muscular dystrophy, and corneal diseases. Glycobiology 12:107R-116R, 2002.
3. Leitinger B, Hohenester E (2007) Mammalian collagen receptors. Matrix Biol 26:146-155.
4. Heino J (2007) The collagen family members as cell adhesion proteins. Bioessays 29:1001-1010.
5. Sweeney SM, et al. (2008) Candidate cell and matrix interaction domains on the collagen fibril, the predominant protein of vertebrates. J Biol Chem 283:21187-21197.
6. Brodsky B, Persikov AV (2005) Molecular structure of the collagen triple helix. Adv Protein Chem 70:301-339.
7. Farndale RW, et al. (2008) Cell-collagen interactions: The use of peptide Toolkits to investigate collagen-receptor interactions. Biochem Soc Trans 36:241-250.
8. Knight CG, et al. (2000) The collagen-binding A-domains of integrins α1β1 and α2β1 recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem 275:35-40.
9. Xu Y, et al. (2000) Multiple binding sites in collagen type I for the integrins α1β1 and α2β1. J Biol Chem 275:38981-38989.
10. Emsley J, et al. (2000) Structural basis of collagen recognition by integrin α2β1. Cell 101:47-56.
11. Lisman T, et al. (2006) A single high-affinity binding site for von Willebrand factor in collagen III, identified using synthetic triple-helical peptides. Blood 108:3753-3756.
12. 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.
13. Giudici C, et al. (2008) Mapping of SPARC/BM-40/osteonectin- binding sites on fibrillar collagens. J Biol Chem 283:19551-19560.
14. Bradshaw AD, Sage EH (2001) SPARC, a matricellular protein that functions in cellular differentiation and tissue response to injury. J Clin Invest 107:1049-1054.
15. Rentz TJ, et al. (2007) SPARC regulates processing of procollagen I and collagen fibrillogenesis in dermal fibroblasts. J Biol Chem 282:22062-22071.
16. Fitzgerald MC, Schwarzbauer JE (1998) Importance of the basement membrane protein SPARC for viability and fertility in Caenorhabditis elegans. Curr Biol 8:1285-1288.
17. Martinek N, Shahab J, Saathoff M, Ringuette M (2008) Haemocyte-derived SPARC is required for collagen-IV-dependent stability of basal laminae in Drosophila embryos. J Cell Sci 121:1671-1680.
18. 2+--binding module in BM-40. Nat Struct Biol 3:67-73.
19. Hohenester E, Maurer P, Timpl R (1997) Crystal structure of a pair of follistatin-like and EF-hand calcium-binding domains in BM-40. EMBO J 16:3778-3786.
20. Sasaki T, Hohenester E, Göhring W, Timpl R (1998) Crystal structure and mapping by site-directed mutagenesis of the collagen-binding epitope of an activated form of BM-40/SPARC/osteonectin. EMBO J 17:1625-1634.
21. Bella J, Eaton M, Brodsky B, Berman HM (1994) Crystal and molecular structure of a collagen-like peptide at 1.9 Å resolution. Science 266:75-81.
22. Okuyama K, et al. (2006) Helical twists of collagen model peptides. Biopolymers 84:421-432.
23. Brandl M, et al. (2001) C-H⋯π-interactions in proteins. J Mol Biol 307:357-377.
24. Xie RL, Long GL (1995) Role of N-linked glycosylation in human osteonectin. Effect of carbohydrate removal by N-glycanase and site-directed mutagenesis on structure and binding of type V collagen. J Biol Chem 270:23212-23217.
25. Kaufmann B, et al. (2004) Structural variability of BM-40/SPARC/osteonectin glycosylation: Implications for collagen affinity. Glycobiology 14:609-619.
26. 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.
27. Maurer P, et al. (1995) The C-terminal portion of BM-40 (SPARC/osteonectin) is an autonomously folding and crystallisable domain that binds calcium and collagen IV. J Mol Biol 253:347-357.
28. Horii K, Kahn ML, Herr AB (2006) Structural basis for platelet collagen responses by the immune-type receptor glycoprotein VI. Blood 108:936-942.
29. Ichikawa O, et al. (2007) Structural basis of the collagen-binding mode of discoidin domain receptor 2. EMBO J 26:4168-4176.
30. Bella J, Brodsky B, Berman HM (1995) Hydration structure of a collagen peptide. Structure 3:893-906.
31. Maurer P, et al. (1997) Structural and functional characterization of the extracellular calcium-binding protein BM-40/secreted protein, acidic, rich in cysteine/osteonectin from the nematode Caenorhabditis elegans. Eur J Biochem 248:209-216.
32. Khoshnoodi J, Pedchenko V, Hudson BG (2008) Mammalian collagen IV. Microsc Res Tech 71:357-370.
33. Golbik R, Eble JA, Ries A, Kühn K (2000) The spatial orientation of the essential amino acid residues arginine and aspartate within the α1β1 integrin recognition site of collagen IV has been resolved using fluorescence resonance energy transfer. J Mol Biol 297:501-509.
34. Mayer U, et al. (1991) Calcium-dependent binding of basement membrane protein BM-40 (osteonectin, SPARC) to basement membrane collagen type IV. Eur J Biochem 198:141-150.
35. Bienkowska J, et al. (1997) The von Willebrand factor A3 domain does not contain a metal ion-dependent adhesion site motif. J Biol Chem 272:25162-25167.
36. Huizinga EG, et al. (1997) Crystal structure of the A3 domain of human von Willebrand factor: Implications for collagen binding. Structure 5:1147-1156.
37. Nishida N, et al. (2003) Collagen-binding mode of vWF-A3 domain determined by a transferred cross-saturation experiment. Nat Struct Biol 10:53-58.
38. Romijn RA, et al. (2003) Mapping the collagen-binding site in the von Willebrand factor-A3 domain. J Biol Chem 278:15035-15039.
39. Hellings M, et al. (2004) Experimental indication for the existence of multiple Trp rotamers in von Willebrand Factor A3 domain. Proteins 57:596-601.
40. Jarvis GE, et al. (2008) Identification of a major GpVI-binding locus in human type III collagen. Blood 111:4986-4996.
41. Zong Y, et al. (2005) A "Collagen Hug" model for Staphylococcus aureus CNA binding to collagen. EMBO J 24:4224-4236.