The crystal structure of the signature domain of cartilage oligomeric matrix protein: Implications for collagen, glycosaminoglycan and integrin binding

FASEB Journal

Volumn 23, Issue 8, 2009, Pages 2490-2501

  Tan, Kemin ^a   Duquette, Mark ^b   Joachimiak, Andrzej ^a   Lawler, Jack ^b  

^a ARGONNE NATIONAL LABORATORY   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Multiple epiphyseal dysplasia; Pseudoachondroplasia; Thrombospondins

Indexed keywords

CARTILAGE OLIGOMERIC MATRIX PROTEIN; COLLAGEN; EPIDERMAL GROWTH FACTOR; GLYCOSAMINOGLYCAN; INTEGRIN; LIGAND; METAL ION; RECOMBINANT PROTEIN; THROMBOSPONDIN; ARGINYL-GLYCYL-ASPARTIC ACID; ARGINYLGLYCYLASPARTIC ACID; CARTILAGE MATRIX PROTEIN; COMPLEMENTARY DNA; CYSTEINE; GLYCOPROTEIN; OLIGOPEPTIDE; SCLEROPROTEIN; THROMBOSPONDIN 1; THROMBOSPONDIN 2;

ARTICLE; BETA SHEET; BINDING SITE; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; CARTILAGE; CRYSTAL STRUCTURE; DISULFIDE BOND; LIGAND BINDING; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; IN VITRO STUDY; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; STATIC ELECTRICITY;

BASE SEQUENCE; BINDING SITES; COLLAGEN; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; DNA, COMPLEMENTARY; EXTRACELLULAR MATRIX PROTEINS; GLYCOPROTEINS; GLYCOSAMINOGLYCANS; HUMANS; INTEGRINS; LIGANDS; MODELS, MOLECULAR; MUTATION; OLIGOPEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; STATIC ELECTRICITY; THROMBOSPONDIN 1; THROMBOSPONDINS;

EID: 68849117986     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-128090     Document Type: Article

References (57)

1. Chen, F. H., Thomas, A. O., Hecht, J. T., Goldring, M. B., and Lawler, J. (2005) Cartilage oligomeric matrix protein/thrombospondin 5 supports chondrocyte attachment through interaction with integrins. J. Biol. Chem. 280, 32655-32661
2. Kipnes, J., Carlberg, A. L., Loredo, G. A., Lawler, J., Tuan, R. S., and Hall, D. J. (2003) Effect of cartilage oligomeric matrix protein on mesenchymal chondrogenesis in vitro. Osteoarthritis Cartilage 11, 442-454 (Pubitemid 36722658)
3. Xu, K., Zhang, Y., Ilalov, K., Carlson, C. S., Feng, J. Q., Di Cesare, P. E., and Liu, C. J. (2007) Cartilage oligomeric matrix protein associates with granulin-epithelin precursor (GEP) and potentiates GEP-stimulated chondrocyte proliferation. J. Biol. Chem. 282, 11347-11355
4. Budde, B., Blumbach, K., Ylostalo, J., Zaucke, F., Ehlen, H. W., Wagener, R., Ala-Kokko, L., Paulsson, M., Bruckner, P., and Grassel, S. (2005) Altered integration of matrilin-3 into cartilage extracellular matrix in the absence of collagen IX. Mol. Cell. Biol. 25, 10465-10478
5. Chen, F. H., Herndon, M. E., Patel, N., Hecht, J. T., Tuan, R. S., and Lawler, J. (2007) Interaction of cartilage oligomeric matrix protein/thrombospondin 5 with aggrecan. J. Biol. Chem. 282, 24591-24598
6. Di Cesare, P. E., Chen, F. S., Moergelin, M., Carlson, C. S., Leslie, M. P., Perris, R., and Fang, C. (2002) Matrix-matrix interaction of cartilage oligomeric matrix protein and fibronectin. Matrix Biol. 21, 461-470 (Pubitemid 35286612)
7. Halasz, K., Kassner, A., Morgelin, M., and Heinegard, D. (2007) COMP acts as a catalyst in collagen fibrillogenesis. J. Biol. Chem. 282, 31166-31173
8. Mann, H. H., Ozbek, S., Engel, J., Paulsson, M., and Wagener, R. (2004) Interactions between the cartilage oligomeric matrix protein and matrilins. Implications for matrix assembly and the pathogenesis of chondrodysplasias. J. Biol. Chem. 279, 25294-25298
9. Thur, J., Rosenberg, K., Nitsche, D. P., Pihlajamaa, T., Ala-Kokko, L., Heinegard, D., Paulsson, M., and Maurer, P. (2001) Mutations in cartilage oligomeric matrix protein causing pseudoachondroplasia and multiple epiphyseal dysplasia affect binding of calcium and collagen I, II, and IX. J. Biol. Chem. 276, 6083-6092 (Pubitemid 37373460)
10. Briggs, M. D., and Chapman, K. L. (2002) Pseudoachondroplasia and multiple epiphyseal dysplasia: mutation review, molecular interactions, and genotype to phenotype correlations. Hum. Mutat. 19, 465-478
11. Hecht, J. T., Hayes, E., Haynes, R., and Cole, W. G. (2005) COMP mutations, chondrocyte function and cartilage matrix. Matrix Biol. 23, 525-533 (Pubitemid 40202751)
12. Holden, P., Meadows, R. S., Chapman, K. L., Grant, M. E., Kadler, K. E., and Briggs, M. D. (2001) Cartilage oligomeric matrix protein interacts with type IX collagen, and disruptions to these interactions identify a pathogenetic mechanism in a bone dysplasia family. J. Biol. Chem. 276, 6046-6055
13. Rosenberg, K., Olsson, H., Morgelin, M., and Heinegard, D. (1998) Cartilage oligomeric matrix protein shows high affinity zinc-dependent interaction with triple helical collagen. J. Biol. Chem. 273, 20397-20403
14. Emsley, J., Knight, C. G., Farndale, R. W., Barnes, M. J., and Liddington, R. C. (2000) Structural basis of collagen recognition by integrin α2β1. Cell 101, 47-56
15. Giannoni, P., Siegrist, M., Hunziker, E. B., and Wong, M. (2003) The mechanosensitivity of cartilage oligomeric matrix protein (COMP). Biorheology 40, 101-109
16. Dinser, R., Zaucke, F., Kreppel, F., Hultenby, K., Kochanek, S., Paulsson, M., and Maurer, P. (2002) Pseudoachondroplasia is caused through both intra- and extracellular pathogenic pathways. J. Clin. Invest. 110, 505-513
17. Posey, K. L., Hankenson, K., Veerisetty, A. C., Bornstein, P., Lawler, J., and Hecht, J. T. (2008) Skeletal abnormalities in mice lacking extracellular matrix proteins, thrombospondin-1, thrombospondin-3, thrombospondin-5, and type IX collagen. Am. J. Pathol. 172, 1664-1674
18. Stanescu, R., Stanescu, V., Muriel, M. P., and Maroteaux, P. (1993) Multiple epiphyseal dysplasia, Fairbank type: morphologic and biochemical study of cartilage. Am. J. Med. Genet. 45, 501-507
19. Carlson, C. B., Bernstein, D. A., Annis, D. S., Misenheimer, T. M., Hannah, B. L., Mosher, D. F., and Keck, J. L. (2005) Structure of the calcium-rich signature domain of human thrombospondin-2. Nat. Struct. Mol. Biol. 12, 910-914
20. Kvansakul, M., Adams, J. C., and Hohenester, E. (2004) Structure of a thrombospondin C-terminal fragment reveals a novel calcium core in the type 3 repeats. EMBO. J. 23, 1223-1233 (Pubitemid 38524995)
21. Minor, W., Cymborowski, M., Otwinowski, Z., and Chruszcz, M. (2006) HKL-3000: the integration of data reduction and structure solution - from diffraction images to an initial model in minutes. Acta Crystallogr. 62, 859-866 (Pubitemid 44125661)
22. Brèunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. 54, 905-921 (Pubitemid 28443603)
23. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
24. Rudenko, G., Hohenester, E., and Muller, Y. A. (2001) LG/LNS domains: multiple functions - one business end? Trends Biochem. Sci. 26, 363-368 (Pubitemid 32530654)
25. Kawaji, H., Nishimura, G., Watanabe, S., Mabuchi, A., Ikeda, T., Ohashi, H., Sasaki, A., Sano, T., and Ikegawa, S. (2002) Autosomal dominant precocious osteoarthropathy due to a mutation of the cartilage oligomeric matrix protein (COMP) gene: further expansion of the phenotypic variations of COMP defects. Skel. Radiol. 31, 730-737
26. Lacy, D. B., Wigelsworth, D. J., Scobie, H. M., Young, J. A., and Collier, R. J. (2004) Crystal structure of the von Willebrand factor A domain of human capillary morphogenesis protein 2: an anthrax toxin receptor. Proc. Natl. Acad. Sci. U. S. A. 101, 6367-6372
27. Lee, J. O., Rieu, P., Arnaout, M. A., and Liddington, R. (1995) Crystal structure of the A domain from the alpha subunit of integrin CR3 (CD11b/CD18). Cell 80, 631-638
28. Shimaoka, M., Xiao, T., Liu, J. H., Yang, Y., Dong, Y., Jun, C. D., McCormack, A., Zhang, R., Joachimiak, A., Takagi, J., Wang, J. H., and Springer, T. A. (2003) Structures of the alpha L I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell 112, 99-111 (Pubitemid 36106422)
29. Song, G., Yang, Y., Liu, J. H., Casasnovas, J. M., Shimaoka, M., Springer, T. A., and Wang, J. H. (2005) An atomic resolution view of ICAM recognition in a complex between the binding domains of ICAM-3 and integrin αLβ2. Proc. Natl. Acad. Sci. U. S. A. 102, 3366-3371
30. Tan, K., Duquette, M., Liu, J. H., Shanmugasundaram, K., Joachimiak, A., Gallagher, J. T., Rigby, A. C., Wang, J. H., and Lawler, J. (2008) Heparin-induced cis- and trans-dimerization modes of the thrombospondin-1 N-terminal domain. J. Biol. Chem. 283, 3932-3941
31. Adams, J. C., Monk, R., Taylor, A. L., Ozbek, S., Fascetti, N., Baumgartner, S., and Engel, J. (2003) Characterisation of Drosophila thrombospondin defines an early origin of pentameric thrombospondins. J. Mol. Biol. 328, 479-494
32. Adams, J. C. (2004) Functions of the conserved thrombospondin carboxy-terminal cassette in cell-extracellular matrix interactions and signaling. Int. J. Biochem. Cell Biol. 36, 1102-1114
33. Adams, J. C., Bentley, A. A., Kvansakul, M., Hatherley, D., and Hohenester, E. (2008) Extracellular matrix retention of thrombospondin 1 is controlled by its conserved C-terminal region. J. Cell Sci. 121, 784-795 (Pubitemid 351578114)
34. Lawler, J., Ferro, P., and Duquette, M. (1992) Expression and mutagenesis of thrombospondin. Biochemistry 31, 1173-1180
35. Hecht, J. T., Makitie, O., Hayes, E., Haynes, R., Susic, M., Montufar-Solis, D., Duke, P. J., and Cole, W. G. (2004) Chondrocyte cell death and intracellular distribution of COMP and type IX collagen in the pseudoachondroplasia growth plate. J. Orthop. Res. 22, 759-767
36. Merritt, T. M., Bick, R., Poindexter, B. J., Alcorn, J. L., and Hecht, J. T. (2007) Unique matrix structure in the rough endoplasmic reticulum cisternae of pseudoachondroplasia chondrocytes. Am. J. Pathol. 170, 293-300
37. Vranka, J., Mokashi, A., Keene, D. R., Tufa, S., Corson, G., Sussman, M., Horton, W. A., Maddox, K., Sakai, L., and Bachinger, H. P. (2001) Selective intracellular retention of extracellular matrix proteins and chaperones associated with pseudoachondroplasia. Matrix Biol. 20, 439-450 (Pubitemid 33016381)
38. Hecht, J. T., Montufar-Solis, D., Decker, G., Lawler, J., Daniels, K., and Duke, P. J. (1998) Retention of cartilage oligomeric matrix protein and cell death in redifferentiated pseudoachondroplasia chondrocytes. Matrix Biol. 17, 625-633 (Pubitemid 29017229)
39. Hecht, J. T., Hayes, E., Snuggs, M., Decker, G., Montufar-Solis, D., Doege, K., Mwalle, F., Poole, R., Stevens, J., and Duke, P. J. (2001) Calreticulin, PDI, Grp94 and BiP chaperone proteins are associated with retained COMP in pseudoachondroplasia chondrocytes. Matrix Biol. 20, 251-262 (Pubitemid 32722196)
40. Schmitz, M., Becker, A., Schmitz, A., Weirich, C., Paulsson, M., Zaucke, F., and Dinser, R. (2006) Disruption of extracellular matrix structure may cause pseudoachondroplasia phenotypes in the absence of impaired cartilage oligomeric matrix protein secretion. J. Biol. Chem. 281, 32587-32595
41. Weirich, C., Keene, D. R., Kirsch, K., Heil, M., Neumann, E., and Dinser, R. (2007) Expression of PSACH-associated mutant COMP in tendon fibroblasts leads to increased apoptotic cell death irrespective of the secretory characteristics of mutant COMP. Matrix Biol. 26, 314-323 (Pubitemid 46660591)
42. Pirog-Garcia, K. A., Meadows, R. S., Knowles, L., Heinegard, D., Thornton, D. J., Kadler, K. E., Boot-Handford, R. P., and Briggs, M. D. (2007) Reduced cell proliferation and increased apoptosis are significant pathological mechanisms in a murine model of mild pseudoachondroplasia resulting from a mutation in the C-terminal domain of COMP. Hum. Mol. Genet. 16, 2072-2088
43. Carlson, C. B., Gunderson, K. A., and Mosher, D. F. (2008) Mutations targeting intermodular interfaces or calcium binding destabilize the thrombospondin-2 signature domain. J. Biol. Chem. 283, 27089-27099
44. Chen, T. L., Posey, K. L., Hecht, J. T., and Vertel, B. M. (2008) COMP mutations: domain-dependent relationship between abnormal chondrocyte trafficking and clinical PSACH and MED phenotypes. J. Cell. Biochem. 103, 778-787
45. Kawaji, H., Schonbach, C., Matsuo, Y., Kawai, J., Okazaki, Y., Hayashizaki, Y., and Matsuda, H. (2002) Exploration of novel motifs derived from mouse cDNA sequences. Genome Res. 12, 367-378 (Pubitemid 34233011)
46. Kennedy, J., Jackson, G., Ramsden, S., Taylor, J., Newman, W., Wright, M. J., Donnai, D., Elles, R., and Briggs, M. D. (2005) COMP mutation screening as an aid for the clinical diagnosis and counselling of patients with a suspected diagnosis of pseudoachondroplasia or multiple epiphyseal dysplasia. Eur. J. Hum. Genet. 13, 547-555
47. Arnaout, M. A., Goodman, S. L., and Xiong, J. P. (2002) Coming to grips with integrin binding to ligands. Curr. Opin. Cell Biol. 14, 641-651
48. Hynes, R. O. (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687
49. Luo, B. H., Carman, C. V., and Springer, T. A. (2007) Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25, 619-647
50. Springer, T. A., Zhu, J., and Xiao, T. (2008) Structural basis for distinctive recognition of fibrinogen γC peptide by the platelet integrin αIIbβ3. J. Cell Biol. 182, 791-800
51. Valdramidou, D., Humphries, M. J., and Mould, A. P. (2008) Distinct roles of β1 metal ion-dependent adhesion site (MIDAS), adjacent to MIDAS (ADMIDAS), and ligand-associated metal-binding site (LIMBS) cation-binding sites in ligand recognition by integrin α2β1. J. Biol. Chem. 283, 32704-32714
52. Pihlajamaa, T., Lankinen, H., Ylostalo, J., Valmu, L., Jaalinoja, J., Zaucke, F., Spitznagel, L., Gosling, S., Puustinen, A., Morgelin, M., Peranen, J., Maurer, P., Ala-Kokko, L., and Kilpelainen, I. (2004) Characterization of recombinant amino-terminal NC4 domain of human collagen IX: interaction with glycosaminoglycans and cartilage oligomeric matrix protein. J. Biol. Chem. 279, 24265-24273
53. Kyriakides, T. R., Zhu, Y. H., Smith, L. T., Bain, S. D., Yang, Z., Lin, M. T., Danielson, K. G., Iozzo, R. V., LaMarca, M., McKinney, C. E., Ginns, E. I., and Bornstein, P. (1998) Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis. J. Cell Biol. 140, 419-430 (Pubitemid 28078405)
54. Arnaout, M. A., Goodman, S. L., and Xiong, J. P. (2007) Structure and mechanics of integrin-based cell adhesion. Curr. Opin. Cell Biol. 19, 495-507
55. Xiong, J. P., Stehle, T., Zhang, R., Joachimiak, A., Frech, M., Goodman, S. L., and Arnaout, M. A. (2002) Crystal structure of the extracellular segment of integrin α Vβ3 in complex with an Arg-Gly-Asp ligand. Science 296, 151-155
56. Takagi, J. (2007) Structural basis for ligand recognition by integrins. Curr. Opin. Cell Biol. 19, 557-564
57. Mulloy, B., and Forster, M. J. (2000) Conformation and dynamics of heparin and heparan sulfate. Glycobiology 10, 1147-1156