Collagen XII and XIV, new partners of cartilage oligomeric matrix protein in the skin extracellular matrix suprastructure

Journal of Biological Chemistry

Volumn 287, Issue 27, 2012, Pages 22549-22559

  Agarwal, Pallavi ^a   Zwolanek, Daniela ^a   Keene, Douglas R ^b   Schulz, Jan Niklas ^a   Blumbach, Katrin ^a   Heinegård, Dick ^c   Zaucke, Frank ^a   Paulsson, Mats ^a   Krieg, Thomas ^a   Koch, Manuel ^a   Eckes, Beate ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b SHRINERS HOSPITAL FOR CHILDREN   (United States)

^c LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTER PROTEINS; BASEMENT MEMBRANE; COLLAGEN I; COLOCALIZATION; EXTRACELLULAR MATRICES; HEALTHY HUMANS; HUMAN SKIN; MATRIX PROTEINS; PAPILLARY DERMIS; PROTEOGLYCANS; STRUCTURAL COMPONENT; TRIPLE-HELICES; VASCULATURE;

CARTILAGE; CELL CULTURE; OLIGOMERS;

COLLAGEN;

CARTILAGE OLIGOMERIC MATRIX PROTEIN; COLLAGEN TYPE 14; COLLAGEN TYPE 7;

ARTICLE; BASEMENT MEMBRANE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DERMIS; EMBRYO; EPIDERMIS; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SKIN FIBROBLAST; SKIN STRUCTURE; STRUCTURE ANALYSIS; ULTRASTRUCTURE;

ANIMALS; BASEMENT MEMBRANE; CHILD, PRESCHOOL; COLLAGEN; COLLAGEN TYPE I; COLLAGEN TYPE XII; DERMIS; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FIBROBLASTS; GLYCOPROTEINS; HEK293 CELLS; HUMANS; INFANT; KERATINOCYTES; MICE; MICROSCOPY, IMMUNOELECTRON; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SURFACE PLASMON RESONANCE;

EID: 84863319697     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.335935     Document Type: Article

References (68)

1. Kadler, K. E., Baldock, C., Bella, J., and Boot-Handford, R. P. (2007) Collagens at a glance. J. Cell Sci. 120, 1955-1958 (Pubitemid 47009991)
2. Myllyharju, J., and Kivirikko, K. I. (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20, 33-43 (Pubitemid 38032818)
3. Sorrell, J. M., and Caplan, A. I. (2004) Fibroblast heterogeneity. More than skin deep. J. Cell Sci. 117, 667-675 (Pubitemid 38263212)
4. Ezura, Y., Chakravarti, S., Oldberg, A., Chervoneva, I., and Birk, D. E. (2000) Differential expression of lumican and fibromodulin regulate collagen fibrillogenesis in developing mouse tendons. J. Cell Biol. 151, 779-788
5. Danielson, K. G., Baribault, H., Holmes, D. F., Graham, H., Kadler, K. E., and Iozzo, R. V. (1997) Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J. Cell Biol. 136, 729-743 (Pubitemid 27083772)
6. Rada, J. A., Cornuet, P. K., and Hassell, J. R. (1993) Regulation of corneal collagen fibrillogenesis in vitro by corneal proteoglycan (lumican and decorin) core proteins. Exp. Eye Res. 56, 635-648 (Pubitemid 23183821)
7. Birk, D. E., and Mayne, R. (1997) Localization of collagen types I, III and V during tendon development. Changes in collagen types I and III are correlated with changes in fibril diameter. Eur. J. Cell Biol. 72, 352-361 (Pubitemid 27170632)
8. Blaschke, U. K., Eikenberry, E. F., Hulmes, D. J., Galla, H. J., and Bruckner, P. (2000) Collagen XI nucleates self-assembly and limits lateral growth of cartilage fibrils. J. Biol. Chem. 275, 10370-10378 (Pubitemid 30202096)
9. Wotton, S. F., Duance, V. C., and Fryer, P. R. (1988) Type IX collagen. A possible function in articular cartilage. FEBS Lett. 234, 79-82
10. Shaw, L. M., and Olsen, B. R. (1991) FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem. Sci. 16, 191-194 (Pubitemid 121004433)
11. Ansorge, H. L., Meng, X., Zhang, G., Veit, G., Sun, M., Klement, J. F., Beason, D. P., Soslowsky, L. J., Koch, M., and Birk, D. E. (2009) Type XIV collagen regulates fibrillogenesis: Premature collagen fibril growth and tissue dysfunction in null mice. J. Biol. Chem. 284, 8427-8438
12. Keene, D. R., Lunstrum, G. P., Morris, N. P., Stoddard, D. W., and Burgeson, R. E. (1991) Two type XII-like collagens localize to the surface of banded collagen fibrils. J. Cell Biol. 113, 971-978 (Pubitemid 21909730)
13. Koch, M., Bohrmann, B., Matthison, M., Hagios, C., Trueb, B., and Chiquet, M. (1995) Large and small splice variants of collagen XII. Differential expression and ligand binding. J. Cell Biol. 130, 1005-1014
14. Veit, G., Hansen, U., Keene, D. R., Bruckner, P., Chiquet-Ehrismann, R., Chiquet, M., and Koch, M. (2006) Collagen XII interacts with avian tenascin-X through its NC3 domain. J. Biol. Chem. 281, 27461-27470 (Pubitemid 44401773)
15. Font, B., Eichenberger, D., Rosenberg, L. M., and van der Rest, M. (1996) Characterization of the interactions of type XII collagen with two small proteoglycans from fetal bovine tendon, decorin and fibromodulin. Matrix Biol. 15, 341-348 (Pubitemid 26419879)
16. Font, B., Aubert-Foucher, E., Goldschmidt, D., Eichenberger, D., and van der Rest, M. (1993) Binding of collagen XIV with the dermatan sulfate side chain of decorin. J. Biol. Chem. 268, 25015-25018 (Pubitemid 23335523)
17. Lethias, C., Carisey, A., Comte, J., Cluzel, C., and Exposito, J. Y. (2006) A model of tenascin-X integration within the collagenous network. FEBS Lett. 580, 6281-6285 (Pubitemid 44666814)
18. Giry-Lozinguez, C., Aubert-Foucher, E., Penin, F., Deleage, G., Dublet, B., and van der Rest, M. (1998) Identification and characterization of a heparin binding site within the NC1 domain of chicken collagen XIV. Matrix Biol. 17, 145-149 (Pubitemid 28310248)
19. Wälchli, C., Koch, M., Chiquet, M., Odermatt, B. F., and Trueb, B. (1994) Tissue-specific expression of the fibril-associated collagens XII and XIV. J. Cell Sci. 107, 669-681 (Pubitemid 24072898)
20. Hedbom, E., Antonsson, P., Hjerpe, A., Aeschlimann, D., Paulsson, M., Rosa-Pimentel, E., Sommarin, Y., Wendel, M., Oldberg, A., and Heinegård, D. (1992) Cartilage matrix proteins. An acidic oligomeric protein (COMP) detected only in cartilage. J. Biol. Chem. 267, 6132-6136
21. Oldberg, A., Antonsson, P., Lindblom, K., and Heinegård, D. (1992) COMP (cartilage oligomeric matrix protein) is structurally related to the thrombospondins. J. Biol. Chem. 267, 22346-22350
22. Mörgelin, M., Heinegård, D., Engel, J., and Paulsson, M. (1992) Electron microscopy of native cartilage oligomeric matrix protein purified from the Swarm rat chondrosarcoma reveals a five-armed structure. J. Biol. Chem. 267, 6137-6141
23. Efimov, V. P., Lustig, A., and Engel, J. (1994) The thrombospondin-like chains of cartilage oligomeric matrix protein are assembled by a five-stranded α-helical bundle between residues 20 and 83. FEBS Lett. 341, 54-58 (Pubitemid 24089189)
24. Briggs, M. D., Hoffman, S. M., King, L. M., Olsen, A. S., Mohrenweiser, H., Leroy, J. G., Mortier, G. R., Rimoin, D. L., Lachman, R. S., and Gaines, E. S. (1995) Pseudoachondroplasia and multiple epiphyseal dysplasia due to mutations in the cartilage oligomeric matrix protein gene. Nat. Genet. 10, 330-336
25. Hecht, J. T., Nelson, L. D., Crowder, E., Wang, Y., Elder, F. F., Harrison, W. R., Francomano, C. A., Prange, C. K., Lennon, G. G., and Deere, M. (1995) Mutations in exon 17B of cartilage oligomeric matrix protein (COMP) cause pseudoachondroplasia. Nat. Genet. 10, 325-329
26. Maddox, B. K., Keene, D. R., Sakai, L. Y., Charbonneau, N. L., Morris, N. P., Ridgway, C. C., Boswell, B. A., Sussman, M. D., Horton, W. A., Bächinger, H. P., and Hecht, J. T. (1997) The fate of cartilage oligomeric matrix protein is determined by the cell type in the case of a novel mutation in pseudoachondroplasia. J. Biol. Chem. 272, 30993-30997 (Pubitemid 27527544)
27. 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 (Pubitemid 47339208)
28. Hashimoto, Y., Tomiyama, T., Yamano, Y., and Mori, H. (2003) Mutation (D472Y) in the type 3 repeat domain of cartilage oligomeric matrix protein affects its early vesicle trafficking in endoplasmic reticulum and induces apoptosis. Am. J. Pathol. 163, 101-110 (Pubitemid 36759595)
29. 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)
30. 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 (Pubitemid 34919705)
31. 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
32. Piróg-Garcia, K. A., Meadows, R. S., Knowles, L., Heinegård, 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 (Pubitemid 47354890)
33. Suleman, F., Gualeni, B., Gregson, H. J., Leighton, M. P., Piróg, K. A., Edwards, S., Holden, P., Boot-Handford, R. P., and Briggs, M. D. (2012) A novel form of chondrocyte stress is triggered by a COMP mutation causing pseudoachondroplasia. Hum. Mutat. 33, 218-231
34. Svensson, L., Aszódi, A., Heinegård, D., Hunziker, E. B., Reinholt, F. P., Fässler, R., and Oldberg, A. (2002) Cartilage oligomeric matrix proteindeficient mice have normal skeletal development. Mol. Cell Biol. 22, 4366-4371 (Pubitemid 34556603)
35. Rosenberg, K., Olsson, H., Mörgelin, M., and Heinegård, D. (1998) Cartilage oligomeric matrix protein shows high affinity zinc-dependent interaction with triple helical collagen. J. Biol. Chem. 273, 20397-20403 (Pubitemid 28377606)
36. Halász, K., Kassner, A., Mörgelin, M., and Heinegård, D. (2007) COMP acts as a catalyst in collagen fibrillogenesis. J. Biol. Chem. 282, 31166-31173
37. 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
38. Thur, J., Rosenberg, K., Nitsche, D. P., Pihlajamaa, T., Ala-Kokko, L., Heinegård, 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
39. Vaughan, L., Mendler, M., Huber, S., Bruckner, P., Winterhalter, K. H., Irwin, M. I., and Mayne, R. (1988) D-periodic distribution of collagen type IX along cartilage fibrils. J. Cell Biol. 106, 991-997 (Pubitemid 18089999)
40. 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 (Pubitemid 38756782)
41. 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 (Pubitemid 47347530)
42. Hansen, U., Platz, N., Becker, A., Bruckner, P., Paulsson, M., and Zaucke, F. (2011) A secreted variant of cartilage oligomeric matrix protein carrying a chondrodysplasia-causing mutation (p.H587R) disrupts collagen fibrillogenesis. Arthritis Rheum. 63, 159-167
43. Spitznagel, L., Nitsche, D. P., Paulsson, M., Maurer, P., and Zaucke, F. (2004) Characterization of a pseudoachondroplasia-associated mutation (His-5873Arg) in the C-terminal, collagen-binding domain of cartilage oligomeric matrix protein (COMP). Biochem. J. 377, 479-487 (Pubitemid 38142203)
44. Koch, M., Schulze, J., Hansen, U., Ashwodt, T., Keene, D. R., Brunken, W. J., Burgeson, R. E., Bruckner, P., and Bruckner-Tuderman, L. (2004) A novel marker of tissue junctions, collagen XXII. J. Biol. Chem. 279, 22514-22521 (Pubitemid 38679451)
45. Gara, S. K., Grumati, P., Urciuolo, A., Bonaldo, P., Kobbe, B., Koch, M., Paulsson, M., and Wagener, R. (2008) Three novel collagen VI chains with high homology to the α3 chain. J. Biol. Chem. 283, 10658-10670
46. Koch, M., Veit, G., Stricker, S., Bhatt, P., Kutsch, S., Zhou, P., Reinders, E., Hahn, R. A., Song, R., Burgeson, R. E., Gerecke, D. R., Mundlos, S., and Gordon, M. K. (2006) Expression of type XXIII collagen mRNA and protein. J. Biol. Chem. 281, 21546-21557 (Pubitemid 44115491)
47. Kessler, D., Dethlefsen, S., Haase, I., Plomann, M., Hirche, F., Krieg, T., and Eckes, B. (2001) Fibroblasts in mechanically stressed collagen lattices assume a "synthetic" phenotype. J. Biol. Chem. 276, 36575-36585
48. Walzer, C., Benathan, M., and Frenk, E. (1989) Thermolysin treatment. A new method for dermo-epidermal separation. J. Invest. Dermatol. 92, 78-81 (Pubitemid 19027695)
49. Saalbach, A., Aust, G., Haustein, U. F., Herrmann, K., and Anderegg, U. (1997) The fibroblast-specific MAb AS02: a novel tool for detection and elimination of human fibroblasts. Cell Tissue Res. 290, 593-599 (Pubitemid 27522259)
50. Fuchs, E., and Green, H. (1980) Changes in keratin gene expression during terminal differentiation of the keratinocyte. Cell 19, 1033-1042 (Pubitemid 10155237)
51. Moll, R., Franke, W. W., Schiller, D. L., Geiger, B., and Krepler, R. (1982) The catalog of human cytokeratins. Patterns of expression in normal epithelia, tumors and cultured cells. Cell 31, 11-24 (Pubitemid 13215192)
52. Heinegård, D., and Saxne, T. (2011) The role of the cartilage matrix in osteoarthritis. Nat. Rev. Rheumatol. 7, 50-56
53. Di Cesare, P. E., Chen, F. S., Mörgelin, 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)
54. Farina, G., Lemaire, R., Korn, J. H., and Widom, R. L. (2006) Cartilage oligomeric matrix protein is overexpressed by scleroderma dermal fibroblasts. Matrix Biol. 25, 213-222 (Pubitemid 43729069)
55. Farina, G., Lemaire, R., Pancari, P., Bayle, J., Widom, R. L., and Lafyatis, R. (2009) Cartilage oligomeric matrix protein expression in systemic sclerosis reveals heterogeneity of dermal fibroblast responses to transforming growth factor beta. Ann. Rheum. Dis. 68, 435-441
56. Hesselstrand, R., Kassner, A., Heinegård, D., and Saxne, T. (2008) COMP. A candidate molecule in the pathogenesis of systemic sclerosis with a potential as a disease marker. Ann. Rheum. Dis. 67, 1242-1248
57. Gordon, M. K., and Olsen, B. R. (1990) The contribution of collagenous proteins to tissue-specific matrix assemblies. Curr. Opin. Cell Biol. 2, 833-838
58. Young, B. B., Gordon, M. K., and Birk, D. E. (2000) Expression of type XIV collagen in developing chicken tendons. Association with assembly and growth of collagen fibrils. Dev. Dyn. 217, 430-439 (Pubitemid 30185566)
59. Piróg, K. A., Jaka, O., Katakura, Y., Meadows, R. S., Kadler, K. E., Boot- Handford, R. P., and Briggs, M. D. (2010) A mouse model offers novel insights into the myopathy and tendinopathy often associated with pseudoachondroplasia and multiple epiphyseal dysplasia. Hum. Mol. Genet. 19, 52-64
60. Södersten, F., Ekman, S., Eloranta, M. L., Heinegård, D., Dudhia, J., and Hultenby, K. (2005) Ultrastructural immunolocalization of cartilage oligomeric matrix protein (COMP) in relation to collagen fibrils in the equine tendon. Matrix Biol. 24, 376-385 (Pubitemid 41021641)
61. Keene, D. R., Sakai, L. Y., Lunstrum, G. P., Morris, N. P., and Burgeson, R. E. (1987) Type VII collagen forms an extended network of anchoring fibrils. J. Cell Biol. 104, 611-621 (Pubitemid 17024716)
62. Villone, D., Fritsch, A., Koch, M., Bruckner-Tuderman, L., Hansen, U., and Bruckner, P. (2008) Supramolecular interactions in the dermo-epidermal junction zone. Anchoring fibril-collagen VII tightly binds to banded collagen fibrils. J. Biol. Chem. 283, 24506-24513
63. Sakai, L. Y., Keene, D. R., Morris, N. P., and Burgeson, R. E. (1986) Type VII collagen is a major structural component of anchoring fibrils. J. Cell Biol. 103, 1577-1586 (Pubitemid 17174180)
64. Krieg, T., Perlish, J. S., Mauch, C., and Fleischmajer, R. (1985) Collagen synthesis by scleroderma fibroblasts. Ann. N.Y. Acad. Sci. 460, 375-386 (Pubitemid 16074837)
65. Perlish, J. S., Lemlich, G., and Fleischmajer, R. (1988) Identification of collagen fibrils in scleroderma skin. J. Invest. Dermatol. 90, 48-54 (Pubitemid 18026954)
66. Haudenschild, D. R., Hong, E., Yik, J. H., Chromy, B., Mörgelin, M., Snow, K. D., Acharya, C., Takada, Y., and Di Cesare, P. E. (2011) Enhanced activity of transforming growth factor β1 (TGF-β1) bound to cartilage oligomeric matrix protein. J. Biol. Chem. 286, 43250-43258
67. Gabrielli, A., Avvedimento, E. V., and Krieg, T. (2009) Scleroderma. N. Engl. J. Med. 360, 1989-2003
68. Varga, J., and Abraham, D. (2007) Systemic sclerosis. A prototypic multisystem fibrotic disorder. J. Clin. Invest. 117, 557-567 (Pubitemid 46348510)