The shed ectodomain of type XIII collagen associates with the fibrillar fibronectin matrix and may interfere with its assembly in vitro

Biochemical Journal

Volumn 393, Issue 1, 2006, Pages 43-50

  Väisänen, Marja Riitta ^a   Väisänen, Timo ^a   Tu, Hongmin ^a   Pirilä, Päivi ^a   Sormunen, Raija ^a   Pihlajaniemi, Taina ^a  

^a UNIVERSITY OF OULU   (Finland)

Author keywords

Assembly; Extracellular matrix; Fibronectin; Remodelling; Shedding; Type XIII collagen

Indexed keywords

CELL CULTURE; ENZYMES; FIBROUS MEMBRANES; MODEL STRUCTURES; MOLECULES;

EXTRACELLULAR MATRIX; FIBRONECTIN; REMODELLING; SHEDDING; TYPE XIII COLLAGEN;

COLLAGEN;

COLLAGEN TYPE 13; FIBRILLAR COLLAGEN; FIBRONECTIN; SCLEROPROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRUCTURE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; IN VITRO STUDY; MAMMAL CELL; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; SKIN FIBROBLAST;

ANIMALS; CATTLE; CELLS, CULTURED; COLLAGEN TYPE XIII; CRICETINAE; EXTRACELLULAR MATRIX; FIBRONECTINS; GENE DELETION; HUMANS; PROCOLLAGEN; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; UP-REGULATION;

MAMMALIA;

EID: 30044436323     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20051073     Document Type: Article

References (45)

1. Geiger, B., Bershadsky, A., Pankov, R. and Yamada, K. M. (2001) Transmembrane extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2, 793-805
2. Vu, T. H. (2001) Don't mess with the matrix. Nat. Genet. 28, 202-203
3. Behonick, D. J. and Werb, Z. (2003) A bit of give and take: the relationship between the extracellular matrix and the developing chondrocyte. Mech. Dev. 120, 1327-1336
4. Kleinman, H. K., Philp, D. and Hoffman, M. P. (2003) Role of the extracellular matrix in morphogenesis. Curr. Opin. Biotechnol. 14, 526-532
5. Quaranta, V. and Giannelli, G. (2003) Cancer invasion: watch your neighbourhood! Tumori 89, 343-348
6. Weaver, V. M. and Gilbert, P. (2004) Watch thy neighbour: cancer is a communal affair. J. Cell Sci. 117, 1287-1290
7. van der Rest, M. and Garrone, R. (1991) Collagen family of proteins. FASEB J. 5, 2814-2823
8. Wierzbicka-Patynowski, I. and Schwarzbauer, J. E. (2003) The ins and ouls of fibronectin matrix assembly. J. Cell Sci. 116, 3269-3276
9. Romberger, D. J. (1997) Molecules in focus: fibronectin. Int. J. Biochem. Cell Biol. 29, 939-943
10. Schwarzbauer, J. E. and Sechler, J. L. (1999) Fibronectin fibrillogenesis: a paradigm for extracellular matrix assembly. Curr. Opin. Cell Biol. 11, 622-627
11. Armstrong, P. B. and Armstrong, M. T. (2000) Intercellular invasion and the organizational stability of tissues: a role for fibronectin. Biochim. Biophys. Acta 1470, 09-020
12. Pankov, R. and Yamada, K. M. (2002) Fibronectin at a glance. J. Cell Sci. 115, 3861-3863
13. Sasaki, T., Wiedemann, H., Matzner, M., Chu, M.-L. and Timpl, R. (1996) Expression of fibulin-2 by fibroblasts and deposition with fibronectin into a fibrillar matrix. J. Cell Sci. 109, 2895-2904
14. Chung, C. Y. and Erickson, H. P. (1997) Glycosaminoglycans modulate fibronectin matrix assembly and are essential for matrix incorporation of tenascin-C. J. Cell Sci. 110, 1413-1419
15. Pereira, M., Rybarczyk, B. J., Odrljin, T. M., Hocking, D. C., Sottile, J. and Simpson-Haidaris, P. J. (2002) The incorporation ot fibrinogen into extracellular matrix is dependent on active assembly of a fibronectin matrix. J. Cell Sci. 115, 609-617
16. Sottile, J. and Hocking, D. C. (2002) Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions. Mol. Biol. Cell 13, 3546-3559
17. Veiling, T., Risteli, J., Wennerberg, K., Mosher, D. F. and Johansson, S. (2002) Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins α11β1 and α2β1. J. Biol. Chem. 277, 37377-37381
18. Dzamba, B. J., Wu, H., Jaenisch, R. and Peters, D. M. (1993) Fibronectin binding site in type I collagen regulates fibronectin fibril formation. J. Cell Biol. 121, 1165-1172
19. Lebbe, C., Font, J., Bonaventure, J., Pichon, J., Wantyghem, J., Rossi, M., Haentjens, G., Cohen-Solal, L. and Aubery, M. (1997) Altered collagen of human pathological fibroblasts impairs the synthesis of fibronectin. Matrix Biol. 7, 503-507
20. Sabatelli, P., Bonaldo, P., Lattanzi, G., Braghetta, P., Bergamin, N., Capanni, C., Mattioli, E., Columbaro, M., Ognibene, A., Pepe, G. et al. (2001) Collagen VI deficiency affects the organization of fibronectin in the extracellular matrix of cultured fibroblasts. Matrix Biol. 20, 475-486
21. Zoppi, N., Gardella, R., De Paepe, A., Barlati, S. and Colombi, M. (2004) Human fibroblasts with mutations in COL5A1 and COL3A1 genes do not organize collagens and fibronectin in the extracellular matrix, down-regulate α2β1 integrin, and recruit αvβ3 instead of α5β1 integrin. J. Biol. Chem. 279, 18157-18168
22. Chernousov, M. A., Stahl, R. C. and Carey, D. J. (1998) Schwann cells use a novel collagen-dependent mechanism for fibronectin fibril assembly. J. Cell Sci. 111, 2763-2777
23. Engvall, E. and Ruoslahti, E. (1977) Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int. J. Cancer 20, 1-5
24. Kleinman, H., McGoodwin, E. B., Martin, G. R., Klebe, R. J., Fietzek, P. P. and Wooley, D. E. (1978) Localization of the binding site for cell attachment in the α1(1) chain of collagen. J. Biol. Chem. 253, 5642-5646
25. Balian, G., Click, E. M. and Bornstein, P. (1980) Location of a collagen-binding domain in fibronectin. J. Biol. Chem. 255, 3234-3236
26. Ruoslahti, E., Hayman, E. G., Engvall, E., Cothran, W. C. and Butler, W. T. (1981) Alignment of biologically active domains in the fibronectin molecule. J. Biol. Chem. 256, 7277-7281
27. Colombi, M., Zoppi, N., De Patro, G., Marchina, E., Gardella, R., Tavian, D., Ferraboli, S. and Barlati, S. (2003) Matrix assembly induction and cell migration and invasion inhibition by a 13-amino acid fibronectin peptide. J. Biol. Chem. 278, 14346-14355
28. Hägg, P., Rehn, M., Huhtala, P., Väisänen, T., Tamminen, M. and Pihlajaniemi, T. (1998) Type XIII collagen is identified as a plasma membrane protein. J. Biol. Chem. 273, 15590-15597
29. Hägg, P., Väisänen, T., Tuomisto, A., Rehn, M., Tu, H., Huhtala, P., Eskelinen, S. and Pihlajaniemi, T. (2001) Type XIII collagen: a novel cell adhesion component present in a range of cell-matrix adhesions and in the intercalated discs between cardiac muscle cells. Matrix Biol. 19, 727-742
30. Snellman, A., Tu, H., Väisänen, T., Kvist, A.-P., Huhtala, P. and Pihlajaniemi, T. (2000) A short sequence in the N-terminal region is required for the trimerization of type XIII collagen and is conserved in other collagenous transmembrane proteins. EMBO J. 19, 5051-5059
31. Väisänen, M.-R., Väisänen, T. and Pihlajaniemi, T. (2004) The shed ectodomain of type XIII collagen affects cell behaviour in a matrix-dependent manner. Biochem. J. 380, 685-693
32. Väisänen, T., Väisänen, M.-R., Autio-Harmainen, H. and Pihlajaniemi, T. (2005) Type XIII collagen expression is induced during malignant transformation in various epithelial and mesenchymal tumours. J. Pathol. 207, 324-335
33. Tu, H., Sasaki, T., Snellman, A., Göhring, W., Pirilä, P., Timpl, R. and Pihlajaniemi, T. (2002) The type XIII collagen ectodomain is a 150-nm rod and capable of binding to fibronectin, nidogen-2, perlecan and heparin. J. Biol. Chem. 277, 23092-23099
34. Pihlajaniemi, T. and Tamminen, M. (1990) The α1 chain of type XIII collagen consists of three collagenous and four noncollagenous domains, and its primary transcript undergoes complex alternative splicing. J. Biol. Chem. 265, 16922-16928
35. Harlow, E. and Lane, D. (1998) Antibodies, A Laboratory Manual, pp, 72-121, Cold Spring Harbor Laboratory Press, Plainview, NY
36. van Bergen en Henegouwen, P. M. P. (1989) Immunogold labelling of ultrathin cryosections. In Colloidal Gold: Principles, Methods, and Applications, vol. 1 (Hayat, M. A., ed.), pp. 191-216, Academic Press, San Diego, CA
37. Griffiths, G. (ed.) (1993) Labelling reactions for immunocytochemistry. In Fine Structure Immunocytochemistry, pp. 237-278, Springer-Verlag, Heidelberg
38. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989) In Molecular Cloning, A Laboratory Manual, pp, 1.38-1.39, Cold Spring Harbor Laboratory Press, Plainview, NY
39. Dang, D., Yang, Y., Li, X., Atakilit, A., Regezi, J., Eisele, D., Ellis, D. and Ramos, D. M. (2004) Matrix metalloproteinases and TGFβ1 modulate oral tumor cell matrix. Biochem. Biophys. Res. Commun. 316, 937-942
40. Seljelid, R., Jozefowski, S. and Sveinbjornsson, B. (1999) Tumor stroma. Anticancer Res. 19, 4809-4822
41. Sung, S.-Y. and Chung, L. W. K. (2002) Prostate tumor-stroma interaction: molecular mechanisms and opportunities for therapeutic targeting. Differentiation 70, 506-521
42. Tuxhorn, J. A., Ayala, G. E., Smith, M. J., Smith, V. C., Dang, T. D. and Rowley, D. R. (2002) Reactive stroma in human prostate cancer: induction of myofibroblast phenotype and extracellular matrix remodelling. Clin. Cancer Res. 8, 2912-2923
43. Bhowmick, N. A., Neilson, E. G. and Moses, H. L. (2004) Stromal fibroblasts in cancer initiation and progression. Nature (London) 432, 332-337
44. McDonald, J. A., Quade, B. J., Broekelmann, T. J., LaChance, R., Forsman, K., Hasegawa, E. and Akiyama, S. (1987) Fibronectin's cell-adhesive domain and an amino-terminal matrix assembly domain participate in its assembly into fibroblast pericellular matrix. J. Biol. Chem. 262, 2957-2967
45. Steffensen, B., Xu, X., Martin, P. A. and Zardeneta, G. (2002) Human fibronectin and MMP-2 collagen binding domains compete for collagen binding sites and modify activation of MMP-2, Matrix Biol. 21, 399-414