Type III and v collagens modulate the expression and assembly of EDA + fibronectin in the extracellular matrix of defective Ehlers-Danlos syndrome fibroblasts

Biochimica et Biophysica Acta - General Subjects

Volumn 1820, Issue 10, 2012, Pages 1576-1587

  Zoppi, Nicoletta ^a   Ritelli, Marco ^a   Colombi, Marina ^a  

^a UNIVERSITY OF BRESCIA   (Italy)

Author keywords

Alternative splicing; Collagen; EDA region; Ehlers Danlos syndrome; Fibronectin; Integrins

Indexed keywords

ALPHA9 INTEGRIN; COLLAGEN TYPE 3; COLLAGEN TYPE 5; FIBRONECTIN; FOCAL ADHESION KINASE; INTEGRIN; MESSENGER RNA; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5;

ALTERNATIVE RNA SPLICING; ARTICLE; CELL LEVEL; COMPLEX FORMATION; CONTROLLED STUDY; EHLERS DANLOS SYNDROME; ENZYME BINDING; ENZYME PHOSPHORYLATION; EXTRACELLULAR MATRIX; FIBROBLAST; FIBRONECTIN 1 GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENETIC ORGANIZATION; HUMAN; HUMAN CELL; MOLECULAR PATHOLOGY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RNA SYNTHESIS; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION;

CASE-CONTROL STUDIES; CELLS, CULTURED; COLLAGEN TYPE III; COLLAGEN TYPE V; EHLERS-DANLOS SYNDROME; EXTRACELLULAR MATRIX; FEMALE; FIBROBLASTS; FIBRONECTINS; FOCAL ADHESION KINASE 1; GENE EXPRESSION REGULATION; HUMANS; INTEGRIN ALPHA5BETA1; INTEGRINS; MALE; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION;

EID: 84863477505     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2012.06.004     Document Type: Article

References (55)

1. P. Beighton, A. De Paepe, B. Steinmann, P. Tsipouras, and R.J. Wenstrup Ehlers-Danlos syndromes: revised nosology, Villefranche, 1997 Am. J. Med. Genet. 77 1998 31 37
2. B. Steinmann, P.M. Royce, and A. Superti-Furga The Ehlers-Danlos syndrome P.M. Royce, B. Steinmann, Connective Tissue and its Heritable Disorders 2002 Wiley-Liss New-York 431 523
3. I. Hausser, and I. Anton-Lamprecht Differential ultrastructural aberrations of collagen fibrils in Ehlers-Danlos syndrome type I-IV as a mean of diagnostic and classification Hum. Genet. 93 1994 394 407
4. S. Barlati, L. Moro, R. Gardella, and M. Colombi Phenotypic correction of the detective fibronectin extracellular matrix of Ehlers-Danlos syndrome fibroblasts Cell Biol. Int. Rep. 15 1991 1183 1194
5. N. Zoppi, A. Ghinelli, R. Gardella, S. Barlati, and M. Colombi Effect of dexamethasone on the assembly of the matrix of fibronectin and on its receptors organization in Ehlers-Danlos syndrome skin fibroblasts Cell Biol. Int. 22 1998 499 508
6. N. Zoppi, R. Gardella, A. De Paepe, S. Barlati, and M. Colombi Human fibroblasts with mutations in COL5A1 and COL3A1 genes do not organize collagen and fibronectin in the extracellular matrix, down-regulate α2β1 integrin and recruit αvβ3 instead of α5β1 integrin J. Biol. Chem. 279 2004 18157 18168
7. S. Viglio, N. Zoppi, A. Sangalli, A. Gallanti, S. Barlati, M. Mottes, M. Colombi, and M. Valli Rescue of migratory defects of Ehlers-Danlos syndrome fibroblasts in vitro by type V collagen but not insulin-like binding protein-1 J. Invest. Dermatol. 128 2008 1915 1919
8. N. Zoppi, S. Barlati, and M. Colombi FAK independent, αvβ3 integrin-EGFR complexes rescue from anoikis matrix-defective fibroblasts Biochim. Biophys. Acta, Mol. Cell. Res. 1783 2008 1177 1188
9. R.O. Hynes Integrins: versatility, modulation, and signaling in cell adhesion Cell 69 1992 11 25
10. F.G. Giancotti, and E. Rouslahti Integrin signaling Science 285 1999 1028 1032
11. B. Geiger, A. Bershadsky, R. Pankov, and K.M. Yamada Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk Nat. Rev. Mol. Cell Biol. 2 2001 793 805
12. R. Zaidel-Bar, S. Itzkovitz, A. Ma'ayan, R. Iyengar, and B. Geiger Functional atlas of the integrin adhesome Nat. Cell Biol. 9 2007 858 867
13. M. Colombi, L. Moro, N. Zoppi, A. Ghinelli, and S. Barlati Altered fibronectin mRNA splicing in skin fibroblasts from Ehlers-Danlos syndrome patients: in situ hybridization analysis Cell Biol. Int. Rep. 15 1991 1195 1206
14. A.R. Kornblihtt, K. Vibe-Pedersen, and F.E. Baralle Human fibronectin: cell specific alternative mRNA splicing generates polypeptide chains differing in the number of internal repeats Nucleic Acids Res. 12 1984 5853 5868
15. A.R. Kornblihtt, K. Umezawa, K. Vibe-Pedersen, and F.E. Baralle Primary structure of human fibronectin: differential splicing may generate at least 10 polypeptides from a single gene EMBO J. 4 1985 1755 1759
16. R.J. Owens, and F.E. Baralle Exon structure of the collagen-binding domain of human fibronectin FEBS Lett. 204 1986 318 322
17. A. Gutman, and A.R. Kornblihtt Identification of a third region of cell-specific alternative splicing in human fibronectin mRNA Proc. Natl. Acad. Sci. U. S. A. 84 1987 7179 7182
18. M. Colombi, S. Barlati, A. Kornblihtt, F.E. Baralle, and A. Vaheri A family of fibronectin RNAs in human normal and transformed cells Biochim. Biophys. Acta 868 1986 207 214
19. C. ffrench-Constant Alternative splicing of fibronectin - many different proteins but few different functions Exp. Cell Res. 221 1995 261 271
20. A.R. Kornblihtt, C.G. Pesce, C.R. Alonso, A. Cramer, A. Srebrow, S. Werbajh, and A.F. Muro The fibronectin gene as a model for splicing and transcription studies FASEB J. 10 1996 248 257
21. C. ffrench-Constant, L. Van De Water, H.F. Dvorak, and R.O. Hynes Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat J. Cell Biol. 109 1989 903 914
22. A.F. Muro, A.K. Chauhan, S. Gajovic, A. Iaconcig, F. Porro, G. Stanta, and F.E. Baralle Regulated splicing of the fibronectin EDA exon is essential for proper skin wound healing and normal lifespan J. Cell Biol. 162 2003 149 160
23. S. Dufour, J.-L. Duband, A.R. Kornblihtt, and J.P. Thiery The role of fibronectins in embryonic cell migrations Trends Genet. 4 1988 198 203
24. P.A. Norton, and R.O. Hynes Alternative splicing of chicken fibronectin in embryos and in normal and transformed cells Mol. Cell. Biol. 7 1987 4297 4307
25. R. Manabe, N. Ohe, T. Maeda, T. Fukuda, and K. Sekiguchi Modulation of cell-adhesive activity of fibronectin by the alternatively spliced EDA segment J. Cell Biol. 139 1997 295 307
26. R. Manabe, N. Oh-e, and K. Sekiguchi Alternatively spliced EDA segment regulates fibronectin-dependent cell cycle progression and mitogenic signal transduction J. Biol. Chem. 274 1999 5919 5924
27. R.A. Clark, H.J. Winn, H.F. Dvorak, and R.B. Colvin Fibronectin beneath reepithelializing epidermis in vivo: sources and significance J. Invest. Dermatol. 80 1983 26s 30s
28. W.R. Jarnagin, D.C. Rockey, V.E. Koteliansky, S.S. Wang, and D.M. Bissell Expression of variant fibronectins in wound healing: cellular source and biological activity of the EIIIA segment in rat hepatic fibrogenesis J. Cell Biol. 127 1994 2037 2048
29. G. Serini, M.L. Bochaton-Piallat, P. Ropraz, A. Geinoz, L. Borsi, L. Zardi, and G. Gabbiani The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1 J. Cell Biol. 142 1998 873 881
30. L. Moro, M. Colombi, M.P. Molinari Tosatti, and S. Barlati Study of fibronectin mRNA in human laryngeal and ectocervical carcinomas by in situ hybridization and image analysis Int. J. Cancer 51 1992 692 697
31. + mRNA isoforms: molecular markers for hepatocellular carcinoma Int. J. Cancer 56 1994 820 825
32. C.W.J. Smith, and J. Valcárcel Alternative pre-mRNA splicing: the logic of combinatorial control Trends Biochem. Sci. 25 2000 381 388
33. B.J. Blencowe Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases Trends Biochem. Sci. 25 2000 106 110
34. A. Srebrow, and A.R. Kornblihtt The connection between splicing and cancer J. Cell Sci. 119 2006 2635 2641
35. T. Seebacher, M. Manske, A.R. Kornblihtt, and E.G. Bade Cellular fibronectin is induced by epidermal growth factor, but not by dexamethasone or cyclic AMP in rat liver epithelial cells FEBS Lett. 239 1988 113 116
36. L. Borsi, P. Castellani, A.M. Risso, A. Leporini, and L. Zardi Transforming growth factor-beta regulates the splicing pattern of fibronectin messenger RNA precursor FEBS Lett. 261 1990 175 178
37. V.L. Magnuson, M. Young, D.G. Schattenberg, M.A. Mancini, D.L. Chen, B. Steffensen, and R.J. Klebe The alternative splicing of fibronectin pre-mRNA is altered during aging and in response to growth factors J. Biol. Chem. 266 1991 14654 14662
38. T. Inoue, K. Nabeshima, Y. Shimao, and M. Koono Hepatocyte growth factor/scatter factor (HGF/SF) is a regulator of fibronectin splicing in MDCK cells: comparison between the effects of HGF/SF and TGF-beta1 on fibronectin splicing at the EDA region Biochem. Biophys. Res. Commun. 260 1999 225 231
39. A. Srebrow, M. Blaustein, and A.R. Kornblihtt Regulation of fibronectin alternative splicing by a basement membrane-like extracellular matrix FEBS Lett. 514 2002 285 289
40. B. Drera, N. Zoppi, M. Ritelli, G. Tadini, M. Venturini, A. Wischmeijer, M.A. Nicolazzi, A. Musumeci, S. Penco, L. Buscemi, S. Crivelli, C. Danesino, M. Clementi, P. Calzavara-Pinton, S. Viglio, M. Valli, S. Barlati, and M. Colombi Diagnosis of vascular Ehlers-Danlos syndrome in Italy: clinical findings and novel COL3A1 mutations J. Dermatol. Sci. 64 2011 237 248
41. H.M. van der Straaten, M.R. Canniga-van Dijk, L.F. Verdonck, D. Castigliego, H.P.E. Borst, J. Aten, and R. Fijnheer Extra-domain-A fibronectin: a new marker of fibrosis in cutaneous graft-versus-host-disease J. Invest. Dermatol. 123 2004 1057 1062
42. S. Stamm Regulation of alternative splicing by reversible protein phosphorylation J. Biol. Chem. 283 2008 1223 1227
43. M. Blaustein, F. Pelisch, O.A. Coso, M.J. Bissel, A.R. Kornblihtt, and A. Srebrow Mammary epithelial-mesenchymal interaction regulates fibronectin alternative splicing via phosphatidylinositol 3-kinase J. Biol. Chem. 279 2004 21029 21037
44. F. Pelisch, M. Blaustein, A.R. Kornblihtt, and A. Srebrow Cross-talk between signalling pathway regulates alternative splicing J. Biol. Chem. 280 2005 25461 25469
45. M. Blaustein, F. Pelisch, and A. Srebrow Signals, pathways and splicing regulation Int. J. Biochem. Cell Biol. 39 2007 2031 2048
46. M. de la Mata, C.R. Alonso, S. Kadener, J.P. Fededa, M. Blaustein, F. Pelisch, P. Cramer, D. Bentley, and A.R. Kornblihtt A slow RNA polymerase II affects alternative splicing in vivo Mol. Cell 12 2003 525 532
47. P. Cramer, J.F. Cäceres, D. Cazalla, S. Kadener, A.F. Muro, F.E. Baralle, and A.R. Kornblihtt Coupling of transcription with alternative splicing: RNA pol II promoters modulate SF2/ASF and 9G8 effects on an exonic splicing enhancer Mol. Cell 4 1999 251 258
48. E.S. White, F.E. Baralle, and A.F. Muro New insights into form and function of fibronectin splice variants J. Pathol. 216 2008 1 14
49. A.R. Kornblihtt, M. de la Mata, J.P. Fededa, M.J. Muňoz, and G. Nogués Multiple links between transcription and splicing RNA 10 2004 1489 1498
50. A.V. Shinde, C. Bystroff, C. Wang, M.G. Vogelezang, P.A. Vincent, R.O. Hynes, and L. Van De Water Identification of the peptide sequences within the EIIIA (EDA) segment of fibronectin that mediate integrin α9β1- dependent cellular activities J. Biol. Chem. 283 2008 2858 2870
51. Y.-F. Liao, K.G. Wieder, J.M. Classen, and L. van Deee Water Identification of two amino acids within the EIIIA (ED-A) segment of fibronectin constituting the epitope for two function blocking monoclonal antibodies J. Biol. Chem. 274 1999 17876 17884
52. Y.-F. Liao, P.J. Gotwals, V.E. Koteliansky, D. Sheppard, and L. Van De Water The EIIIA segment of fibronectin is a ligand for integrins α9β1 and α4β1 providing a novel mechanism for regulating cell adhesion by alternative splicing J. Biol. Chem. 277 2002 14467 14474
53. P. Singht, C.L. Reimer, J.H. Peters, M.A. Stepp, R.O. Hynes, and L. Van De Water The spatial and temporal expression patterns of integrin α9β1 and one of its ligands, the EIIIA segment of fibronectin, in cutaneous wound healing J. Invest. Dermatol. 123 2004 1176 1181
54. H. Kohan, A.F. Muro, E.S. White, and N. Berkman EDA-containing cellular fibronectin induces fibroblasts differentiation through binding to α4β7 integrin receptor and MAPK/Erk1/2-dependent signalling FASEB J. 24 2010 4503 4512
55. J. Sottile, F. Shi, I. Rublyevska, H.-Y. Chiang, J. Lust, and J. Chandler Fibronectin-dependent collagen I deposition modulates the cell response to fibronectin Am. J. Physiol. Cell Physiol. 293 2007 1934 1946