Nanomechanical Properties of Tenascin-X Revealed by Single-Molecule Force Spectroscopy

Journal of Molecular Biology

Volumn 385, Issue 4, 2009, Pages 1277-1286

  Jollymore, Ashlee ^a   Lethias, Claire ^b   Peng, Qing ^a   Cao, Yi ^a   Li, Hongbin ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b University Lyon i   (France)

Author keywords

FnIII domains; mechanical unfolding; single molecule force spectroscopy; tenascin

Indexed keywords

FIBRONECTIN; FIBRONECTIN TYPE 3; POLYPROTEIN; TENASCIN; TENASCIN X; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; KINETICS; MOLECULAR MECHANICS; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE;

BOVINAE;

EID: 58149512051     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.11.038     Document Type: Article

References (35)

1. Erickson H.P. Tenascin-C, tenascin-R and tenascin-X: a family of talented proteins in search of functions. Curr. Opin. Cell Biol. 5 (1993) 869-876
2. Chiquet-Ehrismann R. Tenascins, a growing family of extracellular matrix proteins. Experientia 51 (1995) 853-862
3. Jones F.S., and Jones P.L. The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev. Dyn. 218 (2000) 235-259
4. Hsia H.C., and Schwarzbauer J.E. Meet the tenascins: multifunctional and mysterious. J. Biol. Chem. 280 (2005) 26641-26644
5. Erickson H.P. A tenascin knockout with a phenotype. Nat. Genet. 17 (1997) 5-7
6. Chiquet M. Regulation of extracellular matrix gene expression by mechanical stress. Matrix Biol. 18 (1999) 417-426
7. Tucker R.P., Drabikowski K., Hess J.F., Ferralli J., Chiquet-Ehrismann R., and Adams J.C. Phylogenetic analysis of the tenascin gene family: evidence of origin early in the chordate lineage. BMC Evol. Biol. 6 (2006) 60
8. Kammerer R.A., Schulthess T., Landwehr R., Lustig A., Fischer D., and Engel J. Tenascin-C hexabrachion assembly is a sequential two-step process initiated by coiled-coil alpha-helices. J. Biol. Chem. 273 (1998) 10602-10608
9. Erickson H.P., and Inglesias J.L. A six-armed oligomer isolated from cell surface fibronectin preparations. Nature 311 (1984) 267-269
10. Oberhauser A.F., Marszalek P.E., Erickson H.P., and Fernandez J.M. The molecular elasticity of the extracellular matrix protein tenascin. Nature 393 (1998) 181-185
11. Rief M., Gautel M., Schemmel A., and Gaub H.E. The mechanical stability of immunoglobulin and fibronectin III domains in the muscle protein titin measured by atomic force microscopy. Biophys. J. 75 (1998) 3008-3014
12. Wang M.J., Cao Y., and Li H.B. The unfolding and folding dynamics of TNfnALL probed by single molecule force-ramp spectroscopy. Polymer 47 (2006) 2548-2554
13. Cao Y., and Li H.B. Single molecule force spectroscopy reveals a weakly populated microstate of the FnIII domains of tenascin. J. Mol. Biol. 361 (2006) 372-381
14. Ng S.P., Rounsevell R.W., Steward A., Geierhaas C.D., Williams P.M., Paci E., and Clarke J. Mechanical unfolding of TNfn3: the unfolding pathway of a fnIII domain probed by protein engineering, AFM and MD simulation. J. Mol. Biol. 350 (2005) 776-789
15. Egging D.F., van Vlijmen I., Starcher B., Gijsen Y., Zweers M.C., Blankevoort L., et al. Dermal connective tissue development in mice: an essential role for tenascin-X. Cell Tissue Res. 323 (2006) 465-474
16. Egging D., van den Berkmortel F., Taylor G., Bristow J., and Schalkwijk J. Interactions of human tenascin-X domains with dermal extracellular matrix molecules. Arch. Dermatol. Res. 298 (2007) 389-396
17. Elefteriou F., Exposito J.Y., Garrone R., and Lethias C. Cell adhesion to tenascin-X mapping of cell adhesion sites and identification of integrin receptors. Eur. J. Biochem. 263 (1999) 840-848
18. Lethias C., Carisey A., Comte J., Cluzel C., and Exposito J.Y. A model of tenascin-X integration within the collagenous network. FEBS Lett. 580 (2006) 6281-6285
19. Elefteriou F., Exposito J.Y., Garrone R., and Lethias C. Binding of tenascin-X to decorin. FEBS Lett. 495 (2001) 44-47
20. Zweers M.C., van Vlijmen-Willems I.M., van Kuppevelt T.H., Mecham R.P., Steijlen P.M., Bristow J., and Schalkwijk J. Deficiency of tenascin-X causes abnormalities in dermal elastic fiber morphology. J. Invest. Dermatol. 122 (2004) 885-891
21. Burch G.H., Gong Y., Liu W., Dettman R.W., Curry C.J., Smith L., et al. Tenascin-X deficiency is associated with Ehlers-Danlos syndrome. Nat. Genet. 17 (1997) 104-108
22. Elefteriou F., Exposito J.Y., Garrone R., and Lethias C. Characterization of the bovine tenascin-X. J. Biol. Chem. 272 (1997) 22866-22874
23. Rief M., Gautel M., Oesterhelt F., Fernandez J.M., and Gaub H.E. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276 (1997) 1109-1112
24. Marko J.F., and Siggia E.D. Macromolecules 28 (1995) 8759-8770
25. Oberhauser A.F., Badilla-Fernandez C., Carrion-Vazquez M., and Fernandez J.M. The mechanical hierarchies of fibronectin observed with single-molecule AFM. J. Mol. Biol. 319 (2002) 433-447
26. Carrion-Vazquez M., Oberhauser A.F., Fowler S.B., Marszalek P.E., Broedel S.E., Clarke J., and Fernandez J.M. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl Acad. Sci. USA 96 (1999) 3694-3699
27. Cao Y., and Li H. Polyprotein of GB1 is an ideal artificial elastomeric protein. Nat. Mater. 6 (2007) 109-114
28. Peng Q., and Li H. Atomic force microscopy reveals parallel mechanical unfolding pathways of T4 lysozyme: evidence for a kinetic partitioning mechanism. Proc. Natl Acad. Sci. USA 105 (2008) 1885-1890
29. Lethias C., Elefteriou F., Parsiegla G., Exposito J.Y., and Garrone R. Identification and characterization of a conformational heparin-binding site involving two fibronectin type III modules of bovine tenascin-X. J. Biol. Chem. 276 (2001) 16432-16438
30. Lethias C., Descollonges Y., Boutillon M.M., and Garrone R. Flexilin: a new extracellular matrix glycoprotein localized on collagen fibrils. Matrix Biol. 15 (1996) 11-19
31. Krammer A., Lu H., Isralewitz B., Schulten K., and Vogel V. Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch. Proc. Natl Acad. Sci. USA 96 (1999) 1351-1356
32. Craig D., Gao M., Schulten K., and Vogel V. Tuning the mechanical stability of fibronectin type III modules through sequence variations. Structure 12 (2004) 21-30
33. Gao M., Craig D., Lequin O., Campbell I.D., Vogel V., and Schulten K. Structure and functional significance of mechanically unfolded fibronectin type III1 intermediates. Proc. Natl Acad. Sci. USA 100 (2003) 14784-14789
34. Wright C.F., Teichmann S.A., Clarke J., and Dobson C.M. The importance of sequence diversity in the aggregation and evolution of proteins. Nature 438 (2005) 878-881
35. Oberhauser A.F., Marszalek P.E., Carrion-Vazquez M., and Fernandez J.M. Single protein misfolding events captured by atomic force microscopy. Nat. Struct. Biol. 6 (1999) 1025-1028