Module-module interactions in the cell binding region of fibronectin: Stability, flexibility and specificity

Journal of Molecular Biology

Volumn 265, Issue 5, 1997, Pages 565-579

  Spitzfaden, Claus ^a,c   Grant, Richard P ^b   Mardon, Helen J ^b   Campbell, Iain D ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^c GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Fluorescence; Nuclear magnetic resonance; Protein folding; Relaxation

Indexed keywords

FIBRONECTIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENETIC ENGINEERING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; THERMODYNAMICS;

EID: 0031556949     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0736     Document Type: Article

References (59)

1. Abragam A. Principles of Nuclear Magnetism. 1961;Oxford University Press, Oxford.
2. Antonsson P., Kammerer R. A., Schulthess T., Hanisch G., Engel J. Stabilization of the α-helical coiled-coil domain in laminin by C-terminal disulfide bonds. J. Mol. Biol. 250:1995;74-79.
3. Aota A., Nagai T., Yamada K. M. Characterization of regions of fibronectin besides the arginine-glycine-aspartic acid sequence required for adhesive function of the cell binding domain using site-directed mutagenesis. J. Biol. Chem. 266:1991;15938-15943.
4. Aota S., Nomizu M., Yamada K. M. The short amino-acid-sequence Pro-His-Ser-Arg-Asn in human fibronectin enhances cell-adhesive function. J. Biol. Chem. 269:1994;24756-24761.
5. 15N relaxation using inverse detected 2-dimensional NMR spectroscopy - the central helix is flexible. Biochemistry. 31:1992;5269-5278.
6. Barlow P. N., Steinkasserer A., Norman D. G., Kieffer B., Wiles A. P., Sim R. B., Campbell I. D. Solution structure of a pair of complement modules by nuclear magnetic-resonance. J. Mol. Biol. 232:1993;268-284.
7. 1H-NMR assignment and secondary structure of the cell-adhesion type-III module of fibronectin. Biochemistry. 31:1992;2068-2073.
8. Bartels C., Xia T.-H., Billeter M., Güntert P., Wüthrich K. The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR. 5:1995;1-10.
9. Bodenhausen G., Ruben D.J. Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Letters. 69:1980;185-188.
10. Bork P., Downing A. K., Kieffer B., Campbell I. D. Structure and distribution of modules in extracellular proteins. Quart. Rev. Biophys. 28:1996;119-167.
11. Bowditch R. D., Hariharan M., Tominna E. F., Smith J. W., Yamada K. M., Getzoff E. D., Ginsberg M. H. Identification of a novel integrin binding-site in fibronectin - differential utilization by β-3 integrins. J. Biol. Chem. 269:1994;10856-10863.
12. 2-terminal domains. Science. 260:1993;979-983.
13. Brüschweiler R., Liao X. B., Wright P. E. Long-range motional restrictions in a multidomain zinc-finger protein from anisotropic tumbling. Science. 268:1995;886-889.
14. Campbell I. D., Downing A. K. Building protein-structure and function from modular units. Trends Biotechnol. 12:1994;168-172.
15. Campbell I. D., Spitzfaden C. Building proteins with fibronectin type III modules. Structure. 2:1994;333-337.
16. 1. J. Biol. Chem. 270:1995;21612-21618.
17. delaTorre J. G., Navarro S., Martinez M. C. L., Diaz F. G., Cascales J. J. L. HYDRO - a computer program for the prediction of hydrodynamic properties of macromolecules. Biophys. J. 67:1994;530-531.
18. Dickinson C. D., Veerapandian B., Dai X. P., Hamlin R. C., Xuong N. H., Ruoslahti E., Ely K. R. Crystal-structure of the 10th type-III cell-adhesion module of human fibronectin. J. Mol. Biol. 236:1994;1079-1092.
19. Doolittle R. F. The multiplicity of domains in proteins. Annu. Rev. Biochem. 236:1995;1079-1092.
20. Eck M. J., Pluskey S., Trub T., Harrison S. C., Shoelson S. E. Spatial constraints on the recognition of phosphoproteins by the tandem SH2 domains of the phosphatase S H-PTP2. Nature. 379:1996;277-280.
21. Eustance R. J., Bustos S. A., Schleif R. F. Locating and lengthening the interdomain linker in araC protein. J. Mol. Biol. 242:1994;330-338.
22. Fersht A. Enzyme Structure and Mechanism. 1977;Freeman, New York.
23. Fesik S. W., Zuiderweg E. R. P. Heteronuclear 3-dimensional NMR-spectroscopy - a strategy for the simplification of homonuclear two-dimensional NMR-spectra. J. Magn. Reson. 78:1988;588-593.
24. Grzesiek S., Bax A. Improved 3D triple resonance NMR techniques applied to a 31 kDa protein. J. Magn. Reson. 96:1992a;432-440.
25. Grzesiek S., Bax A. Correlating backboneamide and side-chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114:1992b;6291-6293.
26. Güntert P., Braun W., Wüthrich K. Efficient computation of 3-dimensional protein structures in solution from nuclear-magnetic-resonance data using the program DIANA and the supporting programs caliba, HABAS and GLOMSA. J. Mol. Biol. 217:1991;517-530.
27. 15N relaxation studies of the amino-terminal fragment of urokinase type plasminogen-activator. Biochemistry. 33:1994;15418-15424.
28. Huber A. H., Wang Y. M. E., Bieber A. J., Bjorkman P. J. Crystal-structure of tandem type-III fibronectin domains from Drosophila neuroglian at 2.0 angstrom. Neuron. 12:1994;717-731.
29. Hynes R. O. Fibronectins. 1990;Springer-Verlag, New York.
30. 15N spectra of larger proteins - heteronuclear triple-resonance 3-dimensional NMR-spectroscopy - application to calmodulin. Biochemistry. 29:1990;4659-4667.
31. Jackson S. E., Elmasry N., Fersht A. R. Structure of the hydrophobic core in the transition-state for folding of chymotrypsin inhibitor-2 - a critical test of the protein engineering method of analysis. Biochemistry. 32:1993a;11270-11278.
32. Jackson S. E., Moracci M., Elmasry N., Johnson C. M., Fersht A. R. Effect of cavity-creating mutations in the hydrophobic core of chymotrypsin inhibitor-2. Biochemistry. 32:1993b;11259-11269.
33. Jones E. Y., Davis S. J., Williams A. F., Harlos K., Stuart D. J. Crystal-structure at 2.8-angstrom resolution of a soluble form of the cell-adhesion molecule CD2. Nature. 360:1992;232-239.
34. Jones E. Y., Harlos K., Bottomley M. J., Robinson R. C., Driscoll P. C., Edwards R. M., Clements J. M., Dudgeon T. J., Stuart D. J. Crystal-structure of an integrin binding fragment of vascular cell-adhesion molecule-1 at 1.8 angstrom resolution. Nature. 373:1995;539-544.
35. 2O. J. Am. Chem. Soc. 115:1993;2055-2057.
36. Kornblihtt A. R., Umezawa K., Vibe-Pedersen K., Baralle F. E. Primary structure of human fibronectin - differential splicing may generate at least 10 polypeptides from a single gene. EMBO J. 4:1985;1755-1759.
37. Kraulis P. J. Molscript - a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
38. Leahy D. J., Aukhil I., Erickson H. P. 2.0 Angstrom crystal-structure of a 4-domain segment of human fibronectin encompassing the RGD loop and synergy region. Cell. 84:1996;155-164.
39. Lipari G., Szabo A. Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104:1982;4546-4559.
40. Litvinovich S. V., Ingham K. C. Interactions between type-III domains in the 110-kDa cell-binding fragment of fibronectin. J. Mol. Biol. 248:1995;611-626.
41. Main A. L., Harvey T. S., Baron M., Boyd J., Campbell I. D. The 3-dimensional structure of the 10th type-III module of fibronectin an insight into RGD-mediated interactions. Cell. 71:1992;671-678.
42. Mardon H. J., Grant K. E. The role of the 9th and 10th type-III domains of human fibronectin in cell-adhesion. FEBS Letters. 340:1994;197-201.
43. Mosher D. F. Fibronectin. 1989;Academic Press, New York.
44. Nakaseko Y., Neuhaus D., Klug A., Rhodes D. Adjacent zinc-finger motifs in multiple zinc-finger peptides from SW15 form structurally independent, flexibly linked domains. J. Mol. Biol. 228:1992;619-636.
45. Obara M., Kang M. S., Yamada K. M. Site-directed mutagenesis of the cell-binding domain of human fibronectin - separable, synergistic sites mediate adhesive function. Cell. 53:1988;649-657.
46. Omichinski J. G., Clore G. M., Robien M., Sakaguchi K., Appella E., Gronenborn A. M. High-resolution solution structure of the double Cys2His2 zinc finger from the human enhancer binding-protein MBP-1. Biochemistry. 31:1992;3907-3917.
47. Pace C. N., Shirley B. A., Thomson J. A. Measuring the conformational stability of a protein. Protein Structure, a Practical Approach. 1989;IRL Press, Oxford.
48. Palmer A. G., Skelton N. J., Chazin W. J., Wright P. E., Rance M. Suppression of the effects of cross-correlation between dipolar and anisotropic chemical shift relaxation mechanisms in the measurement of spin spin relaxation rates. Mol. Phys. 75:1992;699-711.
49. Pierschbacher M. D., Ruoslahti E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature. 309:1984;30-33.
50. Politou A. S., Gautel M., Joseph C., Pastore A. Immunoglobulin-type domains of titin are stabilized by amino-terminal extension. FEBS Letters. 352:1994;27-31.
51. Politou A. S., Gautel M., lmprota S., Vangelista I., Pastore A. The elastic i-band region of titin is assembled in a modular fashion by weakly interacting Ig-like domains. J. Mol. Biol. 255:1996;604-616.
52. Potts J. R., Campbell I. D. Fibronection structure and assembly. Curr. Opin. Cell Biol. 6:1994;648-655.
53. Schleucher J., Schwendinger M., Sattler M., Schmidt P., Schedletzky O., Sorensen O. W., Griesinger C. A general enhancement scheme in heteronuclear multidimensional NMR employing pulsed field gradients. J. Biomol. NMR. 4:1994;301-306.
54. Smith B. O., Downing A. K., Driscoll P. C., Dudgeon T. J., Campbell I. D. The solution structure and backbone dynamics of the fibronectin type-I and epidermal growth factor-like pair of modules of tissue-type plasminogen-activator. Structure. 3:1995;823-833.
55. Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 67:1988;31-40.
56. 15N NMR relaxation. J. Am. Chem. Soc. 117:1995a;12562-12566.
57. 15N-NMR relaxation measurements. Eur. J. Biochem. 230:1995b;1014-1024.
58. Wang J. H., Yan Y. W., Garrett T. P. J., Liu J. H., Rodgers D. W., Garlick R. L., Tarr G. E., Husain Y., Reinherz E. L., Harrison S. C. Atomic-structure of a fragment of human CD4 containing 2 immunoglobulin-like domains. Nature. 348:1990;411-418.
59. Williams M. J., Phan I., Harvey T. S., Rostagno A., Gold L. I., Campbell I. D. Solution structure of a pair of fibronectin type-1 modules with fibrin binding-activity. J. Mol. Biol. 235:1994;1302-1311.