Probing force-induced unfolding intermediates of a single staphylococcal nuclease molecule and the effect of ligand binding

Biochemical and Biophysical Research Communications

Volumn 375, Issue 4, 2008, Pages 586-591

  Ishii, Takaaki ^a   Murayama, Yoshihiro ^b   Katano, Atsuto ^a,b,c,d,e   Maki, Kosuke ^c   Kuwajima, Kunihiro ^d,e   Sano, Masaki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

^d OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

^e GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

Atomic force microscope (AFM); Ligand binding complex; Mechanical unfolding; Staphylococcal nuclease (SNase); Unfolding intermediate

Indexed keywords

GLOBULAR PROTEIN; NUCLEASE; STAPHYLOCOCCAL NUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; DYNAMICS; FORCE; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; STOCHASTIC MODEL; STRUCTURE ANALYSIS; THEORETICAL MODEL;

ACIDS; CALCIUM; LIGANDS; MICROCOCCAL NUCLEASE; MICROSCOPY, ATOMIC FORCE; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY;

EID: 51449113427     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2008.08.073     Document Type: Article

References (31)

1. Levinthal C. Are there pathways for protein folding?. J. Chem. Phys. 65 (1968) 44-45
2. Anfinsen C.B., and Scheraga H.A. Experimental and theoretical aspects of protein folding. Adv. Protein Chem. 29 (1975) 205-300
3. Ptitsyn O.B. Molten globule and protein folding. Adv. Protein Chem. 47 (1995) 83-229
4. Arai M., and Kuwajima K. Role of the molten globule state in protein folding. Adv. Protein Chem. 53 (2000) 209-282
5. Jackson S.E. How do small single-domain proteins fold?. Fold. Des. 3 (1998) R81-R91
6. Dill K.A., and Chan H.S. From Levinthal to pathways to funnels. Nat. Struct. Biol. 4 (1997) 10-19
7. Socci N.D., Onuchic J.N., and Wolynes P.G. Protein folding mechanisms and the multidimensional folding funnel. Proteins 32 (1998) 136-158
8. Radford S.E., Dobson C.M., and Evans P.A. The folding of hen lysozyme involves partially structured intermediates and multiple pathways. Nature 358 (1992) 302-307
9. Goldbeck R.A., Thomas Y.G., Chen E., Esquerra R.M., and Kliger D.S. Multiple pathways on a protein-folding energy landscape: kinetic evidence. Proc. Natl. Acad. Sci. USA 96 (1999) 2782-2787
10. Kamagata K., Sawano Y., Tanokura M., and Kuwajima K. Multiple parallel-pathway folding of proline-free Staphylococcal nuclease. J. Mol. Biol. 332 (2003) 1143-1153
11. Wright C.F., Lindorff-Larsen K., Randles L.G., and Clarke J. Parallel protein-unfolding pathways revealed and mapped. Nat. Struct. Biol. 10 (2003) 658-662
12. Rief M., Gautel M., Oesterhelt F., Fernandez J., and Gaub H.E. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276 (1997) 1109-1112
13. Oberhauser A.F., Hansma P.K., Vazquez M.C., and Fernandez J.M. Stepwise unfolding of titin under force-clamp atomic force microscopy. Proc. Natl. Acad. Sci. USA 98 (2001) 468-472
14. Diets H., and Rief M. Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proc. Natl. Acad. Sci. USA 101 (2004) 16192-16197
15. Taniuchi H., and Anfinsen C.B. An experimental approach to the study of the folding of staphylococcal nuclease. J. Biol. Chem. 244 (1969) 3864-3875
16. Jacobs M.D., and Fox R.O. Staphylococcal nuclease folding intermediate characterized by hydrogen exchange and NMR spectroscopy. Proc. Natl. Acad. Sci. USA 91 (1994) 449-453
17. Wang Y., and Shortle D. The equilibrium folding pathway of staphylococcal nuclease: identification of the most stable chain-chain interaction by NMR and CD spectroscopy. Biochemistry 34 (1995) 15895-15905
18. Walkenhorst W.F., Edwards J.A., Markley J.L., and Roder H. Early formation of a beta hairpin during folding of staphylococcal nuclease H124L as detected by pulsed hydrogen exchange. Protein Sci. 11 (2002) 82-91
19. Nelson E.D., and Grishin N.V. Efficient expansion, folding, and unfolding of proteins. Phys. Rev. E 70 (2004) 051906
20. Maki K., Ikura T., Hayano T., Takahashi N., and Kuwajima K. Effects of proline mutations on the folding of staphylococcal nuclease. Biochemistry 38 (1999) 2213-2223
21. Kunkel T.A. Rapid and efficient site-specific mutagenesis with-out phenotypic selection. Proc. Natl. Acad. Sci. USA 82 (1985) 488-492
22. Florin E.L., Reif M., Lehmann H., Ludwig M., Dornmair K., Moy V.T., and Gaub H. Sensing specific molecular interactions with the atomic force microscope. Biosens. Bioelectr. 10 (1995) 895-901
23. I. Sakane, Single-Molecular Unfolding of Staphylococcal Nuclease Studied by Intermolecular Force Microscopy. Dissertation, University of Tokyo, 2001.
24. Marko J.F., and Siggia E.D. Stretching DNA. Macromolecules 28 (1995) 8759-8770
25. Wang T., Arakawa H., and Ikai A. Force measurement and inhibitor binding assay of monomer and engineered dimer of bovine carbonic anhydrase B. Biochem. Biophys. Res. Commun. 285 (2001) 9-14
26. Hertadi R., Gruswitz F., Silver L., Koide A., Koide S., Arakawa H., and Ikai A. Unfolding mechanics of multiple OspA substructures investigated with single molecule force spectroscopy. J. Mol. Biol. 333 (2003) 993-1002
27. Cecconi C., Shank E.A., Bustamante C.S., and Marqusee S. Direct observation of the three-state folding of a single protein molecule. Science 309 (2005) 2057-2060
28. Gillespie J., and Shortle D. Characterization of long-range structure in the denatured state of staphylococcal nuclease. I. Paramagnetic relaxation enhancement by nitroxide spin labels. J. Mol. Biol. 268 (1997) 158-169
29. Yi Q., Scalley-Kim M.L., Alm E.J., and Baker D. NMR characterization of residual structure in the denatured state of protein L. J. Mol. Biol. 299 (2000) 1341-1351
30. Sugawara T., Kuwajima K., and Sugai S. Folding of staphylococcal nuclease A studied by equilibrium and kinetic circular dichroism spectra. Biochemistry 30 (1991) 2698-2706
31. Cotton F.A., Hazen Jr. E.E., and Legg M.J. Staphylococcal nuclease: Proposed mechanism of action based on structure of enzyme- thymidine 3′,5′-bisphosphate-calcium ion complex at 1.5-angstrom resolution. Proc. Natl. Acad. Sci. USA 76 (1979) 2551-2555