Inhibitor binding increases the mechanical stability of staphylococcal nuclease

Biophysical Journal

Volumn 100, Issue 4, 2011, Pages 1094-1099

  Wang, Chien Chung ^a,b   Tsong, Tian Yow ^b,c   Hsu, Yau Heiu ^a   Marszalek, Piotr E ^d  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b INSTITUTE OF PHYSICS   (Taiwan)

^c UNIVERSITY OF MINNESOTA   (United States)

^d Duke University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79951828755     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.01.011     Document Type: Article

References (58)

1. Schechter, A. N., R. F. Chen, and C. B. Anfinsen. 1970. Kinetics of folding of staphylococcal nuclease. Science. 167:886-887.
2. Chen, H. M., J. L. You, T. Y. Tsong. 1991. Kinetic analysis of the acid and the alkaline unfolded states of staphylococcal nuclease. J. Mol. Biol. 220:771-778.
3. Heins, J. N., J. R. Suriano, C. B. Anfinsen. 1967. Characterization of a nuclease produced by Staphylococcus aureus. J. Biol. Chem. 242:1016-1020.
4. Cotton, F. A., E. E. Hazen, Jr., and M. J. Legg. 1979. Staphylococcal nuclease: proposed mechanism of action based on structure of enzyme-thymidine 3′, 5′-bisphosphate-calcium ion complex at 1.5-Å resolution. Proc. Natl. Acad. Sci. USA. 76:2551-2555. (Pubitemid 9213905)
5. Tucker, P. W., E. E. Hazen, Jr., and F. A. Cotton. 1978. Staphylococcal nuclease reviewed: a prototypic study in contemporary enzymology. I. Isolation; physical and enzymatic properties. Mol. Cell. Biochem. 22:67-77.
6. Tucker, P. W., E. E. Hazen, Jr., and F. A. Cotton. 1979. Staphylococcal nuclease reviewed: a prototypic study in contemporary enzymology. II. Solution studies of the nucleotide binding site and the effects of nucleotide binding. Mol. Cell. Biochem. 23:3-16.
7. Anfinsen, C. B., P. Cuatrecasas, and H. Taniuchi. 1971. The Enzymes. Academic Press, New York.
8. Cuatrecasas, P., M. Wilchek, and C. B. Anfinsen. 1969. The action of staphylococcal nuclease on synthetic substrates. Biochemistry. 8:2277-2284.
9. 2O. J. Biol. Chem. 248:4769-4774.
10. Mikulski, A. J., E. Sulkowski, M. Laskowski, Sr. 1969. Susceptibility of dinucleotides bearing either 3′-or 5′-monophosphate to micrococcal nuclease. J. Biol. Chem. 244:6559-6565.
11. Sulkowski, E., and M. S. Laskowski. 1970. Hydrolysis of ribo-and deoxyribo-dinucleotides by micrococcal nuclease. Biochim. Biophys. Acta. 217:538-540.
12. Sugawara, T., K. Kuwajima, and S. Sugai. 1991. Folding of staphylococcal nuclease A studied by equilibrium and kinetic circular dichroism spectra. Biochemistry. 30:2698-2706.
13. Ishii, T., Y. Murayama, M. Sano. 2008. Probing force-induced unfolding intermediates of a single staphylococcal nuclease molecule and the effect of ligand binding. Biochem. Biophys. Res. Commun. 375:586-591.
14. Taniuchi, H., L. Morávek, and C. B. Anfinsen. 1969. Ligand-induced resistance of staphylococcal nuclease and nuclease-T to proteolysis by subtilisin, α-chymotrypsin, and thermolysin. J. Biol. Chem. 244:4600-4606.
15. Cao, Y., and H. Li. 2007. Polyprotein of GB1 is an ideal artificial elastomeric protein. Nat. Mater. 6:109-114. (Pubitemid 46197646)
16. Cao, Y., and H. Li. 2008. How do chemical denaturants affect the mechanical folding and unfolding of proteins? J. Mol. Biol. 375:316-324. (Pubitemid 350160691)
17. Cao, Y., T. Yoo, and H. Li. 2008. Single molecule force spectroscopy reveals engineered metal chelation is a general approach to enhance mechanical stability of proteins. Proc. Natl. Acad. Sci. USA. 105:11152-11157.
18. Carrion-Vazquez, M., A. F. Oberhauser, J. M. Fernandez. 1999. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl. Acad. Sci. USA. 96:3694-3699. (Pubitemid 29168972)
19. Clausen-Schaumann, H., M. Seitz, H. E. Gaub. 2000. Force spectroscopy with single bio-molecules. Curr. Opin. Chem. Biol. 4:524-530.
20. Dietz, H., F. Berkemeier, M. Rief. 2006. Anisotropic deformation response of single protein molecules. Proc. Natl. Acad. Sci. USA. 103:12724-12728. (Pubitemid 44298628)
21. Dietz, H., and M. Rief. 2004. Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proc. Natl. Acad. Sci. USA. 101:16192-16197. (Pubitemid 39552821)
22. Fernandez, J. M., and H. B. Li. 2004. Force-clamp spectroscopy monitors the folding trajectory of a single protein. Science. 303:1674-1678. (Pubitemid 38338326)
23. Lee, G., K. Abdi, P. E. Marszalek. 2006. Nanospring behavior of ankyrin repeats. Nature. 440:246-249.
24. Marszalek, P. E., H. Lu, J. M. Fernandez. 1999. Mechanical unfolding intermediates in titin modules. Nature. 402:100-103.
25. Oberhauser, A. F., and M. Carrión-Vázquez. 2008. Mechanical biochemistry of proteins one molecule at a time. J. Biol. Chem. 283:6617-6621.
26. Oberhauser, A. F., P. E. Marszalek, J. M. Fernandez. 1998. The molecular elasticity of the extracellular matrix protein tenascin. Nature. 393:181-185. (Pubitemid 28242260)
27. Rief, M., M. Gautel, H. E. Gaub. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 276:1109-1112. (Pubitemid 27218118)
28. Steward, A., J. L. Toca-Herrera, and J. Clarke. 2002. Versatile cloning system for construction of multimeric proteins for use in atomic force microscopy. Protein Sci. 11:2179-2183. (Pubitemid 34919621)
29. Serquera, D., W. Lee, L. S. Itzhaki. 2010. Mechanical unfolding of an ankyrin repeat protein. Biophys. J. 98:1294-1301.
30. Li, H., A. F. Oberhauser, J. M. Fernandez. 2000. Atomic force microscopy reveals the mechanical design of a modular protein. Proc. Natl. Acad. Sci. USA. 97:6527-6531. (Pubitemid 30412747)
31. Williams, P. M., S. B. Fowler, J. Clarke. 2003. Hidden complexity in the mechanical properties of titin. Nature. 422:446-449. (Pubitemid 36411399)
32. Rabbi, M., and P. E. Marszalek. 2008. Probing polysaccharide and protein mechanics by AFM. In Single Molecule Techniques: A Laboratory Manual. Paul R. Selvin, and Taekjip Ha, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 371-394.
33. Marszalek, P. E., A. F. Oberhauser, J. M. Fernandez. 1998. Polysaccharide elasticity governed by chair-boat transitions of the glucopyranose ring. Nature. 396:661-664. (Pubitemid 29003941)
34. Florin, E. L., M. Rief, H. E. Gaub. 1995. Sensing specific molecular-interactions with the atomic-force microscope. Biosens. Bioelectron. 10:895-901.
35. Bustamante, C., J. F. Marko, S. Smith. 1994. Entropic elasticity of λ-phage DNA. Science. 265:1599-1600.
36. Carra, J. H., and P. L. Privalov. 1996. Thermodynamics of denaturation of staphylococcal nuclease mutants: an intermediate state in protein folding. FASEB J. 10:67-74. (Pubitemid 26035508)
37. Dill, K. A., and D. Shortle. 1991. Denatured states of proteins. Annu. Rev. Biochem. 60:795-825.
38. Taniuchi, H., and C. B. Anfinsen. 1969. An experimental approach to the study of the folding of staphylococcal nuclease. J. Biol. Chem. 244:3864-3875.
39. Oberhauser, A. F., C. Badilla-Fernandez, J. M. Fernandez. 2002. The mechanical hierarchies of fibronectin observed with single-molecule AFM. J. Mol. Biol. 319:433-447. (Pubitemid 34729470)
40. Junker, J. P., K. Hell, M. Rief. 2005. Influence of substrate binding on the mechanical stability of mouse dihydrofolate reductase. Biophys. J. 89: L46-L48. (Pubitemid 41636047)
41. Law, R., P. Carl, D. E. Discher. 2003. Cooperativity in forced unfolding of tandem spectrin repeats. Biophys. J. 84:533-544. (Pubitemid 36026420)
42. Rief, M., J. Pascual, H. E. Gaub. 1999. Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles. J. Mol. Biol. 286:553-561. (Pubitemid 29090169)
43. Randles, L. G., R. W. S. Rounsevell, and J. Clarke. 2007. Spectrin domains lose cooperativity in forced unfolding. Biophys. J. 92:571-577. (Pubitemid 46145790)
44. Kim, M., K. Abdi, P. E. Marszalek. 2010. Fast and forceful refolding of stretched α-helical solenoid proteins. Biophys. J. 98:3086-3092.
45. Li, L., S. Wetzel, J. M. Fernandez. 2006. Stepwise unfolding of ankyrin repeats in a single protein revealed by atomic force microscopy. Biophys. J. 90: L30-L32.
46. Lu, H., and K. Schulten. 2000. The key event in force-induced unfolding of Titin's immunoglobulin domains. Biophys. J. 79:51-65. (Pubitemid 30436727)
47. Isralewitz, B., M. Gao, and K. Schulten. 2001. Steered molecular dynamics and mechanical functions of proteins. Curr. Opin. Struct. Biol. 11:224-230. (Pubitemid 32289426)
48. Lu, H., and K. Schulten. 1999. Steered molecular dynamics simulations of force-induced protein domain unfolding. Proteins. 35:453-463. (Pubitemid 29264842)
49. Cao, Y., K. S. Er, H. Li. 2009. A force-spectroscopy-based singlemolecule metal-binding assay. ChemPhysChem. 10:1450-1454.
50. Junker, J. P., F. Ziegler, and M. Rief. 2009. Ligand-dependent equilibrium fluctuations of single calmodulin molecules. Science. 323:633-637.
51. Bertz, M., and M. Rief. 2009. Ligand binding mechanics of maltose binding protein. J. Mol. Biol. 393:1097-1105.
52. Wilcox, A. J., J. Choy, A. Matouschek. 2005. Effect of protein structure on mitochondrial import. Proc. Natl. Acad. Sci. USA. 102:15435-15440. (Pubitemid 41528075)
53. Cao, Y., M. M. Balamurali, H. Li. 2007. A functional single-molecule binding assay via force spectroscopy. Proc. Natl. Acad. Sci. USA. 104:15677-15681. (Pubitemid 350035359)
54. Hann, E., N. Kirkpatrick, D. J. Brockwell. 2007. The effect of protein complexation on the mechanical stability of Im9. Biophys. J. 92: L79-L81. (Pubitemid 46684556)
55. Cao, Y., T. Yoo, H. Li. 2008. Protein-protein interaction regulates proteins' mechanical stability. J. Mol. Biol. 378:1132-1141.
56. Rief, M., J. P. Junker, W. Neupert. 2006. Response to the Comment by Ainavarapu et al. Biophys. J. 91:2011-2012.
57. Ainavarapu, S. R., L. Li, J. M. Fernandez. 2005. Ligand binding modulates the mechanical stability of dihydrofolate reductase. Biophys. J. 89:3337-3344. (Pubitemid 41636089)
58. Ainavarapu, S. R., L. Li, and J. M. Fernandez. 2006. Fingerprinting DHFR in single-molecule AFM studies. Biophys. J. 91:2009-2012.