Direct measurements of the mechanical stability of zinc-thiolate bonds in rubredoxin by single-molecule atomic force microscopy

Biophysical Journal

Volumn 101, Issue 6, 2011, Pages 1467-1473

  Zheng, Peng ^a   Li, Hongbin ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEAL PROTEIN; RUBREDOXIN; SULFUR; ZINC;

ARTICLE; ATOMIC FORCE MICROSCOPY; CHEMICAL STRUCTURE; CHEMISTRY; MECHANICS; PROTEIN CONFORMATION; PYROCOCCUS FURIOSUS;

ARCHAEAL PROTEINS; MECHANICAL PROCESSES; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; PROTEIN CONFORMATION; PYROCOCCUS FURIOSUS; RUBREDOXINS; SULFUR; ZINC;

EID: 80053123524     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.08.021     Document Type: Article

References (50)

1. J. Miller, A.D. McLachlan, and A. Klug Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes EMBO J. 4 1985 1609 1614
2. J.M. Berg, and Y.G. Shi The galvanization of biology: a growing appreciation for the roles of zinc Science 271 1996 1081 1085 (Pubitemid 26075222)
3. C. Andreini, and L. Banci A. Rosato Counting the zinc-proteins encoded in the human genome J. Proteome Res. 5 2006 196 201 (Pubitemid 43100813)
4. W. Maret, and Y. Li Coordination dynamics of zinc in proteins Chem. Rev. 109 2009 4682 4707
5. D.S. Auld Zinc coordination sphere in biochemical zinc sites Biometals 14 2001 271 313 (Pubitemid 34066634)
6. E.H. Cox, and G.L. McLendon Zinc-dependent protein folding Curr. Opin. Chem. Biol. 4 2000 162 165 (Pubitemid 30189306)
7. A.K. Petros, and A.R. Reddi B.R. Gibney Femtomolar Zn(II) affinity in a peptide-based ligand designed to model thiolate-rich metalloprotein active sites Inorg. Chem. 45 2006 9941 9958
8. A.R. Reddi, and B.R. Gibney Role of protons in the thermodynamic contribution of a Zn(II)-Cys4 site toward metalloprotein stability Biochemistry 46 2007 3745 3758 (Pubitemid 46501716)
9. O. Sénque, and J.M. Latour Coordination properties of zinc finger peptides revisited: ligand competition studies reveal higher affinities for zinc and cobalt J. Am. Chem. Soc. 132 2010 17760 17774
10. J.C. Buchsbaum, and J.M. Berg Kinetics of metal binding by a zinc finger peptide Inorg. Chim. Acta 297 2000 217 219
11. J.M. Berg, and H.A. Godwin Lessons from zinc-binding peptides Annu. Rev. Biophys. Biomol. Struct. 26 1997 357 371 (Pubitemid 27255377)
12. A. Janshoff, and M. Neitzert H. Fuchs Force spectroscopy of molecular systems-single molecule spectroscopy of polymers and biomolecules Angew. Chem. Int. Ed. Engl. 39 2000 3212 3237
13. M.K. Beyer, and H. Clausen-Schaumann Mechanochemistry: the mechanical activation of covalent bonds Chem. Rev. 105 2005 2921 2948 (Pubitemid 41226417)
14. F. Kienberger, and A. Ebner P. Hinterdorfer Molecular recognition imaging and force spectroscopy of single biomolecules Acc. Chem. Res. 39 2006 29 36
15. G.I. Bell Models for the specific adhesion of cells to cells Science 200 1978 618 627
16. E. Evans, and K. Ritchie Dynamic strength of molecular adhesion bonds Biophys. J. 72 1997 1541 1555 (Pubitemid 27133095)
17. M. Grandbois, and M. Beyer H.E. Gaub How strong is a covalent bond? Science 283 1999 1727 1730 (Pubitemid 129502058)
18. E.L. Florin, V.T. Moy, and H.E. Gaub Adhesion forces between individual ligand-receptor pairs Science 264 1994 415 417 (Pubitemid 24179839)
19. S.R. Ainavarapu, and J. Brujic J.M. Fernandez Contour length and refolding rate of a small protein controlled by engineered disulfide bonds Biophys. J. 92 2007 225 233 (Pubitemid 46048430)
20. M.M. Caruso, and D.A. Davis J.S. Moore Mechanically-induced chemical changes in polymeric materials Chem. Rev. 109 2009 5755 5798
21. L. Schmitt, and M. Ludwig R. Tampé A metal-chelating microscopy tip as a new toolbox for single-molecule experiments by atomic force microscopy Biophys. J. 78 2000 3275 3285 (Pubitemid 30396955)
22. M. Conti, G. Falini, and B. Samor How strong is the coordination bond between a histidine tag and Ni-nitrilotriacetate? An experiment of mechanochemistry on single molecules Angew. Chem. Int. Ed. Engl. 39 2000 215 218 (Pubitemid 30265721)
23. F. Kienberger, and G. Kada P. Hinterdorfer Recognition force spectroscopy studies of the NTA-His6 bond Single Mol. 1 2000 59 65
24. P. Zheng, and H. Li Highly covalent ferric-thiolate bonds exhibit surprisingly low mechanical stability J. Am. Chem. Soc. 133 2011 6791 6798
25. M. Maher, and M. Cross A.G. Wedd Metal-substituted derivatives of the rubredoxin from Clostridium pasteurianum Acta Crystallogr. 60 2004 298 303 (Pubitemid 41087623)
26. P.R. Blake, and J.B. Park M.W. Adams Determinants of protein hyperthermostability: purification and amino acid sequence of rubredoxin from the hyperthermophilic archaebacterium Pyrococcus furiosus and secondary structure of the zinc adduct by NMR Biochemistry 30 1991 10885 10895
27. M.K. Eidsness, and S.E. O'Dell R.A. Scott Expression of a synthetic gene coding for the amino acid sequence of Clostridium pasteurianum rubredoxin Protein Eng. 5 1992 367 371
28. P.R. Blake, and J.B. Park M.F. Summers Solution-state structure by NMR of zinc-substituted rubredoxin from the marine hyperthermophilic archaebacterium Pyrococcus furiosus Protein Sci. 1 1992 1508 1521 (Pubitemid 23012615)
29. G.N. George, and I.J. Pickering M.W.W. Adams X-ray absorption spectroscopy of Pyrococcus furiosus rubredoxin J. Biol. Inorg. Chem. 1 1996 226 230
30. R.H. Holm, P. Kennepohl, and E.I. Solomon Structural and functional aspects of metal sites in biology Chem. Rev. 96 1996 2239 2314 (Pubitemid 126641104)
31. L.C. Myers, G.L. Verdine, and G. Wagner Solution structure of the DNA methyl phosphotriester repair domain of Escherichia coli Ada Biochemistry 32 1993 14089 14094 (Pubitemid 24024532)
32. W. Maret Zinc and sulfur: a critical biological partnership Biochemistry 43 2004 3301 3309 (Pubitemid 38396774)
33. J. Wastl, and H. Sticht S. Hoffmann Identification and characterization of a eukaryotically encoded rubredoxin in a cryptomonad alga FEBS Lett. 471 2000 191 196 (Pubitemid 30190064)
34. P. Zheng, Y. Cao, and H. Li Facile method of constructing polyproteins for single-molecule force spectroscopy studies Langmuir 27 2011 5713 5718
35. M. Rief, J.M. Fernandez, and H.E. Gaub Elastically coupled two-level systems as a model for biopolymer extensibility Phys. Rev. Lett. 81 1998 4764
36. A.F. Oberhauser, and P.E. Marszalek J.M. Fernandez The molecular elasticity of the extracellular matrix protein tenascin Nature 393 1998 181 185 (Pubitemid 28242260)
37. M. Carrion-Vazquez, and A.F. Oberhauser J.M. Fernandez Mechanical and chemical unfolding of a single protein: a comparison Proc. Natl. Acad. Sci. USA 96 1999 3694 3699 (Pubitemid 29168972)
38. M. Carrion-Vazquez, and A.F. Oberhauser J.M. Fernandez Mechanical design of proteins studied by single-molecule force spectroscopy and protein engineering Prog. Biophys. Mol. Biol. 74 2000 63 91 (Pubitemid 32011689)
39. Y. Cao, and C. Lam H. Li Nonmechanical protein can have significant mechanical stability Angew. Chem. Int. Ed. Engl. 45 2006 642 645 (Pubitemid 43121465)
40. Y. Cao, and H. Li Polyprotein of GB1 is an ideal artificial elastomeric protein Nat. Mater. 6 2007 109 114 (Pubitemid 46197646)
41. J.F. Marko, and E.D. Siggia Stretching DNA Macromolecules 28 1995 8759 8770
42. M. Rief, and M. Gautel H.E. Gaub Reversible unfolding of individual titin immunoglobulin domains by AFM Science 276 1997 1109 1112 (Pubitemid 27218118)
43. D. Picot, G. Ohanessian, and G. Frison Thermodynamic stability versus kinetic lability of ZnS4 core Chem. Asian J. 5 2010 1445 1454
44. J.J. Wilker, and S.J. Lippard Alkyl transfer to metal thiolates: kinetics, active species identification, and relevance to the DNA methyl phosphotriester repair center of Escherichia coli Ada Inorg. Chem. 36 1997 969 978 (Pubitemid 127510380)
45. G. Parkin Synthetic analogues relevant to the structure and function of zinc enzymes Chem. Rev. 104 2004 699 767
46. C.P. Rao, J.R. Dorfman, and R.H. Holm Synthesis and structural systematics of ethane-1,2-dithiolato complexes Inorg. Chem. 25 1986 428 439
47. A. Morleo, and F. Bonomi D.M. Kurtz Jr. Iron-nucleated folding of a metalloprotein in high urea: resolution of metal binding and protein folding events Biochemistry 49 2010 6627 6634
48. S. Karlin, and Z.Y. Zhu Classification of mononuclear zinc metal sites in protein structures Proc. Natl. Acad. Sci. USA 94 1997 14231 14236 (Pubitemid 28041356)
49. D. Lu, M.A. Searles, and A. Klug Crystal structure of a zinc-finger-RNA complex reveals two modes of molecular recognition Nature 426 2003 96 100 (Pubitemid 37432548)
50. E.I. Solomon, S.I. Gorelsky, and A. Dey Metal-thiolate bonds in bioinorganic chemistry J. Comput. Chem. 27 2006 1415 1428