Single molecule recognition between cytochrome C 551 and gold-immobilized azurin by force spectroscopy

Biophysical Journal

Volumn 89, Issue 4, 2005, Pages 2783-2791

  Bonanni, Beatrice ^a   Kamruzzahan, A S M ^b   Bizzarri, A R ^a   Rankl, C ^b   Gruber, H J ^b   Hinterdorfer, P ^b   Cannistraro, S ^a  

^a UNIVERSITY OF TUSCIA   (Italy)

^b JOHANNES KEPLER UNIVERSITY LINZ   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

AZURIN; CYTOCHROME C; GOLD;

ARTICLE; ATOMIC FORCE MICROSCOPY; CROSS LINKING; ELECTRODE; ELECTRON TRANSPORT; FORCE SPECTROSCOPY; IMAGE ANALYSIS; MATHEMATICAL ANALYSIS; MOLECULAR RECOGNITION; NONHUMAN; OXIDATION REDUCTION REACTION; PSEUDOMONAS AERUGINOSA; SPECTROSCOPY;

EID: 25844519133     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.064097     Document Type: Article

References (60)

1. Gilardi, G., and A. Fantuzzi. 2001. Manipulating redox systems: application to nanotechnology. Trends Biotechnol. 19:468-476.
2. Willner, I., and B. Willner. 2001. Biomaterials integrated with electronic elements: en route to bioelectronics. Trends Biotechnol. 19:222-230.
3. Gorton, L., A. Lindgren, T. Larsson, F. D. Munteanu, T. Ruzgas, and I. Gazaryan. 1999. Direct electron transfer between heme-containing enzymes and electrodes as basis for third generation biosensors. Anal. Chim. Acta. 400:91-108.
4. Adams, D. M., L. Brus, C. E. D. Chidsey, S. Creager, C. Creutz, C. R. Kagan, P. V. Kamat, X. M. Lieberman, S. Lindsay, R. A. Marcus, R. M. Metzger, M. E. Michel-Beyerle, J. R. Miller, M. D. Newton, D. R. Rolison, O. Sankey, K. S. Schanze, J. Yardley, and X. Zhu. 2003. Charge transfer on the nanoscale: current status. J. Phys. Chem. B. 107:6668-6697.
5. Willner, I., and E. Katz. 2000. Integration of layered redox-proteins and conductive supports for bioelectronic applications. Angew. Chem. Int. Ed. Engl. 39:1180-1218.
6. Ghindilis, A. L., P. Atansov, M. Wilkins, and E. Wilkins. 1998. Immunosensors: electrochemical sensing and other engineering approaches. Biosens. Bioelectron. 13:113-131.
7. Nakamura, H., and I. Karube. 2003. Current research activity in biosensors. Anal. Bioanal. Chem. 377:446-468.
8. Bonanni, B., D. Alliata, A. R. Bizzarri, and S. Cannistraro. 2003. Topological and electron transfer properties of yeast cytochrome c adsorbed on bare gold electrode. Chem. Phys. Chem. 4:1183-1188.
9. Bonanni, B., D. Alliata, L. Andolfi, A. R. Bizzarri, and S. Cannistraro. 2004. Redox metalloproteins on metal surface as hybrid system for bionanodevices: an extensive characterization at the single molecule level. In Surface Science Research Developments. C.P. Norris, editor. Nova Science Publishers, Commack, NY.
10. Andolfi, L., B. Bonanni, G. W. Canters, M. P. Verbeet, and S. Cannistraro. 2003. Scanning probe microscopy characterization of gold-chemisorbed poplar plastocyanin mutants. Surf. Sci. 530:181-194.
11. Andolfi, L., D. Bruce, S. Cannistraro, G. W. Canters, J. J. Davis, H. A. O. Hill, J. Crozier, M. Ph. Verbeet, C. L. Wrathmell, and Y. Aster. 2004. The electrochemical characteristics of blue copper protein monolayers on gold. J. Electroanal. Chem. 565:21-28.
12. Zhang, J., Q. Chi, J. U. Nielsen, A. G. Hansen, J. E. T. Andersen, H. Wackerbarth, and J. Ulstrup. 2002. Organized monolayers of biological macromolecules on Au(111) surfaces. Russ. J. Electrochem. 38:68-76.
13. Cavalleri, O., C. Natale, M. E. Stroppolo, A. Relini, E. Cosulich, S. Thea, M. Novi, and A. Gliozzi. 2000. Azurin immobilization on thiol covered Au(111). Phys. Chem. Chem. Phys. 2:4630-4635.
14. Marcus, R. A., and N. Sutin. 1985. Electron transfer in chemistry and biology. Biochim. Biophys. Acta. 811:265-322.
15. Bizzarri, A. R., and S. Cannistraro. 2005. Electron transfer in metalloproteins. In Encyclopedia of Condensed Matter Physics. Elsevier, Dordrecht, The Netherlands.
16. Crowley, P. B., and M. Ubbink. 2003. Close encounters of the transient kind: protein interactions in the photosynthetic redox chain investigated by NMR spectroscopy. Acc. Chem. Res. 36:723-730.
17. Hervas, M., J. A. Navarro, A. Diaz, H. Bottin, and M. A. De la Rosa. 1995. Laser-flash kinetic analysis of the fast electron transfer from plastocyanin and cytochrome c-6 to photosystem I. Experimental evidence on the evolution of the reaction mechanism. Biochemistry. 34:11321-11326.
18. Facci, P., D. Alliata, and S. Cannistraro. 2001. Potential-induced resonant tunneling through a redox metalloprotein investigated by electrochemical scanning probe microscopy. Ultramicroscopy. 89:291-298.
19. Chi, Q., J. Zhang, J. U. Nielsen, E. P. Friis, I. Chorkendor, G. W. Canters, J. E. T. Andersen, and J. Ulstrup. 2000. Molecular monolayers and interfacial electron transfer of Pseudomonas aeruginosa azurin on Au(111). J. Am. Chem. Soc. 122:4047-4055.
20. Friis, E. P., J. E. T. Andersen, Y. I. Kharkats, A. M. Kuznestov, R. J. Nichols, J.-D. Zhang, and J. Ulstrup. 1999. An approach to long-range electron transfer mechanisms in metalloproteins: in situ scanning tunneling microscopy with submolecular resolution. Proc. Natl. Acad. Sci. USA. 96:1379-1384.
21. Zannoni, D. 1989. The respiratory chains of pathogenic pseudomonads. Biochim. Biophys. Acta. 975:299-316.
22. Wilson, M. T., C. Greenwood, M. Brunori, and E. Antonini. 1975. Electron transfer between azurin and cytochrome c-551. Biochem. J. 145:449-457.
23. Corin, A. F., R. Bersonhn, and P. E. Cole. 1983. pH Dependence of the reduction-oxidation reaction of azurin with cytochrome c-551: role of histidine-35 of azurin in electron transfer. Biochemistry. 22:2032-2038.
24. Cutruzzolà, F., M. Arese, G. Ranghino, G. van Pouderoyen, G. Canters, and M. Brunori. 2002. Pseudomonas aeruginosa cytochrome C-551: probing the role of the hydrophobic patch in electron transfer. J. Inorg. Biochem. 88:353-361.
25. Rosen, P., and I. Petch. 1976. Conformational equilibria accompanying the electron transfer between cytochrome (P551) and azurin. Biochemistry. 15:775-786.
26. Vajda, S., and C. J. Camacho. 2004. Protein-protein docking: is the glass half-full or half-empty? Trends Biotechnol. 22:110-116.
27. Vakser, I. A., and C. Aflalo. 1994. Hydrophobic docking: a proposed enhancement to molecular recognition techniques. Proteins. 20:320-329.
28. Rief, M., and H. Grubmuller. 2002. Force spectroscopy of single biomolecules. Chem. Phys. Chem. 3:255-261.
29. Lee, G. U., D. A. Kidwell, and R. J. Colton. 1994. Sensing discrete streptavidin-biotin interactions with atomic force microscopy. Langmuir. 10:354-357.
30. Florin, E.-L., V. T. Moy, and H. E. Gaub. 1994. Adhesion forces between individual ligand-receptor pairs. Science. 264:415-417.
31. Moy, V. T., E.-L. Florin, and H. E. Gaub. 1994. Intermolecular forces and energies between ligands and receptors. Science. 266:257-259.
32. Lo, Y.-S., N. D. Huefner, W. S. Chan, F. Stevens, J. M. Harris, and T. P. Beebe, Jr. 1999. Specific interactions between biotin and avidin studied by atomic force microscopy using the Poisson statistical analysis method. Langmuir. 15:1373-1382.
33. Haselgrübler, T., A. Amerstorfer, H. Schindler, and H. J. Gruber. 1995. Synthesis and applications of a new poly(ethylene glycol) derivative for the crosslinking of amines with thiols. Bioconjug. Chem. 6:242-248.
34. Hinterdorfer, P., W. Baumgartner, H. J. Gruber, K. Schilcher, and H. Schindler. 1996. Detection and localization of individual antibody antigen recognition events by atomic force microscopy. Proc. Natl. Acad. Sci. USA. 93:3477-3481.
35. Hinterdorfer, P., F. Kienberger, A. Raab, H. J. Gruber, W. Baumgartner, G. Kada, C. Riener, S. Wielert-Badt, C. Borken, and H. Schindler. 2000. Poly(ethylene glycol): an ideal spacer for molecular recognition force microscopy/spectroscopy. Single Mol. 1:99-103.
36. Kienberger, F., V. P. Pastushenko, G. Kada, H. J. Gruber, C. Riener, H. Schindler, and P. Hinterdorfer. 2000. Static and dynamical properties of single poly(ethylene glycol) molecules investigated by force spectroscopy. Single Mol. 1:123-128.
37. Baumgartner, W., P. Hinterdorfer, W. Ness, A. Raab, D. Vestweber, H. Schindler, and D. Drenckhahn. 2000. Cadherin interaction probed by atomic force microscopy. Proc. Natl. Acad. Sci. USA. 97:4005-4010.
38. 35 Leu of azurin from Pseudomonas aeruginosa. J. Mol. Biol. 218:427-447.
39. Hutter, J. L., and J. Bechhoefer. 1993. Calibration of atomic force microscope tips. Rev. Sci. Instrum. 64:1868-1873.
40. Ros, R., F. Schwesinger, D. Anselmetti, M. Kubon, R. Schäfer, A. Plückthun, and L. Tiefenauer. 1998. Antigen binding forces of individually addressed single-chain Fv antibody molecules. Proc. Natl. Acad. Sci. USA. 95:7402-7405.
41. Wielert-Badt, S., P. Hinterdorfer, H. Gruber, J. T. Lin, D. Badt, B. Wimmer, H. Schindler, and R. K.-H. Kinne. 2002. Single molecule recognition of protein binding epitopes in brush border membranes by force microscopy. Biophys. J. 82:2767-2774.
42. Fritz, J. A., G. Katopodis, F. Kolbinger, and D. Anselmetti. 1998. Force mediated kinetics of single P-selectin/ligand complexes observed by atomic force microscopy. Proc. Natl. Acad. Sci. USA. 95:12283-12288.
43. Yuan, C., A. Chen, P. Kolb, and V. T. Moy. 2000. Energy landscape of streptavidin-biotin complexes measured by atomic force microscopy. Biochemistry. 39:10219-10223.
44. Baumgartner, W., H. J. Gruber, P. Hinterdorfer, and D. Drenckhahn. 2000. Affinity of trans-interacting VE-cadherin determined by atomic force microscopy. Single Mol. 1:119-122.
45. Eckel, R., R. Ros, B. Decker, J. Mattay, and D. Anselmetti. 2005. Supramolecular chemistry at the single-molecule level. Angew. Chem. Int. Ed. Engl. 44:484-488.
46. Ratto, T. V., K. C. Langry, R. E. Rudd, R. L. Balhorn, M. J. Allen, and M. W. McElfresh. 2004. Force spectroscopy of the double-tethered concanavalin-a mannose bond. Biophys. J. 86:2430-2437.
47. Bongrand, P. 1999. Ligand-receptor interactions. Rep. Prog. Phys. 62:921-968.
48. Evans, E., and K. Ritchie. 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541-1555.
49. Strunz, T., K. Oroszlan, I. Schumakovitch, H.-J. Güntherodt, and M. Hegner. 2000. Model energy landscapes and the force-induced dissociation of ligand-receptor bonds. Biophys. J. 79:1206-1212.
50. Bell, G. I. 1978. Models for the specific adhesion of cells to cells. Science. 200:618-627.
51. Evans, E. 1998. Energy landscapes of biomolecular adhesion and receptor anchoring at interfaces explored with dynamic force spectroscopy. Faraday Discuss. 111:1-16.
52. Merkel, R., P. Nassoy, A. Leung, K. Ritchie, and E. Evans. 1999. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature. 397:50-53.
53. Green, N. M., and E. J. Toms. 1973. The properties of subunits of avidin coupled to sepharose. Biochem. J. 133:687-700.
54. Schwesinger, F., R. Ros, T. Strunz, D. Anselmetti, H.-J. Guntherodt, A. Honegger, L. Jermutus, L. Tiefenauer, and A. Pluckthun. 2000. Unbinding forces of single antibody-antigen complexes correlate with their thermal dissociation rates. Proc. Natl. Acad. Sci. USA. 97:9972-9977.
55. 1 integrins. Langmuir. 20:2397-2404.
56. Zhang, X., D. F. Bogorin, and V. T. Moy. 2004. Molecular basis of the dynamic strength of the sialyl Lewis X-selectin interaction. Chem. Phys. Chem. 5:175-182.
57. Berquand, A., N. Xia, D. G. Castner, B. H. Clare, N. L. Abbott, V. Dupres, Y. Adriaensen, and Y. F. Dufrêne. 2005. Antigen binding forces of single antilysozyme Fv fragments explored by atomic force microscopy. Langmuir. 21:5517-5523.
58. Bartels, F. W., B. Baugmarth, D. Anselmetti, R. Ros, and A. Becker. 2003. Specific binding of the regulatory protein ExpG to promoter regions of the galactoglucan biosynthesis gene cluster of Sinorhizobium meliloti-a combined molecular biology and force spectroscopy investigation. J. Struct. Biol. 143:145-152.
59. De Paris, R., T. Strunz, K. Oroszlan, H.-J. Guntherodt, and M. Hegner. 2000. Force spectroscopy and dynamics of the biotin-avidin bond studied by scanning force microscopy. Single Mol. 1:285-290.
60. Kienberger, F., G. Kada, H. Mueller, and P. Hinterdorfer. 2005. Single molecule studies of antibody-antigen interaction strength versus intramolecular antigen stability. J. Mol. Biol. 347:597-606.