Temperature and force dependence of nanoscale electron transport via the Cu protein azurin

ACS Nano

Volumn 6, Issue 12, 2012, Pages 10816-10824

  Li, Wenjie ^a   Sepunaru, Lior ^a   Amdursky, Nadav ^a   Cohen, Sidney R ^a   Pecht, Israel ^a   Sheves, Mordechai ^a   Cahen, David ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Arrhenius activation energy; azurin; biomolecular electronics; conductivity; electron transport; nanometer scale; tunneling

Indexed keywords

ARRHENIUS ACTIVATION ENERGY; AZURIN; BIOMOLECULAR ELECTRONICS; ELECTRON TRANSPORT; NANO-METER SCALE;

ACTIVATION ENERGY; ELECTRIC CONDUCTIVITY; ELECTRON TRANSPORT PROPERTIES; ELECTRON TUNNELING; MONOLAYERS;

PROTEINS;

APOPROTEIN; AZURIN; IMMOBILIZED PROTEIN;

ALCALIGENES FAECALIS; ARTICLE; ATOMIC FORCE MICROSCOPY; CHEMICAL STRUCTURE; CHEMISTRY; ELECTRON TRANSPORT; METABOLISM; METHODOLOGY; NANOTECHNOLOGY; PROTEIN CONFORMATION; TEMPERATURE;

ALCALIGENES FAECALIS; APOPROTEINS; AZURIN; ELECTRON TRANSPORT; IMMOBILIZED PROTEINS; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; NANOTECHNOLOGY; PROTEIN CONFORMATION; TEMPERATURE;

EID: 84871597751     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn3041705     Document Type: Article

References (59)

1. Farver, O.; Pecht, I., Elucidation of Electron-Transfer Pathways in Copper and Iron Proteins by Pulse Radiolysis Experiments. In Progress in Organic Chemistry; Karlin, K. D., Ed.; 2007; Vol. 55, pp 1-78.
2. Gray, H. B.; Winkler, J. R. Electron Tunneling through Proteins Q. Rev. Biophys. 2003, 36, 341-372
3. Regan, J. J.; Dibilio, A. J.; Langen, R.; Skov, L. K.; Winkler, J. R.; Gray, H. B.; Onuchic, J. N. Electron-Tunneling in Azurin-The Coupling across a Beta-Sheet Chem. Biol. 1995, 2, 489-496
4. Chi, Q. J.; Zhang, J. D.; Andersen, J. E. T.; Ulstrup, J. Ordered Assembly and Controlled Electron Transfer of the Blue Copper Protein Azurin at Gold (111) Single-Crystal Substrates J. Phys. Chem. B 2001, 105, 4669-4679
5. Chi, Q. J.; Zhang, J. D.; Nielsen, J. U.; Friis, E. P.; Chorkendorff, I.; Canters, G. W.; Andersen, J. E. T.; Ulstrup, J. Molecular Monolayers and Interfacial Electron Transfer of Pseudomonas aeruginosa Azurin on Au(111) J. Am. Chem. Soc. 2000, 122, 4047-4055
6. Gaigalas, A. K.; Niaura, G. Measurement of Electron Transfer Rates between Adsorbed Azurin and a Gold Electrode Modified with a Hexanethiol Layer J. Colloid Interface Sci. 1997, 193, 60-70
7. Jeuken, L. J. C.; Armstrong, F. A. Electrochemical Origin of Hysteresis in the Electron-Transfer Reactions of Adsorbed Proteins: Contrasting Behavior of the ″Blue″ Copper Protein, Azurin, Adsorbed on Pyrolytic Graphite and Modified Gold Electrodes J. Phys. Chem. B 2001, 105, 5271-5282
8. Alessandrini, A.; Corni, S.; Facci, P. Unravelling Single Metalloprotein Electron Transfer by Scanning Probe Techniques Phys. Chem. Chem. Phys. 2006, 8, 4383-4397
9. Friis, E. P.; Andersen, J. E. T.; Madsen, L. L.; Moller, P.; Ulstrup, J. In Situ STM and AFM of the Copper Protein Pseudomonas aeruginosa Azurin J. Electroanal. Chem. 1997, 431, 35-38
10. Andolfi, L.; Bruce, D.; Cannistraro, S.; Canters, G. W.; Davis, J. J.; Hill, H. A. O.; Crozier, J.; Verbeet, M. P.; Wrathmell, C. L.; Astier, Y. The Electrochemical Characteristics of Blue Copper Protein Monolayers on Gold J. Electroanal. Chem. 2004, 565, 21-28
11. Shinwari, M. W.; Deen, M. J.; Starikov, E. B.; Cuniberti, G. Electrical Conductance in Biological Molecules Adv. Funct. Mater. 2010, 20, 1865-1883
12. Ron, I.; Pecht, I.; Sheves, M.; Cahen, D. Proteins as Solid-State Electronic Conductors Acc. Chem. Res. 2010, 43, 945-953
13. Das, R.; Kiley, P. J.; Segal, M.; Norville, J.; Yu, A. A.; Wang, L. Y.; Trammell, S. A.; Reddick, L. E.; Kumar, R.; Stellacci, F. et al. Integration of Photosynthetic Protein Molecular Complexes in Solid-State Electronic Devices Nano Lett. 2004, 4, 1079-1083
14. Zhao, J. W.; Davis, J. J. Force Dependent Metalloprotein Conductance by Conducting Atomic Force Microscopy Nanotechnology 2003, 14, 1023-1028
15. Davis, J. J.; Peters, B.; Xi, W. Force Modulation and Electrochemical Gating of Conductance in a Cytochrome J. Phys. Condens. Matter 2008, 20
16. Davis, J. J.; Wang, N.; Morgan, A.; Zhang, T. T.; Zhao, J. W. Metalloprotein Tunnel Junctions: Compressional Modulation of Barrier Height and Transport Mechanism Faraday Discuss. 2006, 131, 167-179
17. Davis, J. J.; Wrathmell, C. L.; Zhao, J.; Fletcher, J. The Tunnelling Conductance of Molecularly Ordered Metalloprotein Arrays J. Mol. Recognit. 2004, 17, 167-173
18. Zhao, J. W.; Davis, J. J. Molecular Electron Transfer of Protein Junctions Characterised by Conducting Atomic Force Microscopy Colloids Surf., B 2005, 40, 189-194
19. Zhao, J. W.; Davis, J. J.; Sansom, M. S. P.; Hung, A. Exploring the Electronic and Mechanical Properties of Protein Using Conducting Atomic Force Microscopy J. Am. Chem. Soc. 2004, 126, 5601-5609
20. Ron, I.; Sepunaru, L.; Itzhakov, S.; Belenkova, T.; Friedman, N.; Pecht, I.; Sheves, M.; Cahen, D. Proteins as Electronic Materials: Electron Transport through Solid-State Protein Monolayer Junctions J. Am. Chem. Soc. 2010, 132, 4131-4140
21. Sepunaru, L.; Pecht, I.; Sheves, M.; Cahen, D. Solid-State Electron Transport across Azurin: From a Temperature-Independent to a Temperature-Activated Mechanism J. Am. Chem. Soc. 2011, 133, 2421-2423
22. Bizzarri, A. R.; Andolfi, L.; Taranta, M.; Cannistraro, S. Optical and Electronic Coupling of the Redox Copper Azurin on ITO-Coated Quartz Substrate Biosens. Bioelectron. 2008, 24, 204-209
23. Mentovich, E. D.; Belgorodsky, B.; Richter, S. Resolving the Mystery of the Elusive Peak: Negative Differential Resistance in Redox Proteins J. Phys. Chem. Lett. 2011, 2, 1125-1128
24. Engelkes, V. B.; Beebe, J. M.; Frisbie, C. D. Analysis of the Causes of Variance in Resistance Measurements on Metal-Molecule-Metal Junctions Formed by Conducting-Probe Atomic Force Microscopy J. Phys. Chem. B 2005, 109, 16801-16810
25. Wold, D. J.; Frisbie, C. D. Fabrication and Characterization of Metal-Molecule-Metal Junctions by Conducting Probe Atomic Force Microscopy J. Am. Chem. Soc. 2001, 123, 5549-5556
26. Andolfi, L.; Cannistraro, S. Conductive Atomic Force Microscopy Study of Plastocyanin Molecules Adsorbed on Gold Electrode Surf. Sci. 2005, 598, 68-77
27. Good, R. H. J.; Muller, E. W. Handbuch Der Physik; Springer Verlag: Berlin, 1956; Vol. XXI.
28. Xu, D.; Watt, G. D.; Harb, J. N.; Davis, R. C. Electrical Conductivity of Ferritin Proteins by Conductive AFM Nano Lett. 2005, 5, 571-577
29. Stamouli, A.; Frenken, J. W. M.; Oosterkamp, T. H.; Cogdell, R. J.; Aartsma, T. J. The Electron Conduction of Photosynthetic Protein Complexes Embedded in a Membrane FEBS Lett. 2004, 560, 109-114
30. Rakshit, T.; Mukhopadhyay, R. Solid-State Electron Transport in Mn-, Co-, Holo-, and Cu-Ferritins: Force-Induced Modulation Is Inversely Linked to the Protein Conductivity J. Colloid Interface Sci. 2012, 388, 282-292
31. Marcus, R. A.; Sutin, N. Electron Transfers in Chemistry and Biology Biochim. Biophys. Acta 1985, 811, 265-322
32. Tao, N. J. Probing Potential-Tuned Resonant Tunneling through Redox Molecules with Scanning Tunneling Microscopy Phys. Rev. Lett. 1996, 76, 4066-4069
33. Bar, G.; Thomann, Y.; Brandsch, R.; Cantow, H. J.; Whangbo, M. H. Factors Affecting the Height and Phase Images in Tapping Mode Atomic Force Microscopy. Study of Phase-Separated Polymer Blends of Poly(ethene- co -styrene) and Poly(2,6-dimethyl-1,4-phenylene oxide) Langmuir 1997, 13, 3807-3812
34. Kuhle, A.; Sorensen, A. H.; Bohr, J. Role of Attractive Forces in Tapping Tip Force Microscopy J. Appl. Phys. 1997, 81, 6562-6569
35. San Paulo, A.; Garcia, R. Amplitude, Deformation and Phase Shift in Amplitude Modulation Atomic Force Microscopy: A Numerical Study for Compliant Materials Surf. Sci. 2001, 471, 71-79
36. Shepard, W. E. B.; Kingston, R. L.; Anderson, B. F.; Baker, E. N. Structure of Apo-Azurin from Alcaligenes-denitrificans at 1.8-Angstrom Resolution Acta Crystallogr., Sect. D: Biol. Crystallogr. 1993, 49, 331-343
37. Nar, H.; Messerschmidt, A.; Huber, R.; Vandekamp, M.; Canters, G. W. Crystal-Structure of Pseudomonas-aeruginosa Apo-Azurin at 1.85 Angstrom Resolution FEBS Lett. 1992, 306, 119-124
38. Vandekamp, M.; Canters, G. W.; Wijmenga, S. S.; Lommen, A.; Hilbers, C. W.; Nar, H.; Messerschmidt, A.; Huber, R. Complete Sequential H-1 and N-15 Nuclear-Magnetic-Resonance Assignments and Solution Secondary Structure of the Blue Copper Protein Azurin from Pseudomonas-aeruginosa Biochemistry 1992, 31, 10194-10207
39. Zaballa, M.-E.; Abriata, L. A.; Donaire, A.; Vila, A. J. Flexibility of the Metal-Binding Region in Apo-Cupredoxins Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 9254-9259
40. Rakshit, T.; Banerjee, S.; Mukhopadhyay, R. Near-Metallic Behavior of Warm Holoferritin Molecules on a Gold(111) Surface Langmuir 2010, 26, 16005-16012
41. Maruccio, G.; Marzo, P.; Krahne, R.; Passaseo, A.; Cingolani, R.; Rinaldi, R. Protein Conduction and Negative Differential Resistance in Large-Scale Nanojunction Arrays Small 2007, 3, 1184-1188
42. Engeseth, H. R.; McMillin, D. R. Studies of Thermally Induced Denaturation of Azurin and Azurin Derivatives by Differential Scanning Calorimetry: Evidence for Copper Selectivity Biochemistry 1986, 25, 2448-2455
43. Shen, Y.; Safinya, C. R.; Liang, K. S.; Ruppert, A. F.; Rothschild, K. J. Stabilization of the Membrane Protein Bacteriorhodopsin to 140 C in Two-Dimensional Films Nature 1993, 366, 48-50
44. Bonander, N.; Leckner, J.; Guo, H.; Karlsson, B. G.; Sjölin, L. Crystal Structure of the Disulfide Bond-Deficient Azurin Mutant C3a/C26a Eur. J. Biochem. 2000, 267, 4511-4519
45. Luo, L.; Choi, S. H.; Frisbie, C. D. Probing Hopping Conduction in Conjugated Molecular Wires Connected to Metal Electrodes Chem. Mater. 2010, 23, 631-645
46. Choi, S. H.; Frisbie, C. D. Enhanced Hopping Conductivity in Low Band Gap Donor-Acceptor Molecular Wires up to 20 Nm in Length J. Am. Chem. Soc. 2010, 132, 16191-16201
47. Atsushi, I. Local Rigidity of a Protein Molecule Biophys. Chem. 2005, 116, 187-191
48. Wolfram|Alpha. Http://Www.Wolframalpha.Com/Input/?I= Biological+Material&Lk=1&a=Clashprefs-Materialclass.Biologicalmaterial- (accessed July 17, 2012).
49. Vilan, A.; Cahen, D. Soft Contact Deposition onto Molecularly Modified GaAs. Thin Metal Film Flotation: Principles and Electrical Effects Adv. Funct. Mater. 2002, 12, 795-807
50. Marshall, N. M.; Garner, D. K.; Wilson, T. D.; Gao, Y. G.; Robinson, H.; Nilges, M. J.; Lu, Y. Rationally Tuning the Reduction Potential of a Single Cupredoxin Beyond the Natural Range Nature 2009, 462, 113-116
51. Benning, M. M.; Meyer, T. E.; Rayment, I.; Holden, H. M. Molecular Structure of the Oxidized High-Potential Iron-Sulfur Protein Isolated from Ectothiorhodospira vacuolata Biochemistry 1994, 33, 2476-2483
52. Palfey, B. A.; Basu, R.; Frederick, K. K.; Entsch, B.; Ballou, D. P. Role of Protein Flexibility in the Catalytic Cycle of p -Hydroxybenzoate Hydroxylase Elucidated by the Pro293ser Mutant Biochemistry 2002, 41, 8438-8446
53. Battistuzzi, G.; Borsari, M.; Cowan, J. A.; Ranieri, A.; Sola, M. Control of Cytochrome C Redox Potential: Axial Ligation and Protein Environment Effects J. Am. Chem. Soc. 2002, 124, 5315-5324
54. Beratan, D. N.; Skourtis, S. S.; Balabin, I. A.; Balaeff, A.; Keinan, S.; Venkatramani, R.; Xiao, D. Q. Steering Electrons on Moving Pathways Acc. Chem. Res. 2009, 42, 1669-1678
55. Wierzbinski, E.; de Leon, A.; Davis, K. L.; Bezer, S.; Wolak, M. A.; Kofke, M. J.; Schlaf, R.; Achim, C.; Waldeck, D. H. Charge Transfer through Modified Peptide Nucleic Acids Langmuir 2012, 28, 1971-1981
56. Skov, L. K.; Pascher, T.; Winkler, J. R.; Gray, H. B. Rates of Intramolecular Electron Transfer in Ru(Bpy)2(Im)(His83)-Modified Azurin Increase Below 220 K J. Am. Chem. Soc. 1998, 120, 1102-1103
57. 3+ Electronic Couplings J. Am. Chem. Soc. 1994, 116, 1577-1578
58. Ron, H.; Matlis, S.; Rubinstein, I. Self-Assembled Monolayers on Oxidized Metals. 2. Gold Surface Oxidative Pretreatment, Monolayer Properties, and Depression Formation Langmuir 1998, 14, 1116-1121
59. Ambler, R. P.; Wynn, M. Amino-Acid Sequences of Cytochromes C-551 from 3 Species of Pseudomonas Biochem. J. 1973, 131, 485-498