Surface-enhanced vibrational spectroscopy for probing transient interactions of proteins with biomimetic interfaces: Electric field effects on structure, dynamics and function of cytochrome c

FEBS Journal

Volumn 278, Issue 9, 2011, Pages 1382-1390

  Khoa Ly, Hong ^a   Sezer, Murat ^a   Wisitruangsakul, Nattawadee ^a,b   Feng, Jiu Ju ^a,c   Kranich, Anja ^a   Millo, Diego ^a   Weidinger, Inez M ^a   Zebger, Ingo ^a   Murgida, Daniel H ^d   Hildebrandt, Peter ^a  

^a TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^b Iron and Steel Institute of Thailand   (Thailand)

^c HENAN NORMAL UNIVERSITY   (China)

^d UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

apoptosis; cytochrome c; electric field; electron transfer; protein dynamics; surface enhanced infrared spectroscopy; surface enhanced resonance Raman spectroscopy

Indexed keywords

CYTOCHROME C; HEMOPROTEIN; NANOMATERIAL;

ABSORPTION SPECTROSCOPY; APOPTOSIS; ARTIFICIAL MEMBRANE; BIOMIMETIC INTERFACE; CONTROLLED STUDY; DEVICE; DIFFUSION; ELECTRIC FIELD; ELECTRODE; ELECTRON TRANSPORT; ENZYME IMMOBILIZATION; MEMBRANE MODEL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; RESPIRATORY CHAIN; REVIEW; SPECTROSCOPY; SURFACE ENHANCED INFRARED ABSORPTION; SURFACE ENHANCED RESONANCE RAMAN; SURFACE ENHANCED VIBRATIONAL SPECTROSCOPY; TRANSIENT INTERACTION;

BIOMIMETICS; CYTOCHROMES C; ELECTRONS; MOLECULAR PROBES; MOLECULAR STRUCTURE; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEINS; SPECTRUM ANALYSIS; VIBRATION;

EID: 79955063399     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08064.x     Document Type: Review

References (51)

1. Prudencio M, &, Ubbink M, (2004) Transient complexes of redox proteins: structural and dynamic details from NMR studies. J Mol Recognit 17, 524-539. (Pubitemid 39484220)
2. Bashir Q, Scanu S, &, Ubbink M, (2011) Dynamics in electron transfer protein complexes. FEBS J 278, 1391-1400.
3. Martínez-Fábregas L, Rubio S, Díaz-Quintana A, Díaz-Moreno I, &, De la Rosa M, (2011) Proteomic tools for the analysis of transient interactions between metalloproteins. FEBS J 278, 1401-1410.
4. Murgida DH, &, Hildebrandt P, (2008) Disentangling interfacial redox processes of proteins by SERR spectroscopy. Chem Soc Rev 37, 937-945.
5. Clarke RJ, (2001) The dipole potential of phospholipid membranes and methods for its detection. Adv Colloid Interface Sci 89, 263-281. (Pubitemid 32092488)
6. Neumann E, (1986) Chemical electric effects in biological macromeolecules. Prog Biophys Mol Biol 47, 197-231.
7. Scott RA, &, Mauk AG, eds (1995) Cytochrome c-A Multidisciplinary Approach. University Science Books, Sausalito.
8. Jiang X, &, Wang X, (2004) Cytochrome c-mediated apoptosis. Annu Rev Biochem 73, 87-106. (Pubitemid 39050364)
9. Kagan VE, Tyurin VA, Jiang J, Tyurina YY, Ritov VB, Amoscato AA, Osipov AN, Belikova NA, Kapralov AA, Kini V, et al. (2005) Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol 1, 223-232.
10. Siebert F, &, Hildebrandt P, (2007) Vibrational Spectroscopy in Life Science. Wiley-VCH, Weinheim.
11. Murgida D, &, Hildebrandt P, (2001) Active site structure and dynamics of immobilized cytochrome c on self-assembled monolayers-a time-resolved surface enhanced resonance spectroscopic study. Angew Chem Int Ed 40, 728-731. (Pubitemid 32179730)
12. Ataka K, &, Heberle J, (2003) Electrochemically induced surface enhanced infrared difference absorption (SEIDA) spectroscopy of a protein monolayer. J Am Chem Soc 125, 4986-4987. (Pubitemid 36520422)
13. Feng JJ, Gernert U, Sezer M, Kuhlmann U, Murgida DH, David C, Richter M, Knorr A, Hildebrandt P, &, Weidinger I, (2009) A novel Au-Ag hybrid device for surface enhanced (resonance) Raman spectroscopy. Nano Lett 9, 298-303.
14. Sezer M, Feng JJ, Ly KH, Shen Y, Nakanishi T, Kuhlmann U, Möhwald H, Hildebrandt P, &, Weidinger I, (2010) Multi-layer electron transfer across nanostructured Ag-SAM-Au-SAM junctions probed by surface enhanced Raman spectroscopy. Phys Chem Chem Phys 12, 9822-9829.
15. Feng JJ, Gernert U, Hildebrandt P, &, Weidinger IM, (2010) Novel nano-sandwiched Ag-silica-Au supports with high SER-activity via long range plasmon coupling. Adv Funct Mat 20, 1954-1961.
16. Murgida DH, &, Hildebrandt P, (2005) Redox and redox-coupled processes of heme proteins and enzymes at electrochemical interfaces. Phys Chem Chem Phys 7, 3773-3784. (Pubitemid 41718295)
17. Love JC, Estroff LA, Kriebel JK, Nuzzo RG, &, Whitesides GM, (2005) Self-assembled monolayers of thiolates on metals as a form of nanotechnology. Chem Rev 105, 1103-1169. (Pubitemid 40600878)
18. Suydam IT, Snow CD, Pande VS, &, Boxer SG, (2006) Electric fields at the active site of an enzyme: direct comparison of experiment with theory. Science 313, 200-204. (Pubitemid 44066246)
19. Fafarman AT, Webb LJ, Chuang JI, &, Boxer SG, (2006) Site-specific conversion of cysteine thiols into thiocyanate creates an IR probe for electric fields in proteins. J Am Chem Soc 128, 13356-13357. (Pubitemid 44583010)
20. Suydam IT, &, Boxer SG, (2003) Vibrational Stark effects calibrate the sensitivity of vibrational probes for electric fields in proteins. Biochemistry 42, 12050-12055. (Pubitemid 37280655)
21. Farfarman AT, Sigala PA, Herschlag D, &, Boxer SG, (2010) Decomposition of vibrational shifts of nitriles into electrostatic and hydrogen bonding effects. J Am Chem Soc 132, 12811-12813.
22. Oklejas V, &, Harris JM, (2003) In-situ investigation of binary-component self-assembled monolayers: A SERS-based spectroelectrochemical study of the effects of monolayer composition on interfacial structure. Langmuir 19, 5794-5801.
23. Murgida DH, &, Hildebrandt P, (2001) The heterogeneous electron transfer of cytochrome c adsorbed on coated silver electrodes. Electric field effects on structure and redox potential. J Phys Chem B 105, 1578-1586.
24. Armstrong FA, (2005) Recent developments in dynamic electrochemical studies of adsorbed enzymes and their active sites. Curr Opin Chem Biol 9, 110-117. (Pubitemid 40462482)
25. Murgida DH, &, Hildebrandt P, (2001) Proton coupled electron transfer in cytochrome c. J Am Chem Soc 123, 4062-4068. (Pubitemid 32899493)
26. Wisitruangsakul N, Zebger I, Ly KH, Murgida DH, Egkasit S, &, Hildebrandt P, (2008) Redox-linked protein dynamics probed by time-resolved surface enhanced infrared absorption spectroscopy. Phys Chem Chem Phys 10, 5276-5286.
27. Wackerbarth H, &, Hildebrandt P, (2003) Redox and conformational equilibria and dynamics of cytochrome c at high electric fields. ChemPhysChem 4, 714-724.
28. Kranich A, Ly HK, Hildebrandt P, &, Murgida DH, (2008) Direct observation of the gating step in protein electron transfer: electric field controlled protein dynamics. J Am Chem Soc 130, 9844-9848.
29. Feng ZQ, Imabayashi S, Kakiuchi T, &, Niki K, (1997) Long-range electron-transfer reaction rates to cytochrome c across long- and short-chain alkanethiol self-assembled monolayers: electroreflectance studies. J Chem Soc Faraday Trans 93, 1367-1370. (Pubitemid 127781522)
30. Avila A, Gregory BW, Niki K, &, Cotton TM, (2000) An electrochemical approach to investigate gated electron transfer using a physiological model system: cytochrome c immobilized on carboxylic acid-terminated alkanethiol self-assembled monolayers on gold electrodes. J Phys Chem B 104, 2759-2766. (Pubitemid 33685494)
31. Niki K, Hardy WR, Hill MG, Li H, Sprinkle JR, Margoliash E, Fujita K, Tanimura R, Nakamura N, Ohno H, et al. (2003) Coupling to lysine-13 promotes electron tunneling through carboxylate-terminated alkanethiol self-assembled monolayers to cytochrome c. J Phys Chem B 107, 9947-9949.
32. Wei JJ, Liu HY, Khoshtariya DE, Yamamoto H, Dick A, &, Waldeck DH, (2002) Electron-transfer dynamics of cytochrome c: A change in the reaction mechanism with distance. Angew Chem Int Ed 41, 4700-4703. (Pubitemid 36061443)
33. Murgida DH, Hildebrandt P, Wei J, He YF, Liu HY, &, Waldeck DH, (2004) SERR and electrochemical study of cytochrome c bound on electrodes through coordination with pyridinyl-terminated SAMs. J Phys Chem B 108, 2261-2269.
34. Wei JJ, Liu HY, Niki K, Margoliash E, &, Waldeck DH, (2004) Probing electron tunneling pathways: electrochemical study of rat heart cytochrome c and its mutant on pyridine-terminated SAMs. J Phys Chem B 108, 16912-16917.
35. Yue HJ, &, Waldeck DH, (2005) Understanding interfacial electron transfer to monolayer protein assemblies. Curr Opin Solid State Mater Sci 9, 28-36. (Pubitemid 43816890)
36. Khoshtariya DE, Wei JJ, Liu HY, Yue HJ, &, Waldeck DH, (2003) Charge-transfer mechanism for cytochrome c adsorbed on nanometer thick films. Distinguishing frictional control from conformational gating. J Am Chem Soc 125, 7704-7714. (Pubitemid 36750292)
37. Yue HJ, Khoshtariya D, Waldeck DH, Grochol J, Hildebrandt P, &, Murgida DH, (2006) On the electron transfer mechanism between cytochrome c and metal electrodes. Evidence for dynamic control at short distances. J Phys Chem B 110, 19906-19913. (Pubitemid 44626351)
38. Murgida D, &, Hildebrandt P, (2002) Electrostatic-field dependent activation energies control biological electron transfer. J Phys Chem B 106, 12814-12819.
39. Cheng J, Terrettaz S, Blankman JI, Muller CJ, Dangi B, &, Guiles RD, (1997) Electrochemical comparison of heme proteins by insulated electrode voltammetry. Isr J Chem 37, 259-266.
40. Ly KH, Wisitruangsakul N, Sezer M, Feng JJ, Kranich A, Weidinger I, Zebger I, Murgida DH, &, Hildebrandt P, (2010) Electric field effects on the interfacial electron transfer and protein dynamics of cytochrome c. J Electroanal Chem, in press, doi:.
41. Lockhart DJ, Kirmaier C, Holten D, &, Boxer SG, (1990) Electric field effects on the initial electron-transfer kinetics in bacterial photosynthetic reaction centers. J Phys Chem 94, 6987-6995.
42. Paggi D, Martín DF, Kranich A, Hildebrandt P, Martí M, &, Murgida DH, (2009) Computer simulation and SERR detection of cytochrome c dynamics at SAM-coated electrodes. Electrochim Acta 54, 4963-4970.
43. De Biase PM, Paggi DA, Doctorovich F, Hildebrandt P, Estrin DA, Murgida DH, &, Marti MA, (2009) Molecular basis for the electric field modulation of cytochrome c structure and function. J Am Chem Soc 131, 16248-16256.
44. Georg S, Kabuss J, Weidinger IM, Murgida DH, Hildebrandt P, Knorr A, &, Richter M, (2010) On the distance dependent electron transfer rate of immobilised redox proteins-a statistical physics approach. Phys Rev E 81, 046101(1-10).
45. Moroney PM, Scholes TA, &, Hinkle PC, (1984) Effect of membrane-potential and pH gradient on electron-transfer in cytochrome-oxidase. Biochemistry 23, 4991-4997.
46. Gregory LS, &, Ferguson-Miller S, (1989) Independent control of respiration in cytochrome-c oxidase vesicles by pH and electrical gradients. Biochemistry 28, 2655-2662. (Pubitemid 19094386)
47. Sarti P, Antonini G, Malatesta F, &, Brunori M, (1992) Respiratory control in cytochrome-oxidase vesicles is correlated with the rate of internal electron-transfer. Biochem J 284, 123-127.
48. Oellerich S, Wackerbarth H, &, Hildebrandt P, (2002) Spectroscopic characterization of non-native states of cytochrome c. J Phys Chem B 106, 6566-6580. (Pubitemid 35289249)
49. Oellerich S, Lecomte S, Paternostre M, Heimburg T, &, Hildebrandt P, (2004) Peripheral and integral binding of cytochrome c to phospholipid vesicles. J Phys Chem B 108, 3871-3878.
50. Basova LV, Kurnikov IV, Wang L, Ritov VB, Belikova NA, Vlasova II, Pacheco AA, Winnica DE, Peterson J, Bayir H, et al. (2007) Cardiolipin switch in mitochondria: shutting off the reduction of cytochrome c and turning on the peroxidase activity. Biochemistry 2007, 46.
51. De Biase PM, Doctorovich F, Murgida DH, &, Estrin DA, (2007) Electric field effects on the reactivity of heme model systems. Chem Phys Lett 434, 121-126. (Pubitemid 46053930)