Enhancement of cytochrome c catalytic behaviour by affecting the heme environment using functionalized carbon-based nanomaterials

Process Biochemistry

Volumn 48, Issue 7, 2013, Pages 1010-1017

  Patila, Michaela ^a   Pavlidis, Ioannis V ^a,b   Diamanti, Evmorfia K ^a   Katapodis, Petros ^a   Gournis, Dimitrios ^a   Stamatis, Haralampos ^a  

^a UNIVERSITY OF IOANNINA   (Greece)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Carbon nanotubes; Carbon based nanomaterials; Cytochrome c; Graphene oxide; Peroxidase activity

Indexed keywords

CARBON-BASED; CATALYTIC EFFICIENCIES; CYTOCHROME C; GRAPHENE OXIDES; PEROXIDASE ACTIVITIES; PEROXIDASE-LIKE ACTIVITIES; SECONDARY STRUCTURES; SURFACE FUNCTIONALIZATION;

CARBON NANOTUBES; CIRCULAR DICHROISM SPECTROSCOPY; ENZYME ACTIVITY; GRAPHENE; PORPHYRINS;

NANOSTRUCTURED MATERIALS;

EID: 84880078753     PISSN: 13595113     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.procbio.2013.04.021     Document Type: Article

References (63)

1. J.H. Park, H. Xue, J.S. Jung, and K. Ryu Immobilization of laccase on carbon nanomaterials Korean J Chem Eng 29 2012 1409 1412
2. I.V. Pavlidis, T. Vorhaben, T. Tsoufis, P. Rudolf, U.T. Bornscheuer, and D. Gournis Development of effective nanobiocatalytic systems through the immobilization of hydrolases on functionalized carbon-based nanomaterials Bioresour Technol 115 2012 164 171
3. J. Zhang, F. Zhang, H. Yang, X. Huang, H. Liu, and J. Zhang Graphene oxide as a matrix for enzyme immobilization Langmuir 26 2010 6083 6085
4. W. Shang, J.H. Nuffer, V.A. Muñiz-Papandrea, W. Colón, R.W. Siegel, and J.S. Dordick Cytochrome c on silica nanoparticles: influence of nanoparticles size on protein structure, stability and activity Small 5 2009 470 476
5. W. Feng, and P. Ji Enzymes immobilized on carbon nanotubes Biotechnol Adv 29 2011 889 895
6. L. Wang, L. Wei, Y. Chen, and R. Jiang Specific and reversible immobilization of NADH oxidase on functionalized carbon nanotubes J Biotechnol 150 2010 57 63
7. V.N.T. Satyanarayana, S.V.N.T. Kuchibhatla, A.S. Karakoti, D. Bera, and S. Seal One dimensional nanostructured materials Prog Mater Sci 52 2007 699 913
8. E. Katz, and I. Willner Biomolecule-functionalized carbon nanotubes: applications in nanobioelectronics ChemPhysChem 5 2004 1084 1104
9. P.M. Ajayan Nanotubes from carbon Chem Rev 99 1999 1787 1799
10. H.L. Pang, J. Liu, D. Hu, X.H. Zhang, and J.H. Chen Immobilization of laccase onto 1-amynopyrene functionalized carbon nanotubes and their electrocatalytic activity for oxygen reduction Electrochim Acta 55 2010 6611 6616
11. B.J. Kim, B.K. Kang, Y.Y. Bahk, K.H. Yoo, and K.J. Lim Immobilization of horseradish peroxidase on multi-walled carbon nanotubes and its enzymatic stability Curr Appl Phys 9 2009 263 265
12. T.W. Tsai, G. Heckert, L.F. Neves, Y. Tan, D.W. Kao, and R.G. Harrison Adsorption of glucose oxidase onto single-walled carbon nanotubes and its application in layer-by-layer biosensors Anal Chem 81 2009 7917 7925
13. P. Asuri, S.S. Bale, R.C. Pangule, D.A. Shah, R.S. Kane, and J.S. Dordick Structure, function and stability of enzymes covalently attached to single-walled carbon nanotubes Langmuir 23 2007 12318 12321
14. S. Park, and R.S. Ruoff Chemical methods for the production of graphenes Nat Nanotechnol 4 2009 217 224
15. S. Stankovich, D.A. Dikin, G.H.B. Dommett, K.M. Kohlhaas, E.J. Zimney, and E.A. Stach Graphene-based composite materials Nature 442 2006 282 286
16. T. Kuila, S. Bose, A.K. Mishra, P. Khanra, N.H. Kim, and J.H. Lee Chemical functionalization of graphene and its applications Prog Mater Sci 57 2012 1061 1105
17. D. Chen, H. Feng, and J. Li Graphene oxide: preparation, functionalization, and electrochemical applications Chem Rev 112 2012 6027 6053
18. V. Georgakilas, M. Otyepka, A.B. Bourlinos, V. Chandra, N. Kim, and K.C. Kemp Functionalization of graphene: covalent and non-covalent approaches, derivatives and applications Chem Rev 112 2012 6165 6214
19. Y-L. Zhao, and J.F. Stoddart Non-covalent functionalization of single-walled carbon nanotubes Accounts Chem Res 42 2009 1161 1171
20. I.V. Pavlidis, T. Vorhaben, D. Gournis, G.K. Papadopoulos, U.T. Bornscheuer, and H. Stamatis Regulation of catalytic behaviour of hydrolases through interactions with functionalized carbon-based nanomaterials J Nanopart Res 14 2012 842 852
21. Q. Mu, W. Liu, Y. Xing, H. Zhou, Z. Li, and Y. Zhang Protein binding by functionalized multiwalled carbon nanotubes is governed by the surface chemistry of both parties and the nanotubes diameter J Phys Chem C 112 2008 3300 3307
22. R. Vazquez-Duhalt Cytochrome c as a biocatalyst J Mol Catal B: Enzym 7 1999 241 249
23. S. Alwarappan, R.K. Joshi, M.K. Ram, and A. Kumar Electron transfer mechanism of cytochrome c at graphene electrode Appl Phys Lett 96 2010 263702 263704
24. J-F. Wu, M-Q. Xu, and G-C. Zhao Graphene-based modified electrode for the direct electron transfer of cytochrome c and biosensing Electrochem Commun 12 2010 175 177
25. D.H. Nagaraju, R.K. Pandey, and V. Lakshiminarayanan Electrochemical studies of cytochrome c functionalized single walled carbon nanotubes on self-assembled monlayer of 4-ATP on gold J Electroanal Chem 627 2009 63 68
26. H.A. Heering, K.A. Williams, S. de Vries, and C. Dekker Specific vectorial immobilization of oligonucleotide-modified yeast cytochrome c on carbon nanotubes ChemPhysChem 7 2006 1705 1709
27. Y. Goto, H. Hagihara, D. Hamada, M. Hoshino, and J. Nishi Acid-induced unfolding and refolding transitions of cytochrome c: a three-state mechanism in water and deuterium oxide Biochemistry 32 1993 11878 11885
28. R.W. Noble, and Q.H. Gibson The reaction of ferrous horseradish peroxidase with hydrogen peroxide J Biol Chem 245 1970 2409 2413
29. A.B. Bourlinos, D. Gournis, D. Petridis, T. Szabó, A. Szeri, and I. Dékány Graphite oxide: chemical reduction to graphite and surface modification with primary aliphatic amines and amino acids Langmuir 19 2003 6050 6055
30. I.V. Pavlidis, T. Tsoufis, A. Enotiadis, D. Gournis, and H. Stamatis Functionalized multi-wall carbon nanotubes for lipase immobilization Adv Eng Mater 12 2010 179 183
31. A. Enotiadis, K. Angeli, N. Baldino, I. Nicotera, and D. Gournis Graphene-based nafion nanocomposite membranes: enhanced proton transport and water retention by novel organo-functionalized graphene oxide nanosheets Small 8 2012 3338 3349
32. R.Y.N. Gengler, A. Veligura, A. Enotiadis, E.K. Diamanti, D. Gournis, and C. Józsa Large-yield preparation of high-electronic-quality graphene by a Langmuir-Schaefer approach Small 6 2010 35 39
33. D.V. Stergiou, E.K. Diamanti, D. Gournis, and M.I. Prodromidis Comparative study of different types of graphene as electrocatalysts for ascorbic acid Electrochem Commun 12 2010 1307 1309
34. J.A. Villegas, A.G. Mauk, and R. Vazquez-Duhalt A cytochrome c variant resistant to heme degradation by hydrogen peroxide Chem Biol 7 2000 237 244
35. V.C. Sanchez, A. Jachak, R.H. Hurt, and A.B. Kane Biological interactions of graphene-family nanomaterials: an interdisciplinary review Chem Res Toxicol 25 2012 15 34
36. Q. Shi, D. Yang, Y. Su, J. Li, Z. Jiang, and Y. Jiang Covalent functionalization of multi-walled carbon nanotubes by lipase J Nanopart Res 9 2007 1205 1210
37. J.M. Gómez, M.D. Romero, and T.M. Fernández Immobilization of β-glucosidase on carbon nanotubes Catal Lett 101 2005 275 278
38. X. Zuo, S. He, D. Li, C. Peng, Q. Huang, and S. Sang Graphene oxide-facilitated electron transfer of metalloproteins at electrode surfaces Langmuir 26 2010 1936 1939
39. W. Shang, J.H. Nuffer, J.S. Dordick, and R.W. Siegel Unfolding of ribonuclease A on silica nanoparticles surface Nano Lett 7 2007 1991 1995
40. M. Lundqvist, I. Sethson, and B.H. Jonsson Protein adsorption onto silica nanoparticles: conformational changes on the particles' curvature and the protein stability Langmuir 20 2004 10639 10647
41. T. Xue, S. Jiang, Y. Qu, Q. Su, R. Cheng, and S. Dubin Graphene-supported hemin as a highly active biomimetic oxidation catalyst Angew Chem Int Ed 51 2012 3822 3825
42. E. Valušová, P. Švec, and M. Antalík Structural and thermodynamic behavior of cytochrome c assembled with glutathione-covered gold nanoparticles J Biol Inorg Chem 14 2009 621 630
43. S. Prasad, N.C. Maiti, S. Mazumdar, and S. Mitra Reaction of hydrogen peroxide and peroxidase activity in carboxymethylated cytochrome c: spectroscopic and kinetic studies Biochim Biophys Acta 1596 2002 63 75
44. A. Schejter, and I. Aviram The effects of alkylation of methionyl residues on the properties of horse cytochrome c J Biol Chem 245 1970 1552 1557
45. F. Farivar, A.A. Moosavi-Movahedi, Y. Sevidbakht, K. Nazari, J. Hong, and N. Sheibani Cytochrome c in sodium dodecyl sulfate reverse micelle nanocage: from a classic electron transfer protein to an artificial peroxidase enzyme Biochem Eng J 49 2010 89 94
46. K. Shimojo, N. Kamiya, F. Tani, H. Nagarama, Y. Naruta, and M. Goto Extractive solubilization, structural change, and functional conversion of cytochrome c in ionic liquids via crown ether complexation Anal Chem 78 2006 7735 7742
47. T. Ono, and M. Goto Peroxidative catalytic behaviour of cytochrome c solubilised in reverse micelles Biochem Eng J 28 2006 156 160
48. N. Sanghera, and T.J.T. Pinheiro Unfolding and refolding of cytochrome c driven by the interaction with lipid micelles Protein Sci 9 2000 1194 1202
49. T.J.T. Pinheiro, G.A. Elöve, A. Watts, and H. Roder Structural and kinetic description of cytochrome c unfolding induced by the interaction with lipid vesicles Biochemistry 36 1997 13122 13132
50. L.C.L. Huang, and H.C. Chang Adsorption and immobilization of cytochrome c on nanodiamonds Langmuir 20 2004 5879 5884
51. R.J.P. Williams NMR studies of mobility within protein structure Eur J Biochem 183 1989 479 497
52. Z. Wang, T. Matsuo, S. Nagao, and S. Hirota Peroxidase activity enhancement of horse cytochrome c by dimerization Org Biomol Chem 9 2011 4766 4769
53. Z. Liu, H. Lin, S. Ye, Q.Y. Liu, Z. Meng, and C.M. Zhang Remarkably high activities of testicular cytochrome c in destroying reactive oxygen species and in triggering apoptosis Proc Natl Acad Sci 103 2006 8965 8970
54. T.M. Florence The degradation of cytochrome c by hydrogen peroxide J Inorg Biochem 23 1985 131 141
55. Y. Looze, E. Palastro, C. Gielens, and J. Leonis Iso-cytochrome c species from baker's yeast: analysis of their circular-dichroism spectra Biochem J 157 1976 773 775
56. J.T. Cang-Rong, and G. Pastorin The influence of carbon nanotubes on enzyme activity and structure: investigation of different immobilization procedures through enzyme kinetics and circular dichroism studies Nanotechnology 20 2009 25102 25122
57. R.W. Woody, and M.C. Hsu Origin of the heme Cotton effects in myoglobin and hemoglobin J Am Chem Soc 93 1971 3515 3525
58. Y.P. Meyer Far ultraviolet circular dichroism spectra of cytochrome c Biochim Biophys Acta 154 1968 84 90
59. W. Wei, and N.D. Danielson Fluorescence and circular dichroism spectroscopy of cytochrome c in alkylammonium formate ionic liquids Biomacromolecules 12 2011 290 297
60. U. Ahluwalia, S.M. Nayeem, and S. Deep The non-native conformations of cytochrome c in sodium dodecyl sulfate and their modulation by ATP Eur Biophys J 40 2011 259 271
61. Y.P. Meyer Circular dichroism studies of electron-transport components Curr Top Bioenerg 14 1985 149 188
62. Y.G. Thomas, R.A. Goldbeck, and D.S. Kliger Characterization of equilibrium intermediates in denaturant-induced unfolding of ferrous and ferric cytochromes c using magnetic circular dichroism, circular dichroism, and optical absorption spectroscopies Biopolymers 57 2000 29 36
63. P. Asuri, S.S. Bale, R.C. Pangule, D.A. Shah, R.S. Kane, and J.S. Dordick Structure, function, and stability of enzymes covalently attached to single-walled carbon nanotubes Langmuir 23 2007 12318 12321