Design and improvement of artificial redox modules by molecular fusion of flavodoxin and flavodoxin reductase from Escherichia coli

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Bakkes, Patrick J ^a   Biemann, Stefan ^a   Bokel, Ansgar ^a   Eickholt, Marc ^a   Girhard, Marco ^a   Urlacher, Vlada B ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; FLAVODOXIN; FLAVODOXIN NADPH OXIDOREDUCTASE; HYBRID PROTEIN; OXIDOREDUCTASE;

ENZYMOLOGY; ESCHERICHIA COLI; METABOLISM; OXIDATION REDUCTION REACTION;

ELECTRON TRANSPORT COMPLEX IV; ESCHERICHIA COLI; FLAVODOXIN; NADH, NADPH OXIDOREDUCTASES; OXIDATION-REDUCTION; RECOMBINANT FUSION PROTEINS;

EID: 84937605477     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep12158     Document Type: Article

References (54)

1. Fujii, K. & Huennekens, F. M. Activation of methionine synthetase by a reduced triphosphopyridine nucleotide-dependent flavoprotein system. J. Biol. Chem. 249, 6745-6753 (1974).
2. Birch, O. M., Fuhrmann, M. & Shaw, N. M. Biotin synthase from Escherichia coli, an investigation of the low molecular weight and protein components required for activity in vitro. J. Biol. Chem. 270, 19158-19165 (1995).
3. Blaschkowski, H. P., Neuer, G., Ludwig-Festl, M. & Knappe, J. Routes of flavodoxin and ferredoxin reduction in Escherichia coli. CoA-acylating pyruvate: flavodoxin and NADPH: flavodoxin oxidoreductases participating in the activation of pyruvate formatelyase. Eur. J. Biochem. 123, 563-569 (1982).
4. Bianchi, V. et al. Flavodoxin is required for the activation of the anaerobic ribonucleotide reductase. Biochem. Biophys. Res. Commun. 197, 792-797 (1993).
5. Bianchi, V. et al. Escherichia coli ferredoxin NADP+ reductase: activation of E. coli anaerobic ribonucleotide reduction, cloning of the gene (fpr), and overexpression of the protein. J. Bacteriol. 175, 1590-1595 (1993).
6. McIver, L. et al. Characterisation of flavodoxin NADP+ oxidoreductase and flavodoxin; key components of electron transfer in Escherichia coli. Eur. J. Biochem. 257, 577-585 (1998).
7. Lamb, D. C. et al. The cytochrome P450 complement (CYPome) of Streptomyces coelicolor A3(2). J. Biol. Chem. 277, 24000-24005 (2002).
8. Barnes, H. J., Arlotto, M. P. & Waterman, M. R. Expression and enzymatic activity of recombinant cytochrome P450 17 alphahydroxylase in Escherichia coli. Proc. Natl Acad. Sci. USA. 88, 5597-5601 (1991).
9. Jenkins, C. M. & Waterman, M. R. NADPH-flavodoxin reductase and flavodoxin from Escherichia coli: characteristics as a soluble microsomal P450 reductase. Biochemistry 37, 6106-6113 (1998).
10. Dong, M. S., Yamazaki, H., Guo, Z. & Guengerich, F. P. Recombinant human cytochrome P450 1A2 and an N-terminal-truncated form: construction, purification, aggregation properties, and interactions with flavodoxin, ferredoxin, and NADPH-cytochrome P450 reductase. Arch. Biochem. Biophys. 327, 11-19 (1996).
11. Yamazaki, H., Ueng, Y. F., Shimada, T. & Guengerich, F. P. Roles of divalent metal ions in oxidations catalyzed by recombinant cytochrome P450 3A4 and replacement of NADPH-cytochrome P450 reductase with other flavoproteins, ferredoxin, and oxygen surrogates. Biochemistry 34, 8380-8389 (1995).
12. Girhard, M., Klaus, T., Khatri, Y., Bernhardt, R. & Urlacher, V. B. Characterization of the versatile monooxygenase CYP109B1 from Bacillus subtilis. Appl. Microbiol. Biotechnol. 87, 595-607 (2010).
13. Jenkins, C. M. & Waterman, M. R. Flavodoxin and NADPH-flavodoxin reductase from Escherichia coli support bovine cytochrome P450c17 hydroxylase activities. J. Biol. Chem. 269, 27401-27408 (1994).
14. Urlacher, V. B. & Girhard, M. Cytochrome P450 monooxygenases: an update on perspectives for synthetic application. Trends Biotechnol. 30, 26-36 (2012).
15. Lewis, J. C., Coelho, P. S. & Arnold, F. H. Enzymatic functionalization of carbon-hydrogen bonds. Chem. Soc. Rev. 40, 2003-2021 (2011).
16. Bernhardt, R. Cytochromes P450 as versatile biocatalysts. J. Biotechnol. 124, 128-145 (2006).
17. McLean, K. J., Girvan, H. M. & Munro, A. W. Cytochrome P450/redox partner fusion enzymes: biotechnological and toxicological prospects. Expert Opin. Drug Metab. Toxicol. 3, 847-863 (2007).
18. Hlavica, P. Assembly of non-natural electron transfer conduits in the cytochrome P450 system: a critical assessment and update of artificial redox constructs amenable to exploitation in biotechnological areas. Biotechnol. Adv. 27, 103-121 (2009).
19. Sadeghi, S. J. & Gilardi, G. Chimeric P450 enzymes: activity of artificial redox fusions driven by different reductases for biotechnological applications. Biotechnol. Appl. Biochem. 60, 102-110 (2013).
20. Hannemann, F., Bichet, A., Ewen, K. M. & Bernhardt, R. Cytochrome P450 systems-biological variations of electron transport chains. Biochim. Biophys. Acta 1770, 330-344 (2007).
21. Munro, A. W., Girvan, H. M. & McLean, K. J. Variations on a (t)heme-novel mechanisms, redox partners and catalytic functions in the cytochrome P450 superfamily. Nat. Prod. Rep. 24, 585-609 (2007).
22. Whitehouse, C. J., Bell, S. G. & Wong, L. L. P450(BM3) (CYP102A1): connecting the dots. Chem. Soc. Rev. 41, 1218-1260 (2012).
23. Munro, A. W., Girvan, H. M. & McLean, K. J. Cytochrome P450-redox partner fusion enzymes. Biochim. Biophys. Acta 1770, 345-359 (2007).
24. Chen, X., Zaro, J. L. & Shen, W. C. Fusion protein linkers: property, design and functionality. Adv. Drug. Deliv. Rev. 65, 1357- 1369 (2013).
25. George, R. A. & Heringa, J. An analysis of protein domain linkers: their classification and role in protein folding. Protein Eng. 15, 871-879 (2002).
26. Argos, P. An investigation of oligopeptides linking domains in protein tertiary structures and possible candidates for general gene fusion. J. Mol. Biol. 211, 943-958 (1990).
27. Sibbesen, O., De Voss, J. J. & Montellano, P. R. Putidaredoxin reductase-putidaredoxin-cytochrome P450cam triple fusion protein. Construction of a self-sufficient Escherichia coli catalytic system. J. Biol. Chem. 271, 22462-22469 (1996).
28. Cao, P. R., Bulow, H., Dumas, B. & Bernhardt, R. Construction and characterization of a catalytic fusion protein system: P-450(11beta)-adrenodoxin reductase-adrenodoxin. Biochim. Biophys. Acta 1476, 253-264 (2000).
29. Mandai, T., Fujiwara, S. & Imaoka, S. Construction and engineering of a thermostable self-sufficient cytochrome P450. Biochem. Biophys. Res. Commun. 384, 61-65 (2009).
30. Harikrishna, J. A., Black, S. M., Szklarz, G. D. & Miller, W. L. Construction and function of fusion enzymes of the human cytochrome P450scc system. DNA Cell Biol. 12, 371-379 (1993).
31. Wittenberg, G., Sheffler, W., Darchi, D., Baker, D. & Noy, D. Accelerated electron transport from photosystem I to redox partners by covalently linked ferredoxin. Phys. Chem. Chem. Phys. 15, 19608-19614 (2013).
32. Lacour, T. & Ohkawa, H. Engineering and biochemical characterization of the rat microsomal cytochrome P4501A1 fused to ferredoxin and ferredoxin-NADP(+ ) reductase from plant chloroplasts. Biochim. Biophys. Acta. 1433, 87-102 (1999).
33. Ingelman, M., Bianchi, V. & Eklund, H. The three-dimensional structure of flavodoxin reductase from Escherichia coli at 1.7 A resolution. J. Mol. Biol. 268, 147-157 (1997).
34. Hoover, D. M. & Ludwig, M. L. A flavodoxin that is required for enzyme activation: the structure of oxidized flavodoxin from Escherichia coli at 1.8 A resolution. Protein Sci. 6, 2525-2537 (1997).
35. Belsare, K. D. et al. P-LinK: A method for generating multicomponent cytochrome P450 fusions with variable linker length. Biotechniques 57, 13-20 (2014).
36. Sadeghi, S. J., Meharenna, Y. T., Fantuzzi, A., Valetti, F. & Gilardi, G. Engineering artificial redox chains by molecular 'Lego'. Faraday Discuss. 116, 135-153 (2000).
37. Gilardi, G. et al. Molecular Lego: design of molecular assemblies of P450 enzymes for nanobiotechnology. Biosens. Bioelectron. 17, 133-145 (2002).
38. Sabbadin, F., Grogan, G. & Bruce, N. C. LICRED: a versatile drop-in vector for rapid generation of redox-self-sufficient cytochromes P450. Methods Mol. Biol. 987, 239-249 (2013).
39. Sabbadin, F. et al. LICRED: a versatile drop-in vector for rapid generation of redox-self-sufficient cytochrome P450s. Chembiochem. 11, 987-994 (2010).
40. Hirakawa, H. & Nagamune, T. Use of Sulfolobus solfataricus PCNA subunit proteins to direct the assembly of multimeric enzyme complexes. Methods Mol. Biol. 978, 149-163 (2013).
41. Aliverti, A. & Zanetti, G. A three-domain iron-sulfur flavoprotein obtained through gene fusion of ferredoxin and ferredoxin- NADP+ reductase from spinach leaves. Biochemistry 36, 14771-14777 (1997).
42. Deng, Z. et al. A productive NADP+ binding mode of ferredoxin-NADP + reductase revealed by protein engineering and crystallographic studies. Nat. Struct. Biol. 6, 847-853 (1999).
43. Piubelli, L. et al. Competition between C-terminal tyrosine and nicotinamide modulates pyridine nucleotide affinity and specificity in plant ferredoxin-NADP(+ ) reductase. J. Biol. Chem. 275, 10472-10476 (2000).
44. Nogues, I. et al. Role of the C-terminal tyrosine of ferredoxin-nicotinamide adenine dinucleotide phosphate reductase in the electron transfer processes with its protein partners ferredoxin and flavodoxin. Biochemistry 43, 6127-6137 (2004).
45. Moser, C. C., Keske, J. M., Warncke, K., Farid, R. S. & Dutton, P. L. Nature of biological electron transfer. Nature 355, 796-802 (1992).
46. Tanaka, T., Yokoyama, S. & Kuroda, Y. Improvement of domain linker prediction by incorporating loop-length-dependent characteristics. Biopolymers 84, 161-168 (2006).
47. Sambook, J. & Russell, D. W. Molecular cloning: a laboratory manual, 3nd ed. (Cold Spring Harbor Laboratory Press, 2001).
48. Girhard, M. et al. Regioselective biooxidation of (+ )-valencene by recombinant E. coli expressing CYP109B1 from Bacillus subtilis in a two-liquid-phase system. Microb. Cell Fact. 8, 36 (2009).
49. Omura, T. & Sato, R. The Carbon Monoxide-Binding Pigment of Liver Microsomes. I. Evidence for Its Hemoprotein Nature. J. Biol. Chem. 239, 2370-2378 (1964a).
50. Omura, T. & Sato, R. The Carbon Monoxide-Binding Pigment of Liver Microsomes. II. Solubilization, Purification, and Properties. J. Biol. Chem. 239, 2379-2385 (1964b).
51. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 (1976).
52. Vermilion, J. L. & Coon, M. J. Highly purified detergent-solubilized NADPH-cytochrome P-450 reductase from phenobarbitalinduced rat liver microsomes. Biochem. Biophys. Res. Commun. 60, 1315-1322 (1974).
53. van Gelder, B. & Slater, E. C. The extinction coefficient of cytochrome c. Biochim. Biophys. Acta 58, 593-595 (1962).
54. Girhard, M., Tieves, F., Weber, E., Smit, M. S. & Urlacher, V. B. Cytochrome P450 reductase from Candida apicola: versatile redox partner for bacterial P450s. Appl. Microbiol. Biotechnol. 97, 1625-1635 (2013).