De novo protein components for oxidoreductase assembly and biological integration

Current Opinion in Chemical Biology

Volumn 19, Issue 1, 2014, Pages 90-98

  Watkins, Daniel W ^a   Armstrong, Craig T ^a   Anderson, J L Ross ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; LIGAND; OXIDOREDUCTASE; PROTEIN; CYTOCHROME; PROTEIN BINDING;

ELECTRON TRANSPORT; ENZYME MECHANISM; ENZYME SUBSTRATE; HUMAN; IN VIVO STUDY; LIGAND BINDING; LIGHT HARVESTING SYSTEM; OXYGENATION; PROTEIN ASSEMBLY; PROTEIN ENGINEERING; PROTEIN FUNCTION; PROTEIN INTERACTION; REVIEW; BIOCATALYSIS; CHEMISTRY; ENZYME SPECIFICITY; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BIOCATALYSIS; BIOLOGICAL TRANSPORT; CYTOCHROMES; HUMANS; OXIDOREDUCTASES; PROTEIN BINDING; SUBSTRATE SPECIFICITY;

EID: 84896747528     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2014.01.016     Document Type: Review

References (55)

1. Channon K., Bromley E.H.C., Woolfson D.N. Synthetic biology through biomolecular design and engineering. Curr Opin Struct Biol 2008, 18:491-498.
2. Peralta-Yahya P.P., Zhang F., del Cardayre S.B., Keasling J.D. Microbial engineering for the production of advanced biofuels. Nature 2012, 488:320-328.
3. Discher B., Koder R.L., Moser C.C., Dutton P.L. Hydrophilic to amphiphilic design in redox protein maquettes. Curr Opin Chem Biol 2003, 7:741-748.
4. Lichtenstein B.R., Farid T.A., Kodali G., Solomon L.A., Anderson J.L.R., Sheehan M.M., Ennist N.M., Fry B.A., Chobot S.E., Bialas C., et al. Engineering oxidoreductases: maquette proteins designed from scratch. Biochem Soc Trans 2012, 40:561-566.
5. Page C.C., Moser C.C., Dutton P.L. Mechanism for electron transfer within and between proteins. Curr Opin Chem Biol 2003, 7:551-556.
6. Page C.C., Moser C.C., Chen X., Dutton P.L. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 1999, 402:47-52.
7. Moser C.C., Keske J.M., Warncke K., Farid R.S., Dutton P.L. Nature of biological electron transfer. Nature 1992, 355:796-801.
8. Mowat C.G., Chapman S.K. Multi-heme cytochromes-new structures, new chemistry. Dalton Trans 2005, 21:3381-3389.
9. 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 2007, 24:585-609.
10. Sono M., Roach M.P., Coulter E.D., Dawson J.H. Heme-containing oxygenases. Chem Rev 1996, 96:2841-2888.
11. Barber J. Photosynthetic energy conversion: natural and artificial. Chem Soc Rev 2009, 38:185-196.
12. Robertson D.E., Farid R.S., Moser C.C., Urbauer J.L., Mulholland S.E., Pidikiti R., Lear J.D., Wand A.J., DeGrado W.F., Dutton P.L. Design and synthesis of multi-haem proteins. Nature 1994, 368:425-432.
13. Röthlisberger D., Khersonsky O., Wollacott A.M., Jiang L., DeChancie J., Betker J., Gallaher J.L., Althoff E.A., Zanghellini A., Dym O., et al. Kemp elimination catalysts by computational enzyme design. Nature 2008, 453:190-197.
14. Blomberg R., Kries H., Pinkas D.M., Mittl P.R.E., Grütter M.G., Privett H.K., Mayo S.L., Hilvert D. Precision is essential for efficient catalysis in an evolved Kemp eliminase. Nature 2013, 10.1038/nature12623.
15. Kiss G., Çelebi-Ölçüm N., Moretti R., Baker D., Houk K.N. Computational enzyme design. Angew Chem Int Ed Engl 2013, 52:5700-5725.
16. Armstrong C.T., Watkins D.W., Anderson J.L.R. Constructing manmade enzymes for oxygen activation. Dalton Trans 2013, 9:3136-3650.
17. Farid T.A., Kodali G., Solomon L.A., Lichtenstein B.R., Sheehan M.M., Fry B.A., Bialas C., Ennist N.M., Siedlecki J.A., Zhao Z., et al. Elementary tetrahelical protein design for diverse oxidoreductase functions. Nat Chem Biol 2013, 9:826-833.
18. Summa C.M., Lombardi A., Lewis M., DeGrado W.F. Tertiary templates for the design of diiron proteins. Curr Opin Struct Biol 1999, 9:500-508.
19. Nanda V., Koder R.L. Designing artificial enzymes by intuition and computation. Nat Chem 2010, 2:15-24.
20. Moffet D.A., Hecht M.H. De novo proteins from combinatorial libraries. Chem Rev 2001, 101:3191-3203.
21. Smith B.A., Hecht M.H. Novel proteins: from fold to function. Curr Opin Chem Biol 2011, 15:421-426.
22. Regan L., DeGrado W.F. Characterization of a helical protein designed from first principles. Science 1988, 241:976-978.
23. Shifman J.M., Gibney B.R., Sharp R.E., Dutton P.L. Heme redox potential control in de novo designed four-alpha-helix bundle proteins. Biochemistry 2000, 39:14813-14821.
24. Gibney B.R., Isogai Y., Rabanal F., Reddy K.S., Grosset A.M., Moser C.C., Dutton P.L. Self-assembly of heme A and heme B in a designed four-helix bundle: implications for a cytochrome c oxidase maquette. Biochemistry 2000, 39:11041-11049.
25. Anderson J.L.R., Armstrong C.T., Kodali G., Lichtenstein B.R., Watkins D.W., Mancini J.A., Boyle A.L., Farid T.A., Crump M.P., Moser C., et al. Constructing a man-made, oxygen binding c-type cytochrome maquette in vivo. Chem Sci 2014, 5:507-514.
26. Gibney B.R., Mulholland S.E., Rabanal F., Dutton P.L. Ferredoxin and ferredoxin-heme maquettes. Proc Natl Acad Sci USA. 1996, 93:15041-15046.
27. Huang S.S., Koder R.L., Lewis M., Wand A.J., Dutton P.L. The HP-1 maquette: from an apoprotein structure to a structured hemoprotein designed to promote redox-coupled proton exchange. Proc Natl Acad Sci USA 2004, 101:5536-5541.
28. Discher B.M., Noy D., Strzalka J., Ye S., Moser C.C., Lear J.D., Blasie J.K., Dutton P.L. Design of amphiphilic protein maquettes: controlling assembly, membrane insertion, and cofactor interactions. Biochemistry 2005, 44:12329-12343.
29. Noy D., Discher B.M., Rubtsov I.V., Hochstrasser R.M., Dutton P.L. Design of amphiphilic protein maquettes: enhancing maquette functionality through binding of extremely hydrophobic cofactors to lipophilic domains. Biochemistry 2005, 44:12344-12354.
30. Grzyb J., Xu F., Nanda V., Łuczkowska R., Reijerse E., Lubitz W., Noy D. Empirical and computational design of iron-sulfur cluster proteins. Biochim Biophys Acta 2012, 1817:1256-1262.
31. Grzyb J., Xu F., Weiner L., Reijerse E.J., Lubitz W., Nanda V., Noy D. De novo design of a non-natural fold for an iron-sulfur protein: alpha-helical coiled-coil with a four-iron four-sulfur cluster binding site in its central core. Biochim Biophys Acta 2010, 1797:406-413.
32. Roy A., Sarrou I., Vaughn M.D., Astashkin A.V., Ghirlanda G. De novo design of an artificial bis[4Fe-4S] binding protein. Biocemistry 2013, 1797:7586-7594.
33. Bender G.M., Lehmann A., Zou H., Cheng H., Fry H.C., Engel D., Therien M.J., Blasie J.K., Roder H., Saven J.G., et al. De novo design of a single-chain diphenylporphyrin metalloprotein. J Am Chem Soc 2007, 129:10732-10740.
34. Korendovych I., Senes A., Kim Y.H., Lear J.D., Fry C.H., Therien M.J., Blasie J.K., Walker F.A., DeGrado W.F. De novo design and molecular assembly of a transmembrane diporphyrin-binding protein complex. J Am Chem Soc 2010, 132:15516-15518.
35. Fry H.C., Lehmann A., Sinks L.E., Asselberghs I., Tronin A., Krishnan V., Blasie J.K., Clays K., DeGrado W.F., Saven J.G., et al. Computational de novo design and characterization of a protein that selectively binds a highly hyperpolarizable abiological chromophore. J Am Chem Soc 2013, 135:13914-13926.
36. Faiella M., Andreozzi C., de Rosales R.T.M., Pavone V., Maglio O., Nastri F., DeGrado W.F., Lombardi A. An artificial di-iron oxo-protein with phenol oxidase activity. Nat Chem Biol 2009, 5:882-884.
37. Kaplan J., DeGrado W.F. De novo design of catalytic proteins. Proc Natl Acad Sci USA 2004, 101:11566-11570.
38. Cherny I., Korolev M., Koehler A.N., Hecht M.H. Proteins from an unevolved library of de novo designed sequences bind a range of small molecules. ACS Synth Biol 2012, 1:130-138.
39. 2 transport protein. Nature 2009, 458:305-309.
40. Patel S.C., Hecht M.H. Directed evolution of the peroxidase activity of a de novo-designed protein. Protein Eng Des Sel 2012, 25:445-451.
41. Calhoun J.R., Bell C.B., Smith T.J., Thamann T.J., DeGrado W.F., Solomon E.I. Oxygen reactivity of the biferrous site in the de novo designed four helix bundle peptide DFsc: nature of the "intermediate" and reaction mechanism. J Am Chem Soc 2008, 130:9188-9189.
42. Reig A.J., Pires M.M., Snyder R.A., Wu Y., Jo H., Kulp D.W., Butch S.E., Calhoun J.R., Szyperski T., Solomon E.I., et al. Alteration of the oxygen-dependent reactivity of de novo Due Ferri proteins. Nat Chem 2012, 4:900-906.
43. Tegoni M., Yu F., Bersellini M., Penner-Hahn J.E., Pecoraro V.L. Designing a functional type 2 copper center that has nitrite reductase activity within α-helical coiled coils. Proc Natl Acad Sci USA 2012, 109:21234-21239.
44. Yu F., Penner-Hahn J.E., Pecoraro V.L. De novo designed metallopeptides with type 2 copper centers: modulation of reduction potentials and nitrite reductase activities. J Am Chem Soc 2013, 135:18096-18107.
45. Roy A., Madden C., Ghirlanda G. Photo-induced hydrogen production in a helical peptide incorporating a [FeFe] hydrogenase active site mimic. Chem Commun (Camb) 2012, 48:9816-9818.
46. Arpino J.A.J., Czapinska H., Piasecka A., Edwards W.R., Barker P., Gajda M.J., Bochtler M., Jones D.D. Structural basis for efficient chromophore communication and energy transfer in a constructed didomain protein scaffold. J Am Chem Soc 2012, 134:13632-13640.
47. Dodhia V.R., Fantuzzi A., Gilardi G. Engineering human cytochrome P450 enzymes into catalytically self-sufficient chimeras using molecular Lego. J Biol Inorg Chem 2006, 11:903-916.
48. Kries H., Blomberg R., Hilvert D. De novo enzymes by computational design. Curr Opin Chem Biol 2013, 17:221-228.
49. Mavridou D.A.I., Ferguson S.J., Stevens J.M. Cytochrome c assembly. IUBMB Life 2013, 65:209-216.
50. Stevens J.M., Daltrop O., Allen J.W.A., Ferguson S.J. C-type cytochrome formation: chemical and biological enigmas. Acc Chem Res 2004, 37:999-1007.
51. San Francisco B., Bretsnyder E.C., Kranz R.G. Human mitochondrial holocytochrome c synthase's heme binding, maturation determinants, and complex formation with cytochrome c. Proc Natl Acad Sci USA 2013, 110:E788-E797.
52. 3 oxidase in Escherichia coli. Biochem Biophys Res Commun 1998, 251:744-747.
53. Mavridou D.A.I., Clark M.N., Choulat C., Ferguson S.J., Stevens J.M. Probing heme delivery processes in cytochrome c biogenesis system I. Biochemistry 2013, 52:7262-7270.
54. Jasion V.S., Doukov T., Pineda S.H., Li H., Poulos T.L. Crystal structure of the Leishmania major peroxidase-cytochrome c complex. Proc Natl Acad Sci USA 2012, 109:18390-18394.
55. Craig D.H., Chapman S.K., Daff S. Calmodulin activates electron transfer through neuronal nitric-oxide synthase reductase domain by releasing an NADPH-dependent conformational lock. J Biol Chem 2002, 277:33987-33994.