Elementary tetrahelical protein design for diverse oxidoreductase functions

Nature Chemical Biology

Volumn 9, Issue 12, 2013, Pages 826-833

  Farid, Tammer A ^a   Kodali, Goutham ^a   Solomon, Lee A ^a   Lichtenstein, Bruce R ^a,b   Sheehan, Molly M ^a   Fry, Bryan A ^a   Bialas, Chris ^a   Ennist, Nathan M ^a   Siedlecki, Jessica A ^a   Zhao, Zhenyu ^a   Stetz, Matthew A ^a   Valentine, Kathleen G ^a   Anderson, J L Ross ^a,c   Wand, A Joshua ^a   Discher, Bohdana M ^a   Moser, Christopher C ^a   Dutton, P Leslie ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME; CYTOCHROME C; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; MONOMER; OXIDOREDUCTASE; OXYGEN; PEROXIDE; SUPEROXIDE;

ALPHA HELIX; ARTICLE; BIOENGINEERING; CHEMICAL BINDING; ELECTRON TRANSPORT; ENERGY TRANSFER; PARTICLE SIZE; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; SEPARATION TECHNIQUE;

HEME; MODELS, MOLECULAR; MOLECULAR STRUCTURE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXIDOREDUCTASES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEINS;

EID: 84888010557     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1362     Document Type: Article

References (51)

1. Fischer, E. Nobel Lectures, Chemistry 1901-1921 Vol.1 (ed. Nobelstiftelsen) 21-35 (Elsevier, Amsterdam, 1966).
2. Brustad, E.M. & Arnold, F.H. Optimizing non-natural protein function with directed evolution. Curr. Opin. Chem. Biol. 15, 201-210 (2011).
3. Baker, D. An exciting but challenging road ahead for computational enzyme design. Protein Sci. 19, 1817-1819 (2010).
4. Prabhulkar, S., Tian, H., Wang, X.T., Zhu, J.J. & Li, C.Z. Engineered proteins: redox properties and their applications. Antioxid. Redox Signal. 17, 1796-1822 (2012).
5. Edelman, G.M. & Gally, J.A. Degeneracy and complexity in biological systems. Proc. Natl. Acad. Sci. USA 98, 13763-13768 (2001).
6. Lichtenstein, B.R. et al. Engineering oxidoreductases: maquette proteins designed from scratch. Biochem. Soc. Trans. 40, 561-566 (2012).
7. Regan, L. & DeGrado, W.F. Characterization of a helical protein designed from first principles. Science 241, 976-978 (1988).
8. Page, C.C., Moser, C.C., Chen, X. & Dutton, P.L. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402, 47-52 (1999).
9. Robertson, D.E. et al. Design and synthesis of multi-heme proteins. Nature 368, 425-432 (1994).
10. Sharp, R.E., Moser, C.C., Rabanal, F. & Dutton, P.L. Design, synthesis, and characterization of a photoactivatable flavocytochrome molecular maquette. Proc. Natl. Acad. Sci. USA 95, 10465-10470 (1998).
11. Shifman, J.M., Moser, C.C., Kalsbeck, W.A., Bocian, D.F. & Dutton, P.L. Functionalized de novo designed proteins: mechanism of proton coupling to oxidation/reduction in heme protein maquettes. Biochemistry 37, 16815-16827 (1998).
12. Grosset, A.M., Gibney, B.R., Rabanal, F., Moser, C.C. & Dutton, P.L. Proof of principle in a de novo designed protein maquette: an allosterically regulated, charge-activated conformational switch in a tetra-?-helix bundle. Biochemistry 40, 5474-5487 (2001).
13. Anderson, J.L.R., Koder, R.L., Moser, C.C. & Dutton, P.L. Controlling complexity and water penetration in functional de novo protein design. Biochem. Soc. Trans. 36, 1106-1111 (2008).
14. Koder, R.L. et al. Design and engineering of an O2 transport protein. Nature 458, 305-309 (2009).
15. Bender, G.M. et al. De novo design of a single-chain diphenylporphyrin metalloprotein. J. Am. Chem. Soc. 129, 10732-10740 (2007).
16. Ku, J. & Schultz, P.G. Alternate protein frameworks for molecular recognition. Proc. Natl. Acad. Sci. USA 92, 6552-6556 (1995).
17. Predki, P.F. & Regan, L. Redesigning the topology of a four-helix-bundle protein: monomeric Rop. Biochemistry 34, 9834-9839 (1995).
18. Westerlund, K. et al. Making a single-chain four-helix bundle for redox chemistry studies. Protein Eng. Des. Sel. 21, 645-652 (2008).
19. Huang, S.S., Gibney, B.R., Stayrook, S.E., Dutton, P.L. & Lewis, M. X-ray structure of a Maquette scaffold. J. Mol. Biol. 326, 1219-1225 (2003).
20. Aurora, R. & Rose, G.D. Helix capping. Protein Sci. 7, 21-38 (1998).
21. Koder, R.L. et al. Native like structure in designed four ?-helix bundles driven by buried polar interactions. J. Am. Chem. Soc. 128, 14450-14451 (2006).
22. Caffrey, M.S. & Cusanovich, M.A. Site-specific mutagenesis studies of cytochromes c. Biochim. Biophys. Acta 1187, 277-288 (1994).
23. Davies, A.M. et al. Redesign of the interior hydrophilic region of mitochondrial cytochrome c by site-directed mutagenesis. Biochemistry 32, 5431-5435 (1993).
24. Trent, J.T., Hvitved, A.N. & Hargrove, M.S. A model for ligand binding to hexacoordinate hemoglobins. Biochemistry 40, 6155-6163 (2001).
25. Kiger, L. et al. Electron transfer function versus oxygen delivery: a comparative study for several hexacoordinated globins across the animal kingdom. PLoS ONE 6, e20478 (2011).
26. Hamdane, D. et al. Hyperthermal stability of neuroglobin and cytoglobin. FEBS J. 272, 2076-2084 (2005).
27. Fago, A., Mathews, A.J., Moens, L., Dewilde, S. & Brittain, T. The reaction of neuroglobin with potential redox protein partners cytochrome b5 and cytochrome c. FEBS Lett. 580, 4884-4888 (2006).
28. Margoliash, E. & Bosshard, H.R. Guided by electrostatics, a textbook protein comes of age. Trends Biochem. Sci. 8, 316-320 (1983).
29. Moser, C.C. & Dutton, P.L. Cytochrome c and c2 binding dynamics and electron transfer with photosynthetic reaction center protein and other integral membrane redox proteins. Biochemistry 27, 2450-2461 (1988).
30. Ku, H.H., Brunk, U.T. & Sohal, R.S. Relationship between mitochondrial superoxide and hydrogen-peroxide production and longevity of mammalian-species. Free Radic. Biol. Med. 15, 621-627 (1993).
31. Muir Wood, P. The redox potential of the system oxygen-superoxide. FEBS Lett. 44, 22-24 (1974).
32. Zhang, L., Andersen, E.M.E., Khajo, A., Magliozzo, R.S. & Koder, R.L. Dynamic factors affecting gaseous ligand binding in an artificial oxygen transport protein. Biochemistry 52, 447-455 (2013).
33. Cross, A.R., Parkinson, J.F. & Jones, O.T.G. Mechanism of the superoxide-producing oxidase of neutrophils-O2 is necessary for the fast reduction of cytochrome b245 by NADPH. Biochem. J. 226, 881-884 (1985).
34. Lin, C. et al. Association of flavin adenine-dinucleotide with the Arabidopsis blue-light receptor Cry1. Science 269, 968-970 (1995).
35. Aubert, C., Vos, M.H., Mathis, P., Eker, A.P. & Brettel, K. Intraprotein radical transfer during photoactivation of DNA photolyase. Nature 405, 586-590 (2000).
36. Muthiah, C., Ptaszek, M., Nguyen, T.M., Flack, K.M. & Lindsey, J.S. Two complementary routes to 7-substituted chlorins. Partial mimics of chlorophyll b. J. Org. Chem. 72, 7736-7749 (2007).
37. Moser, C.C., Anderson, J.L. & Dutton, P.L. Guidelines for tunneling in enzymes. Biochim. Biophys. Acta 1797, 1573-1586 (2010).
38. Moser, C.C., Keske, J.M., Warncke, K., Farid, R.S. & Dutton, P.L. Nature of biological electron transfer. Nature 355, 796-802 (1992).
39. Massey, V., Stankovich, M. & Hemmerich, P. Light-mediated reduction of flavoproteins with flavins as catalysts. Biochemistry 17, 1-8 (1978).
40. Grzyb, J. et al. Empirical and computational design of iron-sulfur cluster proteins. Biochim. Biophys. Acta 1817, 1256-1262 (2012).
41. Reedy, C.J. & Gibney, B.R. Heme protein assemblies. Chem. Rev. 104, 617-649 (2004).
42. Monien, B.H., Drepper, F., Sommerhalter, M., Lubitz, W. & Haehnel, W. Detection of heme oxygenase activity in a library of four-helix bundle proteins: towards the de novo synthesis of functional heme proteins. J. Mol. Biol. 371, 739-753 (2007).
43. Patel, S.C. & Hecht, M.H. Directed evolution of the peroxidase activity of a de novo-designed protein. Protein Eng. Des. Sel. 25, 445-452 (2012).
44. Smith, B.A. & Hecht, M.H. Novel proteins: from fold to function. Curr. Opin. Chem. Biol. 15, 421-426 (2011).
45. Fry, H.C., Lehmann, A., Saven, J.G., DeGrado, W.F. & Therien, M.J. Computational design and elaboration of a de novo heterotetrameric ?-helical protein that selectively binds an emissive abiological (porphinato)zinc chromophore. J. Am. Chem. Soc. 132, 3997-4005 (2010).
46. Reig, A.J. et al. Alteration of the oxygen-dependent reactivity of de novo Due Ferri proteins. Nat. Chem. 4, 900-906 (2012).
47. Röthlisberger, D. et al. Kemp elimination catalysts by computational enzyme design. Nature 453, 190-195 (2008).
48. Miner, K.D. et al. A designed functional metalloenzyme that reduces O2 to H2O with over one thousand turnovers. Angew. Chem. Int. Ed. Engl. 51, 5589-5592 (2012).
49. Gibney, B.R., Mulholland, S.E., Rabanal, F. & Dutton, P.L. Ferredoxin and ferredoxin-heme maquettes. Proc. Natl. Acad. Sci. USA 93, 15041-15046 (1996).
50. Fisher, M.A., McKinley, K.L., Bradley, L.H., Viola, S.R. & Hecht, M.H. De novo designed proteins from a library of artificial sequences function in Escherichia coli and enable cell growth. PLoS ONE 6, e15364 (2011).
51. Berry, E.A. & Trumpower, B.L. Simultaneous determination of hemes a, b and c from pyridine hemochrome spectra. Anal. Biochem. 161, 1-15 (1987).