Hydrophilic to amphiphilic design in redox protein maquettes

Current Opinion in Chemical Biology

Volumn 7, Issue 6, 2003, Pages 741-748

  Discher, Bohdana M ^a   Koder, Ronald L ^a   Moser, Christopher C ^a   Dutton, P Leslie ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; AMPHOPHILE; MEMBRANE PROTEIN; OXIDOREDUCTASE; PROTON;

ALPHA HELIX; COMPLEX FORMATION; ELECTRIC FIELD; ELECTRON TRANSPORT; HUMAN; HYDROGEN BOND; HYDROPHILICITY; LIPOPHILICITY; OXIDATION REDUCTION REACTION; PROTEIN STRUCTURE; REVIEW; SOLUBILITY;

EID: 0344851884     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2003.10.013     Document Type: Review

References (60)

1. Fischer E: Synthesen in der Purin- und Zuckergruppe. In Les Prix Nobel en 1902. Edited by Cleve PT, Hasselberg C-B, Morner K-A-H: P-A Norstedt & Fils; 1905.
2. Hecht M.H., Richardson J.S., Richardson D.C., Ogden R.C. De novo design, expression, and characterization of Felix - a 4-helix bundle protein of native-like sequence. Science. 249:1990;884-891.
3. Silverman J.A., Balakrishnan R., Harbury P.B. Reverse engineering the (beta/alpha)(8) barrel fold. Proc. Natl. Acad. Sci. USA. 98:2001;3092-3097.
4. Ramirez-Alvarado M., Blanco F.J., Serrano L. De novo design and structural analysis of a model beta-hairpin peptide system. Nat. Struct. Biol. 3:1996;604-612.
5. Wei Y.N., Liu T., Sazinsky S.L., Moffet D.A., Pelczer I., Hecht M.H. Stably folded de novo proteins from a designed combinatorial library. Protein Sci. 12:2003;92-102 The technique of template-assisted bundle assembly using combinatorial libraries dramatically improved the probability of getting uniquely structured four helix bundles by extending helices from 14 to 20 residues.
6. Dai Q.H., Tommos C., Fuentes E.J., Blomberg M.R.A., Dutton P.L., Wand A.J. Structure of a de novo designed protein model of radical enzymes. J. Am. Chem. Soc. 124:2002;10952-10953.
7. Di Costanzo L., Wade H., Geremia S., Randaccio L., Pavone V., DeGrado W.F., Lombardi A. Toward the de novo design of a catalytically active helix bundle: a substrate-accessible carboxylate-bridged dinuclear metal center. J Am Chem Soc. 123:2001;12749-12757 The most sophisticated example to date of a catalytic bundle self-assembled by the redox center.
8. Huang S.S., Gibney B.R., Stayrook S.E., Dutton P.L., Lewis M. X-ray structure of a Maquette scaffold. J. Mol. Biol. 326:2003;1219-1225 This X-ray structure of a four-helix apo-maquette clearly resolved the non-interdigitated packing interface between helices and thereby suggests how to make a mobile inter-subunit interface non-mobile.
9. 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-heme proteins. Nature. 368:1994;425-431.
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. 95:1998;10465-10470.
11. Kennedy M.L., Gibney B.R. Proton coupling to 4Fe-4S (2+/+) and 4Fe-4Se (2+/+) oxidation and reduction in a designed protein. J. Am. Chem. Soc. 124:2002;6826-6827.
12. Noy D, Moser CC, Dutton PL: Bacteriochlorophyll protein Maquettes. In Biochemistry and Biophysics of Chlorophylls. Edited by Grimm B, Porra W, Ruediger W, Scheer H: Kluwer, Dorderecht; 2003: in press.
13. Razeghifard A.R., Wydrzynski T. Binding of Zn-chlorin to a synthetic four-helix bundle peptide through histidine ligation. Biochemistry. 42:2003;1024-1030.
14. Magistrato A., DeGrado W.F., Laio A., Rothlisberger U., VandeVondele J., Klein M.L. Characterization of the dizinc analogue of the synthetic diiron protein DF1 using ab initio and hybrid quantum/classical molecular dynamics simulations. J. Phys. Chem. B. 107:2003;4182-4188.
15. Maglio O., Nastri F., Pavone V., Lombardi A., DeGrado W.F. Preorganization of molecular binding sites in designed diiron proteins. Proc. Natl. Acad. Sci. USA. 100:2003;3772-3777.
16. Summa C.M., Rosenblatt M.M., Hong J.K., Lear J.D., DeGrado W.F. Computational de novo design, and characterization of an A(2)B(2) diiron protein. J. Mol. Biol. 321:2002;923-938.
17. 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. 39:2000;11041-11049.
18. 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. 37:1998;16815-16827.
19. 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-alpha-helix bundle. Biochemistry. 40:2001;5474-5487.
20. Chen X., Discher B.M., Pilloud D.L., Gibney B.R., Moser C.C., Dutton P.L. De novo design of a cytochrome b maquette for electron transfer and coupled reactions on electrodes. J. Phys. Chem. B. 106:2002;617-624.
21. Moffet D.A., Hecht M.H. De novo proteins from combinatorial libraries. Chem. Rev. 101:2001;3191-3203.
22. Rau H.K., DeJonge N., Haehnel W. Modular synthesis of de novo designed metalloproteins for light-induced electron transfer. Proc. Natl. Acad. Sci. USA. 95:1998;11526-11531.
23. Springs S.L., Bass S.E., Bowman G., Nodelman I., Schutt C.E., McLendon G.L. A multigeneration analysis of Cytochrome b(562) redox variants: evolutionary strategies for modulating redox potential revealed using a library approach. Biochemistry. 41:2002;4321-4328.
24. Gibney B.R., Rabanal F., Skalicky J.J., Wand A.J., Dutton P.L. Iterative protein redesign. J. Am. Chem. Soc. 121:1999;4952-4960.
25. Gibney B.R., Johansson J.S., Rabanal F., Skalicky J.J., Wand A.J., Dutton P.L. Global topology & stability and local structure & dynamics in a synthetic spin-labeled four-helix bundle protein. Biochemistry. 36:1997;2798-2806.
26. Tronin A., Strzalka J., Chen X., Dutton P.L., Ocko B.M., Blaise J.K. Orientational distributions of the di-alpha-helical synthetic peptide ZnPPM-BBC16 in Langmuir monolayers by X-ray reflectivity and polarized epifluorescence. Langmuir. 17:2001;3061-3066.
27. Ye S.X., Strzalka J., Chen X., Moser C.C., Dutton P.L., Blasie J.K. Assembly of a vectorially oriented four-helix bundle at the air/wAter interface via directed electrostatic interactions. Langmuir. 19:2003;1515-1521.
28. White S.H., Wimley W.C. Hydrophobic interactions of peptides with membrane interfaces. Biochim. Biophys. Acta. 1376:1998;339-352.
29. White S.H., Wimley W.C. Membrane protein folding and stability: Physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:1999;319-365.
30. Davis J.H., Clare D.M., Hodges R.S., Bloom M. Interaction of a synthetic amphiphilic polypeptide and lipids in a bilayer structure. Biochemistry. 22:1983;5298-5305.
31. Killian J.A. Hydrophobic mismatch between proteins and lipids in membranes. Biochim. Biophys. Acta. 1376:1998;401-416.
32. de Planque M.R.R., Boots J.W.P., Rijkers D.T.S., Liskamp R.M.J., Greathouse D.V., Killian J.A. The effects of hydrophobic mismatch between phosphatidylcholine bilayers and transmembrane alpha-helical peptides depend on the nature of interfacially exposed aromatic and charged residues. Biochemistry. 41:2002;8396-8404.
33. de Planque M.R.R., Bonev B.B., Demmers J.A.A., Greathouse D.V., Koeppe R.E., Separovic F., Watts A., Killian J.A. Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions. Biochemistry. 42:2003;5341-5348.
34. Strandberg E., Morein S., Rijkers D.T.S., Liskamp R.M.J., van der Wel P.C.A., Killian J.A. Lipid dependence of membrane anchoring properties and snorkeling behavior of aromatic and charged residues in transmembrane peptides. Biochemistry. 41:2002;7190-7198.
35. Strandberg E., Killian J.A. Snorkeling of lysine side chains in transmembrane helices: how easy can it get? FEBS Lett. 544:2003;69-73 First estimate for the free energy cost of snorkeling calculated from the effects of WALP and KALP model peptides on lipid phase transition and phase separation. In contrast to partitioning of charged residue in hydrophobic interior of membranes, the energy barrier for snorkeling is much lower.
36. Keske JM, Bruce JM, Dutton PL: The role of aqueous solvation in protein folding: Insights from aqueous-alkane partitioning. In Techniques in Protein Chemistry III. Edited by Angeletti R. New York: Academic Press; 1992:355-362.
37. Wimley W.C., White S.H. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3:1996;842-848.
38. Jayasinghe S., Hristova K., White S.H. Energetics, stability, and prediction of transmembrane helices. J. Mol. Biol. 312:2001;927-934.
39. Wimley W.C., White S.H. Designing transmembrane alpha-helices that insert spontaneously. Biochemistry. 39:2000;4432-4442.
40. Noy D., Calhoun J.R., Lear J.D. Direct analysis of protein sedimentation equilibrium in detergent solutions without density matching. Anal. Biochem. 320:2003;185-192.
41. Russ W.P., Engelman D.M. TOXCAT: A measure of transmembrane helix association in a biological membrane. Proc. Natl. Acad. Sci. USA. 96:1999;863-868.
42. Schneider D., Engelman D.M. GALLEX, a measurement of heterologous association of transmembrane helices in a biological membrane. J. Biol. Chem. 278:2003;3105-3111 The clever TOXCAT assay for homodimeric helix-helix association in membranes is extended to evaluate heterodimer interactions. Assaying multiple TM helix association still remains a great challenge.
43. Choma C., Gratkowski H., Lear J.D., DeGrado W.F. Asparagine-mediated self-association of a model transmembrane helix. Nat. Struct. Biol. 7:2000;161-166.
44. Zhou F.X., Cocco M.J., Russ W.P., Brunger A.T., Engelman D.M. Interhelical hydrogen bonding drives strong interactions in membrane proteins. Nat. Struct. Biol. 7:2000;154-160.
45. Bowie J.U. Understanding membrane protein structure by design. Nat. Struct. Biol. 7:2000;91-94.
46. Lear J.D., Gratkowski H., Adamian L., Liang J., DeGrado W.F. Position-dependence of stabilizing polar interactions of asparagine in transmembrane helical bundles. Biochemistry. 42:2003;6400-6407 Combined analysis of crystal structures of helical membrane proteins with measurements of free energies of trimerization of model TM helices reveals a new principle for membrane protein engineering: control of the degree of stabilization by positioning Asn residues along the helix.
47. Membrane Proteins of Known 3D Structure from the Stephen White Laboratory at UC Irvine on World Wide Web URL: http://blanco.biomol.uci.edu/ Membrane_Proteins_xtal.html .
48. Dutzler R., Campbell E.B., Cadene M., Chait B.T., MacKinnon R. X-ray structure of a CIC chloride channel at 3.0 angstrom reveals the molecular basis of anion selectivity. Nature. 415:2002;287-294.
49. Bass R.B., Strop P., Barclay M., Rees D.C. Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science. 298:2002;1582-1587.
50. Nishimura K., Kim S.G., Zhang L., Cross T.A. The closed state of a H+ channel helical bundle combining precise orientational and distance restraints from solid state NMR-1. Biochemistry. 41:2002;13170-13177 Elegant solution to solving the structure of a channel in its natural environment: highly oriented hydrated lipid bilayers. The result provides an important inspiration for the de novo design and proton translocation fields.
51. Jiang Y.X., Lee A., Chen J.Y., Ruta V., Cadene M., Chait B.T., MacKinnon R. X-ray structure of a voltage-dependent K+ channel. Nature. 423:2003;33-41.
52. Jiang Y.X., Lee A., Chen J.Y., Cadene M., Chait B.T., MacKinnon R. Crystal structure and mechanism of a calcium-gated potassium channel. Nature. 417:2002;515-522 One of this group's astonishing series of X-ray channel structures. This one demonstrates the modular nature of construction and proposes a mechanism for pore opening.
53. Doyle D.A., Cabral J.M., Pfuetzner R.A., Kuo A.L., Gulbis J.M., Cohen S.L., Chait B.T., MacKinnon R. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science. 280:1998;69-77.
54. Jiang Y.X., Lee A., Chen J.Y., Cadene M., Chait B.T., MacKinnon R. The open pore conformation of potassium channels. Nature. 417:2002;523-526.
55. Khosla C., Harbury P.B. Modular enzymes. Nature. 409:2001;247-252.
56. Lear J.D., Wasserman Z.R., DeGrado W.F. Synthetic amphiphilic peptide models for protein ion channels. Science. 240:1988;1177-1181.
57. Montal M. Molecular mimicry in channel-protein structure. Curr. Opin. Struct. Biol. 5:1995;501-506.
58. Montal M. Design of molecular function - channels of communication. Annu. Rev. Biophys. Biomol. Struct. 24:1995;31-57.
59. Humphrey W., Dalke A., Schulten K. VMD: visual molecular dynamics. J. Mol. Graph. 14:1996;33-38.
60. Iwata S., Lee J.W., Okada K., Lee J.K., Iwata M., Rasmussen B., Link T.A., Ramaswamy S., Jap B.K. Complete structure of the 11-subunit bovine mitochondrial cytochrome bc(1) complex. Science. 281:1998;64-71.