Engineering model proteins for Photosystem II function

Photosynthesis Research

Volumn 94, Issue 2-3, 2007, Pages 225-233

  Wydrzynski, Tom ^a   Hillier, Warwick ^a   Conlan, Brendon ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Biocatalyst; H2 production; Photosystem II; Protein engineering; Water splitting

Indexed keywords

HYDROGEN; OXYGEN; PROTEIN; WATER;

CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; METHODOLOGY; PHOTOSYSTEM II; PROTEIN ENGINEERING; REVIEW;

HYDROGEN; MODELS, MOLECULAR; OXYGEN; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN ENGINEERING; PROTEINS; WATER;

EID: 36849037465     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-007-9271-0     Document Type: Review

References (84)

1. Amunts A, Droy O, Nelson N (2007) The structure of plant Photosystem I supercomplex at 3.4 Å resolution. Nature 447:58-63
2. Arnsano F, Banci L, Bertini I, Faraone-Mennella J, Rosato A, Barker PD, Fersht AR (1999) The solution structure of oxidized Escherichia coli cytochrome b 562. Biochemistry 38:8657-8670
3. Barker PD, Nerou EP, Cheesman MR, Thomson AJ, de Oliveira P, Hill HA (1996) Bis-methionine ligation to heme iron in mutants of cytochrome b562 1: spectroscopic and electrochemical characterization of the electronic properties. Biochemistry 35:13618-13626
4. Calvin M, Benson AA (1948) Path of carbon in photosynthesis. Science 107:476-480
5. Cheeseman MR, Thomson AJ, Greenwood C, Moore GR, Kadir F (1990) Bis-methionine axial ligation of haem in bacterioferritin from Pseudomononas aeruglinosa. Nat Lett 346:771-773
6. Chen M, Eggink LL, Hoober JK, Larkum AWD (2005) Influence of structure on binding chlorophylls to peptide ligands. J Am Chem Soc 127:2052-2053
7. Chen-Barrett Y, Harrison PM, Treffry A, Quail MA, Arosio P, Sabtanbriui P, Chasteen ND (1995) Tyrosyl radical formation during the oxidative deposition of iron in human apoferritin. Biochemistry 34:7847-7853
8. Conlan BHW, Wydrzynski T (2007) Designing artificial photosynthesis: production of a light-activated metallo protein. In: Allen JF, Osmod B, Golbeck JH, Gantt E (eds) Proceedings of the 14th congress on Photosynthesis. Springer (in press)
9. Dautant A, Meyer J-B, YarivJ, Precigoux G, Sweet RM, Kalb AJ, Frolow F (1998) Structure of a monoclonic crystal form of cytochrome b1 (bacterioferritin from E. coli). Acta Cryst D54:1-24
10. DeGrado WF, Summa CM, Pavone V, Nastri F, Lombardi A. (1999) De novo design and structural characterization of proteins and metalloproteins. Annu Rev Biochem 68:779-819
11. Deisenhofer J, Epp O, Sinning I, Michel H (1995) Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction center from Rhodopseudomonas viridis. J Mol Biol 246:429-457
12. D. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Advances in photosynthesis and respiration, vol 22. Springer, Dordrecht, pp 753-775
13. Discher BM, Koder RL, Moser CC, Dutton PL (2003) Hydrophilic to amphiphilic design in redox protein maquettes. Curr Opin Chem Biol 7:741-748
14. Discher BM, Noy D, Strzalka J, Shixin Y, Moser CC, Lear JD, Blaise JK, Dutton PL (2005) Design of amphiphilic protein maquettes: controlling assembly, membrane insertion and cofactor interactions. Biochemistry 44:12329-12343
15. Eggink LL, Hoober JK (2000) Chlorophyll binding to peptide maquettes containing a retention motif. J Biol Chem 275:9087-9090
16. Ferreira KN, Iverson T, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831-1838
17. Frolow F, Kalb (Gilboa) AJ, Yariv J (1994) Structure of a unique twofold symmetric haem binding site. Nat Struct Biol 1:453-460
18. Gaffron H, Fager EW, Rosenberg JL (1951) Intermediates in photosynthesis: formation and transformation of phosphoglyceric acid. Exp Plant Physiol 2:87-114
19. Gibney BR, Dutton PL (2001) De novo design and synthesis of heme proteins. Adv Inorg Chem 51:409-455
20. Gibney BR, Mulholland SE, Rabanal F, Dutton PL (1996) Ferridoxin and ferredoxin-heme maquettes. Proc Natl Acad Sci USA 93:15041-15046
21. Gibney BR, Rabanal F, Skalicky JJ, Wand AJ, Dutton LP (1999) Iterative protein design. J Am Chem Soc 121:4952-4960
22. Hamada K, Bethge PH, Mathews FS (1995) Refined structure of cytochrome b562 from Escherichia coli. J Mol Biol 247:947-962
23. Hay S, Wydrzynski T (2005) Conversion of the Escherichia coli cytochrome b562 to an archtype cytochrome b: a mutant with bis-histidine ligation of heme iron. Biochemistry 44:431-439
24. Hay S, Wallace BB, Smith TA, Ghiggino KP, Wydrzynski T (2004) Protein engineering of cytochrome b562 for quinone binding and light-induced electron transfer. Proc Natl Acad Sci USA 101:17675-17680
25. A. Biochemistry 44:11891-118902
26. Hay S, Westerlund K, Tommos C (2007) Redox characteristics of a de novo quinone protein. J Phys Chem 111:3488-3495
27. Hughes JL, Razeghifard R, Logue M Oakley A, Wydezynski T, Krausz E (2006) Magneto-optic spectroscopy of a protein tetramer binding two exciton-coupled chlorophylls. J Am Chem Soc 128:3649-3658
28. Ingenhousz J (1798) Über die Nahrung der Pflanzen und die Düngung des Bodens. Voigt, Magazin, I (Hft.2):97-105
29. Johnson ET, Parson WW (2002) Electrostatic interactions in an integral membrane protein. Biochemistry 41:6483-6494
30. Jordon P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909-917
31. Kalman L, LoBrutto R, Allen JC, Williams JP (1999) Modified reaction centers oxidize tyrosine in reactions that mirror photosystem II. Nature 402:696-699
32. Kalman L, Williams JC, JP Allen (2005) Mimicking the properties of photosystem II in bacterial reaction centers. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Advances in photosynthesis and respiration, vol 22. Springer, Dordrecht, pp 715-727
33. Kalman L, LoBrutto R, Williams JC, Allen JP (2006) Iron as a bound secondary electron donor in modified bacterial reaction centers. Biochemistry 45:13869-13874
34. Kessler E, Arthur W, Brugger JE (1957) Influence of manganese on delayed light emission, fluorescence, photochemistry, and photosynthesis in algae. Arch Biochem Biophys 71:326-335
35. Koder RL, Dutton PL (2006) Intelligent design: the de novo engineering of proteins with specified functions. Dalton Trans 3045-3051
36. Kruse O, Rupprecht J, Mussgnug JH, Dismukes GC, Hankamer B (2005) Photosynthesis: a blueprint for solar energy capture and biohydrogen production technologies. Photochem Photobiol Sci 4:957-969
37. Kurisu G, Zhang H, Smith JL, Cramer WA (2003) The structure of a plant Photosystem I super-complex at 3.4 Å resolution. Science 302:1009-1014
38. Laplaza CE, Holm RH (2001) Helix-loop-helix peptides as scaffolds for the construction of bridged metal assemblies in proteins: the spectroscopic A-cluster structure in carbon monoxide dehydrogenase. J Am Chem Soc 123:10255-10264
39. Le Brun NE, Andrews SC, Guest JR, Harrison OM, Moore GR, Thomson AJ (1995) Identification of the ferroxidase centre of E. coli bacterioferritin. Biochem J 312:385-392
40. Lewis NS, Nocera DG (2006) Powering the planet: chemical challenges in solar energy utilization. Proc Natl Acad Sci USA 103:15729-15735
41. Li W-W, Heinze J, Haehnel W (2005) Site-specific binding of quinones to proteins through thiol addition-elimination reactions. J Am Chem Soc 127:6140-6141
42. Lin X, Murchison HA, Nagarajan V, Parson WW, Allen JP, Williams JC (1994) Specific alteration of the oxidation potential of the electron donor in reaction centers from Rhodobacter sphaeroides. Proc Natl Acad Sci USA 91:10265-10269
43. Liu Z, Yan H, Wang J, Kuang T, Zhang J, Gul L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428:287-292
44. Loll A, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040-1044
45. Lubitz W (1991) EPR and ENDOR studies of chlorophyll cation and anion radicals. In: Scheer H (ed) Chlorophyll. CRC Press, Inc., Boca Raton, pp 903-944
46. Lubitz W, Lendzian F, Bittl R (2002) Radicals, radical pairs and triplet states in photosynthesis. Acc Chem Res 35:313-320
47. Maglio O, Nastri F, Calhoun JR, Lahr H Wade H, Pavone V, DeGrado WF (2005) Artificial di-iron proteins: solution characterization of four helix bundles containing two distinct types of inter-helical loops. J Biol Inorg Chem 10:539-549
48. Magnuson A, Styring S (2005) Understanding photosystem II function by artificial photosynthesis. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Advances in photosynthesis and respiration, vol 22. Springer, Dordrecht, pp 753-775
49. McLuskey K, Prince SM, Cogdell RJ, Isaacs NM (2001) The crystallographic structure of the B800-820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila strain. Biochemistry 40:8783-8789
50. Meadows KA, Parkes-Loach PS, Kehoe JW, Loach PA (1998) Reconstitution of core light-harvesting complexes of photosynthetic bacteria using chemically synthesized polypeptides: minimal requirements for subunit formation. Biochemistry 37:3411-3417
51. Mennenga A, Gärtner W, Lubitz W, Görner H (2006) Effects of non-covalently bound quinones on the ground and triplet states of zinc-chlorins in solution and bound to de novo synthesized peptides. Phys Chem Chem Phys 8:5444-5453
52. Moffet DA, Hecht (2001) De novo proteins from combinatorial libraries. Chem Rev 101:3191-3203
53. Moore GR, Williams RJP, Peterson J, Thomson AJ, Mathews FS (1985) A spectroscopic investigation of the structure and redox properties of Escherichia coli cytochrome b652. Biochim Biophys Acta 829:83-96
54. Moore TA, Moore AL, Gust D (2002) The design and synthesis of artificial photosynthetic antennas, reaction centers and membranes. Phil Trans Roy Soc London 257:1481-1498
55. Narvatz AJ, Kalman L, LoBrutto R, Allen JP, Williams JC (2002) Influence of the protein environment on the properties of a tyrosyl radical in reaction centers from Rhodobacter sphaeriodes. Biochemistry 41:15253-15258
56. Noy D, Dutton PL (2006) Design of a minimal polypeptide unit for bacteriochlorophyll binding and self-assembly based on photosynthetic bacterial light-harvesting proteins. Biochemistry 45:2103-2113
57. Noy D, Discher BM, Rubtsov IV, Hochstrasser RM, Dutton PL (2005) Design of amphiphilic protein maquettes: enhancing maquette functionality through binding of extremely hydrophobic cofactors to lipophilic domains. Biochemistry 44:12344-12354
58. Page CC, Moser CC, Chen X, Dutton PL (1999) Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402:47-52
59. Priestley J (1772) Observations on different kinds of air. Phil Trans Roy Soc London 62:147-264
60. Rabanal F, Gibney BR, DeGrado WF, Moser CC, Dutton Pl (1996) Engineering photosynthesis: synthetic redox proteins. Inorg Chem Acta 243:213-218
61. Rabinowitch EI (1945) Photosynthesis and related topics, vol I. Wiley (Interscience), New York, pp 281-299
62. Rabinowitch EI (1951) Photosynthesis and related topics, vol II, part 1. Wiley (Interscience), New York
63. Rabinowitch EI (1956) Photosynthesis and related topics, vol II, part 2. Wiley (Interscience), New York
64. Rau HK, Snigula H, Struck A, Robert B, Scheer H, Haehnel W (2001) Design, synthesis and properties of synthetic chlorophyll proteins. Eur J Biochem 268:3284-3295
65. Rautter J, Lendzian F, Schulz C, Fetsch A, Kuhn M, Lin X, Williams JC, Allen JP, Lubitz W (1995) ENDOR-Studies of the primary donor cation radical in mutant reaction centers of Rhodobacter sphaeroides with altered hydrogen-bond interactions. Biochemistry 34:8130-8143
66. Razeghifard R, Wydrzynski (2003) Binding of Zn-chlorin to a synthetic four-helix bundle peptide through histidine ligation. Biochemistry 42:1024-1030
67. Razeghifard R, Wallace BD, Pace RJ, Wydrzynski T (2007) Creating functional artificial proteins. Curr Protein Pept Sci 8:3-18
68. Robinson Cr, Liu Y, Thomson AJ, Sturtevant JM, Sliger SG (1997) Eneregetics of heme binding to native and denatured cytochrome b562. Biochemstry 36:16141-16146
69. 18O) as a tracer in the study of photosynthesis. J Am Chem Soc 63:877-878
70. Satoh H, Nakayama K, Okada M (1998) Molecular cloning and functional expression of a water-soluble chlorophyll protein, a putative carrier of chlorophyll molecules in cauliflower. J Biol Chem 273:30568-30575
71. Schneider G, Lindqvist Y, Brändén C-I, Lorimer G (1986) Three-dimensional structure of ribulose-1,5-bisphosphate carboxylase/oxygenase from Rhodospirillum rubrum at 2.9 Å resolution. EMBO J 5:3409-3415
72. Senebier J (1782) Mémoires physicochimiques sur la l'influence de la lumiere solaire pour modifier les étres de trios régbes, surtout ceux dy régne végérl. 3 vols. Chirol, Geneva
73. Sharp RE, Moser CC, Rabanal F, Dutton PL (1998) Design, synthesis and characterization of photoactivable flavocytochrome molecular maquette. Proc Natl Acad Sci USA 95:10465-10470
74. Shifman JJ, Gibney BR, Sharp RE, Dutton PL (2000) Heme redox potential control in de novo designed four-α-helix bundle proteins. Biochemistry 39:14813-14821
75. Smith JMA, Smith Quirk AV, Plank RWH, Diffin FM, Ford GC, Harrison PM (1988) The identity of E. coli bacterioferritin and cytochrome b1. Biochem J 255:757-740
76. Springs SL, Bass SE, Bowman G, Nodelman I, Schutt CE, McLenden GL (2002) A multigeneration analysis of cytochrome b562 redox variants: evolutionary strategies for modulating redox potential revealed using a library approach. Biochemistry 41:4321-4328
77. Taylor TC, Backlund A, Bjorhall K, Spreitzer RJ, Andersson I (2001) First crystal structure of Rubisco from the green alga, Chlamydomonas reinhardtii. J Biol Chem 276:48159-48164
78. Thielges M, Uyeda G, Canaarap-Artigas A, Kalman L, Williams JC, Allen JP (2005) Design of a redox-linked active metal site: manganese bound to bacterial reaction centers at a site resembling that of Photosystem II. Biochemistry 44:7389-7394
79. Tronud DE, Schmid MF, Mathews BW (1986) Structure and amino acid sequence of a bacteriochlorophyll protein from Prosthecochloris aestuarii at 1.9 Å. J Mol Biol 188:443-454
80. Wade H, Stayrook SE, DeGrado WF (2006) The structure of a designed di-iron (III) protein: implications for cofactor stabilization and catalysis. Angew Chem Int Ed 45:4951-4954
81. Westerlund K, Berry BW, Privet HK, Tommos C (2005) Exploring amino-acid radical chemistry: protein engineering and de novo design. Biochim Biophys Acta 1707:103-116
82. Whittaker JW, Whittaker MM (2003) Outer sphere mutagenesis of Lactobacillus plantarum manganese catalase disrupts the cluster core. Eur J Biochem 270:1102-1116
83. Williams JC, Haffa ALM, McCulley JL, Woodbury NW, Allen JP (2001) Electrostatic interactions between charged amino acid residues and the bacteriochlorophyll dimer in reaction centers from Rhodobacter sphaeroides. Biochemistry 40:15403-15407
84. Wydrzynski T, Satoh K (eds) (2005) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Advances in photosynthesis and respiration, vol 22. Springer, Dordrecht