Probing the Accessibility of the Mn4Ca Cluster in Photosystem II: Channels Calculation, Noble Gas Derivatization, and Cocrystallization with DMSO

Structure

Volumn 17, Issue 9, 2009, Pages 1223-1234

  Gabdulkhakov, Azat ^a   Guskov, Albert ^a   Broser, Matthias ^b   Kern, Jan ^b,c   Müh, Frank ^a,b   Saenger, Wolfram ^a   Zouni, Athina ^b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

PROTEINS

Indexed keywords

CALCIUM DERIVATIVE; DIMETHYL SULFOXIDE; INERT GAS; KRYPTON; LIPID; LYSINE; MANGANESE DERIVATIVE; OXYGEN; PROTON;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; CYANOBACTERIUM; DERIVATIZATION; ELECTRON; HYDROPHOBICITY; MEMBRANE STRUCTURE; NONHUMAN; OXIDATION; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTON TRANSPORT; STRUCTURE ANALYSIS; THERMOSYNECHOCOCUS ELONGATUS;

CRYSTALLIZATION; DIMETHYL SULFOXIDE; MANGANESE; MODELS, MOLECULAR; MOLECULAR PROBES; NOBLE GASES; OXYGEN; PHOTOSYSTEM II PROTEIN COMPLEX;

THERMOSYNECHOCOCCUS ELONGATUS;

EID: 69849088750     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2009.07.010     Document Type: Article

References (51)

1. Ahrling K.A., Evans M.C., Nugent J.H., Ball R.J., and Pace R.J. ESEEM studies of substrate water and small alcohol binding to the oxygen-evolving complex of photosystem II during functional turnover. Biochemistry 45 (2006) 7069-7082
2. Anderson J.M. Does functional photosystem II complex have an oxygen channel?. FEBS Lett. 488 (2001) 1-4
3. Barber J., Ferreira K.N., Maghlaoui K., and Iwata S. Structural model of the oxygen-evolving centre of photosystem II with mechanistic implications. Phys. Chem. Chem. Phys. 6 (2004) 4737-4742
4. Boussac A., Kuhl H., Ghibaudi E., Rögner M., and Rutherford A.W. Detection of an electron paramagnetic resonance signal in the S0 state of the manganese complex of photosystem II from Synechococcus elongatus. Biochemistry 38 (1999) 11942-11948
5. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D. Biol. Crystallogr. 54 (1998) 905-921
6. Brunori M., Cutruzzola F., Savino C., Travaglini-Allocatelli C., Vallone B., and Gibson Q.H. Structural dynamics of ligand diffusion in the protein matrix: A study on a new myoglobin mutant Y(B10) Q(E7) R(E10). Biophys. J. 76 (1999) 1259-1269
7. Brzezinski P., and Adelroth P. Design principles of proton-pumping haem-copper oxidases. Curr. Opin. Struct. Biol. 16 (2006) 465-472
8. Chu H.A., Nguyen A.P., and Debus R.J. Amino acid residues that influence the binding of manganese or calcium to photosystem II. 1. The lumenal interhelical domains of the D1 polypeptide. Biochemistry 34 (1995) 5839-5858
9. Clausen J., and Junge W. Detection of an intermediate of photosynthetic water oxidation. Nature 430 (2004) 480-483
10. Clausen J., and Junge W. The inhibitory effects of acidification and augmented oxygen pressure on water oxidation. Photosynth. Res. 98 (2008) 229-233
11. Clausen J., Junge W., Dau H., and Haumann M. Photosynthetic water oxidation at high O-2 backpressure monitored by delayed chlorophyll fluorescence. Biochemistry 44 (2005) 12775-12779
12. Cohen J., Arkhipov A., Braun R., and Schulten K. Imaging the migration pathways for O2, CO, NO, and Xe inside myoglobin. Biophys. J. 91 (2006) 1844-1857
13. Cukierman S. Et tu, Grotthuss! and other unfinished stories. Biochim. Biophys. Acta 1757 (2006) 876-885
14. De Las Rivas J., and Barber J. Analysis of the structure of the PsbO protein and its implications. Photosynth. Res. 81 (2004) 329-343
15. DeLano W.L. The PyMOL Molecular Graphics System (2008), DeLano Scientific LLC, Palo Alto, CA, USA
16. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
17. Ferreira K.N., Iverson T.M., Maghlaoui K., Barber J., and Iwata S. Architecture of the photosynthetic oxygen-evolving center. Science 303 (2004) 1831-1838
18. Force D.A., Randall D.W., Lorigan G.A., Clemens K.L., and Britt R.D. ESEEM studies of alcohol binding to the manganese cluster of the oxygen evolving complex of Photosystem II. J. Am. Chem. Soc. 120 (1998) 13321-13333
19. Frasch W.D., Mei R., and Sanders M. Oxidation of alcohols catalyzed by the oxygen-evolving complex. Biochemistry 27 (1988) 3715-3719
20. Guskov A., Kern J., Gabdulkhakov A., Broser M., Zouni A., and Saenger W. Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. 16 (2009) 334-342
21. Ho F.M. Uncovering channels in photosystem II by computer modelling: current progress, future prospects, and lessons from analogous systems. Photosynth. Res. 98 (2008) 503-522
22. 4 cluster in Photosystem II based on solvent accessibility simulations, with implications for substrate water access. Biochim. Biophys. Acta 1777 (2008) 140-153
23. Ishikita H., Saenger W., Loll B., Biesiadka J., and Knapp E.W. Energetics of a possible proton exit pathway for water oxidation in Photosystem II. Biochemistry 45 (2006) 2063-2071
24. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Cryst. 26 (1993) 795-800
25. Kern J., and Renger G. Photosystem II: Structure and mechanism of the water:plastoquinone oxidoreductase. Photosynth. Res. 94 (2007) 183-202
26. Kern J., Loll B., Lüneberg C., DiFiore D., Biesiadka J., Irrgang K.D., and Zouni A. Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor. Biochim. Biophys. Acta 1706 (2005) 147-157
27. Kok B., Forbush B., and McGloin M. Cooperation of charges in photosynthetic oxygen evolution: I. A linear four step mechanism. Photochem. Photobiol. 11 (1970) 457-475
28. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26 (1993) 283-291
29. Loll B., Kern J., Saenger W., Zouni A., and Biesiadka J. Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438 (2005) 1040-1044
30. Luna V.M., Chen Y., Fee J.A., and Stout C.D. Crystallographic studies of Xe and Kr binding within the large internal cavity of cytochrome ba3 from Thermus thermophilus: structural analysis and role of oxygen transport channels in the heme-Cu oxidases. Biochemistry 47 (2008) 4657-4665
31. Marsh D., Dzikovski B.G., and Livshits V.A. Oxygen profiles in membranes. Biophys. J. 90 (2006) L49-L51
32. Mueller-Dieckmann C., Polentarutti M., Djinovic Carugo K., Panjikar S., Tucker P.A., and Weiss M.S. On the routine use of soft X-rays in macromolecular crystallography. Part II. Data-collection wavelength and scaling models. Acta Crystallogr. D. Biol. Crystallogr. 60 (2004) 28-38
33. Murray J.W., and Barber J. Structural characteristics of channels and pathways in photosystem II including the identification of an oxygen channel. J. Struct. Biol. 159 (2007) 228-237
34. Murray J.W., Maghlaoui K., Kargul J., Sugiura M., and Barber J. Analysis of xenon binding to photosystem II by X-ray crystallography. Photosynth. Res. 98 (2008) 523-527
35. Norberg J., and Nilsson L. Solvent influence on base stacking. Biophys. J. 74 (1998) 394-402
36. Nöring B., Shevela D., Renger G., and Messinger J. Effects of methanol on the Si-state transitions in photosynthetic water-splitting. Photosynth. Res. 98 (2008) 251-260
37. Okumura A., Ohta H., Inoue Y., and Enami I. Identification of functional domains of the extrinsic 12 kDa protein in red algal PSII by limited proteolysis and directed mutagenesis. Plant Cell Physiol. 42 (2001) 1331-1337
38. Olesen K., and Andreasson L.E. The function of the chloride ion in photosynthetic oxygen evolution. Biochemistry 42 (2003) 2025-2035
39. Pacak P. Polarizability and molecular radius of dimethyl-sulfoxide and dimethylformamide from refractive index data. J. Solution Chem. 16 (1987) 71-77
40. Petrek M., Otyepka M., Banas P., Kosinova P., Koca J., and Damborsky J. CAVER: a new tool to explore routes from protein clefts, pockets and cavities. BMC Bioinformatics 7 (2006) 316
41. Prange T., Schiltz M., Pernot L., Colloc'h N., Longhi S., Bourguet W., and Fourme R. Exploring hydrophobic sites in proteins with xenon or krypton. Proteins 30 (1998) 61-73
42. Quillin M.L., Breyer W.A., Griswold I.J., and Matthews B.W. Size versus polarizability in protein-ligand interactions: binding of noble gases within engineered cavities in phage T4 lysozyme. J. Mol. Biol. 302 (2000) 955-977
43. In: Renger G. (Ed). Primary Processes of Photosynthesis - Principles and Apparatus (2008), RCS Publishing, Cambridge
44. Rutherford A.W., and Faller P. The heart of photosynthesis in glorious 3D. Trends Biochem. Sci. 26 (2001) 341-344
45. Subczynski W.K., and Wisniewska A. Physical properties of lipid bilayer membranes: relevance to membrane biological functions. Acta Biochim. Pol. 47 (2000) 613-625
46. Svensson-Ek M., Abramson J., Larsson G., Tornroth S., Brzezinski P., and Iwata S. The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J. Mol. Biol. 321 (2002) 329-339
47. Vaguine A.A., Richelle J., and Wodak S.J. SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model. Acta Crystallogr. D. Biol. Crystallogr. 55 (1999) 191-205
48. In: Wydrzynski T., and Satoh K. (Eds). Photosystem II: The light-driven Water:Plastoquinone oxidoreductase (2005), Springer, Dordrecht, The Netherlands
49. Yocum C.F. The calcium and chloride requirements of the O2 evolving complex. Coord. Chem. Rev. 252 (2008) 296-305
50. Zouni A., Witt H.T., Kern J., Fromme P., Krauss N., Saenger W., and Orth P. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409 (2001) 739-743
51. Zouni A., Kern J., Frank J., Hellweg T., Behlke J., Saenger W., and Irrgang K.D. Size determination of cyanobacterial and higher plant Photosystem II by gel permeation chromatography, light scattering, and ultracentrifugation. Biochemistry 44 (2005) 4572-4581