Short Hydrogen bond between redox-active tyrosine Y Z and D1-His190 in the photosystem II crystal structure

Biochemistry

Volumn 50, Issue 45, 2011, Pages 9836-9844

  Saito, Keisuke ^a   Shen, Jian Ren ^b   Ishida, Toyokazu ^c   Ishikita, Hiroshi ^a,d  

^a KYOTO UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DONOR-ACCEPTOR DISTANCE; NEUTRAL STATE; OXIDIZED STATE; OXYGEN-EVOLVING COMPLEXES; PHOTOSYSTEM II; QUANTUM MECHANICAL/MOLECULAR MECHANICAL CALCULATIONS; REDOX-ACTIVE TYROSINES; WATER MOLECULE;

AMINO ACIDS; HYDROGEN; HYDROGEN BONDS; MOLECULAR MODELING; MOLECULES;

CRYSTAL STRUCTURE;

CALCIUM ION; TYROSINE;

ARTICLE; CRYSTAL STRUCTURE; HYDROGEN BOND; MOLECULAR MECHANICS; PHOTOOXIDATION; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTON TRANSPORT; QUANTUM MECHANICS;

BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; CYANOBACTERIA; HYDROGEN BONDING; MODELS, MOLECULAR; OXIDATION-REDUCTION; PHOTOSYSTEM II PROTEIN COMPLEX; PROTONS; THERMODYNAMICS; TYROSINE; WATER;

EID: 80755122862     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201366j     Document Type: Article

References (38)

1. Prokhorenko, V. I. and Holzwarth, A. R. (2000) Primary process and structure of the photosystem II reaction center: A photon echo study J. Phys. Chem. B 104, 11563-11578
2. Ishikita, H., Biesiadka, J., Loll, B., Saenger, W., and Knapp, E. W. (2006) Cationic state of accessory chlorophyll and electron transfer through pheophytin to plastoquinone in photosystem II Angew. Chem., Int. Ed. 45, 1964-1965 (Pubitemid 44105229)
3. Renger, G. and Renger, T. (2008) Photosystem II: The machinery of photosynthetic water splitting Photosynth. Res. 98, 53-80 (Pubitemid 50289510)
4. Noguchi, T., Inoue, Y., and Tang, X.-S. (1997) Structural coupling between the oxygen-evolving Mn cluster and a tyrosine residue in photosystem II as revealed by Fourier transform infrared spectroscopy Biochemistry 36, 14705-14711 (Pubitemid 27524391)
5. Berthomieu, C., Hienerwadel, R., Boussac, A., Breton, J., and Diner, B. A. (1998) Hydrogen bonding of redox-active tyrosine Z of photosystem II probed by FTIR difference spectroscopy Biochemistry 37, 10547-10554 (Pubitemid 28357854)
6. Rappaport, F., Boussac, A., Force, D. A., Peloquin, J., Brynda, M., Sugiura, M., Un, S., Britt, R. D., and Diner, B. A. (2009) Probing the coupling between proton and electron transfer in photosystem II core complexes containing a 3-fluorotyrosine J. Am. Chem. Soc. 131, 4425-4433
7. Rappaport, F. and Lavergne, J. (2001) Coupling of electron and proton transfer in the photosynthetic water oxidase Biochim. Biophys. Acta 1503, 246-259
8. Z in photosystem II from multiple-electron magnetic-resonance spectroscopies: Implications for photosynthetic oxygen evolution J. Am. Chem. Soc. 117, 10325-10335
9. Z in manganese-depleted photosystem II Biochemistry 38, 11851-11865 (Pubitemid 29450809)
10. Rutherford, A. W. and Boussac, A. (2004) Water photolysis in biology Science 303, 1782-1784 (Pubitemid 38374857)
11. 2 formation tracked by time-resolved X-ray experiments Science 310, 1019-1021 (Pubitemid 41611914)
12. Umena, Y., Kawakami, K., Shen, J.-R., and Kamiya, N. (2011) Crystal structure of oxygen-evolving photosystem II at 1.9 Å resolution Nature 473, 55-60
13. Kawakami, K., Umena, Y., Kamiya, N., and Shen, J.-R. (2011) Structure of the catalytic, inorganic core of oxygen-evolving photosystem II at 1.9 Å resolution J. Photochem. Photobiol., B 104, 9-18
14. Loll, B., Kern, J., Saenger, W., Zouni, A., and Biesiadka, J. (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II Nature 438, 1040-1044 (Pubitemid 43093979)
15. Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A., and Saenger, W. (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride Nat. Struct. Mol. Biol. 16, 334-342
16. Faller, P., Goussias, C., Rutherford, A. W., and Un, S. (2003) Resolving intermediates in biological proton-coupled electron transfer: A tyrosyl radical pair to proton movement Proc. Natl. Acad. Sci. U.S.A. 100, 8732-8735 (Pubitemid 36899167)
17. Yan, S., Kang, S., Hayashi, T., Mukamel, S., and Lee, J. Y. (2009) Computational studies on electron and proton transfer in phenol-imidazole-base triads J. Comput. Chem. 31, 393-402
18. Z* state of photosystem II from Thermosynechococcus elongatus Biochemistry 46, 3138-3150 (Pubitemid 46449136)
19. Saito, K., Ishida, T., Sugiura, M., Kawakami, K., Umena, Y., Kamiya, N., Shen, J.-R., and Ishikita, H. (2011) Distribution of the cationic state over the chlorophyll pair of photosystem II reaction center J. Am. Chem. Soc. 133, 14379-14388
20. Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., Swaminathan, S., and Karplus, M. (1983) CHARMM: A program for macromolecular energy minimization and dynamics calculations J. Comput. Chem. 4, 187-217
21. MacKerell, A. D., Jr. , Bashford, D., Bellott, R. L., Dunbrack, R. L., Jr. , Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., III, Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiorkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102, 3586-3616 (Pubitemid 128576688)
22. Bayly, C. I., Cieplak, P., Cornell, W. D., and Kollman, P. A. (1993) A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model J. Phys. Chem. 97, 10269-10280
23. Jaguar, version 7.5 (2008) Schrödinger, LLC, New York.
24. 2-evolving complex of photosystem II Biochemistry 50, 6308-6311
25. QSite, version 5.6 (2010) Schrödinger, LLC, New York.
26. Haumann, M. and Junge, W. (1999) Photosynthetic water oxidation: A simplex-scheme of its partial reactions Biochim. Biophys. Acta 1411, 86-91 (Pubitemid 29182798)
27. Haumann, M., Mulkidjanian, A., and Junge, W. (1999) Tyrosine-Z in oxygen-evolving photosystem II: A hydrogen-bonded tyrosinate Biochemistry 38, 1258-1267
28. Perrin, C. L. and Nielson, J. B. (1997) "Strong" hydrogen bonds in chemistry and biology Annu. Rev. Phys. Chem. 48, 511-544 (Pubitemid 127443917)
29. Z in photosystem II Biochemistry 39, 6275-6287 (Pubitemid 30347131)
30. Ahlbrink, R., Haumann, M., Cherepanov, D., Bogershausen, O., Mulkidjanian, A., and Junge, W. (1998) Function of tyrosine Z in water oxidation by photosystem II: Electrostatical promotor instead of hydrogen abstractor Biochemistry 37, 1131-1142 (Pubitemid 28100616)
31. Petrouleas, V., Koulougliotis, D., and Ioannidis, N. (2005) Trapping of metalloradical intermediates of the S-states at liquid helium temperatures. Overview of the phenomenology and mechanistic implications Biochemistry 44, 6723-6728 (Pubitemid 40632391)
32. Cleland, W. W. and Kreevoy, M. M. (1994) Low-barrier hydrogen bonds and enzymic catalysis Science 264, 1887-1890 (Pubitemid 24245628)
33. Frey, P. A., Whitt, S. A., and Tobin, J. B. (1994) A low-barrier hydrogen bond in the catalytic triad of serine proteases Science 264, 1927-30 (Pubitemid 24245638)
34. Warshel, A., Papazyan, A., and Kollman, P. A. (1995) On low-barrier hydrogen bonds and enzyme catalysis Science 269, 102-106
35. Ishida, T. and Kato, S. (2003) Theoretical perspectives on the reaction mechanism of serine proteases: The reaction free energy profiles of the acylation process J. Am. Chem. Soc. 125, 12035-12048 (Pubitemid 37175434)
36. Schutz, C. N. and Warshel, A. (2004) The low barrier hydrogen bond (LBHB) proposal revisited: The case of the Asp..His pair in serine proteases Proteins 55, 711-723 (Pubitemid 38620094)
37. Fuhrmann, C. N., Daugherty, M. D., and Agard, D. A. (2006) Subangstrom crystallography reveals that short ionic hydrogen bonds, and not a His-Asp low-barrier hydrogen bond, stabilize the transition state in serine protease catalysis J. Am. Chem. Soc. 128, 9086-9102 (Pubitemid 44078992)
38. Ishida, T. (2006) Low-barrier hydrogen bond hypothesis in the catalytic triad residue of serine proteases: Correlation between structural rearrangement and chemical shifts in the acylation process Biochemistry 45, 5413-5420 (Pubitemid 43673172)