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Modeling Manganese Redox Enzymes

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Cytotoxic, Mutagenic and Carcinogenic Potential of Heavy Metals Related to Human Environment

Part of the book series: NATO ASI Series ((ASEN2,volume 26))

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Abstract

Manganese is an essential element in many biological processes. Two functional values can be distinguished; the MnII as a Lewis acid, like divalent ions, Magnesium, Calcium, Zinc and in higher oxidation states(MnIII, MnIV) as an oxidation catalyst, like Copper, Iron, Cobalt. Manganese redox enzymes1 with manganese in oxidation states 2+, 3+ and 4+ are: a manganese-containing ribonucleotide reductase 2, 3, 15 isolated from B. ammoniagemes; Mn ThiosulfateOxidase 4 containing a binuclear MnII site; Manganese SOD 5, 6 catalyzing the dismutasion of Superoxide radicals to oxygen and hydrogen peroxide with a single MnIII center; The Manganese Peroxidase(MnP) 7–10 is one of the two known enzymes capable for the oxidative degradation of lignin containing protoporphyrin IX heme prosthetic group; non heme manganese catalase 11–19 containing two manganese per subunit and the Oxygen Evolving Complex 20–40, catalyzing one of the most important reactions occurring in the plants, the light driven oxidation of water to oxygen and protons, containing four manganese atoms while the presence of calcium and chloride ions is required for proper functioning. In this report we will describe how modeling chemistry provides insight into the structure, chemical properties and reactivity of some manganese redox enzymes.

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References

  1. Pecoraro, V. L.(1992), Manganese Redox Enzymes, VCH Publishers Inc, New York.

    Google Scholar 

  2. Stube, J.(1990), Ribonucleotide Reductases: Amazing and Confusing, J. Biol. Chem. 265, 5329–5332.

    Google Scholar 

  3. Lynch, J.B., Juarez-Garcia C., Munck, E. and Que, L. Jr., (1989), Mössbauer and EPR Studies of the Binuclear Iron Center in Ribonucleotide Reductase from Escherichia coli. A new Manganese—containing enzyme, J. Biol. Chem. 264, 8091–8096.

    CAS  Google Scholar 

  4. Cammack, R., Chapman, A., Wei-Ping, Lu, Katagouni, A. and Kelly, D.P.(1989) Evidence that Protein-B of the Thiosulfate-Oxidizing System of Thiobacillus-Versutus Contains a Binuclear Manganese Cluster FEBS Letters 253, 239–243.

    Article  CAS  Google Scholar 

  5. Stallmgs, W.C., Partridge, K.A., Strong, R.K. and Ludwig, M.L.(1985), The Structure of Manganese Superoxide Dismutase from Thermus thermophilus HB8 at 2.4-Ă Resolution, J. Biol. Chem., 260, 16424–16432.

    Google Scholar 

  6. Ludwig, M.L., Metzger, A.L., Pattridge, K.A. and Stellings, W.C. (1991), Manganese Superoxide Dismutase from Thermus thermophilus. A structural model refined at 1.8Ă Resolution J. Mol. Biol. 219(2), 335–358.

    Article  CAS  Google Scholar 

  7. Wariishi, H., Valli, K. and Gold, M.H. (1989), Oxidative Cleavage of a Phenolic Diarylpropane Lignin Model Dimer by Manganese Peroxidase from Phanerochiate chrysporium, Biochemistry, 28, 6017–6023.

    Article  CAS  Google Scholar 

  8. Wariishi, H. and Gold, M.H.(1990), Lignin Peroxidase Compound III. Mechanism of Formation and Decomposition, J. Biol. Chem. 265, 2070–2077.

    CAS  Google Scholar 

  9. Wariishi, H., Dunford, H. B., MacDonald, I. D. and Gold, M. H.(1989), Manganese Peroxidase from the Lignin — degrading Basidiomycete Phanerochaete chrysporium. Transient State Kinetics and Reaction Mechanism, J. Biol. Chem., 264, 3335–3340.

    CAS  Google Scholar 

  10. Wariishi, H., Valli, K., Renganathan, V. and Gold, M.H. (1989), Thiol-mediated oxidation of Nonphenolic Lignin Model Compounds by Manganese Peroxidase of Phanerochaete chrysosporium, J. Biol. Chem., 264, 14185–14191.

    CAS  Google Scholar 

  11. Kono, Y. and Fridovich, I. (1983), Isolation and Characterization of the Pseudocatalase of Lactobacillus plantarum, I. J. Biol. Chem., 258, 6015–6019.

    CAS  Google Scholar 

  12. Kono, Y. and Fridovich, I. (1983), Inhibition and Reactivation of Mn — Catalase. Implication for Valence Changes at the Active Site Manganese, I. J. Biol. Chem., 258, 13646–13648.

    CAS  Google Scholar 

  13. Penner-Hahn, J. E.(1992) Structural Properties of the Manganese Site in the Manganese Catalases, In Manganese Redox Enzymes, V. L. Pecoraro, Ed., VCH Publishers, Inc.: New York, pp 29–45.

    Google Scholar 

  14. Waldo, G. S., Fronko, R. M. and Penner-Hahn, J. E. (1991), Inactivation and Reactivation of Manganese Catalase: Oxidation-Stat Assignements Using X-ray Absorption Spectroscopy, Biochemistry, 30, 10486–10490.

    Article  CAS  Google Scholar 

  15. Sheats, J. E., Czernaszewise, R. S., Dismukes, G. C., Rheingold, A. L., Petrouleas, V., Stubbe, J., Armstrong, W. H., Beer, R. H., Lippard, S. J. (1987), Binuclear Manganese (III) Complexes of Potential Biological Significance, J. Am. Chem. Soc., 109, 1435–1444.

    Article  CAS  Google Scholar 

  16. Wieghardt, K. (1989), The Active Sites in Manganese — Containing Metalloproteins and Inorganic Model Complexes, Angew. Chem. Int. Ed. Engl. 28, 1153–1172.

    Article  Google Scholar 

  17. Fronko, R. M., Penner-Hahn, J. E. and Bender, C. J. (1988), EPR Spectral Evidence for a Dinuclear Active Site in the Lactobacillus Plantarum Manganese Catalase, J. Am. Chem. Soc. 110, 7554–7555.

    Article  CAS  Google Scholar 

  18. Cooper, S. R., Dismukes, G. C., Klein, M. P, Calvin, M. (1978), Mixed Valence Interactions in Di-μ-oxo Bridged Manganese Complexes. Electron Paramagnetic Resonance and Magnetic Susceptibility Studies, J. Am. Chem. Soc. 100, 7248–7252.

    Article  CAS  Google Scholar 

  19. Gamelin, D. R., Kirk, M. L., Stemmler, T. L., Pal, S., Armstrong, W. H., Penner-Hahn J. E. and Solomon, E. I.(1994) Electronic Structure and Spectroscopy of Manganese Catalase and di-μ-Oxo [Mn(III)Mn(IV)] Model Complexes, J. Am. Chem. Soc. 116, 2392–2399.

    Article  CAS  Google Scholar 

  20. Dismukes, G. C. and Siderer, Y. (1980), EPR Spectroscopic Observations of a Manganese Center Associated with Water Oxidation in Spinach Chloroplasts, FEBS Lett. 121, 78–80.

    Article  CAS  Google Scholar 

  21. Dismukes, G. C. and Siderer, Y. (1981), Intermediates of a Polynuclear Manganese Center Involved in Photosynthetic Oxidation of Water Proc. Natl. Acad. Sci. U.S.A. 78, 274–278.

    Article  CAS  Google Scholar 

  22. Wille, B.and Lavergne, J. (1982), Measurement of Proton Translocation in Thylakoids under Flashing Light Using a Spin-labeled amine, Photobiochem. Photobiophys. 4, 131–144.

    CAS  Google Scholar 

  23. Brudvig, G. W., Casey, J. L. and Sauer, K. (1983), The Effect of Temperature on the Formation and Decay of the Multiline EPR Signal Species Associated with Photosynthetic Oxygen Evolution Biochim. Biophys. Acta 723, 366–371.

    Article  CAS  Google Scholar 

  24. Zimmerman, J.-L. and Rutherford, A. W. (1984), EPR Studies of the Oxygen Evolving Enzyme in Photosystem II, Biochim. Biophys. Acta, 767, 160–167.

    Article  Google Scholar 

  25. Casey, J. L. and Sauer, K.(1984), EPR Detection of a Cryogenically Photogenerated Intermediate in Photosynthetic Oxygen Evolution, Biochim. Biophys. Acta 761, 21–28.

    Google Scholar 

  26. Beck, W. F., de Paula, J. C. and Brudvig, G. W. (1985), Active and Resting States of the O2- Evolving Complex of Photosystem II, Biochemistry 24, 3035–3043.

    Article  CAS  Google Scholar 

  27. Brudvig, G. W. and Crabtree, R. H. (1986), Mechanism for Photosynthetic Oxygen Evolution, Proc. Natl. Acad. Sci. USA 83, 4586–4588.

    Article  CAS  Google Scholar 

  28. Yachandra, V. K., Guiles, R. D., McDermott, A., Britt, R. D., Dexheimer, S. L., Sauer, K. and Klein, M. P.(1986) The State of Manganese in the Photosynthetic Apparatus. 4. Structure of the Manganese Complex in Photosystem-II Studied Using EXAFS Spectroscopy. The S1 State of the O2 Evolving Photosystem-II Complex from Spinach, Biochim. Biophys. Acta 850, 324–332.

    Article  CAS  Google Scholar 

  29. Hansson, O., Aasa, R. and Vaenngaard, T. (1987), The Origin of the Multiline and g = 4.1 Electron Paramagnetic Resonance Signals from the Oxygen — evolving System of Photosystem II, Biophys. J. 51, 825–832.

    Article  CAS  Google Scholar 

  30. Cole, J., Yachandra, V. K., Guiles, R. D., McDermott, A. E., Britt, R. D., Dexheimer, S. L., Sauer, K. and Klein, M. P. (1987), Assignment of the g = 4.1 EPR Signal to Manganese in the S2 State of the Photosynthetic Oxygen — Evolving Comlex: An X-Ray Absorption Edge Spectroscopy Study, Biochim. Biophys. Acta, 890, 395–398.

    Article  CAS  Google Scholar 

  31. Yachandra, V. K., Guiles, R. D., McDermott, A. E., Cole, J. L., Britt, R. D., Dexheimer, S. L., Sauer, K. and Klein, M. P. (1987), Comparison of the Structure of the Manganese complex in the S1 and S2 States of the Photosynthetic O2- Evolving Complex: An X-ray Absorption Spectroscopy Study, Biochemistry, 26, 5974–5981.

    Article  CAS  Google Scholar 

  32. George, G. N., Prince, R. C. and Cramer, S. P. (1989), The Manganese Site of the Photosynthetic Water-splitting Enzyme, Science, 243, 789–791.

    Article  CAS  Google Scholar 

  33. Sivaraja, M., Philo, J. S., Lary, J. and Dismukes, G. C. (1989), Photosynthetic Oxygen Evolution: Changes in Magnetism of Water — Oxidizing Enzymes, J. Am. Chem. Soc., 111, 3221–3225.

    Article  CAS  Google Scholar 

  34. Boussac, A., Zimmermann, J.-L., Rutherford, A. W. and Lavergne, J. (1990), Histidine Oxidation in the Oxygen-Evolving Photosystem-II Enzyme, Nature, 347, 303–306.

    Article  CAS  Google Scholar 

  35. Penner-Hahn, J. E., Fronko, R. M., Pecoraro, V. L., Yocum, C. F., Betts, S. D. and Bowlby, N. R.(1990) Structural Characterization of the Manganese Sites in the Photosynthetic Oxygen Evolving Complex Using X-Ray Absorption-Spectroscopy, J. Am. Chem. Soc. 112, 2549–2557

    Article  CAS  Google Scholar 

  36. Jahns, P., Lavergne, J., Rappaport, F. and Junge, W. (1991), Stoichiometry of Proton Release during Photosynthetic Water Oxidation: A Reinterpretation of the Responses of Neutral Red Leads to a Non-integer Pattern, Biochim. Biophys. Acta 1057, 313–319.

    Article  CAS  Google Scholar 

  37. Dexheimer, S. L. and Klein, M. P.(1992) Detection of a Paramagnetic Intermediate in the S1 State of the Photosynthetic Oxyg en-Evolving Complex, J. Am. Chem. Soc. 114, 2821–2826.

    Article  CAS  Google Scholar 

  38. Koulougliotis, D., Hirsh, D. J. and Brudvig, G. W.(1992) The O2-Evolving Center of Photosystem II Is Diamagnetic in the S1 Resting State, J. Am. Chem. Soc. 114, 8322–8323.

    Article  CAS  Google Scholar 

  39. Ono, T.−a., Noguchi, T., Inoue, Y., Kusunoki, M., Matsushita, T. and Oyanagi, H.(1992) X-ray Detection of the Period-Four Cycling of the Manganese Cluster in Photosynthetic Water Oxidizing Enzyme, Science 258, 1335–1337

    Article  CAS  Google Scholar 

  40. a)Klein, M. P., Sauer, K. and Yachandra, V. K. Photosyn. Res. 1993, 38, 265. b)Liang, W., Latimer, M. J., Dau, H., Roelofs, T. A., Yachandra, V. K., Sauer, K. and Klein, M. P. (1994) Correlation Between Structure and Magnetic Spin State of the Manganese Cluster in the Oxygen Evolving Complex of Photosystem II in the S2 State Determination by X-Ray Absorption Spectroscopy, Biochemistry 33, 4923-4932

    Google Scholar 

  41. Wieghardt, K.(1989) The Active Sites in Manganese Containing Metalloproteins and Inorganic Model Complexes, Angew. Chem.-Inter. Edit. in English 28, 1153–1172

    Google Scholar 

  42. Vincent, J.B. and Christou, G. (1989), Higher Oxidation State Manganese Biomolecules, Adv. Inorg. Chem. Radiochem., 33, 197–257.

    Article  CAS  Google Scholar 

  43. Christou, G. (1989), Manganese Carboxylate Chemistry and Its Biological Relevance, Acc. Chem. Res., 22, 328–335

    Article  CAS  Google Scholar 

  44. Rardin, R. L., Bino, A., Poganiuch, P., Tolman, W. B., Liu, S. and Lippard, S. J.(1990), Synthesis and Characterization of the Linear Trinuclear Complexes [M3 II (O2CCH3)6 (biphme)2] M = Mn, Fe, Angew. Chem. Int. Ed. Engl., 29, 812

    Article  Google Scholar 

  45. Rardin, R. L., Poganiuch, P., Bino, A., Goldberg, D. P., Tolman, W. B., Liu, S. and Lippard, S. J.(1992) Synthesis and Characterization of Trinuclear Iron(II) and Manganese(II) Carboxylate Complexes. Structural Trends in Low Valent Iron and Manganese Carboxylates, J. Am. Chem. Soc., 114, 5240–5249.

    Article  CAS  Google Scholar 

  46. Kessissoglou, D. P., Butler, W. M. and Pecoraro, V. L.(1986) Structural and spectro-scopic Characterization of the Manganese(IV)Schiff-Base Complex Mn(saladhp)2 (saladhp=2-salicylideniminato-l, 3-dihydroxy-2-methyl-propane) J. Chem. Soc. Chem. Commun. 1253–1255

    Google Scholar 

  47. Kessissoglou, D. P., Li, X.-h., Butler, W. M. and Pecoraro, V. L.(1987) Mononuclear Manganese(IV) Complexes of Hydroxyl-Rich Schiff Base Ligands, Inorg. Chem. 26, 2487–2492

    Article  CAS  Google Scholar 

  48. Li, X-h., Kessissoglou, D. P., Kirk, M. L., Bender, C. and Pecoraro, V. L.(1988) Isolation of a mixed-Valence Trinuclear Manganese Complex Potentially Relevant to the Photosynthetic Oxygen-Evolving Complex, Inorg. Chem. 27, 1–3

    Article  CAS  Google Scholar 

  49. Kessissoglou, D. P., Kirk, M. L., Bender, C. A., Lah, M. S. and Pecoraro, V. L.(1989) A Bent Mixed-valence Manganese(III/II/III) Complex: A New Class of Trinuclear, Acetate Bridged Schiff’s Base Compounds Exhibiting a g=2 Multiline E.S.R. Signal, J. Chem. Soc., Chem. Commun. 84–86

    Google Scholar 

  50. Bonadies, J. A., Kirk, M. L., Lah, M. S., Kessissoglou, D. P., Hatfield, W. E. and Pecoraro, V. L.(1989) Structurally Diverse Manganese(III) Schiff Base Complexes:Chains, Dimers, and Cages, Inorg. Chem. 28, 2037–2044

    Article  CAS  Google Scholar 

  51. Kessissoglou, D. P., Butler, W. M. and Pecoraro, V. L.(1987) Characterization of Mono-and Binuclear Manganese(II)Schiff-Base Complexes with Metal-Disulfide Ligation, Inorg. Chem. 26, 495–503

    Article  CAS  Google Scholar 

  52. Kessissoglou, D. P., Kirk, M. L., Lah, M. S., Li, X.-h., Raptopoulou, C. A., Hatfield, W. E. and Pecoraro, V. L.(1992), Structural and Magnetic Characterization of Trinuclear, Mixed — Valence Manganese Acetates, Inorg. Chem. 31, 5424–5432

    Article  CAS  Google Scholar 

  53. Malamatari, D. A., Hitou, P., Hatzidimitriou, A. G., Inscore, F. E., Gourdon, A., Kirk, M. L. and Kessissoglou, D. P.(1995) First Example of a Mixed Valence Mn(III)Mn(II)Mn(III) Schiff-base Polymeric Complex having a Trimeric Repeat Unit; The Crystal Structure of [Mn3(Hsaladhp)2(acetato)2(5-Cl-salicylato)2]n, Inorg. Chem. 34, 2493–2494

    Article  CAS  Google Scholar 

  54. Kirk, M. L., Lah, M. S., Raptopoulou, C. A., Kessissoglou, D. P., Hatfield, W. E. and Pecoraro, V. L.(1991) Cationic Control of Spin Dimensionality in Infinite Chains of (Cation)2 [MnIII(salicylate)2(CH3OH)2][MnIII(salicylate)2], Inorg. Chem. 30, 3900–3908

    Article  CAS  Google Scholar 

  55. Larson, E. J, Haddy, A., Kirk, M. L., Sands, R., Hatfield, W. E. and Pecoraro, V. L.(1992), The Assymetric Mixed—Valent Complex [Mn(2-OH-3, 5-Cl2-SALPN)]2(THF)ClO4 Shows a Temperature—Dependent Interconversion between g = 2 Multiline and Low—Field EPR Signals, J. Am. Chem. Soc. 114, 6263–6265.

    Article  CAS  Google Scholar 

  56. Tangoulis, V., Malamatari, D. A., Soulti, K., Stergiou, V., Raptopoulou, C. P., Terzis, A., Kabanos, T. A. and Kessissoglou, D. P.(1996) ManganeseII/II/II and ManganeseII/II/II Trinuclear Compounds. Structure and solution behavior, Inorg. Chem., 35, 4974–4983

    Article  CAS  Google Scholar 

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  1. Department of General and Inorganic Chemistry, Aristotle University of Thessaloniki, Thessaloniki, 54006, Greece

    Dimitris P. Kessissoglou

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  1. Dimitris P. Kessissoglou
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  1. Laboratory of Inorganic and General Chemistry, Department of Chemistry, University of Ioannina, Ioannina, Greece

    Nick D. Hadjiliadis

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Kessissoglou, D.P. (1997). Modeling Manganese Redox Enzymes. In: Hadjiliadis, N.D. (eds) Cytotoxic, Mutagenic and Carcinogenic Potential of Heavy Metals Related to Human Environment. NATO ASI Series, vol 26. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-5780-3_17

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  • DOI: https://doi.org/10.1007/978-94-011-5780-3_17

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