Skip to main content
SpringerLink
Log in

Multifrequency pulsed EPR studies of biologically relevant manganese(II) complexes

  • Published:
Applied Magnetic Resonance Aims and scope Submit manuscript

Abstract

Electron paramagnetic resonance studies at multiple frequencies (MF EPR) can provide detailed electronic structure descriptions of unpaired electrons in organic radicals, inorganic complexes, and metalloenzymes. Analysis of these properties aids in the assignment of the chemical environment surrounding the paramagnet and provides mechanistic insight into the chemical reactions in which these systems take part. Herein, we present results from pulsed EPR studies performed at three different frequencies (9, 31, and 130 GHz) on [Mn(II)(H2O)6]2+, Mn(II) adducts with the nucleotides ATP and GMP, and the Mn(II)-bound form of the hammerhead ribozyme (MnHH). Through line shape analysis and interpretation of the zero-field splitting values derived from successful simulations of the corresponding continuous-wave and field-swept echo-detected spectra, these data are used to exemplify the ability of the MF EPR approach in distinguishing the nature of the first ligand sphere. A survey of recent results from pulsed EPR, as well as pulsed electron-nuclear double resonance and electron spin echo envelope modulation spectroscopic studies applied to Mn(II)-dependent systems, is also presented.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Wieghardt K.: Angew. Chem.101, 1179–1198 (1989)

    Article  Google Scholar 

  2. Pecoraro V.L. (ed.): Manganese Redox Enzymes. Weinheim: VCH 1992.

    Google Scholar 

  3. Yocum C.F., Pecoraro V.L.: Curr. Opin. Chem. Biol.3, 182–187 (1999)

    Article  Google Scholar 

  4. Sigel A., Sigel H. (eds.):Manganese and Its Role in Biological Processes. Metal Ions in Biological Systems, vol. 37. New York: Marcel Dekker 2000.

    Google Scholar 

  5. Miller A.-F., Sorkin D.L.: Comments Mol. Cell. Biophys.9, 1–48 (1997)

    Google Scholar 

  6. Jackson T.A., Yikilmaz E., Miller A.-F., Brunold T.C.: J. Am. Chem. Soc.125, 8348–8363 (2003)

    Article  Google Scholar 

  7. Miller A.-F., Padmakumar K., Sorkin D.L., Karapetian A., Vance C.K.: J. Inorg. Biochem.93, 71–83 (2003)

    Article  Google Scholar 

  8. Miller A.-F.: Curr. Opin. Chem. Biol.8, 162–168 (2004)

    Article  Google Scholar 

  9. Jackson T.A., Brunold T.C.: Acc. Chem. Res.37, 461–470 (2004)

    Article  Google Scholar 

  10. Gold M.H., Glenn J.K.: Methods Enzymol.161, 258–264 (1988)

    Article  Google Scholar 

  11. van Aken B., Agathos S.N.: Appl. Microbiol. Biotechnol.58, 345–351 (2002)

    Article  Google Scholar 

  12. Sundaramoorthy M., Youngs H.L., Gold M.H., Poulos T.L.: Biochemistry44, 6463–6470 (2005)

    Article  Google Scholar 

  13. Su C., Sahlin M., Oliw E.H.: Adv. Exp. Med. Biol.507, 171–176 (2002)

    Google Scholar 

  14. Oliw E.H.: Prostaglandins Other Lipid Mediators68–69, 313–323 (2002)

    Article  Google Scholar 

  15. Gaffney B.J., Su C., Oliw E.H.: Appl. Magn. Reson.21, 411–422 (2001)

    Article  Google Scholar 

  16. Su C., Oliw E.H.: J. Biol. Chem.273, 13072–13079 (1998)

    Article  Google Scholar 

  17. Chang C.H., Svedruzic D., Ozarowski A., Walker L., Yeagle G., Britt R.D., Angerhofer A., Richards N.G.J.: J. Biol. Chem.279, 52840–52849 (2004)

    Article  Google Scholar 

  18. Tanner A., Bowater L., Fairhurst S.A., Bornemann S.: J. Biol. Chem.276, 43627–43634 (2001)

    Article  Google Scholar 

  19. Emerson J.P., Wagner M.L., Reynolds M.F., Que L. Jr., Sadowsky M.J., Wackett L.P.: J. Biol. Inorg. Chem.10, 751–760 (2005)

    Article  Google Scholar 

  20. Que L. Jr., Reynolds M.F. in: Manganese and Its Role in Biological Processes. Metal Ions in Biological Systems, vol. 37 (Sigel A., Sigel H., eds.), pp. 505–525. New York: Marcel Dekker 2000.

    Google Scholar 

  21. Whiting A.K., Boldt Y.R., Hendrich M.P., Wackett L.P., Que L. Jr.: Biochemistry35, 160–170 (1996)

    Article  Google Scholar 

  22. Dismukes G.C.: Chem. Rev.96, 2909–2926 (1996)

    Article  Google Scholar 

  23. Khangulov S.V., Barynin V.V., Melik-Adamyan V.R., Grebenko A.I., Voevodskaya N.V., Blyumenfel’d L.A., Dobryakov S.N., Il’yasova V.B.: Bioorg. Khim.12, 741–748 (1986)

    Google Scholar 

  24. Khangulov S.V., Barynin V.V., Voevodskaya N.V., Grebenko A.I.: Biochim. Biophys. Acta1020, 305–310 (1990)

    Article  Google Scholar 

  25. Yoder D.W., Hwang J., Penner-Hahn J.E. in: Manganese and Its Role in Biological Processes. Metal Ions in Biological Systems, vol. 37 (Sigel A., Sigel H., eds.), pp. 527–557. New York: Marcel Dekker 2000.

    Google Scholar 

  26. Barynin V.V., Whittaker M.M., Antonyuk S.V., Lamzin V.S., Harrison P.M., Artymiuk P.J., Whittaker J.W.: Structure9, 725–738 (2001)

    Article  Google Scholar 

  27. Willing A., Follmann H., Auling G.: Eur. J. Biochem.170, 603–611 (1988)

    Article  Google Scholar 

  28. Stubbe J.: Proc. Natl. Acad. Sci. USA95, 2723–2724 (1998)

    Article  ADS  Google Scholar 

  29. Goussias C., Boussac A., Rutherford A.W.: Philos. Trans. R. Soc. Lond. B357, 1369–1381 (2002)

    Article  Google Scholar 

  30. Barber J.Q.: Rev. Biophys.36, 71–89 (2003)

    Article  Google Scholar 

  31. Reed G.H., Markham G.D.: Biol. Magn. Reson.6, 73–142 (1984)

    Google Scholar 

  32. Copik A.J., Nocek B.P., Swierczek S.I., Ruebush S., Jang S.B., Lu M., D’Souza V.M., Peters J.W., Bennett B., Holz R.C.: Biochemistry,44, 121–129 (2005)

    Article  Google Scholar 

  33. DeRose V.J.: Curr. Opin. Struct. Biol.13, 317–324 (2003)

    Article  Google Scholar 

  34. Hammann C., Lilley D.M.J.: ChemBioChem3, 690–700 (2002)

    Article  Google Scholar 

  35. Morrissey S.R., Horton T.E., DeRose V.J.: J. Am. Chem. Soc.122, 3473–3481 (2000)

    Article  Google Scholar 

  36. Dowsing R.D., Gibson J.F.: J. Chem. Phys.50, 294–303 (1969)

    Article  ADS  Google Scholar 

  37. Abragam A., Bleaney B.: Electron Paramagnetic Resonance of Transition Ions. Oxford: Clarendon Press 1970.

    Google Scholar 

  38. Markham G.D., Rao B.D.N., Reed G.H.: J. Magn. Reson.33, 595–602 (1979)

    Google Scholar 

  39. Coffino A.R., Peisach J.: J. Magn. Reson.111, 127–134 (1996)

    Article  Google Scholar 

  40. Tan X., Bernardo M., Thomann H., Scholes C.P.: J. Chem. Phys.98, 5147–5157 (1993)

    Article  ADS  Google Scholar 

  41. Benetis P.N., Dave P.C., Goldfarb D.: J. Magn. Reson.158, 126–142 (2002)

    Article  ADS  Google Scholar 

  42. Un S., Tabares L.C., Cortez N., Hiraoka B.Y., Yamakura F.: J. Am. Chem. Soc.126, 2720–2726 (2004)

    Article  Google Scholar 

  43. LoBrutto R., Smithers G.W., Reed G.H., Orme-Johnson W.H., Tan S.L., Leigh J.S. Jr.: Biochemistry25, 5654–5660 (1986)

    Article  Google Scholar 

  44. Sturgeon B.E., Ball J.A., Randall D.W., Britt R.D.: J. Phys. Chem.98, 12871–12883 (1994)

    Article  Google Scholar 

  45. Duboc C., Astier-Perret V., Chen H., Pecaut J., Crabtree R.H., Brudvig G.W., Collomb M.-N.: Inorg. Chim. Acta359, 1541–1548 (2006)

    Article  Google Scholar 

  46. Meirovitch E., Luz Z., Kalb A.J.: J. Am. Chem. Soc.96, 7538–7542 (1974)

    Article  Google Scholar 

  47. Meirovitch E., Luz Z., Kalb A.J.: J. Am. Chem. Soc.96, 7542–7546 (1974)

    Article  Google Scholar 

  48. Cohn M., Townsend J.: Nature (London)173, 1090–1091 (1954)

    Article  ADS  Google Scholar 

  49. Jallon J.M., Cohn M.: Biochim. Biophys. Acta222, 542–545 (1970)

    Google Scholar 

  50. Reed G.H., Cohn M.: J. Biol. Chem.245, 662–664 (1970)

    Google Scholar 

  51. Reed G.H., Diefenbach H., Cohn M.: J. Biol. Chem.247, 3066–3072 (1972)

    Google Scholar 

  52. Reed G.H., Cohn M.: J. Biol. Chem.248, 6436–6442 (1973)

    Google Scholar 

  53. Buttlaire D.H., Cohn M.: J. Biol. Chem.249, 5733–5740 (1974)

    Google Scholar 

  54. Wilson G.E. Jr., Cohn M.: J. Biol. Chem.252, 2004–2009 (1977)

    Google Scholar 

  55. Feher G.: Phys. Rev.103, 500–501 (1956)

    Article  ADS  Google Scholar 

  56. Deigen M.F., Maevskii V.M., Zevin V.Y., Vitrikhovskii N.I.: Radiospektrosk. Tverd. Tela1967 317–320.

  57. Seamonds B., Blumberg W.E., Peisach J.: Biochim. Biophys. Acta263, 507–514 (1972)

    Google Scholar 

  58. Mailer C., Taylor C.P.: Biochim. Biophys. Acta322, 195–203 (1973)

    Google Scholar 

  59. Smoukov S.K., Telser J., Bernat B.A., Rife C.L., Armstrong R.N., Hoffman B.M.: J. Am. Chem. Soc.124, 2318–2326 (2002)

    Article  Google Scholar 

  60. Hyde J.S., Dalton L.: Chem. Phys. Lett.16, 568–572 (1972)

    Article  ADS  Google Scholar 

  61. Britt R.D.: Curr. Opin. Struct. Biol.3, 774–779 (1993)

    Article  Google Scholar 

  62. Britt R.D.: ACS Symp. Ser.858, 16–54 (2003)

    Article  Google Scholar 

  63. Campbell K.A., Yikilmaz E., Grant C.V., Gregor W., Miller A.-F., Britt R.D.: J. Am. Chem. Soc.121, 4714–4715 (1999)

    Article  Google Scholar 

  64. Tabares L.C., Cortez N., Agalidis I., Un S.: J. Am. Chem. Soc.127, 6039–6047 (2005)

    Article  Google Scholar 

  65. Jackson T.A., Karapetian A., Miller A.-F., Brunold T.C.: J. Am. Chem. Soc.126, 12477–12491 (2004)

    Article  Google Scholar 

  66. Jackson T.A., Xie J., Yikilmaz E., Miller A.-F., Brunold T.C.: J. Am. Chem. Soc.124, 10833–10845 (2002)

    Article  Google Scholar 

  67. Hoganson C.W., Babcock G.T.: Biochemistry31, 11874–11880 (1992)

    Article  Google Scholar 

  68. Britt R.D., Force D.A., Campbell K.A., Randall D.W., Gilchrist L.M., Clemens K.L., Gingell D.M., Peloquin J.M., Pham D.P., Debus R.J.: ACS Symp. Ser.692, 272–285 (1998)

    Article  Google Scholar 

  69. Britt R.D., Campbell K.A., Peloquin J.M., Gilchrist M.L., Aznar C.P., Dicus M.M., Robblee J., Messinger J.: Biochim. Biophys. Acta1655, 158–171 (2004)

    Article  Google Scholar 

  70. Debus R.J., Campbell K.A., Gregor W., Li Z.-L., Burnap R.L., Britt R.D.: Biochemistry40, 3690–3699 (2001)

    Article  Google Scholar 

  71. Debus R.J., Aznar C., Campbell K.A., Gregor W., Diner B.A., Britt R.D.: Biochemistry42, 10600–10608 (2003)

    Article  Google Scholar 

  72. Kim S.H., Gregor W., Peloquin J.M., Brynda M., Britt R.D.: J. Am. Chem. Soc.126, 7228–7237 (2004)

    Article  Google Scholar 

  73. Clemens K.L., Force D.A., Britt R.D.: J. Am. Chem. Soc.124, 10921–10933 (2002)

    Article  Google Scholar 

  74. Åhrling K.A., Evans M.C.W., Nugent J.H.A., Ball R.J., Pace R.J.: Biochemistry45, 7069–7082 (2006)

    Article  Google Scholar 

  75. Evans M.C.W., Nugent J.H.A., Ball R.J., Muhiuddin I., Pace R.J.: Biochemistry43, 989–994 (2004)

    Article  Google Scholar 

  76. Kok B., Forbush B., McGloin M.: Photochem. Photobiol.11, 457–475 (1970)

    Article  Google Scholar 

  77. Kulik L.V., Epel B., Lubitz W., Messinger J.: J. Am. Chem. Soc.127, 2392–2393 (2005)

    Article  Google Scholar 

  78. Zaltsman L., Ananyev G.M., Bruntrager E., Dismukes G.C.: Biochemistry36, 8914–8922 (1997)

    Article  Google Scholar 

  79. Campbell K.A., Force D.A., Nixon P.J., Dole F., Diner B.A., Britt R.D.: J. Am. Chem. Soc.122, 3754–3761 (2000)

    Article  Google Scholar 

  80. Baranov S.V., Tyryshkin A.M., Katz D., Dismukes G.C., Ananyev G.M., Klimov V.V.: Biochemistry43, 2070–2079 (2004)

    Article  Google Scholar 

  81. Kozlov Y.N., Zharmukhamedov S.K., Tikhonov K.G., Dasgupta J., Kazakova A.A., Dismukes G.C., Klimov V.V.: Phys. Chem. Chem. Phys.6, 4905–4911 (2004)

    Article  Google Scholar 

  82. Dasgupta J., Tyryshkin A.M., Kozlov Y.N., Klimov V.V., Dismukes G.C.: J. Phys. Chem. B110, 5099–5111 (2006)

    Article  Google Scholar 

  83. Bollinger J.M. Jr., Edmondson D.E., Huynh B.H., Filley J., Norton J.R., Stubbe J.: Science253, 292–298 (1991)

    Article  ADS  Google Scholar 

  84. Atta M., Nordlund P., Aaberg A., Eklund H., Fontecave M.: J. Biol. Chem.267, 20682–20688 (1992)

    Google Scholar 

  85. Pierce B.S., Elgren T.E., Hendrich M.P.: J. Am. Chem. Soc.125, 8748–8759 (2003)

    Article  Google Scholar 

  86. Pierce B.S., Hendrich M.P.: J. Am. Chem. Soc.127, 3613–3623 (2005)

    Article  Google Scholar 

  87. Walsby C.J., Telser J., Rigsby R.E., Armstrong R.N., Hoffman B.M.: J. Am. Chem. Soc.127, 8310–8319 (2005)

    Article  Google Scholar 

  88. Law N.A., Caudle M.T., Pecoraro V.L.: Adv. Inorg. Chem.46, 305–440 (1998)

    Article  Google Scholar 

  89. Pecoraro V.L., Gelasco A., Baldwin M.J.: Adv. Chem. Ser.246, 265–301 (1995)

    Article  Google Scholar 

  90. Wu A.J., Penner-Hahn J.E., Pecoraro V.L.: Chem. Rev.104, 903–938 (2004)

    Article  Google Scholar 

  91. Scott W.G.: Curr. Opin. Chem. Biol.3, 705–709 (1999)

    Article  Google Scholar 

  92. Horton T.E., Clardy D.R., DeRose V.J.: Biochemistry37, 18094–18101 (1998)

    Article  Google Scholar 

  93. Blount K.F., Uhlenbeck O.C.: Annu. Rev. Biophys. Biomol. Struct.34, 415–440 (2005)

    Article  Google Scholar 

  94. Morrissey S.R., Horton T.E., Grant C.V., Hoogstraten C.G., Britt R.D., DeRose V.J.: J. Am. Chem. Soc.121, 9215–9218 (1999)

    Article  Google Scholar 

  95. Scott W.G., Murray J.B., Arnold J.R.P., Stoddard B.L., Klug A.: Science274, 2065–2069 (1996)

    Article  ADS  Google Scholar 

  96. Scott W.G., Murray J.B.: Methods Enzymol.317, 180–198 (2000)

    Article  Google Scholar 

  97. Murray J.B., Scott W.G.: J. Mol. Biol.296, 33–41 (2000)

    Article  Google Scholar 

  98. Murray J.B., Terwey D.P., Maloney L., Karpeisky A., Usman N., Beigelman L., Scott W.G.: Cell92, 665–673 (1998)

    Article  Google Scholar 

  99. Vogt M., Lahiri S., Hoogstraten C., Britt R.D., DeRose V.J.: J. Am. Chem. Soc. (2006) in press.

  100. Sturgeon B.E., Britt R.D.: Rev. Sci. Instrum.63, 2187–2192 (1992)

    Article  ADS  Google Scholar 

  101. Dorlet P., Seibold S.A., Babcock G.T., Gerfen G.J., Smith W.L., Tsai A.-I., Un S.: Biochemistry41, 6107–6114 (2002)

    Article  Google Scholar 

  102. Stoll S., Schweiger A.: J. Magn. Reson.178, 42–55 (2006)

    Article  ADS  Google Scholar 

  103. Stoll S., Schweiger A.: J. Magn. Reson.163, 248–256 (2003)

    Article  ADS  Google Scholar 

  104. Hoogstraten C.G., Grant C.V., Horton T.E., DeRose V.J., Britt R.D.: J. Am. Chem. Soc.124, 834–842 (2002)

    Article  Google Scholar 

  105. Bleaney B., Rubins R.S.: Proc. Phys. Soc. Lond.77, 103–112 (1961)

    Article  Google Scholar 

  106. Tan X., Bernardo M., Thomann H., Scholes C.P.: J. Chem. Phys.102, 2675–2690 (1995)

    Article  ADS  Google Scholar 

  107. Halkides C.J., Farrar C.T., Singel D.J.: J. Magn. Reson.134, 142–153 (1998)

    Article  ADS  Google Scholar 

  108. Hoogstraten C.G., Britt R.D.: RNA8, 252–260 (2002)

    Article  Google Scholar 

  109. Schiemann O., Fritscher J., Kisseleva N., Sigurdsson S.T., Prisner T.F.: ChemBioChem4, 1057–1065 (2003)

    Article  Google Scholar 

  110. More K.M., Eaton G.R., Eaton S.S.: Inorg. Chem.25, 2638–2646 (1986)

    Article  Google Scholar 

  111. Wood R.M., Stucker D.M., Jones L.M., Lynch W.B., Misra S.K., Freed J.H.: Inorg. Chem.38, 5384–5388 (1999)

    Article  Google Scholar 

  112. Richards S., Pedersen B., Silverton J.V., Hoard J.L.: Inorg. Chem.3, 27–33 (1964)

    Article  Google Scholar 

  113. Zetter M.S., Grant M.W., Wood E.J., Dodgen H.W., Hunt J.P.: Inorg. Chem.11, 2701–2706 (1972)

    Article  Google Scholar 

  114. McCracken J., Peisach J., Bhattacharyya L., Brewer F.: Biochemistry30, 4486–4491 (1991)

    Article  Google Scholar 

  115. Eaton G.R., Eaton S.S.: Appl. Magn. Reson.16, 161–166 (1999)

    Article  Google Scholar 

  116. Bar G., Bennati M., Nguyen H.-H.T., Ge J., Stubbe J., Griffin R.G.: J. Am. Chem. Soc.123, 3569–3576 (2001)

    Article  Google Scholar 

  117. Andersson K.K., Schmidt P.P., Katterle B., Strand K.R., Palmer A.E., Lee S.-K., Solomon E.I., Graeslund A., Barra A.-L.: J. Biol. Inorg. Chem.8, 235–247 (2003)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemistry, University of California-Davis, One Shields Avenue, 95616, Davis, CA, USA

    T. A. Stich, S. Lahiri, G. Yeagle, M. Dicus, M. Brynda, A. Gunn, C. Aznar & R. D. Britt

  2. Department of Chemistry, University of Oregon, Eugene, Oregon, USA

    V. J. DeRose

Authors
  1. T. A. Stich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Lahiri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. Yeagle
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Dicus
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Brynda
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. Gunn
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. C. Aznar
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. V. J. DeRose
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. R. D. Britt
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stich, T.A., Lahiri, S., Yeagle, G. et al. Multifrequency pulsed EPR studies of biologically relevant manganese(II) complexes. Appl. Magn. Reson. 31, 321–341 (2007). https://doi.org/10.1007/BF03166263

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03166263

Keywords

Search

Navigation