Mechanisms of Nitric Oxide Reactions Mediated by Biologically Relevant Metal Centers

  • Peter C. Ford
  • Jose Clayston Melo Pereira
  • Katrina M. Miranda
Chapter

Abstract

Here, we present an overview of mechanisms relevant to the formation and several key reactions of nitric oxide (nitrogen monoxide) complexes with biologically relevant metal centers. The focus will be largely on iron and copper complexes. We will discuss the applications of both thermal and photochemical methodologies for investigating such reactions quantitatively.

Graphical Abstract

Keywords

Copper Heme models Hemes Iron Metalloproteins Nitric oxide 

Abbreviations

AN

Acetonitrile

aq

Aqueous

Cbl

Cobalamin

cGMP

Cyclic guanylyl monophosphate

CysSH

Cysteine

CytII

Ferrous cytochrome c

DAC

Bis(9-Anthracylmethyl)cyclam

DFT

Density functional theory

dmp

2,9-Dimethyl-1,10-phenanthroline

DNIC

Dinitrosyl iron complexes

dpp

2,9-Diphenyl-1,10-phenanthroline

EDTA4–

Ethylenediamintetraacetate

EPR

Electron paramagnetic resonance

F8Por

Tetrakis(2,6-difluorophenyl)-porphyrinato

GSH

Glutathione

GSNO

S-Nitrosoglutathione

GTP

Guanylyl triphosphate

Hb

Hemoglobin

Mb

Myoglobin

metMb

Metmyoglobin

MLCT

Metal-to-ligand charge transfer

MNIC

Mononitrosyl iron complexes

NiR

Nitrite reductase

NOS

Nitric oxide synthase

Por

Porphyrinato

PPIX

Protoporphyrin IX

RBS

Roussin’s black salt

RRE

Roussin’s red esters

RRS

Roussin’s red salt

sGC

Soluble guanylyl cyclase

THF

Tetrahydrofuran

TMPS

Tetra(sulfonato-mesityl)porphyrinato

TPP

Tetraphenylporphyrinato

TPPS

Tetra(4-sulfonatophenyl)porphyrin

tren

Bis-(2-aminoethyl)amine

UV

Ultraviolet

References

  1. 1.
    Ignarro LJ (1999) Angew Chemie I Ed 38:1882Google Scholar
  2. 2.
    Furchgott RF (1999) Angew Chemie I Ed 38:1870Google Scholar
  3. 3.
    Murad F (1999) Angew Chemie I Ed 38:1856Google Scholar
  4. 4.
    Ignarro LJ (2010) Nitric oxide: biology and pathobiology. 2nd edn. Elsevier Inc., BurlingtonGoogle Scholar
  5. 5.
    Bellamy TC, Garthwaite J (2001) J Biol Chem 276Google Scholar
  6. 6.
    Boon EM, Huang SH, Marletta MA (2005) Nature Chem Biol 1:53Google Scholar
  7. 7.
    Griffith OW, Stuehr DJ (1995) Ann Rev Physiol 57:707Google Scholar
  8. 8.
    Greenwood NN, Earnshaw A (1993) Chemistry of the elements. Pergamon, Oxford, Chapter 11Google Scholar
  9. 9.
    Coppens P, Novozhilova I, Kovalevsky A (2002) Chem Rev 102:861Google Scholar
  10. 10.
    Novozhilova IV, Coppens P, Lee J, Richter-Addo GB, Bagley KA (2006) J Am Chem Soc 128:2093Google Scholar
  11. 11.
    Tocheva EI, Rosell FI, Mauk AG, Murphy MEP (2004) Science 304:867Google Scholar
  12. 12.
    Tocheva EI, Rosell FI, Mauk AG, Murphy MEP (2007) Biochemistry 46:12366Google Scholar
  13. 13.
    Merkle AC, Lehnert N (2012) Dalton Trans 41:3355Google Scholar
  14. 14.
    Periyasamy G, Sundararajan M, Hillier IH, Burton NA, McDouall JJW (2007) Phys Chem 9:2498Google Scholar
  15. 15.
    Mingos DMP (1973) Inorg Chem 12:1209Google Scholar
  16. 16.
    Enemark JH, Feltham RD (1974) Coord Chem Rev 13:339Google Scholar
  17. 17.
    Wyllie GRA, Scheidt WR (2002) Chem Rev 102:1067Google Scholar
  18. 18.
    Copeland DM, Soares AS, West AH, Richter-Addo GB (2006) J Inorg Biochem 100:1413Google Scholar
  19. 19.
    Cohn JN, McInnes GT, Shepherd AM (2011) J Clin Hyperten 13:690Google Scholar
  20. 20.
    Roussin J (1858) Ann Chim Phys 52:285Google Scholar
  21. 21.
    Rauchfuss TB, Weatherill TD (1982) Inorg Chem 21:827Google Scholar
  22. 22.
    Mokh VP, Poltorakov AP, Serezhenkov VA, Vanin AF (2010) Nitric Oxide Biol Chem 22:266Google Scholar
  23. 23.
    Flitney FW, Megson IL, Thomson JLM, Kennovin GD, Butler AR (1996) Br J Pharmacol 117:1549Google Scholar
  24. 24.
    Bourassa J, DeGraff W, Kudo S, Wink DA, Mitchell JB, Ford PC (1997) J Am Chem Soc 119:2853Google Scholar
  25. 25.
    Kudo S, Bourassa JL, Boggs SE, Sato Y, Ford PC (1997) Analyt Biochem 247:193Google Scholar
  26. 26.
    Conrado CL, Bourassa JL, Egler C, Wecksler S, Ford PC (2003) Inorg Chem 42:2288Google Scholar
  27. 27.
    Wecksler SR, Mikhailovsky A, Korystov D, Ford PC (2006) J Amer Chem Soc 128:3831Google Scholar
  28. 28.
    Zheng Q, Bonoiu A, Ohulchanskyy TY, He GS, Prasad PN (2008) Mol Pharm 5:389Google Scholar
  29. 29.
    Chen TN, Lo FC, Tsai ML, Shih KN, Chiang MH, Lee GH, Liaw WF (2006) Inorg Chim Acta 359:2525Google Scholar
  30. 30.
    Kim YM, Chung HT, Simmons RL, Billiar TR (2000) J Biol Chem 275:10954Google Scholar
  31. 31.
    Butler AR, Megson IL (2002) Chem Rev 102:1155Google Scholar
  32. 32.
    Bosworth CA, Toledo JC Jr, Zmijewski JW, Li Q, Lancaster JR Jr (2009) Proc Natl Acad Sci USA 106:4671Google Scholar
  33. 33.
    Tonzetich ZJ, McQuade LE, Lippard SJ (2010) Inorg Chem 49:6338Google Scholar
  34. 34.
    Hickok JR, Sahni S, Shen H, Arvind A, Antoniou C, Fung LWM, Thomas DD (2011) Free Radic Biol Med 51:1558Google Scholar
  35. 35.
    Manoharan PT, Hamilton WC (1963) Inorg Chem 2:1043Google Scholar
  36. 36.
    Lu TT, Tsou CC, Huang HW, Hsu IJ, Chen JM, Kuo TS, Wang Y, Liaw WF (2008) Inorg Chem 47:6040Google Scholar
  37. 37.
    Bryar TR, Eaton DR (1992) Canad J Chem 70:1917Google Scholar
  38. 38.
    Johansson G, Lipscomb WN (1957) J Chem Phys 27:1417Google Scholar
  39. 39.
    Ruggiero CF, Carrier SM, Antholine WE, Whitataker JW, Cramer CJ, Tolman WB (1993) J Am Chem Soc 115:11285Google Scholar
  40. 40.
    Fujisawa K, Tateda A, Miyashita Y, Okamoto K, Paulat F, Praneeth VKK, Merkle A, Lehnert N (2008) (I) J Am Chem Soc 130:1205Google Scholar
  41. 41.
    Wright AM, Wu G, Hayton TW (2010) J Am Chem Soc 132:14336Google Scholar
  42. 42.
    Scheidt WR, Frisse ME (1975) J Am Chem Soc 97:17Google Scholar
  43. 43.
    Nasri H, Haller KJ, Wang Y, Huynh BH, Scheidt WR (1992) Inorg Chem 31:3459Google Scholar
  44. 44.
    Scheidt WR, Brinegar AC, Ferro EB, Kerner JF (1977) J Am Chem Soc 99:7315Google Scholar
  45. 45.
    Brucker EA, Olson JS, Ikeda-Saito M, Philips GN Jr (1998) Proteins Struct Funct Genet 30:352Google Scholar
  46. 46.
    Chan NL, Kavanaug JS, Rogers PH, Arnone A (2004) Biochemistry 43:118Google Scholar
  47. 47.
    Wayland BB, Olson LW (1974) J Am Chem Soc 95:6037Google Scholar
  48. 48.
    Hoffman BM, Weschler CJ, Basolo F (1976) J Am Chem Soc 98:5473Google Scholar
  49. 49.
    Palmer G (1979) In: Dolphin D (ed) The porphyrins, vol 4. Academic, New York, Chap. 6Google Scholar
  50. 50.
    Gouterman M (1961) J Mol Spectrosc 6:138Google Scholar
  51. 51.
    Westcott BL, Enemark JH (1999) In: Solomon EI, Lever ABP (eds) Inorganic electronic structure and spectroscopy, vol 2. Wiley, New York pp 403–450Google Scholar
  52. 52.
    Scheidt WR, Hatano K, Rupprecht GA, Piciulo PL (1979) Inorg Chem 18:292Google Scholar
  53. 53.
    Traylor TG, Sharma VS (1992) Biochemistry 31:2847Google Scholar
  54. 54.
    Perutz MF, Kilmartin JV, Nagai K, Szabo A, Simon SR (1976) Biochem 15:378Google Scholar
  55. 55.
    Dierks EA, Hu S, Vogel KM, Yu AE, Sprio TG, Burstyn JN (1997) J Am Chem Soc 119:7316Google Scholar
  56. 56.
    Derbyshire ER, Marletta MA (2012) Ann Rev Biochem 81:559Google Scholar
  57. 57.
    Patterson JC, Lorkovic IM, Ford PC (2003) Inorg Chem 42:4902Google Scholar
  58. 58.
    Toledo JC, Silva HAS, Scarpellini M, Mori V, Camargo AJ, Bertotti M, Franco DW (2004) Eur J Inorg Chem 1879Google Scholar
  59. 59.
    Goodrich LE, Paulat F, Praneeth VKK, Lehnert N (2010) Inorg Chem 49:6293Google Scholar
  60. 60.
    Caramori GF, Kunitz AG, Andriani KF, Doro FG, Frenking G, Tfouni E (2012) Dalton Trans 41:7327Google Scholar
  61. 61.
    Heinecke JL, Khin C, Pereira JCM, Suárez SA, Iretskii AV, Doctorovich F, Ford PC (2013) J Am Chem Soc 135:4007Google Scholar
  62. 62.
    Conradie J, Hopmann KH, Ghosh A (2010) J Phys Chem B 114:8517Google Scholar
  63. 63.
    Olson JS, Phillips GN (1996) J Biol Chem 271:17593Google Scholar
  64. 64.
    Strickland N, Harvey JN (2007) J Phys Chem B 111:841Google Scholar
  65. 65.
    Praneeth VKK, Paulat F, Berto TC, George SD, Näther C, Sulok CD, Lehnert N (2008) J Am Chem Soc 130:15288Google Scholar
  66. 66.
    Walda KN, Liu XY, Sharma VS, Magde D (1994) Biochem 33:2198Google Scholar
  67. 67.
    Benabbas A, Ye X, Kubo M, Zhang ZY, Maes EM, Montfort WR, Champion PM (2010) J Am Chem Soc132:2811Google Scholar
  68. 68.
    Park J, Lee T, Park J, Lim M (2013) J Phys Chem B 117:2850Google Scholar
  69. 69.
    Armor JN, Scheidegger HA, Taube H (1973) J Am Chem Soc 90:1968Google Scholar
  70. 70.
    Armor JN, Pell SD (1973) J Am Chem Soc 95:7625Google Scholar
  71. 71.
    Czap A, van Eldik R (2003) Dalton Trans 32:665Google Scholar
  72. 72.
    Ford PC, Fernandez BO, Lim MD (2005) Chem Rev 105:2439Google Scholar
  73. 73.
    Moore EG, Gibson QH (1976) J Biol Chem 251:2788Google Scholar
  74. 74.
    Tamura M, Kobayashi K, Hayashi K (1978) FEBS Let 88:124Google Scholar
  75. 75.
    Hoffman BM, Gibson QH (1978) Proc Natl Acad Sci USA 75:21Google Scholar
  76. 76.
    Rose EJ, Hoffman BM (1983) J Am Chem Soc 105:2866Google Scholar
  77. 77.
    Hoshino M, Arai S, Yamaji M, Hama Y (1986) J Phys Chem 90:2109Google Scholar
  78. 78.
    Ionascu D, Gruia F, Ye X, Yu A, Rosca F, Beck C, Demidov A, Olson JS, Champion PM (2005) J Am Chem Soc 127:16921Google Scholar
  79. 79.
    Purwar N, McGarry JM, Kostera J, Pacheco AA, Schmidt M (2011) Biochemistry 50:4491Google Scholar
  80. 80.
    Hoshino M, Kogure M (1989) J Phys Chem 93:5478Google Scholar
  81. 81.
    Hoshino M, Ozawa K, Seki H, Ford PC (1993) J Am Chem Soc 115:9568Google Scholar
  82. 82.
    Laverman LE, Ford PC (2001) J Am Chem Soc 123:11614Google Scholar
  83. 83.
    Laverman LE, Wanat A, Oszajca J, Stochel G, Ford PC, van Eldik R (2001) J Am Chem Soc 123:285Google Scholar
  84. 84.
    Ford PC (2010) Inorg Chem 49:6226Google Scholar
  85. 85.
    Wolak M, van Eldik R (2005) J Am Chem Soc 127:13312Google Scholar
  86. 86.
    Abu-Soud HM, Ichimori K, Presta A, Stuehr DJ (2000) J Biol Chem 275:17349Google Scholar
  87. 87.
    Scheele JS, Bruner E, Kharitonov VG, Martasek P, Roman LJ, Masters BS, Sharma VS, Magde D (1999) J Biol Chem 274:13105Google Scholar
  88. 88.
    Andersen JF, Ding XD, Balfour C, Shokhireva TK, Champagne DE, Walker FA, Montfort WR (2000) Biochem 39:10118Google Scholar
  89. 89.
    Ouellet H, Lang J, Couture MR, Ortiz de Montellano P (2009) Biochem 48:863Google Scholar
  90. 90.
    Franke A, Stochel G, Jung C, Van Eldik R (2004) J Am Chem Soc 126:4181Google Scholar
  91. 91.
    Kharitonov VG, Russwurm M, Madge D, Sharma VS, Koesling D (1997) Biochem Biophys Res Comm 239:284Google Scholar
  92. 92.
    Quaroni LG, Seward HE, McLean KJ, Girvan HM, Ost, TWB, Noble MA, Kelly SM, Price NC, Cheesman MR, Smith WE, Munro AW (2004) Biochem 43:16416Google Scholar
  93. 93.
    Rinaldo S, Arcovito A, Brunori M, Cutruzzolà F (2007) J Biol Chem 282:14761Google Scholar
  94. 94.
    Kakar S, Hoffman FG, Storz JF, Fabian M, Hargrove MS (2010) Biophys Chem152:1Google Scholar
  95. 95.
    Abbruzzetti S, Faggiano S, Spyrakis F, Bruno S, Mozzarelli A, Astegno A, Dominici P, Viappiani C (2011) IUBMB Life 63:1094Google Scholar
  96. 96.
    Condorelli P, George SC (2001) Biophys J 80:2110Google Scholar
  97. 97.
    Ostrich IJ, Gordon L, Dodgen HW, Hunt JP (1980) Inorg Chem 19:619Google Scholar
  98. 98.
    Schneppensieper T, Zahl A, van Eldik R (2001) Angew Chemie Int Ed Eng 40:1678Google Scholar
  99. 99.
    Hickok JR, Vasudevan D, Thatcher GRJ, Thomas DD (2012) Antioxi Redox Sig 17:962Google Scholar
  100. 100.
    Nhut G T, Kalyvas H, Skodje KM, Hayashi T, Moenne-Loccoz P, Callan PE, Shearer J, Kirschenbaum LJ, Kim E (2011) J Am Chem Soc 133 5 1184Google Scholar
  101. 101.
    Lin ZS, Lo FC, Li CH, Chen CH, Huang WN, Hsu IJ, Lee JF, Horng JC, Liaw WF (2011) Inorg Chem 50:10417Google Scholar
  102. 102.
    Vanin AF (2009) Nitric Oxide Biol Chem 21:1Google Scholar
  103. 103.
    Tonzetich ZJ, Do LH, Lippard SJ (2009) J Am Chem Soc 131:7964Google Scholar
  104. 104.
    Bourassa JL, Ford PC (2000) Coord Chem Rev 200:887Google Scholar
  105. 105.
    Sanina NA, Syrtsova LA, Shkondina NI, Rudneva TN, Malkova ES, Bazanov TA, Kotel'nikov AI, Aldoshin SM (2007) Nitric Oxide Biol Chem 16:181Google Scholar
  106. 106.
    Bourassa J, Lee B, Bernhard S, Schoonover J, Ford PC (1999) Inorg Chem 38:2947Google Scholar
  107. 107.
    Vanin AF, Papina AA, Serezhenkov VA, Koppenol WH (2004) Nitric Oxide 10:60Google Scholar
  108. 108.
    Wanat A, Schneppensieper T, Stochel G, van Eldik R, Bill E, Wieghardt K (2002) Inorg Chem 41:2Google Scholar
  109. 109.
    Schneppensieper T, Wanat A, Stochel G, Goldstein S, Meyerstein D, van Eldik R (2001) Euro J. Inorg Chem 2317Google Scholar
  110. 110.
    Lucas HR, Meyer GJ, Karlin KD (2009) J Am Chem Soc 131:13924Google Scholar
  111. 111.
    Zheng D, Birke R (2001) J Am Chem Soc 123:4637Google Scholar
  112. 112.
    Wolak M, Zahl A, Schneppensieper T, Stochel G, van Eldik R (2001) J Am Chem Soc 123:9780Google Scholar
  113. 113.
    Bakac A, Pestovsky O, Durfey BL, Kristian KE (2013) Chem Sci 4:2185Google Scholar
  114. 114.
    Gladwin MT, Grubina R, Doyle MP (2009) Accts Chem Res 42:157Google Scholar
  115. 115.
    He C, Knipp M (2009) J Am Chem Soc 131:12042Google Scholar
  116. 116.
    Yi J, Heinecke J, Tan H, Ford PC, Richter-Addo GB (2009) J Am Chem Soc 131:18119Google Scholar
  117. 117.
    Heinecke J, Ford PC (2010) Coord Chem Rev 254:235Google Scholar
  118. 118.
    Olabe JA (2008) Dalton Trans 3633Google Scholar
  119. 119.
    Cohn JN, McInnes GT, Shepherd AMJ (2011) Clin Hyperten 13:690Google Scholar
  120. 120.
    Vaughan CJ, Delanty N (2000) Lancet 356:411Google Scholar
  121. 121.
    Ascenzi P, Pesce A, Nardini M, Bolognesi M, Ciaccio C, Coletta M, Dewilde S (2013) Biochem Biophys Res Comm 430:1301Google Scholar
  122. 122.
    Hoshino M, Maeda M, Konishi R, Seki H, Ford PC (1996) J Am Chem Soc 118:5702Google Scholar
  123. 123.
    Koppenol WH (2012) Inorg Chem 51:5637Google Scholar
  124. 124.
    Reichenbach G, Sabatini S, Palombari R, Palmerini CA (2001) Nitric Oxide 5:395Google Scholar
  125. 125.
    Luchsinger BP, Rich EN, Gow AJ, Williams EM, Stamler JS, Singel DJ (2003) Proc Natl Acad Sci USA 100:461Google Scholar
  126. 126.
    Broniowska KA, Keszler A, Basu S, Kim-Shapiro DB, Hogg N (2012) Biochem J 442:191Google Scholar
  127. 127.
    Fernandez BO, Lorkovic IM, Ford PC (2004) Inorg Chem 43:5393Google Scholar
  128. 128.
    Fernandez BO, Ford PC (2003) J Am Chem Soc 125:10510Google Scholar
  129. 129.
    Basu S, Grubina R, Huang J, Conradie J, Huang Z, Jeffers A, Jiang A, He X, Azarov I, Seibert R, Mehta A, Patel R, King SB, Hogg N, Ghosh A, Gladwin MT, Kim-Shapiro DB (2007) Nature Chem Biol 3:785Google Scholar
  130. 130.
    Tejero J, Basu S, Helms C, Hogg N, King SB, Kim-Shapiro DB, Gladwin MT, Low NO (2012) J Biol Chem 287:18262Google Scholar
  131. 131.
    Lundberg J, Weitzberg E, Gladwin MT (2008) Nat Rev Drug Discov 7:156Google Scholar
  132. 132.
    Feelisch M, Fernandez BO, Bryan NS, Garcia-Saura MF, Bauer S, Whitlock DR, Ford PC, Janero DR, Rodriguez J, Ashrafian H (2008) J Biol Chem 283:33927Google Scholar
  133. 133.
    Lei Y, Anson FC (1994) Inorg Chem 33:5003Google Scholar
  134. 134.
    Tran D, Shelton BW, White Al. H, Laverman LE, Ford PC (1998) Inorg Chem 37:2505Google Scholar
  135. 135.
    Lim MD, Capps KB, Karpishin TB, Ford PC (2005) Nitric Oxide 12:244Google Scholar
  136. 136.
    Tsuge K, DeRosa F, Lim MD, Ford PC (2004) J Am Chem Soc 126:6564Google Scholar
  137. 137.
    Khin C, Lim MD, Tsuge K, Iretskii A, Wu G, Ford PC (2007) Inorg Chem 46:9323Google Scholar
  138. 138.
    Weichsel W, Maes EM, Andersen JF, Valenzuela JG, Shokhireva TK, Walker FA, Montfort WR (2005) Proc Natl Acad Sci USA 102:594Google Scholar
  139. 139.
    Franke A, Stochel G, Suzuki N, Higuchi T, Okuzono K, van Eldik R (2005) J Am Chem Soc 127:5360Google Scholar
  140. 140.
    Dicks AP, Swift HR, Williams DL, H, Butler AR, Al-Sa'doni HH, Cox BG (1996) J Chem Soc Perkin Trans 2:481Google Scholar
  141. 141.
    Melzer Marie M, Mossin S, Cardenas AJP, Williams KD, Zhang S, Meyer K, Warren TH (2012) Inorg Chem 5:8658Google Scholar
  142. 142.
    Franz KJ, Singh N, Lippard SJ (2000) Angew Chem I E 39:2120Google Scholar
  143. 143.
    Riklin M, Tran D, Bu X, Laverman LE, Ford PC (2001) JCS Dalton Trans 1813:1819Google Scholar
  144. 144.
    McMillin DR, Kirchoff JR, Goodwin KV (1985) Coord Chem Rev 64:83Google Scholar
  145. 145.
    Lim MH, Lippard SJ (2005) J Am Chem Soc 127:12170Google Scholar
  146. 146.
    Lim MH, Xu D, Lippard (2006) SJ Nat Chem Biol 2:375Google Scholar
  147. 147.
    McQuade LE, Pluth MD, Lippard SJ (2010) Inorg Chem 49:8025Google Scholar
  148. 148.
    Kumar P, Kalita A, Mondal B (2012) Dalton Trans 41:10543Google Scholar
  149. 149.
    Sarma M, Kalita A, Kumar P, Mondal B (2010) J Am Chem Soc 132:7846Google Scholar
  150. 150.
    Sarma M, Mondal B (2011) Inorg Chem 50:3206Google Scholar
  151. 151.
    Shiva S, Wang X, Ringwood LA, Xu X, Yuditskaya S, Annavajjhala V, Miyajima H, Hogg N, Harris ZL, Gladwin MT (2006) Nature Chem Biol 2:486Google Scholar
  152. 152.
    Grundy KR, Reed CA, Roper WR (1970) Chem Commun 1501Google Scholar
  153. 153.
    Wilson RD, Ibers JA (1979) Inorg Chem 18:336Google Scholar
  154. 154.
    Marhenke J, Joseph CA, Corliss MZ, Dunn T, Ford PC (2007) Polyhedron 26:4638Google Scholar
  155. 155.
    Lin R, Farmer PJ (2000) J Am Chem Soc 122:2393Google Scholar
  156. 156.
    Montenegro AC, Amorebieta VT, Slep LD, Martin DF, Roncaroli F, Murgida DH, Bari SE, Olabe JA (2009) Angew Chem Int Ed 48:4213Google Scholar
  157. 157.
    Khin C, Heinecke JL, Ford PC (2008) J Am Chem Soc 130:13830Google Scholar
  158. 158.
    Smith PAS, Hein GE (1960) J Am Chem Soc 82:5731Google Scholar
  159. 159.
    Miranda KM (2005) Coord Chem Rev 249:433Google Scholar
  160. 160.
    Doctorovich F, Bikiel D, Pellegrino J, Suarez SA, Larsen A, Marti MA (2011) Coord Chem Rev 255:2764Google Scholar
  161. 161.
    Fukuto JM, Cisneros CJ, Kinkade RL (2013) J Inorg Biochem 118:201Google Scholar
  162. 162.
    Ford PC, Wink DA, Stanbury DM (1993) FEBS Lett 326:1Google Scholar
  163. 163.
    Wink DA, Darbyshire JF, Nims RW, Saveedra JE, Ford PC (1993) Chem Res Toxicol 6:23Google Scholar
  164. 164.
    Silkstone RS, Mason MG, Nicholls P, Cooper CE (2012) Free Rad Biol Med 52:80Google Scholar
  165. 165.
    Ford E, Hughes MN, Wardman P (2002) Free Rad Biol Med 32:1314Google Scholar
  166. 166.
    Liu X, Miller MJS, Joshi MS, Thomas DD, Lancaster JR Jr (1998) Proc Natl Acad Sci USA 95:2175Google Scholar
  167. 167.
    Doyle MP, Hoekstra JW (1981) J Inorg Biochem14:351Google Scholar
  168. 168.
    Herold S, Exner M, Nauser T (2001) Biochemical 40:3385Google Scholar
  169. 169.
    Olson JS, Foley EW, Rogge C, Tsai AL, Doyle MP, Lemon DD (2004) Free Rad. Biol Med 36:685Google Scholar
  170. 170.
    Gardner PR, Gardner AM, Brashear WT, Suzuki T, Hvitved AN, Setchell KDR, Olson JS (2006) J Inorg Biochem 100:542Google Scholar
  171. 171.
    Kurtikyan TS, Ford PC (2010) Chem Commun 46:8570Google Scholar
  172. 172.
    Blomberg LM, Blomberg MRA, Siegbahn PEM (2004) J Inorg Biol Chem 9:923Google Scholar
  173. 173.
    Mishra S, Meuwly M (2010) J Am Chem Soc 132:2968Google Scholar
  174. 174.
    Møller JKS, Skibsted LH (2004) Chem Eur J 10:2291Google Scholar
  175. 175.
    Arnold EV (1996) Bohle DS 269:41Google Scholar
  176. 176.
    Munk MB, Huvaere K, Van Bocxlaer J, Skibsted LH (2010) Food Chem 121:472Google Scholar
  177. 177.
    Sarti P, Forte E, Mastronicola D, Giuffre A, Arese M (2012) Biochim Biophys Acta Bioenerget 1817:610Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Peter C. Ford
    • 1
  • Jose Clayston Melo Pereira
    • 1
  • Katrina M. Miranda
    • 2
  1. 1.Department of Chemistry and BiochemistryUniversity of CaliforniaSanta BarbaraUSA
  2. 2.Department of Chemistry and BiochemistryUniversity of ArizonaTucsonUSA

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