Biological Outer-Sphere Coordination

Part of the Structure and Bonding book series (STRUCTURE, volume 142)

Abstract

The concept of outer-sphere coordination (OSC) is surveyed in the context of bioinorganic chemistry. A distinction is made between electronic and structural OSC, both arising from the interaction of the protein matrix with inner sphere ligands. Electronic OSC entails the electronic interaction between the polypeptide and inner-sphere ligands. These effects principally arise from hydrogen-bonding interactions, though through-space dipolar interactions are also encountered. Structural OSC comprises primarily steric effects that do not necessarily impact ligand electronics but rather influence inner sphere topology. Additionally, the protein matrix can be envisioned as a local “solvent” whose bulk dielectric and point charges influence the metal center. Recurring themes are highlighted where OSC regulates the properties of various metalloproteins distinguished by cofactors and/or function. Finally, cases are presented where OSC has guided molecular design.

Keywords

Bioinorganic chemistry Outer sphere coordination Protein design 

References

  1. 1.
    Bjerrum J (1967) Coordination in the second sphere. In: Werner centennial. Advances in chemistry, vol 62. American Chemical Society, Washington, DC, pp 178–186Google Scholar
  2. 2.
    Werner A (1913) Neuere anschauungen auf dem gebiete der anorganischen chemie, 3rd edn. Vieweg und Sohn, BraunschweigGoogle Scholar
  3. 3.
    Colquhoun HM, Stoddart JF, Williams DJ (1986) Second-sphere coordination–a novel rǒle for molecular receptors. Angew Chem Int Ed 25:487–507Google Scholar
  4. 4.
    Lehn J-M (1995) Supramolecular chemistry: concepts and perspectives. Wiley-VCH, WeinheimGoogle Scholar
  5. 5.
    Vance CK, Miller AF (1998) Simple proposal that can explain the inactivity of metal-substituted superoxide dismutases. J Am Chem Soc 120:461–467Google Scholar
  6. 6.
    Stein J, Fackler JP, Mcclune GJ, Fee JA, Chan LT (1979) Superoxide and manganese(III) - reactions of Mn-EDTA and Mn-CYDTA complexes with O2- - X-ray structure of KMnEDTA•2H2O. Inorg Chem 18:3511–3519Google Scholar
  7. 7.
    Miller AF (2008) Redox tuning over almost 1 V in a structurally conserved active site: lessons from Fe-containing superoxide dismutase. Acc Chem Res 41(4):501–510Google Scholar
  8. 8.
    Jackson TA, Brunold TC (2004) Combined spectroscopic/computational studies on Fe- and Mn-dependent superoxide dismutases: insights into second-sphere tuning of active site properties. Acc Chem Res 37:461–470Google Scholar
  9. 9.
    Grove LE, Xie J, Yikilmaz E, Miller AF, Brunold TC (2008) Spectroscopic and computational investigation of second-sphere contributions to redox tuning in Escherichia coli iron superoxide dismutase. Inorg Chem 47:3978–3992Google Scholar
  10. 10.
    Vance CK, Miller AF (1998) Spectroscopic comparisons of the pH dependencies of Fe-substituted (Mn)superoxide dismutase and Fe-superoxide dismutase. Biochemistry 37:5518–5527Google Scholar
  11. 11.
    Dawson JH (1988) Probing structure-function relations in heme-containing oxygenases and peroxidases. Science 240:433–439Google Scholar
  12. 12.
    Yikilmaz E, Porta J, Grove LE, Vahedi-Faridi A, Bronshteyn Y, Brunold TC, Borgstahl GEO, Miller AF (2007) How can a single second sphere amino acid substitution cause reduction midpoint potential changes of hundreds of millivolts? J Am Chem Soc 129:9927–9940Google Scholar
  13. 13.
    Vance CK, Kang YM, Miller AF (1997) Selective N-15 labeling and direct observation by NMR of the active-site glutamine of Fe-containing superoxide dismutase. J Biomol NMR 9:201–206Google Scholar
  14. 14.
    Costa-Neto CM, Mikakawa AA, Oliveira L, Hjorth SA, Schwartz TW, Paiva ACM (2000) Mutational analysis of the interaction of the N- and C-terminal ends of angiotensin II with the rat AT(1A) receptor. Br J Pharmacol 130:1263–1268Google Scholar
  15. 15.
    Price JC, Barr EW, Tirupati B, Bollinger JM, Krebs C (2003) The first direct characterization of a high-valent iron intermediate in the reaction of an alpha-ketoglutarate-dependent dioxygenase: a high-spin Fe(IV) complex in taurine/alpha-ketoglutarate dioxygenase (TauD) from Escherichia coli. Biochemistry 42:7497–7508Google Scholar
  16. 16.
    Saban E, Chen Y-H, Hangasky J, Taabazuing C, Holmes BE, Knapp MJ (2011) The second coordination sphere of FIH controls hydroxylation. Biochemistry. doi:10.1021/bi102042t
  17. 17.
    McNeill LA, Hewitson KS, Claridge TD, Seibel JF, Horsfall LE, Schofield CJ (2002) Hypoxia-inducible factor asparaginyl hydroxylase (FIH-1) catalyses hydroxylation at the beta-carbon of asparagine-803. Biochem J 367:571–575Google Scholar
  18. 18.
    Gray HB, Malmstrom BG, Williams RJP (2000) Copper coordination in blue proteins. J Biol Inorg Chem 5(5):551–559Google Scholar
  19. 19.
    Malkin R, Malmström BG (1970) The state and function of copper in biological systems. Adv Enzymol Relat Areas Mol Biol 33:177–244Google Scholar
  20. 20.
    Solomon EI (2006) Spectroscopic methods in bioinorganic chemistry: blue to green to red copper sites. Inorg Chem 45:8012–8025Google Scholar
  21. 21.
    Canters GW, Gilardi G (1993) Engineering type 1 copper sites in proteins. FEBS Lett 325:39–48Google Scholar
  22. 22.
    Holland PL, Tolman WB (1999) Three-coordinate Cu(II) complexes: structural models of trigonal-planar type 1 copper protein active sites. J Am Chem Soc 121(31):7270–7271Google Scholar
  23. 23.
    Li H, Webb SP, Ivanic J, Jensen JH (2004) Determinants of the relative reduction potentials of type-1 copper sites in proteins. J Am Chem Soc 126(25):8010–8019Google Scholar
  24. 24.
    Hart PJ, Eisenberg D, Nersissian AM, Valentine JS, Herrmann RG, Nalbandyan RM (1996) A missing link in cupredoxins: crystal structure of cucumber stellacyanin at 1.6 Å resolution. Protein Sci 5:2175–2183Google Scholar
  25. 25.
    Guss JM, Bartunik HD, Freeman HC (1992) Accuracy and precision in protein structure analysis: restrained least-squares refinement of the structure of poplar plastocyanin at 1.33 A resolution. Acta Crystallogr B 48:790–811Google Scholar
  26. 26.
    Barrett ML, Harvey I, Sundararajan M, Surendran R, Hall JF, Ellis MJ, Hough MA, Strange RW, Hillier IH, Hasnain SS (2006) Atomic resolution crystal structures, EXAFS, and quantum chemical studies of rusticyanin and its two mutants provide insight into its unusual properties. Biochemistry 45:2927–2939Google Scholar
  27. 27.
    Nar H, Messerschmidt A, Huber R, Vandekamp M, Canters GW (1991) Crystal-structure analysis of oxidized pseudomonas aeruginosa azurin at pH 5.5 and oH 9.0 - a pH-induced conformational transition involves a peptide-bond flip. J Mol Biol 221:765–772Google Scholar
  28. 28.
    Reinhammar BRM (1972) Oxidation-reduction potentials of electron acceptors in laccases and stellacyanin. Biochim Biophys Acta 275:245Google Scholar
  29. 29.
    Nersissian AM, Immoos C, Hill MG, Hart PJ, Williams G, Herrmann RG, Valentine JS (1998) Uclacyanins, stellacyanins, and plantacyanins are distinct subfamilies of phytocyanins: plant-specific mononuclear blue copper proteins. Protein Sci 7:1915–1929Google Scholar
  30. 30.
    Rosen P, Pecht I (1976) Conformational equilibria accompanying electron-transfer between cytochrome-c (P551) and azurin from pseudomonas aeruginosa. Biochemistry 15:775–786Google Scholar
  31. 31.
    Ingledew WJ, Cobley JG (1980) A potentiometric and kinetic study on the respiratory chain of ferrous iron grown thiobacillus ferrooxidans. Biochim Biophys Acta 590:141–158Google Scholar
  32. 32.
    Berry SM, Ralle M, Low DW, Blackburn NJ, Lu Y (2003) Probing the role of axial methionine in the blue copper center of azurin with unnatural amino acids. J Am Chem Soc 125:8760–8768Google Scholar
  33. 33.
    Pascher T, Karlsson BG, Nordling M, Malmstrom BG, Vanngard T (1993) Reduction potentials and their pH-dependence in site-directed-mutant forms of azurin from Pseudomonas-aeruginosa. Eur J Biochem 212(2):289–296Google Scholar
  34. 34.
    Berry SM, Baker MH, Reardon NJ (2010) Reduction potential variations in azurin through secondary coordination sphere phenylalanine incorporations. J Inorg Biochem 104(10):1071–1078Google Scholar
  35. 35.
    Sinnecker S, Neese F (2006) QM/MM calculations with DFT for taking into account protein effects on the EPR and optical spectra of metalloproteins. Plastocyanin as a case study. J Comput Chem 27:1463–1475Google Scholar
  36. 36.
    Battistuzzi G, Borsari M, Loschi L, Menziani MC, De Rienzo F, Sola M (2001) Control of metalloprotein reduction potential: the role of electrostatic and solvation effects probed on plastocyanin mutants. Biochemistry 40:6422–6430Google Scholar
  37. 37.
    Malmstrom BG (1994) Rack-induced bonding in blue-copper proteins. Eur J Biochem 223:711–718Google Scholar
  38. 38.
    Dong SL, Ybe JA, Hecht MH, Spiro TG (1999) H-bonding maintains the active site of type 1 copper proteins: mutagenesis of Asn38 in poplar plastocyanin. Biochemistry 38:3379–3385Google Scholar
  39. 39.
    Yanagisawa S, Banfield MJ, Dennison C (2006) The role of hydrogen bonding at the active site of a cupredoxin: the Phe114Pro azurin variant. Biochemistry 45:8812–8822Google Scholar
  40. 40.
    Kataoka K, Hirota S, Maeda Y, Kogi H, Shinohara N, Sekimoto M, Sakurai T (2011) Enhancement of laccase activity through the construction and breakdown of a hydrogen bond at the type I copper center in Escherichia coli CueO and the deletion mutant delta alpha 5-7 CueO. Biochemistry 50:558–565Google Scholar
  41. 41.
    Roberts SA, Weichsel A, Grass G, Thakali K, Hazzard JT, Tollin G, Rensing C, Montfort WR (2002) Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli. Proc Natl Acad Sci USA 99:2766–2771Google Scholar
  42. 42.
    Solomon EI, Sundaram UM, Machonkin TE (1996) Multicopper oxidases and oxygenases. Chem Rev 96:2563–2605Google Scholar
  43. 43.
    Stoj CS, Augustine AJ, Zeigler L, Solomon EI, Kosman DJ (2006) Structural basis of the ferrous iron specificity of the yeast ferroxidase, Fet3p. Biochemistry 45:12741–12749Google Scholar
  44. 44.
    Marcus RA, Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811:265–322Google Scholar
  45. 45.
    Vanpouderoyen G, Mazumdar S, Hunt NI, Hill HAO, Canters GW (1994) The introduction of a negative charge into the hydrophobic patch of Pseudomonas aeruginosa azurin affects the alectron self-exchange rate and the electrochemistry. Eur J Biochem 222:583–588Google Scholar
  46. 46.
    van Amsterdam IMC, Ubbink M, Einsle O, Messerschmidt A, Merli A, Cavazzini D, Rossi GL, Canters GW (2002) Dramatic modulation of electron transfer in protein complexes by crosslinking. Nat Struct Biol 9:48–52Google Scholar
  47. 47.
    Shepard WEB, Anderson BF, Lewandoski DA, Norris GE, Baker EN (1990) Copper coordination geometry in azurin undergoes minimal change on reduction of copper(II) to copper(I). J Am Chem Soc 112:7817–7819Google Scholar
  48. 48.
    Farver O, Pecht I (1997) The role of the medium in long-range electron transfer. J Biol Inorg Chem 2:387–392Google Scholar
  49. 49.
    Mizoguchi TJ, Dibilio AJ, Gray HB, Richards JH (1992) Blue to type-2 binding - copper(II) and cobalt(II) derivatives of a Cys112Asp Mutant of Pseudomonas aeruginosa azurin. J Am Chem Soc 114:10076–10078Google Scholar
  50. 50.
    Lancaster KM, Yokoyama K, Richards JH, Winkler JR, Gray HB (2009) High-potential C112D/M121X (X = M, E H, L) Pseudomonas aeruginosa azurins. Inorg Chem 48:1278–1280Google Scholar
  51. 51.
    Lancaster KM, Sproules S, Palmer JH, Richards JH, Gray HB (2010) Outer-sphere effects on reduction potentials of copper sites in proteins: the curious case of high potential type 2 C112D/M121E Pseudomonas aeruginosa azurin. J Am Chem Soc 132:14590–14595Google Scholar
  52. 52.
    Lancaster KM, George SD, Yokoyama K, Richards JH, Gray HB (2009) Type-zero copper proteins. Nat Chem 1:711–715Google Scholar
  53. 53.
    Lancaster KM, Zaballa M-E, Sproules S, Sundararajan M, DeBeer S, Neese F, Vila AJ, Richards JH, Gray HB (In Preparation) The type zero copper site: Type 1 copper without thiolate ligationGoogle Scholar
  54. 54.
    DeBeer S, Kiser CN, Mines GA, Richards JH, Gray HB, Solomon EI, Hedman B, Hodgson KO (1999) X-ray absorption spectra of the oxidized and reduced forms of C112D azurin from Pseudomonas aeruginosa. Inorg Chem 38:433–438Google Scholar
  55. 55.
    Lancaster KM, Farver O, Wherland S, Crane EJ, Richards JH, Pecht I, Gray HB (2011) Electron transfer reactivity of type zero Pseudomonas aeruginosa azurin. J Am Chem Soc 133:4865–4873Google Scholar
  56. 56.
    Fisher JF, Meroueh SO, Mobashery S (2005) Bacterial resistance to beta-lactam antibiotics: compelling opportunism, compelling opportunity. Chem Rev 105:395–424Google Scholar
  57. 57.
    Crowder MW, Spencer J, Vila AJ (2006) Metallo-beta-lactamases: novel weaponry for antibiotic resistance in bacteria. Acc Chem Res 39:721–728Google Scholar
  58. 58.
    Tomatis PE, Fabiane SM, Simona F, Carloni P, Sutton BJ, Vila AJ (2008) Adaptive protein evolution grants organismal fitness by improving catalysis and flexibility. Proc Natl Acad Sci USA 105:20605–20610Google Scholar
  59. 59.
    Weinreich DM, Watson RA, Chao L (2005) Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59:1165–1174Google Scholar
  60. 60.
    Abriata LA, Gonzalez LJ, Llarrull LI, Tomatis PE, Myers WK, Costello AL, Tierney DL, Vila AJ (2008) Engineered mononuclear variants in Bacillus cereus metallo-beta-lactamase BcII are inactive. Biochemistry 47:8590–8599Google Scholar
  61. 61.
    Gonzalez JM, Martin FJM, Costello AL, Tierney DL, Vila AJ (2007) The zn2 position in metallo-beta-lactamases is critical for activity: a study on chimeric metal sites on a conserved protein scaffold. J Mol Biol 373:1141–1156Google Scholar
  62. 62.
    Cammack R (1992) Iron–sulfur clusters in enzymes: themes and variations. In: Richard C (ed) Advances in inorganic chemistry, vol 38. Academic Press, San Diego, pp 281–322Google Scholar
  63. 63.
    Rose K, Shadle SE, Eidsness MK, Kurtz DM, Scott RA, Hedman B, Hodgson KO, Solomon EI (1998) Investigation of iron-sulfur covalency in rubredoxins and a model system using sulfur K-edge X-ray absorption spectroscopy. J Am Chem Soc 120:10743–10747Google Scholar
  64. 64.
    Dauter Z, Wilson KS, Sieker LC, Moulis JM, Meyer J (1996) Zinc- and iron-rubredoxins from Clostridium pasteurianum at atomic resolution: A high-precision model of a ZnS4 coordination unit in a protein. Proc Natl Acad Sci USA 93:8836–8840Google Scholar
  65. 65.
    Adman E, Watenpaugh KD, Jensen LH (1975) NH•••S hydrogen-bonds in Peptococcus-aerogenes ferredoxin, Clostridium pasteurianum rubredoxin, and Chromatium high potential iron protein. Proc Natl Acad Sci USA 72:4854–4858Google Scholar
  66. 66.
    Kümmerle R, Zhuang-Jackson H, Gaillard J, Moulis J-M (1997) Site-directed mutagenesis of rubredoxin reveals the molecular basis of its electron transfer properties. Biochemistry 36:15983–15991Google Scholar
  67. 67.
    Okamura T-A, Takamizawa S, Ueyama N, Nakamura A (1998) Novel rubredoxin model tetrathiolato iron(II) and cobalt(II) complexes containing intramolecular single and double NH•••S hydrogen bonds. Inorg Chem 37:18–28Google Scholar
  68. 68.
    Lin IJ, Gebel EB, Machonkin TE, Westler WM, Markley JL (2003) Correlation between hydrogen bond lengths and reduction potentials in Clostridium pasteurianum rubredoxin. J Am Chem Soc 125:1464–1465Google Scholar
  69. 69.
    Xiao ZG, Maher MJ, Cross M, Bond CS, Guss JM, Wedd AG (2000) Mutation of the surface valine residues 8 and 44 in the rubredoxin from Clostridium pasteurianum: solvent access versus structural changes as determinants of reversible potential. J Biol Inorg Chem 5:75–84Google Scholar
  70. 70.
    Lin IJ, Gebel EB, Machonkin TE, Westler WM, Markley JL (2005) Changes in hydrogen-bond strengths explain reduction potentials in 10 rubredoxin variants. Proc Natl Acad Sci USA 102:14581–14586Google Scholar
  71. 71.
    Heering HA, Bulsink YBM, Hagen WR, Meyer TE (1995) Influence of charge and polarity on the redox potentials of high-potential iron-sulfur proteins - evidence for the existence of 2 groups. Biochemistry 34:14675–14686Google Scholar
  72. 72.
    Adman ET (1979) Comparison of the structures of electron-transfer Proteins. Biochim Biophys Acta 549:107–144Google Scholar
  73. 73.
    Backes G, Mino Y, Loehr TM, Meyer TE, Cusanovich MA, Sweeney WV, Adman ET, Sanders-Loehr J (1991) The environment of Fe4S4 clusters in ferredoxins and high-potential iron proteins – new information from X-ray crystallography and resonance Raman-spectroscopy. J Am Chem Soc 113:2055–2064Google Scholar
  74. 74.
    Carter CW (1977) New stereochemical analogies between iron-sulfur electron-transport proteins. J Biol Chem 252(21):7802–7811Google Scholar
  75. 75.
    Low DW, Hill MG (2000) Backbone-engineered high-potential iron proteins: effects of active-site hydrogen bonding on reduction potential. J Am Chem Soc 122:11039–11040Google Scholar
  76. 76.
    Kassner RJ, Yang W (1977) Theoretical-model for effects of solvent and protein dielectric on redox potentials of iron-sulfur clusters. J Am Chem Soc 99(13):4351–4355Google Scholar
  77. 77.
    Dey A, Francis EJ, Adams MWW, Babini E, Takahashi Y, Fukuyama K, Hodgson KO, Hedman B, Solomon EI (2007) Solvent tuning of electrochemical potentials in the active sites of HiPIP versus ferredoxin. Science 318:1464–1468Google Scholar
  78. 78.
    Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC (1998) X-ray crystal structure of the Fe-only hydrogenase (Cpl) from Clostridium pasteurianum to 1.8 Ångström resolution. Science 282:1853–1858Google Scholar
  79. 79.
    Nicolet Y, Piras C, Legrand P, Hatchikian CE, Fontecilla-Camps JC (1999) Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Structure 7:13–23Google Scholar
  80. 80.
    Tard C, Pickett CJ (2009) Structural and functional analogues of the active Sites of the [Fe]-, [NiFe]-, and [FeFe]-hydrogenases. Chem Rev 109:2245–2274Google Scholar
  81. 81.
    Silakov A, Wenk B, Reijerse E, Lubitz W (2009) N-14 HYSCORE investigation of the H-cluster of [FeFe] hydrogenase: evidence for a nitrogen in the dithiol bridge. Phys Chem Chem Phys 11:6592–6599Google Scholar
  82. 82.
    Walker FA (2004) Models of the bis-histidine-ligated electron-transferring cytochromes. Comparative geometric and electronic structure of low-spin ferro- and ferrihemes. Chem Rev 104:589–616Google Scholar
  83. 83.
    Banci L, Bertini I, Kuan IC, Tien M, Turano P, Vila AJ (1993) NMR investigation of isotopically labeled cyanide derivatives of lignin peroxidase and manganese peroxidase. Biochemistry 32:13483–13489Google Scholar
  84. 84.
    Bowman SEJ, Bren KL (2010) Variation and analysis of second-sphere interactions and axial histidinate character in c-type cytochromes. Inorg Chem 49:7890–7897Google Scholar
  85. 85.
    Springer BA, Sligar SG, Olson JS, Phillips GN (1994) Mechanisms of ligand recognition in myoglobin. Chem Rev 94:699–714Google Scholar
  86. 86.
    Collman JP, Brauman JI, Halbert TR, Suslick KS (1976) Nature of O2 and CO Binding to metalloporphyrins and heme proteins. Proc Natl Acad Sci USA 73:3333–3337Google Scholar
  87. 87.
    Pauling L, Weiss JJ (1964) Nature of iron-oxygen bond in oxyhaemoglobin. Nature 203:182–183Google Scholar
  88. 88.
    Perutz MF (1989) Myoglobin and hemoglobin – role of distal residues in reactions with heme ligands. Trends Biochem Sci 14:42–44Google Scholar
  89. 89.
    Phillips SEV (1980) Structure and refinement of oxymyoglobin at 1.6 Å resolution. J Mol Biol 142:531–554Google Scholar
  90. 90.
    Phillips SEV, Schoenborn BP (1981) Neutron-diffraction reveals oxygen-histidine hydrogen-Bond in oxymyoglobin. Nature 292:81–82Google Scholar
  91. 91.
    Jameson GB, Molinaro FS, Ibers JA, Collman JP, Brauman JI, Rose E, Suslick KS (1978) Structural changes upon oxygenation of an iron(II)(porphyrinato)(imidazole) complex. J Am Chem Soc 100:6769–6770Google Scholar
  92. 92.
    Peng SM, Ibers JA (1976) Stereochemistry of carbonylmetalloporphyrins – structure of (pyridine)(carbonyl)(5,10,15,20-tetraphenylporphinato)Iron(Ii). J Am Chem Soc 98:8032–8036Google Scholar
  93. 93.
    Olson JS, Mathews AJ, Rohlfs RJ, Springer BA, Egeberg KD, Sligar SG, Tame J, Renaud JP, Nagai K (1988) The role of the distal histidine in myoglobin and hemoglobin. Nature 336:265–266Google Scholar
  94. 94.
    Springer BA, Egeberg KD, Sligar SG, Rohlfs RJ, Mathews AJ, Olson JS (1989) Discrimination between oxygen and carbon monoxide and inhibition of autooxidation by myoglobin - site-directed mutagenesis of the distal histidine. J Biol Chem 264:3057–3060Google Scholar
  95. 95.
    Brantley RE, Smerdon SJ, Wilkinson AJ, Singleton EW, Olson JS (1993) The mechanism of autooxidation of myoglobin. J Biol Chem 268:6995–7010Google Scholar
  96. 96.
    Weiss JJ (1964) Nature of iron-oxygen bond in oxyhaemoglobin. Nature 202:83–84Google Scholar
  97. 97.
    McClure DS (1960) Electronic structure of transition metal complex ions. Radiat Res Suppl 2:218–242Google Scholar
  98. 98.
    Goddard WA, Olafson BD (1975) Ozone model for bonding of an O2 to heme in oxyhemoglobin. Proc Natl Acad Sci USA 72:2335–2339Google Scholar
  99. 99.
    Chen H, Ikeda-Saito M, Shaik S (2008) Nature of the Fe-O2 bonding in oxy-myoglobin: effect of the Protein. J Am Chem Soc 130:14778–14790Google Scholar
  100. 100.
    Berglund GI, Carlsson GH, Smith AT, Szöke H, Henriksen A, Hajdu J (2002) The catalytic pathway of horseradish peroxidase at high resolution. Nature 417:463–468Google Scholar
  101. 101.
    Denisov IG, Makris TM, Sligar SG, Schlichting I (2005) Structure and chemistry of cytochrome P450. Chem Rev 105:2253–2278Google Scholar
  102. 102.
    Dawson JH, Holm RH, Trudell JR, Barth G, Linder RE, Bunnenberg E, Djerassi C, Tang SC (1976) Oxidized cytochrome-P450 – magnetic circular dichroism evidence for thiolate ligation in substrate-bound form – implications for catalytic mechanism. J Am Chem Soc 98:3707–3709Google Scholar
  103. 103.
    Sono M, Andersson LA, Dawson JH (1982) Sulfur donor ligand-binding to ferric cytochrome-P450cam and myoglobin – ultraviolet-visible absorption, magnetic circular-dichroism, and electron-paramagnetic resonance spectroscopic investigation of the complexes. J Biol Chem 257:8308–8320Google Scholar
  104. 104.
    Poulos TL, Finzel BC, Howard AJ (1987) High-resolution crystal structure of cytochrome-P450cam. J Mol Biol 195:687–700Google Scholar
  105. 105.
    Yoshioka S, Takahashi S, Ishimori K, Morishima I (2000) Roles of the axial push effect in cytochrome P450cam studied with the site-directed mutagenesis at the heme proximal site. J Inorg Biochem 81:141–151Google Scholar
  106. 106.
    Yoshioka S, Tosha T, Takahashi S, Ishimori K, Hori H, Morishima I (2002) Roles of the proximal hydrogen bonding network in cytochrome P450(cam)-catalyzed oxygenation. J Am Chem Soc 124:14571–14579Google Scholar
  107. 107.
    Galinato MGI, Spolitak T, Ballou DP, Lehnert N (2011) Elucidating the role of the proximal cysteine hydrogen-bonding network in ferric cytochrome P450cam and corresponding mutants using magnetic circular dichroism spectroscopy. Biochemistry 50:1053–1069Google Scholar
  108. 108.
    Chen ZC, Ost TWB, Schelvis JPM (2004) Phe393 mutants of cytochrome P450BM3 with modified heme redox potentials have altered heme vinyl and propionate conformations. Biochemistry 43:1798–1808Google Scholar
  109. 109.
    Argos P, Mathews FS (1975) Structure of ferrocytochrome-B5 at 2.8 Å resolution. J Biol Chem 250:747–751Google Scholar
  110. 110.
    Reid LS, Taniguchi VT, Gray HB, Mauk AG (1982) Oxidation reduction equilibrium of cytochrome-B5. J Am Chem Soc 104:7516–7519Google Scholar
  111. 111.
    Reid LS, Mauk MR, Mauk AG (1984) Role of heme propionate groups in cytochrome-B5 electron transfer. J Am Chem Soc 106:2182–2185Google Scholar
  112. 112.
    Reid LS, Lim AR, Mauk AG (1986) Role of heme vinyl groups in cytochrome-B5 electron-transfer. J Am Chem Soc 108:8197–8201Google Scholar
  113. 113.
    Lee KB, Jun ES, Lamar GN, Rezzano IN, Pandey RK, Smith KM, Walker FA, Buttlaire DH (1991) Influence of heme vinyl-protein and carboxylate protein contacts on structure and redox properties of bovine cytochrome-B5. J Am Chem Soc 113:3576–3583Google Scholar
  114. 114.
    Pellicena P, Karow DS, Boon EM, Marletta MA, Kuriyan J (2004) Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases. Proc Natl Acad Sci USA 101:12854–12859Google Scholar
  115. 115.
    Olea C, Boon EM, Pellicena P, Kuriyan J, Marletta MA (2008) Probing the function of heme distortion in the H-NOX family. ACS Chem Biol 3(11):703–710Google Scholar
  116. 116.
    Olea C, Kuriyan J, Marletta MA (2010) Modulating heme redox potential through protein-induced porphyrin distortion. J Am Chem Soc 132:12794–12795Google Scholar
  117. 117.
    Lu Y, Yeung N, Sieracki N, Marshall NM (2009) Design of functional metalloproteins. Nature 460:855–862Google Scholar
  118. 118.
    Lu Y, Berry SM, Pfister TD (2001) Engineering novel metalloproteins: design of metal-binding sites into native protein scaffolds. Chem Rev 101:3047–3080Google Scholar
  119. 119.
    Ozaki SI, Roach MP, Matsui T, Watanabe Y (2001) Investigations of the roles of the distal heme environment and the proximal heme iron ligand in peroxide activation by heme enzymes via molecular engineering of myoglobin. Acc Chem Res 34:818–825Google Scholar
  120. 120.
    Matsui T, Ozaki S, Liong E, Phillips GN, Watanabe Y (1999) Effects of the location of distal histidine in the reaction of myoglobin with hydrogen peroxide. J Biol Chem 274:2838–2844Google Scholar
  121. 121.
    Shifman JM, Gibney BR, Sharp RE, Dutton PL (2000) Heme redox potential control in de novo designed four-alpha-helix bundle proteins. Biochemistry 39:14813–14821Google Scholar
  122. 122.
    Marshall NM, Garner DK, Wilson TD, Gao YG, Robinson H, Nilges MJ, Lu Y (2009) Rationally tuning the reduction potential of a single cupredoxin beyond the natural range. Nature 462:113–127Google Scholar
  123. 123.
    Shook RL, Borovik AS (2010) Role of the secondary coordination sphere in metal-mediated dioxygen activation. Inorg Chem 49:3646–3660Google Scholar
  124. 124.
    Kurtz DM (1990) Oxo- and hydroxo-bridged diiron complexes: a chemical perspective on a biological unit. Chem Rev 90:585–606Google Scholar
  125. 125.
    Collman JP, Gagne RR, Reed C, Halbert TR, Lang G, Robinson WT (1975) Picket fence porphyrins. Synthetic models for oxygen binding hemoproteins. J Am Chem Soc 97:1427–1439Google Scholar
  126. 126.
    Castro-Rodriguez I, Nakai H, Zakharov LN, Rheingold AL, Meyer K (2004) A linear, O-coordinated η1-CO2 bound to uranium. Science 305:1757–1759Google Scholar
  127. 127.
    Rosenthal J, Nocera DG (2008) Oxygen activation chemistry of pacman and hangman porphyrin architectures based on xanthene and dibenzofuran spacers. Progress in Inorganic Chemistry. Wiley, Hoboken, NJGoogle Scholar
  128. 128.
    Dogutan DK, Stoian SA, McGuire R, Schwalbe M, Teets TS, Nocera DG (2010) Hangman corroles: efficient synthesis and oxygen reaction chemistry. J Am Chem Soc 133:131–140Google Scholar
  129. 129.
    Sen Soo H, Komor AC, Iavarone AT, Chang CJ (2009) A hydrogen-bond facilitated cycle for oxygen reduction by an acid- and base-compatible iron Pplatform. Inorg Chem 48:10024–10035Google Scholar

Copyright information

© Springer Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Department of Chemistry and Chemical BiologyCornell UniversityIthacaUSA

Personalised recommendations