JBIC Journal of Biological Inorganic Chemistry

, Volume 19, Issue 7, pp 1057–1067 | Cite as

Bis-Fe(IV): nature’s sniper for long-range oxidation

Minireview

Abstract

Iron-dependent enzymes are prevalent in nature and participate in a wide range of biological redox activities. Frequently, high-valence iron intermediates are involved in the catalytic events of iron-dependent enzymes, especially when the activation of peroxide or molecular oxygen is involved. Building on the fundamental framework of iron–oxygen chemistry, these reactive intermediates constantly attract significant attention from the enzymology community. During the past few decades, tremendous efforts from a number of laboratories have been dedicated to the capture and characterization of these intermediates to improve mechanistic understandings. In 2008, an unprecedented bis-Fe(IV) intermediate was reported in a c-type diheme enzyme, MauG, which is involved in the maturation of a tryptophan tryptophylquinone cofactor of methylamine dehydrogenase. This intermediate, although chemically equivalent to well-characterized high-valence iron intermediates, such as compound I, compound ES, and intermediate Q in methane monooxygenase, as well as the hypothetical Fe(V) species in Rieske non-heme oxygenases, is orders of magnitude more stable than these other high-valence species in the absence of its primary substrate. It has recently been discovered that the bis-Fe(IV) intermediate exhibits a unique near-IR absorption feature which has been attributed to a novel charge-resonance phenomenon. This review compares the properties of MauG with structurally related enzymes, summarizes the current knowledge of this new high-valence iron intermediate, including its chemical origin and structural basis, explores the formation and consequences of charge resonance, and recounts the long-range catalytic mechanism in which bis-Fe(IV) participates. Biological strategies for storing oxidizing equivalents with iron ions are also discussed.

Keywords

High-valent iron Charge resonance Long-range catalysis Radical enzymology Posttranslational modification 

References

  1. 1.
    Minnihan EC, Nocera DG, Stubbe J (2013) Acc Chem Res 46:2524–2535PubMedCrossRefGoogle Scholar
  2. 2.
    Abu Tarboush N, Jensen LMR, Yukl ET, Geng J, Liu A, Wilmot CM, Davidson VL (2011) Proc Natl Acad Sci USA 108:16956–16961CrossRefGoogle Scholar
  3. 3.
    Gray HB, Winkler JR (2010) Biochim Biophys Acta 1797:1563–1572PubMedCrossRefGoogle Scholar
  4. 4.
    Warren JJ, Ener ME, Vlček A Jr, Winkler JR, Gray HB (2012) Coord Chem Rev 256:2478–2487PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    McIntire WS, Wemmer DE, Chistoserdov A, Lidstrom ME (1991) Science 252:817–824PubMedCrossRefGoogle Scholar
  6. 6.
    Eady RR, Large PJ (1968) Biochem J 106:245–255PubMedPubMedCentralGoogle Scholar
  7. 7.
    Chen L, Doi M, Durley RC, Chistoserdov AY, Lidstrom ME, Davidson VL, Mathews FS (1998) J Mol Biol 276:131–149PubMedCrossRefGoogle Scholar
  8. 8.
    Wang Y, Graichen ME, Liu A, Pearson AR, Wilmot CM, Davidson VL (2003) Biochemistry 42:7318–7325PubMedCrossRefGoogle Scholar
  9. 9.
    Pearson AR, De la Mora-Rey T, Graichen ME, Wang Y, Jones LH, Marimanikkupam S, Agger SA, Grimsrud PA, Davidson VL, Wilmot CM (2004) Biochemistry 43:5494–5502PubMedCrossRefGoogle Scholar
  10. 10.
    Yukl ET, Liu F, Krzystek J, Shin S, Jensen LMR, Davidson VL, Wilmot CM, Liu A (2013) Proc Natl Acad Sci USA 110:4569–4573PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Li X, Jones LH, Pearson AR, Wilmot CM, Davidson VL (2006) Biochemistry 45:13276–13283PubMedCrossRefGoogle Scholar
  12. 12.
    Li X, Fu R, Lee S, Krebs C, Davidson VL, Liu A (2008) Proc Natl Acad Sci USA 105:8597–8600PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Chistoserdov AY, Boyd J, Mathews FS, Lidstrom ME (1992) Biochem Biophys Res Commun 184:1181–1189PubMedCrossRefGoogle Scholar
  14. 14.
    Li X, Fu R, Liu A, Davidson VL (2008) Biochemistry 47:2908–2912PubMedCrossRefGoogle Scholar
  15. 15.
    Jensen LMR, Sanishvili R, Davidson VL, Wilmot CM (2010) Science 327:1392–1394PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Fu R, Liu F, Davidson VL, Liu A (2009) Biochemistry 48:11603–11605PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Li X, Feng M, Wang Y, Tachikawa H, Davidson VL (2006) Biochemistry 45:821–828PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Yukl ET, Goblirsch BR, Davidson VL, Wilmot CM (2011) Biochemistry 50:2931–2938PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Seidel J, Schmitt G, Hoffmann M, Jendrossek D, Einsle O (2013) Proc Natl Acad Sci USA 110:13833–13838PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Poulos TL (2014) Chem Rev. doi:10.1021/cr400415k
  21. 21.
    Braaz R, Fischer P, Jendrossek D (2004) Appl Environ Microbiol 70:7388–7395PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Hoffmann M, Seidel J, Einsle O (2009) J Mol Biol 393:951–965PubMedCrossRefGoogle Scholar
  23. 23.
    Echalier A, Goodhew CF, Pettigrew GW, Fulop V (2006) Structure 14:107–117PubMedCrossRefGoogle Scholar
  24. 24.
    Arciero DM, Hooper AB (1994) J Biol Chem 269:11878–11886PubMedGoogle Scholar
  25. 25.
    Zahn JA, Arciero DM, Hooper AB, Coats JR, DiSpirito AA (1997) Arch Microbiol 168:362–372PubMedCrossRefGoogle Scholar
  26. 26.
    Bewley KD, Ellis KE, Firer-Sherwood MA, Elliott SJ (2013) Biochim Biophys Acta 1827:938–948PubMedCrossRefGoogle Scholar
  27. 27.
    Pettigrew GW, Echalier A, Pauleta SR (2006) J Inorg Biochem 100:551–567PubMedCrossRefGoogle Scholar
  28. 28.
    Jensen LMR, Meharenna YT, Davidson VL, Poulos TL, Hedman B, Wilmot CM, Sarangi R (2012) J Biol Inorg Chem 17:1241–1255PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Fülöp V, Ridout CJ, Greenwood C, Hajdu J (1995) Structure 3:1225–1233PubMedCrossRefGoogle Scholar
  30. 30.
    Bollinger JM Jr, Matthews ML (2010) Science 327:1337–1338PubMedCrossRefGoogle Scholar
  31. 31.
    Fu R, Gupta R, Geng J, Dornevil K, Wang S, Zhang Y, Hendrich MP, Liu A (2011) J Biol Chem 286:26541–26554PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Geng J, Dornevil K, Liu A (2012) J Am Chem Soc 134:12209–12218PubMedCrossRefGoogle Scholar
  33. 33.
    Behan RK, Hoffart LM, Stone KL, Krebs C, Green MT (2006) J Am Chem Soc 128:11471–11474PubMedCrossRefGoogle Scholar
  34. 34.
    Stone KL, Hoffart LM, Behan RK, Krebs C, Green MT (2006) J Am Chem Soc 128:6147–6153PubMedCrossRefGoogle Scholar
  35. 35.
    Geng J, Liu A (2014) Arch Biochem Biophys 544:18–26PubMedCrossRefGoogle Scholar
  36. 36.
    Groves JT, Quinn R, McMurry TJ, Nakamura M, Lang G, Boso B (1985) J Am Chem Soc 107:354–360CrossRefGoogle Scholar
  37. 37.
    Bill E, Schünemann V, Trautwein AX, Weiss R, Fischer J, Tabard A, Guilard R (2002) Inorg Chim Acta 339:420–426CrossRefGoogle Scholar
  38. 38.
    Ikezaki A, Takahashi M, Nakamura M (2013) Chem Commun 49:3098–3100CrossRefGoogle Scholar
  39. 39.
    Abu Tarboush N, Jensen LMR, Feng M, Tachikawa H, Wilmot CM, Davidson VL (2010) Biochemistry 49:9783–9791PubMedCrossRefGoogle Scholar
  40. 40.
    Abu Tarboush N, Shin S, Geng J, Liu A, Davidson VL (2012) FEBS Lett 586:4339–4343PubMedCrossRefGoogle Scholar
  41. 41.
    Feng M, Jensen LMR, Yukl ET, Wei X, Liu A, Wilmot CM, Davidson VL (2012) Biochemistry 51:1598–1606PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Yukl ET, Williamson HR, Higgins L, Davidson VL, Wilmot CM (2013) Biochemistry 52:9447–9455PubMedCrossRefGoogle Scholar
  43. 43.
    Dias JM, Alves T, Bonifacio C, Pereira AS, Trincao J, Bourgeois D, Moura I, Romao MJ (2004) Structure 12:961–973PubMedCrossRefGoogle Scholar
  44. 44.
    Prazeres S, Moura JJG, Moura I, Gilmour R, Goodhew CF, Pettigrew GW, Ravi N, Huynh BH (1995) J Biol Chem 270:24264–24269PubMedCrossRefGoogle Scholar
  45. 45.
    Chen Y, Naik SG, Krzystek J, Shin S, Nelson WH, Xue S, Yang JJ, Davidson VL, Liu A (2012) Biochemistry 51:1586–1597PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Shin S, Feng M, Chen Y, Jensen LM, Tachikawa H, Wilmot CM, Liu A, Davidson VL (2011) Biochemistry 50:144–150PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Geng J, Dornevil K, Davidson VL, Liu A (2013) Proc Natl Acad Sci USA 110:9639–9644PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Lee S, Shin S, Li X, Davidson VL (2009) Biochemistry 48:2442–2447PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Badger B, Brocklehurst B (1968) Nature 219:263CrossRefGoogle Scholar
  50. 50.
    Hausser KH, Murrell JN (1957) J Chem Phys 27:500–504CrossRefGoogle Scholar
  51. 51.
    Fajer J, Borg DC, Forman A, Dolphin D, Felton RH (1970) J Am Chem Soc 92:3451–3459PubMedCrossRefGoogle Scholar
  52. 52.
    Fuhrhop JH, Wasser P, Riesner D, Mauzerall D (1972) J Am Chem Soc 94:7996–8001PubMedCrossRefGoogle Scholar
  53. 53.
    Lü JM, Rosokha SV, Kochi JK (2003) J Am Chem Soc 125:12161–12171PubMedCrossRefGoogle Scholar
  54. 54.
    Takai A, Gros CP, Barbe JM, Guilard R, Fukuzumi S (2009) Chem Eur J 15:3110–3122PubMedCrossRefGoogle Scholar
  55. 55.
    Rosokha SV, Sun D, Kochi JK (2002) J Phys Chem A 106:2283–2292CrossRefGoogle Scholar
  56. 56.
    Lindeman SV, Rosokha SV, Sun D, Kochi JK (2002) J Am Chem Soc 124:843–855PubMedCrossRefGoogle Scholar
  57. 57.
    Sun D, Rosokha SV, Lindeman SV, Kochi JK (2003) J Am Chem Soc 125:15950–15963PubMedCrossRefGoogle Scholar
  58. 58.
    Heckmann A, Lambert C (2012) Angew Chem Int Ed 51:326–392CrossRefGoogle Scholar
  59. 59.
    Song H, Orosz RD, Reed CA, Scheidt WR (1990) Inorg Chem 29:4274–4282CrossRefGoogle Scholar
  60. 60.
    Marcus RA, Sutin N (1985) Biochim Biophys Acta 811:265–322CrossRefGoogle Scholar
  61. 61.
    Kurnikov IV (2000) HARLEM. Available via http://harlem.chem.cmu.edu/index.php/Main_Page
  62. 62.
    Barry SM, Challis GL (2013) ACS Catal 3:2362–2370CrossRefGoogle Scholar
  63. 63.
    Bugg TD, Ramaswamy S (2008) Curr Opin Chem Biol 12:134–140PubMedCrossRefGoogle Scholar
  64. 64.
    Wackett LP (2002) Enzyme Microb Technol 31:577–587CrossRefGoogle Scholar
  65. 65.
    Kovaleva EG, Neibergall MB, Chakrabarty S, Lipscomb JD (2007) Acc Chem Res 40:475–483PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Chakrabarty S, Austin RN, Deng D, Groves JT, Lipscomb JD (2007) J Am Chem Soc 129:3514–3515PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Tiago de Oliveira F, Chanda A, Banerjee D, Shan X, Mondal S, Que L Jr, Bominaar EL, Münck E, Collins TJ (2007) Science 315:835–838PubMedCrossRefGoogle Scholar
  68. 68.
    Prat I, Mathieson JS, Guell M, Ribas X, Luis JM, Cronin L, Costas M (2011) Nat Chem 3:788–793PubMedCrossRefGoogle Scholar
  69. 69.
    Torres-Alacan J, Das U, Filippou AC, Vohringer P (2013) Angew Chem Int Ed 52:12833–12837CrossRefGoogle Scholar
  70. 70.
    Sono M, Roach MP, Coulter ED, Dawson JH (1996) Chem Rev 96:2841–2888PubMedCrossRefGoogle Scholar
  71. 71.
    Denisov IG, Makris TM, Sligar SG, Schlichting I (2005) Chem Rev 105:2253–2277PubMedCrossRefGoogle Scholar
  72. 72.
    Rittle J, Green MT (2010) Science 330:933–937PubMedCrossRefGoogle Scholar
  73. 73.
    Lang G, Spartalian K, Yonetani T (1976) Biochim Biophys Acta 451:250–258PubMedCrossRefGoogle Scholar
  74. 74.
    Ho PS, Hoffman BM, Kang CH, Margoliash E (1983) J Biol Chem 258:4356–4363PubMedGoogle Scholar
  75. 75.
    Lee SK, Nesheim JC, Lipscomb JD (1993) J Biol Chem 268:21569–21577PubMedGoogle Scholar
  76. 76.
    Shu L, Nesheim JC, Kauffmann K, Münck E, Lipscomb JD, Que L Jr (1997) Science 275:515–518PubMedCrossRefGoogle Scholar
  77. 77.
    Battistuzzi G, Bellei M, Bortolotti CA, Sola M (2010) Arch Biochem Biophys 500:21–36PubMedCrossRefGoogle Scholar
  78. 78.
    DeFelippis MR, Murthy CP, Faraggi M, Klapper MH (1989) Biochemistry 28:4847–4853PubMedCrossRefGoogle Scholar
  79. 79.
    Byrdin M, Villette S, Eker AP, Brettel K (2007) Biochemistry 46:10072–10077PubMedCrossRefGoogle Scholar

Copyright information

© SBIC 2014

Authors and Affiliations

  1. 1.Department of ChemistryGeorgia State UniversityAtlantaUSA

Personalised recommendations