Skip to main content
SpringerLink
Log in

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

  • Minireview
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

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.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Minnihan EC, Nocera DG, Stubbe J (2013) Acc Chem Res 46:2524–2535

    Article  PubMed  CAS  Google Scholar 

  2. Abu Tarboush N, Jensen LMR, Yukl ET, Geng J, Liu A, Wilmot CM, Davidson VL (2011) Proc Natl Acad Sci USA 108:16956–16961

    Article  Google Scholar 

  3. Gray HB, Winkler JR (2010) Biochim Biophys Acta 1797:1563–1572

    Article  PubMed  CAS  Google Scholar 

  4. Warren JJ, Ener ME, Vlček A Jr, Winkler JR, Gray HB (2012) Coord Chem Rev 256:2478–2487

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  5. McIntire WS, Wemmer DE, Chistoserdov A, Lidstrom ME (1991) Science 252:817–824

    Article  PubMed  CAS  Google Scholar 

  6. Eady RR, Large PJ (1968) Biochem J 106:245–255

    PubMed  CAS  PubMed Central  Google Scholar 

  7. Chen L, Doi M, Durley RC, Chistoserdov AY, Lidstrom ME, Davidson VL, Mathews FS (1998) J Mol Biol 276:131–149

    Article  PubMed  CAS  Google Scholar 

  8. Wang Y, Graichen ME, Liu A, Pearson AR, Wilmot CM, Davidson VL (2003) Biochemistry 42:7318–7325

    Article  PubMed  CAS  Google Scholar 

  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 43:5494–5502

    Article  PubMed  CAS  Google Scholar 

  10. Yukl ET, Liu F, Krzystek J, Shin S, Jensen LMR, Davidson VL, Wilmot CM, Liu A (2013) Proc Natl Acad Sci USA 110:4569–4573

    Article  PubMed  PubMed Central  Google Scholar 

  11. Li X, Jones LH, Pearson AR, Wilmot CM, Davidson VL (2006) Biochemistry 45:13276–13283

    Article  PubMed  CAS  Google Scholar 

  12. Li X, Fu R, Lee S, Krebs C, Davidson VL, Liu A (2008) Proc Natl Acad Sci USA 105:8597–8600

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  13. Chistoserdov AY, Boyd J, Mathews FS, Lidstrom ME (1992) Biochem Biophys Res Commun 184:1181–1189

    Article  PubMed  CAS  Google Scholar 

  14. Li X, Fu R, Liu A, Davidson VL (2008) Biochemistry 47:2908–2912

    Article  PubMed  CAS  Google Scholar 

  15. Jensen LMR, Sanishvili R, Davidson VL, Wilmot CM (2010) Science 327:1392–1394

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  16. Fu R, Liu F, Davidson VL, Liu A (2009) Biochemistry 48:11603–11605

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  17. Li X, Feng M, Wang Y, Tachikawa H, Davidson VL (2006) Biochemistry 45:821–828

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  18. Yukl ET, Goblirsch BR, Davidson VL, Wilmot CM (2011) Biochemistry 50:2931–2938

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  19. Seidel J, Schmitt G, Hoffmann M, Jendrossek D, Einsle O (2013) Proc Natl Acad Sci USA 110:13833–13838

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  20. Poulos TL (2014) Chem Rev. doi:10.1021/cr400415k

  21. Braaz R, Fischer P, Jendrossek D (2004) Appl Environ Microbiol 70:7388–7395

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  22. Hoffmann M, Seidel J, Einsle O (2009) J Mol Biol 393:951–965

    Article  PubMed  CAS  Google Scholar 

  23. Echalier A, Goodhew CF, Pettigrew GW, Fulop V (2006) Structure 14:107–117

    Article  PubMed  CAS  Google Scholar 

  24. Arciero DM, Hooper AB (1994) J Biol Chem 269:11878–11886

    PubMed  CAS  Google Scholar 

  25. Zahn JA, Arciero DM, Hooper AB, Coats JR, DiSpirito AA (1997) Arch Microbiol 168:362–372

    Article  PubMed  CAS  Google Scholar 

  26. Bewley KD, Ellis KE, Firer-Sherwood MA, Elliott SJ (2013) Biochim Biophys Acta 1827:938–948

    Article  PubMed  CAS  Google Scholar 

  27. Pettigrew GW, Echalier A, Pauleta SR (2006) J Inorg Biochem 100:551–567

    Article  PubMed  CAS  Google Scholar 

  28. Jensen LMR, Meharenna YT, Davidson VL, Poulos TL, Hedman B, Wilmot CM, Sarangi R (2012) J Biol Inorg Chem 17:1241–1255

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  29. Fülöp V, Ridout CJ, Greenwood C, Hajdu J (1995) Structure 3:1225–1233

    Article  PubMed  Google Scholar 

  30. Bollinger JM Jr, Matthews ML (2010) Science 327:1337–1338

    Article  PubMed  CAS  Google Scholar 

  31. Fu R, Gupta R, Geng J, Dornevil K, Wang S, Zhang Y, Hendrich MP, Liu A (2011) J Biol Chem 286:26541–26554

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  32. Geng J, Dornevil K, Liu A (2012) J Am Chem Soc 134:12209–12218

    Article  PubMed  CAS  Google Scholar 

  33. Behan RK, Hoffart LM, Stone KL, Krebs C, Green MT (2006) J Am Chem Soc 128:11471–11474

    Article  PubMed  CAS  Google Scholar 

  34. Stone KL, Hoffart LM, Behan RK, Krebs C, Green MT (2006) J Am Chem Soc 128:6147–6153

    Article  PubMed  CAS  Google Scholar 

  35. Geng J, Liu A (2014) Arch Biochem Biophys 544:18–26

    Article  PubMed  CAS  Google Scholar 

  36. Groves JT, Quinn R, McMurry TJ, Nakamura M, Lang G, Boso B (1985) J Am Chem Soc 107:354–360

    Article  CAS  Google Scholar 

  37. Bill E, Schünemann V, Trautwein AX, Weiss R, Fischer J, Tabard A, Guilard R (2002) Inorg Chim Acta 339:420–426

    Article  CAS  Google Scholar 

  38. Ikezaki A, Takahashi M, Nakamura M (2013) Chem Commun 49:3098–3100

    Article  CAS  Google Scholar 

  39. Abu Tarboush N, Jensen LMR, Feng M, Tachikawa H, Wilmot CM, Davidson VL (2010) Biochemistry 49:9783–9791

    Article  PubMed  CAS  Google Scholar 

  40. Abu Tarboush N, Shin S, Geng J, Liu A, Davidson VL (2012) FEBS Lett 586:4339–4343

    Article  PubMed  CAS  Google Scholar 

  41. Feng M, Jensen LMR, Yukl ET, Wei X, Liu A, Wilmot CM, Davidson VL (2012) Biochemistry 51:1598–1606

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  42. Yukl ET, Williamson HR, Higgins L, Davidson VL, Wilmot CM (2013) Biochemistry 52:9447–9455

    Article  PubMed  CAS  Google Scholar 

  43. Dias JM, Alves T, Bonifacio C, Pereira AS, Trincao J, Bourgeois D, Moura I, Romao MJ (2004) Structure 12:961–973

    Article  PubMed  CAS  Google Scholar 

  44. Prazeres S, Moura JJG, Moura I, Gilmour R, Goodhew CF, Pettigrew GW, Ravi N, Huynh BH (1995) J Biol Chem 270:24264–24269

    Article  PubMed  CAS  Google Scholar 

  45. Chen Y, Naik SG, Krzystek J, Shin S, Nelson WH, Xue S, Yang JJ, Davidson VL, Liu A (2012) Biochemistry 51:1586–1597

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  46. Shin S, Feng M, Chen Y, Jensen LM, Tachikawa H, Wilmot CM, Liu A, Davidson VL (2011) Biochemistry 50:144–150

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  47. Geng J, Dornevil K, Davidson VL, Liu A (2013) Proc Natl Acad Sci USA 110:9639–9644

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  48. Lee S, Shin S, Li X, Davidson VL (2009) Biochemistry 48:2442–2447

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  49. Badger B, Brocklehurst B (1968) Nature 219:263

    Article  CAS  Google Scholar 

  50. Hausser KH, Murrell JN (1957) J Chem Phys 27:500–504

    Article  CAS  Google Scholar 

  51. Fajer J, Borg DC, Forman A, Dolphin D, Felton RH (1970) J Am Chem Soc 92:3451–3459

    Article  PubMed  CAS  Google Scholar 

  52. Fuhrhop JH, Wasser P, Riesner D, Mauzerall D (1972) J Am Chem Soc 94:7996–8001

    Article  PubMed  CAS  Google Scholar 

  53. Lü JM, Rosokha SV, Kochi JK (2003) J Am Chem Soc 125:12161–12171

    Article  PubMed  Google Scholar 

  54. Takai A, Gros CP, Barbe JM, Guilard R, Fukuzumi S (2009) Chem Eur J 15:3110–3122

    Article  PubMed  CAS  Google Scholar 

  55. Rosokha SV, Sun D, Kochi JK (2002) J Phys Chem A 106:2283–2292

    Article  CAS  Google Scholar 

  56. Lindeman SV, Rosokha SV, Sun D, Kochi JK (2002) J Am Chem Soc 124:843–855

    Article  PubMed  CAS  Google Scholar 

  57. Sun D, Rosokha SV, Lindeman SV, Kochi JK (2003) J Am Chem Soc 125:15950–15963

    Article  PubMed  CAS  Google Scholar 

  58. Heckmann A, Lambert C (2012) Angew Chem Int Ed 51:326–392

    Article  CAS  Google Scholar 

  59. Song H, Orosz RD, Reed CA, Scheidt WR (1990) Inorg Chem 29:4274–4282

    Article  CAS  Google Scholar 

  60. Marcus RA, Sutin N (1985) Biochim Biophys Acta 811:265–322

    Article  CAS  Google Scholar 

  61. Kurnikov IV (2000) HARLEM. Available via http://harlem.chem.cmu.edu/index.php/Main_Page

  62. Barry SM, Challis GL (2013) ACS Catal 3:2362–2370

    Article  CAS  Google Scholar 

  63. Bugg TD, Ramaswamy S (2008) Curr Opin Chem Biol 12:134–140

    Article  PubMed  CAS  Google Scholar 

  64. Wackett LP (2002) Enzyme Microb Technol 31:577–587

    Article  CAS  Google Scholar 

  65. Kovaleva EG, Neibergall MB, Chakrabarty S, Lipscomb JD (2007) Acc Chem Res 40:475–483

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  66. Chakrabarty S, Austin RN, Deng D, Groves JT, Lipscomb JD (2007) J Am Chem Soc 129:3514–3515

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  67. Tiago de Oliveira F, Chanda A, Banerjee D, Shan X, Mondal S, Que L Jr, Bominaar EL, Münck E, Collins TJ (2007) Science 315:835–838

    Article  PubMed  CAS  Google Scholar 

  68. Prat I, Mathieson JS, Guell M, Ribas X, Luis JM, Cronin L, Costas M (2011) Nat Chem 3:788–793

    Article  PubMed  CAS  Google Scholar 

  69. Torres-Alacan J, Das U, Filippou AC, Vohringer P (2013) Angew Chem Int Ed 52:12833–12837

    Article  CAS  Google Scholar 

  70. Sono M, Roach MP, Coulter ED, Dawson JH (1996) Chem Rev 96:2841–2888

    Article  PubMed  CAS  Google Scholar 

  71. Denisov IG, Makris TM, Sligar SG, Schlichting I (2005) Chem Rev 105:2253–2277

    Article  PubMed  CAS  Google Scholar 

  72. Rittle J, Green MT (2010) Science 330:933–937

    Article  PubMed  CAS  Google Scholar 

  73. Lang G, Spartalian K, Yonetani T (1976) Biochim Biophys Acta 451:250–258

    Article  PubMed  CAS  Google Scholar 

  74. Ho PS, Hoffman BM, Kang CH, Margoliash E (1983) J Biol Chem 258:4356–4363

    PubMed  CAS  Google Scholar 

  75. Lee SK, Nesheim JC, Lipscomb JD (1993) J Biol Chem 268:21569–21577

    PubMed  CAS  Google Scholar 

  76. Shu L, Nesheim JC, Kauffmann K, Münck E, Lipscomb JD, Que L Jr (1997) Science 275:515–518

    Article  PubMed  CAS  Google Scholar 

  77. Battistuzzi G, Bellei M, Bortolotti CA, Sola M (2010) Arch Biochem Biophys 500:21–36

    Article  PubMed  CAS  Google Scholar 

  78. DeFelippis MR, Murthy CP, Faraggi M, Klapper MH (1989) Biochemistry 28:4847–4853

    Article  PubMed  CAS  Google Scholar 

  79. Byrdin M, Villette S, Eker AP, Brettel K (2007) Biochemistry 46:10072–10077

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The work in the Liu laboratory at Georgia State University on this project has been supported by National Science Foundation grants MCB-0843537 and CHE-1309942, and the Georgia Research Alliance Distinguished Scientist Program (A.L.). We also acknowledge the Molecular Basis of Disease Area of Focus graduate fellowship support to J.G. and the Center for Diagnostics and Therapeutics fellowship support to F.L..

Author information

Authors and Affiliations

  1. Department of Chemistry, Georgia State University, Atlanta, GA, 30303, USA

    Jiafeng Geng, Ian Davis, Fange Liu & Aimin Liu

Authors
  1. Jiafeng Geng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ian Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fange Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aimin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aimin Liu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Geng, J., Davis, I., Liu, F. et al. Bis-Fe(IV): nature’s sniper for long-range oxidation. J Biol Inorg Chem 19, 1057–1067 (2014). https://doi.org/10.1007/s00775-014-1123-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-014-1123-8

Keywords

Search

Navigation