Skip to main content
SpringerLink
Log in

Oxoiron(IV) porphyrin π-cation radical complexes with a chameleon behavior in cytochrome P450 model reactions

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

Abstract

There is an intriguing, current controversy on the involvement of multiple oxidizing species in oxygen transfer reactions by cytochromes P450 and iron porphyrin complexes. The primary evidence for the “multiple oxidants” theory was that products and/or product distributions obtained in the catalytic oxygenations were different depending on reaction conditions such as catalysts, oxidants, and solvents. In the present work, we carried out detailed mechanistic studies on competitive olefin epoxidation, alkane hydroxylation, and C=C epoxidation versus allylic C–H hydroxylation in olefin oxygenation with in situ generated oxoiron(IV) porphyrin π-cation radicals (1) under various reaction conditions. We found that the products and product distributions were markedly different depending on the reaction conditions. For example, 1 bearing different axial ligands showed different product selectivities in competitive epoxidations of cis-olefins and trans-olefins and of styrene and para-substituted styrenes. The hydroxylation of ethylbenzene by 1 afforded different products, such as 1-phenylethanol and ethylbenzoquinone, depending on the axial ligands of 1 and substrates. Moreover, the regioselectivity of C=C epoxidation versus C–H hydroxylation in the oxygenation of cyclohexene by 1 changed dramatically depending on the reaction temperatures, the electronic nature of the iron porphyrins, and substrates. These results demonstrate that 1 can exhibit diverse reactivity patterns under different reaction conditions, leading us to propose that the different products and/or product distributions observed in the catalytic oxygenation reactions by iron porphyrin models might not arise from the involvement of multiple oxidizing species but from 1 under different circumstances. This study provides strong evidence that 1 can behave like a “chameleon oxidant” that changes its reactivity and selectivity under the influence of environmental changes.

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

Fig. 1
Scheme 1
Fig. 2
Scheme 2
Scheme 3
Scheme 4
Fig. 3

Similar content being viewed by others

Abbreviations

BDE:

Bond dissociation energy

m-CPBA:

m-Chloroperbenzoic acid

CYP 450:

Cytochrome P450

EB:

Ethylbenzene

EB-d10:

Ethylbenzene-d10

EB-para-Br:

1-Bromo-4-ethylbenzene

GC:

Gas chromatography

GC-MS:

Gas chromatography–mass spectrometry

HPLC:

High performance liquid chromatography

KIE:

Kinetic isotope effect

TDCPP:

meso-Tetrakis(2,6-dichlorophenyl)porphyrin dianion

TDFPP:

meso-Tetrakis(2,6-difluorophenyl)porphyrin dianion

TDMPP:

meso-Tetrakis(2,6-dimethylphenyl)porphyrin dianion

TMP:

meso-Tetramesitylporphyrin dianion

TPFPP:

meso-Tetrakis(pentafluorophenyl)porphyrin dianion

References

  1. Meunier B, de Visser SP, Shaik S (2004) Chem Rev 104:3947–3980

    Google Scholar 

  2. Nam W (2003) In: Que L, Tolman WB (eds) Comprehensive coordination chemistry II, vol 8. Elsevier, Oxford, pp 281–307

  3. McLain J, Lee J, Groves JT (2000) In: Meunier B (ed) Biomimetic oxidations catalyzed by transition metal complexes. Imperial College Press, London, pp 91–169

  4. Sono M, Roach MP, Coulter ED, Dawson JH (1996) Chem Rev 96:2841–2887

    Article  CAS  PubMed  Google Scholar 

  5. Ortiz de Montellano PR (ed) (1995) Cytochrome P450: structure, mechanism, and biochemistry, 2nd edn. Plenum, New York

    Google Scholar 

  6. Traylor TG, Traylor PS (1995) In: Valentine JS, Foote CS, Greenberg A, Liebman JF (eds) Active oxygen in biochemistry. Blackie Academic and Professional, Chapman & Hall, London, pp 84–187

  7. Jin S, Bryson TA, Dawson JH (2004) J Biol Inorg Chem 9:644–653

    Google Scholar 

  8. Nam W, Ryu YO, Song WJ (2004) J Biol Inorg Chem 9:654–660

    Google Scholar 

  9. Shaik S, de Visser SP, Kumar D (2004) J Biol Inorg Chem 9:661–668

    Google Scholar 

  10. Hlavica P (2004) Eur J Biochem 271:4335–4360

    Google Scholar 

  11. Groves JT (2003) Proc Natl Acad Sci USA 100:3569–3574

    Article  CAS  PubMed  Google Scholar 

  12. Newcomb M, Hollenberg PF, Coon MJ (2003) Arch Biochem Biophys 409:72–79

    Article  CAS  PubMed  Google Scholar 

  13. Coon MJ (2003) Biochem Biophys Res Commun 312:163–168

    Google Scholar 

  14. Ortiz de Montellano PR, De Voss JJ (2002) Nat Prod Rep 19:477–493

    Article  PubMed  Google Scholar 

  15. Watanabe Y (2001) J Biol Inorg Chem 6:846–856

    Article  CAS  PubMed  Google Scholar 

  16. Vaz ADN, Pernecky SJ, Raner GM, Coon MJ (1996) Proc Natl Acad Sci USA 93:4644–4648

    Article  CAS  PubMed  Google Scholar 

  17. Vaz ADN, McGinnity DF, Coon MJ (1998) Proc Natl Acad Sci USA 95:3555–3560

    Article  CAS  PubMed  Google Scholar 

  18. Vatsis KP, Coon MJ (2002) Arch Biochem Biophys 397:119–129

    Article  CAS  PubMed  Google Scholar 

  19. Newcomb M, Toy PH (2000) Acc Chem Res 33:449–455

    Article  CAS  PubMed  Google Scholar 

  20. Toy PH, Newcomb M, Coon MJ, Vaz ADN (1998) J Am Chem Soc 120:9718–9719

    Article  CAS  Google Scholar 

  21. Newcomb M, Shen R, Choi SY, Toy PH, Hollenberg PF, Vaz ADN, Coon MJ (2000) J Am Chem Soc 122:2677–2686

    Article  CAS  Google Scholar 

  22. Newcomb M, Shen R, Lu Y, Coon MJ, Hollenberg PF, Kopp DA, Lippard SJ (2002) J Am Chem Soc 124:6879–6886

    Article  CAS  PubMed  Google Scholar 

  23. Newcomb M, Aebisher D, Shen R, Chandrasena REP, Hollenberg PF, Coon MJ (2003) J Am Chem Soc 125:6064–6065

    Article  CAS  PubMed  Google Scholar 

  24. Chandrasena REP, Vatsis KP, Coon MJ, Hollenberg PF, Newcomb M (2004) J Am Chem Soc 126:115–126

    CAS  PubMed  Google Scholar 

  25. Jin S, Makris TM, Bryson TA, Sligar SG, Dawson JH (2003) J Am Chem Soc 125:3406–3407

    Article  CAS  PubMed  Google Scholar 

  26. Volz TJ, Rock DA, Jones JP (2002) J Am Chem Soc 124:9724–9725

    Article  CAS  PubMed  Google Scholar 

  27. Nam W, Lim MH, Lee HJ, Kim C (2000) J Am Chem Soc 122:6641–6647

    Article  CAS  Google Scholar 

  28. Nam W, Lim MH, Moon SK, Kim C (2000) J Am Chem Soc 122:10805–10809

    Article  CAS  Google Scholar 

  29. Nam W, Lee HJ, Oh SY, Kim C, Jang HG (2000) J Inorg Biochem 80:219–225

    Article  CAS  PubMed  Google Scholar 

  30. Nam W, Jin SW, Lim MH, Ryu JY, Kim C (2002) Inorg Chem 41:3647–3652

    Article  CAS  PubMed  Google Scholar 

  31. Machii K, Watanabe Y, Morishima I (1995) J Am Chem Soc 117:6691–6697

    CAS  Google Scholar 

  32. Collman JP, Chien AS, Eberspacher TA, Brauman JI (2000) J Am Chem Soc 122:11098–11100

    Article  CAS  Google Scholar 

  33. Wadhwani P, Mukherjee M, Bandyopadhyay D (2001) J Am Chem Soc 123:12430–12431

    Article  CAS  PubMed  Google Scholar 

  34. Suzuki N, Higuchi T, Nagano T (2002) J Am Chem Soc 124:9622–9628

    Article  CAS  PubMed  Google Scholar 

  35. Adam W, Roschmann KJ, Saha-Möller CR, Seebach D (2002) J Am Chem Soc 124:5068–5073

    Article  CAS  PubMed  Google Scholar 

  36. Collman JP, Zeng L, Decréau RA (2003) Chem Commun :2974–2975

    Google Scholar 

  37. Collman JP, Zeng L, Brauman JI (2004) Inorg Chem 43:2672–2679

    Article  CAS  PubMed  Google Scholar 

  38. Wang SH, Mandimutsira BS, Todd R, Ramdhanie B, Fox JP, Goldberg DP (2004) J Am Chem Soc 126:18–19

    CAS  PubMed  Google Scholar 

  39. Shaik S, Cohen S, de Visser SP, Sharma PK, Kumar D, Kozuch S, Ogliaro F, Danovich D (2004) Eur J Inorg Chem 2:207–226

    Google Scholar 

  40. Shaik S, de Visser SP, Ogliaro F, Schwarz H, Schröder D (2002) Curr Opin Chem Biol 6:556–567

    Google Scholar 

  41. Schröder D, Shaik S, Schwarz H (2000) Acc Chem Res 33:139–145

    Google Scholar 

  42. Ogliaro F, de Visser SP, Cohen S, Sharma PK, Shaik S (2002) J Am Chem Soc 124:2806–2817

    Article  CAS  PubMed  Google Scholar 

  43. Kamachi T, Shiota Y, Ohta T, Yoshizawa K (2003) Bull Chem Soc Jpn 76:721–732

    Article  CAS  Google Scholar 

  44. Sharma PK, de Visser SP, Shaik S (2003) J Am Chem Soc 125:8698–8699

    Article  CAS  PubMed  Google Scholar 

  45. Schöneboom JC, Cohen S, Lin H, Shaik S, Thiel W (2004) J Am Chem Soc 126:4017–4034

    Article  PubMed  Google Scholar 

  46. Dowers TS, Rock DA, Rock DA, Jones JP (2004) J Am Chem Soc 126:8868–8869

    Google Scholar 

  47. Auclair K, Hu Z, Little DM, Ortiz de Montellano PR, Groves JT (2002) J Am Chem Soc 124:6020–6027

    Article  CAS  PubMed  Google Scholar 

  48. He X, Ortiz de Montellano PR (2004) J Biol Chem 279:39479–39484

    Google Scholar 

  49. Pratt JM, Ridd TI, King LJ (1995) J Chem Soc Chem Commun 2297–2298

  50. Lindsey JS, Wagner RW (1989) J Org Chem 54:828–836

    Google Scholar 

  51. Jockers R, Schmid RD, Rieger H, Krohn K (1991) Liebigs Ann Chem 315–321

  52. The reaction of Fe(TPFPP)Cl with m-CPBA in a solvent mixture of CH3CN and CH2Cl2 (1:1) at −40°C did not form 3-A but (TPFPP)FeIV=O. Lowering the reaction temperature to −80°C and changing the solvent mixture to CH2Cl2 allowed us to generate and use 3-A directly in reactivity studies

  53. Nam W, Lim MH, Oh SY, Lee JH, Lee HJ, Woo SK, Kim C, Shin W (2000) Angew Chem Int Ed 39:3646–3649

    Article  Google Scholar 

  54. It has been well demonstrated that when oxoiron(IV) porphyrin π-cation radicals are generated by reacting iron(III) porphyrin complexes and m-CPBA, the axial ligand present in the starting iron(III) porphyrins is retained in the intermediates

  55. Wolter T, Meyer-Klaucke W, Müther M, Mandon D, Winkler H, Trautwein AX, Weiss R (2000) J Inorg Biochem 78:117–122

    Google Scholar 

  56. Fujii H, Yoshimura T, Kamada H (1997) Inorg Chem 36:6142–6143

    Google Scholar 

  57. Czarnecki K, Nimri S, Gross Z, Proniewicz LM, Kincaid JR (1996) J Am Chem Soc 118:2929–2935

    Google Scholar 

  58. The cis-olefin selectivity resulted from the steric effect of porphyrin ligands has been reported previously

  59. Groves JT, Nemo TE (1983) J Am Chem Soc 105:5786–5791

    CAS  Google Scholar 

  60. Hammett ρ+ value of −1.9 was reported in the kinetic studies of [(TMP)+· FeIV=O]+ and styrens, whereas Hammett ρ+ value of −0.9 was determined in the catalytic competitive epoxidation of styrene and para-substituted styrenes by iron(III) porphyrin chlorides and PhIO. The different Hammett ρ+ values observed previously are now rationalized with the axial ligand effect discussed in this paper

  61. Groves JT, Watanabe Y (1986) J Am Chem Soc 108:507–508

    Google Scholar 

  62. Lindsay Smith JR, Sleath PR (1982) J Chem Soc Perkin Trans II :1009–1015

    Google Scholar 

  63. Traylor TG, Xu F (1988) J Am Chem Soc 110:1953–1958

    Google Scholar 

  64. Gross Z, Nimri S (1994) Inorg Chem 33:1731–1732

    CAS  Google Scholar 

  65. Gross Z, Nimri S, Barzilay CM, Simkhovich L (1997) J Biol Inorg Chem 2:492–506

    Google Scholar 

  66. The formation of quinone product has been often observed in the hydroxylation of aromatic compounds by metalloporphyrins

  67. Song R, Sorokin A, Bernadou J, Meunier B (1997) J Org Chem 62:673–678

    Google Scholar 

  68. Khavasi HR, Davarani SSH, Safari N (2002) J Mol Catal A Chem 188:115–122

    Google Scholar 

  69. Atkinson JK, Hollenberg PF, Ingold KU, Johnson CC, Le Tadic MH, Newcomb M, Putt DA (1994) Biochemistry 33:10630–10637

    Google Scholar 

  70. Kumar D, de Visser SP, Sharma PK, Cohen S, Shaik S (2004) J Am Chem Soc 126:1907–1920

    CAS  PubMed  Google Scholar 

  71. Kumar D, de Visser SP, Shaik S (2003) J Am Chem Soc 125:13024–13025

    Article  CAS  PubMed  Google Scholar 

  72. Ogliaro F, Filatov M, Shaik S (2000) Eur J Inorg Chem 12:2455–2458

    Google Scholar 

  73. Martinis SA, Atkins WM, Stayton PS, Sligar SG (1989) J Am Chem Soc 111:9252–9253

    CAS  Google Scholar 

  74. Imai M, Shimada H, Watanabe Y, Matsushima-Hibiya Y, Makino R, Koga H, Horiuchi T, Ishimura Y (1989) Proc Natl Acad Sci USA 86:7823–7827

    CAS  PubMed  Google Scholar 

  75. Vidakovic M, Sligar SG, Li H, Poulos TL (1998) Biochemistry 37:9211–9219

    Google Scholar 

  76. Groves JT, Gross Z, Stern MK (1995) In: Kessissoglon DP (ed) Bioinorganic chemistry: an inorganic perspective of life. NATO Advanced Study Institute Series 459. Kluwer, The Netherlands, pp39–47

  77. Farinas ET, Alcalde M, Arnold F (2004) Tetrahedron 60:525–528

    Google Scholar 

  78. Lim MH, Jin SW, Lee YJ, Jhon GJ, Nam W, Kim C (2001) Bull Korean Chem Soc 22:93–96

    Google Scholar 

  79. Ohno T, Suzuki N, Dokoh T, Urano Y, Kikuchi K, Hirobe M, Higuchi T, Nagano T (2000) J Inorg Biochem 82:123–125

    Google Scholar 

  80. Bartoli JF, Brigaud O, Battioni P, Mansuy D (1991) J Chem Soc Chem Commun :440–442

    Google Scholar 

  81. Ruettinger RT, Fulco AJ (1981) J Biol Chem 256:5728–5734

    Google Scholar 

  82. Traylor TG, Kim C, Richards JL, Xu F, Perrin CL (1995) J Am Chem Soc 117:3468–3474

    Google Scholar 

  83. A reviewer suggested that the high reactivity of allylic C–H bonds of cyclohexene, compared to those of cyclooctene, is due to that the allylic C–H bonds are parallel to the π-bond of olefin

  84. de Visser SP, Ogliaro F, Sharma PK, Shaik S (2002) J Am Chem Soc 124:11809–11826

    Article  PubMed  Google Scholar 

  85. de Visser SP, Ogliaro F, Sharma PK, Shaik S (2002) Angew Chem Int Ed 41:1947–1951

    Article  Google Scholar 

  86. Shaik S, de Visser SP, Kumar D (2004) J Am Chem Soc 126:11746–11749

    Article  Google Scholar 

  87. Groves JT, Haushalter RC, Nakamura M, Nemo TE, Evans BJ (1981) J Am Chem Soc 103:2884–2886

    CAS  Google Scholar 

  88. Davydov R, Perera R, Jin S, Yang TC, Bryson TA, Sono M, Dawson JH, Hoffman BM (2005) J Am Chem Soc 127:1403–1413

    Google Scholar 

Download references

Acknowledgement

This research was supported by the Ministry of Science and Technology of Korea through the Creative Research Initiative Program.

Author information

Authors and Affiliations

  1. Division of Nano Sciences, and Center for Biomimetic Systems, Department of Chemistry, Ewha Womans University, Seoul, 120-750, Korea

    Woon Ju Song, Yon Ok Ryu, Rita Song & Wonwoo Nam

Authors
  1. Woon Ju Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yon Ok Ryu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rita Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wonwoo Nam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wonwoo Nam.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Song, W.J., Ryu, Y.O., Song, R. et al. Oxoiron(IV) porphyrin π-cation radical complexes with a chameleon behavior in cytochrome P450 model reactions. J Biol Inorg Chem 10, 294–304 (2005). https://doi.org/10.1007/s00775-005-0641-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-005-0641-9

Keywords

Search

Navigation