Stalking intermediates in oxygen activation by iron enzymes: Motivation and method

Research output: Contribution to journalReview article

101 Citations (Scopus)

Abstract

The study of high-valent-iron enzyme intermediates began in the mid-1900s with the discovery of compounds I (or ES) and II in the heme peroxidases, progressed to non-heme-diiron enzymes in the 1990s with the detection and characterization of the FeIII-FeIV complex, X, and the FeIV-FeIV complex, Q, in O2 activation by ribonucleotide reductase R2 (RNR-R2) and soluble methane monooxygenase (sMMO), respectively, and was most recently extended to mononuclear non-heme-iron oxygenases with the trapping and spectroscopic characterization of the FeIV-oxo intermediate, J, in the reaction of taurine:α-ketoglutarate dioxygenase (TauD). Individually, each of these landmark studies helped reveal the chemical logic of that particular enzyme system. Collectively, they have significantly advanced our understanding of Nature's strategies for oxidative transformation of biomolecules (both natural and "xenobiotic"). With high-valent complexes now having been described in representatives of three major classes of iron enzymes, it is an appropriate time to ask whether and what additional insights might be gleaned from further stalking of related intermediates in other systems. In this review, we advocate that there is still much to be learned from this pursuit and summarize the insight provided by two of the landmark discoveries mentioned above (the latter two) and the subsequent studies that they spurred to support our contention. In addition, we attempt to provide, to the extent that it is possible to do so, a "how-to" guide for detection and characterization of such intermediates, focusing primarily on enzymes in which they form by activation of molecular oxygen. In this latter objective, we have drawn from an earlier review by Johnson (Enzymes, third ed. vol. 20, 1992, pp. 1-61) covering, more generally, dissection of enzyme reaction pathways by transient-state kinetic methods. That work elegantly illustrated that, although it may be impossible to develop a true algorithm for the process, a synthesis of guidelines and general principles can be of considerable value.

Original languageEnglish (US)
Pages (from-to)586-605
Number of pages20
JournalJournal of Inorganic Biochemistry
Volume100
Issue number4
DOIs
StatePublished - Apr 1 2006

Fingerprint

Stalking
Enzyme Activation
Motivation
Iron
Chemical activation
Oxygen
Enzymes
methane monooxygenase
Ribonucleotide Reductases
Peroxidases
Dioxygenases
Dissection
Oxygenases
Molecular oxygen
Taurine
Biomolecules
Xenobiotics
Heme
Guidelines
Kinetics

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Inorganic Chemistry

Cite this

@article{5c166686bd2241cfb061fa8dbf6c7ca1,
title = "Stalking intermediates in oxygen activation by iron enzymes: Motivation and method",
abstract = "The study of high-valent-iron enzyme intermediates began in the mid-1900s with the discovery of compounds I (or ES) and II in the heme peroxidases, progressed to non-heme-diiron enzymes in the 1990s with the detection and characterization of the FeIII-FeIV complex, X, and the FeIV-FeIV complex, Q, in O2 activation by ribonucleotide reductase R2 (RNR-R2) and soluble methane monooxygenase (sMMO), respectively, and was most recently extended to mononuclear non-heme-iron oxygenases with the trapping and spectroscopic characterization of the FeIV-oxo intermediate, J, in the reaction of taurine:α-ketoglutarate dioxygenase (TauD). Individually, each of these landmark studies helped reveal the chemical logic of that particular enzyme system. Collectively, they have significantly advanced our understanding of Nature's strategies for oxidative transformation of biomolecules (both natural and {"}xenobiotic{"}). With high-valent complexes now having been described in representatives of three major classes of iron enzymes, it is an appropriate time to ask whether and what additional insights might be gleaned from further stalking of related intermediates in other systems. In this review, we advocate that there is still much to be learned from this pursuit and summarize the insight provided by two of the landmark discoveries mentioned above (the latter two) and the subsequent studies that they spurred to support our contention. In addition, we attempt to provide, to the extent that it is possible to do so, a {"}how-to{"} guide for detection and characterization of such intermediates, focusing primarily on enzymes in which they form by activation of molecular oxygen. In this latter objective, we have drawn from an earlier review by Johnson (Enzymes, third ed. vol. 20, 1992, pp. 1-61) covering, more generally, dissection of enzyme reaction pathways by transient-state kinetic methods. That work elegantly illustrated that, although it may be impossible to develop a true algorithm for the process, a synthesis of guidelines and general principles can be of considerable value.",
author = "Bollinger, {J. Martin} and Carsten Krebs",
year = "2006",
month = "4",
day = "1",
doi = "10.1016/j.jinorgbio.2006.01.022",
language = "English (US)",
volume = "100",
pages = "586--605",
journal = "Journal of Inorganic Biochemistry",
issn = "0162-0134",
publisher = "Elsevier Inc.",
number = "4",

}

Stalking intermediates in oxygen activation by iron enzymes : Motivation and method. / Bollinger, J. Martin; Krebs, Carsten.

In: Journal of Inorganic Biochemistry, Vol. 100, No. 4, 01.04.2006, p. 586-605.

Research output: Contribution to journalReview article

TY - JOUR

T1 - Stalking intermediates in oxygen activation by iron enzymes

T2 - Motivation and method

AU - Bollinger, J. Martin

AU - Krebs, Carsten

PY - 2006/4/1

Y1 - 2006/4/1

N2 - The study of high-valent-iron enzyme intermediates began in the mid-1900s with the discovery of compounds I (or ES) and II in the heme peroxidases, progressed to non-heme-diiron enzymes in the 1990s with the detection and characterization of the FeIII-FeIV complex, X, and the FeIV-FeIV complex, Q, in O2 activation by ribonucleotide reductase R2 (RNR-R2) and soluble methane monooxygenase (sMMO), respectively, and was most recently extended to mononuclear non-heme-iron oxygenases with the trapping and spectroscopic characterization of the FeIV-oxo intermediate, J, in the reaction of taurine:α-ketoglutarate dioxygenase (TauD). Individually, each of these landmark studies helped reveal the chemical logic of that particular enzyme system. Collectively, they have significantly advanced our understanding of Nature's strategies for oxidative transformation of biomolecules (both natural and "xenobiotic"). With high-valent complexes now having been described in representatives of three major classes of iron enzymes, it is an appropriate time to ask whether and what additional insights might be gleaned from further stalking of related intermediates in other systems. In this review, we advocate that there is still much to be learned from this pursuit and summarize the insight provided by two of the landmark discoveries mentioned above (the latter two) and the subsequent studies that they spurred to support our contention. In addition, we attempt to provide, to the extent that it is possible to do so, a "how-to" guide for detection and characterization of such intermediates, focusing primarily on enzymes in which they form by activation of molecular oxygen. In this latter objective, we have drawn from an earlier review by Johnson (Enzymes, third ed. vol. 20, 1992, pp. 1-61) covering, more generally, dissection of enzyme reaction pathways by transient-state kinetic methods. That work elegantly illustrated that, although it may be impossible to develop a true algorithm for the process, a synthesis of guidelines and general principles can be of considerable value.

AB - The study of high-valent-iron enzyme intermediates began in the mid-1900s with the discovery of compounds I (or ES) and II in the heme peroxidases, progressed to non-heme-diiron enzymes in the 1990s with the detection and characterization of the FeIII-FeIV complex, X, and the FeIV-FeIV complex, Q, in O2 activation by ribonucleotide reductase R2 (RNR-R2) and soluble methane monooxygenase (sMMO), respectively, and was most recently extended to mononuclear non-heme-iron oxygenases with the trapping and spectroscopic characterization of the FeIV-oxo intermediate, J, in the reaction of taurine:α-ketoglutarate dioxygenase (TauD). Individually, each of these landmark studies helped reveal the chemical logic of that particular enzyme system. Collectively, they have significantly advanced our understanding of Nature's strategies for oxidative transformation of biomolecules (both natural and "xenobiotic"). With high-valent complexes now having been described in representatives of three major classes of iron enzymes, it is an appropriate time to ask whether and what additional insights might be gleaned from further stalking of related intermediates in other systems. In this review, we advocate that there is still much to be learned from this pursuit and summarize the insight provided by two of the landmark discoveries mentioned above (the latter two) and the subsequent studies that they spurred to support our contention. In addition, we attempt to provide, to the extent that it is possible to do so, a "how-to" guide for detection and characterization of such intermediates, focusing primarily on enzymes in which they form by activation of molecular oxygen. In this latter objective, we have drawn from an earlier review by Johnson (Enzymes, third ed. vol. 20, 1992, pp. 1-61) covering, more generally, dissection of enzyme reaction pathways by transient-state kinetic methods. That work elegantly illustrated that, although it may be impossible to develop a true algorithm for the process, a synthesis of guidelines and general principles can be of considerable value.

UR - http://www.scopus.com/inward/record.url?scp=33645879244&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33645879244&partnerID=8YFLogxK

U2 - 10.1016/j.jinorgbio.2006.01.022

DO - 10.1016/j.jinorgbio.2006.01.022

M3 - Review article

C2 - 16513177

AN - SCOPUS:33645879244

VL - 100

SP - 586

EP - 605

JO - Journal of Inorganic Biochemistry

JF - Journal of Inorganic Biochemistry

SN - 0162-0134

IS - 4

ER -