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Dioxygen activation by nonheme iron enzymes with the 2-His-1-carboxylate facial triad that generate high-valent oxoiron oxidants

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Abstract

The 2-His-1-carboxylate facial triad is a widely used scaffold to bind the iron center in mononuclear nonheme iron enzymes for activating dioxygen in a variety of oxidative transformations of metabolic significance. Since the 1990s, over a hundred different iron enzymes have been identified to use this platform. This structural motif consists of two histidines and the side chain carboxylate of an aspartate or a glutamate arranged in a facial array that binds iron(II) at the active site. This triad occupies one face of an iron-centered octahedron and makes the opposite face available for the coordination of O2 and, in many cases, substrate, allowing the tailoring of the iron-dioxygen chemistry to carry out a plethora of diverse reactions. Activated dioxygen-derived species involved in the enzyme mechanisms include iron(III)-superoxo, iron(III)-peroxo, and high-valent iron(IV)-oxo intermediates. In this article, we highlight the major crystallographic, spectroscopic, and mechanistic advances of the past 20 years that have significantly enhanced our understanding of the mechanisms of O2 activation and the key roles played by iron-based oxidants.

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Abbreviations

l-Aba:

l-2-Aminobutyric acid

ACCO:

1-Aminocyclopropane-1-carboxylate oxidase

ACV:

δ-(l-α-Aminoadipoyl)-l-cysteinyl-d-valine

AIB:

(α-Aminoisobutyric acid)

AlkB:

Enzymes involved in oxidative DNA and RNA repair

AsqJ:

4′-Methoxyviridicatin synthase

AsnO:

Asparagine oxygenase

BH4 :

6(R)-l-erythro-5,6,7,8-tetrahydrobiopterin

BphC:

2,3-Dihydroxybiphenyl 1,2-dioxygenase

BZDO:

Benzoate 1,2-dioxygense

BDPP:

2,6-Bis[[(S)-2-(diphenylhydroxymethyl)-1-pyrrolidinyl]methyl]pyridine dianion

CarC:

Carbapenem synthase

CARDO:

Carbazole 1,9a-dioxygenase

CAS:

Clavaminate synthase

CloR:

3-Dimethylallyl-4-hydroxybenzoate synthase

l-Cpg:

l-Cyclopropylglycine

Cur Hal:

Halogenase in the biosynthesis of curacin A

CytC2:

Substrate carrier protein for CytC3 in the biosynthesis of cytotrienin

CytC3:

Halogenase in the biosynthesis of cytotrienin

DAOCS:

Deacetoxycephalosporin C synthase

DdaC:

Epoxidase in biosynthesis of N β -epoxysuccinamoyl-DAP-Val

DFT:

Density functional theory

DMO:

Dicamba O-demethylase

l-DOPA:

l-3,4-Dihydroxyphenylalanine

EFE:

Ethylene forming enzyme

ENDOR:

Electron nuclear double resonance

EPR:

Electron paramagnetic resonance

EXAFS:

Extended X-ray absorption fine structure

FIH-1:

Factor-inhibiting hypoxia-inducible factor-1

FtmOx1:

Fumitremorgin B endoperoxidase

HEPD:

2-Hydroxyethylphosphonate dioxygenase

HMS:

4-Hydroxymandelate synthase

1-HPP:

1-Hydroxypropylphosphonate

2-HPP:

2-Hydroxypropyl-1-phosphonate

HPPD:

4-Hydroxyphenylpyruvate dioxygenase

HppE:

(S)-2-Hydroxypropylphosphonate epoxidase

HYSCORE:

Hyperfine sublevel correlation spectroscopy

IPNS:

Isopenicillin N synthase

α-KG:

α-Ketoglutarate

KIE:

Kinetic isotope effect

KshAB:

3-Ketosteroid 9α-hydroxylase

MCD:

Magnetic circular dichroism

NDO:

Naphthalene 1,2-dioxygenase

N4Py:

N,N-bis(2-pyridylmethyl)-N-bis(2-pyridyl)methylamine

NRVS:

Nuclear resonance vibrational spectroscopy

l-Nva:

l-Norvaline

OMO:

2-Oxoquinoline 8-monooxygenase

OrfP:

Enzyme that catalyzes conversion of l-Arg into (3R,4R)-(OH)2-l-Arg

P4H:

Prolyl-4-hydroxylase

PenD:

Epoxidase in biosynthesis of pentalenolactone

PheH:

Phenylalanine hydroxylase

PrnD:

Aminopyrrolnitrin oxygenase

RedG:

Rieske enzyme that catalyzes the oxidative carbocyclization of undecylprodigiosin to form streptorubin B

RFQ:

Rapid-freeze-quench

SIE:

Solvent isotope effect

SnoK:

Carbocyclase in nogalamycin biosynthesis

SnoN:

Epimerase in nogalamycin biosynthesis

Stc2:

Stachydrine demethylase

SyrB1:

Substrate carrier protein for SyrB2 in syringomycin biosynthesis

SyrB2:

Halogenase in syringomycin biosynthesis

TauD:

Taurine:α-KG dioxygenase

TDO:

Toluene dioxygenase

THA:

3-(2-Thienyl)-l-alanine

TMC:

1,4,8,11-Tetramethyl-1,4,8,11-tetraazacyclotetradecane

TQA:

Tris(quinolyl-2-methyl)amine

TrpH:

Tryptophan hydroxylase

TyrH:

Tyrosine hydroxylase

WelO5:

Halogenase involved in the maturation process to form welwitindolinones

XRD:

X-ray diffraction

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Acknowledgements

We thank the U. S. National Science Foundation for funding (CHE-1361773 to L.Q.) and are grateful to Dr. Caleb Allpress and Dr. Johannes E. M. N. Klein for valuable input and discussions.

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  1. Department of Chemistry, Center for Metals in Biocatalysis, University of Minnesota, Minneapolis, MN, 55455, USA

    Subhasree Kal & Lawrence Que

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Kal, S., Que, L. Dioxygen activation by nonheme iron enzymes with the 2-His-1-carboxylate facial triad that generate high-valent oxoiron oxidants. J Biol Inorg Chem 22, 339–365 (2017). https://doi.org/10.1007/s00775-016-1431-2

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