Theoretical investigation of thermal decomposition of peroxidized coelenterazines with and without external perturbations

Hiroshi Isobe, Syusuke Yamanaka, Mitsutaka Okumura, Kizashi Yamaguchi

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Thermal decomposition of peroxidized coelenterazines with and without external perturbations has been studied theoretically using the hybrid density functional theory (B3LYP) and the Coulomb-attenuating method (CAM). Possible roles of a hydrogen-bonding interface constituted by amino acid residues in the coelenterazine-biding site of aequorin are addressed by using simple model clusters with a polarizable continuum model to grasp some important aspects that may affect the electronic mechanism operating within the photoprotein. Calculations have revealed that the electronic property and stability of the peroxide are greatly affected by its protonation state and/or environmental effects, such as a polarizing medium and specific (localized) short-range electrostatic interactions, which may be critical for the bioluminescence activity. Theory highlights two mechanisms by which the neutral species can be activated, which otherwise decomposes by a homolytic 0-0 dissociation with a high barrier. In the first mechanism, the Tyr82Hisl6-Trp86 triad motif facilitates the deprotonation process of the phenolic OH group at the CO position of the coelenterazine and thereby makes it a sufficiently good electron donor to activate the 0-0 bond. In the second mechanism, intramolecular charge transfer is accomplished within the neutral peroxide by a proton delivery mediated via another triad motif, Tyr l84-His l69-Trp l73, without the activation of the substrate itself. The combination of the first and second mechanisms leads to complete electron transfer for the formation of a radical pair as a local intermediate stabilized by the nearby triad motifs.

Original languageEnglish
Pages (from-to)15171-15187
Number of pages17
JournalJournal of Physical Chemistry A
Volume113
Issue number52
DOIs
Publication statusPublished - Dec 31 2009
Externally publishedYes

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thermal decomposition
Pyrolysis
Peroxides
perturbation
Luminescent Proteins
Aequorin
Bioluminescence
peroxides
Deprotonation
Electrons
Protonation
Carbon Monoxide
Coulomb interactions
Electronic properties
Density functional theory
Environmental impact
Protons
Charge transfer
Hydrogen bonds
bioluminescence

ASJC Scopus subject areas

  • Physical and Theoretical Chemistry

Cite this

Theoretical investigation of thermal decomposition of peroxidized coelenterazines with and without external perturbations. / Isobe, Hiroshi; Yamanaka, Syusuke; Okumura, Mitsutaka; Yamaguchi, Kizashi.

In: Journal of Physical Chemistry A, Vol. 113, No. 52, 31.12.2009, p. 15171-15187.

Research output: Contribution to journalArticle

Isobe, Hiroshi ; Yamanaka, Syusuke ; Okumura, Mitsutaka ; Yamaguchi, Kizashi. / Theoretical investigation of thermal decomposition of peroxidized coelenterazines with and without external perturbations. In: Journal of Physical Chemistry A. 2009 ; Vol. 113, No. 52. pp. 15171-15187.
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