Oxidative Cleavage of a Phenolic Diarylpropane Lignin Model Dimer by Manganese Peroxidase from Phanerochaete chrysosporium

Hiroyuki Wariishi, Khadar Valli, Michael H. Gold

Research output: Contribution to journalArticle

114 Citations (Scopus)

Abstract

In the presence of MnII and H2O2, homogeneous manganese peroxidase oxidized 1-(3,5-dimethoxy-4-hydroxyphenyl)-2-(4-methoxyphenyl)-1,3-dihydroxypropane (I) to yield 1-(3,5-dimethoxy-4-hydroxyphenyl)-2-(4-methoxyphenyl)-1-oxo-3-hydroxypropane (II), 2,6-dimethoxy-1,4-benzoquinone (III), 2,6-dimethoxy-1,4-dihydroxybenzene (IV), 1-(4-methoxyphenyl)-1-oxo-2-hydroxyethane (V), 1-(4-methoxyphenyl)-1,2-dihydroxyethane (VI), syringaldehyde (VIII), and 2-(4-methoxyphenyl)-3-hydroxypropanal (IX). Chemically prepared manganese(III) malonate catalyzed the same reactions. Oxidation of I in H218O under argon resulted in >80% incorporation of 18O into the phenylglycol VI, the hydroquinone IV, and the quinone III. Oxidation of I in H218O under aerobic conditions resulted in 40% incorporation of 18O into VI but no 18O incorporation into V. Finally, oxidation of I under 18O2 resulted in 89% and 28% incorporation of 18O into V and VI, respectively. These results are explained by mechanisms involving the one-electron oxidation of the substrate I by enzyme-generated MnIII to produce a phenoxy radical intermediate I'. Subsequent Cα-Cβ bond cleavage of the radical intermediate yields syringaldehyde (VIII) and a C6-C2 benzylic radical. Syringaldehyde is oxidized by MnIII in several steps to a cyclohexadiene cation intermediate I'', which is attacked by water to yield the benzoquinone III. The C6-C2 radical is scavenged by O2 to form a peroxy radical that decomposes to V and VI. The C6-C2 radical is also oxidized by MnIII, leading to the formation of VI. Alternatively, the radical I' undergoes subsequent oxidation by MnIII to yield a cyclohexadiene cation I''. Attack of the cation by water yields a triol that undergoes alkylphenyl cleavage to yield the phenylpropanal IX and the hydroquinone IV. The latter is oxidized by MnIII to yield the quinone III. Finally, the cation intermediate I'' loses a proton to yield a quinone methide that rearranges to form the diarylpropanone II. In these reactions, MnIII generated by manganese peroxidase catalyzes both formation of the substrate phenoxy radical and oxidation of carbon-centered radical intermediates, to yield reactive cations.

Original languageEnglish
Pages (from-to)6017-6023
Number of pages7
JournalBiochemistry
Volume28
Issue number14
DOIs
Publication statusPublished - Jul 1 1989
Externally publishedYes

Fingerprint

manganese peroxidase
Phanerochaete
Lignin
Dimers
Cations
Oxidation
Ethylene Glycols
Water
Argon
Manganese
Substrates
Protons
Carbon
Electrons

All Science Journal Classification (ASJC) codes

  • Biochemistry

Cite this

Oxidative Cleavage of a Phenolic Diarylpropane Lignin Model Dimer by Manganese Peroxidase from Phanerochaete chrysosporium. / Wariishi, Hiroyuki; Valli, Khadar; Gold, Michael H.

In: Biochemistry, Vol. 28, No. 14, 01.07.1989, p. 6017-6023.

Research output: Contribution to journalArticle

@article{830c8893043a412b9e8ae97c581b8679,
title = "Oxidative Cleavage of a Phenolic Diarylpropane Lignin Model Dimer by Manganese Peroxidase from Phanerochaete chrysosporium",
abstract = "In the presence of MnII and H2O2, homogeneous manganese peroxidase oxidized 1-(3,5-dimethoxy-4-hydroxyphenyl)-2-(4-methoxyphenyl)-1,3-dihydroxypropane (I) to yield 1-(3,5-dimethoxy-4-hydroxyphenyl)-2-(4-methoxyphenyl)-1-oxo-3-hydroxypropane (II), 2,6-dimethoxy-1,4-benzoquinone (III), 2,6-dimethoxy-1,4-dihydroxybenzene (IV), 1-(4-methoxyphenyl)-1-oxo-2-hydroxyethane (V), 1-(4-methoxyphenyl)-1,2-dihydroxyethane (VI), syringaldehyde (VIII), and 2-(4-methoxyphenyl)-3-hydroxypropanal (IX). Chemically prepared manganese(III) malonate catalyzed the same reactions. Oxidation of I in H218O under argon resulted in >80{\%} incorporation of 18O into the phenylglycol VI, the hydroquinone IV, and the quinone III. Oxidation of I in H218O under aerobic conditions resulted in 40{\%} incorporation of 18O into VI but no 18O incorporation into V. Finally, oxidation of I under 18O2 resulted in 89{\%} and 28{\%} incorporation of 18O into V and VI, respectively. These results are explained by mechanisms involving the one-electron oxidation of the substrate I by enzyme-generated MnIII to produce a phenoxy radical intermediate I'. Subsequent Cα-Cβ bond cleavage of the radical intermediate yields syringaldehyde (VIII) and a C6-C2 benzylic radical. Syringaldehyde is oxidized by MnIII in several steps to a cyclohexadiene cation intermediate I'', which is attacked by water to yield the benzoquinone III. The C6-C2 radical is scavenged by O2 to form a peroxy radical that decomposes to V and VI. The C6-C2 radical is also oxidized by MnIII, leading to the formation of VI. Alternatively, the radical I' undergoes subsequent oxidation by MnIII to yield a cyclohexadiene cation I''. Attack of the cation by water yields a triol that undergoes alkylphenyl cleavage to yield the phenylpropanal IX and the hydroquinone IV. The latter is oxidized by MnIII to yield the quinone III. Finally, the cation intermediate I'' loses a proton to yield a quinone methide that rearranges to form the diarylpropanone II. In these reactions, MnIII generated by manganese peroxidase catalyzes both formation of the substrate phenoxy radical and oxidation of carbon-centered radical intermediates, to yield reactive cations.",
author = "Hiroyuki Wariishi and Khadar Valli and Gold, {Michael H.}",
year = "1989",
month = "7",
day = "1",
doi = "10.1021/bi00440a044",
language = "English",
volume = "28",
pages = "6017--6023",
journal = "Biochemistry",
issn = "0006-2960",
publisher = "American Chemical Society",
number = "14",

}

TY - JOUR

T1 - Oxidative Cleavage of a Phenolic Diarylpropane Lignin Model Dimer by Manganese Peroxidase from Phanerochaete chrysosporium

AU - Wariishi, Hiroyuki

AU - Valli, Khadar

AU - Gold, Michael H.

PY - 1989/7/1

Y1 - 1989/7/1

N2 - In the presence of MnII and H2O2, homogeneous manganese peroxidase oxidized 1-(3,5-dimethoxy-4-hydroxyphenyl)-2-(4-methoxyphenyl)-1,3-dihydroxypropane (I) to yield 1-(3,5-dimethoxy-4-hydroxyphenyl)-2-(4-methoxyphenyl)-1-oxo-3-hydroxypropane (II), 2,6-dimethoxy-1,4-benzoquinone (III), 2,6-dimethoxy-1,4-dihydroxybenzene (IV), 1-(4-methoxyphenyl)-1-oxo-2-hydroxyethane (V), 1-(4-methoxyphenyl)-1,2-dihydroxyethane (VI), syringaldehyde (VIII), and 2-(4-methoxyphenyl)-3-hydroxypropanal (IX). Chemically prepared manganese(III) malonate catalyzed the same reactions. Oxidation of I in H218O under argon resulted in >80% incorporation of 18O into the phenylglycol VI, the hydroquinone IV, and the quinone III. Oxidation of I in H218O under aerobic conditions resulted in 40% incorporation of 18O into VI but no 18O incorporation into V. Finally, oxidation of I under 18O2 resulted in 89% and 28% incorporation of 18O into V and VI, respectively. These results are explained by mechanisms involving the one-electron oxidation of the substrate I by enzyme-generated MnIII to produce a phenoxy radical intermediate I'. Subsequent Cα-Cβ bond cleavage of the radical intermediate yields syringaldehyde (VIII) and a C6-C2 benzylic radical. Syringaldehyde is oxidized by MnIII in several steps to a cyclohexadiene cation intermediate I'', which is attacked by water to yield the benzoquinone III. The C6-C2 radical is scavenged by O2 to form a peroxy radical that decomposes to V and VI. The C6-C2 radical is also oxidized by MnIII, leading to the formation of VI. Alternatively, the radical I' undergoes subsequent oxidation by MnIII to yield a cyclohexadiene cation I''. Attack of the cation by water yields a triol that undergoes alkylphenyl cleavage to yield the phenylpropanal IX and the hydroquinone IV. The latter is oxidized by MnIII to yield the quinone III. Finally, the cation intermediate I'' loses a proton to yield a quinone methide that rearranges to form the diarylpropanone II. In these reactions, MnIII generated by manganese peroxidase catalyzes both formation of the substrate phenoxy radical and oxidation of carbon-centered radical intermediates, to yield reactive cations.

AB - In the presence of MnII and H2O2, homogeneous manganese peroxidase oxidized 1-(3,5-dimethoxy-4-hydroxyphenyl)-2-(4-methoxyphenyl)-1,3-dihydroxypropane (I) to yield 1-(3,5-dimethoxy-4-hydroxyphenyl)-2-(4-methoxyphenyl)-1-oxo-3-hydroxypropane (II), 2,6-dimethoxy-1,4-benzoquinone (III), 2,6-dimethoxy-1,4-dihydroxybenzene (IV), 1-(4-methoxyphenyl)-1-oxo-2-hydroxyethane (V), 1-(4-methoxyphenyl)-1,2-dihydroxyethane (VI), syringaldehyde (VIII), and 2-(4-methoxyphenyl)-3-hydroxypropanal (IX). Chemically prepared manganese(III) malonate catalyzed the same reactions. Oxidation of I in H218O under argon resulted in >80% incorporation of 18O into the phenylglycol VI, the hydroquinone IV, and the quinone III. Oxidation of I in H218O under aerobic conditions resulted in 40% incorporation of 18O into VI but no 18O incorporation into V. Finally, oxidation of I under 18O2 resulted in 89% and 28% incorporation of 18O into V and VI, respectively. These results are explained by mechanisms involving the one-electron oxidation of the substrate I by enzyme-generated MnIII to produce a phenoxy radical intermediate I'. Subsequent Cα-Cβ bond cleavage of the radical intermediate yields syringaldehyde (VIII) and a C6-C2 benzylic radical. Syringaldehyde is oxidized by MnIII in several steps to a cyclohexadiene cation intermediate I'', which is attacked by water to yield the benzoquinone III. The C6-C2 radical is scavenged by O2 to form a peroxy radical that decomposes to V and VI. The C6-C2 radical is also oxidized by MnIII, leading to the formation of VI. Alternatively, the radical I' undergoes subsequent oxidation by MnIII to yield a cyclohexadiene cation I''. Attack of the cation by water yields a triol that undergoes alkylphenyl cleavage to yield the phenylpropanal IX and the hydroquinone IV. The latter is oxidized by MnIII to yield the quinone III. Finally, the cation intermediate I'' loses a proton to yield a quinone methide that rearranges to form the diarylpropanone II. In these reactions, MnIII generated by manganese peroxidase catalyzes both formation of the substrate phenoxy radical and oxidation of carbon-centered radical intermediates, to yield reactive cations.

UR - http://www.scopus.com/inward/record.url?scp=33845185357&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33845185357&partnerID=8YFLogxK

U2 - 10.1021/bi00440a044

DO - 10.1021/bi00440a044

M3 - Article

AN - SCOPUS:33845185357

VL - 28

SP - 6017

EP - 6023

JO - Biochemistry

JF - Biochemistry

SN - 0006-2960

IS - 14

ER -