Thiol-mediated oxidation of nonphenolic lignin model compounds by manganese peroxidase of Phanerochaete chrysosporium.

Hiroyuki Wariishi, K. Valli, V. Renganathan, M. H. Gold

Research output: Contribution to journalArticle

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Abstract

In the presence of MnII, H2O2, and glutathione (GSH), manganese peroxidase oxidized veratryl alcohol (I) to veratraldehyde (IV). Anisyl alcohol (II) and benzyl alcohol (III) were also oxidized by this system to their corresponding aldehydes (V and VI). In the presence of GSH, chemically prepared MnIII or gamma-irradiation also catalyzed the oxidation of I, II, and III to IV, V, and VI, respectively. GSH and dithiothreitol rapidly reduced MnIII to MnII in the absence of aromatic substrates and the dithiothreitol was oxidized to its disulfide (4,5-dihydroxyl-1,2-dithiane). These results indicate that the thiol is oxidized by enzyme-generated MnIII to a thiyl radical. The latter abstracts a hydrogen from the substrate, forming a benzylic radical which reacts with another thiyl radical to yield an intermediate which decomposes to the benzaldehyde product. In the presence of MnII, GSH, and H2O2, manganese peroxidase also oxidized 1-(4-ethoxy-3-methoxy-phenyl)-2-(4'-hydroxymethyl-2'-methoxyphenoxy)- 1,3-dihydroxypropane (XII) to yield vanillyl alcohol (VII), vanillin (VIII), 1-(4-ethoxy-3-methoxyphenyl)-1,3-dihydroxypropane (XVI), 1-(4-ethoxy-3-methoxyphenyl)-1-oxo-3-hydroxypropane (XIX), and several C alpha oxidized dimeric products. Abstraction of the C alpha (A ring) hydrogen of the dimer (XII) yields a benzylic radical, leading to C beta oxygen ether cleavage. The resultant intermediates yield the ketone (XIX) and vanillyl alcohol (VII) or vanillin (VIII). Alternatively, benzylic radical formation at the C' alpha position (B ring) leads to radical cleavage, yielding a quinone methide and a C beta radical, which yield vanillin and the 1,3-diol (XVI), respectively. In these reactions, MnIII oxidizes a thiol to a thiyl radical which subsequently abstracts a hydrogen from the substrate to form a benzylic radical. The latter undergoes nonenzymatic reactions to yield the final products.

Original languageEnglish
Pages (from-to)14185-14191
Number of pages7
JournalThe Journal of biological chemistry
Volume264
Issue number24
Publication statusPublished - Jan 1 1989
Externally publishedYes

Fingerprint

manganese peroxidase
Phanerochaete
Lignin
Sulfhydryl Compounds
Hydrogen
Oxidation
Dithiothreitol
Substrates
Benzyl Alcohol
Ketones
Aldehydes
Disulfides
Dimers
Ether
Glutathione
Irradiation
Oxygen
vanillin
Enzymes

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

Thiol-mediated oxidation of nonphenolic lignin model compounds by manganese peroxidase of Phanerochaete chrysosporium. / Wariishi, Hiroyuki; Valli, K.; Renganathan, V.; Gold, M. H.

In: The Journal of biological chemistry, Vol. 264, No. 24, 01.01.1989, p. 14185-14191.

Research output: Contribution to journalArticle

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title = "Thiol-mediated oxidation of nonphenolic lignin model compounds by manganese peroxidase of Phanerochaete chrysosporium.",
abstract = "In the presence of MnII, H2O2, and glutathione (GSH), manganese peroxidase oxidized veratryl alcohol (I) to veratraldehyde (IV). Anisyl alcohol (II) and benzyl alcohol (III) were also oxidized by this system to their corresponding aldehydes (V and VI). In the presence of GSH, chemically prepared MnIII or gamma-irradiation also catalyzed the oxidation of I, II, and III to IV, V, and VI, respectively. GSH and dithiothreitol rapidly reduced MnIII to MnII in the absence of aromatic substrates and the dithiothreitol was oxidized to its disulfide (4,5-dihydroxyl-1,2-dithiane). These results indicate that the thiol is oxidized by enzyme-generated MnIII to a thiyl radical. The latter abstracts a hydrogen from the substrate, forming a benzylic radical which reacts with another thiyl radical to yield an intermediate which decomposes to the benzaldehyde product. In the presence of MnII, GSH, and H2O2, manganese peroxidase also oxidized 1-(4-ethoxy-3-methoxy-phenyl)-2-(4'-hydroxymethyl-2'-methoxyphenoxy)- 1,3-dihydroxypropane (XII) to yield vanillyl alcohol (VII), vanillin (VIII), 1-(4-ethoxy-3-methoxyphenyl)-1,3-dihydroxypropane (XVI), 1-(4-ethoxy-3-methoxyphenyl)-1-oxo-3-hydroxypropane (XIX), and several C alpha oxidized dimeric products. Abstraction of the C alpha (A ring) hydrogen of the dimer (XII) yields a benzylic radical, leading to C beta oxygen ether cleavage. The resultant intermediates yield the ketone (XIX) and vanillyl alcohol (VII) or vanillin (VIII). Alternatively, benzylic radical formation at the C' alpha position (B ring) leads to radical cleavage, yielding a quinone methide and a C beta radical, which yield vanillin and the 1,3-diol (XVI), respectively. In these reactions, MnIII oxidizes a thiol to a thiyl radical which subsequently abstracts a hydrogen from the substrate to form a benzylic radical. The latter undergoes nonenzymatic reactions to yield the final products.",
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T1 - Thiol-mediated oxidation of nonphenolic lignin model compounds by manganese peroxidase of Phanerochaete chrysosporium.

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AU - Renganathan, V.

AU - Gold, M. H.

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N2 - In the presence of MnII, H2O2, and glutathione (GSH), manganese peroxidase oxidized veratryl alcohol (I) to veratraldehyde (IV). Anisyl alcohol (II) and benzyl alcohol (III) were also oxidized by this system to their corresponding aldehydes (V and VI). In the presence of GSH, chemically prepared MnIII or gamma-irradiation also catalyzed the oxidation of I, II, and III to IV, V, and VI, respectively. GSH and dithiothreitol rapidly reduced MnIII to MnII in the absence of aromatic substrates and the dithiothreitol was oxidized to its disulfide (4,5-dihydroxyl-1,2-dithiane). These results indicate that the thiol is oxidized by enzyme-generated MnIII to a thiyl radical. The latter abstracts a hydrogen from the substrate, forming a benzylic radical which reacts with another thiyl radical to yield an intermediate which decomposes to the benzaldehyde product. In the presence of MnII, GSH, and H2O2, manganese peroxidase also oxidized 1-(4-ethoxy-3-methoxy-phenyl)-2-(4'-hydroxymethyl-2'-methoxyphenoxy)- 1,3-dihydroxypropane (XII) to yield vanillyl alcohol (VII), vanillin (VIII), 1-(4-ethoxy-3-methoxyphenyl)-1,3-dihydroxypropane (XVI), 1-(4-ethoxy-3-methoxyphenyl)-1-oxo-3-hydroxypropane (XIX), and several C alpha oxidized dimeric products. Abstraction of the C alpha (A ring) hydrogen of the dimer (XII) yields a benzylic radical, leading to C beta oxygen ether cleavage. The resultant intermediates yield the ketone (XIX) and vanillyl alcohol (VII) or vanillin (VIII). Alternatively, benzylic radical formation at the C' alpha position (B ring) leads to radical cleavage, yielding a quinone methide and a C beta radical, which yield vanillin and the 1,3-diol (XVI), respectively. In these reactions, MnIII oxidizes a thiol to a thiyl radical which subsequently abstracts a hydrogen from the substrate to form a benzylic radical. The latter undergoes nonenzymatic reactions to yield the final products.

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