Reversible binding of nitric oxide to tyrosyl radicals in photosystem II. Nitric oxide quenches formation of the S3 EPR signal species in acetate-inhibited photosystem II

Veronika A. Szalai, Gary W. Brudvig

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Abstract

Continuous illumination at temperatures above 250 K of photosystem II samples which have been depleted of calcium or chloride or treated with fluoride, acetate, or ammonia results in production of a broad radical EPR signal centered at g = 2.0. This EPR signal, called the S3 EPR signal, has been attributed to an organic radical interacting with the S2 state of the oxygen-evolving complex to give the species S2X+ (X+ = organic radical). A tyrosine radical has been proposed as the species responsible for the S3 EPR signal. On the basis of experiments demonstrating that nitric oxide binds reversibly to the tyrosyl radical in ribonucleotide reductase, nitric oxide has been used to probe the S3 EPR signal in acetate-treated photosystem II. In experiments using manganese-depleted photosystem II, nitric oxide was found to bind reversibly to both redox-active tyrosines, YD and YZ , to form EPR-silent adducts. Next, acetate-treated photosystem II was illuminated to form the S3 EPR signal in the presence of nitric oxide to test whether the S3 EPR signal behaves like YZ . Under conditions that produce the maximum yield of the S3 EPR signal in acetate-treated photosystem II, no S3 EPR signal was observed in the presence of nitric oxide. Upon removal of nitric oxide, the S3 EPR signal could be induced. Quenching of the S3 EPR signal by nitric oxide yielded an S2-state multiline EPR signal. Its amplitude was 45% of that found for uninhibited photosystem II illuminated at 200 K; this yield is the same as the yield of the S3 EPR signal under equivalent conditions but without nitric oxide. These results suggest that the S3 EPR signal is due to the configuration S2YZ in which the S2 state of the oxygen-evolving complex gives a broadened multiline EPR signal as a result of exchange and dipolar interactions with YZ . The binding of nitric oxide to YZ to form a diamagnetic YZ-NO species uncouples the S2 state from YZ , yielding a noninteracting S2-state multiline EPR signal species.

Original languageEnglish
Pages (from-to)15080-15087
Number of pages8
JournalBiochemistry
Volume35
Issue number47
Publication statusPublished - Nov 26 1996

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Photosystem II Protein Complex
Paramagnetic resonance
Nitric Oxide
Acetates
Oxygen
Ribonucleotide Reductases
Calcium Chloride
Manganese
Lighting
Fluorides
Ammonia
Oxidation-Reduction
Tyrosine
Temperature

ASJC Scopus subject areas

  • Biochemistry

Cite this

@article{47b3db6193fc46b2ab87120a3041bab1,
title = "Reversible binding of nitric oxide to tyrosyl radicals in photosystem II. Nitric oxide quenches formation of the S3 EPR signal species in acetate-inhibited photosystem II",
abstract = "Continuous illumination at temperatures above 250 K of photosystem II samples which have been depleted of calcium or chloride or treated with fluoride, acetate, or ammonia results in production of a broad radical EPR signal centered at g = 2.0. This EPR signal, called the S3 EPR signal, has been attributed to an organic radical interacting with the S2 state of the oxygen-evolving complex to give the species S2X+ (X+ = organic radical). A tyrosine radical has been proposed as the species responsible for the S3 EPR signal. On the basis of experiments demonstrating that nitric oxide binds reversibly to the tyrosyl radical in ribonucleotide reductase, nitric oxide has been used to probe the S3 EPR signal in acetate-treated photosystem II. In experiments using manganese-depleted photosystem II, nitric oxide was found to bind reversibly to both redox-active tyrosines, YD • and YZ •, to form EPR-silent adducts. Next, acetate-treated photosystem II was illuminated to form the S3 EPR signal in the presence of nitric oxide to test whether the S3 EPR signal behaves like YZ •. Under conditions that produce the maximum yield of the S3 EPR signal in acetate-treated photosystem II, no S3 EPR signal was observed in the presence of nitric oxide. Upon removal of nitric oxide, the S3 EPR signal could be induced. Quenching of the S3 EPR signal by nitric oxide yielded an S2-state multiline EPR signal. Its amplitude was 45{\%} of that found for uninhibited photosystem II illuminated at 200 K; this yield is the same as the yield of the S3 EPR signal under equivalent conditions but without nitric oxide. These results suggest that the S3 EPR signal is due to the configuration S2YZ • in which the S2 state of the oxygen-evolving complex gives a broadened multiline EPR signal as a result of exchange and dipolar interactions with YZ •. The binding of nitric oxide to YZ • to form a diamagnetic YZ-NO species uncouples the S2 state from YZ •, yielding a noninteracting S2-state multiline EPR signal species.",
author = "Szalai, {Veronika A.} and Brudvig, {Gary W.}",
year = "1996",
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T1 - Reversible binding of nitric oxide to tyrosyl radicals in photosystem II. Nitric oxide quenches formation of the S3 EPR signal species in acetate-inhibited photosystem II

AU - Szalai, Veronika A.

AU - Brudvig, Gary W.

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N2 - Continuous illumination at temperatures above 250 K of photosystem II samples which have been depleted of calcium or chloride or treated with fluoride, acetate, or ammonia results in production of a broad radical EPR signal centered at g = 2.0. This EPR signal, called the S3 EPR signal, has been attributed to an organic radical interacting with the S2 state of the oxygen-evolving complex to give the species S2X+ (X+ = organic radical). A tyrosine radical has been proposed as the species responsible for the S3 EPR signal. On the basis of experiments demonstrating that nitric oxide binds reversibly to the tyrosyl radical in ribonucleotide reductase, nitric oxide has been used to probe the S3 EPR signal in acetate-treated photosystem II. In experiments using manganese-depleted photosystem II, nitric oxide was found to bind reversibly to both redox-active tyrosines, YD • and YZ •, to form EPR-silent adducts. Next, acetate-treated photosystem II was illuminated to form the S3 EPR signal in the presence of nitric oxide to test whether the S3 EPR signal behaves like YZ •. Under conditions that produce the maximum yield of the S3 EPR signal in acetate-treated photosystem II, no S3 EPR signal was observed in the presence of nitric oxide. Upon removal of nitric oxide, the S3 EPR signal could be induced. Quenching of the S3 EPR signal by nitric oxide yielded an S2-state multiline EPR signal. Its amplitude was 45% of that found for uninhibited photosystem II illuminated at 200 K; this yield is the same as the yield of the S3 EPR signal under equivalent conditions but without nitric oxide. These results suggest that the S3 EPR signal is due to the configuration S2YZ • in which the S2 state of the oxygen-evolving complex gives a broadened multiline EPR signal as a result of exchange and dipolar interactions with YZ •. The binding of nitric oxide to YZ • to form a diamagnetic YZ-NO species uncouples the S2 state from YZ •, yielding a noninteracting S2-state multiline EPR signal species.

AB - Continuous illumination at temperatures above 250 K of photosystem II samples which have been depleted of calcium or chloride or treated with fluoride, acetate, or ammonia results in production of a broad radical EPR signal centered at g = 2.0. This EPR signal, called the S3 EPR signal, has been attributed to an organic radical interacting with the S2 state of the oxygen-evolving complex to give the species S2X+ (X+ = organic radical). A tyrosine radical has been proposed as the species responsible for the S3 EPR signal. On the basis of experiments demonstrating that nitric oxide binds reversibly to the tyrosyl radical in ribonucleotide reductase, nitric oxide has been used to probe the S3 EPR signal in acetate-treated photosystem II. In experiments using manganese-depleted photosystem II, nitric oxide was found to bind reversibly to both redox-active tyrosines, YD • and YZ •, to form EPR-silent adducts. Next, acetate-treated photosystem II was illuminated to form the S3 EPR signal in the presence of nitric oxide to test whether the S3 EPR signal behaves like YZ •. Under conditions that produce the maximum yield of the S3 EPR signal in acetate-treated photosystem II, no S3 EPR signal was observed in the presence of nitric oxide. Upon removal of nitric oxide, the S3 EPR signal could be induced. Quenching of the S3 EPR signal by nitric oxide yielded an S2-state multiline EPR signal. Its amplitude was 45% of that found for uninhibited photosystem II illuminated at 200 K; this yield is the same as the yield of the S3 EPR signal under equivalent conditions but without nitric oxide. These results suggest that the S3 EPR signal is due to the configuration S2YZ • in which the S2 state of the oxygen-evolving complex gives a broadened multiline EPR signal as a result of exchange and dipolar interactions with YZ •. The binding of nitric oxide to YZ • to form a diamagnetic YZ-NO species uncouples the S2 state from YZ •, yielding a noninteracting S2-state multiline EPR signal species.

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