Myosin is reversibly inhibited by S-nitrosylation

Nogueira, Leonardo; Figueiredo-Freitas, Cicero; Casimiro-Lopes, Gustavo; Magdesian, Margaret H.; Assreuy, Jamil; Sorenson, Martha M.

doi:10.1042/bj20091144

Cited by 67Redox biology and oxidative stressNitric Oxide and Endothelin EffectsMuscle Physiology and Disorders

Myosin is reversibly inhibited by S-nitrosylation

Nogueira, Leonardo, Figueiredo-Freitas, Cicero, Casimiro-Lopes, Gustavo, Magdesian, Margaret H., Assreuy, Jamil, Sorenson, Martha M.·2009·Biochemical Journal

DOI 10.1042/bj20091144

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Abstract

Nitric oxide (NO*) is synthesized in skeletal muscle and its production increases during contractile activity. Although myosin is the most abundant protein in muscle, it is not known whether myosin is a target of NO* or NO* derivatives. In the present study, we have shown that exercise increases protein S-nitrosylation in muscle, and, among contractile proteins, myosin is the principal target of exogenous SNOs (S-nitrosothiols) in both skinned skeletal muscle fibres and differentiated myotubes. The reaction of isolated myosin with S-nitrosoglutathione results in S-nitrosylation at multiple cysteine thiols and produces two populations of protein-bound SNOs with different stabilities. The less-stable population inhibits the physiological ATPase activity, without affecting the affinity of myosin for actin. However, myosin is neither inhibited nor S-nitrosylated by the NO* donor diethylamine NONOate, indicating a requirement for transnitrosylation between low-mass SNO and myosin cysteine thiols rather than a direct reaction of myosin with NO* or its auto-oxidation products. Interestingly, alkylation of the most reactive thiols of myosin by N-ethylmaleimide does not inhibit formation of a stable population of protein-SNOs, suggesting that these sites are located in less accessible regions of the protein than those that affect activity. The present study reveals a new link between exercise and S-nitrosylation of skeletal muscle contractile proteins that may be important under (patho)physiological conditions.

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Various contractile-related proteins can undergo reversible post-translation modifications at cysteine residues on thiols, such as myosin, troponin, SERCA and ryanodine receptors, and these modifications are likely dependent on interactions between NO, reactive oxygen species and glutathione bioavailability.
“The potential influence of S-nitrosylation on excitation–contraction coupling is complex given that various contractile-related proteins can undergo reversible post-translation modifications at cysteine residues on thiols, such as myosin [140], troponin [141], SERCA [142] and ryanodine receptors (RyRs) [143,144], and that these post-translation protein modifications are likely dependent on inter”
From Effects of Dietary Nitrate Supplementation on Weightlifting Exercise Performance in Healthy Adults: A Systematic Review (2020) · cites this paper as [140]

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Authors: Nogueira, L., Figueiredo-Freitas, C., Casimiro-Lopes, G., Magdesian, M. H., Assreuy, J., & Sorenson, M. M.
Affiliations: Universidade Federal do Rio de Janeiro (BR)
Instituto de Bioquímica Médica, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro, Cidade Universitária, Rio de Janeiro, RJ 21941-590, Brazil
Universidade Federal de Santa Catarina (BR)
Corresponding author: Nogueira, Leonardo
ORCID: Nogueira, Leonardo
Casimiro-Lopes, Gustavo
Assreuy, Jamil
Sorenson, Martha M.
Venue: Biochemical Journal
Publisher: Portland Press Ltd.
Published: 2009-11-11
Volume: 424
Issue: 2
Pages: 221-231
ISSN: 0264-6021 (ISSN-L)
1470-8728
DOI: 10.1042/bj20091144
OpenAlex: W2007799395
Cited by: 67
References: 55
Citations by year: 2025: 1 · 2024: 2 · 2023: 5 · 2022: 4 · 2021: 3 · 2020: 10 · 2019: 6 · 2018: 3 · 2017: 4 · 2016: 5 · 2015: 2 · 2014: 4 · 2013: 3 · 2012: 3
FWCI: 2.00
Type: journal article
Language: en
Open access: closed
Locations: Biochemical Journal (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Keywords: myosin, S-nitrosylation, S-nitrosothiols, nitric oxide, skeletal muscle, physical activity, transnitrosation, ATPase activity, cysteine thiols, S-nitrosoglutathione, N-ethylmaleimide, contractile proteins, skinned muscle fibers, myotubes
MeSH terms: Actins, Sodium-Potassium-Exchanging ATPase, Animals, Cell Line, Male, Muscle Contraction, Myosins, Nitric Oxide, Rabbits, Nitrosation, Rats, Sprague-Dawley, Ca(2+) Mg(2+)-ATPase, Muscle Fibers, Skeletal, Tissue Culture Techniques, Mice, Rats, Protein Stability

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Myosin is reversibly inhibited by S-nitrosylation

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