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Methionine sulfoxide and the methionine sulfoxide reductase system as modulators of signal transduction pathways: a review

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Abstract

Methionine oxidation and reduction is a common phenomenon occurring in biological systems under both physiological and oxidative-stress conditions. The levels of methionine sulfoxide (MetO) are dependent on the redox status in the cell or organ, and they are usually elevated under oxidative-stress conditions, aging, inflammation, and oxidative-stress related diseases. MetO modification of proteins may alter their function or cause the accumulation of toxic proteins in the cell/organ. Accordingly, the regulation of the level of MetO is mediated through the ubiquitous and evolutionary conserved methionine sulfoxide reductase (Msr) system and its associated redox molecules. Recent published research has provided new evidence for the involvement of free MetO or protein-bound MetO of specific proteins in several signal transduction pathways that are important for cellular function. In the current review, we will focus on the role of MetO in specific signal transduction pathways of various organisms, with relation to their physiological contexts, and discuss the contribution of the Msr system to the regulation of the observed MetO effect.

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References

  • Ahmed ZM, Yousaf R, Lee BC, Khan SN, Lee S, Lee K, Husnain T, Rehman AU, Bonneux S, Ansar M et al (2011) Functional null mutations of MSRB3 encoding methionine sulfoxide reductase are associated with human deafness DFNB74. Am J Hum Genet 88:19–29

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bar-Noy S, Moskovitz J (2002) Mouse methionine sulfoxide reductase B: effect of selenocysteine incorporation on its activity and expression of the seleno-containing enzyme in bacterial and mammalian cells. Biochem Biophys Res Commun 297(4):956–961

    CAS  PubMed  Google Scholar 

  • Baum KR, Ahmad Z, Singh VK (2015) Regulation of expression of oxacillin-inducible methionine sulfoxide reductases in Staphylococcus aureus. Int J Microbiol 2015:617925

    PubMed  PubMed Central  Google Scholar 

  • Bigelow DJ, Squier TC (2005) Redox modulation of cellular signaling and metabolism through reversible oxidation of methionine sensors in calcium regulatory proteins. Biochim Biophys Acta 1703:121–134

    CAS  PubMed  Google Scholar 

  • Bitan G, Tarus B, Vollers SS, Lashuel HA, Condron MM, Straub JE, Teplow DB (2003) A molecular switch in amyloid assembly: Met35 and amyloid beta-protein oligomerization. J Am Chem Soc 25:15359–15365

    Google Scholar 

  • Boutte AM, Woltjer RL, Zimmerman LJ, Stamer SL, Montine KS, Manno MV, Cimino PJ, Liebler DC, Montine TJ (2006) Selectively increased oxidative modifications mapped to detergent-insoluble forms of Abeta and beta-III tubulin in Alzheimer’s disease. FASEB J 20:1473–1483

    CAS  PubMed  Google Scholar 

  • Brennan LA, Kantorow M (2009) Mitochondrial function and redox control in the aging eye: role of MsrA and other repair systems in cataract and macular degenerations. Exp Eye Res 88(2):195–203

    CAS  PubMed  Google Scholar 

  • Brot N, Weissbach L, Werth J, Weissbach H (1981) Enzymatic reduction of protein-bound methionine sulfoxide. Proc Natl Acad Sci U S A 78(4):2155–2158

    CAS  PubMed  PubMed Central  Google Scholar 

  • Butterfield DA, Boyd-Kimball D (2005) The critical role of methionine 35 in Alzheimer’s amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity. Biochim Biophys Acta 1703:149–156

    CAS  PubMed  Google Scholar 

  • Campos AI, García-Marín LM, Byrne EM, Martin NG, Cuéllar-Partida G, Rentería ME (2020) Insights into the aetiology of snoring from observational and genetic investigations in the UK Biobank. Nat Commun 11(1):817–829

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chandler JD, Margaroli C, Horati H, Kilgore MB, Veltman M, Liu HK, Taurone AJ, Peng L, Guglani L, Uppal K, Go YM, Tiddens HAWM, Scholte BJ, Tirouvanziam R, Jones DP, Janssens HM (2018) Myeloperoxidase oxidation of methionine associates with early cystic fibrosis lung disease. Eur Respir J 52(4):1801118

    PubMed  PubMed Central  Google Scholar 

  • Chung H, Kim AK, Jung SA, Kim SW, Yu K, Lee JH (2010) The Drosophila homolog of methionine sulfoxide reductase A extends lifespan and increases nuclear localization of FOXO. FEBS Lett 584:3609–3614

    CAS  PubMed  Google Scholar 

  • Deng Y, Jiang B, Rankin CL, Toyo-Oka K, Richter ML, Maupin-Furlow JA, Moskovitz J (2018) Methionine sulfoxide reductase A (MsrA) mediates the ubiquitination of 14–3–3 protein isotypes in brain. Free Radic Biol Med 129:600–607

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong J, Atwood CS, Anderson VE, Siedlak SL, Smith MA, Perry G, Carey PR (2003) Metal binding and oxidation of amyloid-beta within isolated senile plaque cores: Raman microscopic evidence. Biochemistry 42:2768–2773

    CAS  PubMed  Google Scholar 

  • Drazic A, Miura H, Peschek J, Le Y, Bach NC, Kriehuber T, Winter J (2013) Methionine oxidation activates a transcription factor in response to oxidative stress. Proc Natl Acad Sci U S A 110(23):9493–9498

    CAS  PubMed  PubMed Central  Google Scholar 

  • Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, Lowe JS, O’Donnell SE, Aykin-Burns N et al (2008) A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133:462–474

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ezraty B, Grimaud R, El Hassouni M, Moinier D, Barras F (2004) Methionine sulfoxide reductases protect Ffh from oxidative damages in Escherichia coli. EMBO J 23(8):1868–1877

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fan H, Wu PF, Zhang L, Hu ZL, Wang W, Guan XL, Luo H, Ni M, Yang JW, Li MX, Chen JG, Wang F (2015) Methionine sulfoxide reductase A negatively controls microglia-mediated neuroinflammation via inhibiting ROS/MAPKs/NF-κB signaling pathways through a catalytic antioxidant function. Antioxid Redox Signal 22(10):832–847

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fomenko DE, Novoselov SV, Natarajan SK, Lee BC, Koc A, Carlson BA, Lee TH, Kim HY, Hatfield DL, Gladyshev VN (2009) MsrB1 (methionine-R-sulfoxide reductase 1) knock-out mice: roles of MsrB1 in redox regulation and identification of a novel selenoprotein form. J Biol Chem 284(9):5986–5993

    CAS  PubMed  PubMed Central  Google Scholar 

  • Franklin JM, Carrasco GA, Moskovitz J (2013) Induction of methionine sulfoxide reductase activity by pergolide, pergolide sulfoxide, and S-adenosyl-methionine in neuronal cells. Neurosci Lett 533:86–89

    CAS  PubMed  Google Scholar 

  • Fu X, Adams Z, Liu R, Hepowit NL, Wu Y, Bowmann CF, Moskovitz J, Maupin-Furlow JA (2017) Methionine sulfoxide reductase A (MsrA) and its function in ubiquitin-like protein modification in archaea. Mbio 8(5):e01169-e1217. https://doi.org/10.1128/mBio.01169-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallmetzer A, Silvestrini L, Schinko TB, Hortschansky P, Dattenböck C, Muro-Pastor MI, Kungl A, Brakhage AA, Scazzocchio C, Strauss J (2015) Reversible oxidation of a conserved methionine in the nuclear export sequence determines subcellular distribution and activity of the fungal nitrate regulator NirA. PLoS Genet 11(7):e1005297

    PubMed  PubMed Central  Google Scholar 

  • García-Bermúdez M, López-Mejías R, González-Juanatey C, Castañeda S, Miranda-Filloy JA, Blanco R, Fernández-Gutiérrez B, Balsa A, González-Álvaro I, Gómez-Vaquero C, Llorca J, Martín J, González-Gay MA (2012) Association of the methionine sulfoxide reductase A rs10903323 gene polymorphism with cardiovascular disease in patients with rheumatoid arthritis. Scand J Rheumatol 41(5):350–353

    PubMed  Google Scholar 

  • Glaser CB, Yamin G, Uversky VN, Fink AL (2005) Methionine oxidation, alpha-synuclein and Parkinson’s disease. Biochim Biophys Acta 1703(2):157–169

    CAS  PubMed  Google Scholar 

  • Grimaud R, Ezraty B, Mitchell JK, Lafitte D, Briand C, Derrick PJ, Barras F (2001) Repair of oxidized proteins. Identification of a new methionine sulfoxide reductase. J Biol Chem 276(52):48915–48920

    CAS  PubMed  Google Scholar 

  • Gu H, Chen W, Yin J, Chen S, Zhang J, Gong J (2013) Methionine sulfoxide reductase A rs10903323 G/A polymorphism is associated with increased risk of coronary artery disease in a Chinese population. Clin Biochem 46(16–17):1668–1672

    CAS  PubMed  Google Scholar 

  • Hanbauer I, Moskovitz J (2006) The yeast cytosolic thioredoxins are involved in the regulation of methionine sulfoxide reductase A. Free Radic Biol Med 40(8):1391–1396

    CAS  PubMed  Google Scholar 

  • Hanbauer I, Boja ES, Moskovitz J (2003) A homologue of elongation factor 1 gamma regulates methionine sulfoxide reductase A gene expression in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 100(14):8199–8204

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hardin SC, Larue CT, Oh MH, Jain V, Huber SC (2009) Coupling oxidative signals to protein phosphorylation via methionine oxidation in Arabidopsis. Biochem J 422(2):305–312

    CAS  PubMed  Google Scholar 

  • He Q, Li H, Meng F, Sun X, Feng X, Chen J, Li L, Liu J (2018) Methionine sulfoxide reductase B1 regulates hepatocellular carcinoma cell proliferation and invasion via the mitogen-activated protein kinase pathway and epithelial-mesenchymal transition. Oxid Med Cell Longev 2018:5287971

    PubMed  PubMed Central  Google Scholar 

  • Hunnicut JL, Liu Y, Richardson A, Salmon AB (2015) MsrA overexpression targeted to the mitochondria, but not cytosol, preserves insulin sensitivity in diet-induced obese mice. PLoS ONE 10(10):e0139844

    PubMed  PubMed Central  Google Scholar 

  • Jiang B, Moskovitz J (2018) The functions of the mammalian methionine sulfoxide reductase system and related diseases. Antioxidants (basel) 7(9):E122. https://doi.org/10.3390/antiox7090122

    Article  CAS  Google Scholar 

  • Jiang J, Adams Z, Moonah S, Shi S, Furlow JM, Moskovitz J (2020) The antioxidant enzyme methionine sulfoxide reductase A (MsrA) interacts with Jab1/CSN5 and regulates its function. Antioxidants (basel) 9(5):452–469

    CAS  Google Scholar 

  • Kanayama A, Inoue J, Sugita-Konishi Y, Shimizu M, Miyamoto Y (2002) Oxidation of IκBα at methionine 45 is one cause of taurine chloramine-induced inhibition of NF-κB activation. J Biol Chem 277:24049–24056

    CAS  PubMed  Google Scholar 

  • Knowles MR, Drumm M (2012) The influence of genetics on cystic fibrosis phenotypes. Cold Spring Harb Perspect Med 2(12):a009548

    PubMed  PubMed Central  Google Scholar 

  • Kwak GH, Kim HY (2017) MSRB3 deficiency induces cancer cell apoptosis through p53-independent and ER stress-dependent pathways. Arch Biochem Biophys 621:1–5

    CAS  PubMed  Google Scholar 

  • Kwon TJ, Cho HJ, Kim UK, Lee E, Oh SK, Bok J, Bae YC, Yi JK, Lee JW, Ryoo ZY et al (2014) Methionine sulfoxide reductase B3 deficiency causes hearing loss due to stereocilia degeneration and apoptotic cell death in cochlear hair cells. Hum Mol Genet 23:1591–1601

    CAS  PubMed  Google Scholar 

  • Lee E, Kwak GH, Kamble K, Kim HY (2014) Methionine sulfoxide reductase B3 deficiency inhibits cell growth through the activation of p53–p21 and p27 pathways. Arch Biochem Biophys 547:1–5

    CAS  PubMed  Google Scholar 

  • Lee BC, Lee SG, Choo MK, Kim JH, Lee HM, Kim S, Fomenko DE, Kim HY, Park JM, Gladyshev VN (2017) Selenoprotein MsrB1 promotes anti-inflammatory cytokine gene expression in macrophages and controls immune response in vivo. Sci Rep 7(1):5119–5128

    PubMed  PubMed Central  Google Scholar 

  • Lee SH, Lee S, Du J, Jain K, Ding M, Kadado AJ, Atteya G, Jaji Z, Tyagi T, Kim WH, Herzog RI, Patel A, Ionescu CN, Martin KA, Hwa J (2019) Mitochondrial MsrB2 serves as a switch and transducer for mitophagy. EMBO Mol Med 11(8):e10409

    PubMed  PubMed Central  Google Scholar 

  • Lee HJ, Park JS, Yoo HJ, Lee HM, Lee BC, Kim JH (2020) The selenoprotein MsrB1 instructs dendritic cells to induce T-helper 1 immune responses. Antioxidants (basel) 9(10):1021–1039

    CAS  Google Scholar 

  • Liu JS, Cui ZJ (2019) Pancreatic stellate cells serve as a brake mechanism on pancreatic acinar cell calcium signaling modulated by methionine sulfoxide reductase expression. Cells 8(2):109–133

    CAS  PubMed Central  Google Scholar 

  • Liu F, Hindupur J, Nguyen JL, Ruf KJ, Zhu J, Schieler JL, Bonham CC, Wood KV, Davisson VJ, Rochet JC (2008) Methionine sulfoxide reductase A protects dopaminergic cells from Parkinson’s disease-related insults. Free Radic Biol Med 45:242–255

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lowther WT, Weissbach H, Etienne F, Brot N, Matthews BW (2002) The mirrored methionine sulfoxide reductases of Neisseria gonorrhoeae pilB. Nat Struct Biol 9(5):348–352

    CAS  PubMed  Google Scholar 

  • Ma X, Deng W, Liu X, Li M, Chen Z, He Z, Wang Y, Wang Q, Hu X, Collier DA, Li T (2011) A genome-wide association study for quantitative traits in schizophrenia in China. Genes Brain Behav 10(7):734–739

    CAS  PubMed  Google Scholar 

  • Magon NJ, Turner R, Gearry RB, Hampton MB, Sly PD, Kettle AJ (2015) Oxidation of calprotectin by hypochlorous acid prevents chelation of essential metal ions and allows bacterial growth: relevance to infections in cystic fibrosis. Free Radic Biol Med 86:133–144

    CAS  PubMed  Google Scholar 

  • Miernyk JA, Johnston ML, Huber SC, Tovar-Méndez A, Hoyos E, Randal DD (2009) Oxidation of an adjacent methionine residueinhibits regulatory seryl-phosphorylation of pyruvate dehydrogenase. Proteom Insights 2:15–22

    CAS  Google Scholar 

  • Minniti AN, Cataldo R, Trigo C, Vasquez L, Mujica P, Leighton F, Inestrosa NC, Aldunate R (2009) Methionine sulfoxide reductase A expression is regulated by the DAF-16/FOXO pathway in Caenorhabditis elegans. Aging Cell 8(6):690–705

    CAS  PubMed  Google Scholar 

  • Misiti F, Clementi ME, Giardina B (2010) Oxidation of methionine 35 reduces toxicity of the amyloid β-peptide(1–42) in neuroblastoma cells (IMR-32) via enzyme methionine sulfoxide reductase A expression and function. Neurochem Int 56:597–602

    CAS  PubMed  Google Scholar 

  • Mochin MT, Underwood KF, Cooper B, McLenithan JC, Pierce AD, Nalvarte C, Arbiser J, Karlsson AI, Moise AR, Moskovitz J, Passaniti A (2015) Hyperglycemia and redox status regulate RUNX2 DNA-binding and an angiogenic phenotype in endothelial cells. Microvasc Res 7:55–64

    Google Scholar 

  • Morel AP, Ginestier C, Pommier RM, Cabaud O, Ruiz E, Wicinski J, Devouassoux-Shisheboran M, Combaret V, Finetti P, Chassot C et al (2017a) A stemness-related ZEB1-MSRB3 axis governs cellular pliancy and breast cancer genome. Nat Med 23:568–578

    CAS  PubMed  Google Scholar 

  • Morel AP, Ginestier C, Pommier RM, Cabaud O, Ruiz E, Wicinski J, Devouassoux-Shisheboran M, Combaret V, Finetti P, Chassot C et al (2017b) A stemness-related ZEB1-MSRB3 axis governs cellular pliancy and breast cancer genome. Nat Med 23:568–578

    CAS  PubMed  Google Scholar 

  • Moskovitz J, Stadtman ER (2003) Selenium-deficient diet enhances protein oxidation and affects methionine sulfoxide reductase (MsrB) protein level in certain mouse tissues. Proc Natl Acad Sci USA 100(13):7486–7490

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moskovitz J, Rahman MA, Strassman J, Yancey SO, Kushner SR, Brot N, Weissbach H (1995) Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage. J Bacteriol 177(3):502–507

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moskovitz J, Weissbach H, Brot N (1996) Cloning the expression of a mammalian gene involved in the reduction of methionine sulfoxide residues in proteins. Proc Natl Acad Sci U S A 93(5):2095–2099

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moskovitz J, Poston M, Berlett BS, Nosworthy JN, Szczepanowski R, Stadtman ER (2000) Identification and characterization of a putative active site for peptide-methionine sulfoxide reductase (MsrA) and its substrate stereospecificity. J Biol Chem 275:14167–14172

    CAS  PubMed  Google Scholar 

  • Moskovitz J, Bar-Noy S, Williams WM, Requena J, Berlett BS, Stadtman ER (2001) Methionine sulfoxide reductase (MsrA) is a regulator of antioxidant defense and lifespan in mammals. Proc Natl Acad Sci U S A 98(23):12920–12925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moskovitz J, Singh VK, Requena J, Wilkinson BJ, Jayaswal RK, Stadtman ER (2002) Purification and characterization of methionine sulfoxide reductases from mouse and Staphylococcus aureus and their substrate stereospecificity. Biochem Biophys Res Commun 290(1):62–65

    CAS  PubMed  Google Scholar 

  • Moskovitz J, Maiti P, Lopes DH, Oien DB, Attar A, Liu T, Mittal S, Hayes J, Bitan G (2011) Induction of methionine-sulfoxide reductases protects neurons from amyloid β-protein insults in vitro and in vivo. Biochemistry 50(49):10687–10697

    CAS  PubMed  Google Scholar 

  • Moskovitz J, Du F, Bowman CF, Yan SS (2016) Methionine sulfoxide reductase A affects -amyloid solubility and mitochondrial function in a mouse model of Alzheimer’s disease. Am J Physiol Endocrinol Metab 310:E388–E393

    PubMed  PubMed Central  Google Scholar 

  • Noh MR, Kim KY, Han SJ, Kim JI, Kim HY, Park KM (2017) Methionine sulfoxide Reductase A deficiency exacerbates cisplatin-induced nephrotoxicity via increased mitochondrial damage and renal cell death. Antioxid Redox Signal 27:727–741

    CAS  PubMed  Google Scholar 

  • Ogawa F, Sander CS, Hansel A, Oehrl W, Kasperczyk H, Elsner P, Shimizu K, Heinemann SH, Thiele LL (2006) The repair enzyme peptide methionine-S-sulfoxide reductase is expressed in human epidermis and upregulated by UVA radiation. J Invest Dermatol 126(5):1128–1134

    CAS  PubMed  Google Scholar 

  • Oien DB, Moskovitz J (2008) Substrates of the methionine sulfoxide reductase system and their physiological relevance. Curr Top Dev Biol 80:93–133

    CAS  PubMed  Google Scholar 

  • Oien DB, Moskovitz J (2019) Genetic regulation of longevity and age-associated diseases through the methionine sulfoxide reductase system. Biochim Biophys Acta Mol Basis Dis 1865(7):1756–1762

    CAS  PubMed  Google Scholar 

  • Oien DB, Osterhaus GL, Latif SA, Pinkston JW, Fulks J, Johnson MA, Fowler SC, Moskovitz J (2008) MsrA knockout mouse exhibits abnormal behavior and brain dopamine levels. Free Radic Biol Med 45(2):193–200

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oien DB, Shinogle HE, Moore DS, Moskovitz J (2009) Clearance and phosphorylation of alpha-synuclein are inhibited in methionine Sulfoxide reductase A null Yeast cells. J Mol Neuroscience 39(3):323–332

    CAS  Google Scholar 

  • Oien DB, Carrasco GA, Moskovitz J (2011) Decreased phophorylation and increased methionine oxidation of α-synuclein in the methionine sulfoxide reductase A knockout mouse. J Amino Acids (Article ID, 721094)

  • Otte DM, Raskó T, Wang M, Dreiseidler M, Drews E, Schrage H, Wojtalla A, Höhfeld J, Wanker E, Zimmer A (2014) Identification of the mitochondrial MSRB2 as a binding partner of LG72. Cell Mol Neurobiol 34(8):1123–1130

    CAS  PubMed  Google Scholar 

  • Penningtona SM, Kluthoa PR, Xiea L, Broadhursta K, Kovala OM, McCormickb ML, Spitzb DR, Grumbacha IM (2018) Defective protein repair under methionine sulfoxide A deletion drives autophagy and ARE-dependent gene transcription. Red Biol 16:401–408

    Google Scholar 

  • Rey P, Tarrago I (2018) Physiological roles of plant methionine sulfoxide reductases in redox homeostasis and signaling. Antioxidants (basel) 7(9):114. https://doi.org/10.3390/antiox7090114

    Article  CAS  Google Scholar 

  • Rose AH, Hoffmann PR (2015) Selenoproteins and cardiovascular stress. Thromb Haemost 113(3):494–504

    PubMed  Google Scholar 

  • Singh VK, Moskovitz J, Wilkinson BJ, Jayaswal RK (2001) Staphylococcus aureus that contributes to oxidative defence and is highly induced by the cell-wall-active antibiotic oxacillin. Microbiology 147(Pt 11):3037–3045

    CAS  PubMed  Google Scholar 

  • Singh MP, Kwak GH, Kim KY, Kim HY (2017a) Methionine sulfoxide reductase A protects hepatocytes against acetaminophen-induced toxicity via regulation of thioredoxin reductase 1 expression. Biochem Biophys ResCommun 487:695–701

    CAS  Google Scholar 

  • Singh MP, Kim KY, Kwak GH, Baek SH, Kim HY (2017b) Methionine sulfoxide reductase A protects against lipopolysaccharide-induced septic shock via negative regulation of the proinflammatory responses. Arch Biochem Biophys 631:42–48

    CAS  PubMed  Google Scholar 

  • Sreekumar PG, Kannan R, Yaung J, Spee CK, Ryan SJ, Hinton DR (2005) Protection from oxidative stress by methionine sulfoxide reductases in RPE cells. Biochem Biophys Res Commun 334(1):245–253

    CAS  PubMed  Google Scholar 

  • Sreekumar PG, Hinton DR, Kannan R (2011) Methionine sulfoxide reductase A: Structure, function and role in ocular pathology. World J Biol Chem 2(8):184–192

    PubMed  PubMed Central  Google Scholar 

  • Tomoda K, Kubota Y, Arata Y, Mori S, Maeda M, Tanaka T, Yoshida M, Yoneda-Kato N, Kato JY (2002) The cytoplasmic shuttling and subsequent degradation of p27Kip1 mediated by Jab1/CSN5 and the COP9 signalosome complex. J Biol Chem 277:2302–2310

    CAS  PubMed  Google Scholar 

  • Triguero L, Singh R, Prabhakar R (2008) Comparative molecular dynamics studies of wild-type and oxidized forms of full-length Alzheimer amyloid beta-peptides Abeta (1–40) and Abeta (1–42). J Phys Chem B 112:7123–7131

    CAS  PubMed  Google Scholar 

  • Walss-Bass C, Soto-Bernardini MC, Johnson-Pais T, Leach RJ, Ontiveros A, Nicolini H, Mendoza R, Jerez A, Dassori A, Chavarria-Siles I, Escamilla MA, Raventos H (2009) Methionine sulfoxide reductase: a novel schizophrenia candidate gene. Am J Med Genet B Neuropsychiatr Genet 150B(2):219–225

    CAS  PubMed  Google Scholar 

  • Wassef R, Haenold R, Hansel A, Brot N, Heinemann SH, Hoshi T (2007) Methionine sulfoxide reductase A and a dietary supplement S-methyl-l-cysteine prevent Parkinson’s-like symptoms. J Neurosci 27:12808–12816

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu PF, Xie N, Zhang JJ, Guan XL, Zhou J, Long LH, Li YL, Xiong QJ, Zeng JH, Wang F, Chen JG (2013) Resveratrol preconditioning increases methionine sulfoxide reductases A expression and enhances resistance of human neuroblastoma cells to neurotoxins. J Nutr Biochem 24(6):1070–1077

    CAS  PubMed  Google Scholar 

  • Zhong G, He Y, Wan F, Wu S, Jiang X, Tang Z, Hu L (2021) Effects of long-term exposure to copper on the Keap1/Nrf2 signaling pathway and Msr-related redox status in the kidneys of rats. Biol Trace Elem Res. https://doi.org/10.1007/s12011-020-02557-2

    Article  PubMed  Google Scholar 

  • Zhou L, Jiang Y, Luo Q, Li L, Jia L (2019) Neddylation: a novel modulator of the tumor microenvironment. Mol Cancer 18:77–88

    PubMed  PubMed Central  Google Scholar 

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  1. Department of Pharmacology and Toxicology, School of Pharmacy, University of Kansas, Lawrence, KS, 66045, USA

    Jackob Moskovitz & Adam Smith

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Moskovitz, J., Smith, A. Methionine sulfoxide and the methionine sulfoxide reductase system as modulators of signal transduction pathways: a review. Amino Acids 53, 1011–1020 (2021). https://doi.org/10.1007/s00726-021-03020-9

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