Skip to main content

Advertisement

Log in

Modulating protein activity and cellular function by methionine residue oxidation

  • Review Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

The sulfur-containing amino acid residue methionine (Met) in a peptide/protein is readily oxidized to methionine sulfoxide [Met(O)] by reactive oxygen species both in vitro and in vivo. Methionine residue oxidation by oxidants is found in an accumulating number of important proteins. Met sulfoxidation activates calcium/calmodulin-dependent protein kinase II and the large conductance calcium-activated potassium channels, delays inactivation of the Shaker potassium channel ShC/B and L-type voltage-dependent calcium channels. Sulfoxidation at critical Met residues inhibits fibrillation of atherosclerosis-related apolipoproteins and multiple neurodegenerative disease-related proteins, such as amyloid beta, α-synuclein, prion, and others. Methionine residue oxidation is also correlated with marked changes in cellular activities. Controlled key methionine residue oxidation may be used as an oxi-genetics tool to dissect specific protein function in situ.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abiria SA, Colbran RJ (2010) CaMKII associates with CaV1.2 L-type calcium channels via selected beta subunits to enhance regulatory phosphorylation. J Neurochem 112:150–161

    Article  PubMed  CAS  Google Scholar 

  • An YP, Xiao R, Cui H, Cui ZJ (2003) Selective activation by photodynamic action of cholecystokinin receptor in the freshly isolated rat pancreatic acini. Br J Pharmacol 139:872–880

    Article  PubMed  CAS  Google Scholar 

  • Anbanandam A, Bieber Urbauer RJ, Bartlett RK, Smallwood HS, Squier TC, Urbauer JL (2005) Mediating molecular recognition by methionine oxidation: conformational switching by oxidation of methionine in the carboxyl-terminal domain of calmodulin. Biochemistry 44:9486–9496

    Article  PubMed  CAS  Google Scholar 

  • Bartlett RK, Bieber Urbauer RJ, Anbanandam A, Smallwood HS, Urbauer JL, Squier TC (2003) Oxidation of Met144 and Met145 in calmodulin blocks calmodulin dependent activation of the plasma membrane Ca-ATPase. Biochemistry 42:3231–3238

    Article  PubMed  CAS  Google Scholar 

  • Bergström AL, Chabry J, Bastholm L, Heegaard PM (2007) Oxidation reduces the fibrillation but not the neurotoxicity of the prion peptide PrP106–126. Biochim Biophys Acta 1774:1118–1127

    Article  PubMed  CAS  Google Scholar 

  • Bertolotti-Ciarlet A, Wang W, Lownes R, Pristatsky P, Fang Y, McKelvey T, Li Y, Li Y, Drummond J, Prueksaritanont T, Vlasak J (2009) Impact of methionine oxidation on the binding of human IgG1 to Fc Rn and Fc gamma receptors. Mol Immunol 46:1878–1882

    Article  PubMed  CAS  Google Scholar 

  • Binger KJ, Griffin MD, Heinemann SH, Howlett GJ (2010) Methionine-oxidized amyloid fibrils are poor substrates for human methionine sulfoxide reductases A and B2. Biochemistry 49:2981–2983

    Article  PubMed  CAS  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 125:15359–15365

    Article  PubMed  CAS  Google Scholar 

  • Bolanos-Garcia VM, Miguel RN (2003) On the structure and function of apolipoproteins: more than a family of lipid-binding proteins. Prog Biophys Mol Biol 83:47–68

    Article  PubMed  CAS  Google Scholar 

  • Breitenbach T, Ogilby PR, Lambert JD (2010) Effect of intracellular photosensitized singlet oxygen production on the electrophysiological properties of cultured rat hippocampal neurons. Photochem Photobiol Sci 9:1621–1633

    Article  PubMed  CAS  Google Scholar 

  • Breydo L, Bocharova OV, Makarava N, Salnikov VV, Anderson M, Baskakov IV (2005) Methionine oxidation interferes with conversion of the prion protein into the fibrillar proteinase K-resistant conformation. Biochemistry 44:15534–15543

    Article  PubMed  CAS  Google Scholar 

  • Brosnan JT, Brosnan ME, Bertolo RFP (2007) Methionine: a metabolically unique amino acid. Livest Sci 112:2–7

    Article  Google Scholar 

  • Bulina ME, Chudakov DM, Britanova OV, Yanushevich YG, Staroverov DB, Chepurnykh TV, Merzlyak EM, Shkrob MA, Lukyanov S, Lukyanov KA (2006) A genetically encoded photosensitizer. Nat Biotechnol 24:95–99

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Butterfield DA, Galvan V, Lange MB, Tang H, Sowell RA, Spilman P, Fombonne J, Gorostiza O, Zhang J, Sultana R, Bredesen DE (2010) In vivo oxidative stress in brain of Alzheimer disease transgenic mice: requirement for methionine 35 in amyloid beta-peptide of APP. Free Radic Biol Med 48:136–144

    Article  PubMed  CAS  Google Scholar 

  • Canello T, Engelstein R, Moshel O, Xanthopoulos K, Juanes ME, Langeveld J, Sklaviadis T, Gasset M, Gabizon R (2008) Methionine sulfoxides on PrPSc: a prion-specific covalent signature. Biochemistry 47:8866–8873

    Article  PubMed  CAS  Google Scholar 

  • Canello T, Frid K, Gabizon R, Lisa S, Friedler A, Moskovitz J, Gasset M, Gabizon R (2010) Oxidation of Helix-3 methionines precedes the formation of PK resistant PrP. PLoS Pathol 6:e1000977

    Article  CAS  Google Scholar 

  • Carpentier P, Violot S, Blanchoin L, Bourgeois D (2009) Structural basis for the phototoxicity of the fluorescent protein KillerRed. FEBS Lett 583:2839–2842

    Article  PubMed  CAS  Google Scholar 

  • Chen J, Avdonin V, Ciorba MA, Heinemann SH, Hoshi T (2000) Acceleration of P/C-type inactivation in voltage-gated K+ channels by methionine oxidation. Biophys J 78:174–187

    Article  PubMed  CAS  Google Scholar 

  • Choi J, Sullards MC, Olzmann JA, Rees HD, Weintraub ST, Bostwick DE, Gearing M, Levey AI, Chin LS, Li L (2006) Oxidative damage of DJ-1 is linked to sporadic Parkinson and Alzheimer diseases. J Biol Chem 281:10816–10824

    Article  PubMed  CAS  Google Scholar 

  • Chu ST, Chu CC, Tseng CC, Chen YH (1993) Met-8 of the beta 1-bungarotoxin phospholipase A2 subunit is essential for the phospholipase A2-independent neurotoxic effect. Biochem J 295:713–718

    PubMed  CAS  Google Scholar 

  • Ciorba MA, Heinemann SH, Weissbach H, Brot N, Hoshi T (1997) Modulation of potassium channel function by methionine oxidation and reduction. Proc Natl Acad Sci USA 94:9932–9937

    Article  PubMed  CAS  Google Scholar 

  • Clementi ME, Pezzotti M, Orsini F, Sampaolese B, Mezzogori D, Grassi C, Giardina B, Misiti F (2006) Alzheimer’s amyloid beta-peptide (1–42) induces cell death in human neuroblastoma via bax/bcl-2 ratio increase: an intriguing role for methionine 35. Biochem Biophys Res Commun 342:206–213

    Article  PubMed  CAS  Google Scholar 

  • Colbran RJ (1993) Inactivation of Ca2+/calmodulin-dependent protein kinase II by basal autophosphorylation. J Biol Chem 268:7163–7170

    PubMed  CAS  Google Scholar 

  • Colombo G, Meli M, Morra G, Gabizon R, Gasset M (2009) Methionine sulfoxides on prion protein Helix-3 switch on the alpha-fold destabilization required for conversion. PLoS One 4:e4296

    Article  PubMed  CAS  Google Scholar 

  • Cui ZJ (1997) Muscarinic stimulation of calcium/calmodulin-dependent protein kinase II in isolated rat pancreatic acini. Acta Pharmacol Sin 18:61–63

    Google Scholar 

  • Cui ZJ (2005) Ligand-independent receptor activation. In: Chen YZ, Lin QS (eds) Single molecule behaviors in the life sciences. The Science Press, Beijing, pp 86–102 (in Chinese)

    Google Scholar 

  • Cui ZJ, Kanno T (1997) Photodynamic triggering of calcium oscillation in the isolated rat pancreatic acini. J Physiol (Lond) 504:47–55

    Article  CAS  Google Scholar 

  • Cui ZJ, Habara Y, Wang DY, Kanno T (1997) A novel aspect of photodynamic action: induction of recurrent spikes in cytosolic calcium concentration. Photochem Photobiol 65:382–386

    Article  PubMed  CAS  Google Scholar 

  • Cui J, Yang H, Lee US (2009) Molecular mechanisms of BK channel activation. Cell Mol Life Sci 66:852–875

    Article  PubMed  CAS  Google Scholar 

  • Dalle-Donne I, Rossi R, Giustarini D, Gagliano N, Di Simplicio P, Colombo R, Milzani A (2002) Methionine oxidation as a major cause of the functional impairment of oxidized actin. Free Radic Biol Med 32:927–937

    Article  PubMed  CAS  Google Scholar 

  • Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, Lowe JS, O’Donnell SE, Aykin-Burns N, Zimmerman MC, Zimmerman K, Ham AJ, Weiss RM, Spitz DR, Shea MA, Colbran RJ, Mohler PJ, Anderson ME (2008) A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133:462–474

    Article  PubMed  CAS  Google Scholar 

  • Fernández-Irigoyen J, Santamaría E, Sesma L, Muñoz J, Riezu JI, Caballería J, Lu SC, Prieto J, Mato JM, Avila MA, Corrales FJ (2005) Oxidation of specific methionine and tryptophan residues of apolipoprotein A-I in hepatocarcinogenesis. Proteomics 5:4964–4972

    Article  PubMed  CAS  Google Scholar 

  • Garner B, Waldeck AR, Witting PK, Rye KA, Stocker R (1998a) Oxidation of high density lipoproteins. II. Evidence for direct reduction of lipid hydroperoxides by methionine residues of apolipoproteins AI and AII. J Biol Chem 273:6088–6095

    Article  PubMed  CAS  Google Scholar 

  • Garner B, Witting PK, Waldeck AR, Christison JK, Raftery M, Stocker R (1998b) Oxidation of high density lipoproteins. I. Formation of methionine sulfoxide in apolipoproteins AI and AII is an early event that accompanies lipid peroxidation and can be enhanced by alpha-tocopherol. J Biol Chem 273:6080–6087

    Article  PubMed  CAS  Google Scholar 

  • Gaza-Bulseco G, Faldu S, Hurkmans K, Chumsae C, Liu H (2008) Effect of methionine oxidation of a recombinant monoclonal antibody on the binding affinity to protein A and protein G. J Chromatogr B Anal Technol Biomed Life Sci 870:55–62

    Article  CAS  Google Scholar 

  • Giglione C, Vallon O, Meinnel T (2003) Control of protein life-span by N-terminal methionine excision. EMBO J 22:13–23

    Article  PubMed  CAS  Google Scholar 

  • Glaser CB, Morser J, Clarke JH, Blasko E, McLean K, Kuhn I, Chang RJ, Lin JH, Vilander L, Andrews WH, Light DR (1992) Oxidation of a specific methionine in thrombomodulin by activated neutrophil products blocks cofactor activity. A potential rapid mechanism for modulation of coagulation. J Clin Invest 90:2565–2573

    Article  PubMed  CAS  Google Scholar 

  • Grabenauer M, Wu C, Soto P, Shea JE, Bowers MT (2010) Oligomers of the prion protein fragment 106–126 are likely assembled from beta-hairpins in solution, and methionine oxidation inhibits assembly without altering the peptide’s monomeric conformation. J Am Chem Soc 132:532–539

    Article  PubMed  CAS  Google Scholar 

  • Han ZQ, Cui ZJ (2010) Reversible methionine residue oxidation in signalling proteins and methionine sulfoxide reductases. Acta Biophys Sin 26:861–879

    Google Scholar 

  • Hatters DM, Howlett GJ (2002) The structural basis for amyloid formation by plasma apolipoproteins: a review. Eur Biophys J 31:2–8

    Article  PubMed  CAS  Google Scholar 

  • Hokenson MJ, Uversky VN, Goers J, Yamin G, Munishkina LA, Fink AL (2004) Role of individual methionines in the fibrillation of methionine-oxidized alpha-synuclein. Biochemistry 43:4621–4633

    Article  PubMed  CAS  Google Scholar 

  • Hou L, Kang I, Marchant RE, Zagorski MG (2002) Methionine 35 oxidation reduces fibril assembly of the amyloid abeta-(1–42) peptide of Alzheimer’s disease. J Biol Chem 277:40173–40176

    Article  PubMed  CAS  Google Scholar 

  • Hou L, Shao H, Zhang Y, Li H, Menon NK, Neuhaus EB, Brewer JM, Byeon IJ, Ray DG, Vitek MP, Iwashita T, Makula RA, Przybyla AB, Zagorski MG (2004) Solution NMR studies of the A beta(1–40) and A beta(1–42) peptides establish that the Met35 oxidation state affects the mechanism of amyloid formation. J Am Chem Soc 126:1992–2005

    Article  PubMed  CAS  Google Scholar 

  • Hou S, Heinemann SH, Hoshi T (2009) Modulation of BKCa channel gating by endogenous signaling molecules. Physiology (Bethesda) 24:26–35

    Google Scholar 

  • Huang Z, Prusiner SB, Cohen FE (1996) Scrapie prions: a three-dimensional model of an infectious fragment. Fold Des 1:13–19

    Article  PubMed  CAS  Google Scholar 

  • Johansson AS, Bergquist J, Volbracht C, Päiviö A, Leist M, Lannfelt L, Westlind-Danielsson A (2007a) Attenuated amyloid-beta aggregation and neurotoxicity owing to methionine oxidation. Neuroreport 18:559–563

    Article  PubMed  CAS  Google Scholar 

  • Johansson AS, Garlind A, Berglind-Dehlin F, Karlsson G, Edwards K, Gellerfors P, Ekholm-Pettersson F, Palmblad J, Lannfelt L (2007b) Docosahexaenoic acid stabilizes soluble amyloid-beta protofibrils and sustains amyloid-beta-induced neurotoxicity in vitro. FEBS J 274:990–1000

    Article  PubMed  CAS  Google Scholar 

  • Kadlcik V, Sicard-Roselli C, Mattioli TA, Kodicek M, Houee-Levin C (2004) One-electron oxidation of beta-amyloid peptide: sequence modulation of reactivity. Free Radic Biol Med 37:881–891

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kassmann M, Hansel A, Leipold E, Birkenbeil J, Lu SQ, Hoshi T, Heinemann SH (2008) Oxidation of multiple methionine residues impairs rapid sodium channel inactivation. Pflugers Arch 456:1085–1095

    Article  PubMed  CAS  Google Scholar 

  • Kornfelt T, Persson E, Palm L (1999) Oxidation of methionine residues in coagulation factor VIIa. Arch Biochem Biophys 363:43–54

    Article  PubMed  CAS  Google Scholar 

  • Legge FS, Binger KJ, Griffin MD, Howlett GJ, Scanlon D, Treutlein H, Yarovsky I (2009) Effect of oxidation and mutation on the conformational dynamics and fibril assembly of amyloidogenic peptides derived from apolipoprotein C-II. J Phys Chem B 113:14006–14014

    Article  PubMed  CAS  Google Scholar 

  • Leong SL, Pham CL, Galatis D, Fodero-Tavoletti MT, Perez K, Hill AF, Masters CL, Ali FE, Barnham KJ, Cappai R (2009) Formation of dopamine-mediated alpha-synuclein-soluble oligomers requires methionine oxidation. Free Radic Biol Med 46:1328–1337

    Article  PubMed  CAS  Google Scholar 

  • Li A, Ségui J, Heinemann SH, Hoshi T (1998) Oxidation regulates cloned neuronal voltage-dependent Ca2+ channels expressed in Xenopus oocytes. J Neurosci 18:6740–6747

    PubMed  CAS  Google Scholar 

  • Liu D, Ren D, Huang H, Dankberg J, Rosenfeld R, Cocco MJ, Li L, Brems DN, Remmele RL Jr (2008a) Structure and stability changes of human IgG1 Fc as a consequence of methionine oxidation. Biochemistry 47:5088–5100

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Maiti P, Piacentini R, Ripoli C, Grassi C, Bitan G (2011) Surprising toxicity and assembly behaviour of amyloid β-protein oxidized to sulfone. Biochem J 433:323–332

    Article  PubMed  CAS  Google Scholar 

  • Meyer T, Hanson PI, Stryer L, Schulman H (1992) Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science 256:1199–1202

    Article  PubMed  CAS  Google Scholar 

  • Midwinter RG, Cheah FC, Moskovitz J, Vissers MC, Winterbourn CC (2006) IkappaB is a sensitive target for oxidation by cell-permeable chloramines: inhibition of NF-kappaB activity by glycine chloramine through methionine oxidation. Biochem J 396:71–78

    Article  PubMed  CAS  Google Scholar 

  • Misiti F, Martorana GE, Nocca G, Di Stasio E, Giardina B, Clementi ME (2004) Methionine 35 oxidation reduces toxic and pro-apoptotic effects of the amyloid beta-protein fragment (31–35) on isolated brain mitochondria. Neuroscience 126:297–303

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nakao LS, Iwai LK, Kalil J, Augusto O (2003) Radical production from free and peptide-bound methionine sulfoxide oxidation by peroxynitrite and hydrogen peroxide/iron(II). FEBS Lett 547:87–91

    Article  PubMed  CAS  Google Scholar 

  • Nohl H, Gille L, Staniek K (2005) Intracellular generation of reactive oxygen species by mitochondria. Biochem Pharmacol 69:719–723

    Article  PubMed  CAS  Google Scholar 

  • Nomura T, Kamada R, Ito I, Chuman Y, Shimohigashi Y, Sakaguchi K (2009) Oxidation of methionine residue at hydrophobic core destabilizes p53 tetrameric structure. Biopolymers 91:78–84

    Article  PubMed  CAS  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 Neurosci 39:323–332

    Article  PubMed  CAS  Google Scholar 

  • Pal R, Oien DB, Ersen FY, Moskovitz J (2007) Elevated levels of brain-pathologies associated with neurodegenerative diseases in the methionine sulfoxide reductase A knockout mouse. Exp Brain Res 180:765–774

    Article  PubMed  CAS  Google Scholar 

  • Pan H, Chen K, Chu L, Kinderman F, Apostol I, Huang G (2009) Methionine oxidation in human IgG2 Fc decreases binding affinities to protein A and FcRn. Protein Sci 18:424–433

    Article  PubMed  CAS  Google Scholar 

  • Piacentini R, Ripoli C, Leone L, Misiti F, Clementi ME, D’Ascenzo M, Giardina B, Azzena GB, Grassi C (2008) Role of methionine 35 in the intracellular Ca2+ homeostasis dysregulation and Ca2+-dependent apoptosis induced by amyloid beta-peptide in human neuroblastoma IMR32 cells. J Neurochem 107:1070–1082

    PubMed  CAS  Google Scholar 

  • Pooler J (1972) Photodynamic alteration of sodium currents in lobster axons. J Gen Physiol 60:367–387

    Article  PubMed  CAS  Google Scholar 

  • Prusiner SB (2001) Shattuck lecture—neurodegenerative diseases and prions. N Engl J Med 344:1516–1526

    Google Scholar 

  • Redecke L, Binder S, Elmallah MI, Broadbent R, Tilkorn C, Schulz B, May P, Goos A, Eich A, Rübhausen M, Betzel C (2009) UV-light-induced conversion and aggregation of prion proteins. Free Radic Biol Med 46:1353–1361

    Google Scholar 

  • Rekas A, Knott RB, Sokolova A, Barnham KJ, Perez KA, Masters CL, Drew SC, Cappai R, Curtain CC, Pham CL (2010) The structure of dopamine induced alpha-synuclein oligomers. Eur Biophys J 39:1407–1419

    Article  PubMed  CAS  Google Scholar 

  • Requena JR, Dimitrova MN, Legname G, Teijeira S, Prusiner SB, Levine RL (2004) Oxidation of methionine residues in the prion protein by hydrogen peroxide. Arch Biochem Biophys 432:188–195

    Article  PubMed  CAS  Google Scholar 

  • Robison AJ, Winder DG, Colbran RJ, Bartlett RK (2007) Oxidation of calmodulin alters activation and regulation of CaMKII. Biochem Biophys Res Commun 356:97–101

    Article  PubMed  CAS  Google Scholar 

  • Roy A, Carpentier P, Bourgeois D, Field M (2010) Diffusion pathways of oxygen species in the phototoxic fluorescent protein KillerRed. Photochem Photobiol Sci 9:1342–1350

    Article  PubMed  CAS  Google Scholar 

  • Sacksteder CA, Whittier JE, Xiong Y, Li J, Galeva NA, Jacoby ME, Purvine SO, Williams TD, Rechsteiner MC, Bigelow DJ, Squier TC (2006) Tertiary structural rearrangements upon oxidation of Methionine145 in calmodulin promotes targeted proteasomal degradation. Biophys J 91:1480–1493

    Article  PubMed  CAS  Google Scholar 

  • Santarelli LC, Chen J, Heinemann SH, Hoshi T (2004) The beta1 subunit enhances oxidative regulation of large-conductance calcium-activated K+ channels. J Gen Physiol 124:357–370

    Article  PubMed  CAS  Google Scholar 

  • Santarelli LC, Wassef R, Heinemann SH, Hoshi T (2006) Three methionine residues located within the regulator of conductance for K+ (RCK) domains confer oxidative sensitivity to large-conductance Ca2+-activated K+ channels. J Physiol 571:329–348

    Article  PubMed  CAS  Google Scholar 

  • Schöneich C (2005) Methionine oxidation by reactive oxygen species: reaction mechanisms and relevance to Alzheimer’s disease. Biochim Biophys Acta 1703:111–119

    Article  PubMed  CAS  Google Scholar 

  • Shao B, Oda MN, Bergt C, Fu X, Green PS, Brot N, Oram JF, Heinecke JW (2006) Myeloperoxidase impairs ABCA1-dependent cholesterol efflux through methionine oxidation and site-specific tyrosine chlorination of apolipoprotein A-I. J Biol Chem 281:9001–9004

    Article  PubMed  CAS  Google Scholar 

  • Shao B, Cavigiolio G, Brot N, Oda MN, Heinecke JW (2008) Methionine oxidation impairs reverse cholesterol transport by apolipoprotein A-I. Proc Natl Acad Sci USA 105:12224–12229

    Article  PubMed  CAS  Google Scholar 

  • Sharov VS, Schöneich C (2000) Diastereoselective protein methionine oxidation by reactive oxygen species and diastereoselective repair by methionine sulfoxide reductase. Free Radic Biol Med 29:986–994

    Article  PubMed  CAS  Google Scholar 

  • Sigalov AB, Stern LJ (2001) Oxidation of methionine residues affects the structure and stability of apolipoprotein A-I in reconstituted high density lipoprotein particles. Chem Phys Lipids 113:133–146

    Article  PubMed  CAS  Google Scholar 

  • Silva CJ, Onisko BC, Dynin I, Erickson ML, Vensel WH, Requena JR, Antaki EM, Carter JM (2010) Assessing the role of oxidized methionine at position 213 in the formation of prions in hamsters. Biochemistry 49:1854–1861

    Article  PubMed  CAS  Google Scholar 

  • Song YH, Cho H, Ryu SY, Yoon JY, Park SH, Noh CI, Lee SH, Ho WK (2010) L-type Ca2+ channel facilitation mediated by H2O2-induced activation of CaMKII in rat ventricular myocytes. J Mol Cell Cardiol 48:773–780

    Article  PubMed  CAS  Google Scholar 

  • Sroussi HY, Berline J, Palefsky JM (2007) Oxidation of methionine 63 and 83 regulates the effect of S100A9 on the migration of neutrophils in vitro. J Leukoc Biol 81:818–824

    Article  PubMed  CAS  Google Scholar 

  • Su Z, Limberis J, Martin RL, Xu R, Kolbe K, Heinemann SH, Hoshi T, Cox BF, Gintant GA (2007) Functional consequences of methionine oxidation of hERG potassium channels. Biochem Pharmacol 74:702–711

    Article  PubMed  CAS  Google Scholar 

  • Sun H, Gao J, Ferrington DA, Biesiada H, Williams TD, Squier TC (1999) Repair of oxidized calmodulin by methionine sulfoxide reductase restores ability to activate the plasma membrane Ca-ATPase. Biochemistry 38:105–112

    Article  PubMed  CAS  Google Scholar 

  • Taggart C, Cervantes-Laurean D, Kim G, McElvaney NG, Wehr N, Moss J, Levine RL (2000) Oxidation of either methionine 351 or methionine 358 in alpha 1-antitrypsin causes loss of anti-neutrophil elastase activity. J Biol Chem 275:27258–27265

    PubMed  CAS  Google Scholar 

  • Tang XD, Daggett H, Hanner M, Garcia ML, McManus OB, Brot N, Weissbach H, Heinemann SH, Hoshi T (2001) Oxidative regulation of large conductance calcium-activated potassium channels. J Gen Physiol 117:253–274

    Article  PubMed  CAS  Google Scholar 

  • Teh C, Chudakov DM, Poon KL, Mamedov IZ, Sek JY, Shidlovsky K, Lukyanov S, Korzh V (2010) Optogenetic in vivo cell manipulation in KillerRed-expressing zebrafish transgenics. BMC Dev Biol 10:110

    Article  PubMed  CAS  Google Scholar 

  • Tsvetkov PO, Ezraty B, Mitchell JK, Devred F, Peyrot V, Derrick PJ, Barras F, Makarov AA, Lafitte D (2005) Calorimetry and mass spectrometry study of oxidized calmodulin interaction with target and differential repair by methionine sulfoxide reductases. Biochimie 87:473–480

    Article  PubMed  CAS  Google Scholar 

  • Uversky VN, Yamin G, Souillac PO, Goers J, Glaser CB, Fink AL (2002) Methionine oxidation inhibits fibrillation of human alpha-synuclein in vitro. FEBS Lett 517:239–244

    Article  PubMed  CAS  Google Scholar 

  • Vogt W (1995) Oxidation of methionyl residues in proteins: tools, targets, and reversal. Free Radic Biol Med 18:93–105

    Article  PubMed  CAS  Google Scholar 

  • Vougier S, Mary J, Dautin N, Vinh J, Friguet B, Ladant D (2004) Essential role of methionine residues in calmodulin binding to Bordetella pertussis adenylate cyclase, as probed by selective oxidation and repair by the peptide methionine sulfoxide reductases. J Biol Chem 279:30210–30218

    Article  PubMed  CAS  Google Scholar 

  • Wolschner C, Giese A, Kretzschmar HA, Huber R, Moroder L, Budisa N (2009) Design of anti- and pro-aggregation variants to assess the effects of methionine oxidation in human prion protein. Proc Natl Acad Sci USA 106:7756–7761

    Article  PubMed  CAS  Google Scholar 

  • Wong BS, Wang H, Brown DR, Jones IM (1999) Selective oxidation of methionine residues in prion proteins. Biochem Biophys Res Commun 259:352–355

    Article  PubMed  CAS  Google Scholar 

  • Wong YQ, Binger KJ, Howlett GJ, Griffin MD (2010) Methionine oxidation induces amyloid fibril formation by full-length apolipoprotein A-I. Proc Natl Acad Sci USA 107:1977–1982

    Article  PubMed  CAS  Google Scholar 

  • Yamin G, Glaser CB, Uversky VN, Fink AL (2003) Certain metals trigger fibrillation of methionine-oxidized alpha-synuclein. J Biol Chem 278:27630–27635

    Article  PubMed  CAS  Google Scholar 

  • Yan P, Xiong Y, Chen B, Negash S, Squier TC, Mayer MU (2006) Fluorophore-assisted light inactivation of calmodulin involves singlet-oxygen mediated cross-linking and methionine oxidation. Biochemistry 45:4736–4748

    Article  PubMed  CAS  Google Scholar 

  • Yonuschot G, Vaughn JM, Novotny JF (1992) Intracellular calcium during photodynamic permeabilization of cardiomyocytes. J Mol Cell Cardiol 24:1079–1088

    Article  PubMed  CAS  Google Scholar 

  • Zhou W, Long C, Reaney SH, Di Monte DA, Fink AL, Uversky VN (2010) Methionine oxidation stabilizes non-toxic oligomers of alpha-synuclein through strengthening the auto-inhibitory intra-molecular long-range interactions. Biochim Biophys Acta 1802:322–330

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Work supported by The MOST China “973” Program (2011CB809101), by NSFC (No. 30728020, 30870580; 30970675), and by NSFBJ (No. 5102020).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zong Jie Cui.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cui, Z.J., Han, Z.Q. & Li, Z.Y. Modulating protein activity and cellular function by methionine residue oxidation. Amino Acids 43, 505–517 (2012). https://doi.org/10.1007/s00726-011-1175-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-011-1175-9

Keywords

Navigation