Non-enzymatic covalent modifications: a new link between metabolism and epigenetics
Qingfei Zheng, Igor Maksimovic, Akhil Upad, Yael David
Non-enzymatic covalent modifications: a new link between metabolism and epigenetics
Epigenetic modifications, including those on DNA and histones, have been shown to regulate cellular metabolism by controlling expression of enzymes involved in the corresponding metabolic pathways. In turn, metabolic flux influences epigenetic regulation by affecting the biosynthetic balance of enzyme cofactors or donors for certain chromatin modifications. Recently, non-enzymatic covalent modifications (NECMs) by chemically reactive metabolites have been reported to manipulate chromatin architecture and gene transcription through multiple mechanisms. Here, we summarize these recent advances in the identification and characterization of NECMs on nucleic acids, histones, and transcription factors, providing an additional mechanistic link between metabolism and epigenetics.
epigenetics / metabolism / non-enzymatic modification / chromatin / human disease
[1] |
Allaman I, Bélanger M, Magistretti PJ (2015) Methylglyoxal, the dark side of glycolysis. Front Neurosci 9:23
CrossRef
Google scholar
|
[2] |
Ammar R, Torti D, Tsui K, Gebbia M, Durbic T, Bader GD, Giaever G, Nislow C (2012) Chromatin is an ancient innovation conserved between Archaea and Eukarya. Elife 1:e00078
CrossRef
Google scholar
|
[3] |
Ariga H, Takahashi-Niki K, Kato I, Maita H, Niki T, Iguchi-Ariga SM (2013) Neuroprotective function of DJ-1 in Parkinson’s disease. Oxid Med Cell Longev 2013:683920
CrossRef
Google scholar
|
[4] |
Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395
CrossRef
Google scholar
|
[5] |
Basu MK, Koonin EV (2005) Evolution of eukaryotic cysteine sulfinic acid reductase, sulfiredoxin (Srx), from bacterial chromosome partitioning protein ParB. Cell Cycle 4:947–952
CrossRef
Google scholar
|
[6] |
Bierhaus A, Fleming T, Stoyanov S, Leffler A, Babes A, Neacsu C, Sauer SK, Eberhardt M, Schnölzer M, Lasitschka F
CrossRef
Google scholar
|
[7] |
Bollong MJ, Lee G, Coukos JS, Yun H, Zambaldo C, Chang JW, Chin EN, Ahmad I, Chatterjee AK, Lairson LL
CrossRef
Google scholar
|
[8] |
Bondoc FY, Bao Z, Hu WY, Gonzalez FJ, Wang Y, Yang CS, Hong JY (1999) Acetone catabolism by cytochrome P450 2E1: studies with CYP2E1-null mice. Biochem Pharmacol 58:461–463
CrossRef
Google scholar
|
[9] |
Chauvin JR, Pratt DA (2017) On the reactions of thiols, sulfenic acids, and sulfinic acids with hydrogen peroxide. Angew Chem Int Ed Engl 56:6255–6259
CrossRef
Google scholar
|
[10] |
Chen Y, Qin W, Li Z, Guo Z, Liu Y, Lan T, Wang C (2019) Site- specific chemoproteomic profiling of targets of glyoxal. Future Med Chem 11:2979–2987
CrossRef
Google scholar
|
[11] |
Commerford SL, Carsten AL, Cronkite EP (1982) Histone turnover within nonproliferating cells. Proc Natl Acad Sci USA 79:1163–1165
CrossRef
Google scholar
|
[12] |
Cripps MJ, Hanna K, Lavilla C Jr, Sayers SR, Caton PW, Sims C, De Girolamo L, Sale C, Turner MD (2017) Carnosine scavenging of glucolipotoxic free radicals enhances insulin secretion and glucose uptake. Sci Rep 7:13313
CrossRef
Google scholar
|
[13] |
Cryan JF, O’Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS, Boehme M, Codagnone MG, Cussotto S, Fulling C, Golubeva AV
CrossRef
Google scholar
|
[14] |
Cui Y, Li X, Lin J, Hao Q, Li XD (2017) Histone ketoamide adduction by 4-oxo-2-nonenal is a reversible posttranslational modification regulated by Sirt2. ACS Chem Biol 12:47–51
CrossRef
Google scholar
|
[15] |
Cuthbert GL, Daujat S, Snowden AW, Erdjument-Bromage H, Hagiwara T, Yamada M, Schneider R, Gregory PD, Tempst P, Bannister AJ
CrossRef
Google scholar
|
[16] |
Dalmasso G, Cougnoux A, Delmas J, Darfeuille-Michaud A, Bonnet R (2014) The bacterial genotoxin colibactin promotes colon tumor growth by modifying the tumor microenvironment. Gut Microbes 5:675–680
CrossRef
Google scholar
|
[17] |
Distler MG, Palmer AA (2012) Role of Glyoxalase 1 (Glo1) and methylglyoxal (MG) in behavior: recent advances and mechanis- tic insights. Front Genet 3:250
CrossRef
Google scholar
|
[18] |
Doorn JA, Petersen DR (2002) Covalent modification of amino acid nucleophiles by the lipid peroxidation products 4-hydroxy-2- nonenal and 4-oxo-2-nonenal. Chem Res Toxicol 15:1445–1450
CrossRef
Google scholar
|
[19] |
Drazic A, Myklebust LM, Ree R, Arnesen T (2016) The world of protein acetylation. Biochim Biophys Acta 1864:1372–1401
CrossRef
Google scholar
|
[20] |
Drozak J, Veiga-da-Cunha M, Vertommen D, Stroobant V, Van Schaftingen E (2010) Molecular identification of carnosine synthase as ATP-grasp domain-containing protein 1 (ATPGD1). J Biol Chem 285:9346–9356
CrossRef
Google scholar
|
[21] |
Duan X, Kelsen SG, Merali S (2008) Proteomic analysis of oxidative stress-responsive proteins in human pneumocytes: insight into the regulation of DJ-1 expression. J Proteome Res 7:4955–4961
CrossRef
Google scholar
|
[22] |
Erler J, Zhang R, Petridis L, Cheng X, Smith JC, Langowski J (2014) The role of histone tails in the nucleosome: a computational study. Biophys J 107:2911–2922
CrossRef
Google scholar
|
[23] |
Etchegaray JP, Mostoslavsky R (2016) Interplay between metabo- lism and epigenetics: A nuclear adaptation to environmental changes. Mol Cell 62:695–711
CrossRef
Google scholar
|
[24] |
Fournet M, Bonté F, Desmoulière A (2018) Glycation damage: A possible hub for major pathophysiological disorders and aging. Aging Dis 9:880–900
CrossRef
Google scholar
|
[25] |
Gaffney DO, Jennings EQ, Anderson CC, Marentette JO, Shi T, Schou Oxvig AM, Streeter MD, Johannsen M, Spiegel DA, Chapman E
|
[26] |
Galligan JJ, Rose KL, Beavers WN, Hill S, Tallman KA, Tansey WP, Marnett LJ (2014) Stable histone adduction by 4-oxo-2-nonenal: a potential link between oxidative stress and epigenetics. J Am Chem Soc 136:11864–11866
CrossRef
Google scholar
|
[27] |
Galligan JJ, Wepy JA, Streeter MD, Kingsley PJ, Mitchener MM, Wauchope OR, Beavers WN, Rose KL, Wang T, Spiegel DA
CrossRef
Google scholar
|
[28] |
García-Giménez JL, Òlaso G, Hake SB, Bönisch C, Wiedemann SM, Markovic J, Dasí F, Gimeno A, Pérez-Quilis C, Palacios O
CrossRef
Google scholar
|
[29] |
Geerlings SE, Hoepelman AI (1999) Immune dysfunction in patients with diabetes mellitus (DM). FEMS Immunol Med Microbiol 26:259–265
CrossRef
Google scholar
|
[30] |
Greetham D, Vickerstaff J, Shenton D, Perrone GG, Dawes IW, Grant CM (2010) Thioredoxins function as deglutathionylase enzymes in the yeast Saccharomyces cerevisiae. BMC Biochem 11:3
CrossRef
Google scholar
|
[31] |
Guo CJ, Chang FY, Wyche TP, Backus KM, Acker TM, Funabashi M, Taketani M, Donia MS, Nayfach S, Pollard KS
CrossRef
Google scholar
|
[32] |
Hake SB, Allis CD (2006) Histone H3 variants and their potential role in indexing mammalian genomes: the “H3 barcode hypothesis”. Proc Natl Acad Sci USA 103:6428–6435
CrossRef
Google scholar
|
[33] |
Hand CE, Honek JF (2005) Biological chemistry of naturally occurring thiols of microbial and marine origin. J Nat Prod 68:293–308
CrossRef
Google scholar
|
[34] |
Harmel R, Fiedler D (2018) Features and regulation of non- enzymatic post-translational modifications. Nat Chem Biol 14:244–252
CrossRef
Google scholar
|
[35] |
Hellwig M, Henle T (2014) Baking, ageing, diabetes: a short history of the Maillard reaction. Angew Chem Int Ed Engl 53(39):10316–10329
CrossRef
Google scholar
|
[36] |
Jakubowski H (2000) Homocysteine thiolactone: metabolic origin and protein homocysteinylation in humans. J Nutr 130:377S–381S
CrossRef
Google scholar
|
[37] |
Janke R, Dodson AE, Rine J (2015) Metabolism and epigenetics. Annu Rev Cell Dev Biol 31:473–496
CrossRef
Google scholar
|
[38] |
Jaramillo R, Shuck SC, Chan YS, Liu X, Bates SE, Lim PP, Tamae D, Lacoste S, O’Connor TR, Termini J (2017) DNA Advanced glycation end products (DNA-AGEs) are elevated in urine and tissue in an animal model of type 2 diabetes. Chem Res Toxicol 30:689–698
CrossRef
Google scholar
|
[39] |
Jawahar MC, Murgatroyd C, Harrison EL, Baune BT (2015) Epigenetic alterations following early postnatal stress: a review on novel aetiological mechanisms of common psychiatric disor- ders. Clin Epigenet 7:122
CrossRef
Google scholar
|
[40] |
Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080
CrossRef
Google scholar
|
[41] |
Jiang T, Zhou X, Taghizadeh K, Dong M, Dedon PC (2007) N-formylation of lysine in histone proteins as a secondary modification arising from oxidative DNA damage. Proc Natl Acad Sci USA 104:60–65
CrossRef
Google scholar
|
[42] |
Kansanen E, Kuosmanen SM, Leinonen H, Levonen AL (2013) The Keap1-Nrf2 pathway: Mechanisms of activation and dysregula- tion in cancer. Redox Biol 1:45–49
CrossRef
Google scholar
|
[43] |
Kawai Y, Garduño L, Theodore M, Yang J, Arinze IJ (2011) Acetylation-deacetylation of the transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2) regulates its transcriptional activity and nucleocytoplasmic localization. J Biol Chem 286:7629–7640
CrossRef
Google scholar
|
[44] |
Keum YS (2011) Regulation of the Keap1/Nrf2 system by chemo- preventive sulforaphane: implications of posttranslational modifi- cations. Ann N Y Acad Sci 1229:184–189
CrossRef
Google scholar
|
[45] |
Kim NY, Goddard TN, Sohn S, Spiegel DA, Crawford JM (2019) Biocatalytic reversal of advanced glycation end product modifi- cation. Chembiochem 20:2402–2410
CrossRef
Google scholar
|
[46] |
Kopelman P (2007) Health risks associated with overweight and obesity. Obes Rev 1:13–17
CrossRef
Google scholar
|
[47] |
Lee JY, Song J, Kwon K, Jang S, Kim C, Baek K, Kim J, Park C (2012) Human DJ-1 and its homologs are novel glyoxalases. Hum Mol Genet 21:3215–3225
CrossRef
Google scholar
|
[48] |
Li J, Liu D, Sun L, Lu Y, Zhang Z (2012) Advanced glycation end products and neurodegenerative diseases: mechanisms and perspective. J Neurol Sci 317:1–5
CrossRef
Google scholar
|
[49] |
Li Z, Quan G, Jiang X, Yang Y, Ding X, Zhang D, Wang X, Hardwidge PR, Ren W, Zhu G (2018) Effects of metabolites derived from gut microbiota and hosts on pathogens. Front Cell Infect Microbiol 8:314
CrossRef
Google scholar
|
[50] |
Linetsky M, Shipova E, Cheng R, Ortwerth BJ (2007) Glycation by ascorbic acid oxidation products leads to the aggregation of lens proteins. Biochim Biophys Acta 1782:22–34
CrossRef
Google scholar
|
[51] |
Little WC, Zile MR, Kitzman DW, Hundley WG, O’Brien TX, Degroof RC (2005) The effect of alagebrium chloride (ALT-711), a novel glucose cross-link breaker, in the treatment of elderly patients with diastolic heart failure. J Card Fail 11:191–195
CrossRef
Google scholar
|
[52] |
Maksimovic I, Ray D, Zheng Q, David Y (2019) Utilizing intein trans- splicing for in vivo generation of site-specifically modified proteins. Methods Enzymol 626:203–222
CrossRef
Google scholar
|
[53] |
Marinho HS, Real C, Cyrne L, Soares H, Antunes F (2014) Hydrogen peroxide sensing, signaling and regulation of tran- scription factors. Redox Biol 2:535–562
CrossRef
Google scholar
|
[54] |
Matafome P, Sena C, Seiça R (2013) Methylglyoxal, obesity, and diabetes. Endocrine 43:472–484
CrossRef
Google scholar
|
[55] |
Matsuda R, Bi C, Anguizola J, Sobansky M, Rodriguez E, Vargas Badilla J, Zheng X, Hage B, Hage DS (2013) Studies of metabolite-protein interactions: a review. J Chromatogr B Analyt Technol Biomed Life Sci 966:48–58
CrossRef
Google scholar
|
[56] |
Matsuda N, Kimura M, Queliconi BB, Kojima W, Mishima M, Takagi K, Koyano F, Yamano K, Mizushima T, Ito Y
CrossRef
Google scholar
|
[57] |
May-Zhang LS, Yermalitsky V, Huang J, Pleasent T, Borja MS, Oda MN, Jerome WG, Yancey PG, Linton MF, Davies SS (2018) Modification by isolevuglandins, highly reactive γ-ketoaldehydes, deleteriously alters high-density lipoprotein structure and func- tion. J Biol Chem 293:9176–9187
CrossRef
Google scholar
|
[58] |
McGinty RK, Tan S (2015) Nucleosome structure and function. Chem Rev 115:2255–2273
CrossRef
Google scholar
|
[59] |
Mitchell D 3rd, Ritchey LE, Park H, Babitzke P, Assmann SM, Bevilacqua PC (2018) Glyoxals as in vivo RNA structural probes of guanine base-pairing. RNA 24:114–124
CrossRef
Google scholar
|
[60] |
Moellering RE, Cravatt BF (2013) Functional lysine modification by an intrinsically reactive primary glycolytic metabolite. Science 341:549–553
CrossRef
Google scholar
|
[61] |
Montellier E, Gaucher J (2019) Targeting the interplay between metabolism and epigenetics in cancer. Curr Opin Oncol 31:92–99
CrossRef
Google scholar
|
[62] |
Nair DN, Prasad R, Singhal N, Bhattacharjee M, Sudhakar R, Singh P, Thanumalayan S, Kiran U, Sharma Y, Sijwali PS (2018) A conserved human DJ1-subfamily motif (DJSM) is critical for anti- oxidative and deglycase activities of Plasmodium falciparum DJ1. Mol Biochem Parasitol 222:70–80
CrossRef
Google scholar
|
[63] |
Näsström T, Fagerqvist T, Barbu M, Karlsson M, Nikolajeff F, Kasrayan A, Ekberg M, Lannfelt L, Ingelsson M, Bergström J (2011) The lipid peroxidation products 4-oxo-2-nonenal and 4-hydroxy-2-nonenal promote the formation of α-synuclein oligomers with distinct biochemical, morphological, and functional properties. Free Radic Biol Med 50:428–437
CrossRef
Google scholar
|
[64] |
Obata T (2006) Diabetes and semicarbazide-sensitive amine oxidase (SSAO) activity: a review. Life Sci 79:417–422
CrossRef
Google scholar
|
[65] |
Ochs R (2019) An idea to explore: understanding redox reactions in biochemistry. Biochem Mol Biol Educ 47:25–28
CrossRef
Google scholar
|
[66] |
Parrish JP, Kastrinsky DB, Wolkenberg SE, Igarashi Y, Boger DL (2003) NA alkylation properties of yatakemycin. J Am Chem Soc 125:10971–10976
CrossRef
Google scholar
|
[67] |
Poole LB (2015) The basics of thiols and cysteines in redox biology and chemistry. Free Radic Biol Med 80:148–157
CrossRef
Google scholar
|
[68] |
Raiber EA, Portella G, Martínez Cuesta S, Hardisty R, Murat P, Li Z, Iurlaro M, Dean W, Spindel J, Beraldi D
CrossRef
Google scholar
|
[69] |
Reid MA, Dai Z, Locasale JW (2017) The impact of cellular metabolism on chromatin dynamics and epigenetics. Nat Cell Biol 19:1298–1306
CrossRef
Google scholar
|
[70] |
Repici M, Giorgini F (2019) DJ-1 in Parkinson’s disease: Clinical insights and therapeutic perspectives. J Clin Med 8:1377
CrossRef
Google scholar
|
[71] |
Richarme G, Dairou J (2017) Parkinsonism-associated protein DJ-1 is a bona fide deglycase. Biochem Biophys Res Commun 483:387–391
CrossRef
Google scholar
|
[72] |
Richarme G, Mihoub M, Dairou J, Bui LC, Leger T, Lamouri A (2015) Parkinsonism-associated protein DJ-1/Park7 is a major protein deglycase that repairs methylglyoxal- and glyoxal-glycated cys- teine, arginine, and lysine residues. J Biol Chem 290:1885–1897
CrossRef
Google scholar
|
[73] |
Richarme G, Liu C, Mihoub M, Abdallah J, Leger T, Joly N, Liebart JC, Jurkunas UV, Nadal M, Bouloc P
CrossRef
Google scholar
|
[74] |
Rinschen MM, Ivanisevic J, Giera M, Siuzdak G (2019) Identification of bioactive metabolites using activity metabolomics. Nat Rev Mol Cell Biol 20:353–367
CrossRef
Google scholar
|
[75] |
Rydberg B, Lindahl T (1982) Nonenzymatic methylation of DNA by the intracellular methyl group donor S-adenosyl-L-methionine is a potentially mutagenic reaction. EMBO J 1:211–216
CrossRef
Google scholar
|
[76] |
Sanghvi VR, Leibold J, Mina M, Mohan P, Berishaj M, Li Z, Miele MM, Lailler N, Zhao C, de Stanchina E
CrossRef
Google scholar
|
[77] |
Schalkwijk CG, Stehouwer CDA (2020) Methylglyoxal, a highly reactive dicarbonyl compound, in diabetes, its vascular compli- cations, and other age-related diseases. Physiol Rev 100:407–461
CrossRef
Google scholar
|
[78] |
Schumacker PT (2006) Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell 10:175–176
CrossRef
Google scholar
|
[79] |
Shuck SC, Wuenschell GE, Termini JS (2018) Product studies and mechanistic analysis of the reaction of methylglyoxal with deoxyguanosine. Chem Res Toxicol 31:105–115
CrossRef
Google scholar
|
[80] |
Shuker DE, Prevost V, Friesen MD, Lin D, Ohshima H, Bartsch H (1993) Urinary markers for measuring exposure to endogenous and exogenous alkylating agents and precursors. Environ Health Perspect 99:33–37
CrossRef
Google scholar
|
[81] |
Singh R, Barden A, Mori T, Beilin L (2001) Advanced glycation end- products: a review. Diabetologia 44:129–146
CrossRef
Google scholar
|
[82] |
Spiro RG (2002) Protein glycosylation: nature, distribution, enzy- matic formation, and disease implications of glycopeptide bonds. Glycobiology 12:43R–56R
CrossRef
Google scholar
|
[83] |
Sun R, Fu L, Liu K, Tian C, Yang Y, Tallman KA, Porter NA, Liebler DC, Yang J (2017) Chemoproteomics reveals chemical diversity and dynamics of 4-oxo-2-nonenal modifications in cells. Mol Cell Proteomics 16:1789–1800
CrossRef
Google scholar
|
[84] |
Suzuki A, Yamada R, Chang X, Tokuhiro S, Sawada T, Suzuki M, Nagasaki M, Nakayama-Hamada M, Kawaida R, Ono M
CrossRef
Google scholar
|
[85] |
Synold T, Xi B, Wuenschell GE, Tamae D, Figarola JL, Rahbar S, Termini J (2008) Advanced glycation end products of DNA: quantification of N2-(1-Carboxyethyl)-2’-deoxyguanosine in bio- logical samples by liquid chromatography electrospray ionization tandem mass spectrometry. Chem Res Toxicol 21:2148–2155
CrossRef
Google scholar
|
[86] |
Szende B, Tyihák E (2010) Effect of formaldehyde on cell prolifer- ation and death. Cell Biol Int 34:1273–1282
CrossRef
Google scholar
|
[87] |
Szwergold BS, Howell S, Beisswenger PJ (2001) Human fruc- tosamine-3-kinase: purification, sequencing, substrate specificity, and evidence of activity in vivo. Diabetes 50:2139–2147
CrossRef
Google scholar
|
[88] |
Taira T, Saito Y, Niki T, Iguchi-Ariga SM, Takahashi K, Ariga H (2004) DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep 5:213–218
CrossRef
Google scholar
|
[89] |
Talasz H, Wasserer S, Puschendorf B (2002) Nonenzymatic glycation of histones in vitro and in vivo. J Cell Biochem 85:24–34
CrossRef
Google scholar
|
[90] |
Tamae D, Lim P, Wuenschell GE, Termini J (2011) Mutagenesis and repair induced by the DNA advanced glycation end product N2-1- (carboxyethyl)-2’-deoxyguanosine in human cells. Biochemistry 50:2321–2329
CrossRef
Google scholar
|
[91] |
Teodorowicz M, Hendriks WH, Wichers HJ, Savelkoul HFJ (2018) Immunomodulation by Processed Animal Feed: the role of maillard reaction products and advanced glycation end-products (AGEs). Front Immunol 9:2088
CrossRef
Google scholar
|
[92] |
Toyoda Y, Erkut C, Pan-Montojo F, Boland S, Stewart MP, Müller DJ, Wurst W, Hyman AA, Kurzchalia TV (2014) Products of the Parkinson’s disease-related glyoxalase DJ-1, D-lactate and glycolate, support mitochondrial membrane potential and neu- ronal survival. Biol Open 3:777–784
CrossRef
Google scholar
|
[93] |
Trerotola M, Relli V, Simeone P, Alberti S (2015) Epigenetic inheritance and the missing heritability. Hum Genomics 9:17
CrossRef
Google scholar
|
[94] |
Tzika E, Dreker T, Imhof A (2018) Epigenetics and metabolism in health and disease. Front Genet 9:361
CrossRef
Google scholar
|
[95] |
Van Laer K, Hamilton CJ, Messens J (2013) Low-molecular-weight thiols in thiol-disulfide exchange. Antioxid Redox Signal 18:1642–1653
CrossRef
Google scholar
|
[96] |
Van Schaftingen E, Delpierre G, Collard F, Fortpied J, Gemayel R, Wiame E, Veiga-da-Cunha M (2007) Fructosamine 3-kinase and other enzymes involved in protein deglycation. Adv Enzyme Regul 47:261–269
CrossRef
Google scholar
|
[97] |
Veiga da-Cunha M, Jacquemin P, Delpierre G, Godfraind C, Théate I, Vertommen D, Clotman F, Lemaigre F, Devuyst O, Van Schaftingen E (2006) Increased protein glycation in fructosamine 3-kinase-deficient mice. Biochem J 399:257–264
CrossRef
Google scholar
|
[98] |
Wagner GR, Hirschey MD (2014) Nonenzymatic protein acylation as a carbon stress regulated by sirtuin deacylases. Mol Cell 54:5–16
CrossRef
Google scholar
|
[99] |
Wang Y, Wysocka J, Sayegh J, Lee YH, Perlin JR, Leonelli L, Sonbuchner LS, McDonald CH, Cook RG, Dou Y
CrossRef
Google scholar
|
[100] |
Wanner MJ, Zuidinga E, Tromp DS, Vilím J, Jørgensen SI, van Maarseveen JH (2020) Synthetic evidence of the Amadori-type alkylation of biogenic amines by the neurotoxic metabolite dopegal. J Org Chem 85:1202–1207
CrossRef
Google scholar
|
[101] |
Wei B, Berning K, Quan C, Zhang YT (2017) Glycation of antibodies: Modification, methods and potential effects on biological func- tions. MAbs 9:586–594
CrossRef
Google scholar
|
[102] |
Weng X, Gong J, Chen Y, Wu T, Wang F, Yang S, Yuan Y, Luo G, Chen K, Hu L
|
[103] |
Wilson MR, Jiang Y, Villalta PW, Stornetta A, Boudreau PD, Carrá A, Brennan CA, Chun E, Ngo L, Samson LD
CrossRef
Google scholar
|
[104] |
Wuenschell GE, Tamae D, Cercillieux A, Yamanaka R, Yu C, Termini J (2010) Mutagenic potential of DNA glycation: miscoding by (R)- and (S)-N2-(1-carboxyethyl)-2’-deoxyguanosine. Biochemistry 49:1814–1821
CrossRef
Google scholar
|
[105] |
Xu Y, Chen X (2006) Glyoxalase II, a detoxifying enzyme of glycolysis byproduct methylglyoxal and a target of p63 and p73, is a pro-survival factor of the p53 family. J Biol Chem 281:26702–26713
CrossRef
Google scholar
|
[106] |
Xu H, Huang W, He QL, Zhao ZX, Zhang F, Wang R, Kang J, Tang GL (2012) Self-resistance to an antitumor antibiotic: a DNA glycosylase triggers the base-excision repair system in yatake- mycin biosynthesis. Angew Chem Int Ed Engl 51:10532–10536
CrossRef
Google scholar
|
[107] |
Xu L, Chen J, Gao J, Yu H, Yang P (2015) Crosstalk of homocysteinylation, methylation and acetylation on histone H3. Analyst 140:3057–3063
CrossRef
Google scholar
|
[108] |
Zhang Z, Smith BA, Wang L, Brock A, Cho C, Schultz PG (2003) A new strategy for the site-specific modification of proteins in vivo. Biochemistry 42:6735–6746
CrossRef
Google scholar
|
[109] |
Zhang DD, Lo SC, Cross JV, Templeton DJ, Hannink M (2004) Keap1 is a redox-regulated substrate adaptor protein for a Cul3- dependent ubiquitin ligase complex. Mol Cell Biol 24:10941–10953
CrossRef
Google scholar
|
[110] |
Zhang Q, Bai B, Mei X, Wan C, Cao H, Li Dan, Wang S, Zhang M, Wang Z, Wu J
CrossRef
Google scholar
|
[111] |
Zhang D, Tang Z, Huang H, Zhou G, Cui C, Weng Y, Liu W, Kim S, Lee S, Perez-Neut M
CrossRef
Google scholar
|
[112] |
Zheng Q, Prescott NA, Maksimovic I, David Y (2019a) (De)Toxifying the epigenetic code. Chem Res Toxicol 32:796–807
CrossRef
Google scholar
|
[113] |
Zheng Q, Omans ND, Leicher R, Osunsade A, Agustinus AS, Finkin-Groner E, D’Ambrosio H, Liu B, Chandarlapaty S, Liu S
CrossRef
Google scholar
|
[114] |
Zheng Q, Osunsade A, David Y (2019) Protein arginine deiminase 4 antagonizes methylglyoxal-induced histone glycation. bioRxiv
CrossRef
Google scholar
|
[115] |
Zheng Q, Maksimovic I, Upad A, Guber D, David Y (2020) Synthesis of an alkynyl methylglyoxal probe to investigate nonenzymatic histone glycation. J Org Chem 85:1691–1697
CrossRef
Google scholar
|
[116] |
Zhu Y, Snooks H, Sang S (2018) Complexity of advanced glycation end products in foods: Where are we now? J Agric Food Chem 66:1325
CrossRef
Google scholar
|
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