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• W2522495093 abstract "Cellular proteins are constantly damaged by reactive oxygen species generated by cellular respiration. Because of its metal-chelating property, the histidine residue is easily oxidized in the presence of Cu/Fe ions and H2O2 via metal-catalyzed oxidation, usually converted to 2-oxohistidine. We hypothesized that cells may have evolved antioxidant defenses against the generation of 2-oxohistidine residues on proteins, and therefore there would be cellular proteins which specifically interact with this oxidized side chain. Using two chemically synthesized peptide probes containing 2-oxohistidine, high-throughput interactome screening was conducted using the E. coli K12 proteome microarray containing >4200 proteins. Ten interacting proteins were identified, and successfully validated using a third peptide probe, fluorescence polarization assays, as well as binding constant measurements. We discovered that 9 out of 10 identified proteins seemed to be involved in redox-related cellular functions. We also built the functional interaction network to reveal their interacting proteins. The network showed that our interacting proteins were enriched in oxido-reduction processes, ion binding, and carbon metabolism. A consensus motif was identified among these 10 bacterial interacting proteins based on bioinformatic analysis, which also appeared to be present on human S100A1 protein. Besides, we found that the consensus binding motif among our identified proteins, including bacteria and human, were located within α-helices and faced the outside of proteins. The combination of chemically engineered peptide probes with proteome microarrays proves to be an efficient discovery platform for protein interactomes of unusual post-translational modifications, and sensitive enough to detect even the insertion of a single oxygen atom in this case. Cellular proteins are constantly damaged by reactive oxygen species generated by cellular respiration. Because of its metal-chelating property, the histidine residue is easily oxidized in the presence of Cu/Fe ions and H2O2 via metal-catalyzed oxidation, usually converted to 2-oxohistidine. We hypothesized that cells may have evolved antioxidant defenses against the generation of 2-oxohistidine residues on proteins, and therefore there would be cellular proteins which specifically interact with this oxidized side chain. Using two chemically synthesized peptide probes containing 2-oxohistidine, high-throughput interactome screening was conducted using the E. coli K12 proteome microarray containing >4200 proteins. Ten interacting proteins were identified, and successfully validated using a third peptide probe, fluorescence polarization assays, as well as binding constant measurements. We discovered that 9 out of 10 identified proteins seemed to be involved in redox-related cellular functions. We also built the functional interaction network to reveal their interacting proteins. The network showed that our interacting proteins were enriched in oxido-reduction processes, ion binding, and carbon metabolism. A consensus motif was identified among these 10 bacterial interacting proteins based on bioinformatic analysis, which also appeared to be present on human S100A1 protein. Besides, we found that the consensus binding motif among our identified proteins, including bacteria and human, were located within α-helices and faced the outside of proteins. The combination of chemically engineered peptide probes with proteome microarrays proves to be an efficient discovery platform for protein interactomes of unusual post-translational modifications, and sensitive enough to detect even the insertion of a single oxygen atom in this case. The complexity of the proteome arises in a large part because of the hundreds of post-translational modifications (PTMs) 1The abbreviations used are:PTMpost-translational modificationMCOmetal-catalyzed oxidationRAGEreceptors for advanced glycation end-productsAβamyloid betaADAlzheimer's diseaseGOGene OntologyKEGGKyoto Encyclopedia of Genes and GenomesBSAbovine serum albuminTBSTTris-buffered saline with Tween 20Kddissociation constantAG peptideAGAQVAHGNEVAG, SE peptideSEAGVNHGSAGQAIA peptideIAVENVHAQGLAOxo-AG peptide, AG peptide with 2-oxohistidine residueOxo-SE peptideSE peptide with 2-oxohistidine residueOxo-IA peptideIA peptide with 2-oxohistidine residueNADPHdihydronicotinamide-adenine dinucleotide phosphate. already discovered. Many PTMs are enzyme-catalyzed, such as phosphorylation, glycosylation, or ubiquitination (1.Wold F. In vivo chemical modification of proteins (post-translational modification).Annu. Rev. Biochem. 1981; 50: 783-814Crossref PubMed Scopus (331) Google Scholar, 2.Walsh C.T. Garneau-Tsodikova S. Gatto Jr., G.J. Protein posttranslational modifications: the chemistry of proteome diversifications.Angew Chem. Int. Ed. 2005; 44: 7342-7372Crossref PubMed Scopus (1025) Google Scholar), but there are also numerous nonenzymatic PTMs caused by chemical reactions between reactive molecules and protein side chains, such as glycation, nitrosylation, and oxidation by reactive oxygen species (ROS) (3.Harding J.J. Nonenzymatic covalent posttranslational modification of proteins in vivo.Adv. Protein Chem. 1985; 37: 247-334Crossref PubMed Scopus (176) Google Scholar, 4.Davies M.J. The oxidative environment and protein damage.Biochim. Biophys. Acta. 2005; 1703: 93-109Crossref PubMed Scopus (1097) Google Scholar). When protein side chains are enzymatically modified, there are generally specialized factors in the cell to recognize such changes. For instance, 14-3-3 family protein can recognize protein phosphorylation motifs (5.Morrison D.K. The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development.Trends Cell Biol. 2009; 19: 16-23Abstract Full Text Full Text PDF PubMed Scopus (490) Google Scholar) and various lectins can recognize protein glycosylation (6.Kilpatrick D.C. Animal lectins: a historical introduction and overview.Biochim. Biophys. Acta. 2002; 1572: 187-197Crossref PubMed Scopus (373) Google Scholar). However, recognition factors may also exist for nonenzymatic PTMs, such as receptor for advanced glycation end-products (RAGE) (7.Sparvero L.J. Asafu-Adjei D. Kang R. Tang D. Amin N. Im J. Rutledge R. Lin B. Amoscato A.A. Zeh H.J. Lotze M.T. RAGE (Receptor for Advanced Glycation Endproducts), RAGE ligands, and their role in cancer and inflammation.J. Transl. Med. 2009; 7: 17Crossref PubMed Scopus (446) Google Scholar). In this study we seek to uncover cellular binding factors for 2-oxohistidine, the oxidized product of histidine, which is an important but little-understood nonenzymatic PTM. post-translational modification metal-catalyzed oxidation receptors for advanced glycation end-products amyloid beta Alzheimer's disease Gene Ontology Kyoto Encyclopedia of Genes and Genomes bovine serum albumin Tris-buffered saline with Tween 20 dissociation constant AGAQVAHGNEVAG, SE peptide IA peptide Oxo-AG peptide, AG peptide with 2-oxohistidine residue SE peptide with 2-oxohistidine residue IA peptide with 2-oxohistidine residue dihydronicotinamide-adenine dinucleotide phosphate. The generation of ROS is an unavoidable consequence of cellular respiration, which leads to the oxidation of proteins, lipids, and nucleic acids (4.Davies M.J. The oxidative environment and protein damage.Biochim. Biophys. Acta. 2005; 1703: 93-109Crossref PubMed Scopus (1097) Google Scholar, 8.Muller F.L. Lustgarten M.S. Jang Y. Richardson A. Van Remmen H. Trends in oxidative aging theories.Free Radic. Biol. Med. 2007; 43: 477-503Crossref PubMed Scopus (845) Google Scholar). ROS play regulatory roles in cellular signaling pathways under low levels (9.Ray P.D. Huang B.W. Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling.Cell Signal. 2012; 24: 981-990Crossref PubMed Scopus (2799) Google Scholar), but high levels of ROS are cytotoxic and lead to the accumulation of damaged cellular components (10.Martin K.R. Barrett J.C. Reactive oxygen species as double-edged swords in cellular processes: low-dose cell signaling versus high-dose toxicity.Hum. Exp. Toxicol. 2002; 21: 71-75Crossref PubMed Scopus (284) Google Scholar, 11.Jang Y.Y. Sharkis S.J. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche.Blood. 2007; 110: 3056-3063Crossref PubMed Scopus (652) Google Scholar). The reactions of proteins with ROS may lead to almost 100 types of side chain modifications (12.Shacter E. Quantification and significance of protein oxidation in biological samples.Drug Metab. Rev. 2000; 32: 307-326Crossref PubMed Scopus (658) Google Scholar, 13.Xu G. Chance M.R. Hydroxyl radical-mediated modification of proteins as probes for structural proteomics.Chem. Rev. 2007; 107: 3514-3543Crossref PubMed Scopus (539) Google Scholar). Histidine is highly susceptible to ROS damage, because it has strong metal chelation affinity and often constitutes the binding site for metal ions (14.Tainer J.A. Roberts V.A. Getzoff E.D. Metal-binding sites in proteins.Curr. Opin. Biotechnol. 1991; 2: 582-591Crossref PubMed Scopus (120) Google Scholar, 15.Regan L. The design of metal-binding sites in proteins.Annu. Rev. Biophys. Biomol. Struct. 1993; 22: 257-287Crossref PubMed Scopus (145) Google Scholar). The presence of H2O2 and redox-active metals (Cu and Fe) can lead to metal-catalyzed oxidation (MCO, also called Fenton-type chemistry), which converts histidine side chain to 2-oxohistidine (16.Uchida K. Kawakishi S. Identification of oxidized histidine generated at the active site of Cu, Zn-superoxide dismutase exposed to H2O2. Selective generation of 2-oxo-histidine at the histidine 118.J. Biol. Chem. 1994; 269: 2405-2410Abstract Full Text PDF PubMed Google Scholar, 17.Lewisch S.A. Levine R.L. Determination of 2-oxohistidine by amino acid analysis.Anal. Biochem. 1995; 231: 440-446Crossref PubMed Scopus (56) Google Scholar). The conversion of histidine to 2-oxohistidine alters its charge state, hydrogen bonding property, and metal chelation affinity, and hence may have serious impacts on protein structure and function. The net reaction is oxygen insertion (+16 Da), which makes it an irreversible PTM. It is unclear if cells simply tolerate such damages on histidines or employ active mechanisms to recognize them and use them as redox sensors or as damage markers for promoting protein degradation. The only known biological function of 2-oxohistidine is to serve as a redox sensor on bacterial transcription factor PerR (18.Traore D.A. El Ghazouani A. Jacquamet L. Borel F. Ferrer J.L. Lascoux D. Ravanat J.L. Jaquinod M. Blondin G. Caux-Thang C. Duarte V. Latour J.M. Structural and functional characterization of 2-oxo-histidine in oxidized PerR protein.Nat. Chem. Biol. 2009; 5: 53-59Crossref PubMed Scopus (91) Google Scholar), whereas other studies have used 2-oxohistidine as a stable marker of protein damage during oxidative stress (12.Shacter E. Quantification and significance of protein oxidation in biological samples.Drug Metab. Rev. 2000; 32: 307-326Crossref PubMed Scopus (658) Google Scholar, 19.Davies M.J. Fu S. Wang H. Dean R.T. Stable markers of oxidant damage to proteins and their application in the study of human disease.Free Radic. Biol. Med. 1999; 27: 1151-1163Crossref PubMed Scopus (416) Google Scholar). Judging by the potential biological significance of 2-oxohistidine modification, we hypothesized that there may be cellular factors to recognize it. Previous research on 2-oxohistidine had been impeded by the difficulty in generating this side chain with reasonable yields. Recently, we managed to greatly improve the yield of 2-oxohistidine conversion by optimizing MCO reaction conditions using the copper/ascorbate system (20.Huang C.F. Liu Y.H. Tai H.C. Synthesis of peptides containing 2-oxohistidine residues and their characterization by liquid chromatography-tandem mass spectrometry.J. Pept. Sci. 2015; 21: 114-119Crossref PubMed Scopus (1) Google Scholar), allowing us to synthesize and purify peptide probes containing 100% 2-oxohistidine for this study. Here, we used 2-oxohistidine-containing peptides to mimic the oxidative conversion of histidine residues on native proteins. Then, we utilized the Escherichia coli (E. coli) K12 proteome chip to identify 2-oxohistidine-interacting proteins via high-throughput screening, and the interactors turned out to be largely involved redox-related metabolism. From the bacterial interactors we predicted a consensus binding motif, which could be validated across different species and correctly predicted S100A1 as a human binding factor for 2-oxohistidine. Thus, recognition of 2-oxohistidine appears to be an evolutionarily conserved capacity from bacteria to human. The high throughput protein expression, protein purification, and protein printing were modified from the previous study (21.Chen C.S. Korobkova E. Chen H. Zhu J. Jian X. Tao S.C. He C. Zhu H. A proteome chip approach reveals new DNA damage recognition activities in Escherichia coli.Nat. Methods. 2008; 5: 69-74Crossref PubMed Scopus (101) Google Scholar). Briefly, we expressed and purified E. coli K12 proteins in 96-well plate format and subsequently printed the proteome microarray. All purified proteins were spotted in duplicate on each aldehyde slide (BaiO, Shanghai, China) by SmartArrayer 136 (CapitalBio, Beijing, China) at 4 °C. After printing proteins, the proteome microarray chips were kept at 4 °C for protein immobilization on the slides for 12 h. The chips were stored at −80 °C before probing with samples. Solutions containing 1 mm peptide, 5 mm Cu2+ and 200 mm sodium ascorbate were exposed to air with gentle shaking at 37 °C for 24 h (AG and SE peptide) or 6 h (IA peptide). The oxidation reaction was quenched with 20 mm EDTA and analyzed by reverse-phase high-performance liquid chromatography (HPLC) (10–30% acetonitrile and 0.1% TFA in water, C18 column from Dr. Maisch, Ammerbuch, Germany) to determine the reaction yield. For liquid chromatography-tandem mass spectrometry (LC-MS/MS) analysis of crude reaction mixtures and HPLC fractions, 10 μl samples were acidified with 2 μl 10% TFA and desalted with ZipTip (Millipore, Billerica, MA) following manufacturer's protocols. Oxidized peptides were purified by semi-preparative HPLC (C18 column, Dr. Maisch). LC-MS/MS experiments were conducted under previously reported conditions (20.Huang C.F. Liu Y.H. Tai H.C. Synthesis of peptides containing 2-oxohistidine residues and their characterization by liquid chromatography-tandem mass spectrometry.J. Pept. Sci. 2015; 21: 114-119Crossref PubMed Scopus (1) Google Scholar). Oxidized and nonoxidized peptides were dissolved in 50 mm sodium borate buffer at pH 7.5 and analyzed by HPLC to determine peptide concentration by 210 nm absorbance. DyLight-conjugated NHS esters (Thermo, Waltham, MA) were dissolved in anhydrous DMF to 10 mg/ml and added to peptide solutions for 1 h incubation at room temperature, at the following fluorophore/peptide ratios: DyLight 650/AG = 3:1, DyLight 650/SE = 5:1, DyLight 650/oxo-IA = 1.5:1; DyLight 550/oxo-AG = 5:1, DyLight 550/oxo-SE = 7:1, DyLight 550/IA = 3:1. Labeled peptides were analyzed and purified by HPLC as described above. Labeled products were verified by LC-MS/MS, and quantified by absorbance measurements based on known fluorophore properties. The chips were first blocked with 3% bovine serum albumin (BSA) (Sigma, St. Louis, MO) for 5 min. DyLight 550-conjugated 2-oxohistidine peptide and DyLight 650-conjugated nonoxidized peptide (10 μm each) were probed together onto the chip with LifterSlips (Thermo) at room temperature for 45 min. Finally, the chips were washed by Tris-buffered saline-Tween 20 (TBST) on an orbital shaker three times and 5 min each time. The chip was dried by centrifugation and then scanned with a LuxScan microarray scanner (CapitalBio). Signal intensities, defined as foreground median subtracted by background median, were acquired and analyzed using GenePix Pro 6.0 software. Then, we used quantile normalization to normalize the signal intensity from both 2-oxohistidine containing probes and nonoxidized probes. To identify positive 2-oxohistidine interacting proteins, four cutoff criteria were set: (1) The signal from experimental group was >1.5 standard deviations above the mean for all experimental groups. (2) To identify large signal differences between experimental groups and negative controls, the delta, defined as signal difference between experimental group and control group, was >1.5 standard deviations above the mean for all deltas. (3) To exclude the nonspecific binding to 2-oxohistidine residue, the signal from the negative control was >1.5 standard deviations below the mean for all control groups. (4) To remove irreproducible hits among triplicate chip assays, the student's t test p values between experimental groups and negative controls were less than 0.05. The R programming language (22.Team R.C. R: A Language and Environment for Statistical Computing.R Foundation for Statistical Computing. 2015; Google Scholar) was used to display heat map. The data was presented by the signal intensity of foreground subtracted by background. The gplots package (23.Warnes G.R. Bolker B. Bonebakker L. Gentleman R. Huber W. Liaw A. Lumley T. Maechler M. Magnusson A. Moeller S. gplots: Various R programming tools for plotting data. 2009; (R package Version 2)Google Scholar) was used for classifying 2-oxohistidine containing peptides and nonoxidized peptides in hierarchy. The identified proteins were used for functional interaction analyses by using EcID (24.Andres Leon E. Ezkurdia I. Garcia B. Valencia A. Juan D. EcID. A database for the inference of functional interactions in E. coli.Nucleic Acids Res. 2009; 37: D629-D635Crossref PubMed Scopus (25) Google Scholar) and Cytoscape (25.Shannon P. Markiel A. Ozier O. Baliga N.S. Wang J.T. Ramage D. Amin N. Schwikowski B. Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks.Genome Res. 2003; 13: 2498-2504Crossref PubMed Scopus (25321) Google Scholar). Briefly, the files of EcID entities and EcID pairs were downloaded from EcID database. Before mapping identified proteins to their EcID entities and EcID pairs, we removed the pairs that were based on the prediction mode, such as phylogenetic profiles, gene neighborhood, mirror tree, in silico two-hybrid, or context mirror. After mapping, we used Cytoscape to generate the functional interaction network, and visualized the identified proteins and their interacting proteins. Subsequently, we used AmiGO 2 (26.Carbon S. Ireland A. Mungall C.J. Shu S. Marshall B. Lewis S. Ami G.O.H. Web Presence Working, G AmiGO: online access to ontology and annotation data.Bioinformatics. 2009; 25: 288-289Crossref PubMed Scopus (1175) Google Scholar) and KOBAS 2.0 (27.Xie C. Mao X. Huang J. Ding Y. Wu J. Dong S. Kong L. Gao G. Li C.Y. Wei L. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases.Nucleic Acids Res. 2011; 39: W316-W322Crossref PubMed Scopus (2909) Google Scholar) to generate gene ontology (GO) (28.Ashburner M. Ball C.A. Blake J.A. Botstein D. Butler H. Cherry J.M. Davis A.P. Dolinski K. Dwight S.S. Eppig J.T. Harris M.A. Hill D.P. Issel-Tarver L. Kasarskis A. Lewis S. Matese J.C. Richardson J.E. Ringwald M. Rubin G.M. Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium.Nat. Genet. 2000; 25: 25-29Crossref PubMed Scopus (27012) Google Scholar) and Kyoto Encyclopedia of Genes and Genomes (KEGG) (29.Kanehisa M. Goto S. KEGG: kyoto encyclopedia of genes and genomes.Nucleic Acids Res. 2000; 28: 27-30Crossref PubMed Scopus (17971) Google Scholar) results, respectively. After blocking the 96-well black plate (Thermo) with 1% BSA at room temperature for 1 h, the identified proteins were added to the plate. The concentrations of 10 identified proteins (ThrS, YqjG, YajL, HemE, IlvA, PrpD, Zwf, Eda, Gor, and PqqL) were 12.0, 25.7, 10.7, 15.6, 3.4, 18.6, 19.5, 11.8, 26.1, and 5.9 μm, respectively. The concentrations of BSA, as a negative control, were identical to the protein being compared with. A 10 nm solution of DyLight 550-conjugated 2-oxohistidine peptide was incubated with target protein or BSA in a Micromixer MX4 (FINEPCR, Gunpo, Korea) at room temperature for 1 h. After incubation, the degree of polarization of each well was detected by a Synergy 2 (BioTek, Winooski, VT), using an excitation wavelength of 540 nm and an emission wavelength of 590 nm with a dichroic mirror of 570 nm. Identified proteins and S100A1 (Abnova, Taipei, Taiwan) were printed on aldehyde chips in a multiple-well format. After printing, the chips were immobilized at 4 °C for 12 h and then stored at −80 °C. The printed chips were blocked at room temperature for 5 min with 3% BSA. Two-fold serial-diluted DyLight 550-conjugated 2-oxohistidine peptides, DyLight 650-conjugated nonoxidized peptides, and quenched fluorescent dyes were added into the chip wells individually with Multi-Well Microarray Hybridization Cassettes (Arrayit, Sunnyvale, CA), and incubated at room temperature for 45 min. The fluorescent dyes, NHS esters of DyLight 550 and DyLight 650, were already quenched by Tris-HCl (Bionovas, Toronto, Canada). To check whether calcium affects interaction between S100A1 and 2-oxohistidine, 1 mm CaCl2 was added in the assay buffer. After several washes with TBST, the chips were dried by centrifugation and then scanned with a microarray scanner. The Kd value was calculated by double-reciprocal plot analysis, in which y is one divided by fluorescence intensity, and x is one divided by peptide concentration. We set the regression line formula in the form of y = ax, where “a” is the slope of regression line. The Kd value will be “a” multiplied by the concentration of identified protein. All identified proteins were converted to FASTA format and analyzed by Gapped Local Alignment of Motifs (GLAM2) (30.Frith M.C. Saunders N.F. Kobe B. Bailey T.L. Discovering sequence motifs with arbitrary insertions and deletions.PLoS Comput. Biol. 2008; 4: e1000071Crossref PubMed Scopus (235) Google Scholar) for surveying consensus motif. The parameters of GLAM2 were set as default. The resultant motif was then searched in entire E. coli K12 proteome and human proteome by GLAM2SCAN (30.Frith M.C. Saunders N.F. Kobe B. Bailey T.L. Discovering sequence motifs with arbitrary insertions and deletions.PLoS Comput. Biol. 2008; 4: e1000071Crossref PubMed Scopus (235) Google Scholar). All protein 3D structures were obtained from published studies (31..PDB ID: 1SZQ. Rajashankar, K. R., Kniewel, R., Solorzano, V., Lima, C. D., Burley, S. K., New York SGXResearch Center for Structural Genomics. Crystal structure of 2-methylcitrate dehydratase.Google Scholar, 32.Mittl P.R. Berry A. Scrutton N.S. Perham R.N. Schulz G.E. Anatomy of an engineered NAD-binding site.Protein Sci. 1994; 3: 1504-1514Crossref PubMed Scopus (47) Google Scholar, 33.Gallagher D.T. Gilliland G.L. Xiao G. Zondlo J. Fisher K.E. Chinchilla D. Eisenstein E. Structure and control of pyridoxal phosphate dependent allosteric threonine deaminase.Structure. 1998; 6: 465-475Abstract Full Text Full Text PDF PubMed Scopus (160) Google Scholar, 34.Dock-Bregeon A.C. Rees B. Torres-Larios A. Bey G. Caillet J. Moras D. Achieving error-free translation; the mechanism of proofreading of threonyl-tRNA synthetase at atomic resolution.Mol. Cell. 2004; 16: 375-386Abstract Full Text Full Text PDF PubMed Scopus (98) Google Scholar, 35.Wright N.T. Varney K.M. Ellis K.C. Markowitz J. Gitti R.K. Zimmer D.B. Weber D.J. The three-dimensional solution structure of Ca(2+)-bound S100A1 as determined by NMR spectroscopy.J. Mol. Biol. 2005; 353: 410-426Crossref PubMed Scopus (76) Google Scholar, 36.Wilson M.A. Ringe D. Petsko G.A. The atomic resolution crystal structure of the YajL (ThiJ) protein from Escherichia coli: a close prokaryotic homologue of the Parkinsonism-associated protein DJ-1.J. Mol. Biol. 2005; 353: 678-691Crossref PubMed Scopus (57) Google Scholar, 37.Fullerton S.W. Griffiths J.S. Merkel A.B. Cheriyan M. Wymer N.J. Hutchins M.J. Fierke C.A. Toone E.J. Naismith J.H. Mechanism of the Class I KDPG aldolase.Bioorg. Med. Chem. 2006; 14: 3002-3010Crossref PubMed Scopus (46) Google Scholar, 38.Green A.R. Hayes R.P. Xun L. Kang C. Structural understanding of the glutathione-dependent reduction mechanism of glutathionyl-hydroquinone reductases.J. Biol. Chem. 2012; 287: 35838-35848Abstract Full Text Full Text PDF PubMed Scopus (12) Google Scholar) and RCSB PDB (39.Berman H.M. Westbrook J. Feng Z. Gilliland G. Bhat T.N. Weissig H. Shindyalov I.N. Bourne P.E. The Protein Data Bank.Nucleic Acids Res. 2000; 28: 235-242Crossref PubMed Scopus (27327) Google Scholar), and visualized by RasMol software (40.Sayle R.A. Milner-White E.J. RASMOL: biomolecular graphics for all.Trends Biochem. Sci. 1995; 20: 374Abstract Full Text PDF PubMed Scopus (2320) Google Scholar). We used the EcoGene 3.0 (41.Zhou J. Rudd K.E. EcoGene 3.0.Nucleic Acids Res. 2013; 41: D613-D624Crossref PubMed Scopus (151) Google Scholar), which contained the QUARK prediction method (42.Xu D. Zhang Y. Ab initio protein structure assembly using continuous structure fragments and optimized knowledge-based force field.Proteins. 2012; 80: 1715-1735Crossref PubMed Scopus (29) Google Scholar), to predict the secondary structure of proteins without reported 3D structures. Many studies have reported that 2-oxohistidine residue had been found in various peptides and proteins (16.Uchida K. Kawakishi S. Identification of oxidized histidine generated at the active site of Cu, Zn-superoxide dismutase exposed to H2O2. Selective generation of 2-oxo-histidine at the histidine 118.J. Biol. Chem. 1994; 269: 2405-2410Abstract Full Text PDF PubMed Google Scholar, 43.Uchida K. Kawakishi S. 2-Oxo-histidine as a novel biological marker for oxidatively modified proteins.FEBS Lett. 1993; 332: 208-210Crossref PubMed Scopus (119) Google Scholar, 44.Lewisch S.A. Levine R.L. Determination of 2-oxohistidine by amino acid analysis.Methods Enzymol. 1999; 300: 120-124Crossref PubMed Scopus (4) Google Scholar, 45.Atwood C.S. Huang X. Khatri A. Scarpa R.C. Kim Y.S. Moir R.D. Tanzi R.E. Roher A.E. Bush A.I. Copper catalyzed oxidation of Alzheimer Abeta.Cell Mol Biol. 2000; 46: 777-783PubMed Google Scholar, 46.Schoneich C. Mechanisms of metal-catalyzed oxidation of histidine to 2-oxo-histidine in peptides and proteins.J. Pharm. Biomed. Anal. 2000; 21: 1093-1097Crossref PubMed Scopus (92) Google Scholar, 47.Gunther M.R. Peters J.A. Sivaneri M.K. Histidinyl radical formation in the self-peroxidation reaction of bovine copper-zinc superoxide dismutase.J. Biol. Chem. 2002; 277: 9160-9166Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar, 48.Hovorka S.W. Biesiada H. Williams T.D. Huhmer A. Schoneich C. High sensitivity of Zn2+ insulin to metal-catalyzed oxidation: detection of 2-oxo-histidine by tandem mass spectrometry.Pharm. Res. 2002; 19: 530-537Crossref PubMed Scopus (15) Google Scholar, 49.Schoneich C. Williams T.D. Cu(II)-catalyzed oxidation of beta-amyloid peptide targets His13 and His14 over His6: Detection of 2-Oxo-histidine by HPLC-MS/MS.Chem. Res. Toxicol. 2002; 15: 717-722Crossref PubMed Scopus (103) Google Scholar, 50.Schiewe A.J. Margol L. Soreghan B.A. Thomas S.N. Yang A.J. Rapid characterization of amyloid-beta side-chain oxidation by tandem mass spectrometry and the scoring algorithm for spectral analysis.Pharm. Res. 2004; 21: 1094-1102Crossref PubMed Scopus (16) Google Scholar, 51.Inoue K. Garner C. Ackermann B.L. Oe T. Blair I.A. Liquid chromatography/tandem mass spectrometry characterization of oxidized amyloid beta peptides as potential biomarkers of Alzheimer's disease.Rapid Commun. Mass Spectrom. 2006; 20: 911-918Crossref PubMed Scopus (41) Google Scholar). To identify proteins which may bind specifically to 2-oxohistidine residue, we devised an experimental strategy illustrated in Fig. 1. First, we fabricated the E. coli K12 proteome chip, generated the 2-oxohistidine containing peptides, and probed these peptides with E. coli K12 proteome chips. After identifying the positive hits, we used fluorescence polarization assays to validate the interactions and measured the binding affinity by dose-response measurements. Then, we surveyed the consensus motif among these identified proteins and applied to human proteome to look for possible human 2-oxohistidine interacting proteins. Finally, we used the functional interaction network to find out the possible interacting proteins and used GO and KEGG to figure out related processes and pathways (Fig. 1). To synthesize peptide probes, histidine residues were placed in the middle of 12-mer or 13-mer peptides to eliminate possible charge effects at N terminus and C terminus, creating a context similar to proteins. Easily oxidized amino acids, such as methionine, cysteine, tyrosine, tryptophan, phenylalanine, lysine, and arginine, were avoided. Three peptides containing a single histidine residue and random selections of other residues, namely AGAQVAHGNEVAG (AG), SEAGVNHGSAGQA (SE), and IAVENVHGGLA (IA), were used for chip assays. We carried out MCO reactions using the copper/ascorbate/air system shown in Fig. 2 to convert them to 2-oxohistidine containing peptides (Oxo-AG, Oxo-SE, Oxo-IA). The HPLC yield of peptides Oxo-AG and Oxo-SE were around 10%, and for Oxo-IA peptide around 20% (Fig. 2). The site of oxidative modification was confirmed by LC-MS/MS for all peptides (supplemental Fig. S1). To investigate 2-oxohistidine interacting proteins, AGAQVAH*GNEVAG (Oxo-AG peptide) and SEAGVNH*GSAGQA (Oxo-SE peptide) were conjugated to DyLight 550 fluo" @default.
• W2522495093 created "2016-09-30" @default.
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• W2522495093 date "2016-12-01" @default.
• W2522495093 modified "2023-10-16" @default.
• W2522495093 title "Identification of 2-oxohistidine Interacting Proteins Using E. coli Proteome Chips" @default.
• W2522495093 cites W1488105116 @default.
• W2522495093 cites W1489331825 @default.
• W2522495093 cites W1508123066 @default.
• W2522495093 cites W1553843803 @default.
• W2522495093 cites W1555383578 @default.
• W2522495093 cites W1810862543 @default.
• W2522495093 cites W1967361018 @default.
• W2522495093 cites W1980148600 @default.
• W2522495093 cites W1980584256 @default.
• W2522495093 cites W1990140653 @default.
• W2522495093 cites W1991605406 @default.
• W2522495093 cites W1992681584 @default.
• W2522495093 cites W1993747379 @default.
• W2522495093 cites W1994769872 @default.
• W2522495093 cites W1995980300 @default.
• W2522495093 cites W1999643597 @default.
• W2522495093 cites W2004068264 @default.
• W2522495093 cites W2004972062 @default.
• W2522495093 cites W2021966623 @default.
• W2522495093 cites W2023200476 @default.
• W2522495093 cites W2024849484 @default.
• W2522495093 cites W2026258231 @default.
• W2522495093 cites W2027847170 @default.
• W2522495093 cites W2028161249 @default.
• W2522495093 cites W2033628455 @default.
• W2522495093 cites W2036806484 @default.
• W2522495093 cites W2043938667 @default.
• W2522495093 cites W2045565319 @default.
• W2522495093 cites W2046032622 @default.
• W2522495093 cites W2047447331 @default.
• W2522495093 cites W2050000125 @default.
• W2522495093 cites W2050284387 @default.
• W2522495093 cites W2050892986 @default.
• W2522495093 cites W2052120254 @default.
• W2522495093 cites W2060382254 @default.
• W2522495093 cites W2060897125 @default.
• W2522495093 cites W2064455390 @default.
• W2522495093 cites W2070370023 @default.
• W2522495093 cites W2075000549 @default.
• W2522495093 cites W2084299658 @default.
• W2522495093 cites W2090630635 @default.
• W2522495093 cites W2091167718 @default.
• W2522495093 cites W2097026233 @default.
• W2522495093 cites W2099121794 @default.
• W2522495093 cites W2103017472 @default.
• W2522495093 cites W2103825172 @default.
• W2522495093 cites W2104382960 @default.
• W2522495093 cites W2109434922 @default.
• W2522495093 cites W2117690477 @default.
• W2522495093 cites W2123863402 @default.
• W2522495093 cites W2123997826 @default.
• W2522495093 cites W2130479394 @default.
• W2522495093 cites W2132673369 @default.
• W2522495093 cites W2135470678 @default.
• W2522495093 cites W2137749693 @default.
• W2522495093 cites W2139008698 @default.
• W2522495093 cites W2140922027 @default.
• W2522495093 cites W2141545183 @default.
• W2522495093 cites W2141734808 @default.
• W2522495093 cites W2149790826 @default.
• W2522495093 cites W2152951933 @default.
• W2522495093 cites W2155972151 @default.
• W2522495093 cites W2159675211 @default.
• W2522495093 cites W2160243391 @default.
• W2522495093 cites W2163351331 @default.
• W2522495093 cites W2165003189 @default.
• W2522495093 cites W2171559274 @default.
• W2522495093 cites W2172867362 @default.
• W2522495093 cites W2181365731 @default.
• W2522495093 cites W2409936908 @default.
• W2522495093 cites W2410505691 @default.
• W2522495093 cites W4294216483 @default.
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