Insights into H₂O₂-induced signaling in Jurkat cells from analysis of gene expression

References

• Barrett T, Wilhite SE, Ledoux P, et al. NCBI GEO: archive for functional genomics data sets – update. Nucleic Acids Res. 2013;41(Database issue):D991–995.
   PubMed Web of Science ®Google Scholar
• Marinho HS, Real C, Cyrne L, et al. Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol. 2014;2:535–562.
   PubMed Web of Science ®Google Scholar
• García-Santamarina S, Boronat S, Hidalgo E. Reversible cysteine oxidation in hydrogen peroxide sensing and signal transduction. Biochemistry. 2014;53(16):2560–2580.
   PubMed Web of Science ®Google Scholar
• Sies H. Role of metabolic H2O2 generation: redox signaling and oxidative stress. J Biol Chem. 2014;289(13):8735–8741.
   PubMed Web of Science ®Google Scholar
• Winterbourn CC. Biological production, detection, and fate of hydrogen peroxide. Antioxid Redox Signal. 2018;29(6):541–551.
   PubMed Web of Science ®Google Scholar
• Sies H, Jones DP. Reactive oxygen species (ROS) as pleiotropic physiological signaling agents. Nat Rev Mol Cell Biol. 2020;21(7):363–383.
   PubMed Web of Science ®Google Scholar
• Sies H, Belousov VV, Chandel NS, et al. Defining roles of specific reactive oxygen species (ROS) in cell biology and physiology. Nat Rev Mol Cell Biol. 2022;23(7):499–515.
   PubMed Web of Science ®Google Scholar
• Oakley FD, Abbott D, Li Q, et al. Signaling components of redox active endosomes: the redoxosomes. Antioxid Redox Signal. 2009;11(6):1313–1333.
   PubMed Web of Science ®Google Scholar
• Begum R, Thota S, Abdulkadir A, et al. NADPH oxidase family proteins: signaling dynamics to disease management. Cell Mol Immunol. 2022;19(6):660–686.
   PubMed Web of Science ®Google Scholar
• Murphy MP. How mitochondria produce reactive oxygen species. Biochem J. 2009;417(1):1–13.
   PubMed Web of Science ®Google Scholar
• Sundaresan M, Yu ZX, Ferrans VJ, et al. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science. 1995;270(5234):296–299.
   PubMed Web of Science ®Google Scholar
• Bae YS, Kang SW, Seo MS, et al. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J Biol Chem. 1997;272(1):217–221.
   PubMed Web of Science ®Google Scholar
• Ichijo H, Nishida E, Irie K, et al. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science. 1997;275(5296):90–94.
   PubMed Web of Science ®Google Scholar
• Nadeau PJ, Charette SJ, Toledano MB, et al. Disulfide bond-mediated multimerization of Ask1 and its reduction by thioredoxin-1 regulate H2O2-induced c-Jun NH2-terminal kinase activation and apoptosis. Mol Biol Cell. 2007;18(10):3903–3913.
   PubMed Web of Science ®Google Scholar
• Jarvis RM, Hughes SM, Ledgerwood EC. Peroxiredoxin 1 functions as a signal peroxidase to receive, transduce, and transmit peroxide signals in mammalian cells. Free Radic Biol Med. 2012;53(7):1522–1530.
   PubMed Web of Science ®Google Scholar
• Gasch AP, Spellman PT, Kao CM, et al. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell. 2000;11(12):4241–4257.
   PubMed Web of Science ®Google Scholar
• Chuang YY, Chen Y, Gadisetti Chandramouli VR, et al. Gene expression after treatment with hydrogen peroxide, menadione, or t-butyl hydroperoxide in breast cancer cells. Cancer Res. 2002;62(21):6246–6254.
   PubMed Web of Science ®Google Scholar
• Chen D, Toone WM, Mata J, et al. Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell. 2003;14(1):214–229.
   PubMed Web of Science ®Google Scholar
• Murray JI, Whitfield ML, Trinklein ND, et al. Diverse and specific gene expression responses to stresses in cultured human cells. Mol Biol Cell. 2004;15(5):2361–2374.
   PubMed Web of Science ®Google Scholar
• Desaint S, Luriau S, Aude JC, et al. Mammalian antioxidant defenses are not inducible by H2O2. J Biol Chem. 2004;279(30):31157–31163.
   PubMed Web of Science ®Google Scholar
• Vandenbroucke K, Robbens S, Vandepoele K, et al. Hydrogen peroxide-induced gene expression across kingdoms: a comparative analysis. Mol Biol Evol. 2008;25(3):507–516.
   PubMed Web of Science ®Google Scholar
• Fomenko DE, Koc A, Agisheva N, et al. Thiol peroxidases mediate specific genome-wide regulation of gene expression in response to hydrogen peroxide. Proc Natl Acad Sci USA. 2011;108(7):2729–2734.
   PubMed Web of Science ®Google Scholar
• Purcell M, Kruger A, Tainsky MA. Gene expression profiling of replicative and induced senescence. Cell Cycle. 2014;13(24):3927–3937.
   PubMed Web of Science ®Google Scholar
• Wang R, Wei B, Wei J, et al. Caspase-related apoptosis genes in gliomas by RNA-seq and bioinformatics analysis. J Clin Neurosci. 2016;33:259–263.
   PubMed Web of Science ®Google Scholar
• Barandalla M, Shi H, Xiao H, et al. Global gene expression profiling and senescence biomarker analysis of hESC exposed to H2O2 induced non-cytotoxic oxidative stress. Stem Cell Res Ther. 2017;8(1):160.
   PubMedGoogle Scholar
• Sastry KS, Naeem H, Mokrab Y, et al. RNA-seq reveals dysregulation of Novel melanocyte genes upon oxidative stress: implications in vitiligo pathogenesis. Oxid Med Cell Longev. 2019;2019:2841814.
   PubMed Web of Science ®Google Scholar
• Huang X, He C, Hua X, et al. Oxidative stress induces monocyte-to-myofibroblast transdifferentiation through p38 in pancreatic ductal adenocarcinoma. Clin Transl Med. 2020;10(2):e41.
   PubMed Web of Science ®Google Scholar
• Chen X, Wang X, Shen M, et al. Combined RNA-seq and molecular biology technology revealed the protective effect of Cyclocarya paliurus polysaccharide on H2O2-induced oxidative damage in L02 cells thought regulating mitochondrial function, oxidative stress and PI3K/Akt and MAPK signaling pathways. Food Res Int. 2022;155:111080.
   PubMed Web of Science ®Google Scholar
• Müller N, Warwick T, Noack K, et al. Reactive oxygen species differentially modulate the metabolic and transcriptomic response of endothelial cells. Antioxidants. 2022;11(2):434.
   Web of Science ®Google Scholar
• Stone JR, Yang S. Hydrogen peroxide: a signaling messenger. Antioxid Redox Signal. 2006;8(3–4):243–270.
   PubMed Web of Science ®Google Scholar
• Antunes F, Brito PM. Quantitative biology of hydrogen peroxide signaling. Redox Biol. 2017;13:1–7.
   PubMed Web of Science ®Google Scholar
• Pace PE, Peskin AV, Konigstorfer A, et al. Peroxiredoxin interaction with the cytoskeletal-regulatory protein CRMP2: investigation of a putative redox relay. Free Radic Biol Med. 2018;129:383–393.
   PubMed Web of Science ®Google Scholar
• Andrews S. 2010. FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
   Google Scholar
• Dobin A, Davis CA, Schlesinger F, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21.
   PubMed Web of Science ®Google Scholar
• Anders S, Pyl PT, Huber W. HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31(2):166–169.
   PubMed Web of Science ®Google Scholar
• Law CW, Chen Y, Shi W, et al. Voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 2014;15(2):R29.
   PubMed Web of Science ®Google Scholar
• Ritchie ME, Phipson B, Wu D, et al. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7):e47.
   PubMed Web of Science ®Google Scholar
• Warnes GR, Bolker B, Bonebakker L, et al. 2009. Various R programming tools for plotting data. https://CRAN.R-project.org/package=gplots.
   Google Scholar
• R Core Team. 2017. A language and environment for statistical computing. In R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
   Google Scholar
• Benjamini Y, Hochberg Y. Controlling the false discovery rate – a practical and powerful approach to multiple testing. J. R. Stat. Soc. B. 1995;57(1):289–300.
   Google Scholar
• Blighe K, Rana S, Lewis M. 2021. EnhancedVolcano: publication-ready volcano plots with enhanced colouring and labeling. https://github.com/kevinblighe/EnhancedVolcano.
   Google Scholar
• Pagès H, Carlson M, Falcon S, et al. 2021. AnnotationDbi: Manipulation of SQLite-based annotations in Bioconductor., R package version 1.54.1 Ed., https://bioconductor.org/packages/AnnotationDbi.
   Google Scholar
• Young MD, Wakefield MJ, Smyth GK, et al. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010;11(2):R14.
   PubMed Web of Science ®Google Scholar
• Gillespie M, Jassal B, Stephan R, et al. The reactome pathway knowledgebase 2022. Nucleic Acids Res. 2022;50(D1):D687–D692.
   PubMed Web of Science ®Google Scholar
• Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102(43):15545–15550.
   PubMed Web of Science ®Google Scholar
• Yu G, He QY. ReactomePA: an R/bioconductor package for reactome pathway analysis and visualization. Mol Biosyst. 2016;12(2):477–479.
   PubMedGoogle Scholar
• Andersen CL, Jensen JL, Orntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and Colon cancer data sets. Cancer Res. 2004;64(15):5245–5250.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods. 2001;25(4):402–408.
   PubMed Web of Science ®Google Scholar
• Roider HG, Kanhere A, Manke T, et al. Predicting transcription factor affinities to DNA from a biophysical model. Bioinformatics. 2007;23(2):134–141.
   PubMed Web of Science ®Google Scholar
• Thomas-Chollier M, Hufton A, Heinig M, et al. Transcription factor binding predictions using TRAP for the analysis of ChIP-seq data and regulatory SNPs. Nat Protoc. 2011;6(12):1860–1869.
   PubMed Web of Science ®Google Scholar
• Keenan AB, Torre D, Lachmann A, et al. ChEA3: transcription factor enrichment analysis by orthogonal omics integration. Nucleic Acids Res. 2019;47(W1):W212–W224.
   PubMed Web of Science ®Google Scholar
• Hampton MB, Orrenius S. Dual regulation of caspase activity by hydrogen peroxide: implications for apoptosis. FEBS Lett. 1997;414(3):552–556.
   PubMed Web of Science ®Google Scholar
• Pita-Juárez Y, Altschuler G, Kariotis S, et al. The pathway coexpression network: revealing pathway relationships. PLoS Comput Biol. 2018;14(3):e1006042.
   PubMed Web of Science ®Google Scholar
• Trostle AJ, Wang J, Li L, et al. Most high throughput expression data sets are underpowered. BioRxiv. 2022. DOI: 10.1101/2022.08.03.502688
   Google Scholar
• Lennicke C, Cocheme HM. Redox metabolism: ROS as specific molecular regulators of cell signaling and function. Mol Cell. 2021;81(18):3691–3707.
   PubMed Web of Science ®Google Scholar
• Seddon AR, Liau Y, Pace PE, et al. Genome-wide impact of hydrogen peroxide on maintenance DNA methylation in replicating cells. Epigenetics Chromatin. 2021;14:17.
   PubMed Web of Science ®Google Scholar
• O’Connor KM, Das AB, Winterbourn CC, et al. Inhibition of DNA methylation in proliferating human lymphoma cells by immune cell oxidants. J Biol Chem. 2020;295(23):7839–7848.
   PubMed Web of Science ®Google Scholar
• Brown AK, Webb AE. Regulation of FOXO factors in mammalian cells. Curr Top Dev Biol. 2018;127:165–192.
   PubMed Web of Science ®Google Scholar
• Huang H, Tindall DJ. Dynamic FoxO transcription factors. J Cell Sci. 2007;120(Pt 15):2479–2487.
   PubMed Web of Science ®Google Scholar
• Klotz LO, Sanchez-Ramos C, Prieto-Arroyo I, et al. Redox regulation of FoxO transcription factors. Redox Biol. 2015;6:51–72.
   PubMed Web of Science ®Google Scholar
• Essers MAG, Weijzen S, de Vries-Smits AMM, et al. FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J. 2004;23(24):4802–4812.
   PubMed Web of Science ®Google Scholar
• Essaghir A, Dif N, Marbehant CY, et al. The transcription of FOXO genes is stimulated by FOXO3 and repressed by growth factors. J Biol Chem. 2009;284(16):10334–10342.
   PubMed Web of Science ®Google Scholar
• Hechtman JF. NTRK insights: best practices for pathologists. Mod Pathol. 2022;35(3):298–305.
   PubMed Web of Science ®Google Scholar
• Wang H, Wang R, Thrimawithana T, et al. The nerve growth factor signaling and its potential as therapeutic target for glaucoma. Biomed Res Int. 2014;2014:759473.
   PubMed Web of Science ®Google Scholar
• Vaishnavi A, Le AT, Doebele RC. TRKing down an old oncogene in a new era of targeted therapy. Cancer Discov. 2015;5(1):25–34.
   PubMed Web of Science ®Google Scholar
• Lange AM, Lo HW. Inhibiting TRK proteins in clinical cancer therapy. Cancers. 2018;10(4):105.
   PubMed Web of Science ®Google Scholar
• Xanthoudakis S, Miao G, Wang F, et al. Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO J. 1992;11(9):3323–3335.
   PubMed Web of Science ®Google Scholar
• Beiqing L, Chen M, Whisler RL. Sublethal levels of oxidative stress stimulate transcriptional activation of c-jun and suppress IL-2 promoter activation in Jurkat T cells. J. Immunol. 1996;157(1):160–169.
   PubMed Web of Science ®Google Scholar
• Klatt P, Molina EP, De Lacoba MG, et al. Redox regulation of c-Jun DNA binding by reversible S-glutathiolation. FASEB J. 1999;13(12):1481–1490.
   PubMed Web of Science ®Google Scholar
• Ghosh S, May MJ, Kopp EB. NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol. 1998;16:225–260.
   PubMed Web of Science ®Google Scholar
• Schreck R, Rieber P, Baeuerle PA. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-κB transcription factor and HIV-1. EMBO J. 1991;10(8):2247–2258.
   PubMed Web of Science ®Google Scholar
• Sohn SH, Sul HJ, Kim B, et al. TRK inhibitors block NFKB and induce NRF2 in TRK fusion-positive colon cancer. J Cancer. 2021;12(21):6356–6362.
   PubMed Web of Science ®Google Scholar