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Research Paper

Deoxynivalenol globally affects the selection of 3’ splice sites in human cells by suppressing the splicing factors, U2AF1 and SF1

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Pages 584-595 | Received 09 May 2019, Accepted 17 Jan 2020, Published online: 06 Feb 2020

References

  • Sharp PA. The discovery of split genes and RNA splicing: trends in biochemical sciences. Trends Biochem Sci. 2005;30:279–281.
  • Sharp PA. Split genes and RNA splicing (Nobel Lecture). Angew Chem. 2010;33:1229–1240.
  • Kim E, Magen A, Ast G. Different levels of alternative splicing among eukaryotes. Nucleic Acids Res. 2007;35:125–131.
  • Merkin J, Russell C, Chen P, et al. Evolutionary dynamics of gene and isoform regulation in mammalian tissues. Science. 2012;338:1593–1599.
  • Barbosamorais NL, Irimia M, Pan Q, et al. The evolutionary landscape of alternative splicing in vertebrate species. Science. 2013;338:1587–1593.
  • Nilsen TW, Graveley BR. Expansion of the eukaryotic proteome by alternative splicing. Nature. 2010;463:457–463.
  • Irimia M, Blencowe BJ. Alternative splicing: decoding an expansive regulatory layer. Curr Opin Cell Biol. 2012;24:323–332.
  • Modrek B, Resch A, Grasso C, et al. Genome-wide detection of alternative splicing in expressed sequences of human genes. Nucleic Acids Res. 2001;29:2850–2859.
  • Garcia-Blanco MA, Baraniak AP, Lasda EL. Alternative splicing in disease and therapy. Nat Biotechnol. 2004;22:535–546.
  • Aoki-Suzuki M, Yamada K, Meerabux J, et al. A family-based association study and gene expression analyses of netrin-G1 and -G2 genes in schizophrenia. Biol Psychiatry. 2005;57:382–393.
  • Newman A. Specific accessory sequences in Saccharomyces cerevisiae introns control assembly of pre‐mRNAs into spliceosomes. Embo J. 1987;6:3833–3839.
  • Ma L, Tan Z, Teng Y, et al. In vivo effects on intron retention and exon skipping by the U2AF large subunit and SF1/BBP in the nematode Caenorhabditis elegans. RNA. 2011;17:2201–2211.
  • Wahl MC, Will CL, Lührmann R. The spliceosome: design principles of a dynamic RNP machine. Cell. 2009;136:701–718.
  • Berglund JA, Chua K, Abovich N, et al. The splicing factor BBP interacts specifically with the pre-mRNA branchpoint sequence UACUAAC. Cell. 1997;89:781.
  • Berglund JA, Abovich N, Rosbash M. A cooperative interaction between U2AF65 and mBBP/SF1 facilitates branchpoint region recognition. Genes Dev. 1998;12:858–867.
  • Angela C, Flore R, Ivona B, et al. Mammalian splicing factor SF1 interacts with SURP domains of U2 snRNP-associated proteins. Nucleic Acids Res. 2015;43:10456–10473.
  • Moore MJ. Intron recognition comes of AGe. Nat Struct Biol. 2000;7:14–16.
  • Schothorst RC, Egmond HPV. Report from SCOOP task 3.2.10“collection of occurrence data of Fusarium toxins in food and assessment of dietary intake by the population of EU member states”: subtask: trichothecenes. Toxicol Lett. 2004;153:133–143.
  • Pestka JJ, Smolinski AT. Deoxynivalenol: toxicology and Potential Effects on Humans. J Toxicol Environ Health B Crit Rev. 2005;8:39–69.
  • Knutsen HK, Alexander J, Barregård L, et al. Risks to human and animal health related to the presence of deoxynivalenol and its acetylated and modified forms in food and feed. Efsa J. 2017;15:4718.
  • Rotter BA, Prelusky DB, Pestka JJ. Toxicology of deoxynivalenol (vomitoxin). J Toxicol Environ Health. 1996;48:1–34.
  • Wells L, Hardie L, Williams C, et al. Deoxynivalenol Biomarkers in the Urine of UK Vegetarians. Toxins (Basel). 2017;9:196.
  • Berthiller F, Dall’Asta C, Schuhmacher R, et al. Masked mycotoxins: determination of a deoxynivalenol glucoside in artificially and naturally contaminated wheat by liquid chromatography−tandem mass spectrometry. J Agric Food Chem. 2005;53:3421–3425.
  • Listed N. Evaluation of certain mycotoxins in food. Fifty-sixth report of the Joint FAO/WHO Expert Committee on Food Additives. World Health Organ Tech Rep. 2002;906:1–62.
  • Bhat R, Ramakrishna Y, Beedu S, et al. Outbreak of trichothecene mycotoxicosis associated with consumption of mould-damaged wheat products in Kashmir Valley, India. Lancet. 1989;333:35–37.
  • Mishra S, Dwivedi PD, Pandey HP, et al. Role of oxidative stress in Deoxynivalenol induced toxicity. Food Chem Toxicol. 2014;72:20–29.
  • Friend DW, Thompson BK, Trenholm HL, et al. Effects of feeding deoxynivalenol (DON)-contaminated wheat diets to pregnant and lactating gilts and on their progeny. Can Vet J. 1986;66:229–236.
  • Dänicke S, Valenta H, Spilke J. Effects of long-term storage on Fusarium toxin concentrations in wheat - sources of error of the analytical results. Arch Tierernahr. 2004;58:507–515.
  • Pinton P, Tsybulskyy D, Lucioli J, et al. Toxicity of deoxynivalenol and its acetylated derivatives on the intestine: differential effects on morphology, barrier function, tight junction proteins, and mitogen-activated protein kinases. Toxicol Sci. 2012;130:180–190.
  • Juan-García A, Juan C, König S, et al. Cytotoxic effects and degradation products of three mycotoxins: alternariol, 3-acetyl-deoxynivalenol and 15-acetyl-deoxynivalenol in liver hepatocellular carcinoma cells. Toxicol Lett. 2015;235:8–16.
  • Shifrin VI, Anderson P. Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. J Biol Chem. 1999;274:13985–13992.
  • Pestka JJ. Deoxynivalenol-Induced Proinflammatory Gene Expression: mechanisms and Pathological Sequelae. Toxins (Basel). 2010;2:1300–1317.
  • Zhu J, Krainer AR. Pre-mRNA splicing in the absence of an SR protein RS domain. Genes Dev. 2000;14:3166–3178.
  • Nilsen TW. The spliceosome: the most complex macromolecular machine in the cell? Bioessays. 2003;25:1147–1149.
  • Yuan L, Mu P, Huang B, et al. EGR1 is essential for deoxynivalenol-induced G2/M cell cycle arrest in HepG2 cells via the ATF3ΔZip2a/2b-EGR1-p21 pathway. Toxicol Lett. 2018;299:95–103.
  • Xiaoming L, Peiqiang M, Han Q, et al. JNK-AKT-NF-κB controls P-glycoprotein expression to attenuate the cytotoxicity of Deoxynivalenol in mammalian cells. Biochem Pharmacol. 2018;156:120–134.
  • Krämer A, Utans U. Three protein factors (SF1, SF3 and U2AF) function in pre‐splicing complex formation in addition to snRNPs. The EMBO Journal. 2010;2:1300–1317.
  • Nielsen C, Casteel M, Didier A, et al. Trichothecene-induced cytotoxicity on human cell lines. Mycotoxin Res. 2009;25:77–84.
  • Kanaar R, Roche SE, Beall EL, et al. The conserved pre-mRNA splicing factor U2AF from Drosophila: requirement for viability. Science. 1993;262:569–573.
  • Golling G, Amsterdam A, Sun Z, et al. Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development. Nat Genet. 2002;31:135–140.
  • Dvinge H, Kim E, Abdelwahab O, et al. RNA splicing factors as oncoproteins and tumour suppressors. Nat Rev Cancer. 2016;16:413–430.
  • Yoshida K, Sanada M, Shiraishi Y, et al. Frequent pathway mutations of splicing machinery in myelodysplasia. Nature. 2011;478:64–69.
  • Yip BH, Steeples V, Repapi E, et al. The U2AF1 S34F mutation induces lineage-specific splicing alterations in myelodysplastic syndromes. J Clin Investig. 2017;127:2206–2221.
  • Wang L, Brooks AN, Fan J, et al. Transcriptomic Characterization of SF3B1 Mutation Reveals Its Pleiotropic Effects in Chronic Lymphocytic Leukemia. Cancer Cell. 2016;30:750–763.
  • Graubert TA, Shen D, Ding L, et al. Recurrent mutations in the U2AF1 splicing factor in myelodysplastic syndromes. Nat Genet. 2012;44:53–57.
  • Black DL, Grabowski PJ. Alternative pre-mRNA splicing and neuronal function. Prog Mol Subcell Biol. 2003;31:187–216.
  • Sun Y, Wen J, Chen R, et al. Variable protein homeostasis in housekeeping and non-housekeeping pathways under mycotoxins stress. Sci Rep. 2019;9:7819.
  • Reed R. Protein composition of mammalian spliceosomes assembled in vitro. Proc Natl Acad Sci U S A. 1990;87:8031–8035.
  • Michaud S, Reed R. An ATP-independent complex commits pre-mRNA to the mammalian spliceosome assembly pathway. Genes Dev. 1991;5:2534–2546.
  • Hinnebusch AG. Translational control of GCN4: an in vivo barometer of initiation-factor activity. Trends Biochem Sci. 1994;19:409–414.
  • Shufeng S, Jun J, Yiqun D. Chicken cytochrome P450 1A5 is the key enzyme for metabolizing T-2 toxin to 3ʹOH-T-2. Int J Mol Sci. 2013;14:10809–10818.
  • Chatrikhi R, Wang W, Gupta A, et al. SF1 Phosphorylation Enhances Specific Binding to U2AF65 and Reduces Binding to 3â2-Splice-Site RNA. Biophys J. 2016;111:2570–2586.
  • Komeno Y, Huang YJ, Qiu J, et al. SRSF2 Is Essential for Hematopoiesis, and Its Myelodysplastic Syndrome-Related Mutations Dysregulate Alternative Pre-mRNA Splicing. Mol Cell Biol. 2015;35:3071–3082.
  • Dvinge H, Bertone P. HTqPCR: high-throughput analysis and visualization of quantitative real-time PCR data in R. Bioinformatics. 2009;25:3325–3326.
  • Hurgobin B. Short Read Alignment Using SOAP2. Methods Mol Biol. 2016;1374:241–252.

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