Alternative Splicing of the Aryl Hydrocarbon Receptor Nuclear Translocator (ARNT) Is Regulated by RBFOX2 in Lymphoid Malignancies

REFERENCES

• Bersten DC, Sullivan AE, Peet DJ, Whitelaw ML. 2013. bHLH-PAS proteins in cancer. Nat Rev Cancer 13:827–841. https://doi.org/10.1038/nrc3621.
   PubMed Web of Science ®Google Scholar
• Kewley RJ, Whitelaw ML, Chapman-Smith A. 2004. The mammalian basic helix-loop-helix/PAS family of transcriptional regulators. Int J Biochem Cell Biol 36:189–204. https://doi.org/10.1016/S1357-2725(03)00211-5.
   PubMed Web of Science ®Google Scholar
• McIntosh BE, Hogenesch JB, Bradfield CA. 2010. Mammalian Per-Arnt-Sim proteins in environmental adaptation. Annu Rev Physiol 72:625–645. https://doi.org/10.1146/annurev-physiol-021909-135922.
   PubMed Web of Science ®Google Scholar
• Gu C, Gonzalez J, Zhang T, Kamel-Reid S, Wells RA. 2013. The aryl hydrocarbon receptor nuclear translocator (ARNT) modulates the antioxidant response in AML cells. Leuk Res 37:1750–1756. https://doi.org/10.1016/j.leukres.2013.10.010.
   PubMed Web of Science ®Google Scholar
• Hassen W, Kassambara A, Reme T, Sahota S, Seckinger A, Vincent L, Cartron G, Moreaux J, Hose D, Klein B. 2015. Drug metabolism and clearance system in tumor cells of patients with multiple myeloma. Oncotarget 6:6431–6447. https://doi.org/10.18632/oncotarget.3237.
   PubMedGoogle Scholar
• Shi S, Yoon DY, Hodge-Bell KC, Bebenek IG, Whitekus MJ, Zhang R, Cochran AJ, Huerta-Yepez S, Yim S-H, Gonzalez FJ, Jaiswal AK, Hankinson O. 2009. The aryl hydrocarbon receptor nuclear translocator (Arnt) is required for tumor initiation by benzo[a]pyrene. Carcinogenesis 30:1957–1961. https://doi.org/10.1093/carcin/bgp201.
   PubMed Web of Science ®Google Scholar
• Shieh J-M, Shen C-J, Chang W-C, Cheng H-C, Chan Y-Y, Huang W-C, Chang W-C, Chen B-K. 2014. An increase in reactive oxygen species by deregulation of ARNT enhances chemotherapeutic drug-induced cancer cell death. PLoS One 9:e99242. https://doi.org/10.1371/journal.pone.0099242.
   Google Scholar
• Huang C-R, Lee C-T, Chang K-Y, Chang W-C, Liu Y-W, Lee J-C, Chen B-K. 2015. Down-regulation of ARNT promotes cancer metastasis by activating the fibronectin/integrin β1/FAK axis. Oncotarget 6:11530–11546. https://doi.org/10.18632/oncotarget.3448.
   PubMedGoogle Scholar
• Hoffman EC, Reyes H, Chu F-F, Sander F, Conley LH, Brooks BA, Hankinson O. 1991. Cloning of a factor required for activity of the Ah (dioxin) receptor. Science 252:954–958. https://doi.org/10.1126/science.1852076.
   PubMed Web of Science ®Google Scholar
• Gardella KA, Muro I, Fang G, Sarkar K, Mendez O, Wright CW. 2016. Aryl hydrocarbon receptor nuclear translocator (ARNT) isoforms control lymphoid cancer cell proliferation through differentially regulating tumor suppressor p53 activity. Oncotarget 7:10710–10722. https://doi.org/10.18632/oncotarget.7539.
   PubMedGoogle Scholar
• Black DL. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72:291–336. https://doi.org/10.1146/annurev.biochem.72.121801.161720.
   PubMed Web of Science ®Google Scholar
• Climente-González H, Porta-Pardo E, Godzik A, Eyras E. 2017. The functional impact of alternative splicing in cancer. Cell Rep 20:2215–2226. https://doi.org/10.1016/j.celrep.2017.08.012.
   PubMed Web of Science ®Google Scholar
• Dvinge H, Bradley RK. 2015. Widespread intron retention diversifies most cancer transcriptomes. Genome Med 7:45. https://doi.org/10.1186/s13073-015-0168-9.
   PubMed Web of Science ®Google Scholar
• Kahles A, Lehmann K-V, Toussaint NC, Hüser M, Stark SG, Sachsenberg T, Stegle O, Kohlbacher O, Sander C, Rätsch G, Caesar-Johnson SJ, Demchok JA, Felau I, Kasapi M, Ferguson ML, Hutter CM, Sofia HJ, Tarnuzzer R, Wang Z, Yang L, Zenklusen JC, Zhang JJ, Chudamani S, Liu J, Lolla L, Naresh R, Pihl T, Sun Q, Wan Y, Wu Y, Cho J, DeFreitas T, Frazer S, Gehlenborg N, Getz G, Heiman DI, Kim J, Lawrence MS, Lin P, Meier S, Noble MS, Saksena G, Voet D, Zhang H, Bernard B, Chambwe N, Dhankani V, Knijnenburg T, Kramer R, Leinonen K, Cancer Genome Atlas Research Network, et al. 2018. Comprehensive analysis of alternative splicing across tumors from 8,705 patients. Cancer Cell 34:211–224.e6.
   PubMed Web of Science ®Google Scholar
• Dvinge H, Kim E, Abdel-Wahab O, Bradley RK. 2016. RNA splicing factors as oncoproteins and tumour suppressors. Nat Rev Cancer 16:413–430. https://doi.org/10.1038/nrc.2016.51.
   PubMed Web of Science ®Google Scholar
• Sebestyén E, Singh B, Miñana B, Pagès A, Mateo F, Pujana MA, Valcárcel J, Eyras E. 2016. Large-scale analysis of genome and transcriptome alterations in multiple tumors unveils novel cancer-relevant splicing networks. Genome Res 26:732–744. https://doi.org/10.1101/gr.199935.115.
   PubMed Web of Science ®Google Scholar
• Conboy JG. 2017. Developmental regulation of RNA processing by Rbfox proteins. Wires Rna 8:e1398. https://doi.org/10.1002/wrna.1398.
   Google Scholar
• Huh GS, Hynes RO. 1994. Regulation of alternative pre-mRNA splicing by a novel repeated hexanucleotide element. Genes Dev 8:1561–1574. https://doi.org/10.1101/gad.8.13.1561.
   PubMed Web of Science ®Google Scholar
• Jin Y, Suzuki H, Maegawa S, Endo H, Sugano S, Hashimoto K, Yasuda K, Inoue K. 2003. A vertebrate RNA-binding protein Fox-1 regulates tissue-specific splicing via the pentanucleotide GCAUG. EMBO J 22:905–912. https://doi.org/10.1093/emboj/cdg089.
   PubMed Web of Science ®Google Scholar
• Kuroyanagi H. 2009. Fox-1 family of RNA-binding proteins. Cell Mol Life Sci 66:3895–3907. https://doi.org/10.1007/s00018-009-0120-5.
   PubMed Web of Science ®Google Scholar
• Nakahata S, Kawamoto S. 2005. Tissue-dependent isoforms of mammalian Fox-1 homologs are associated with tissue-specific splicing activities. Nucleic Acids Res 33:2078–2089. https://doi.org/10.1093/nar/gki338.
   PubMed Web of Science ®Google Scholar
• Underwood JG, Boutz PL, Dougherty JD, Stoilov P, Black DL. 2005. Homologues of the Caenorhabditis elegans Fox-1 protein are neuronal splicing regulators in mammals. Mol Cell Biol 25:10005–10016. https://doi.org/10.1128/MCB.25.22.10005-10016.2005.
   PubMed Web of Science ®Google Scholar
• Zhang C, Zhang Z, Castle J, Sun S, Johnson J, Krainer AR, Zhang MQ. 2008. Defining the regulatory network of the tissue-specific splicing factors Fox-1 and Fox-2. Genes Dev 22:2550–2563. https://doi.org/10.1101/gad.1703108.
   PubMed Web of Science ®Google Scholar
• Ge X, Yamamoto S, Tsutsumi S, Midorikawa Y, Ihara S, Wang S, Aburatani H. 2005. Interpreting expression profiles of cancers by genome-wide survey of breadth of expression in normal tissues. Genomics 86:127–141. https://doi.org/10.1016/j.ygeno.2005.04.008.
   PubMed Web of Science ®Google Scholar
• Lapuk A, Marr H, Jakkula L, Pedro H, Bhattacharya S, Purdom E, Hu Z, Simpson K, Pachter L, Durinck S, Wang N, Parvin B, Fontenay G, Speed T, Garbe J, Stampfer M, Bayandorian H, Dorton S, Clark TA, Schweitzer A, Wyrobek A, Feiler H, Spellman P, Conboy J, Gray JW. 2010. Exon-level microarray analyses identify alternative splicing programs in breast cancer. Mol Cancer Res 8:961–974. https://doi.org/10.1158/1541-7786.MCR-09-0528.
   PubMed Web of Science ®Google Scholar
• Venables JP, Klinck R, Koh C, Gervais-Bird J, Bramard A, Inkel L, Durand M, Couture S, Froehlich U, Lapointe E, Lucier J-F, Thibault P, Rancourt C, Tremblay K, Prinos P, Chabot B, Elela SA. 2009. Cancer-associated regulation of alternative splicing. Nat Struct Mol Biol 16:670–676. https://doi.org/10.1038/nsmb.1608.
   PubMed Web of Science ®Google Scholar
• Braeutigam C, Rago L, Rolke A, Waldmeier L, Christofori G, Winter J. 2014. The RNA-binding protein Rbfox2: an essential regulator of EMT-driven alternative splicing and a mediator of cellular invasion. Oncogene 33:1082–1092. https://doi.org/10.1038/onc.2013.50.
   PubMed Web of Science ®Google Scholar
• Shapiro IM, Cheng AW, Flytzanis NC, Balsamo M, Condeelis JS, Oktay MH, Burge CB, Gertler FB. 2011. An EMT-driven alternative splicing program occurs in human breast cancer and modulates cellular phenotype. PLoS Genet 7:e1002218. https://doi.org/10.1371/journal.pgen.1002218.
   PubMed Web of Science ®Google Scholar
• Venables JP, Brosseau J-P, Gadea G, Klinck R, Prinos P, Beaulieu J-F, Lapointe E, Durand M, Thibault P, Tremblay K, Rousset F, Tazi J, Abou Elela S, Chabot B. 2013. RBFOX2 is an important regulator of mesenchymal tissue-specific splicing in both normal and cancer tissues. Mol Cell Biol 33:396–405. https://doi.org/10.1128/MCB.01174-12.
   PubMed Web of Science ®Google Scholar
• Quentmeier H, Icgc M-SC, Pommerenke C, Bernhart SH, Dirks WG, Hauer V, Hoffmann S, Nagel S, Siebert R, Uphoff CC, Zaborski M, Drexler HG, ICGC MMML-Seq Consortium. 2018. RBFOX2 and alternative splicing in B-cell lymphoma. Blood Cancer J 8. https://doi.org/10.1038/s41408-018-0114-3.
   Google Scholar
• Van Nostrand EL, Pratt GA, Yee BA, Wheeler EC, Blue SM, Mueller J, Park SS, Garcia KE, Gelboin-Burkhart C, Nguyen TB, Rabano I, Stanton R, Sundararaman B, Wang R, Fu X-D, Graveley BR, Yeo GW. 2020. Principles of RNA processing from analysis of enhanced CLIP maps for 150 RNA binding proteins. Genome Biol 21. https://doi.org/10.1186/s13059-020-01982-9.
   Google Scholar
• Kalsotra A, Xiao X, Ward AJ, Castle JC, Johnson JM, Burge CB, Cooper TA. 2008. A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart. Proc Natl Acad Sci USA 105:20333–20338. https://doi.org/10.1073/pnas.0809045105.
   PubMed Web of Science ®Google Scholar
• Yeo GW, Coufal NG, Liang TY, Peng GE, Fu X-D, Gage FH. 2009. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat Struct Mol Biol 16:130–137. https://doi.org/10.1038/nsmb.1545.
   PubMed Web of Science ®Google Scholar
• Chan Y-Y, Kalpana S, Chang W-C, Chang W-C, Chen B-K. 2013. Expression of aryl hydrocarbon receptor nuclear translocator enhances cisplatin resistance by upregulating MDR1 expression in cancer cells. Mol Pharmacol 84:591–602. https://doi.org/10.1124/mol.113.087197.
   PubMed Web of Science ®Google Scholar
• Liang Y, Li W-W, Yang B-W, Tao Z-H, Sun H-C, Wang L, Xia J-L, Qin L-X, Tang Z-Y, Fan J, Wu W-Z. 2012. Aryl hydrocarbon receptor nuclear translocator is associated with tumor growth and progression of hepatocellular carcinoma. Int J Cancer 130:1745–1754. https://doi.org/10.1002/ijc.26166.
   PubMed Web of Science ®Google Scholar
• Barash Y, Calarco JA, Gao W, Pan Q, Wang X, Shai O, Blencowe BJ, Frey BJ. 2010. Deciphering the splicing code. Nature 465:53–59. https://doi.org/10.1038/nature09000.
   PubMed Web of Science ®Google Scholar
• Schultz A-S, Preussner M, Bunse M, Karni R, Heyd F. 2017. Activation-dependent TRAF3 exon 8 alternative splicing is controlled by CELF2 and hnRNP C binding to an upstream intronic element. Mol Cell Biol 37. https://doi.org/10.1128/MCB.00488-16.
   Google Scholar
• Lovci MT, Ghanem D, Marr H, Arnold J, Gee S, Parra M, Liang TY, Stark TJ, Gehman LT, Hoon S, Massirer KB, Pratt GA, Black DL, Gray JW, Conboy JG, Yeo GW. 2013. Rbfox proteins regulate alternative mRNA splicing through evolutionarily conserved RNA bridges. Nat Struct Mol Biol 20:1434–1442. https://doi.org/10.1038/nsmb.2699.
   PubMed Web of Science ®Google Scholar
• Verma SK, Deshmukh V, Nutter CA, Jaworski E, Jin W, Wadhwa L, Abata J, Ricci M, Lincoln J, Martin JF, Yeo GW, Kuyumcu-Martinez MN. 2016. Rbfox2 function in RNA metabolism is impaired in hypoplastic left heart syndrome patient hearts. Sci Rep 6:30896. https://doi.org/10.1038/srep30896.
   PubMed Web of Science ®Google Scholar
• Belanger K, Nutter CA, Li J, Tasnim S, Liu P, Yu P, Kuyumcu-Martinez MN. 2018. CELF1 contributes to aberrant alternative splicing patterns in the type 1 diabetic heart. Biochem Biophys Res Commun 503:3205–3211. https://doi.org/10.1016/j.bbrc.2018.08.126.
   PubMed Web of Science ®Google Scholar