HuR Regulates Alternative Splicing of the TRA2β Gene in Human Colon Cancer Cells under Oxidative Stress

REFERENCES

• Hinman MN, Lou H. 2008. Diverse molecular functions of Hu proteins. Cell. Mol. Life Sci. 65:3168–3181. http://dx.doi.org/10.1007/s00018-008-8252-6.
   PubMed Web of Science ®Google Scholar
• Lopez de Silanes I, Zhan M, Lal A, Yang X, Gorospe M. 2004. Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. U. S. A. 101:2987–2992. http://dx.doi.org/10.1073/pnas.0306453101.
   PubMed Web of Science ®Google Scholar
• Abdelmohsen K, Kuwano Y, Kim HH, Gorospe M. 2008. Posttranscriptional gene regulation by RNA-binding proteins during oxidative stress: implications for cellular senescence. Biol. Chem. 389:243–255. http://dx.doi.org/10.1515/BC.2008.022.
   PubMed Web of Science ®Google Scholar
• Abdelmohsen K, Pullmann RJr, Lal A, Kim HH, Galban S, Yang X, Blethrow JD, Walker M, Shubert J, Gillespie DA, Furneaux H, Gorospe M. 2007. Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol. Cell 25:543–557. http://dx.doi.org/10.1016/j.molcel.2007.01.011.
   PubMed Web of Science ®Google Scholar
• Abdelmohsen K, Lal A, Kim HH, Gorospe M. 2007. Posttranscriptional orchestration of an anti-apoptotic program by HuR. Cell Cycle 6:1288–1292. http://dx.doi.org/10.4161/cc.6.11.4299.
   PubMed Web of Science ®Google Scholar
• Kim HH, Abdelmohsen K, Lal A, Pullmann RJr, Yang X, Galban S, Srikantan S, Martindale JL, Blethrow J, Shokat KM, Gorospe M. 2008. Nuclear HuR accumulation through phosphorylation by Cdk1. Genes Dev. 22:1804–1815. http://dx.doi.org/10.1101/gad.1645808.
   PubMed Web of Science ®Google Scholar
• Kim HH, Kuwano Y, Srikantan S, Lee EK, Martindale JL, Gorospe M. 2009. HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev. 23:1743–1748. http://dx.doi.org/10.1101/gad.1812509.
   PubMed Web of Science ®Google Scholar
• Kullmann M, Gopfert U, Siewe B, Hengst L. 2002. ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5′ UTR. Genes Dev. 16:3087–3099. http://dx.doi.org/10.1101/gad.248902.
   PubMed Web of Science ®Google Scholar
• Lal A, Kawai T, Yang X, Mazan-Mamczarz K, Gorospe M. 2005. Antiapoptotic function of RNA-binding protein HuR effected through prothymosin alpha. EMBO J. 24:1852–1862. http://dx.doi.org/10.1038/sj.emboj.7600661.
   PubMed Web of Science ®Google Scholar
• Lal A, Mazan-Mamczarz K, Kawai T, Yang X, Martindale JL, Gorospe M. 2004. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23:3092–3102. http://dx.doi.org/10.1038/sj.emboj.7600305.
   PubMed Web of Science ®Google Scholar
• Levy NS, Chung S, Furneaux H, Levy AP. 1998. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 273:6417–6423. http://dx.doi.org/10.1074/jbc.273.11.6417.
   PubMed Web of Science ®Google Scholar
• Mazan-Mamczarz K, Galban S, Lopez de Silanes I, Martindale JL, Atasoy U, Keene JD, Gorospe M. 2003. RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc. Natl. Acad. Sci. U. S. A. 100:8354–8359. http://dx.doi.org/10.1073/pnas.1432104100.
   PubMed Web of Science ®Google Scholar
• Dixon DA, Tolley ND, King PH, Nabors LB, McIntyre TM, Zimmerman GA, Prescott SM. 2001. Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J. Clin. Invest. 108:1657–1665. http://dx.doi.org/10.1172/JCI200112973.
   PubMed Web of Science ®Google Scholar
• Wang W, Caldwell MC, Lin S, Furneaux H, Gorospe M. 2000. HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J. 19:2340–2350. http://dx.doi.org/10.1093/emboj/19.10.2340.
   PubMed Web of Science ®Google Scholar
• Wang W, Furneaux H, Cheng H, Caldwell MC, Hutter D, Liu Y, Holbrook N, Gorospe M. 2000. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20:760–769. http://dx.doi.org/10.1128/MCB.20.3.760-769.2000.
   PubMed Web of Science ®Google Scholar
• Izquierdo JM. 2008. Hu antigen R (HuR) functions as an alternative pre-mRNA splicing regulator of Fas apoptosis-promoting receptor on exon definition. J. Biol. Chem. 283:19077–19084. http://dx.doi.org/10.1074/jbc.M800017200.
   PubMed Web of Science ®Google Scholar
• Lebedeva S, Jens M, Theil K, Schwanhausser B, Selbach M, Landthaler M, Rajewsky N. 2011. Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol. Cell 43:340–352. http://dx.doi.org/10.1016/j.molcel.2011.06.008.
   PubMed Web of Science ®Google Scholar
• Mukherjee N, Corcoran DL, Nusbaum JD, Reid DW, Georgiev S, Hafner M, Ascano MJr, Tuschl T, Ohler U, Keene JD. 2011. Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol. Cell 43:327–339. http://dx.doi.org/10.1016/j.molcel.2011.06.007.
   PubMed Web of Science ®Google Scholar
• Zhu H, Zhou HL, Hasman RA, Lou H. 2007. Hu proteins regulate polyadenylation by blocking sites containing U-rich sequences. J. Biol. Chem. 282:2203–2210. http://dx.doi.org/10.1074/jbc.M609349200.
   PubMed Web of Science ®Google Scholar
• Kornblihtt AR, Schor IE, Allo M, Dujardin G, Petrillo E, Munoz MJ. 2013. Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat. Rev. Mol. Cell Biol. 14:153–165. http://dx.doi.org/10.1038/nrm3525.
   PubMed Web of Science ®Google Scholar
• Matlin AJ, Clark F, Smith CW. 2005. Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell Biol. 6:386–398. http://dx.doi.org/10.1038/nrm1645.
   PubMed Web of Science ®Google Scholar
• Wang Z, Burge CB. 2008. Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA 14:802–813. http://dx.doi.org/10.1261/rna.876308.
   PubMed Web of Science ®Google Scholar
• Schwartz SH, Silva J, Burstein D, Pupko T, Eyras E, Ast G. 2008. Large-scale comparative analysis of splicing signals and their corresponding splicing factors in eukaryotes. Genome Res. 18:88–103. http://dx.doi.org/10.1101/gr.6818908.
   PubMedGoogle Scholar
• Barbosa-Morais NL, Carmo-Fonseca M, Aparicio S. 2006. Systematic genome-wide annotation of spliceosomal proteins reveals differential gene family expansion. Genome Res. 16:66–77. http://dx.doi.org/10.1101/gr.3936206.
   PubMed Web of Science ®Google Scholar
• Novoyatleva T, Heinrich B, Tang Y, Benderska N, Butchbach ME, Lorson CL, Lorson MA, Ben-Dov C, Fehlbaum P, Bracco L, Burghes AH, Bollen M, Stamm S. 2008. Protein phosphatase 1 binds to the RNA recognition motif of several splicing factors and regulates alternative pre-mRNA processing. Hum. Mol. Genet. 17:52–70. http://dx.doi.org/10.1093/hmg/ddm284.
   PubMedGoogle Scholar
• Kondo S, Yamamoto N, Murakami T, Okumura M, Mayeda A, Imaizumi K. 2004. Tra2 beta, SF2/ASF and SRp30c modulate the function of an exonic splicing enhancer in exon 10 of tau pre-mRNA. Genes Cells 9:121–130. http://dx.doi.org/10.1111/j.1356-9597.2004.00709.x.
   PubMed Web of Science ®Google Scholar
• Singh NN, Androphy EJ, Singh RN. 2004. In vivo selection reveals combinatorial controls that define a critical exon in the spinal muscular atrophy genes. RNA 10:1291–1305. http://dx.doi.org/10.1261/rna.7580704.
   PubMed Web of Science ®Google Scholar
• Tran Q, Coleman TP, Roesser JR. 2003. Human transformer 2beta and SRp55 interact with a calcitonin-specific splice enhancer. Biochim. Biophys. Acta 1625:141–152. http://dx.doi.org/10.1016/S0167-4781(02)00600-0.
   PubMedGoogle Scholar
• Anderson ES, Lin CH, Xiao X, Stoilov P, Burge CB, Black DL. 2012. The cardiotonic steroid digitoxin regulates alternative splicing through depletion of the splicing factors SRSF3 and TRA2B. RNA 18:1041–1049. http://dx.doi.org/10.1261/rna.032912.112.
   PubMedGoogle Scholar
• Nayler O, Cap C, Stamm S. 1998. Human transformer-2-beta gene (SFRS10): complete nucleotide sequence, chromosomal localization, and generation of a tissue-specific isoform. Genomics 53:191–202. http://dx.doi.org/10.1006/geno.1998.5471.
   PubMed Web of Science ®Google Scholar
• Ashibe B, Hirai T, Higashi K, Sekimizu K, Motojima K. 2007. Dual subcellular localization in the endoplasmic reticulum and peroxisomes and a vital role in protecting against oxidative stress of fatty aldehyde dehydrogenase are achieved by alternative splicing. J. Biol. Chem. 282:20763–20773. http://dx.doi.org/10.1074/jbc.M611853200.
   PubMed Web of Science ®Google Scholar
• Hang X, Li P, Li Z, Qu W, Yu Y, Li H, Shen Z, Zheng H, Gao Y, Wu Y, Deng M, Sun Z, Zhang C. 2009. Transcription and splicing regulation in human umbilical vein endothelial cells under hypoxic stress conditions by exon array. BMC Genomics 10:126. http://dx.doi.org/10.1186/1471-2164-10-126.
   PubMed Web of Science ®Google Scholar
• Hirschfeld M, zur Hausen A, Bettendorf H, Jager M, Stickeler E. 2009. Alternative splicing of Cyr61 is regulated by hypoxia and significantly changed in breast cancer. Cancer Res. 69:2082–2090. http://dx.doi.org/10.1158/0008-5472.CAN-08-1997.
   PubMed Web of Science ®Google Scholar
• Matsuo N, Ogawa S, Imai Y, Takagi T, Tohyama M, Stern D, Wanaka A. 1995. Cloning of a novel RNA binding polypeptide (RA301) induced by hypoxia/reoxygenation. J. Biol. Chem. 270:28216–28222. http://dx.doi.org/10.1074/jbc.270.47.28216.
   PubMed Web of Science ®Google Scholar
• Kattapuram T, Yang S, Maki JL, Stone JR. 2005. Protein kinase CK1alpha regulates mRNA binding by heterogeneous nuclear ribonucleoprotein C in response to physiologic levels of hydrogen peroxide. J. Biol. Chem. 280:15340–15347. http://dx.doi.org/10.1074/jbc.M500214200.
   PubMedGoogle Scholar
• Panchenko MP, Silva N, Stone JR. 2009. Up-regulation of a hydrogen peroxide-responsive pre-mRNA binding protein in atherosclerosis and intimal hyperplasia. Cardiovasc. Pathol. 18:167–172. http://dx.doi.org/10.1016/j.carpath.2008.03.008.
   PubMed Web of Science ®Google Scholar
• Takeo K, Kawai T, Nishida K, Masuda K, Teshima-Kondo S, Tanahashi T, Rokutan K. 2009. Oxidative stress-induced alternative splicing of transformer 2beta (SFRS10) and CD44 pre-mRNAs in gastric epithelial cells. Am. J. Physiol. Cell Physiol. 297:C330–C338. http://dx.doi.org/10.1152/ajpcell.00009.2009.
   PubMed Web of Science ®Google Scholar
• Masuda K, Abdelmohsen K, Kim MM, Srikantan S, Lee EK, Tominaga K, Selimyan R, Martindale JL, Yang X, Lehrmann E, Zhang Y, Becker KG, Wang JY, Kim HH, Gorospe M. 2011. Global dissociation of HuR-mRNA complexes promotes cell survival after ionizing radiation. EMBO J. 30:1040–1053. http://dx.doi.org/10.1038/emboj.2011.24.
   PubMed Web of Science ®Google Scholar
• Kinoshita E, Kinoshita-Kikuta E, Takiyama K, Koike T. 2006. Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics 5:749–757. http://dx.doi.org/10.1074/mcp.T500024-MCP200.
   PubMed Web of Science ®Google Scholar
• Kajita K, Kuwano Y, Kitamura N, Satake Y, Nishida K, Kurokawa K, Akaike Y, Honda M, Masuda K, Rokutan K. 2013. Ets1 and heat shock factor 1 regulate transcription of the Transformer 2beta gene in human colon cancer cells. J. Gastroenterol. 48:1222–1233. http://dx.doi.org/10.1007/s00535-012-0745-2.
   PubMedGoogle Scholar
• Stoilov P, Daoud R, Nayler O, Stamm S. 2004. Human tra2-beta1 autoregulates its protein concentration by influencing alternative splicing of its pre-mRNA. Hum. Mol. Genet. 13:509–524. http://dx.doi.org/10.1093/hmg/ddh051.
   PubMed Web of Science ®Google Scholar
• Amadio M, Bucolo C, Leggio GM, Drago F, Govoni S, Pascale A. 2010. The PKCbeta/HuR/VEGF pathway in diabetic retinopathy. Biochem. Pharmacol. 80:1230–1237. http://dx.doi.org/10.1016/j.bcp.2010.06.033.
   PubMed Web of Science ®Google Scholar
• Doller A, Akool el, Huwiler SA, Muller R, Radeke HH, Pfeilschifter J, Eberhardt W. 2008. Posttranslational modification of the AU-rich element binding protein HuR by protein kinase Cdelta elicits angiotensin II-induced stabilization and nuclear export of cyclooxygenase 2 mRNA. Mol. Cell. Biol. 28:2608–2625. http://dx.doi.org/10.1128/MCB.01530-07.
   PubMed Web of Science ®Google Scholar
• Doller A, Huwiler A, Muller R, Radeke HH, Pfeilschifter J, Eberhardt W. 2007. Protein kinase C alpha-dependent phosphorylation of the mRNA-stabilizing factor HuR: implications for posttranscriptional regulation of cyclooxygenase-2. Mol. Biol. Cell 18:2137–2148. http://dx.doi.org/10.1091/mbc.E06-09-0850.
   PubMed Web of Science ®Google Scholar
• Lafarga V, Cuadrado A, Lopez de Silanes I, Bengoechea R, Fernandez-Capetillo O, Nebreda AR. 2009. p38 mitogen-activated protein kinase- and HuR-dependent stabilization of p21(Cip1) mRNA mediates the G1/S checkpoint. Mol. Cell. Biol. 29:4341–4351. http://dx.doi.org/10.1128/MCB.00210-09.
   PubMed Web of Science ®Google Scholar
• Zhu H, Hasman RA, Barron VA, Luo G, Lou H. 2006. A nuclear function of Hu proteins as neuron-specific alternative RNA processing regulators. Mol. Biol. Cell 17:5105–5114. http://dx.doi.org/10.1091/mbc.E06-02-0099.
   PubMed Web of Science ®Google Scholar
• Zhu H, Hinman MN, Hasman RA, Mehta P, Lou H. 2008. Regulation of neuron-specific alternative splicing of neurofibromatosis type 1 pre-mRNA. Mol. Cell. Biol. 28:1240–1251. http://dx.doi.org/10.1128/MCB.01509-07.
   PubMed Web of Science ®Google Scholar
• Bellavia D, Mecarozzi M, Campese AF, Grazioli P, Talora C, Frati L, Gulino A, Screpanti I. 2007. Notch3 and the Notch3-upregulated RNA-binding protein HuD regulate Ikaros alternative splicing. EMBO J. 26:1670–1680. http://dx.doi.org/10.1038/sj.emboj.7601626.
   PubMedGoogle Scholar
• Zhou HL, Hinman MN, Barron VA, Geng C, Zhou G, Luo G, Siegel RE, Lou H. 2011. Hu proteins regulate alternative splicing by inducing localized histone hyperacetylation in an RNA-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 108:E627–E635. http://dx.doi.org/10.1073/pnas.1103344108.
   PubMed Web of Science ®Google Scholar
• Abdelmohsen K, Srikantan S, Yang X, Lal A, Kim HH, Kuwano Y, Galban S, Becker KG, Kamara D, de Cabo R, Gorospe M. 2009. Ubiquitin-mediated proteolysis of HuR by heat shock. EMBO J. 28:1271–1282. http://dx.doi.org/10.1038/emboj.2009.67.
   PubMed Web of Science ®Google Scholar
• Alvarez E, Castello A, Carrasco L, Izquierdo JM. 2013. Poliovirus 2A protease triggers a selective nucleo-cytoplasmic redistribution of splicing factors to regulate alternative pre-mRNA splicing. PLoS One 8:e73723. http://dx.doi.org/10.1371/journal.pone.0073723.
   PubMed Web of Science ®Google Scholar
• Eberhardt W, Doller A, Pfeilschifter J. 2012. Regulation of the mRNA-binding protein HuR by posttranslational modification: spotlight on phosphorylation. Curr. Protein Pept. Sci. 13:380–390. http://dx.doi.org/10.2174/138920312801619439.
   PubMed Web of Science ®Google Scholar
• Wilusz CJ, Wilusz J. 2007. HuR-SIRT: the hairy world of posttranscriptional control. Mol. Cell 25:485–487. http://dx.doi.org/10.1016/j.molcel.2007.02.001.
   PubMedGoogle Scholar
• Bakheet T, Frevel M, Williams BR, Greer W, Khabar KS. 2001. ARED: human AU-rich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins. Nucleic Acids Res. 29:246–254. http://dx.doi.org/10.1093/nar/29.1.246.
   PubMedGoogle Scholar
• Bakheet T, Williams BR, Khabar KS. 2003. ARED 2.0: an update of AU-rich element mRNA database. Nucleic Acids Res. 31:421–423. http://dx.doi.org/10.1093/nar/gkg023.
   PubMed Web of Science ®Google Scholar
• Chen CY, Shyu AB. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465–470. http://dx.doi.org/10.1016/S0968-0004(00)89102-1.
   PubMed Web of Science ®Google Scholar
• Dean JL, Wait R, Mahtani KR, Sully G, Clark AR, Saklatvala J. 2001. The 3′ untranslated region of tumor necrosis factor alpha mRNA is a target of the mRNA-stabilizing factor HuR. Mol. Cell. Biol. 21:721–730. http://dx.doi.org/10.1128/MCB.21.3.721-730.2001.
   PubMed Web of Science ®Google Scholar
• Jain RG, Andrews LG, McGowan KM, Pekala PH, Keene JD. 1997. Ectopic expression of Hel-N1, an RNA-binding protein, increases glucose transporter (GLUT1) expression in 3T3-L1 adipocytes. Mol. Cell. Biol. 17:954–962.
   PubMedGoogle Scholar
• Levine TD, Gao F, King PH, Andrews LG, Keene JD. 1993. Hel-N1: an autoimmune RNA-binding protein with specificity for 3′ uridylate-rich untranslated regions of growth factor mRNAs. Mol. Cell. Biol. 13:3494–3504.
   PubMed Web of Science ®Google Scholar
• Uren PJ, Burns SC, Ruan J, Singh KK, Smith AD, Penalva LO. 2011. Genomic analyses of the RNA-binding protein Hu antigen R (HuR) identify a complex network of target genes and novel characteristics of its binding sites. J. Biol. Chem. 286:37063–37066. http://dx.doi.org/10.1074/jbc.C111.266882.
   PubMed Web of Science ®Google Scholar
• Abdelmohsen K, Gorospe M. 2010. Posttranscriptional regulation of cancer traits by HuR. Wiley Interdiscip. Rev. RNA 1:214–229. http://dx.doi.org/10.1002/wrna.4.
   PubMed Web of Science ®Google Scholar
• Denkert C, Koch I, von Keyserlingk N, Noske A, Niesporek S, Dietel M, Weichert W. 2006. Expression of the ELAV-like protein HuR in human colon cancer: association with tumor stage and cyclooxygenase-2. Mod. Pathol. 19:1261–1269. http://dx.doi.org/10.1038/modpathol.3800645.
   PubMed Web of Science ®Google Scholar
• Lim SJ, Lee SH, Joo SH, Song JY, Choi SI. 2009. Cytoplasmic expression of HuR is related to cyclooxygenase-2 expression in colon cancer. Cancer Res. Treat. 41:87–92. http://dx.doi.org/10.4143/crt.2009.41.2.87.
   PubMedGoogle Scholar
• Lopez de Silanes I, Fan J, Yang X, Zonderman AB, Potapova O, Pizer ES, Gorospe M. 2003. Role of the RNA-binding protein HuR in colon carcinogenesis. Oncogene 22:7146–7154. http://dx.doi.org/10.1038/sj.onc.1206862.
   PubMed Web of Science ®Google Scholar