Transcript Stabilization by the RNA-Binding Protein HuR Is Regulated by Cellular Retinoic Acid-Binding Protein 2

REFERENCES

• Chambon P. 1996. A decade of molecular biology of retinoic acid receptors. FASEB J. 10:940–954.
   PubMed Web of Science ®Google Scholar
• Schug TT, Berry DC, Shaw NS, Travis SN, Noy N. 2007. Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 129:723–733. http://dx.doi.org/10.1016/j.cell.2007.02.050.
   PubMed Web of Science ®Google Scholar
• Shaw N, Elholm M, Noy N. 2003. Retinoic acid is a high affinity selective ligand for the peroxisome proliferator-activated receptor beta/delta. J. Biol. Chem. 278:41589–41592. http://dx.doi.org/10.1074/jbc.C300368200.
   PubMed Web of Science ®Google Scholar
• Storch J, Corsico B. 2008. The emerging functions and mechanisms of mammalian fatty acid-binding proteins. Annu. Rev. Nutr. 28:73–95. http://dx.doi.org/10.1146/annurev.nutr.27.061406.093710.
   PubMed Web of Science ®Google Scholar
• Noy N. 2000. Retinoid-binding proteins: mediators of retinoid action. Biochem. J. 348(Part 3):481–495.
   PubMedGoogle Scholar
• Sessler RJ, Noy N. 2005. A ligand-activated nuclear localization signal in cellular retinoic acid binding protein-II. Mol. Cell 18:343–353. http://dx.doi.org/10.1016/j.molcel.2005.03.026.
   PubMed Web of Science ®Google Scholar
• Ayers SD, Nedrow KL, Gillilan RE, Noy N. 2007. Continuous nucleocytoplasmic shuttling underlies transcriptional activation of PPARgamma by FABP4. Biochemistry 46:6744–6752. http://dx.doi.org/10.1021/bi700047a.
   PubMed Web of Science ®Google Scholar
• Dong D, Ruuska SE, Levinthal DJ, Noy N. 1999. Distinct roles for cellular retinoic acid-binding proteins I and II in regulating signaling by retinoic acid. J. Biol. Chem. 274:23695–23698. http://dx.doi.org/10.1074/jbc.274.34.23695.
   PubMedGoogle Scholar
• Budhu AS, Noy N. 2002. Direct channeling of retinoic acid between cellular retinoic acid-binding protein II and retinoic acid receptor sensitizes mammary carcinoma cells to retinoic acid-induced growth arrest. Mol. Cell. Biol. 22:2632–2641. http://dx.doi.org/10.1128/MCB.22.8.2632-2641.2002.
   PubMed Web of Science ®Google Scholar
• Tan NS, Shaw NS, Vinckenbosch N, Liu P, Yasmin R, Desvergne B, Wahli W, Noy N. 2002. Selective cooperation between fatty acid binding proteins and peroxisome proliferator-activated receptors in regulating transcription. Mol. Cell. Biol. 22:5114–5127. http://dx.doi.org/10.1128/MCB.22.14.5114-5127.2002.
   PubMed Web of Science ®Google Scholar
• Soprano DR, Qin P, Soprano KJ. 2004. Retinoic acid receptors and cancers. Annu. Rev. Nutr. 24:201–221. http://dx.doi.org/10.1146/annurev.nutr.24.012003.132407.
   PubMed Web of Science ®Google Scholar
• Donato LJ, Noy N. 2005. Suppression of mammary carcinoma growth by retinoic acid: proapoptotic genes are targets for retinoic acid receptor and cellular retinoic acid-binding protein II signaling. Cancer Res. 65:8193–8199. http://dx.doi.org/10.1158/0008-5472.CAN-05-1177.
   PubMedGoogle Scholar
• Donato LJ, Suh JH, Noy N. 2007. Suppression of mammary carcinoma cell growth by retinoic acid: the cell cycle control gene Btg2 is a direct target for retinoic acid receptor signaling. Cancer Res. 67:609–615. http://dx.doi.org/10.1158/0008-5472.CAN-06-0989.
   PubMed Web of Science ®Google Scholar
• Noy N. 2010. Between death and survival: retinoic acid in regulation of apoptosis. Annu. Rev. Nutr. 30:201–217. http://dx.doi.org/10.1146/annurev.nutr.28.061807.155509.
   PubMed Web of Science ®Google Scholar
• Di-Poï N, Michalik L, Tan NS, Desvergne B, Wahli W. 2003. The anti-apoptotic role of PPARbeta contributes to efficient skin wound healing. J. Steroid Biochem. Mol. Biol. 85:257–265. http://dx.doi.org/10.1016/S0960-0760(03)00215-2.
   PubMed Web of Science ®Google Scholar
• Di-Poï N, Tan NS, Michalik L, Wahli W, Desvergne B. 2002. Antiapoptotic role of PPARbeta in keratinocytes via transcriptional control of the Akt1 signaling pathway. Mol. Cell 10:721–733. http://dx.doi.org/10.1016/S1097-2765(02)00646-9.
   PubMed Web of Science ®Google Scholar
• Wang D, Wang H, Guo Y, Ning W, Katkuri S, Wahli W, Desvergne B, Dey SK, DuBois RN. 2006. Crosstalk between peroxisome proliferator-activated receptor delta and VEGF stimulates cancer progression. Proc. Natl. Acad. Sci. U. S. A. 103:19069–19074. http://dx.doi.org/10.1073/pnas.0607948103.
   PubMed Web of Science ®Google Scholar
• Schug TT, Berry DC, Toshkov IA, Cheng L, Nikitin AY, Noy N. 2008. Overcoming retinoic acid-resistance of mammary carcinomas by diverting retinoic acid from PPARbeta/delta to RAR. Proc. Natl. Acad. Sci. U. S. A. 105:7546–7551. http://dx.doi.org/10.1073/pnas.0709981105.
   PubMed Web of Science ®Google Scholar
• Manor D, Shmidt EN, Budhu A, Flesken-Nikitin A, Zgola M, Page R, Nikitin AY, Noy N. 2003. Mammary carcinoma suppression by cellular retinoic acid binding protein-II. Cancer Res. 63:4426–4433.
   PubMed Web of Science ®Google Scholar
• Levi L, Lobo G, Doud MK, von Lintig J, Seachrist D, Tochtrop GP, Noy N. 2013. Genetic ablation of the fatty acid binding protein FABP5 suppresses HER2-induced mammary tumorigenesis. Cancer Res. 73:4770. http://dx.doi.org/10.1158/0008-5472.CAN-13-0384.
   PubMed Web of Science ®Google Scholar
• Campos B, Warta R, Chaisaingmongkol J, Geiselhart L, Popanda O, Hartmann C, von Deimling A, Unterberg A, Plass C, Schmezer P, Herold-Mende C. 2012. Epigenetically mediated downregulation of the differentiation-promoting chaperon protein CRABP2 in astrocytic gliomas. Int. J. Cancer 131:1963–1968. http://dx.doi.org/10.1002/ijc.27446.
   PubMedGoogle Scholar
• Calmon MF, Rodrigues RV, Kaneto CM, Moura RP, Silva SD, Mota LD, Pinheiro DG, Torres C, de Carvalho AF, Cury PM, Nunes FD, Nishimoto IN, Soares FA, da Silva AM, Kowalski LP, Brentani H, Zanelli CF, Silva WAJr, Rahal P, Tajara EH, Carraro DM, Camargo AA, Valentini SR. 2009. Epigenetic silencing of CRABP2 and MX1 in head and neck tumors. Neoplasia 11:1329–1339.
   PubMed Web of Science ®Google Scholar
• Gupta S, Pramanik D, Mukherjee R, Campbell NR, Elumalai S, de Wilde RF, Hong SM, Goggins MG, De Jesus-Acosta A, Laheru D, Maitra A. 2012. Molecular determinants of retinoic acid sensitivity in pancreatic cancer. Clin. Cancer Res. 18:280–289. http://dx.doi.org/10.1158/1078-0432.CCR-11-2165.
   PubMedGoogle Scholar
• Fu YS, Wang Q, Ma JX, Yang XH, Wu ML, Zhang KL, Kong QY, Chen XY, Sun Y, Chen NN, Shu XH, Li H, Liu J. 2012. CRABP-II methylation: a critical determinant of retinoic acid resistance of medulloblastoma cells. Mol. Oncol. 6:48–61. http://dx.doi.org/10.1016/j.molonc.2011.11.004.
   PubMedGoogle Scholar
• 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
• Myer VE, Fan XC, Steitz JA. 1997. Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay. EMBO J. 16:2130–2139. http://dx.doi.org/10.1093/emboj/16.8.2130.
   PubMed Web of Science ®Google Scholar
• Brennan CM, Steitz JA. 2001. HuR and mRNA stability. Cell. Mol. Life Sci. 58:266–277. http://dx.doi.org/10.1007/PL00000854.
   PubMed Web of Science ®Google Scholar
• Chen CY, Xu N, Shyu AB. 2002. Highly selective actions of HuR in antagonizing AU-rich element-mediated mRNA destabilization. Mol. Cell. Biol. 22:7268–7278. http://dx.doi.org/10.1128/MCB.22.20.7268-7278.2002.
   PubMed Web of Science ®Google Scholar
• López 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
• Ghosh M, Aguila HL, Michaud J, Ai Y, Wu MT, Hemmes A, Ristimaki A, Guo C, Furneaux H, Hla T. 2009. Essential role of the RNA-binding protein HuR in progenitor cell survival in mice. J. Clin. Invest. 119:3530–3543. http://dx.doi.org/10.1172/JCI38263.
   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
• Budhu A, Gillilan R, Noy N. 2001. Localization of the RAR interaction domain of cellular retinoic acid binding protein-II. J. Mol. Biol. 305:939–949. http://dx.doi.org/10.1006/jmbi.2000.4340.
   PubMedGoogle Scholar
• Keene JD, Tenenbaum SA. 2002. Eukaryotic mRNPs may represent posttranscriptional operons. Mol. Cell 9:1161–1167. http://dx.doi.org/10.1016/S1097-2765(02)00559-2.
   PubMed Web of Science ®Google Scholar
• Donato LJ, Noy N. 2006. A fluorescence-based method for analyzing retinoic acid in biological samples. Anal. Biochem. 357:249–256. http://dx.doi.org/10.1016/j.ab.2006.07.020.
   PubMedGoogle Scholar
• Norris AW, Cheng L, Giguere V, Rosenberger M, Li E. 1994. Measurement of subnanomolar retinoic acid binding affinities for cellular retinoic acid binding proteins by fluorometric titration. Biochim. Biophys. Acta 1209:10–18. http://dx.doi.org/10.1016/0167-4838(94)90130-9.
   PubMedGoogle Scholar
• Giles KM, Daly JM, Beveridge DJ, Thomson AM, Voon DC, Furneaux HM, Jazayeri JA, Leedman PJ. 2003. The 3′-untranslated region of p21WAF1 mRNA is a composite cis-acting sequence bound by RNA-binding proteins from breast cancer cells, including HuR and poly(C)-binding protein. J. Biol. Chem. 278:2937–2946. http://dx.doi.org/10.1074/jbc.M208439200.
   PubMed Web of Science ®Google Scholar
• Majumdar A, Petrescu AD, Xiong Y, Noy N. 2011. Nuclear translocation of cellular retinoic acid-binding protein II is regulated by retinoic acid-controlled SUMOylation. J. Biol. Chem. 286:42749–42757. http://dx.doi.org/10.1074/jbc.M111.293464.
   PubMed Web of Science ®Google Scholar
• Guy CT, Webster MA, Schaller M, Parsons TJ, Cardiff RD, Muller WJ. 1992. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc. Natl. Acad. Sci. U. S. A. 89:10578–10582. http://dx.doi.org/10.1073/pnas.89.22.10578.
   PubMed Web of Science ®Google Scholar
• Barreau C, Paillard L, Osborne HB. 2005. AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res. 33:7138–7150. http://dx.doi.org/10.1093/nar/gki1012.
   PubMed Web of Science ®Google Scholar
• Al-Ahmadi W, Al-Ghamdi M, Al-Haj L, Al-Saif M, Khabar KS. 2009. Alternative polyadenylation variants of the RNA binding protein, HuR: abundance, role of AU-rich elements and auto-regulation. Nucleic Acids Res. 37:3612–3624. http://dx.doi.org/10.1093/nar/gkp223.
   PubMedGoogle Scholar
• Lakowicz JR. 1983. Principles of fluorescence spectroscopy. Plenum Press, New York, NY.
   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
• Pullmann RJr, Juhaszova M, Lopez de Silanes I, Kawai T, Mazan-Mamczarz K, Halushka MK, Gorospe M. 2005. Enhanced proliferation of cultured human vascular smooth muscle cells linked to increased function of RNA-binding protein HuR. J. Biol. Chem. 280:22819–22826. http://dx.doi.org/10.1074/jbc.M501106200.
   PubMedGoogle 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
• Latorre E, Tebaldi T, Viero G, Sparta AM, Quattrone A, Provenzani A. 2012. Downregulation of HuR as a new mechanism of doxorubicin resistance in breast cancer cells. Mol. Cancer 11:13. http://dx.doi.org/10.1186/1476-4598-11-13.
   PubMed Web of Science ®Google Scholar
• Gubin MM, Calaluce R, Davis JW, Magee JD, Strouse CS, Shaw DP, Ma L, Brown A, Hoffman T, Rold TL, Atasoy U. 2010. Overexpression of the RNA binding protein HuR impairs tumor growth in triple negative breast cancer associated with deficient angiogenesis. Cell Cycle 9:3337–3346. http://dx.doi.org/10.4161/cc.9.16.12711.
   PubMed Web of Science ®Google Scholar
• Mazroui R, Di Marco S, Clair E, von Roretz C, Tenenbaum SA, Keene JD, Saleh M, Gallouzi IE. 2008. Caspase-mediated cleavage of HuR in the cytoplasm contributes to pp32/PHAP-I regulation of apoptosis. J. Cell Biol. 180:113–127. http://dx.doi.org/10.1083/jcb.200709030.
   PubMed Web of Science ®Google Scholar
• Minocha A, Long BH. 1984. Inhibition of the DNA catenation activity of type II topoisomerase by VP16-213 and VM26. Biochem. Biophys. Res. Commun. 122:165–170. http://dx.doi.org/10.1016/0006-291X(84)90454-6.
   PubMed Web of Science ®Google Scholar
• Gillilan RE, Ayers SD, Noy N. 2007. Structural basis for activation of fatty acid-binding protein 4. J. Mol. Biol. 372:1246–1260. http://dx.doi.org/10.1016/j.jmb.2007.07.040.
   PubMed Web of Science ®Google Scholar
• Ortega AD, Sala S, Espinosa E, Gonzalez-Baron M, Cuezva JM. 2008. HuR and the bioenergetic signature of breast cancer: a low tumor expression of the RNA-binding protein predicts a higher risk of disease recurrence. Carcinogenesis 29:2053–2061. http://dx.doi.org/10.1093/carcin/bgn185.
   PubMed Web of Science ®Google Scholar