Stabilization of the G-quadruplex at the VEGF IRES represses cap-independent translation

RNA Biology

Volumn 12, Issue 3, 2015, Pages 320-329

  Cammas, Anne ^a   Dubrac, Alexandre ^a   Morel, Benjamin ^a   Lamaa, Assala ^a   Touriol, Christian ^a   Teulade Fichou, Marie Paule ^b   Prats, Hervé ^a   Millevoi, Stefania ^a  

^a CANCER RESEARCH CENTER OF TOULOUSE   (France)

^b CNRS   (France)

Author keywords

Cap independent; G quadruplex; IRES; Ligands; mRNA translation; VEGF

Indexed keywords

GUANINE QUADRUPLEX; INITIATION FACTOR 2ALPHA; MESSENGER RNA; VASCULOTROPIN; X BOX BINDING PROTEIN 1; 5' UNTRANSLATED REGION; GUANOSINE TRIPHOSPHATASE; INTERNAL RIBOSOME ENTRY SITE; LUCIFERASE; MEMBRANE PROTEIN; NRAS PROTEIN, HUMAN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

5' UNTRANSLATED REGION; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DISULFIDE BOND; DNA STRUCTURE; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE EXPRESSION; HELA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERNAL RIBOSOME ENTRY SITE; OPEN READING FRAME; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN STABILITY; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION; RNA TRANSLATION; SEQUENCE ANALYSIS; START CODON; STOP CODON; STRUCTURE ACTIVITY RELATION; TRANSLATION INITIATION; UNFOLDED PROTEIN RESPONSE; UPREGULATION; WILD TYPE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; POLYSOME; REPORTER GENE;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; G-QUADRUPLEXES; GENE EXPRESSION REGULATION; GENES, REPORTER; GTP PHOSPHOHYDROLASES; HELA CELLS; HUMANS; INTERNAL RIBOSOME ENTRY SITES; LUCIFERASES; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84928237878     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.1080/15476286.2015.1017236     Document Type: Article

References (46)

1. Ji X, Sun H, Zhou H, Xiang J, Tang Y, Zhao C. Research progress of RNA quadruplex. Nucleic Acid Ther 2011; 21:185–200. PMID:21749296. http://dx.doi.org/10.1089/nat.2010.0272
2. Millevoi S, Moine H, Vagner S. G-quadruplexes in RNA biology. Wiley Interdiscip Rev RNA 2012; 3:495–507. PMID:22488917. http://dx.doi.org/10.1002/wrna.1113
3. Beaudoin JD, Perreault JP. 5’-UTR G-quadruplex structures acting as translational repressors. Nucleic Acids Res 2010; 38:7022–36. PMID:20571090. http://dx.doi.org/10.1093/nar/gkq557
4. Kumari S, Bugaut A, Huppert JL, Balasubramanian S. An RNA G-quadruplex in the 5’ UTR of the NRAS proto-oncogene modulates translation. Nat Chem Biol 2007; 3:218–21. PMID:17322877. http://dx.doi.org/10.1038/nchembio864
5. Bugaut A, Balasubramanian S. 5’-UTR RNA G-quadruplexes: translation regulation and targeting. Nucleic Acids Res 2012; 40:4727–41. PMID:22351747. http://dx.doi.org/10.1093/nar/gks068
6. Halder K, Wieland M, Hartig JS. Predictable suppression of gene expression by 5’-UTR-based RNA quadruplexes. Nucleic Acids Res 2009; 37:6811–7. PMID:19740765. http://dx.doi.org/10.1093/nar/gkp696
7. Halder K, Largy E, Benzler M, Teulade-Fichou MP, Hartig JS. Efficient suppression of gene expression by targeting 5’-UTR-based RNA quadruplexes with bisquinolinium compounds. Chembiochem 2011; 12:1663–8. PMID:21681881. http://dx.doi.org/10.1002/cbic.201100228
8. Kumari S, Bugaut A, Balasubramanian S. Position and stability are determining factors for translation repression by an RNA G-quadruplex-forming sequence within the 5’ UTR of the NRAS proto-oncogene. Biochemistry 2008; 47:12664–9. PMID:18991403. http://dx.doi.org/10.1021/bi8010797
9. Wieland M, Hartig JS. RNA quadruplex-based modulation of gene expression. Chem Biol 2007; 14:757–63. PMID:17656312. http://dx.doi.org/10.1016/j. chembiol.2007.06.005
10. Bugaut A, Rodriguez R, Kumari S, Hsu ST, Balasubramanian S. Small molecule-mediated inhibition of translation by targeting a native RNA G-quadruplex. Org Biomol Chem 2010; 8:2771–6. PMID:20436976. http://dx.doi.org/10.1039/c002418j
11. Gomez D, Guedin A, Mergny JL, Salles B, Riou JF, Teulade-Fichou MP, Calsou P. A G-quadruplex structure within the 5’-UTR of TRF2 mRNA represses translation in human cells. Nucleic Acids Res 2010; 38:7187–98. PMID:20571083. http://dx.doi.org/10.1093/nar/gkq563
12. Ofer N, Weisman-Shomer P, Shklover J, Fry M. The quadruplex r(CGG)n destabilizing cationic porphyrin TMPyP4 cooperates with hnRNPs to increase the translation efficiency of fragile X premutation mRNA. Nucleic Acids Res 2009; 37:2712–22. PMID:19273535. http://dx.doi.org/10.1093/nar/gkp130
13. Ito K, Go S, Komiyama M, Xu Y. Inhibition of translation by small RNA-stabilized mRNA structures in human cells. J Am Chem Soc 2011; 133:19153–9. PMID:22007660. http://dx.doi.org/10.1021/ja206353c
14. Wolfe AL, Singh K, Zhong Y, Drewe P, Rajasekhar VK, Sanghvi VR, Mavrakis KJ, Jiang M, Roderick JE, Van der Meulen J., et al. RNA G-quadruplexes cause eIF4A-dependent oncogene translation in cancer. Nature 2014; 513:65–70. PMID:25079319. http://dx.doi.org/10.1038/nature13485
15. Arcondeguy T, Lacazette E, Millevoi S, Prats H, Touriol C. VEGF-A mRNA processing, stability and translation: a paradigm for intricate regulation of gene expression at the post-transcriptional level. Nucleic Acids Res 2013; 41:7997–8010. PMID:23851566. http://dx.doi.org/10.1093/nar/gkt539
16. Huez I, Creancier L, Audigier S, Gensac MC, Prats AC, Prats H. Two independent internal ribosome entry sites are involved in translation initiation of vascular endothelial growth factor mRNA. Mol Cell Biol 1998; 18:6178–90. PMID:9774635
17. Miller DL, Dibbens JA, Damert A, Risau W, Vadas MA, Goodall GJ. The vascular endothelial growth factor mRNA contains an internal ribosome entry site. FEBS Lett 1998; 434:417–20. PMID:9742966. http://dx.doi.org/10.1016/S0014-5793(98)01025-4
18. Akiri G, Nahari D, Finkelstein Y, Le SY, Elroy-Stein O, Levi BZ. Regulation of vascular endothelial growth factor (VEGF) expression is mediated by internal initiation of translation and alternative initiation of transcription. Oncogene 1998; 17:227–36. PMID:9674707. http://dx.doi.org/10.1038/sj. onc.1202019
19. Stein I, Itin A, Einat P, Skaliter R, Grossman Z, Keshet E. Translation of vascular endothelial growth factor mRNA by internal ribosome entry: implications for translation under hypoxia. Mol Cell Biol 1998; 18:3112–9. PMID:9584152
20. Lang KJ, Kappel A, Goodall GJ. Hypoxia-inducible factor-1alpha mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. Mol Biol Cell 2002; 13:1792–801. PMID:12006670. http://dx.doi.org/10.1091/mbc.02- 02-0017
21. Bornes S, Prado-Lourenco L, Bastide A, Zanibellato C, Iacovoni JS, Lacazette E, Prats AC, Touriol C, Prats H. Translational induction of VEGF internal ribosome entry site elements during the early response to ischemic stress. Circ Res 2007; 100:305–8. PMID:17255526. http://dx.doi.org/10.1161/01. RES.0000258873.08041.c9
22. Spriggs KA, Bushell M, Willis AE. Translational regulation of gene expression during conditions of cell stress. Mol Cell 2010; 40:228–37. PMID:20965418. http://dx.doi.org/10.1016/j.molcel.2010.09.028
23. Komar AA, Hatzoglou M. Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle 2011; 10:229–40. PMID:21220943. http://dx.doi.org/10.4161/cc.10.2.14472
24. Plank TD, Kieft JS. The structures of nonprotein-coding RNAs that drive internal ribosome entry site function. Wiley Interdiscip Rev RNA 2012; 3:195–212. PMID:22215521. http://dx.doi.org/10.1002/wrna.1105
25. Morris MJ, Negishi Y, Pazsint C, Schonhoft JD, Basu S. An RNA G-quadruplex is essential for cap-independent translation initiation in human VEGF IRES. J Am Chem Soc 2010; 132:17831–9. PMID:21105704. http://dx.doi.org/10.1021/ja106287x
26. Decorsiere A, Cayrel A, Vagner S, Millevoi S. Essential role for the interaction between hnRNP H/F and a G quadruplex in maintaining p53 pre-mRNA 3’-end processing and function during DNA damage. Genes Dev 2011; 25:220–5. PMID:21289067. http://dx.doi. org/10.1101/gad.607011
27. Koumenis C, Naczki C, Koritzinsky M, Rastani S, Diehl A, Sonenberg N, Koromilas A, Wouters BG. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol 2002; 22:7405–16. PMID:12370288. http://dx.doi.org/10.1128/MCB.22.21.7405-7416.2002
28. Blais JD, Addison CL, Edge R, Falls T, Zhao H, Wary K, Koumenis C, Harding HP, Ron D, Holcik M., et al. Perk-dependent translational regulation promotes tumor cell adaptation and angiogenesis in response to hypoxic stress. Mol Cell Biol 2006; 26:9517–32. PMID:17030613. http://dx.doi.org/10.1128/MCB.01145-06
29. Kroemer G, Marino G, Levine B. Autophagy and the integrated stress response. Mol Cell; 40:280–93. PMID:20965422. http://dx.doi.org/10.1016/j. molcel.2010.09.023
30. Sundquist WI, Klug A. Telomeric DNA dimerizes by formation of guanine tetrads between hairpin loops. Nature 1989; 342:825–9. PMID:2601741. http://dx.doi.org/10.1038/342825a0
31. Kochetov AV. Alternative translation start sites and hidden coding potential of eukaryotic mRNAs. Bioessays 2008; 30:683–91. PMID:18536038. http://dx.doi.org/10.1002/bies.20771
32. Sachs MS, Geballe AP. Downstream control of upstream open reading frames. Genes Dev 2006; 20:915–21. PMID:16618802. http://dx.doi.org/10.1101/gad.1427006
33. Bastide A, Karaa Z, Bornes S, Hieblot C, Lacazette E, Prats H, Touriol C. An upstream open reading frame within an IRES controls expression of a specific VEGFA isoform. Nucleic Acids Res 2008; 36:2434–45. PMID:18304943. http://dx.doi.org/10.1093/nar/gkn093
34. Huppert JL, Bugaut A, Kumari S, Balasubramanian S. G-quadruplexes: the beginning and end of UTRs. Nucleic Acids Res 2008; 36:6260–8. PMID:18832370. http://dx.doi.org/10.1093/nar/gkn511
35. Wu Y, Zan LP, Wang XD, Lu YJ, Ou TM, Lin J, Huang ZS, Gu LQ. Stabilization of VEGF G-quadruplex and inhibition of angiogenesis by quindoline derivatives. Biochim Biophys Acta 2014; 1840:2970–7. PMID:24931695. http://dx.doi.org/10.1016/j. bbagen.2014.06.002
36. Sun D, Liu WJ, Guo K, Rusche JJ, Ebbinghaus S, Gokhale V, Hurley LH. The proximal promoter region of the human vascular endothelial growth factor gene has a G-quadruplex structure that can be targeted by G-quadruplex-interactive agents. Mol Cancer Ther 2008; 7:880–9. PMID:18413801. http://dx.doi.org/10.1158/1535-7163.MCT-07-2119
37. Sun D, Guo K, Rusche JJ, Hurley LH. Facilitation of a structural transition in the polypurine/polypyrimidine tract within the proximal promoter region of the human VEGF gene by the presence of potassium and G-quadruplex-interactive agents. Nucleic Acids Res 2005; 33:6070–80. PMID:16239639. http://dx.doi. org/10.1093/nar/gki917
38. Salvati E, Zizza P, Rizzo A, Iachettini S, Cingolani C, D’Angelo C, Porru M, Randazzo A, Pagano B, Novellino E, et al. Evidence for G-quadruplex in the promoter of vegfr-2 and its targeting to inhibit tumor angiogenesis. Nucleic Acids Res 2014; 42:2945–57. PMID:24335081. http://dx.doi.org/10.1093/nar/gkt1289
39. Mitchell SA, Spriggs KA, Coldwell MJ, Jackson RJ, Willis AE. The Apaf-1 internal ribosome entry segment attains the correct structural conformation for function via interactions with PTB and unr. Mol Cell 2003; 11:757–71. PMID:12667457. http://dx.doi.org/10.1016/S1097-2765(03)00093-5
40. Pickering BM, Mitchell SA, Spriggs KA, Stoneley M, Willis AE. Bag-1 internal ribosome entry segment activity is promoted by structural changes mediated by poly(rC) binding protein 1 and recruitment of polypyrimidine tract binding protein 1. Mol Cell Biol 2004; 24:5595–605. PMID:15169918. http://dx.doi.org/10.1128/MCB.24.12.5595-5605.2004
41. Gonzalez V, Hurley LH. The C-terminus of nucleolin promotes the formation of the c-MYC G-quadruplex and inhibits c-MYC promoter activity. Biochemistry 2010; 49:9706–14. PMID:20932061. http://dx.doi. org/10.1021/bi100509s
42. Arimondo PB, Riou JF, Mergny JL, Tazi J, Sun JS, Garestier T, Helene C. Interaction of human DNA topoisomerase I with G-quartet structures. Nucleic Acids Res 2000; 28:4832–8. PMID:11121473. http://dx.doi.org/10.1093/nar/28.24.4832
43. Welsh SJ, Dale AG, Lombardo CM, Valentine H, de la Fuente M, Schatzlein A, Neidle S. Inhibition of the hypoxia-inducible factor pathway by a G-quadruplex binding small molecule. Sci Rep 2013; 3:2799. PMID:24165797. http://dx.doi.org/10.1038/srep02799
44. Karaa ZS, Iacovoni JS, Bastide A, Lacazette E, Touriol C, Prats H. The VEGF IRESes are differentially susceptible to translation inhibition by miR-16. RNA 2009; 15:249–54. PMID:19144909. http://dx.doi.org/10.1261/rna.1301109
45. Bornes S, Boulard M, Hieblot C, Zanibellato C, Iacovoni JS, Prats H, Touriol C. Control of the vascular endothelial growth factor internal ribosome entry site (IRES) activity and translation initiation by alternatively spliced coding sequences. J Biol Chem 2004; 279:18717–26. PMID:14764596. http://dx.doi.org/10.1074/jbc.M308410200
46. Creancier L, Mercier P, Prats AC, Morello D. c-myc Internal ribosome entry site activity is developmentally controlled and subjected to a strong translational repression in adult transgenic mice. Mol Cell Biol 2001; 21:1833–40. PMID:11238920. http://dx.doi. org/10.1128/MCB.21.5.1833-1840.2001