The RNA Stem-Loop to G-Quadruplex Equilibrium Controls Mature MicroRNA Production inside the Cell

Biochemistry

Volumn 54, Issue 48, 2015, Pages 7067-7078

  Pandey, Satyaprakash ^a,b   Agarwala, Prachi ^a,b   Jayaraj, Gopal G ^a,b   Gargallo, Raimundo ^d   Maiti, Souvik ^a,b,c  

^a CSIR INSTITUTE OF GENOMICS AND INTEGRATIVE BIOLOGY   (India)

^b NATIONAL CHEMICAL LABORATORY   (India)

^c ACADEMY OF SCIENTIFIC AND INNOVATIVE RESEARCH ACSIR   (India)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DNA SEQUENCES;

BIOLOGICAL PROCESS; COMBINED ANALYSIS; G-QUADRUPLEXES; GC-RICH SEQUENCES; IN-VITRO ANALYSIS; MODEL SYSTEM; STEM-LOOP STRUCTURES; STRUCTURAL SHIFTS;

RNA;

DICER; GUANINE QUADRUPLEX; MAGNESIUM; MICRORNA; POTASSIUM; MIRN27 MICRORNA, HUMAN; MIRNLET7 MICRORNA, HUMAN; RIBONUCLEASE III; RIBONUCLEASE T1;

ARTICLE; BIOGENESIS; CONTROLLED STUDY; IN VITRO STUDY; MCF 7 CELL LINE; MOLECULAR BEACON; PRIORITY JOURNAL; PROTEIN STABILITY; RNA CLEAVAGE; RNA STRUCTURE; RNA TRANSCRIPTION; CHEMISTRY; CONFORMATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

BASE SEQUENCE; G-QUADRUPLEXES; GENE EXPRESSION REGULATION; HUMANS; MCF-7 CELLS; MICRORNAS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RIBONUCLEASE III; RIBONUCLEASE T1; TRANSCRIPTION, GENETIC;

EID: 84948947294     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00574     Document Type: Article

References (49)

1. Burge, S., Parkinson, G. N., Hazel, P., Todd, A. K., and Neidle, S. (2006) Quadruplex DNA: sequence, topology and structure Nucleic Acids Res. 34, 5402-5415 10.1093/nar/gkl655
2. Huppert, J. L. and Balasubramanian, S. (2006) G-quadruplexes in promoters throughout the human genome Nucleic Acids Res. 35, 406-413 10.1093/nar/gkl1057
3. Huppert, J. L., Bugaut, A., Kumari, S., and Balasubramanian, S. (2008) G-quadruplexes: the beginning and end of UTRs Nucleic Acids Res. 36, 6260-6268 10.1093/nar/gkn511
4. Kumari, S., Bugaut, A., and Balasubramanian, S. (2008) 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 47, 12664-12669 10.1021/bi8010797
5. Zhang, A. Y., Bugaut, A., and Balasubramanian, S. (2011) A sequence-independent analysis of the loop length dependence of intramolecular RNA G-quadruplex stability and topology Biochemistry 50, 7251-7258 10.1021/bi200805j
6. Bugaut, A., Murat, P., and Balasubramanian, S. (2012) An RNA hairpin to G-quadruplex conformational transition J. Am. Chem. Soc. 134, 19953-19956 10.1021/ja308665g
7. Pandey, S., Agarwala, P., and Maiti, S. (2013) Effect of loops and G-quartets on the stability of RNA G-quadruplexes J. Phys. Chem. B 117, 6896-6905 10.1021/jp401739m
8. Jodoin, R., Bauer, L., Garant, J. M., Mahdi Laaref, A., Phaneuf, F., and Perreault, J. P. (2014) The folding of 5′-UTR human G-quadruplexes possessing a long central loop RNA 20, 1129-1141 10.1261/rna.044578.114
9. Arora, A., Dutkiewicz, M., Scaria, V., Hariharan, M., Maiti, S., and Kurreck, J. (2008) Inhibition of translation in living eukaryotic cells by an RNA G-quadruplex motif RNA 14, 1290-1296 10.1261/rna.1001708
10. Kumari, S., Bugaut, A., Huppert, J. L., and Balasubramanian, S. (2007) An RNA G-quadruplex in the 5′ UTR of the NRAS proto-oncogene modulates translation Nat. Chem. Biol. 3, 218-221 10.1038/nchembio864
11. Morris, M. J. and Basu, S. (2009) An unusually stable G-quadruplex within the 5′-UTR of the MT3 matrix metalloproteinase mRNA represses translation in eukaryotic cells Biochemistry 48, 5313-5319 10.1021/bi900498z
12. Morris, M. J., Negishi, Y., Pazsint, C., Schonhoft, J. D., and Basu, S. (2010) An RNA G-quadruplex is essential for cap-independent translation initiation in human VEGF IRES J. Am. Chem. Soc. 132, 17831-17839 10.1021/ja106287x
13. Collie, G. W., Haider, S. M., Neidle, S., and Parkinson, G. N. (2010) A crystallographic and modelling study of a human telomeric RNA (TERRA) quadruplex Nucleic Acids Res. 38, 5569-5580 10.1093/nar/gkq259
14. Subramanian, M., Rage, F., Tabet, R., Flatter, E., Mandel, J. L., and Moine, H. (2011) G-quadruplex RNA structure as a signal for neurite mRNA targeting EMBO Rep. 12, 697-704 10.1038/embor.2011.76
15. Fisette, J. F., Montagna, D. R., Mihailescu, M. R., and Wolfe, M. S. (2012) A G-rich element forms a G-quadruplex and regulates BACE1 mRNA alternative splicing J. Neurochem. 121, 763-773 10.1111/j.1471-4159.2012.07680.x
16. Biffi, G., Tannahill, D., McCafferty, J., and Balasubramanian, S. (2013) Quantitative visualization of DNA G-quadruplex structures in human cells Nat. Chem. 5, 182-186 10.1038/nchem.1548
17. Biffi, G., Di Antonio, M., Tannahill, D., and Balasubramanian, S. (2013) Visualization and selective chemical targeting of RNA G-quadruplex structures in the cytoplasm of human cells Nat. Chem. 6, 75-80 10.1038/nchem.1805
18. Gros, J., Guedin, A., Mergny, J. L., and Lacroix, L. (2008) G-Quadruplex formation interferes with P1 helix formation in the RNA component of telomerase hTERC ChemBioChem 9, 2075-2079 10.1002/cbic.200800300
19. Wan, Y., Kertesz, M., Spitale, R. C., Segal, E., and Chang, H. Y. (2011) Understanding the transcriptome through RNA structure Nat. Rev. Genet. 12, 641-655 10.1038/nrg3049
20. Jayaraj, G. G., Pandey, S., Scaria, V., and Maiti, S. (2012) Potential G-quadruplexes in the human long non-coding transcriptome RNA Biol. 9, 81-86 10.4161/rna.9.1.18047
21. Bartel, D. P. (2009) MicroRNAs: target recognition and regulatory functions Cell 136, 215-233 10.1016/j.cell.2009.01.002
22. Soifer, H. S., Rossi, J. J., and Saetrom, P. (2007) MicroRNAs in disease and potential therapeutic applications Mol. Ther. 15, 2070-2079 10.1038/sj.mt.6300311
23. Lujambio, A. and Lowe, S. W. (2012) The microcosmos of cancer Nature 482, 347-355 10.1038/nature10888
24. Mendell, J. T. and Olson, E. N. (2012) MicroRNAs in stress signaling and human disease Cell 148, 1172-1187 10.1016/j.cell.2012.02.005
25. Zampetaki, A. and Mayr, M. (2012) MicroRNAs in vascular and metabolic disease Circ. Res. 110, 508-522 10.1161/CIRCRESAHA.111.247445
26. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., and Kim, S. et al. 2003, The nuclear RNase III Drosha initiates microRNA processing Nature 425, 415-419 10.1038/nature01957
27. Kim, V. N., Han, J., and Siomi, M. C. (2009) Biogenesis of small RNAs in animals. Nature reviews Nat. Rev. Mol. Cell Biol. 10, 126-139 10.1038/nrm2632
28. Young, D. D., Connelly, C. M., Grohmann, C., and Deiters, A. (2010) Small molecule modifiers of microRNA miR-122 function for the treatment of hepatitis C virus infection and hepatocellular carcinoma J. Am. Chem. Soc. 132, 7976-7981 10.1021/ja910275u
29. Deiters, A. (2010) Small molecule modifiers of the microRNA and RNA interference pathway AAPS J. 12, 51-60 10.1208/s12248-009-9159-3
30. Bose, D., Jayaraj, G., Suryawanshi, H., Agarwala, P., Pore, S. K., Banerjee, R., and Maiti, S. (2012) The tuberculosis drug streptomycin as a potential cancer therapeutic: inhibition of miR-21 function by directly targeting its precursor Angew. Chem., Int. Ed. 51, 1019-1023 10.1002/anie.201106455
31. Mirihana Arachchilage, G., Dassanayake, A. C., and Basu, S. (2015) A Potassium Ion-Dependent RNA Structural Switch Regulates Human Pre-miRNA 92b Maturation Chem. Biol. 22, 262-272 10.1016/j.chembiol.2014.12.013
32. Jaumot, J., Gargallo, R., de Juan, A., and Tauler, R. (2005) A graphical user-firendly interface of mCR-ALS; a new tool for multivariate curve resolution in MATLAB Chemom. Intell. Lab. Syst. 76, 101-110 10.1016/j.chemolab.2004.12.007
33. Kumar, P., Verma, A., Maiti, S., Gargallo, R., and Chowdhury, S. (2005) Tetraplex DNA transitions within the human c-myc promoter detected by multivariate curve resolution of fluorescence resonance energy transfer Biochemistry 44, 16426-16434 10.1021/bi051452x
34. Jaumot, J., Eritja, R., Tauler, R., and Gargallo, R. (2006) Resolution of a structural competition involving dimeric G-quadruplex and its C-rich complementary strand Nucleic Acids Res. 34, 206-216 10.1093/nar/gkj421
35. Jaumot, J., Tauler, R., and Gargallo, R. (2006) Exploratory data analysis of DNA microarrays by multivariate curve resolution Anal. Biochem. 358, 76-89 10.1016/j.ab.2006.07.028
36. Felten, J., Hall, H., Jaumot, J., Tauler, R., de Juan, A., and Gorzsas, A. (2015) Vibrational spectroscopic image analysis of biological material using multivariate curve resolution-alternating least squares (MCR-ALS) Nat. Protoc. 10, 217-240 10.1038/nprot.2015.008
37. de Oliveira, R. R., de Lima, K. M., Tauler, R., and de Juan, A. (2014) Application of correlation constrained multivariate curve resolution alternating least-squares methods for determination of compounds of interest in biodiesel blends using NIR and UV-visible spectroscopic data Talanta 125, 233-241 10.1016/j.talanta.2014.02.073
38. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res. 29, e45 10.1093/nar/29.9.e45
39. Bose, D., Jayaraj, G. G., Kumar, S., and Maiti, S. (2013) A molecular-beacon-based screen for small molecule inhibitors of miRNA maturation ACS Chem. Biol. 8, 930-938 10.1021/cb300650y
40. Provost, P., Dishart, D., Doucet, J., Frendewey, D., Samuelsson, B., and Radmark, O. (2002) Ribonuclease activity and RNA binding of recombinant human Dicer Embo. J. 21, 5864-5874 10.1093/emboj/cdf578
41. Kypr, J., Kejnovska, I., Renciuk, D., and Vorlickova, M. (2009) Circular dichroism and conformational polymorphism of DNA Nucleic Acids Res. 37, 1713-1725 10.1093/nar/gkp026
42. Jaumot, J., Escaja, N., Gargallo, R., Gonzalez, C., Pedroso, E., and Tauler, R. (2002) Multivariate curve resolution: a powerful tool for the analysis of conformational transitions in nucleic acids Nucleic Acids Res. 30, e92 10.1093/nar/gnf091
43. Kumar, N. and Maiti, S. (2008) Role of molecular crowding in perturbing quadruplex-Watson Crick duplex equilibrium Nucleic Acids Symp. Ser. (Oxf) 52, 157-158 10.1093/nass/nrn080
44. Scaria, V., Hariharan, M., Arora, A., and Maiti, S. (2006) Quadfinder: server for identification and analysis of quadruplex-forming motifs in nucleotide sequences Nucleic Acids Res. 34, W683-685 10.1093/nar/gkl299
45. Kozomara, A. and Griffiths-Jones, S. (2014) miRBase: annotating high confidence microRNAs using deep sequencing data Nucleic Acids Res. 42, D68-73 10.1093/nar/gkt1181
46. Jerome, T., Laurie, P., Louis, B., and Pierre, C. (2007) Enjoy the Silence: The Story of let-7 MicroRNA and Cancer Curr. Genomics 8, 229-233 10.2174/138920207781386933
47. Kumar, M., Ahmad, T., Sharma, A., Mabalirajan, U., Kulshreshtha, A., Agrawal, A., and Ghosh, B. (2011) Let-7 microRNA-mediated regulation of IL-13 and allergic airway inflammation J. Allergy Clin. Immunol. 128, 1077-1085 10.1016/j.jaci.2011.04.034
48. Morris, M. J., Wingate, K. L., Silwal, J., Leeper, T. C., and Basu, S. (2012) The porphyrin TmPyP4 unfolds the extremely stable G-quadruplex in MT3-MMP mRNA and alleviates its repressive effect to enhance translation in eukaryotic cells Nucleic Acids Res. 40, 4137-4145 10.1093/nar/gkr1308
49. Zamiri, B., Reddy, K., Macgregor, R. B., Jr., and Pearson, C. E. (2014) TMPyP4 porphyrin distorts RNA G-quadruplex structures of the disease-associated r(GGGGCC)n repeat of the C9orf72 gene and blocks interaction of RNA-binding proteins J. Biol. Chem. 289, 4653-4659 10.1074/jbc.C113.502336