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 Research

Volumn 40, Issue 9, 2012, Pages 4137-4145

  Morris, Mark J ^a   Wingate, Katherine L ^a   Silwal, Jagannath ^a   Leeper, Thomas C ^b   Basu, Soumitra ^a  

^a KENT STATE UNIVERSITY   (United States)

^b UNIVERSITY OF AKRON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5,10,15,20 TETRA(N METHYL 4 PYRIDYL)PORPHYRIN; MATRIX METALLOPROTEINASE 16; MESSENGER RNA; PORPHYRIN DERIVATIVE; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; EUKARYOTIC CELL; GEL ELECTROPHORESIS; GENE CONSTRUCT; GENE REPRESSION; MOLECULAR INTERACTION; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REPORTER GENE; RNA FOLDING; RNA SEQUENCE; RNA STRUCTURE; STRUCTURE ACTIVITY RELATION; TRANSLATION INITIATION; TRANSLATION REGULATION; ULTRAVIOLET SPECTROSCOPY;

G-QUADRUPLEXES; GENES, REPORTER; HELA CELLS; HUMANS; MATRIX METALLOPROTEINASE 16; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PORPHYRINS; PROTEIN BIOSYNTHESIS; RNA, MESSENGER;

EUKARYOTA;

EID: 84861382319     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1308     Document Type: Article

References (57)

1. Egeblad, M. and Werb, Z. (2002) New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer, 2, 161-174. (Pubitemid 37328786)
2. McQuibban, G.A., Gong, J.H., Tam, E.M., McCulloch, C.A., Clark-Lewis, I. and Overall, C.M. (2000) Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science, 289, 1202-1206. (Pubitemid 30650734)
3. 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.
4. Neidle, S. and Balasubramanian, S. (2006) Quadruplex Nucleic Acids. Royal Society of Chemistry, Cambridge, UK.
5. Huppert, J.L. and Balasubramanian, S. (2005) Prevalence of quadruplexes in the human genome. Nucleic Acids Res., 33, 2908-2916. (Pubitemid 41511230)
6. Eddy, J. and Maizels, N. (2008) Conserved elements with potential to form polymorphic G-quadruplex structures in the first intron of human genes. Nucleic Acids Res., 36, 1321-1333. (Pubitemid 351330947)
7. Mani, P., Yadav, V.K., Das, S.K. and Chowdhury, S. (2009) Genome-wide analyses of recombination prone regions predict role of DNA structural motif in recombination. PLoS ONE, 4, e4399.
8. Todd, A.K., Johnston, M. and Neidle, S. (2005) Highly prevalent putative quadruplex sequence motifs in human DNA. Nucleic Acids Res., 33, 2901-2907. (Pubitemid 41511229)
9. Stephen, N. (2009) The structures of quadruplex nucleic acids and their drug complexes. Curr. Opin. Struct. Biol., 19, 239-250.
10. Siddiqui-Jain, A., Grand, C.L., Bearss, D.J. and Hurley, L.H. (2002) Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription. Proc. Natl Acad. Sci. USA, 99, 11593-11598. (Pubitemid 34994444)
11. Simonsson, T., Pecinka, P. and Kubista, M. (1998) DNA tetraplex formation in the control region of c-myc. Nucleic Acids Res., 26, 1167-1172. (Pubitemid 28291685)
12. Dexheimer, T.S., Sun, D. and Hurley, L.H. (2006) Deconvoluting the structural and drug-recognition complexity of the G-Quadruplex-forming region upstream of the bcl-2 P1 promoter. J. Am. Chem. Soc., 128, 5404-5415.
13. Cogoi, S. and Xodo, L.E. (2006) G-quadruplex formation within the promoter of the KRAS proto-oncogene and its effect on transcription. Nucleic Acids Res., 34, 2536-2549. (Pubitemid 43985618)
14. Sun, D., Guo, K., Rusche, J.J. and Hurley, L.H. (2005) 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., 33, 6070-6080. (Pubitemid 41742625)
15. Kostadinov, R., Malhotra, N., Viotti, M., Shine, R., D'Antonio, L. and Bagga, P. (2006) GRSDB: a database of quadruplex forming G-rich sequences in alternatively processed mammalian pre-mRNA sequences. Nucleic Acids Res., 34, D119-D124.
16. 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. (Pubitemid 46440536)
17. Sundquist, W.I. and Heaphy, S. (1993) Evidence for interstrand quadruplex formation in the dimerization of human immunodeficiency virus 1 genomic RNA. Proc. Natl Acad. Sci. USA, 90, 3393-3397. (Pubitemid 23111372)
18. Schaeffer, C., Bardoni, B., Mandel, J.L., Ehresmann, B., Ehresmann, C. and Moine, H. (2001) The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO J., 20, 4803-4813. (Pubitemid 32848632)
19. Bonnal, S., Schaeffer, C., Creancier, L., Clamens, S., Moine, H., Prats, A.-C. and Vagner, S. (2003) A single internal ribosome entry site containing a G quartet RNA structure drives fibroblast growth factor 2 gene expression at four alternative translation initiation codons. J. Biol. Chem., 278, 39330-39336. (Pubitemid 37248488)
20. 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. (Pubitemid 351872187)
21. Christiansen, J., Kofod, M. and Nielsen, F.C. (1994) A guanosine quadruplex and two stable hairpins flank a major cleavage site in insulin-like growth factor II mRNA. Nucleic Acids Res., 22, 5709-5716.
22. 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.
23. Gomez, D., Guedin, A., Mergny, J.-L., Salles, B., Riou, J.-F.o., Teulade-Fichou, M.-P. and Calsou, P. (2010) A G-quadruplex structure within the 5'-UTR of TRF2 mRNA represses translation in human cells. Nucleic Acids Res., 38, 7187-7198.
24. Wieland, M. and Hartig, J.S. (2007) RNA quadruplex-based modulation of gene expression. Chem. Biol., 14, 757-763. (Pubitemid 47081424)
25. Arora, A. and Maiti, S. (2009) Differential biophysical behavior of human telomeric RNA and DNA quadruplex. J. Phys. Chem. B, 113, 10515-10520.
26. Bugaut, A., Rodriguez, R., Kumari, S., Hsu, S.-T. and Balasubramanian, S. (2010) Small molecule-mediated inhibition of translation by targeting a native RNA G-quadruplex. Org. Biomol. Chem., 21, 2771-2776.
27. Collie, G., Reszka, A.P., Haider, S.M., Gabelica, V., Parkinson, G.N. and Neidle, S. (2009) Selectivity in small molecule binding to human telomeric RNA and DNA quadruplexes. Chem. Commun., 48, 7482-7484.
28. Halder, K., Largy, E., Benzler, M., Teulade-Fichou, M.-P. and Hartig, J.S. (2011) Efficient suppression of gene expression by targeting 50-UTR-Based RNA quadruplexes with bisquinolinium compounds. Chem. Bio. Chem., 12, 1663-1668.
29. Thomas, J.R. and Hergenrother, P.J. (2008) Targeting RNA with small molecules. Chem. Rev., 108, 1171-1224. (Pubitemid 351638813)
30. Monchaud, D. and Teulade-Fichou, M.-P. (2008) A hitchhiker's guide to G-quadruplex ligands. Org. Biomol. Chem., 6, 627-636. (Pubitemid 351972601)
31. de Armond, R., Wood, S., Sun, D., Hurley, L.H. and Ebbinghaus, S.W. (2005) Evidence for the presence of a Guanine quadruplex forming region within a polypurine tract of the Hypoxia Inducible Factor 1 alpha promoter. Biochemistry, 44, 16341-16350. (Pubitemid 41785833)
32. Guo, K., Pourpak, A., Beetz-Rogers, K., Gokhale, V., Sun, D. and Hurley, L.H. (2007) Formation of pseudosymmetrical G-quadruplex and i-motif structures in the proximal promoter region of the RET oncogene. J. Am. Chem. Soc., 129, 10220-10228. (Pubitemid 47312965)
33. Qin, Y., Rezler, E.M., Gokhale, V., Sun, D. and Hurley, L.H. (2007) Characterization of the G-quadruplexes in the duplex nuclease hypersensitive element of the PDGF-A promoter and modulation of PDGF-A promoter activity by TMPyP4. Nucleic Acids Res., 35, 7698-7713.
34. Sun, D., Liu, W.-J., Guo, K., Rusche, J.J., Ebbinghaus, S., Gokhale, V. and Hurley, L.H. (2008) 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., 7, 880-889. (Pubitemid 351551041)
35. Ren, J. and Chaires, J.B. (1999) Sequence and structural selectivity of nucleic acid binding ligands. Biochemistry, 38, 16067-16075. (Pubitemid 129520527)
36. Luedtke, N.W. (2009) Targeting G-quadruplex DNA with small molecules. CHIMIA, 63, 134-139.
37. Weisman-Shomer, P., Cohen, E., Hershco, I., Khateb, S., Wolfovitz-Barchad, O., Hurley, L.H. and Fry, M. (2003) The cationic porphyrin TMPyP4 destabilizes the tetraplex form of the fragile X syndrome expanded sequence d(CGG)n. Nucleic Acids Res., 31, 3963-3970. (Pubitemid 37442275)
38. Puglisi, J.D. and Tinoco, I. (1989) Methods in Enzymol, Vol. 180. Academic Press, pp. 304-325.
39. Pasternack, R.F., Huber, P.R., Boyd, P., Engasser, G., Francesconi, L., Gibbs, E., Fasella, P., Cerio Venturo, G. and Hinds, L.d. (1972) Aggregation of meso-substituted water-soluble porphyrins. J. Am. Chem. Soc., 94, 4511-4517.
40. Keating, L.R. and Szalai, V.A. (2004) Parallel-stranded guanine quadruplex interactions with a copper cationic porphyrin. Biochemistry, 43, 15891-15900. (Pubitemid 39665088)
41. Piotto, M., Saudek, V. and Sklenár, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR, 2, 661-665.
42. Dash, J., Shirude, P.S., Hsu, S.-T.D. and Balasubramanian, S. (2008) Diarylethynyl amides that recognize the parallel conformation of genomic promoter DNA G-quadruplexes. J. Am. Chem. Soc., 130, 15950-15956.
43. Waller, Z.A.E., Sewitz, S.A., Hsu, S.-T.D. and Balasubramanian, S. (2009) A small molecule that disrupts G-quadruplex DNA structure and enhances gene expression. J. Am. Chem. Soc., 131, 12628-12633.
44. Flynn, S., George, S., White, L., Devonish, W. and Takle, G. (1999) Water-soluble, meso-substituted cationic porphyrins- A family of compounds for cellular delivery of oligonucleotides. Biotechniques, 26, 736-742.
45. Ofer, N., Weisman-Shomer, P., Shklover, J. and Fry, M. (2009) 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., 37, 2712-2722.
46. Millet, O., Loria, J.P., Kroenke, C.D., Pons, M. and Palmer, A.G. (2000) The static magnetic field dependence of chemical exchange linebroadening defines the NMR chemical shift time scale. J. Am. Chem. Soc., 122, 2867-2877. (Pubitemid 30191047)
47. Fielding, L. (2003) NMR methods for the determination of protein-ligand dissociation constants. Curr. Top. Med. Chem., 3, 39-53.
48. Johnson, C.E. and Bovey, F.A. (1958) Calculation of nuclear magnetic resonance spectra of aromatic hydrocarbons. J. Chem. Phys., 29, 1012-1014.
49. Perkins, S.J. and Wüthrich, K. (1979) Ring current effects in the conformation dependent NMR chemical shifts of aliphatic protons in the basic pancreatic trypsin inhibitor. Biochim. Biophys. Acta., 576, 409-423.
50. Case, D.A. (1995) Calibration of ring-current effects in proteins and nucleic acids. J. Biomol. NMR, 6, 341-346.
51. Wheelhouse, R.T., Sun, D., Han, H., Han, F.X. and Hurley, L.H. (1998) Cationic porphyrins as telomerase inhibitors: the interaction of tetra-(N-methyl-4-pyridyl)porphine with quadruplex DNA. J. Am. Chem. Soc., 120, 3261-3262. (Pubitemid 28204540)
52. Yamashita, T., Uno, T. and Ishikawa, Y. (2005) Stabilization of guanine quadruplex DNA by the binding of porphyrins with cationic side arms. Bioorg. Med. Chem., 13, 2423-2430. (Pubitemid 40347256)
53. Iverson, B.L., Shreder, K., Král, V., Smith, D.A., Smith, J. and Sessler, J.L. (1994) Interactions between expanded porphyrins and nucleic acids. Pure Appl. Chem., 66, 845-850.
54. Ghazaryan, A.A., Dalyan, Y.B., Haroutiunian, S.G., Tikhomirova, A., Taulier, N., Wells, J.W. and Chalikian, T.V. (2006) Thermodynamics of interactions of water-soluble porphyrins with RNA duplexes. J. Am. Chem. Soc., 128, 1914-1921. (Pubitemid 43277332)
55. Parkinson, G.N., Ghosh, R. and Neidle, S. (2007) Structural basis for binding of porphyrin to human telomeres. Biochemistry, 46, 2390-2397. (Pubitemid 46362413)
56. Shkirman, S., Solov'ev, K., Kachura, T., Arabei, S. and Skakovskii, E. (1999) Interpretation of the soret band of porphyrins based on the polarization spectrum of N-methyltetraphenylporphin fluorescence. J. Appl. Spectros., 66, 68-75.
57. Fernando, H., Reszka, A.P., Huppert, J., Ladame, S., Rankin, S., Venkitaraman, A.R., Neidle, S. and Balasubramanian, S. (2006) A Conserved quadruplex motif located in a transcription activation site of the human c-kit oncogene. Biochemistry, 45, 7854-7860. (Pubitemid 44185502)