Quadruplex formation is necessary for stable PNA invasion into duplex DNA of BCL2 promoter region

Nucleic Acids Research

Volumn 39, Issue 16, 2011, Pages 7114-7123

  Onyshchenko, Mykola I ^a   Gaynutdinov, Timur I ^b   Englund, Ethan A ^c   Appella, Daniel H ^c   Neumann, Ronald D ^b   Panyutin, Igor G ^b  

^a NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

^b Clinical Center   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; AMPHOLYTE; DIMETHYL SULFATE; DOUBLE STRANDED DNA; GLUTAMIC ACID; LYSINE; PEPTIDE NUCLEIC ACID; PROTEIN BCL 2; THYMINE;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; DNA PROBE; DNA PROTEIN COMPLEX; DNA SEQUENCE; GC RICH SEQUENCE; GENE TARGETING; HUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN STRUCTURE;

DNA; G-QUADRUPLEXES; HUMANS; PEPTIDE NUCLEIC ACIDS; PLASMIDS; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 80052463968     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr259     Document Type: Article

References (54)

1. 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.
2. Qin, Y. and Hurley, L.H. (2008) Structures, folding patterns, and functions of intramolecular DNA G-quadruplexes found in eukaryotic promoter regions. Biochimie, 90, 1149-1171.
3. 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)
4. Guo, K., Gokhale, V., Hurley, L.H. and Sun, D. (2008) Intramolecularly folded G-quadruplex and i-motif structures in the proximal promoter of the vascular endothelial growth factor gene. Nucleic Acids Res., 36, 4598-4608.
5. 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)
6. Cogoi, S., Paramasivam, M., Spolaore, B. and Xodo, L.E. (2008) Structural polymorphism within a regulatory element of the human KRAS promoter: formation of G4-DNA recognized by nuclear proteins. Nucleic Acids Res., 36, 3765-3780. (Pubitemid 351917538)
7. Rankin, S., Reszka, A.P., Huppert, J., Zloh, M., Parkinson, G.N., Todd, A.K., Ladame, S., Balasubramanian, S. and Neidle, S. (2005) Putative DNA quadruplex formation within the human c-kit oncogene. J. Am. Chem. Soc., 127, 10584-10589. (Pubitemid 41061432)
8. Hsu, S.T., Varnai, P., Bugaut, A., Reszka, A.P., Neidle, S. and Balasubramanian, S. (2009) A G-rich sequence within the c-kit oncogene promoter forms a parallel G-quadruplex having asymmetric G-tetrad dynamics. J. Am. Chem. Soc., 131, 13399-13409.
9. 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.
10. Dai, J., Chen, D., Jones, R.A., Hurley, L.H. and Yang, D. (2006) NMR solution structure of the major G-quadruplex structure formed in the human BCL2 promoter region. Nucleic Acids Res., 34, 5133-5144. (Pubitemid 44742478)
11. Palumbo, S.L., Ebbinghaus, S.W. and Hurley, L.H. (2009) Formation of a unique end-to-end stacked pair of G-quadruplexes in the hTERT core promoter with implications for inhibition of telomerase by G-quadruplex-interactive ligands. J. Am. Chem. Soc., 131, 10878-10891.
12. Xu, Y. and Sugiyama, H. (2006) Formation of the G-quadruplex and i-motif structures in retinoblastoma susceptibility genes (Rb). Nucleic Acids Res., 34, 949-954. (Pubitemid 43380678)
13. Qin, Y., Fortin, J.S., Tye, D., Gleason-Guzman, M., Brooks, T.A. and Hurley, L.H. Molecular cloning of the human platelet-derived growth factor receptor beta (PDGFR-beta) promoter and drug targeting of the G-quadruplex-forming region to repress PDGFR-beta expression. Biochemistry, 49, 4208-4219.
14. Sun, D. and Hurley, L.H. (2009) The importance of negative superhelicity in inducing the formation of G-quadruplex and i-motif structures in the c-Myc promoter: implications for drug targeting and control of gene expression. J. Med. Chem., 52, 2863-2874.
15. Sun, S., Chen, J., Li, W., Altintas, I., Lin, A., Peltier, S., Stocks, K., Allen, E.E., Ellisman, M., Grethe, J. et al. Community cyberinfrastructure for advanced microbial ecology research and analysis: the CAMERA resource. Nucleic Acids Res., 39, D546-551.
16. Hanvey, J.C., Klysik, J. and Wells, R.D. (1988) Influence of DNA sequence on the formation of non-B right-handed helices in oligopurine.oligopyrimidine inserts in plasmids. J. Biol. Chem., 263, 7386-7396.
17. Panyutin, I.G. and Wells, R.D. (1992) Nodule DNA in the (GA)37.(CT)37 insert in superhelical plasmids. J. Biol. Chem., 267, 5495-5501.
18. Young, R.L. and Korsmeyer, S.J. (1993) A negative regulatory element in the bcl-2 50-untranslated region inhibits expression from an upstream promoter. Mol. Cell. Biol., 13, 3686-3697. (Pubitemid 23157305)
19. Seto, M., Jaeger, U., Hockett, R.D., Graninger, W., Bennett, S., Goldman, P. and Korsmeyer, S.J. (1988) Alternative promoters and exons, somatic mutation and deregulation of the Bcl-2-Ig fusion gene in lymphoma. EMBO J., 7, 123-131.
20. Heckman, C., Mochon, E., Arcinas, M. and Boxer, L.M. (1997) The WT1 protein is a negative regulator of the normal bcl-2 allele in t(14;18) lymphomas. J. Biol. Chem., 272, 19609-19614. (Pubitemid 27337765)
21. Gomez-Manzano, C., Mitlianga, P., Fueyo, J., Lee, H.Y., Hu, M., Spurgers, K.B., Glass, T.L., Koul, D., Liu, T.J., McDonnell, T.J. et al. (2001) Transfer of E2F-1 to human glioma cells results in transcriptional up-regulation of Bcl-2. Cancer Res., 61, 6693-6697. (Pubitemid 32896488)
22. Onyshchenko, M.I., Gaynutdinov, T.I., Englund, E.A., Appella, D.H., Neumann, R.D. and Panyutin, I.G. (2009) Stabilization of G-quadruplex in the BCL2 promoter region in double-stranded DNA by invading short PNAs. Nucleic Acids Res., 37, 7570-7580.
23. Sabo, P.J., Kuehn, M.S., Thurman, R., Johnson, B.E., Johnson, E.M., Cao, H., Yu, M., Rosenzweig, E., Goldy, J., Haydock, A. et al. (2006) Genome-scale mapping of DNase I sensitivity in vivo using tiling DNA microarrays. Nat. Methods, 3, 511-518. (Pubitemid 43941768)
24. Sabo, P.J., Hawrylycz, M., Wallace, J.C., Humbert, R., Yu, M., Shafer, A., Kawamoto, J., Hall, R., Mack, J., Dorschner, M.O. et al. (2004) Discovery of functional noncoding elements by digital analysis of chromatin structure. Proc. Natl Acad. Sci. USA, 101, 16837-16842. (Pubitemid 39601325)
25. Celniker, S.E., Dillon, L.A., Gerstein, M.B., Gunsalus, K.C., Henikoff, S., Karpen, G.H., Kellis, M., Lai, E.C., Lieb, J.D., MacAlpine, D.M. et al. (2009) Unlocking the secrets of the genome. Nature, 459, 927-930.
26. Liu, Y.Z., Boxer, L.M. and Latchman, D.S. (1999) Activation of the Bcl-2 promoter by nerve growth factor is mediated by the p42/p44 MAPK cascade. Nucleic Acids Res., 27, 2086-2090. (Pubitemid 29219236)
27. Nielsen, P.E., Egholm, M., Berg, R.H. and Buchardt, O. (1991) Sequence-selective recognition of DNA by strand displacement with a thymine-substituted polyamide. Science, 254, 1497-1500. (Pubitemid 21917487)
28. Larsen, H.J., Bentin, T. and Nielsen, P.E. (1999) Antisense properties of peptide nucleic acid. Biochim. Biophys. Acta., 1489, 159-166.
29. Nielsen, P.E. and Christensen, L. (1996) Strand displacement binding of a duplex-forming homopurine PNA to a homopyrimidine duplex DNA target. J. Am. Chem. Soc., 118, 2287-2288. (Pubitemid 26106360)
30. Zhang, X., Ishihara, T. and Corey, D.R. (2000) Strand invasion by mixed base PNAs and a PNA-peptide chimera. Nucleic Acids Res., 28, 3332-3338. (Pubitemid 30662298)
31. Bukanov, N.O., Demidov, V.V., Nielsen, P.E. and Frank-Kamenetskii, M.D. (1998) PD-loop: a complex of duplex DNA with an oligonucleotide. Proc. Natl Acad. Sci. USA, 95, 5516-5520.
32. He, Y., Neumann, R.D. and Panyutin, I.G. (2004) Intramolecular quadruplex conformation of human telomeric DNA assessed with 125I-radioprobing. Nucleic Acids Res., 32, 5359-5367. (Pubitemid 39545653)
33. Englund, E.A. and Appella, D.H. (2007) Gamma-substituted peptide nucleic acids constructed from L-lysine are a versatile scaffold for multifunctional display. Angew. Chem. Int. Edn Engl., 46, 1414-1418. (Pubitemid 46964362)
34. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, NY.
35. Maxam, A.M. and Gilbert, W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol., 65, 499-560.
36. Panyutin, I.G., Panyutin, I.V. and Demidov, V.V. (2007) Targeting linear duplex DNA with mixed-base peptide nucleic acid oligomers facilitated by bisPNA openers. Anal. Biochem., 362, 145-147. (Pubitemid 46198794)
37. Dizdaroglu, M., Holwitt, E., Hagan, M.P. and Blakely, W.F. (1986) Formation of cytosine glycol and 5, 6-dihydroxycytosine in deoxyribonucleic acid on treatment with osmium tetroxide. Biochem. J., 235, 531-536. (Pubitemid 16052197)
38. Shen, C., Rattat, D., Buck, A., Mehrke, G., Polat, B., Ribbert, H., Schirrmeister, H., Mahren, B., Matuschek, C. and Reske, S.N. (2003) Targeting bcl-2 by triplex-forming oligonucleotide-a promising carrier for gene-radiotherapy. Cancer Biother. Radiopharm., 18, 17-26. (Pubitemid 36307463)
39. Klasa, R.J., Gillum, A.M., Klem, R.E. and Frankel, S.R. (2002) Oblimersen Bcl-2 antisense: facilitating apoptosis in anticancer treatment. Antisense Nucleic Acid Drug Dev., 12, 193-213. (Pubitemid 34815931)
40. Oltersdorf, T., Elmore, S.W., Shoemaker, A.R., Armstrong, R.C., Augeri, D.J., Belli, B.A., Bruncko, M., Deckwerth, T.L., Dinges, J., Hajduk, P.J. et al. (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature, 435, 677-681. (Pubitemid 40825512)
41. Cutrona, G., Carpaneto, E.M., Ulivi, M., Roncella, S., Landt, O., Ferrarini, M. and Boffa, L.C. (2000) Effects in live cells of a c-myc anti-gene PNA linked to a nuclear localization signal. Nature Biotechnol., 18, 300-303. (Pubitemid 30159481)
42. Boffa, L.C., Scarfi, S., Mariani, M.R., Damonte, G., Allfrey, V.G., Benatti, U. and Morris, P.L. (2000) Dihydrotestosterone as a selective cellular/nuclear localization vector for anti-gene peptide nucleic acid in prostatic carcinoma cells. Cancer Res., 60, 2258-2262. (Pubitemid 30225192)
43. Cutrona, G., Carpaneto, E.M., Ponzanelli, A., Ulivi, M., Millo, E., Scarfi, S., Roncella, S., Benatti, U., Boffa, L.C. and Ferrarini, M. (2003) Inhibition of the translocated c-myc in Burkitt's lymphoma by a PNA complementary to the E mu enhancer. Cancer Res., 63, 6144-6148. (Pubitemid 37255153)
44. Cogoi, S., Codognotto, A., Rapozzi, V., Meeuwenoord, N., van der Marel, G. and Xodo, L.E. (2005) Transcription inhibition of oncogenic KRAS by a mutation-selective peptide nucleic acid conjugated to the PKKKRKV nuclear localization signal peptide. Biochemistry, 44, 10510-10519. (Pubitemid 41098228)
45. Halder, R., Halder, K., Sharma, P., Garg, G., Sengupta, S. and Chowdhury, S. (2010) Guanine quadruplex DNA structure restricts methylation of CpG dinucleotides genome-wide. Mol. BioSyst., 6, 2439-2447.
46. Gonzalez, V. and Hurley, L.H. The c-MYC NHE III(1): function and regulation. Ann. Rev. Pharmacol. Toxicol., 50, 111-129.
47. Brooks, T.A., Kendrick, S. and Hurley, L. Making sense of G-quadruplex and i-motif functions in oncogene promoters. FEBS J., 277, 3459-3469.
48. Strauss, J. and Reyes-Dominguez, Y. (2011) Regulation of secondary metabolism by chromatin structure and epigenetic codes. Fungal Genet. Biol, 48, 62-69.
49. 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)
50. Lundin, K.E., Ge, R., Svahn, M.G., Tornquist, E., Leijon, M., Branden, L.J. and Smith, C.I. (2004) Cooperative strand invasion of supercoiled plasmid DNA by mixed linear PNA and PNA-peptide chimeras. Biomol. Eng., 21, 51-59. (Pubitemid 38534481)
51. Nielsen, P.E. (2001) Peptide nucleic acid targeting of double-stranded DNA. Methods Enzymol., 340, 329-340. (Pubitemid 32751707)
52. Amiard, S., Doudeau, M., Pinte, S., Poulet, A., Lenain, C., Faivre-Moskalenko, C., Angelov, D., Hug, N., Vindigni, A., Bouvet, P. et al. (2007) A topological mechanism for TRF2-enhanced strand invasion. Nature Struct. Mol. Biol., 14, 147-154.
53. Duquette, M.L., Handa, P., Vincent, J.A., Taylor, A.F. and Maizels, N. (2004) Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev., 18, 1618-1629. (Pubitemid 38868912)
54. Belotserkovskii, B.P., Liu, R. and Hanawalt, P.C. (2009) Peptide nucleic acid (PNA) binding and its effect on in vitro transcription in friedreich's ataxia triplet repeats. Mol. Carcinogen., 48, 299-308.