Stabilization of G-quadruplex in the BCL2 promoter region in double-stranded DNA by invading short PNAs

Nucleic Acids Research

Volumn 37, Issue 22, 2009, Pages 7570-7580

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

^a CLINICAL CENTER   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; GUANINE; GUANINE QUADRUPLEX; OLIGOMER; PEPTIDE NUCLEIC ACID; PLASMID DNA; PROTEIN BCL 2; SINGLE STRANDED DNA; THYMINE DERIVATIVE;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; DNA BINDING; DNA CONFORMATION; DNA DENATURATION; DNA FOOTPRINTING; DNA MODIFICATION; DNA PROBE; DNA SEQUENCE; DRUG SCREENING; GC RICH SEQUENCE; GENE TARGETING; GENETIC STABILITY; HUMAN; IN VITRO STUDY; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROMOTER REGION; UPREGULATION;

CIRCULAR DICHROISM; DNA; DNA FOOTPRINTING; G-QUADRUPLEXES; GENES, BCL-2; HUMANS; NUCLEIC ACID DENATURATION; PEPTIDE NUCLEIC ACIDS; PLASMIDS; PROMOTER REGIONS, GENETIC;

EID: 75649151162     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp840     Document Type: Article

References (59)

1. Akagi, T., Kondo, E. and Yoshino, T. (1994) Expression of Bcl-2 protein and Bcl-2 mRNA in normal and neoplastic lymphoid tissues. Leuk. Lymphoma, 13, 81-87.
2. Joensuu, H., Pylkkanen, L. and Toikkanen, S. (1994) Bcl-2 protein expression and long-term survival in breast cancer. Am. J. Pathol, 145, 1191-1198.
3. Tjalma, W., De Cuyper, E., Weyler, J., Van Marck, E., De Pooter, C., Albertyn, G. and van Dam, P. (1998) Expression of bcl-2 in invasive and in situ carcinoma of the uterine cervix. Am. J. Obstet. Gynecol., 178, 113-117.
4. Pezzella, F., Turley, H., Kuzu, I., Tungekar, M.F., Dunnill, M.S., Pierce, C.B., Harris, A., Gatter, K.C. and Mason, D.Y. (1993) bcl-2 protein in non-small-cell lung carcinoma. N. Engl. J. Med., 329, 690-694.
5. McDonnell, T.J., Troncoso, P., Brisbay, S.M., Logothetis, C., Chung, L.W., Hsieh, J.T., Tu, S.M. and Campbell, M.L. (1992) Expression of the protooncogene bcl-2 in the prostate and its association with emergence of androgen-independent prostate cancer. Cancer Res., 52, 6940-6944.
6. Chao, D.T. and Korsmeyer, S.J. (1998) BCL-2 family: regulators of cell death. Annu. Rev. Immunol., 16, 395-419.
7. Kuhlmann, T., Lucchinetti, C., Zettl, U.K., Bitsch, A., Lassmann, H. and Bruck, W. (1999) Bcl-2-expressing oligodendrocytes in multiple sclerosis lesions. Glia, 28, 34-39.
8. Satou, T., Cummings, B.J. and Cotman, C.W. (1995) Immunoreactivity for Bcl-2 protein within neurons in the Alzheimer's disease brain increases with disease severity. Brain Res., 697, 35-43.
9. Marshall, K.A., Daniel, S.E., Cairns, N., Jenner, P. and Halliwell, B. (1997) Upregulation of the anti-apoptotic protein Bcl-2 may be an early event in neurodegeneration: studies on Parkinson's and incidental Lewy body disease. Biochem. Biophys. Res. Commun., 240, 84-87.
10. DeVries, A.C., Joh, H.D., Bernard, O., Hattori, K., Hurn, P.D., Traystman, R.J. and Alkayed, N.J. (2001) Social stress exacerbates stroke outcome by suppressing Bcl-2 expression. Proc. Natl Acad. Sci. USA, 98, 11824-11828.
11. Seki, T., Hida, K., Tada, M., Koyanagi, I. and Iwasaki, Y. (2003) Role of the bcl-2 gene after contusive spinal cord injury in mice. Neurosurgery, 53, 192-198, Discussion 198.
12. Young, R.L. and Korsmeyer, S.J. (1993) A negative regulatory element in the bcl-2 5′-untranslated region inhibits expression from an upstream promoter. Mol. Cell Biol., 13, 3686-3697.
13. Bredow, S., Juri, D.E., Cardon, K. and Tesfaigzi, Y. (2007) Identification of a novel Bcl-2 promoter region that counteracts in a p53-dependent manner the inhibitory P2 region. Gene, 404, 110-116.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. Huppert, J.L. and Balasubramanian, S. (2007) G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res., 35, 406-413.
20. 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.
21. 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.
22. 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.
23. 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.
24. 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.
25. 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.
26. Rich, A., Nordheim, A. and Wang, A.H. (1984) The chemistry and biology of left-handed Z-DNA. Annu. Rev. Biochem., 53, 791-846.
27. Frank-Kamenetskii, M.D. and Mirkin, S.M. (1995) Triplex DNA structures. Annu. Rev. Biochem., 64, 65-95.
28. 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.
29. 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.
30. Larsen, H.J., Bentin, T. and Nielsen, P.E. (1999) Antisense properties of peptide nucleic acid. Biochim. Biophys. Acta, 1489, 159-166.
31. 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.
32. 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.
33. 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.
34. Green, J.J., Ying, L., Klenerman, D. and Balasubramanian, S. (2003) Kinetics of unfolding the human telomeric DNA quadruplex using a PNA trap. J. Am. Chem. Soc., 125, 3763-3767.
35. Roy, S., Tanious, F.A., Wilson, W.D., Ly, D.H. and Armitage, B.A. (2007) High-affinity homologous peptide nucleic acid probes for targeting a quadruplex-forming sequence from a MYC promoter element. Biochemistry, 46, 10433-10443.
36. Paul, A., Sengupta, P., Krishnan, Y. and Ladame, S. (2008) Combining G-quadruplex targeting motifs on a single peptide nucleic acid scaffold: a hybrid (3 + 1) PNA-DNA bimolecular quadruplex. Chemistry, 14, 8682-8689.
37. 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.
38. Kutyavin, I.V., Lokhov, S.G., Afonina, I.A., Dempcy, R., Gall, A.A., Gorn, V.V., Lukhtanov, E., Metcalf, M., Mills, A., Reed, M.W. et al. (2002) Reduced aggregation and improved specificity of G-rich oligodeoxyribonucleotides containing pyrazolo[3, 4-d]pyrimidine guanine bases. Nucleic Acids Res., 30, 4952-4959.
39. 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. Ed. Engl., 46, 1414-1418.
40. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Maxam, A.M. and Gilbert, W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol., 65, 499-560.
42. Gaynutdinov, T.I., Neumann, R.D. and Panyutin, I.G. (2008) Structural polymorphism of intramolecular quadruplex of human telomeric DNA: effect of cations, quadruplex-binding drugs and flanking sequences. Nucleic Acids Res., 36, 4079-4087.
43. Rezler, E.M., Seenisamy, J., Bashyam, S., Kim, M.Y., White, E., Wilson, W.D. and Hurley, L.H. (2005) Telomestatin and diseleno sapphyrin bind selectively to two different forms of the human telomeric G-quadruplex structure. J. Am. Chem. Soc., 127, 9439-9447.
44. Giraldo, R., Suzuki, M., Chapman, L. and Rhodes, D. (1994) Promotion of parallel DNA quadruplexes by a yeast telomere binding protein: a circular dichroism study. Proc. Natl Acad. Sci. USA, 91, 7658-7662.
45. Dapic, V., Abdomerovic, V., Marrington, R., Peberdy, J., Rodger, A., Trent, J.O. and Bates, P.J. (2003) Biophysical and biological properties of quadruplex oligodeoxyribonucleotides. Nucleic Acids Res., 31, 2097-2107.
46. Rujan, I.N., Meleney, J.C. and Bolton, P.H. (2005) Vertebrate telomere repeat DNAs favor external loop propeller quadruplex structures in the presence of high concentrations of potassium. Nucleic Acids Res., 33, 2022-2031.
47. Vorlickova, M., Chladkova, J., Kejnovska, I., Fialova, M. and Kypr, J. (2005) Guanine tetraplex topology of human telomere DNA is governed by the number of (TTAGGG) repeats. Nucleic Acids Res., 33, 5851-5860.
48. Mergny, J.L., Li, J., Lacroix, L., Amrane, S. and Chaires, J.B. (2005) Thermal difference spectra: a specific signature for nucleic acid structures. Nucleic Acids Res., 33, e138.
49. 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.
50. 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.
51. 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.
52. Todd, A.K., Johnston, M. and Neidle, S. (2005) Highly prevalent putative quadruplex sequence motifs in human DNA. Nucleic Acids Res., 33, 2901-2907.
53. Wittung, P., Nielsen, P. and Norden, B. (1996) Direct observation of strand invasion by peptide nucleic acid (PNA) into double-stranded DNA. J. Am. Chem. Soc., 118, 7049-7054.
54. Kuhn, H., Demidov, V.V., Nielsen, P.E. and Frank-Kamenetskii, M.D. (1999) An experimental study of mechanism and specificity of peptide nucleic acid (PNA) binding to duplex DNA. J. Mol. Biol., 286, 1337-1345.
55. Griffith, M.C., Risen, L.M., Greig, M.J., Lesnik, E.A., Sprankle, K.G., Griffey, R.H., Kiely, J.S. and Freier, S.M. (1995) Single and bis peptide nucleic-acids as triplexing agents - binding and stoichiometry. J. Am. Chem. Soc., 117, 831-832.
56. 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.
57. Englund, E.A., Xu, Q., Witschi, M.A. and Appella, D.H. (2006) PNA-DNA duplexes, triplexes, and quadruplexes are stabilized with trans-cyclopentane units. J. Am. Chem. Soc., 128, 16456-16457.
58. Petraccone, L., Barone, G. and Giancola, C. (2005) Quadruplex-forming oligonucleotides as tools in anticancer therapy and aptamers design: energetic aspects. Curr. Med. Chem. Anticancer Agents, 5, 463-475.
59. Amato, J., Oliviero, G., De Pauw, E. and Gabelica, V. (2009) Hybridization of short complementary PNAs to G-quadruplex forming oligonucleotides: an electrospray mass spectrometry study. Biopolymers, 91, 244-255.