mass spectrometry; DNA; PNA; noncovalent; supramolecular chemistry; G-quadruplex
Abstract :
[en] We investigated the interaction of the short PNA strand [acccca]-PNA with oligodeoxynucleotides containing one, two, or four tracts of TGGGGT units. Electrospray ionization mass spectrometry allowed exploring the wide variety of complex stoichiometries that were found to coexist in solution. In water, the PNA strand forms short heteroduplexes with the complementary DNA sequences, but higher-order structures are also found, with PNA(2n)*DNA(n) triplex units, culminating in precipitation at very low ionic strength. In the presence of ammonium acetate, there is a competition between PNA*DNA heteroduplex formation and DNA G-quadruplex formation. Heteroduplex formation is favored when the PNA + DNA mixture in ammonium acetate is heated and cooled at room temperature, but not if the PNA is added at room temperature to the pre-formed G-quadruplex. We also found that the short [acccca]-PNA strand binds to G-quadruplexes. (c) 2008 Wiley Periodicals, Inc. Biopolymers, 2008.
Research center :
Giga-Systems Biology and Chemical Biology - ULiège
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Commentary :
This is the pre-peer reviewed version of the following article: Amato J, Oliviero G, De Pauw E, Gabelica V., Hybridization of short complementary PNAs to G-quadruplex forming oligonucleotides: An electrospray mass spectrometry study. Biopolymers. Published ahead of print on Dec. 8, 2008.
Burge, S.; Parkinson, G. N.; Hazel, P.; Todd, A. K.; Neidle, S. Nucleic Acids Res 2006, 34, 5402-5415.
Simonsson, T. Biol Chem 2001, 382, 621-628.
Davis, J. T. Angew Chem Int Ed 2004, 43, 668-698.
Phan, A.-T.; Kuryavyi, V.; Patel, D. J. Curr Opin Struct Biol 2006, 16, 288-298.
Patel, D. J.; Phan, A. T.; Kuryavyi, V. Nucleic Acids Res 2007, 35, 7429-7455.
Riou, J.-F.; Gomez, D.; Morjani, H.; Trentesaux, C. In Quadruplex Nucleic Acids; Neidle, S.; Balasubramanian, S.; Eds.; The Royal Society of Chemistry: Cambridge, 2006; Chapter 6, pp 154-179.
Sen, D.; Gilbert, W. Nature 1988, 334, 364-366.
Chen, J. P.; Spector, M. S.; Kunos, G.; Gao, B. J Biol Chem 1997, 272, 23144-23150.
Rangan, A.; Fedoroff, O. Y.; Hurley, L. H. J Biol Chem 2001, 276, 4640-4646.
Dai, J.; Dexheimer, T. S.; Chen, D.; Carver, M.; Ambrus, A.; Jones, R. A.; Yang, D. J Am Chem Soc 2006, 128, 1096-1098.
Dexheimer, T. S.; Fry, M.; Hurley, L. H. In Quadruplex Nucleic Acids; Neidle, S.; Balasubramanian, S.; Eds.; The Royal Society of Chemistry: Cambridge, 2006; Chapter 7, pp 180-207.
Todd, A. K.; Haider, S. M.; Parkinson, G. N.; Neidle, S. Nucleic Acids Res 2007, 35, 5799-5808.
Dempsey, L. A.; Sun, H.; Hanakahi, L. A.; Maizels, N. J Biol Chem 1999, 274, 1066-1071.
Rezler, E. M.; Bearss, D. J.; Hurley, L. H. Annu Rev Pharmacol Toxicol 2003, 43, 359-379.
Wang, K. Y.; McCurdy, S.; Shea, R. G.; Swaminathan, S.; Bolton, P. H. Biochemistry 1993, 32, 1899-1904.
Pileur, F.; Andreola, M. L.; Dausse, E.; Michel, J.; Moreau, S.; Yamada, H.; Gaidamakov, S. A.; Crouch, R. J.; Toulme, J. J.; Cazenave, C. Nucleic Acids Res 2003, 31, 5776-5788.
Chou, S. H.; Chin, K. H.; Wang, A. H. J. Trends Biochem Sci 2005, 30, 231-234.
Girvan, A. C.; Teng, Y.; Casson, L. K.; Thomas, S. D.; Juliger, S.; Ball, M. W.; Klein, J. B.; Pierce, W. M.; Barve, S. S.; Bates, P. J. Mol Cancer Ther 2006, 5, 1790-1799.
Levesque, D.; Beaudoin, J. D.; Roy, S.; Perreault, J. P. Biochem J 2007, 403, 129-138.
Phan, A. T.; Kuryavyi, V.; Gaw, H. Y.; Patel, D. J. Nat Chem Biol 2005, 1, 167-173.
White, E. W.; Tanious, F.; Ismail, M. A.; Reszka, A. P.; Neidle, S.; Boykin, D. W.; Wilson, W. D. Biophys Chem 2007, 126, 140-153.
Chen, Q.; Kuntz, I. D.; Shafer, R. H. Proc Natl Acad Sci USA 1996, 93, 2635-2639.
Egholm, M.; Buchardt, O.; Christensen, L.; Behrens, C.; Freier, S. M.; Driver, D. A.; Berg, R. H.; Kim, S. K.; Norden, B.; Nielsen, P. E. Nature 1993, 365, 566-568.
Datta, B.; Armitage, B. A. J Am Chem Soc 2001, 123, 9612-9619.
Green, J. J.; Ying, L. M.; Klenerman, D.; Balasubramanian, S. J Am Chem Soc 2003, 125, 3763-3767.
Marin, V. L.; Armitage, B. A. Biochemistry 2006, 45, 1745-1754.
Marin, V. L.; Armitage, B. A. J Am Chem Soc 2005, 127, 8032-8033.
Datta, B.; Schmitt, C.; Armitage, B. A. J Am Chem Soc 2003, 125, 4111-4118.
Roy, S.; Tanious, F. A.; Wilson, W. D.; Ly, D. H.; Armitage, B. A. Biochemistry 2007, 46, 10433-10443.
Rujan, I. N.; Meleney, J. C.; Bolton, P. H. Nucleic Acids Res 2005, 33, 2022-2031.
Ying, L. M.; Green, J. J.; Li, H. T.; Klenerman, D.; Balasubramanian, S. Proc Natl Acad Sci USA 2003, 100, 14629-14634.
Phan, A.-T.; Modi, Y. S.; Patel, D. J. J Am Chem Soc 2004, 126, 8710-8716.
Hazel, P.; Parkinson, G. N.; Neidle, S. J Am Chem Soc 2006, 128, 5480-5487.
Cevec, M.; Plavec, J. Biochemistry 2005, 44, 15238-15246.
Hazel, P.; Huppert, J.; Balasubramanian, S.; Neidle, S. J Am Chem Soc 2004, 126, 16405-16415.
Risitano, A.; Fox, K. R. Nucleic Acids Res 2004, 32, 2598-2606.
Smirnov, I.; Shafer, R. H. Biochemistry 2000, 39, 1462-1468.
Smargiasso, N.; Rosu, F.; Hsia, W.; Colson, P.; Baker, E. S.; Bowers, M. T.; De Pauw, E.; Gabelica, V. J Am Chem Soc 2008, 130, 10208-10216.
Yamashita, M.; Fenn, J. B. J Phys Chem 1984, 88, 4451-4459.
Whitehouse, M.; Dreyer, R. N.; Yamashita, M.; Fenn, J. B. Anal Chem 1985, 57, 675-679.
Fenn, J. B.; Mann, M.; Meng, C. K.; Wong, S. F.; Whitehouse, C. M. Science 1989, 246, 64-71.
Ganem, B.; Li, Y.-T.; Henion, J. D. Tetrahedron Lett 1993, 34, 1445-1448.
Light-Wahl, K. J.; Springer, D. L.; Winger, B. E.; Edmonds, C. G.; Camp, D. G.; Thrall, B. D.; Smith, R. D. J Am Chem Soc 1993, 115, 803-804.
Goodlett, D. R.; Camp, D. G.;, II Hardin, C. C.; Corregan, M.; Smith, R. D. Biol Mass Spectrom 1993, 22, 181-183.
David, W. M.; Brodbelt, J.; Kerwin, S. M.; Thomas, P. W. Anal Chem 2002, 74, 2029-2033.
Rosu, F.; Gabelica, V.; Houssier, C.; Colson, P.; De Pauw, E. Rapid Commun Mass Spectrom 2002, 16, 1729-1736.
Li, H.; Yuan, G.; Du, D. J Am Soc Mass Spectrom 2008, 19, 550-559.
Greig, M. J.; Gaus, H.-J.; Griffey, R. H. Rapid Commun Mass Spectrom 1996, 10, 47-50.
Baker, E. S.; Hong, J. W.; Gaylord, B. S.; Bazan, G. C.; Bowers, M. T. J Am Chem Soc 2006, 128, 8484-8492.
Modi, S.; Wani, A. H.; Krishnan, Y. Nucleic Acids Res 2006, 34, 4354-4363.
Delvolve, A.; Tabet, J. C.; Bregant, S.; Afonso, C.; Burlina, F.; Fournier, F. J Mass Spectrom 2006, 41, 1498-1508.
Hofstadler, S. A.; Griffey, R. H. Chem Rev 2001, 101, 377-390.
Beck, J.; Colgrave, M. L.; Ralph, S. F.; Sheil, M. M. Mass Spectrom Rev 2001, 20, 61-87.
Rosu, F.; De Pauw, E.; Gabelica, V. Biochimie 2008, 90, 1074-1087.
Gabelica, V.; Baker, E. S.; Teulade-Fichou, M.-P.; De Pauw, E.; Bowers, M. T. J Am Chem Soc 2007, 129, 895-904.
Mergny, J.-L.; De Cian, A.; Gheleb, A.; Sacca, B.; Lacroix, L. Nucleic Acids Res 2005, 33, 81-94.
Mergny, J.-L.; Gros, J.; De Cian, A.; Bourdoncle, A.; Rosu, F.; Sacca, B.; Guittat, L.; Amrane, S.; Mills, M.; Alberti, P.; Takasugi, M.; Lacroix, L. In Quadruplex Nucleic Acids; Neidle, S.; Balasubramanian, S.; Eds.; The Royal Society of Chemistry: Cambridge, 2006; Chapter 2, pp 31-80.
Gros, J.; Rosu, F.; Amrane, S.; De Cian, A.; Gabelica, V.; Lacroix, L.; Mergny, J. L. Nucleic Acids Res 2007, 35, 3064-3075.
Balagurumoorthy, P.; Brahmachari, S. K. J Biol Chem 1994, 269, 21 858-21 869.
Lu, M.; Guo, Q.; Kallenbach, N. R. Biochemistry 1992, 31, 2455-2459.
Rankin, S.; Reszka, A. P.; Huppert, J.; Zloh, M.; Parkinson, G. N.; Todd, A. K.; Ladame, S.; Balasubramanian, S.; Neidle, S. J Am Chem Soc 2005, 127, 10584-10589.
Jing, N.; Rando, R. F.; Pommier, Y.; Hogan, M. E. Biochemistry 1997, 36, 12498-12505.