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Structure of Nucleic Acids in the Gas Phase

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Book cover Nucleic Acids in the Gas Phase

Part of the book series: Physical Chemistry in Action ((PCIA))

Abstract

Evolution has refined nucleic acids to display well-defined three-dimensional structures that are functional under aqueous physiological conditions. While the structure of nucleic acids is well known in solution, it is unclear how nucleic acids react when transferred to a fully anhydrous environment. Simple physical chemistry considerations suggest that a heavily charged poly-anion would adopt fully extended conformations in vacuum, and that multistranded structure would dissociate, to guarantee that charged residues separate as much as possible to reduce Coulomb repulsion. However, and quite counterintuitively, a vast amount of experiments demonstrate that this is not the case and that oligomeric nucleic acids adopt quite compact structures in the gas phase, which in some cases might preserve memories of the original conformation in solution. In this chapter, we review our current understanding of nucleic acid structure in the gas phase.

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Abbreviations

ESI-MS:

Electrospray soft ionization mass spectrometry

IMS:

Ion mobility spectrometry

IVNT:

In vacuum native structure

XFEL:

X-ray free electron laser

CCS:

Collision cross section

MD:

Molecular dynamics

QM:

Quantum mechanics

DFT:

Density functional theory

CCSD(T)/CBS:

Coupled cluster with single, double, and triple excitation/complete basis set

References

  1. Blackburn GM, Gait MJ (1990) Nucleic acids in chemistry and biology. IRL Press, Oxford

    Google Scholar 

  2. Bloomfield VA, Crothers DM, Tinoco I (2000) Nucleic acids. Structure, properties and functions. University Science, Sausalito, CA

    Google Scholar 

  3. Saenger W (1984) Principles of nucleic acid structure. Springer, New York, NY

    Book  Google Scholar 

  4. Sinden RR (1994) DNA structure and function. Academic, San Diego, CA

    Google Scholar 

  5. Hobza P, Sponer J (2002) Toward true DNA base-stacking energies: MP2, CCSD(T), and complete basis set calculations. J Am Chem Soc 124(39):11802–11808

    Article  CAS  Google Scholar 

  6. Pérez A, Šponer J, Jurecka P, Hobza P, Luque FJ, Orozco M (2005) Are the hydrogen bonds of RNA (A⋅ U) stronger than those of DNA (A⋅ T)? A quantum mechanics study. Chem Eur J 11(17):5062–5066

    Article  Google Scholar 

  7. Hobza P, Kabelac M, Sponer J, Mejzlik P, Vondrasek J (1997) Performance of empirical potentials (AMBER, CFF95, CVFF, CHARMM, OPLS, POLTEV), semiempirical quantum chemical methods (AM1, MNDO/M, PM3), and ab initio Hartree–Fock method for interaction of DNA bases: comparison with nonempirical beyond Hartree–Fock results. J Comput Chem 18(9):1136–1150

    Article  CAS  Google Scholar 

  8. Orozco M, Luque FJ (2000) Theoretical methods for the description of the solvent effect in biomolecular systems. Chem Rev 100(11):4187–4226

    Article  CAS  Google Scholar 

  9. Huey R, Mohr SC (1981) Condensed states of nucleic acids. III. psi(+) and psi(-) conformational transitions of DNA induced by ethanol and salt. Biopolymers 20(12):2533–2552

    Article  CAS  Google Scholar 

  10. Pohl FM, Jovin TM (1972) Salt-induced co-operative conformational change of a synthetic DNA: equilibrium and kinetic studies with poly (dG-dC). J Mol Biol 67(3):375–396

    Article  CAS  Google Scholar 

  11. Bernues J et al (1990) DNA-sequence and metal-ion specificity of the formation of *H-DNA. Nucleic Acids Res 18(14):4067–4073

    Article  CAS  Google Scholar 

  12. Wang Y, Patel DJ (1993) Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetraplex. Structure 1(4):263–282

    Article  CAS  Google Scholar 

  13. Williamson JR, Raghuraman MK, Cech TR (1989) Monovalent cation-induced structure of telomeric DNA: the G-quartet model. Cell 59(5):871–880

    Article  CAS  Google Scholar 

  14. Turner DH (2000) Structure, properties and functions. In: Bloomfield V, Crothers D, Tinoco I (eds) Structure, properties and functions, in nucleic acids. University Science Books, Sausalito, CA, pp 308–310

    Google Scholar 

  15. Miyoshi D, Nakamura K, Tateishi-Karimata H, Ohmichi T, Sugimoto N (2009) Hydration of Watson-Crick base pairs and dehydration of Hoogsteen base pairs inducing structural polymorphism under molecular crowding conditions. J Am Chem Soc 131:3522–3531

    Article  CAS  Google Scholar 

  16. Gabelica V et al (2007) Base-dependent electron photodetachment from negatively charged DNA strands upon 260-nm laser irradiation. J Am Chem Soc 129(15):4706–4713

    Article  CAS  Google Scholar 

  17. Gabelica V, Rosu F, Witt M, Baykut G, De Pauw E (2005) Fast gas-phase hydrogen/deuterium exchange observed for a DNA G-quadruplex. Rapid Commun Mass Spectrom 19(2):201–208

    Article  CAS  Google Scholar 

  18. Gale DC, Smith RD (1995) Characterization of noncovalent complexes formed between minor groove binding molecules and duplex DNA by electrospray ionization-mass spectrometry. J Am Soc Mass Spectrom 6(12):1154

    Article  CAS  Google Scholar 

  19. Gidden J, Baker ES, Ferzoco AL, Bowers MT (2005) Structural motifs of DNA complexes in the gas phase. Int J Mass Spectrom 240:183–193

    Article  CAS  Google Scholar 

  20. Hofstadler SA, Griffey RH (2001) Analysis of noncovalent complexes of DNA and RNA by mass spectrometry. Chem Rev 101(2):377–390

    Article  CAS  Google Scholar 

  21. Reyzer ML et al (2001) Evaluation of complexation of metal-mediated DNA-binding drugs to oligonucleotides via electrospray ionization mass spectrometry. Nucleic Acids Res 29(21):E103-3

    Article  Google Scholar 

  22. Rosu F, De Pauw E, Gabelica V (2008) Electrospray mass spectrometry to study drug-nucleic acids interactions. Biochimie 90(7):1074–1087

    Article  CAS  Google Scholar 

  23. Rosu F et al (2002) Triplex and quadruplex DNA structures studied by electrospray mass spectrometry. Rapid Commun Mass Spectrom 16(18):1729–1736

    Article  CAS  Google Scholar 

  24. Rosu F et al (2010) Tetramolecular G-quadruplex formation pathways studied by electrospray mass spectrometry. Nucleic Acids Res 38(15):5217–5225

    Article  CAS  Google Scholar 

  25. Rosu F et al (2007) Ligand binding mode to duplex and triplex DNA assessed by combining electrospray tandem mass spectrometry and molecular modeling. J Am Soc Mass Spectrom 18(6):1052–1062

    Article  CAS  Google Scholar 

  26. Schnier PD et al (1998) Activation energies for dissociation of double strand oligonucleotide anions: evidence for Watson-Crick base pairing in vacuo. J Am Chem Soc 120(37):9605–9613

    Article  CAS  Google Scholar 

  27. Wan C et al (2008) Studies of the intermolecular DNA triplexes of C + .GC and T.AT triplets by electrospray ionization Fourier-transform ion cyclotron resonance mass spectrometry. J Mass Spectrom 43(2):164–172

    Article  CAS  Google Scholar 

  28. Wan KX, Gross ML, Shibue T (2000) Gas-phase stability of double-stranded oligodeoxynucleotides and their noncovalent complexes with DNA-binding drugs as revealed by collisional activation in an ion trap. J Am Soc Mass Spectrom 11(5):450–457

    Article  CAS  Google Scholar 

  29. Gabelica V, De Pauw E, Rosu F (1999) Interaction between antitumor drugs and a double-stranded oligonucleotide studied by electrospray ionization mass spectrometry. J Mass Spectrom 34(12):1328–1337

    Article  CAS  Google Scholar 

  30. Vairamani M, Gross ML (2003) G-quadruplex formation of thrombin-binding aptamer detected by electrospray ionization mass spectrometry. J Am Chem Soc 125(1):42–43

    Article  CAS  Google Scholar 

  31. Wyttenbach T, Bleiholder C, Bowers MT (2013) Factors contributing to the collision cross section of polyatomic ions in the kilodalton to gigadalton range: application to ion mobility measurements. Anal Chem 85:2191–2199

    Article  CAS  Google Scholar 

  32. Meyer T, de la Cruz X, Orozco M (2009) An atomistic view to the gas phase proteome. Structure 17(1):88–95

    Article  CAS  Google Scholar 

  33. Meyer T, Gabelica V, Grubmüller H, Orozco M (2012) Proteins in the gas phase. WIRES Comput Mol Sci

  34. Neutze R, Huldt G, Hajdu J, van der Spoel D (2004) Potential impact of an X-ray free electron laser on structural biology. Radiat Phys Chem 71:905–916

    Article  CAS  Google Scholar 

  35. López AT, T, Vilaseca M, Giralt E (2013) New J Chem 37: 1283–1289

    Google Scholar 

  36. De la Mora F (2000) J Anal Chim Acta (406):93–104

    Google Scholar 

  37. Rayleigh L (1882) Philos Mag: 184–186

    Google Scholar 

  38. Fenn JB (1993) Ion formation from charged droplets: roles of geometry, energy, and time. J Am Soc Mass Spectrom 4:524–535

    Article  CAS  Google Scholar 

  39. Hautreux M, Hue N, Du Fou de Kerdaniel A, Zahir A, Malec V, Laprévote O (2004) Under non‐denaturing solvent conditions, the mean charge state of a multiply charged protein ion formed by electrospray is linearly correlated with the macromolecular surface. Int J Mass Spectrom 231:131–137

    Article  CAS  Google Scholar 

  40. Felitsyn N, Kitova EN, Klassen JS (2002) Thermal dissociation of the protein homodimer ecotin in the gas phase. J Am Soc Mass Spectrom 13(12):1432–1442

    Article  CAS  Google Scholar 

  41. Arcella A et al (2012) Structure of triplex DNA in the gas phase. J Am Chem Soc 134(15):6596–6606

    Article  CAS  Google Scholar 

  42. Rueda M et al (2003) The structure and dynamics of DNA in the gas phase. J Am Chem Soc 125(26):8007–8014

    Article  CAS  Google Scholar 

  43. Rueda M, Luque FJ, Orozco M (2005) Nature of minor-groove binders-DNA complexes in the gas phase. J Am Chem Soc 127(33):11690–11698

    Article  CAS  Google Scholar 

  44. McDaniel EW, Mason EA (1988) Transport properties of ions in gases. Wiley, New York, NY

    Google Scholar 

  45. Wang B, Valentine S, Plasencia M, Raghuraman S, Zhang X (2010) Artificial neural networks for the prediction of peptide drift time in ion mobility mass spectrometry. BMC Bioinforma 11:182

    Article  CAS  Google Scholar 

  46. Rueda M, Luque FJ, Orozco M (2006) G-quadruplexes can maintain their structure in the gas phase. J Am Chem Soc 128(11):3608–3619

    Article  CAS  Google Scholar 

  47. Madsen JA, Brodbelt JS (2010) Asymmetric charge partitioning upon dissociation of DNA duplexes. J Am Soc Mass Spectrom 21:1144–1150

    Article  CAS  Google Scholar 

  48. Cleland WW, Kreevoy MM (1994) Low-barrier hydrogen bonds and enzymic catalysis. Science 264(5167):1887–1890

    Article  CAS  Google Scholar 

  49. Rezác J, Hobza P (2013) Describing noncovalent interactions beyond the common approximations: how accurate is then “gold stgandard”, CCSD(T), at the Complete basis set limit. J Chem Theory Comput 9:2151–2155

    Article  Google Scholar 

  50. Orozco M, Cubero E, Barril X, Colominas C, Luque FJ (1999) Nucleic acid bases in solution. In: Leszczynski J (ed) Computational molecular biology, Theoretical computational chemistry. Elsevier Science, Amsterdam, pp 119–166

    Google Scholar 

  51. Colominas C, Teixidó J, Cemelí JM, Luque FJ, Orozco M (1998) J Phys Chem B 102:2269–2276

    Article  CAS  Google Scholar 

  52. Hernández B, Luque FJ, Orozco M (1996) Tautomerism of xanthine oxidase subtrates hypoxathine and allopurinol. J Org Chem 61:5964–5971

    Article  Google Scholar 

  53. Colominas C, Luque FJ, Orozco M (1996) Tautomerism and protonation of guanine and cytosine. Implications in the formation of triplex DNA. J Am Chem Soc 118:6811–6821

    Article  CAS  Google Scholar 

  54. Blas JR, Luque FJ, Orozco M (2004) Unique tautomeric properties of isoguanine. J Am Chem Soc 126:154–164

    Article  CAS  Google Scholar 

  55. Orozco M, Canela EI, Mallol J, Lluis C, Franco R (1990) Ab initio study of the protonation and the tautomerism of the 7-aminopyrazolopyrimidine molecule. J Org Chem 55:753–756

    Article  CAS  Google Scholar 

  56. Hoaglund CS, Liu Y, Ellington AD, Pagel M, Clemmer DE (1997) Gas-phase DNA: oligothymidine ion conformers. J Am Chem Soc 119:9051–9052

    Article  CAS  Google Scholar 

  57. Gidden J, Bowers MT (2002) Gas-phase conformational and energetic properties of deprotonated dinucleotides. Eur Phys J 20:409–419

    CAS  Google Scholar 

  58. Gidden J et al (2004) Duplex formation and the onset of helicity in poly d(CG)n oligonucleotides in a solvent-free environment. J Am Chem Soc 126(46):15132–15140

    Article  CAS  Google Scholar 

  59. Allemand JF et al (1998) Stretched and overwound DNA forms a Pauling-like structure with exposed bases. Proc Natl Acad Sci U S A 95(24):14152–14157

    Article  CAS  Google Scholar 

  60. Kosikov MK, Gorin AA, Zhurkin VB, Olson WK (1999) DNA stretching and compression: large-scale simulations of double helical structures. J Mol Biol 289:1301

    Article  CAS  Google Scholar 

  61. Laughlan G et al (1994) The high-resolution crystal structure of a parallel-stranded guanine tetraplex. Science 265(5171):520–524

    Article  CAS  Google Scholar 

  62. Parkinson GN, Lee MP, Neidle S (2002) Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 417(6891):876–880

    Article  CAS  Google Scholar 

  63. Phillips K et al (1997) The crystal structure of a parallel-stranded guanine tetraplex at 0.95 A resolution. J Mol Biol 273(1):171–182

    Article  CAS  Google Scholar 

  64. Sen D, Gilbert W (1988) Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis. Nature 334(6180):364–366

    Article  CAS  Google Scholar 

  65. Gabelica V et al (2008) Infrared signature of DNA G-quadruplexes in the gas phase. J Am Chem Soc 130(6):1810–1811

    Article  CAS  Google Scholar 

  66. Rosu F et al (2012) UV spectroscopy of DNA duplex and quadruplex structures in the gas phase. J Phys Chem A 116(22):5383–5391

    Article  CAS  Google Scholar 

  67. Balthasart F, Plavec J, Gabelica V (2013) Ammonium ion binding to DNA G-quadruplexes: do electrospray mass spectra faithfully reflect the solution-phase species? J Am Soc Mass Spectrom 24(1):1–8

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute for Research in Biomedicine (IRB Barcelona), Barcelona, Spain

    Annalisa Arcella, Guillem Portella & Modesto Orozco

  2. Joint Research Program in Computational Biology, Institute for Research in Biomedicine and Barcelona Supercomputing Center, Barcelona, Spain

    Annalisa Arcella, Guillem Portella & Modesto Orozco

  3. Department of Biochemistry and Molecular Biology, University of Barcelona, Barcelona, Spain

    Modesto Orozco

Authors
  1. Annalisa Arcella
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  2. Guillem Portella
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  3. Modesto Orozco
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Corresponding author

Correspondence to Modesto Orozco .

Editor information

Editors and Affiliations

  1. Université de Bordeaux, Institut Européen de Chimie et Biologie, Pessac, France

    Valérie Gabelica

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Arcella, A., Portella, G., Orozco, M. (2014). Structure of Nucleic Acids in the Gas Phase. In: Gabelica, V. (eds) Nucleic Acids in the Gas Phase. Physical Chemistry in Action. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-54842-0_3

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