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Interactions Between Metal Ions and DNA

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The Periodic Table II

Part of the book series: Structure and Bonding ((STRUCTURE,volume 182))

Abstract

84 years elapsed between the announcements of the periodic table and that of the DNA double helix in 1953, and the two have been combined in many ways since then. In this chapter an outline of the fundamentals of DNA structure leads into a range of examples showing how the natural magnesium and potassium ions found in nature can be substituted in a diversity of applications. The dynamic structures found in nature have been studied in the more controlled but artificial environment of the DNA crystal using examples from sodium to platinum and also in a range of DNA-binding metal complexes. While NMR is an essential technique for studying nucleic acid structure and conformation, most of our knowledge of metal ion binding has come from X-ray crystallography. These days the structures studied, and therefore also the diversity of metal binding, go beyond the double helix to triplexes, hairpin loops, junctions and quadruplexes, and the chapter describes briefly how these pieces fit into the DNA jigsaw. In a final section, the roles of metal cations in the crystallisation of new DNA structures are discussed, along with an introduction to the versatility of the periodic table of absorption edges for nucleic acid structure determination.

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Notes

  1. 1.

    DNA bases are A-adenine, C-cytosine, G-guanine and T-thymine.

Abbreviations

Bpy:

2,2′-Bipyridyl

DDD:

Drew-Dickerson dodecamer

DNA:

Deoxyribonucleic acid

dppz:

Dipyridophenazine

FRET:

Fluorescence resonance energy transfer

MLCT:

Metal-to-ligand charge transfer

MPD:

2,4-Dimethylpentanediol

NDB:

Nucleic Acid Database

PDB:

Protein Data Bank

phen:

1,10-Phenanthroline

RNA:

Ribonucleic acid

Salphen:

N,N′-Phenylenebis(salicylideneimine)

TAP:

1,4,5,8-Tetraazaphenanthrene

TEM:

Transmission electron microscopy

References

  1. Kellett A, Molphy Z, Slator C, McKee V, Farrell NP (2019) Molecular methods for assessment of non-covalent metallodrug-DNA interactions. Chem Soc Rev 48(4):971–988

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Thorpe JH, Teixeira SCM, Gale BC, Cardin CJ (2002) Structural characterization of a new crystal form of the four-way Holliday junction formed by the DNA sequence d(CCGGTACCGG)2: sequence versus lattice? Acta Crystallogr. Sect. D Biol. Crystallogr. 58(3):567–569

    Google Scholar 

  3. Kondo J, Yamada T, Hirose C, Okamoto I, Tanaka Y, Ono A (2014) Crystal structure of metallo DNA duplex containing consecutive Watson-Crick-like T-HgII-T base pairs. Angew Chem Int Ed 53(9):2385–2388

    CAS  Google Scholar 

  4. Ennifar E, Walter P, Dumas P (2003) A crystallographic study of the binding of 13 metal ions of two related RNA duplexes. Nucleic Acids Res 31(10):2671–2682

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Todd RC, Lippard SJ (2010) Structure of duplex DNA containing the cisplatin 1,2-{Pt(NH3)2}2+−d(GpG) cross-link at 1.77Å resolution. J Inorg Biochem 104(9):902–908

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Todd AK, Adams A, Thorpe JH, Denny WA, Wakelin LPG, Cardin CJ (1999) Major groove binding and “DNA-Induced” fit in the intercalation of a derivative of the mixed topoisomerase I/II poison N-(2-(dimethylamino)ethyl)acridine-4-carboxamide (DACA) into DNA: X-ray structure complexed to d(CG(5-Bru)ACG)2 at 1.3-Å resolution [2]. J Med Chem 42(4):536–540

    CAS  PubMed  Google Scholar 

  7. Cardin CJ, Hall JP (2018) Structural studies of DNA-binding metal complexes of therapeutic importance. DNA-targeting molecules as therapeutic agents. Royal Society of Chemistry, London, pp 198–227

    Google Scholar 

  8. Dennis C, Campbell P (2003) The eternal molecule. Nature 421(6921):396

    Google Scholar 

  9. Biffi G, Tannahill D, McCafferty J, Balasubramanian S (2013) Quantitative visualization of DNA G-quadruplex structures in human cells. Nat Chem 5(3):182–186

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Evans K, Bhamra I, Wheelhouse RT, Arnold JRP, Cosstick R, Fisher J (2015) Stabilization of a bimolecular triplex by 3′-S-Phosphorothiolate modifications: an NMR and UV thermal melting investigation. Chemistry 21(19):7278–7284

    CAS  PubMed  Google Scholar 

  11. Wing R, Drew H, Takano T, Broka C, Tanaka S, Itakura K, Dickerson RE (1980) Crystal structure analysis of a complete turn of B-DNA. Nature 287(5784):755–758

    CAS  PubMed  Google Scholar 

  12. Hall JP, Sanchez-Weatherby J, Alberti C, Quimper CH, O’Sullivan K, Brazier JA, Winter G, Sorensen T, Kelly JM, Cardin DJ et al (2014) Controlled dehydration of a ruthenium complex-DNA crystal induces reversible DNA kinking. J Am Chem Soc 136(50):17505–17512

    CAS  PubMed  Google Scholar 

  13. Kim D, Hur J, Park K, Bae S, Shin D, Ha SC, Hwang HY, Hohng S, Lee JH, Lee S et al (2014) Distinct Z-DNA binding mode of a PKR-like protein kinase containing a Z-DNA binding domain (PKZ). Nucleic Acids Res 42(9):5937–5948

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Wu Z, Tian T, Yu J, Weng X, Liu Y, Zhou X (2011) Formation of sequence-independent Z-DNA induced by a ruthenium complex at low salt concentrations. Angew Chem Int Ed 50(50):11962–11967

    CAS  Google Scholar 

  15. Hoogsteen K (1959) The structure of crystals containing a hydrogen-bonded complex of 1-methylthymine and 9-methyladenine. Acta Crystallogr 12(10):822–823

    CAS  Google Scholar 

  16. Hoogsteen K (1963) The crystal and molecular structure of a hydrogen-bonded complex between 1-methylthymine and 9-methyladenine. Acta Crystallogr 16(9):907–916

    CAS  Google Scholar 

  17. Nikolova EN, Zhou H, Gottardo FL, Alvey HS, Kimsey IJ, Al-Hashimi HM (2013) A historical account of Hoogsteen base-pairs in duplex DNA. Biopolymers 99(12):955–968

    CAS  PubMed  Google Scholar 

  18. Gill ML, Strobel SA, Loria JP (2006) Crystallization and characterization of the thallium form of the Oxytricha Nova G-Quadruplex. Nucleic Acids Res 34(16):4506–4514

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Fox KR, Brown T (2011) Formation of stable DNA triplexes. Biochem Soc Trans 39(2):629–634

    CAS  PubMed  Google Scholar 

  20. Betts L, Josey JA, Veal JM, Jordan SR (1995) A nucleic acid triple helix formed by a peptide nucleic acid-DNA complex. Science 270(5243):1838–1841

    CAS  PubMed  Google Scholar 

  21. Gurung SP, Schwarz C, Hall JP, Cardin CJ, Brazier JA (2015) The importance of loop length on the stability of I-motif structures. Chem Commun 51(26):5630–5632

    CAS  Google Scholar 

  22. Abdelhamid MAS, Fábián L, Macdonald CJ, Cheesman MR, Gates AJ, Waller ZAE (2018) Redox-dependent control of i-motif DNA structure using copper cations. Nucleic Acids Res 46(12):5886–5893

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Zeraati M, Langley DB, Schofield P, Moye AL, Rouet R (2018) I-motif DNA structures are formed in the nuclei. Nat Chem 10:631–637

    CAS  PubMed  Google Scholar 

  24. Bruner SD, Norman DPG, Verdine GL (2000) Structural basis for recognition of the endogenous mutagen 8-hydroxyguanine. Nature 403:859–866

    CAS  PubMed  Google Scholar 

  25. Keane PM, Poynton FE, Hall JP, Sazanovich IV, Towrie M, Gunnlaugsson T, Quinn SJ, Cardin CJ, Kelly JM (2015) Reversal of a single base-pair step controls guanine photo-oxidation by an intercalating ruthenium(II) dipyridophenazine complex. Angew Chemie 127(29):8484–8488

    Google Scholar 

  26. Hall JP, Poynton FE, Keane PM, Gurung SP, Brazier JA, Cardin DJ, Winter G, Gunnlaugsson T, Sazanovich IV, Towrie M et al (2015) Monitoring one-electron photo-oxidation of guanine in DNA crystals using ultrafast infrared spectroscopy. Nat Chem 7(12):961–967

    CAS  PubMed  Google Scholar 

  27. Hall JP, Keane PM, Beer H, Buchner K, Winter G, Sorensen TL, Cardin DJ, Brazier JA, Cardin CJ (2016) Delta chirality ruthenium ‘light-switch’ complexes can bind in the minor groove of DNA with five different binding modes. Nucleic Acids Res 44(19):9472–9482

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Song H, Kaiser JT, Barton JK (2012) Crystal structure of Δ-[Ru(Bpy)2dppz]2+ bound to mismatched DNA reveals side-by-side metalloinsertion and intercalation. Nat Chem 4(8):615–620

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Thorpe JH, Gale BC, Teixeira SCM, Cardin CJ (2003) Conformational and hydration effects of site-selective sodium, calcium and strontium ion binding to the DNA Holliday junction structure d(TCGGTACCGA)4. J Mol Biol 327(1):97–109

    CAS  PubMed  Google Scholar 

  30. Romani A (2011) Cellular magnesium homeostasis. Arch Biochem Biophys 512:1–23

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Drew HRR, Wing RMM, Takano T, Broka C, Tanaka S, Itakura K, Dickerson REE (1981) Structure of a B-DNA dodecamer: conformation and dynamics. Proc Natl Acad Sci 78(4):2179–2183

    CAS  PubMed  Google Scholar 

  32. Hiller DA, Strobel SA (2011) The chemical versatility of RNA. Philos Trans R Soc B Biol Sci 366(1580):2929–2935

    CAS  Google Scholar 

  33. Crick FHC, Klug A (1975) Kinky helix. Nature 255:530–533

    CAS  PubMed  Google Scholar 

  34. Juo ZS, Kassavetis GA, Wang J, Geiduschek EP, Sigler PB (2003) Crystal structure of a transcription factor IIIB core interface ternary complex. Nature 422:534–539

    CAS  PubMed  Google Scholar 

  35. Wilson JJ, Lippard SJ (2014) Synthetic methods for the preparation of platinum anticancer complexes. Chem Rev 114(8):4470–4495

    CAS  PubMed  Google Scholar 

  36. Reißner T, Schneider S, Schorr S, Carell T (2010) Crystal structure of a cisplatin-(1,3-GTG) cross-link within DNA polymerase η. Angew Chem Int Ed 49(17):3077–3080

    Google Scholar 

  37. Alam MN, Huq F (2016) Comprehensive review on tumour active palladium compounds and structure–activity relationships. Coord Chem Rev 316:36–67

    CAS  Google Scholar 

  38. Cini M, Bradshaw TD, Woodward S (2017) Using titanium complexes to defeat cancer: the view from the shoulders of titans. Chem Soc Rev 46:1040–1051

    CAS  PubMed  Google Scholar 

  39. Howerton BS, Heidary DK, Glazer EC (2012) Strained ruthenium complexes are potent light-activated anticancer agents. J Am Chem Soc 134(20):8324–8327

    CAS  PubMed  Google Scholar 

  40. Lilley DMJ (2002) All change at Holliday junction. Proc Natl Acad Sci 94(18):9513–9515

    Google Scholar 

  41. Hadden JM, Déclais A-C, Carr SB, Lilley DMJ, Phillips SEV (2007) The structural basis of Holliday junction resolution by T7 endonuclease I. Nature 449(7162):621–624

    CAS  PubMed  Google Scholar 

  42. Coll M, Ortiz-Lombardía M, González A, Eritja R, Aymamí J, Azorín F (1999) Crystal structure of a DNA Holliday junction. Nat Struct Biol 6(10):913–917

    PubMed  Google Scholar 

  43. Hays FA, Teegarden A, Jones ZJR, Harms M, Raup D, Watson J, Cavaliere E, Ho PS (2005) How sequence defines structure: a crystallographic map of DNA structure and conformation. Proc Natl Acad Sci U S A 102(20):7157–7162

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Cardin CJ, Thorpe JH, Gale BC, Teixeira SCM. Strontium, a MAD target for the DNA Holliday junction. http://www.rcsb.org/structure/1NVY. Accessed 1 May 2019

  45. Hall JP, O’Sullivan K, Naseer A, Smith JA, Kelly JM, Cardin CJ (2011) Structure determination of an intercalating ruthenium dipyridophenazine complex which kinks DNA by semiintercalation of a tetraazaphenanthrene ligand. Proc Natl Acad Sci 108(43):17610–17614

    CAS  PubMed  Google Scholar 

  46. Naseer A, Cardin CJ. Strontium bound to the Holliday junction sequence d(TCGGCGCCGA)4. https://www.rcsb.org/structure/3GOO. Accessed 1 May 2019

  47. Laughlan G, Murchie AIH, Norman DG, Moore MH, Moody PCE, Lilley DMJ, Luisi B (1994) The high-resolution crystal structure of a parallel-stranded guanine tetraplex. Science 265(5171):520–524

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  49. Haider SM, Neidle S, Parkinson GN (2011) A structural analysis of G-quadruplex/ligand interactions. Biochimie 93(8):1239–1251

    CAS  PubMed  Google Scholar 

  50. Neidle S (2017) Quadruplex nucleic acids as targets for anticancer therapeutics. Nat Rev Chem 1:0041

    CAS  Google Scholar 

  51. Lin C, Wu G, Wang K, Onel B, Sakai S, Shao Y, Yang D (2018) Molecular recognition of the hybrid-2 human telomeric G-quadruplex by epiberberine: insights into conversion of telomeric G-quadruplex structures. Angew Chem Int Ed 57(34):10888–10893

    CAS  Google Scholar 

  52. Tan J-H, Liu H-Y, He J-H, Huang Z-S, Zhao Q, Ou T-M, Ge Y-L, Lv P, Gu L-Q, Li D et al (2016) Conformation selective antibody enables genome profiling and leads to discovery of parallel G-Quadruplex in human telomeres. Cell Chem Biol 23(10):1261–1270

    PubMed  Google Scholar 

  53. Stump S, Mou TC, Sprang SR, Natale NR, Beall HD (2018) Crystal structure of the major quadruplex formed in the promoter region of the human C-MYC oncogene. PLoS One 13(10):1–15

    Google Scholar 

  54. Asamitsu S, Obata S, Yu Z, Bando T, Sugiyama H (2019) Recent progress of targeted G-quadruplex-preferred ligands toward cancer therapy. Molecules 24(3):429

    PubMed Central  Google Scholar 

  55. Tateishi-Karimata H, Kawauchi K, Sugimoto N (2018) Destabilization of DNA G-quadruplexes by chemical environment changes during tumor progression facilitates transcription. J Am Chem Soc 140(2):642–651

    CAS  PubMed  Google Scholar 

  56. Quigley GJ, Wang AH, Ughetto G, van der Marel G, van Boom JH, Rich A (1980) Molecular structure of an anticancer drug-DNA complex: daunomycin plus d(CpGpTpApCpG). Biochemistry 77(12):7204–7208

    CAS  Google Scholar 

  57. Thomas JA (2015) Optical imaging probes for biomolecules: an introductory perspective. Chem Soc Rev 44(14):4494–4500

    CAS  PubMed  Google Scholar 

  58. Heinemann F, Karges J, Gasser G (2017) Critical overview of the use of Ru(II) polypyridyl complexes as photosensitizers in one-photon and two-photon photodynamic therapy. Acc Chem Res 50(11):2727–2736

    CAS  PubMed  Google Scholar 

  59. Mari C, Pierroz V, Ferrari S, Gasser G (2015) Combination of Ru(II) complexes and light: new frontiers in cancer therapy. Chem Sci 6(5):2660–2686

    CAS  PubMed  PubMed Central  Google Scholar 

  60. He Y, Lopez A, Zhang Z, Chen D, Yang R, Liu J (2019) Nucleotides and DNA coordinated lanthanides: from fundamentals to applications. Coord Chem Rev 387:235–248

    CAS  Google Scholar 

  61. Friedman AE, Chambron JC, Sauvage JP, Turro NJ, Barton JK (1990) A molecular light switch for DNA: Ru(Bpy)2(Dppz)2+. J Am Chem Soc 112(12):4960–4962

    CAS  Google Scholar 

  62. Cardin CJ, Kelly JM, Quinn SJ (2017) Photochemically active DNA-intercalating ruthenium and related complexes – insights by combining crystallography and transient spectroscopy. Chem Sci 8(7):4705–4723

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Zeglis BM, Pierre VC, Kaiser JT, Barton JK (2009) A bulky rhodium complex bound to an adenosine-adenosine DNA mismatch: general architecture of the metalloinsertion binding mode. Biochemistry 48(20):4247–4253

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Foxon SP, Phillips T, Gill MR, Towrie M, Parker AW, Webb M, Thomas JA (2007) A multifunctional light switch: DNA binding and cleavage properties of a heterobimetallic ruthenium-rhenium dipyridophenazine complex. Angew Chem Int Ed 46(20):3686–3688

    CAS  Google Scholar 

  65. Brueckmann NE, Kuegel S, Hamacher A, Kassack MU, Kunz PC (2010) Fluorescent polylactides with rhenium(bisimine) cores for tumour diagnostics. Eur J Inorg Chem 32:5063–5068

    Google Scholar 

  66. Wragg A, Gill MR, Turton D, Adams H, Roseveare TM, Smythe C, Su X, Thomas JA (2014) Tuning the cellular uptake properties of luminescent Heterobimetallic iridium(III)-ruthenium(II) DNA imaging probes. Chem A Eur J 20(43):14004–14011

    CAS  Google Scholar 

  67. Poynton FE, Bright SA, Blasco S, Williams DC, Kelly JM, Gunnlaugsson T (2017) The development of ruthenium(II) polypyridyl complexes and conjugates for: in vitro cellular and in vivo applications. Chem Soc Rev 46(24):7706–7756

    CAS  PubMed  Google Scholar 

  68. Wragg A, Gill MR, Hill CJ, Su X, Meijer AJHM, Smythe C, Thomas JA (2014) Dinuclear osmium(II) probes for high-resolution visualisation of cellular DNA structure using Electron microscopy. Chem Commun 50(93):14494–14497

    CAS  Google Scholar 

  69. Niyazi H, Hall JP, O’Sullivan K, Winter G, Sorensen T, Kelly JM, Cardin CJ (2012) Crystal structures of Λ-[Ru(Phen)2dppz]2+ with oligonucleotides containing TA/TA and AT/AT steps show two intercalation modes. Nat Chem 4(8):621–628

    CAS  PubMed  Google Scholar 

  70. Keane PM, Poynton FE, Hall JP, Sazanovich IV, Towrie M, Gunnlaugsson T, Quinn SJ, Cardin CJ, Kelly JM (2015) Reversal of a single base-pair step controls guanine photo-oxidation by an intercalating ruthenium(II) dipyridophenazine complex. Angew Chem Int Ed 54(29):8364–8368

    CAS  Google Scholar 

  71. Hall JP, Cook D, Morte SR, McIntyre P, Buchner K, Beer H, Cardin DJ, Brazier JA, Winter G, Kelly JM et al (2013) X-ray crystal structure of Rac- [Ru(Phen) 2 Dppz] 2+ with d(ATGCAT) 2 shows enantiomer orientations and water ordering. J Am Chem Soc 135(34):12652–12659

    CAS  PubMed  Google Scholar 

  72. McQuaid K, Hall JP, Brazier JA, Cardin DJ, Cardin CJ (2018) X-ray crystal structures show DNA stacking advantage of terminal nitrile substitution in Ru-Dppz complexes. Chemistry 24(59):15859–15867

    CAS  PubMed  Google Scholar 

  73. Gill MR, Garcia-Lara J, Foster SJ, Smythe C, Battaglia G, Thomas JA (2009) A ruthenium(II) polypyridyl complex for direct imaging of DNA structure in living cells. Nat Chem 1(8):662–667

    CAS  PubMed  Google Scholar 

  74. Łęczkowska A, Gonzalez-Garcia J, Perez-Arnaiz C, Garcia B, White AJP, Vilar R (2018) Binding studies of metal–salphen and metal–bipyridine complexes towards G-quadruplex DNA. Chemistry 24(45):11785–11794

    PubMed  Google Scholar 

  75. Ang DL, Harper BWJ, Cubo L, Mendoza O, Vilar R, Aldrich-Wright J (2016) Quadruplex DNA-stabilising dinuclear platinum(II) terpyridine complexes with flexible linkers. Chemistry 22(7):2317–2325

    CAS  PubMed  Google Scholar 

  76. Bazzicalupi C, Ferraroni M, Papi F, Massai L, Bertrand B, Messori L, Gratteri P, Casini A (2016) Determinants for tight and selective binding of a medicinal dicarbene gold(I) complex to a telomeric DNA G-quadruplex: a joint ESI MS and XRD investigation. Angew Chem Int Ed 55(13):4256–4259

    CAS  Google Scholar 

  77. Vilar R (2018) Nucleic acid quadruplexes and metallo-drugs. Metallo-drugs: development and action of anticancer agents. De Gruyter, Berlin, pp 325–350

    Google Scholar 

  78. McQuaid K, Abell H, Gurung SP, Allan D, Winter G, Sorensen T, Cardin DJ, Brazier JA, Cardin CJ, Hall JP (2019) Structural studies reveal the enantiospecific recognition of a DNA G-quadruplex by a ruthenium polypyridyl complex. Angew Chem Int Ed. https://doi.org/10.1002/anie.201814502. [Epub ahead of print]

    CAS  PubMed  Google Scholar 

  79. Wachter E, Moyá D, Parkin S, Glazer EC (2016) Ruthenium complex “Light Switches” that are selective for different G-quadruplex structures. Chemistry 22(2):550–559

    CAS  PubMed  Google Scholar 

  80. Brodersen DE, Clemons WM, Carter AP, Wimberly BT, Ramakrishnan V (2003) Phasing the 30S ribosomal subunit structure. Acta Crystallogr D Biol Crystallogr 59(11):2044–2050

    CAS  PubMed  Google Scholar 

  81. Ramakrishnan V (2002) Ribosome structure and the mechanism of translation. Cell 108(4):557–572

    CAS  PubMed  Google Scholar 

  82. Berger I, Kang C, Sinha ND, Wolters M, Rich A (1996) A highly efficient 24-condition matrix for the crystallization of nucleic acid fragments. Acta Crystallogr D Biol Crystallogr 52:465–468

    CAS  PubMed  Google Scholar 

  83. Viladoms J, Parkinson GN (2014) HELIX: a new modular nucleic acid crystallization screen. J Appl Cryst 47(3):948–955

    CAS  Google Scholar 

  84. Leal RMF, Callow S, Callow P, Blakeley MP, Cardin CJ, Denny WA, Teixeira SCM, Mitchell EP, Forsyth VT (2010) Combined neutron and X-ray diffraction studies of DNA in crystals and solutions. Acta Crystallogr D Biol Crystallogr 66(11):1244–1248

    CAS  PubMed  Google Scholar 

  85. Keane P, Hall J, Poynton F, Poulsen B, Gurung S, Clark I, Sazanovich I, Towrie M, Gunnlaugsson T, Quinn S et al (2017) Inosine can increase DNA’s susceptibility to photo-oxidation by a Ru(II) complex due to structural change in the minor groove. Chemistry 23(43):10344–10351

    CAS  PubMed  Google Scholar 

  86. Chiu TK, Dickerson RE (2000) 1 Å crystal structures of B-DNA reveal sequence-specific binding and groove-specific bending of DNA by magnesium and calcium. J Mol Biol 301(4):915–945

    CAS  PubMed  Google Scholar 

  87. Leal RMF, Teixeira SCM, Blakeley MP, Mitchell EP, Forsyth VT (2009) A preliminary neutron crystallographic study of an A-DNA crystal. Acta Crystallogr Sect F Struct Biol Cryst Commun 65(Pt 3):232–235

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Thorpe JH, Teixeira SCM, Gale BC, Cardin CJ (2003) Crystal structure of the complementary quadruplex formed by d(GCATGCT) at atomic resolution. Nucleic Acids Res 31(3):844–849

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Leonard GA, Zhang S, Peterson MR, Harrop SJ, Helliwell JR, Cruse WB, Langlois d’Estaintot B, Kennard O, Brown T, Hunter WN (1995) Self-association of a DNA loop creates a quadruplex: crystal structure of d(GCATGCT) at 1.8 å resolution. Structure 3(4):335–340

    CAS  PubMed  Google Scholar 

  90. Gan Y, Thorpe JH, Teixeira SCM, Naseer A, Cardin CJ. Calcium and the DNA quadruplex structure formed by d(GCATGCT). https://www.rcsb.org/structure/3T86. Accessed 1 May 2019

  91. Cardin CJ, Gan Y, Thorpe JH, Teixeira SCM, Gale BC, Moraes MIA. Barium and the DNA quadruplex structure formed by d(GCATGCT). http://www.rcsb.org/structure/1QYK. Accessed 1 May 2019

  92. Cardin CJ, Gan Y, Thorpe JH, Teixeira SCM, Gale BC, Moraes MIA. Vanadium and the DNA quadruplex structure formed by d(GCATGCT). http://www.rcsb.org/structure/1QYL. Accessed 1 May 2019

  93. Cardin CJ, Gan Y, Thorpe JH, Teixeira SCM, Gale BC, Moraes MIA. Cobalt and the DNA quadruplex structure formed by d(GCATGCT). http://www.rcsb.org/structure/1QZL

  94. Cardin CJ, Gan Y, Thorpe JH, Teixeira SCM, Gale BC, Moraes MIA. Nickel and the DNA quadruplex structure formed by d(GCATGCT). http://www.rcsb.org/structure/1R2O. Accessed 1 May 2019

  95. Nakano M, Tateishi-Karimata H, Tanaka S, Tama F, Miyashita O, Nakano SI, Sugimoto N (2015) Thermodynamic properties of water molecules in the presence of Cosolute depend on DNA structure: a study using grid inhomogeneous solvation theory. Nucleic Acids Res 43(21):10114–10125

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AGW, McCoy A et al (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. Sect. D Biol. Crystallogr. 67(4):235–242

    CAS  Google Scholar 

  97. Taylor GL (2010) Introduction to phasing. Acta Crystallogr D Biol Crystallogr 66(4):325–338

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Todd AK, Adams A, Powell HR, Wilcock DJ, Thorpe JH, Lausi A, Zanini F, Wakelin LPG, Cardin CJ (1999) Determination by MAD-DM of the structure of the DNA duplex d[ACGTACG(5-BrU)]2 at 1.46 Å and 100 K. Acta Crystallogr D Biol Crystallogr 55(Pt 4):729–735

    CAS  PubMed  Google Scholar 

  99. Todd AK, Adams A, Thorpe JH, Denny WA, Wakelin LPG, Cardin CJ (1999) Major groove binding and ‘DNA-induced’ fit in the intercalation of a derivative of the mixed topoisomerase I/II poison N-(2(dimethylamino)ethyl)acridine-4-carboxamide (DACA) into DNA: X-ray structure complexed to d(CG(5-BrU)ACG)2 at 1.3-Å resolution. J Med Chem 42(4):536–540

    CAS  PubMed  Google Scholar 

  100. Hall JP, Gurung SP, Henle J, Poidl P, Andersson J, Lincoln P, Winter G, Sorensen T, Cardin DJ, Brazier JA et al (2017) Guanine can direct binding specificity of Ru–dipyridophenazine (Dppz) complexes to DNA through steric effects. Chemistry 23(21):4981–4985

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Sheldrick GM (2010) Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr D Biol Crystallogr 66(4):479–485

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Parkhurst JM, Winter G, Waterman DG, Fuentes-Montero L, Gildea RJ, Murshudov GN, Evans G (2016) Robust background modelling in DIALS. J Appl Cryst 49(6):1912–1921

    CAS  Google Scholar 

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Acknowledgements

Many thanks to Kane McQuaid, Jim Thorpe, Susy Teixeira, Andrew Kellett and David Cardin for kindly reading, commenting on and improving the manuscript. Thanks also to the many students and coworkers for so much inspiration over the years; I have aimed to cite as many of you as possible, as there are too many to name here. I very much appreciate the financial support given to our work by BBSRC, EPSRC, the Royal Society, Diamond Light Source and the University of Reading.

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Correspondence to Christine J. Cardin .

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Cardin, C.J. (2019). Interactions Between Metal Ions and DNA. In: Mingos, D. (eds) The Periodic Table II. Structure and Bonding, vol 182. Springer, Cham. https://doi.org/10.1007/430_2019_42

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