Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1993 Dec;65(6):2291–2303. doi: 10.1016/S0006-3495(93)81306-7

A systematic method for studying the spatial distribution of water molecules around nucleic acid bases.

B Schneider 1, D M Cohen 1, L Schleifer 1, A R Srinivasan 1, W K Olson 1, H M Berman 1
PMCID: PMC1225971  PMID: 8312469

Abstract

A new method to analyze the distribution of water molecules around the bases in DNA is presented. This method relies on the notion of a "hydrated building block," which represents the joint observed hydration around all bases of a particular type, in structures of a particular conformation type. The hydrated building blocks were constructed using atomic coordinates from 40 structures contained in the Nucleic Acid Database. Pseudoelectron densities were calculated for water molecules in each hydrated building block using standard crystallographic procedures. The electron densities were fitted to obtain "average building blocks," which represent bases with waters only at average or probable positions. Both types of building blocks were used to construct models of hydrated DNA oligomers. The essential features of the solvent structure around d(CGCGAATTCGCG)2 in the B form and d(CGCGCG)2 in the Z form were reproduced.

Full text

PDF
2291

Images in this article

2299FIGURE 4
on p.2299
2300FIGURE 5
on p.2300

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Berman H. M., Olson W. K., Beveridge D. L., Westbrook J., Gelbin A., Demeny T., Hsieh S. H., Srinivasan A. R., Schneider B. The nucleic acid database. A comprehensive relational database of three-dimensional structures of nucleic acids. Biophys J. 1992 Sep;63(3):751–759. doi: 10.1016/S0006-3495(92)81649-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berman H. M., Sowri A., Ginell S., Beveridge D. A systematic study of patterns of hydration in nucleic acids:(I) guanine and cytosine. J Biomol Struct Dyn. 1988 Apr;5(5):1101–1110. doi: 10.1080/07391102.1988.10506451. [DOI] [PubMed] [Google Scholar]
  3. Chevrier B., Dock A. C., Hartmann B., Leng M., Moras D., Thuong M. T., Westhof E. Solvation of the left-handed hexamer d(5BrC-G-5BrC-G-5 BrC-G) in crystals grown at two temperatures. J Mol Biol. 1986 Apr 20;188(4):707–719. doi: 10.1016/s0022-2836(86)80016-x. [DOI] [PubMed] [Google Scholar]
  4. Cohen D., Kulikowski C., Berman H. Knowledge-based generation of machine learning experiments: learning with DNA crystallography data. Proc Int Conf Intell Syst Mol Biol. 1993;1:92–100. [PubMed] [Google Scholar]
  5. Coll M., Saal D., Frederick C. A., Aymami J., Rich A., Wang A. H. Effects of 5-fluorouracil/guanine wobble base pairs in Z-DNA: molecular and crystal structure of d(CGCGFG). Nucleic Acids Res. 1989 Feb 11;17(3):911–923. doi: 10.1093/nar/17.3.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coll M., Wang A. H., van der Marel G. A., van Boom J. H., Rich A. Crystal structure of a Z-DNA fragment containing thymine/2-aminoadenine base pairs. J Biomol Struct Dyn. 1986 Oct;4(2):157–172. doi: 10.1080/07391102.1986.10506337. [DOI] [PubMed] [Google Scholar]
  7. Conner B. N., Yoon C., Dickerson J. L., Dickerson R. E. Helix geometry and hydration in an A-DNA tetramer: IC-C-G-G. J Mol Biol. 1984 Apr 25;174(4):663–695. doi: 10.1016/0022-2836(84)90089-5. [DOI] [PubMed] [Google Scholar]
  8. DiGabriele A. D., Sanderson M. R., Steitz T. A. Crystal lattice packing is important in determining the bend of a DNA dodecamer containing an adenine tract. Proc Natl Acad Sci U S A. 1989 Mar;86(6):1816–1820. doi: 10.1073/pnas.86.6.1816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Drew H. R., Dickerson R. E. Structure of a B-DNA dodecamer. III. Geometry of hydration. J Mol Biol. 1981 Sep 25;151(3):535–556. doi: 10.1016/0022-2836(81)90009-7. [DOI] [PubMed] [Google Scholar]
  10. Drew H. R., Samson S., Dickerson R. E. Structure of a B-DNA dodecamer at 16 K. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4040–4044. doi: 10.1073/pnas.79.13.4040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Drew H. R., Wing R. M., Takano T., Broka C., Tanaka S., Itakura K., Dickerson R. E. Structure of a B-DNA dodecamer: conformation and dynamics. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2179–2183. doi: 10.1073/pnas.78.4.2179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Egli M., Williams L. D., Gao Q., Rich A. Structure of the pure-spermine form of Z-DNA (magnesium free) at 1-A resolution. Biochemistry. 1991 Dec 3;30(48):11388–11402. doi: 10.1021/bi00112a005. [DOI] [PubMed] [Google Scholar]
  13. Fratini A. V., Kopka M. L., Drew H. R., Dickerson R. E. Reversible bending and helix geometry in a B-DNA dodecamer: CGCGAATTBrCGCG. J Biol Chem. 1982 Dec 25;257(24):14686–14707. [PubMed] [Google Scholar]
  14. Frederick C. A., Quigley G. J., Teng M. K., Coll M., Van der Marel G. A., Van Boom J. H., Rich A., Wang A. H. Molecular structure of an A-DNA decamer d(ACCGGCCGGT). Eur J Biochem. 1989 May 1;181(2):295–307. doi: 10.1111/j.1432-1033.1989.tb14724.x. [DOI] [PubMed] [Google Scholar]
  15. Frederick C. A., Quigley G. J., van der Marel G. A., van Boom J. H., Wang A. H., Rich A. Methylation of the EcoRI recognition site does not alter DNA conformation: the crystal structure of d(CGCGAm6ATTCGCG) at 2.0-A resolution. J Biol Chem. 1988 Nov 25;263(33):17872–17879. doi: 10.2210/pdb4dnb/pdb. [DOI] [PubMed] [Google Scholar]
  16. Geierstanger B. H., Kagawa T. F., Chen S. L., Quigley G. J., Ho P. S. Base-specific binding of copper(II) to Z-DNA. The 1.3-A single crystal structure of d(m5CGUAm5CG) in the presence of CuCl2. J Biol Chem. 1991 Oct 25;266(30):20185–20191. doi: 10.2210/pdb1d40/pdb. [DOI] [PubMed] [Google Scholar]
  17. Gessner R. V., Frederick C. A., Quigley G. J., Rich A., Wang A. H. The molecular structure of the left-handed Z-DNA double helix at 1.0-A atomic resolution. Geometry, conformation, and ionic interactions of d(CGCGCG). J Biol Chem. 1989 May 15;264(14):7921–7935. doi: 10.2210/pdb1dcg/pdb. [DOI] [PubMed] [Google Scholar]
  18. Ginell S. L., Kuzmich S., Jones R. A., Berman H. M. Crystal and molecular structure of a DNA duplex containing the carcinogenic lesion O6-methylguanine. Biochemistry. 1990 Nov 20;29(46):10461–10465. doi: 10.1021/bi00498a005. [DOI] [PubMed] [Google Scholar]
  19. Grzeskowiak K., Yanagi K., Privé G. G., Dickerson R. E. The structure of B-helical C-G-A-T-C-G-A-T-C-G and comparison with C-C-A-A-C-G-T-T-G-G. The effect of base pair reversals. J Biol Chem. 1991 May 15;266(14):8861–8883. doi: 10.2210/pdb1d23/pdb. [DOI] [PubMed] [Google Scholar]
  20. Han F., Watt W., Duchamp D. J., Callahan L., Kézdy F. J., Agarwal K. Molecular structure of deoxycytidyl-3'-methylphosphonate (RP) 5'-deoxyguanidine, d[Cp(CH3)G]. A neutral dinucleotide with Watson-Crick base pairing and a right handed helical twist. Nucleic Acids Res. 1990 May 11;18(9):2759–2767. doi: 10.1093/nar/18.9.2759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Heinemann U., Alings C. Crystallographic study of one turn of G/C-rich B-DNA. J Mol Biol. 1989 Nov 20;210(2):369–381. doi: 10.1016/0022-2836(89)90337-9. [DOI] [PubMed] [Google Scholar]
  22. Heinemann U., Hahn M. C-C-A-G-G-C-m5C-T-G-G. Helical fine structure, hydration, and comparison with C-C-A-G-G-C-C-T-G-G. J Biol Chem. 1992 Apr 15;267(11):7332–7341. [PubMed] [Google Scholar]
  23. Heinemann U., Lauble H., Frank R., Blöcker H. Crystal structure analysis of an A-DNA fragment at 1.8 A resolution: d(GCCCGGGC). Nucleic Acids Res. 1987 Nov 25;15(22):9531–9550. doi: 10.1093/nar/15.22.9531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Heinemann U., Rudolph L. N., Alings C., Morr M., Heikens W., Frank R., Blöcker H. Effect of a single 3'-methylene phosphonate linkage on the conformation of an A-DNA octamer double helix. Nucleic Acids Res. 1991 Feb 11;19(3):427–433. doi: 10.1093/nar/19.3.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kagawa T. F., Geierstanger B. H., Wang A. H., Ho P. S. Covalent modification of guanine bases in double-stranded DNA. The 1.2-A Z-DNA structure of d(CGCGCG) in the presence of CuCl2. J Biol Chem. 1991 Oct 25;266(30):20175–20184. doi: 10.2210/pdb1d39/pdb. [DOI] [PubMed] [Google Scholar]
  26. Kennard O., Cruse W. B., Nachman J., Prange T., Shakked Z., Rabinovich D. Ordered water structure in an A-DNA octamer at 1.7 A resolution. J Biomol Struct Dyn. 1986 Feb;3(4):623–647. doi: 10.1080/07391102.1986.10508452. [DOI] [PubMed] [Google Scholar]
  27. Kopka M. L., Fratini A. V., Drew H. R., Dickerson R. E. Ordered water structure around a B-DNA dodecamer. A quantitative study. J Mol Biol. 1983 Jan 5;163(1):129–146. doi: 10.1016/0022-2836(83)90033-5. [DOI] [PubMed] [Google Scholar]
  28. Langan P., Forsyth V. T., Mahendrasingam A., Pigram W. J., Mason S. A., Fuller W. A high angle neutron fibre diffraction study of the hydration of the A conformation of the DNA double helix. J Biomol Struct Dyn. 1992 Dec;10(3):489–503. doi: 10.1080/07391102.1992.10508664. [DOI] [PubMed] [Google Scholar]
  29. Larsen T. A., Kopka M. L., Dickerson R. E. Crystal structure analysis of the B-DNA dodecamer CGTGAATTCACG. Biochemistry. 1991 May 7;30(18):4443–4449. doi: 10.1021/bi00232a010. [DOI] [PubMed] [Google Scholar]
  30. Lauble H., Frank R., Blöcker H., Heinemann U. Three-dimensional structure of d(GGGATCCC) in the crystalline state. Nucleic Acids Res. 1988 Aug 25;16(16):7799–7816. doi: 10.1093/nar/16.16.7799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lavalle N., Lee S. A., Rupprecht A. Counterion effects on the physical properties and the A to B transition of calf-thymus DNA films. Biopolymers. 1990;30(9-10):877–887. doi: 10.1002/bip.360300903. [DOI] [PubMed] [Google Scholar]
  32. Leonard G. A., Thomson J., Watson W. P., Brown T. High-resolution structure of a mutagenic lesion in DNA. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9573–9576. doi: 10.1073/pnas.87.24.9573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Narayana N., Ginell S. L., Russu I. M., Berman H. M. Crystal and molecular structure of a DNA fragment: d(CGTGAATTCACG). Biochemistry. 1991 May 7;30(18):4449–4455. doi: 10.1021/bi00232a011. [DOI] [PubMed] [Google Scholar]
  34. Neidle S., Berman H. M., Shieh H. S. Highly structured water network in crystals of a deoxydinucleoside---drug complex. Nature. 1980 Nov 13;288(5787):129–133. doi: 10.1038/288129a0. [DOI] [PubMed] [Google Scholar]
  35. Privé G. G., Heinemann U., Chandrasegaran S., Kan L. S., Kopka M. L., Dickerson R. E. Helix geometry, hydration, and G.A mismatch in a B-DNA decamer. Science. 1987 Oct 23;238(4826):498–504. doi: 10.1126/science.3310237. [DOI] [PubMed] [Google Scholar]
  36. Privé G. G., Yanagi K., Dickerson R. E. Structure of the B-DNA decamer C-C-A-A-C-G-T-T-G-G and comparison with isomorphous decamers C-C-A-A-G-A-T-T-G-G and C-C-A-G-G-C-C-T-G-G. J Mol Biol. 1991 Jan 5;217(1):177–199. doi: 10.1016/0022-2836(91)90619-h. [DOI] [PubMed] [Google Scholar]
  37. Quintana J. R., Grzeskowiak K., Yanagi K., Dickerson R. E. Structure of a B-DNA decamer with a central T-A step: C-G-A-T-T-A-A-T-C-G. J Mol Biol. 1992 May 20;225(2):379–395. doi: 10.1016/0022-2836(92)90928-d. [DOI] [PubMed] [Google Scholar]
  38. Ramakrishnan B., Viswamitra M. A. Crystal and molecular structure of the ammonium salt of the dinucleoside monophosphate d(CpG). J Biomol Struct Dyn. 1988 Dec;6(3):511–523. doi: 10.1080/07391102.1988.10506504. [DOI] [PubMed] [Google Scholar]
  39. Schneider B., Cohen D., Berman H. M. Hydration of DNA bases: analysis of crystallographic data. Biopolymers. 1992 Jul;32(7):725–750. doi: 10.1002/bip.360320703. [DOI] [PubMed] [Google Scholar]
  40. Schneider B., Ginell S. L., Jones R., Gaffney B., Berman H. M. Crystal and molecular structure of a DNA fragment containing a 2-aminoadenine modification: the relationship between conformation, packing, and hydration in Z-DNA hexamers. Biochemistry. 1992 Oct 13;31(40):9622–9628. doi: 10.1021/bi00155a014. [DOI] [PubMed] [Google Scholar]
  41. Seeman N. C., Rosenberg J. M., Rich A. Sequence-specific recognition of double helical nucleic acids by proteins. Proc Natl Acad Sci U S A. 1976 Mar;73(3):804–808. doi: 10.1073/pnas.73.3.804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Takusagawa F. The crystal structure of d(GTACGTAC) at 2.25 A resolution: are the A-DNA's always unwound approximately 10 degrees at the C-G steps? J Biomol Struct Dyn. 1990 Feb;7(4):795–809. doi: 10.1080/07391102.1990.10508524. [DOI] [PubMed] [Google Scholar]
  43. Unis M. J., Hearst J. E. On the hydration of DNA. II. Base composition dependence of the net hydration of DNA. Biopolymers. 1968;6(9):1345–1353. doi: 10.1002/bip.1968.360060909. [DOI] [PubMed] [Google Scholar]
  44. Verdaguer N., Aymami J., Fernández-Forner D., Fita I., Coll M., Huynh-Dinh T., Igolen J., Subirana J. A. Molecular structure of a complete turn of A-DNA. J Mol Biol. 1991 Sep 20;221(2):623–635. doi: 10.1016/0022-2836(91)80077-8. [DOI] [PubMed] [Google Scholar]
  45. Wang A. H., Quigley G. J., Kolpak F. J., Crawford J. L., van Boom J. H., van der Marel G., Rich A. Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature. 1979 Dec 13;282(5740):680–686. doi: 10.1038/282680a0. [DOI] [PubMed] [Google Scholar]
  46. Webster G. D., Sanderson M. R., Skelly J. V., Neidle S., Swann P. F., Li B. F., Tickle I. J. Crystal structure and sequence-dependent conformation of the A.G mispaired oligonucleotide d(CGCAAGCTGGCG). Proc Natl Acad Sci U S A. 1990 Sep;87(17):6693–6697. doi: 10.1073/pnas.87.17.6693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Westhof E. Re-refinement of the B-dodecamer d(CGCGAATTCGCG) with a comparative analysis of the solvent in it and in the Z-hexamer d(5BrCG5BrCG5BrCG). J Biomol Struct Dyn. 1987 Dec;5(3):581–600. doi: 10.1080/07391102.1987.10506414. [DOI] [PubMed] [Google Scholar]
  48. Yoon C., Privé G. G., Goodsell D. S., Dickerson R. E. Structure of an alternating-B DNA helix and its relationship to A-tract DNA. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6332–6336. doi: 10.1073/pnas.85.17.6332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Zhou G. W., Ho P. S. Stabilization of Z-DNA by demethylation of thymine bases: 1.3-A single-crystal structure of d(m5CGUAm5CG). Biochemistry. 1990 Aug 7;29(31):7229–7236. doi: 10.1021/bi00483a010. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES