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. 1994 Jun 15;13(12):2737–2746. doi: 10.1002/j.1460-2075.1994.tb06567.x

DNA self-fitting: the double helix directs the geometry of its supramolecular assembly.

Y Timsit 1, D Moras 1
PMCID: PMC395153  PMID: 8026458

Abstract

Groove-backbone interaction is a natural and biologically relevant mechanism for the specific assembly of B-DNA double helices. Crystal engineering and crystal packing analysis of oligonucleotides of different sizes and sequences reveal that the sequence-dependent self-fitting of B-DNA helices is a dominant constraint for their ordered assembly. It can override the other intermolecular interactions and impose the overall geometry of the packing. Analysis of experimental examples of architectural motifs formed by the geometric combination of self-fitted DNA segments leads to general rules for DNA assembly. Like a directing piece for a supramolecular 'construction set', the double helix imposes a limited number of geometric solutions. These basic architectural constraints could direct, in a codified manner, the formation of higher-order structures. DNA architectural motifs exhibit new structural and electrostatic properties which could have some implications for their molecular recognition by proteins acting on DNA.

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Selected References

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

  1. Adachi Y., Luke M., Laemmli U. K. Chromosome assembly in vitro: topoisomerase II is required for condensation. Cell. 1991 Jan 11;64(1):137–148. doi: 10.1016/0092-8674(91)90215-k. [DOI] [PubMed] [Google Scholar]
  2. Adrian M., ten Heggeler-Bordier B., Wahli W., Stasiak A. Z., Stasiak A., Dubochet J. Direct visualization of supercoiled DNA molecules in solution. EMBO J. 1990 Dec;9(13):4551–4554. doi: 10.1002/j.1460-2075.1990.tb07907.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arnott S., Hukins D. W. Optimised parameters for A-DNA and B-DNA. Biochem Biophys Res Commun. 1972 Jun 28;47(6):1504–1509. doi: 10.1016/0006-291X(72)90243-4. [DOI] [PubMed] [Google Scholar]
  4. Bhattacharyya A., Murchie A. I., von Kitzing E., Diekmann S., Kemper B., Lilley D. M. Model for the interaction of DNA junctions and resolving enzymes. J Mol Biol. 1991 Oct 20;221(4):1191–1207. doi: 10.1016/0022-2836(91)90928-y. [DOI] [PubMed] [Google Scholar]
  5. Bordas J., Perez-Grau L., Koch M. H., Vega M. C., Nave C. The superstructure of chromatin and its condensation mechanism. II. Theoretical analysis of the X-ray scattering patterns and model calculations. Eur Biophys J. 1986;13(3):175–185. doi: 10.1007/BF00542561. [DOI] [PubMed] [Google Scholar]
  6. Butler P. J. A defined structure of the 30 nm chromatin fibre which accommodates different nucleosomal repeat lengths. EMBO J. 1984 Nov;3(11):2599–2604. doi: 10.1002/j.1460-2075.1984.tb02180.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Echols H. Nucleoprotein structures initiating DNA replication, transcription, and site-specific recombination. J Biol Chem. 1990 Sep 5;265(25):14697–14700. [PubMed] [Google Scholar]
  8. Fairall L., Finch J. T. Single crystals of long DNA molecules. J Biomol Struct Dyn. 1992 Feb;9(4):633–642. doi: 10.1080/07391102.1992.10507944. [DOI] [PubMed] [Google Scholar]
  9. Filipski J., Leblanc J., Youdale T., Sikorska M., Walker P. R. Periodicity of DNA folding in higher order chromatin structures. EMBO J. 1990 Apr;9(4):1319–1327. doi: 10.1002/j.1460-2075.1990.tb08241.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Finch J. T., Klug A. Solenoidal model for superstructure in chromatin. Proc Natl Acad Sci U S A. 1976 Jun;73(6):1897–1901. doi: 10.1073/pnas.73.6.1897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hansen J. C., Ausio J. Chromatin dynamics and the modulation of genetic activity. Trends Biochem Sci. 1992 May;17(5):187–191. doi: 10.1016/0968-0004(92)90264-a. [DOI] [PubMed] [Google Scholar]
  12. Hansen J. C., Ausio J., Stanik V. H., van Holde K. E. Homogeneous reconstituted oligonucleosomes, evidence for salt-dependent folding in the absence of histone H1. Biochemistry. 1989 Nov 14;28(23):9129–9136. doi: 10.1021/bi00449a026. [DOI] [PubMed] [Google Scholar]
  13. Heichman K. A., Johnson R. C. The Hin invertasome: protein-mediated joining of distant recombination sites at the enhancer. Science. 1990 Aug 3;249(4968):511–517. doi: 10.1126/science.2166334. [DOI] [PubMed] [Google Scholar]
  14. Heinemann U., Alings C., Bansal M. Double helix conformation, groove dimensions and ligand binding potential of a G/C stretch in B-DNA. EMBO J. 1992 May;11(5):1931–1939. doi: 10.1002/j.1460-2075.1992.tb05246.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kanaar R., Klippel A., Shekhtman E., Dungan J. M., Kahmann R., Cozzarelli N. R. Processive recombination by the phage Mu Gin system: implications for the mechanisms of DNA strand exchange, DNA site alignment, and enhancer action. Cell. 1990 Jul 27;62(2):353–366. doi: 10.1016/0092-8674(90)90372-l. [DOI] [PubMed] [Google Scholar]
  16. Koch M. H., Sayers Z., Michon A. M., Sicre P., Marquet R., Houssier C. The superstructure of chromatin and its condensation mechanism. VI. Electric dichroism and model calculations. Eur Biophys J. 1989;17(5):245–255. doi: 10.1007/BF00254282. [DOI] [PubMed] [Google Scholar]
  17. Kornberg R. D., Lorch Y. Irresistible force meets immovable object: transcription and the nucleosome. Cell. 1991 Nov 29;67(5):833–836. doi: 10.1016/0092-8674(91)90354-2. [DOI] [PubMed] [Google Scholar]
  18. Kubista M., Hagmar P., Nielsen P. E., Nordén B. Reinterpretation of linear dichroism of chromatin supports a perpendicular linker orientation in the folded state. J Biomol Struct Dyn. 1990 Aug;8(1):37–54. doi: 10.1080/07391102.1990.10507788. [DOI] [PubMed] [Google Scholar]
  19. Käs E., Laemmli U. K. In vivo topoisomerase II cleavage of the Drosophila histone and satellite III repeats: DNA sequence and structural characteristics. EMBO J. 1992 Feb;11(2):705–716. doi: 10.1002/j.1460-2075.1992.tb05103.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lilley D. M. DNA--protein interactions. HMG has DNA wrapped up. Nature. 1992 May 28;357(6376):282–283. doi: 10.1038/357282a0. [DOI] [PubMed] [Google Scholar]
  21. Lipanov A., Kopka M. L., Kaczor-Grzeskowiak M., Quintana J., Dickerson R. E. Structure of the B-DNA decamer C-C-A-A-C-I-T-T-G-G in two different space groups: conformational flexibility of B-DNA. Biochemistry. 1993 Feb 9;32(5):1373–1389. doi: 10.1021/bi00056a024. [DOI] [PubMed] [Google Scholar]
  22. Marquet R., Colson P., Houssier C. The condensation of chromatin and histone H1-depleted chromatin by spermine. J Biomol Struct Dyn. 1986 Oct;4(2):205–218. doi: 10.1080/07391102.1986.10506340. [DOI] [PubMed] [Google Scholar]
  23. Mizuuchi M., Baker T. A., Mizuuchi K. Assembly of the active form of the transposase-Mu DNA complex: a critical control point in Mu transposition. Cell. 1992 Jul 24;70(2):303–311. doi: 10.1016/0092-8674(92)90104-k. [DOI] [PubMed] [Google Scholar]
  24. Nash H. A. Bending and supercoiling of DNA at the attachment site of bacteriophage lambda. Trends Biochem Sci. 1990 Jun;15(6):222–227. doi: 10.1016/0968-0004(90)90034-9. [DOI] [PubMed] [Google Scholar]
  25. Parker C. N., Halford S. E. Dynamics of long-range interactions on DNA: the speed of synapsis during site-specific recombination by resolvase. Cell. 1991 Aug 23;66(4):781–791. doi: 10.1016/0092-8674(91)90121-e. [DOI] [PubMed] [Google Scholar]
  26. Pruss G. J., Drlica K. DNA supercoiling and prokaryotic transcription. Cell. 1989 Feb 24;56(4):521–523. doi: 10.1016/0092-8674(89)90574-6. [DOI] [PubMed] [Google Scholar]
  27. Roca J., Wang J. C. The capture of a DNA double helix by an ATP-dependent protein clamp: a key step in DNA transport by type II DNA topoisomerases. Cell. 1992 Nov 27;71(5):833–840. doi: 10.1016/0092-8674(92)90558-t. [DOI] [PubMed] [Google Scholar]
  28. Sen D., Mitra S., Crothers D. M. Higher order structure of chromatin: evidence from photochemically detected linear dichroism. Biochemistry. 1986 Jun 3;25(11):3441–3447. doi: 10.1021/bi00359a052. [DOI] [PubMed] [Google Scholar]
  29. Shakked Z., Guzikevich-Guerstein G., Frolow F., Rabinovich D., Joachimiak A., Sigler P. B. Determinants of repressor/operator recognition from the structure of the trp operator binding site. Nature. 1994 Mar 31;368(6470):469–473. doi: 10.1038/368469a0. [DOI] [PubMed] [Google Scholar]
  30. Shaw S. Y., Wang J. C. Knotting of a DNA chain during ring closure. Science. 1993 Apr 23;260(5107):533–536. doi: 10.1126/science.8475384. [DOI] [PubMed] [Google Scholar]
  31. Sikorav J. L., Church G. M. Complementary recognition in condensed DNA: accelerated DNA renaturation. J Mol Biol. 1991 Dec 20;222(4):1085–1108. doi: 10.1016/0022-2836(91)90595-w. [DOI] [PubMed] [Google Scholar]
  32. Stark W. M., Boocock M. R., Sherratt D. J. Site-specific recombination by Tn3 resolvase. Trends Genet. 1989 Sep;5(9):304–309. doi: 10.1016/0168-9525(89)90113-3. [DOI] [PubMed] [Google Scholar]
  33. Surette M. G., Chaconas G. The Mu transpositional enhancer can function in trans: requirement of the enhancer for synapsis but not strand cleavage. Cell. 1992 Mar 20;68(6):1101–1108. doi: 10.1016/0092-8674(92)90081-m. [DOI] [PubMed] [Google Scholar]
  34. Svaren J., Chalkley R. The structure and assembly of active chromatin. Trends Genet. 1990 Feb;6(2):52–56. doi: 10.1016/0168-9525(90)90074-g. [DOI] [PubMed] [Google Scholar]
  35. Timsit Y., Moras D. Groove-backbone interaction in B-DNA. Implication for DNA condensation and recombination. J Mol Biol. 1991 Oct 5;221(3):919–940. doi: 10.1016/0022-2836(91)80184-v. [DOI] [PubMed] [Google Scholar]
  36. Timsit Y., Vilbois E., Moras D. Base-pairing shift in the major groove of (CA)n tracts by B-DNA crystal structures. Nature. 1991 Nov 14;354(6349):167–170. doi: 10.1038/354167a0. [DOI] [PubMed] [Google Scholar]
  37. Timsit Y., Westhof E., Fuchs R. P., Moras D. Unusual helical packing in crystals of DNA bearing a mutation hot spot. Nature. 1989 Oct 5;341(6241):459–462. doi: 10.1038/341459a0. [DOI] [PubMed] [Google Scholar]
  38. Wasserman S. A., Cozzarelli N. R. Biochemical topology: applications to DNA recombination and replication. Science. 1986 May 23;232(4753):951–960. doi: 10.1126/science.3010458. [DOI] [PubMed] [Google Scholar]
  39. Westhof E., Dumas P., Moras D. Crystallographic refinement of yeast aspartic acid transfer RNA. J Mol Biol. 1985 Jul 5;184(1):119–145. doi: 10.1016/0022-2836(85)90048-8. [DOI] [PubMed] [Google Scholar]
  40. Widom J., Klug A. Structure of the 300A chromatin filament: X-ray diffraction from oriented samples. Cell. 1985 Nov;43(1):207–213. doi: 10.1016/0092-8674(85)90025-x. [DOI] [PubMed] [Google Scholar]
  41. Widom J. Physicochemical studies of the folding of the 100 A nucleosome filament into the 300 A filament. Cation dependence. J Mol Biol. 1986 Aug 5;190(3):411–424. doi: 10.1016/0022-2836(86)90012-4. [DOI] [PubMed] [Google Scholar]
  42. Widom J. Toward a unified model of chromatin folding. Annu Rev Biophys Biophys Chem. 1989;18:365–395. doi: 10.1146/annurev.bb.18.060189.002053. [DOI] [PubMed] [Google Scholar]
  43. Yao J., Lowary P. T., Widom J. Linker DNA bending induced by the core histones of chromatin. Biochemistry. 1991 Aug 27;30(34):8408–8414. doi: 10.1021/bi00098a019. [DOI] [PubMed] [Google Scholar]
  44. Zechiedrich E. L., Osheroff N. Eukaryotic topoisomerases recognize nucleic acid topology by preferentially interacting with DNA crossovers. EMBO J. 1990 Dec;9(13):4555–4562. doi: 10.1002/j.1460-2075.1990.tb07908.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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