A zipper-like duplex in DNA: The crystal structure of d(GCGAAAGCT) at 2.1 Å resolution

Structure

Volumn 6, Issue 7, 1998, Pages 849-861

  Shepard, William ^a   Cruse, William B T ^b   Fourme, Roger ^a   De La Fortelle, Eric ^c   Prangé, Thierry ^a,b  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b CSSB Chimie Struct Biomoleculaire   (France)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Adenine tract; G A mismatch; Hairpin; MAD; Single stranded DNA; Zipper like DNA

Indexed keywords

EID: 0032528295     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(98)00087-2     Document Type: Article

References (109)

1. Fiddes, J.C., Barrell, B.C. & Godson, G.N. (1978). Nucleotide sequences of the separate origins of synthesis of bacteriophage G4 viral and complementary DNA strands. Proc. Natl Acad. Sci. USA 75, 1081-1085.
2. Sims, J. & Dressier, D. (1978). Site-specific initiation of a DNA fragment: nucleotide sequence of the bacteriophage G4 negative-strand initiation site. Proc. Natl Acad. Sci. USA 75, 3094-3098.
3. Sims, J., Capon, D. & Dressier, D. (1979). DnaG (primase)-dependent origins of DNA replication. Nucleotide sequences of the negative strand initiation sites of bacteriophages St-1, phi K, and alpha 3. J. Biol. Chem. 254, 12615-12628.
4. Astell, C.R.,Smith, M., Chow, M.B. & Ward, D.C. (1979). Structure of the 3' hairpin termini of four rodent parvovirus genomes: nucleotide sequence homology at origins of DNA replication. Cell 17, 691-703.
5. Hirao, I., Ishida, M., Watanabe, K. & Miura, K. (1990). Unique hairpin structures occurring at the replication origin of phage G4 DNA. Biochim. Biophys. Acta 1087, 199-204.
6. Yoshizawa, S., Ueda, T., Ishido, Y., Miura, K., Watanabe, K. & Hirao I. (1994). Nuclease resistance of an extraordinarily thermostable minihairpin DNA fragment, d(GCGAAGC) and its application to in vitro protein synthesis. Nucleic Acids Res. 22, 2217-2221.
7. Hirao, I., Naraoka, T., Kanamori, S., Nakamura, M. & Miura, K. (1988). Synthetic oligodeoxyribonucleotides showing abnormal mobilities on polyacrylamide gel electrophoresis. Biochem. Int. 16, 157-162.
8. Tanikawa, J., Nishimura, Y., Hirao, I. & Miura, K. (1991). NMR spectroscopic study of single-stranded DNA fragments of d(CGGCGAAAGCCG) and d(CGGCAAAAGCCG). Nucleic Acids Symp. Ser. 25, 47-48.
9. Hirao, I., Nishimura, Y., Tagawa, Y., Watanabe, K. & Miura, K. (1992). Extraordinarily stable mini-hairpins: electrophoretical and thermal properties of the various sequence variants of d(GCGAAAGC) and their effect on DNA sequencing. Nucleic Acids Res. 20, 3891-3896.
10. Hirao, I., Nishimura, Y., Naraoka, T., Watanabe, K., Arata, Y. & Miura, K. (1989). Extraordinary stable structure of short single-stranded DNA fragments containing a specific base sequence: d(GCGAAAGC). Nucleic Acid Res. 17, 2223-2231.
11. Woese, C.R., Winker, S. & Gutell, R.R. (1990). Architecture of ribosomal RNA: constraints on the sequence of "tetra-loops". Proc. Natl Acad. Sci. USA 87, 8467-8471.
12. Antao, V.P., Lai, S.Y. & Tinoco, I. Jr (1991). A thermodynamic study of unusually stable RNA and DNA hairpins. Nucleic Acids Res. 19, 5901-5905.
13. Heus, H.A. & Pardi, A. (1991). Structural features that give rise to the unusual stability of RNA hairpins containing GNRA loops. Science 253, 191-194.
14. Jucker, F.M., Heus, H.A., Yip, P.F., Moors, E.H. & Pardi, A. (1996). A network of heterogeneous hydrogen bonds in GNRA tetraloops. J. Mol. Biol. 264, 968-980.
15. Grady, D.L., Ratliff, R.L., Robinson, D.L., McCanlies, E.G., Meyne, J. & Moyzis, R.K. (1992). Highly conserved repetitive DNA sequences are present at human centromeres. Proc. Natl Acad. Sci. USA 89, 1695-1699.
16. Nakaseko, Y., Adachi, Y., Funahashi, S., Niwa, O. & Yanagida, M. (1986). Chromosome walking shows a highly homologous repetitive sequence present in all the centromere regions of fission yeast. EMBO J. 5, 1011-1021.
17. Nakaseko, Y., Kinoshita, N. & Yanagida, M. (1987). A novel sequence common to the centromere regions of Schizosaccharomyces pombe chromosomes. Nucleic Acids Res. 15, 4705-4715.
18. Masumoto, H., Masukata, H., Muro, Y., Nozaki, N. & Okazaki, T. (1989). A human centromere antigen (CENP-B) interacts with a short specific sequence in alphoid DNA, a human centromeric satellite. J. Cell Biol. 109, 1963-1973.
19. Wevrick, R., Earnshaw, W.C., Howard-Peebles, P.N. & Willard, H.F. (1990). Partial deletion of alpha satellite DNA associated with reduced amounts of the centromere protein CENP-B in a mitotically stable human chromosome rearrangement. Mol. Cell Biol. 10, 6374-6380.
20. Willard, H.F. (1990). Centromeres of mammalian chromosomes. Trends Genet. 6, 410-416.
21. Catasti, P., et al., & Bradbury, E.M. (1994). Unusual structures of the tandem repetitive DNA sequences located at human centromeres. Biochemistry 33, 3819-3830.
22. Chou, S.H., Zhu, L. & Reid, B.R. (1994). The unusual structure of the human centromere (GGA)2 motif. Unpaired guanosine residues stacked between sheared GA pairs. J. Mol. Biol. 244, 259-268.
23. Zhu, L., Chou, S.H. & Reid, B.R. (1995). The structure of a novel DNA duplex formed by human centromere d(TGGAA) repeats with possible implications for chromosome attachment during mitosis. J. Mol. Biol. 254, 623-637.
24. Chou, S.H., Zhu, L. & Reid, B.R. (1996). On the relative ability of centromeric GNA triplets to form hairpins versus self-paired duplexes. J. Mol. Biol. 259, 445-457.
25. Gilbert, D.E. & Feigon, J. (1991). Structural analysis of drug-DNA interactions. Curr. Opin. Struct. Biol. 1, 439-445.
26. Cruse, W.B.T., Saludjian, P., Leroux, Y., Léger, G., El Manouni, D. & Prangé, T. (1996). A continuous transition from A to B DNA in the 1:1 complex between nogalamycin and the hexamer dCCCGGG. J. Biol. Chem. 271, 15558-15566.
27. Chou, S.H., Zhu, L & Reid, B.R. (1997). Sheared purine x purine pairing in biology. J. Mol. Biol. 267, 1055-1067.
28. Pley, H.W., Flaherty, K.M. & McKay, D. (1994). The three-dimensional structure of a hammerhead ribozyme. Nature 372, 68-74.
29. Baeyens, K.J., De Bondt, H.L., Pardi, A. & Holbrook, S.R. (1996). A curved RNA helix incorporating an internal loop with G-A and A-A non Watson-Crick base pairing. Proc. Natl Acad. Sci. USA 93, 12851-12855.
30. Li, Y., Zon, G. & Wilson, W.D. (1991). Thermodynamics of DNA duplexes with adjacent GA mismatches. Biochemistry 30, 7566-7572.
31. Aboul-ela, F., Koh, D., Tinoco, I. Jr & Martin, F.H. (1985). Base-base mismatches. Thermodynamics of double helix formation for dCA3XA3G + dCT3YT3G (X, Y = A,C,G,T). Nucleic Acids Res. 13, 4811-4824.
32. Cruse, W.B.T., Saludjian, P., Biala, E., Strazewski, P., Prangé, T. & Kennard, O. (1994). Structure of a mispaired RNA double helix at 1.6 A resolution and implications for the prediction of RNA secondary structure. Proc. Natl Acad. Sci. USA 91, 4160-4164.
33. Zhu, L., Chou, S.H., Xu, J. & Reid, B.R. (1995). Structure of a single-cytidine hairpin loop formed by the DNA triplet GCA. Nat. Struct. Biol. 2, 1012-1017.
34. Gehring, K., Leroy, J.L. & Gueron, M. (1993). A tetrameric DNA structure with protonated cytosine·cytosine base pairs. Nature 363, 561-565.
35. Ahmed, S. & Henderson, E. (1992). Formation of novel hairpin structures by telomeric C-strand oligonucleotides. Nucleic Acids Res. 20, 507-511.
36. Ahmed, S., Kintanar, A. & Henderson, E. (1994). Human telomeric C-strand tetraplexes. Nat. Struct. Biol. 1, 83-88.
37. Chen, L., Cai, L., Zhang, X. & Rich, A. (1994). Crystal structure of a four-stranded intercalated DNA: d(C4). Biochemistry 33, 13540-13546.
38. Kang, C.H., Berger, I., Lockshin, C., Ratliff, R., Moyzis, R. & Rich, A. (1994). Crystal structure of intercalated four-stranded d(C3T) at 1.4 Å resolution. Proc. Natl Acad. Sci. USA 91, 11636-11640.
39. Rohozinski, J., Hancock, J.M. & Keniry, M.A. (1994). Polycytosine regions contained in DNA hairpin loops interact via a four-stranded, parallel structure similar to the i-motif. Nucleic Acids Res. 22, 4653-4659.
40. Kang, C., Berger, I., Lockshin, C., Ratliff, R., Moyzis, R. & Rich, A. (1995). Stable loop in the crystal structure of the intercalated four-stranded cytosine-rich metazoan telomere. Proc. Natl Acad. Sci. USA 92, 3874-3878.
41. Berger, I., Kang, C., Fredian, A., Ratliff, R., Moyzis, R. & Rich, A. (1995). Extension of the four-stranded intercalated cytosine motif by adenine.adenine base pairing in the crystal structure of d(CCCAAT). Nat. Struct. Biol. 2, 416-425.
42. Leroy, J.L. & Gueron, M. (1995). Solution structures of the i-motif tetramers of d(TCC), d(5methylCCT) and d(T5methylCC): novel NOE connections between amino protons and sugar protons. Structure 3, 101-120.
43. 4 tetramer. J. Mol. Biol. 261, 399-414.
44. Nonin, S., Phan, A.T. & Leroy, J.L. (1997). Solution structure and base pair opening kinetics of the i-motif dimer of d(5mCCTTTACC): a noncanonical structure with possible roles in chromosome stability. Structure 5, 1231-1246.
45. Gallego, J., Chou, S.H. & Reid, B.R. (1997). Centromeric pyrimidine strands fold into an intercalated motif by forming a double hairpin with a novel T:G:G:T tetrad: solution structure of the d(TCCCGTTTCCA) dimer. J. Mol. Biol. 273, 840-856.
46. Zimmermann, G.R., Jenison, R.D., Wick, C.L., Simorre, J.P. & Pardi, A. (1997). Interlocking structural motifs mediate molecular discrimination by a theophylline-binding RNA. Nat Struct. Biol. 4, 644-649.
47. Frederick, C.A., Coll, M., van der Marel, GA., van Boom, J.H. & Wang, A.M. (1988). Molecular structure of cyclic deoxydiadenylic acid at atomic resolution. Biochemistry 27, 8350-8361.
48. Guan, Y., Gao, Y.G., Liaw, Y.C., Robinson, H. & Wang, A.H. (1993). Molecular structure of cyclic diguanylic acid at 1 A resolution of two crystal forms: self-association, interactions with metal ion/planar dyes and modeling studies. J. Biomol. Struct. Dyn. 11, 253-276.
49. Wemmer, D.E., Chou, S.H., Hare, D.R. & Reid, B.R. (1985). Duplex-hairpin transitions in DNA: NMR studies on CGCGTATACGCG. Nucleic Acids Res. 13, 3755-3772.
50. 1H-NMR spectroscopy. 2. The hairpin form. Eur. J. Biochem. 163, 287-296.
51. Miller, M., et al., & Sussman, J.L. (1987). Conformational transitions of synthetic DNA sequences with inserted bases, related to the dodecamer d(CGCGAATTCGCG). Nucleic Acids Res. 15, 3877-3890.
52. Hald, M., Pedersen, J.B., Stein, P.C., Kirpekar, F. & Jacobsen, J.P. (1995). A comparison of the hairpin stability of the palindromic d(CGCG(A/T)4CGCG) oligonucleotides. Nucleic Acids Res. 23, 4576-4582.
53. Boulard, Y., et al., & Fazakerley, G.V. (1991). The solution structure of a DNA hairpin containing a loop of three thymidines determined by nuclear magnetic resonance and molecular mechanics. Nucleic Acids Res. 19, 5159-5167.
54. Summers, M.F., Byrd, R.A., Gallo, K.A., Samson, C.J., Zon, G. & Egan, W. (1985). Nuclear magnetic resonance and circular dichroism studies of a duplex-single-stranded hairpin loop equilibrium for the oligodeoxyribonucleotide sequence d(CGCGATTCGCG). Nucleic Acids Res. 13, 6375-6386.
55. Garcia, A.E., Gupta, G., Sarma, M.H. & Sarma, R.H. (1988). Stability and motion of a hairpin and the corresponding mismatched duplex: a theoretical exploration using molecular mechanics and normal mode analysis of 2D NMR results on d(GCCGCAGC). J. Biomol. Struct. Dyn. 6, 525-542.
56. Garcia, A.E., Gupta, G., Soumpasis, D.M. & Tung, C.S. (1990). Energetics of the hairpin to mismatched duplex transition of d(GCCGCAGC) on NaCI solution. J. Biomol. Struct. Dyn. 8, 173-186.
57. Santhana-Mariappan, S.V., et al., & Gupta, G. (1996). Solution structures of the individual single strands of the fragile X DNA triplets (GCC)n & (GGC)n. Nucleic Acids Res. 24, 784-792.
58. +·cytosine pairs. J. Mol. Biol. 272, 369-382.
59. Singh, S., Patel, P.K. & Hosur, R.V. (1997). Structural polymorphism and dynamism in the DNA segment GATCTTCCCCCCGGAA: NMR investigations of hairpin, dumbbell, nicked duplex, parallel strands, and i-motif. Biochemistry 36, 13214-13222.
60. Hirao, I., et al., & Miura, K. (1994). Most compact hairpin-turn structure exerted by a short DNA fragment, d(GCGAAGC) in solution: an extraordinarily stable structure resistant to nucleases and heat. Nucleic Acids Res. 22, 576-582.
61. Yoshizawa, S., Kawai, G., Watanabe, K., Miura, K. & Hirao, I. (1997). GNA trinucleotide loop sequences producing extraordinarily stable DNA minihairpins. Biochemistry 36, 4761-4767.
62. 1H NMR studies on d(CGCCGCAGC) and d(CGCCGTAGC). Biochemistry 26, 7715-7723.
63. 2+ to A-DNA. Biophys. J. 69, 559-568.
64. Cate, J.H. & Doudna, J.A. (1996). Metal-binding sites in the major groove of a large ribozyme domain. Structure 4, 1221-1229.
65. Nunn, C.M. & Neidle, S. (1996). The high resolution crystal structure of a DNA decamer d(AGGCATGCCT). J. Mol. Biol. 256, 340-351.
66. Nunn, C.M. (1996). Crystal structure of d(AGGBrCATGCCT): implications for cobalt hexammine binding to DNA. J. Biomol. Struct. Dyn. 14, 49-56.
67. Geissner, R.V., Quigley, G.J, Wang, H.J., van der Marel, A., van Boom, J.H. & Rich, A. (1985). Structural basis for stabilization of Z-DNA by cobalt hexaammine and magnesium cations. Biochemistry 24, 237-240.
68. Peck, L.J., Nordheim, A., Rich, A. & Wang, A. (1982). Flipping of cloned d(pCpG).d(pCpG)n DNA sequences from right- to left-handed helical structure by salt, Co(III) or negative supercoiling. Proc. Natl Acad. Sci. USA 79, 4560-4564.
69. 3+ binding to the guanine. J. Biomol. Struct. Dyn. 3, 649-665.
70. Pan, B., Ban, C., Wahl, M.C. & Sundaralingam, M. (1997). Crystal structure of d(GCGCGCG) with 5′-overhang G residues. Biophys. J. 73, 1553-1561.
71. Kieft, J.S. & Tinoco, I. Jr (1997). Solution structure of a metal-binding site in the major groove of RNA complexed with cobalt (III) hexammine. Structure 5, 713-721.
72. 3+. X-ray evidence for hydrogen bonding to pairs of guanine bases in the major groove. Biochim. Biophys. Acta 697, 78-82.
73. +3 salt of d(CGCGCG) at 1.2 Å resolution. J. Biomol. Struct. Dyn. 5, 521-534.
74. Bauer, C. & Wang, A.H. (1997). Bridged cobalt amine complexes induce DNA conformational changes effectively. J. Inorg. Biochem. 68, 129-135.
75. 2 in the presence of hexaamminecobalt(III). Structure 5, 1297-1311.
76. Robinson, H. & Wang, A.H. (1996). Neomycin, spermine and hexaamminecobalt (III) share common structural motifs in converting B- to A-DNA. Nucleic Acids Res. 24, 676-682.
77. Xu, Q., Shoemaker, R.K. & Braunlin, W.H. (1993). Induction of B-A transitions of deoxyoligonucleotides by multivalent cations in dilute aqueous solution. Biophys. J. 65, 1039-1049.
78. Duckett, D.R., Murchie, A.I.H. & Lilley, D.M.J. (1990). The role of metal ions in the conformation of the four-way DNA junctions. EMBO J. 9, 583-590.
79. Gate, J.H., Hanna, R.L. & Doudna, J.A. (1997). A magnesium ion core at the heart of a ribozyme domain. Nat. Struct. Biol. 4, 553-558.
80. Gate, J.H., et al., & Doudna, J.A. (1996). RNA tertiary structure mediation by adenosine platforms. Science 273, 1696-1699.
81. Hampel, A. & Cowan, J.A. (1997). A unique mechanism for RNA catalysis: the role of metal cofactors in hairpin ribozyme cleavage. Chem. Biol. 4, 513-517.
82. Grosschedl, R. & Hobom, G. (1979). DNA sequences and structural homologies of the replication origins of lambdoid bacteriophages. Nature 277, 621-627.
83. Denniston-Thompson, K., Moore, D.D., Kruger, K.E., Furth, M.E. & Blattner, F.R. (1977). Physical structure of the replication origin of bacteriophage lambda. Science 198, 1051-1056.
84. Meijer, M., et al., & Schaller, H. (1979). Nucleotide sequence of the origin of replication of the Escherichia coli K-12 chromosome. Proc. Natl Acad. Sci. USA 76, 580-584.
85. Sugimoto, K., et al., & Hirota, Y. (1979). Nucleotide sequence of Escherichia Coli K-12 replication origin. Proc. Natl Acad. Sci. USA 76, 575-579.
86. Astell, C.R., Chow, M.B. & Ward, D.C. (1985). Sequence analysis of the termini of virion and replicative forms of minute virus of mice DNA suggests a modified rolling hairpin model for autonomous parvovirus DNA replication. J. Virol. 54, 171-177.
87. Willwand, K., Mumtsidu, E., Kuntz-Simon, G. & Rommelaere, J. (1998). Initiation of DNA replication at palindromic telomeres is mediated by a duplex-to-hairpin transition induced by the minute virus of mice nonstructural protein NS1. J. Biol. Chem. 273, 1165-1174.
88. Tattersall, P. & Ward, D.C. (1976). Rolling hairpin model for replication of parvovirus and linear chromosomal DNA. Nature 263, 106-109.
89. Costello, E., Sahli, R., Hirt, B. & Beard, P. (1995). The mismatched nucleotides in the 5′-terminal hairpin of minute virus of mice are required for efficient viral DNA replication. J. Virol. 69, 7489-7496.
90. Marvin, D.A. & Wachtel, E.J. (1 976). Structure and assembly of filamentous bacterial viruses. Phil. Trans. R. Soc. Lond. (Biol. Sci.) B 276, 81-98.
91. Marvin, D.A., Nave, C., Ladner, J.E., Fowler, A.G., Brown, R.S. & Wachtel, E.J. (1981). Macromolecular structural transitions in Pf1 filamentous bacterial virus. In Structural Aspects of Recognition and Assembly in Biological Macromolecules. (Balaban, M., Sussman, J.L., Traub, W. & Yonath, A. eds), pp. 891-910, Balaban ISS, Rehovot, Israel.
92. Marvin, D.A., Nave, C., Bansal, M., Hale, R.D. & Salje, E.K.H. (1992). Two forms of Pf1 inovirus: X-ray diffraction studies on a structural phase transition and a calculated liberation normal mode of the asymmetric unit. Phase Transitions 39, 45-80.
93. Viswamitra, M.A. & Pandit, J. (1983). A proposal for a specific double-helical structure in which the polynucleotide strands intercalate instead of forming base-pairs. J. Biomol. Struct. Dyn. 1, 743-753.
94. Polizzi, C. & Clarke, L. (1991). The chromatin structure of centromeres from fission yeast: differentiation of the central core that correlates with function. J. Cell Biol. 112, 191-201.
95. Takahashi, K., Murakami, S., Chikashige, Y., Funabiki, H., Niwa, O. & Yanagida, M. (1992). A low copy number central sequence with strict symmetry and unusual chromatin structure in fission yeast centromere. Mol. Biol. Cell 3, 819-835.
96. Muro, Y., Masumoto, H., Yoda, K., Nozaki, N., Ohashi, M. & Okazaki, T. (1992). Centromere protein B assembles human centromeric alpha-satellite DNA at the 17-bp sequence, CENP-B box. J. Cell Biol. 116, 585-596.
97. Yoda, K., Kitagawa, K., Masumoto, H., Muro, Y. & Okazaki, T. (1992). A human centromere protein, CENP-B, has a DNA binding domain containing four potential alpha helices at the NH2 terminus, which is separable from dimerizing activity. J. Cell Biol. 119, 1413-1427.
98. Cooke, C.A., Bernat, R.L. & Earnshaw, W.C. (1990). CENP-B: a major human centromere protein located beneath the kinetochore. J. Cell Biol. 110, 1475-1488.
99. Carbon, J. & Clarke, L. (1990). Centromere structure and function in budding and fission yeasts. New Biol. 2, 10-19.
100. Ferrer, N., Azorin, F., Villasante, A., Gutierrez, C. & Abad, J.P. (1995). Centromeric dodeca-satellite DNA sequences form fold-back structures. J. Mol. Biol. 245, 8-21.
101. Collaborative Computational Project Number 4. The CCP4 suite: programs for crystallography (1994). Acta Cryst. D 50 760-763.
102. Peterson, M.R., et al., & Helliwell, J.R. (1996). MAD Phasing strategies explored with a brominated oligonucleotide crystal at 1.65 Å resolution. J. Synchr. Rad. 3, 24-34.
103. Fourme, R., Shepard, W. & Kahn, R. (1996). Application of the anomalous dispersion of X-rays to macromolecular crystallography. Prog. Biophys. Mol. Biol. 64, 167-199.
104. Hendrickson, W.A. (1991). Determination of macromolecular structures from anomalous diffraction of synchrotron radiation. Science 254, 51-58.
105. de La Fortelle, E. & Bricogne, G. (1997). Methods in Enzymology: Macromolecular Crystallography. 276 (Sweet, R.M. & Carter, C.W., Jr., eds), pp. 472-494, Academic Press, New York, USA.
106. Abrahams, J.P. & Leslie, A.G.W. (1996). Methods used in the structure determination of bovine mitochondrial ATPase. Acta Cryst. D 52, 30-42.
107. Brünger, A. (1992). X-PLOR (version 3.0) Manual. The Howard Hughes Medical Institute, Department of Biophysics and Biochemistry, Yale University, New Haven CT, USA.
108. Sheldrick, G. (1997). SHELX97-Program for Refinement of Crystal Structures. University of Goettingen, Germany.
109. Sasaki, S. (1984). Anomalous Scattering Factors for Synchrotron Radiation Users Calculated Using the Cromer and Liberman Method. National Laboratory for High Energy Physics, KEK, Tsukuba, Japan.