Solution structure of r(gaggacug):d(CAGTCCTC) hybrid: Implications for the initiation of HIV-1 (+)-strand synthesis

Journal of Molecular Biology

Volumn 269, Issue 2, 1997, Pages 225-239

  Fedoroff, Oleg Yu ^a,b   Ge, Ying ^a   Reid, Brian R ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

NMR solution structure; Polypurine primer; Reverse transcription; RNA:DNA hybrid; RNase H

Indexed keywords

PRIMER RNA; RIBONUCLEASE H; VIRUS RNA;

ARTICLE; DNA RNA HYBRIDIZATION; DNA STRUCTURE; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; REVERSE TRANSCRIPTION; RNA STRUCTURE;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; UNIDENTIFIED RETROVIRUS;

EID: 0031556022     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1024     Document Type: Article

References (73)

1. Allain F. H.-T., Varani G. Structure of the P1 helix from group I self-splicing introns. J. Mol. Biol. 250:1995;333-353.
2. Arnott S., Hukins D. W. L. Optimized parameters forAB. Biochem. Biophy. Res. Commun. 47:1972;1504-1509.
3. Arnott S., Hukins D. W. L. B. J. Mol. Biol. 81:1973;93-105.
4. Arnott S., Chandrasekaran R., Millane R. P., Park H.-S. DNA-RNA hybrid secondary structures. J. Mol. Biol. 188:1986;631-640.
5. Bishop K. D., Blocker F. J. H., Egan W., James T. L. Hepatitus B virus direct repeat sequence: imino proton exchange rates and distance and torsion angle restraints from NMR. Biochemistry. 33:1994;427-438.
6. Boelens R., Scheek R. M., Dijkstra K., Kaptein R. Sequential assignment of imino- and amino-proton resonances in 1H NMR spectra of oligonucleotides by two-dimensional NMR spectroscopy. Application to a lac operator fragment. J. Magn. Reson. 62:1985;378-386.
7. Bolton P. H., Kearns D. R. Hydrogen bonding interactions of polyamines with the 2′-OH of RNA. Nucl. Acids Res. 5:1978;1315-1324.
8. Champoux J. J., Gilboa E., Baltimore D. Mechanism of RNA primer removal by the RNase H activity of avian myeloblastosis virus reverse transcriptase. J. Virol. 49:1984;686-691.
9. Chou S.-H., Flynn P., Reid B. R. High-resolution NMR study of a synthetic DNA-RNA hybrid dodecamer containing the consensus pribnow promoter sequence: d(CGTTATAATGCG):r(CGCAUUAUAACG). Biochemistry. 28:1989;2435-2443.
10. ntracts and B′-B′ bends in DNA. Biochemistry. 30:1991a;561-568.
11. Chuprina V. P., Lipanov A. A., Fedoroff O. Yu., Kim S.-G., Kintanar A., Reid B. R. Sequence effect on local DNA topology. Proc. Natl Acad. Sci. USA. 88:1991b;9087-9091.
12. Conte M. R., Conn G. L., Brown T., Lane A. N. Hydration of the RNA duplex r(CGCAAAUUUGCG)2 determined by NMR. Nucleic Acids Res. 24:1996;3693-3699.
13. DeStefano J. J. The orientation of binding of HIV reverse transcriptase on nucleic acid hybrids. Nucl. Acids Res. 23:1995;3901-3908.
14. DeStefano J. J., Mallaber L. M., Fay P. J., Bambara R. A. Determinants of the RNase H cleavage specificity of HIV reverse transcriptase. Nucleic Acids Res. 21:1993;4330-4338.
15. Eom S. H., Wang J., Steiz T. A. Structure of Taq polymerase with DNA at the polymerase active site. Nature, 382:1996;278-281.
16. Fedoroff O. Y., Salazar M., Reid B. R. Structure of a DNA:RNA hybrid duplex: why RNase H does not cleave pure RNA. J. Mol. Biol. 233:1993;509-523.
17. Fedoroff O. Y., Salazar M., Reid B. R. Structural variation among retroviral primer-DNA junctions: the solution structure of the HIV-1 (-)-strand Okazaki fragment r(gcca)d(CTGC):d(GCAGTGGC). Biochemistry. 35:1996;11070-11080.
18. Finston W. I., Champoux J. J. RNA-primed initiation of Moloney murine leukemia virus plus strands by reverse transcriptasein vitro. J. Virol. 51:1984;26-33.
19. Fuentes G. M., Rodríguez-Rodríguez L., Fay P. J., Bambara R. A. Use of an oligoribonucleotide containing the polypurine tract sequence as a primer by HIV reverse transcriptase. J. Biol. Chem. 270:1995;28169-28176.
20. Furfine E. S., Reardon J. E. Human immunodeficiency virus reverse transcriptase ribonuclease H: Specificity of tRNA-primer Excision. Biochemistry, 30:1991;7041-7046.
21. Gilboa E., Mitra S. W., Goff S., Baltimore D. A detailed model of reverse transcription and test of crucial aspects. Cell. 18:1979;93-100.
22. González C., Stec W., Kobylanska A., Hogrefe R. I., Reynolds M., James T. L. Structural study of a DNA·RNA hybrid duplex with a chiral phosphorothioate moiety by NMR: extraction of distance and torsion angle constraints and imino proton exchange rates. Biochemistry. 33:1994;11062-11072.
23. González C., Stec W., Reynolds M., James T. L. Structure and dynamics of a DNA·RNA hybrid duplex with a chiral phosphorothioate moiety: NMR and molecular dynamics with conventional and time-averaged restraints. Biochemistry. 34:1995;4969-4982.
24. Gyi J. I, Conn G. L., Lane A. N., Brown T. Comparison of the thermodynamic stabilities and solution conformations of DNA:RNA hybrids containing purine-rich and pyrimidine-rich strands with DNA and RNA duplexes. Biochemistry. 35:1996;12538-12548.
25. Harbison G. S. Interference betweenJ. J. Am. Chem. Soc. 115:1993;3026-3027.
26. Hare D. R., Wemmer D. E., Chou S. H., Drobny G., Reid B. R. Assignment of the non-exchangible proton resonances of d(CGCGAATTCGCG) using two-dimensional NMR methods. J. Mol. Biol. 171:1983;319-336.
27. Huber H. E., Richardson C. C. Processing of the primer for plus strand DNA synthesis by human immunodeficiency virus type 1 reverse transcriptase. J. Biol. Chem. 265:1990;10565-10573.
28. Hung S.-H., Yu Q., Gray D. M., Ratliff R. L. Evidence from CD spectra that d(purine):r(pyrimidine) and r(purine):d(pyrimidine) hybrids are in different structural classes. Nucl. Acids Res. 22:1994;4326-4334.
29. Jacobo-Molina A., Ding J., Nanni R. G., Clark A. D. Jr., Lu X., Tantillo C., Williams R. L., Kamer G., Ferris A. L., Clark P., Hizi A., Hughes S. H., Arnold E. Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double stranded DNA at 3 Å resolution shows bent DNA. Proc. Natl Acad. Sci. USA. 90:1993;6320-6324.
30. Jiang F., Kumar R. A., Jones R. A., Patel D. J. Structural basis of RNA folding and recognition in an AMP-RNA aptamer complex. Nature. 382:1996;183-186.
31. 88. J. Am. Chem. Soc. 112:1990;4508-4512.
32. 1. Biochemistry. 31:1992;3564-3574.
33. Lane A. W., Ebel S., Brown T. NMR assignments and solution conformation of the DNA:RNA hybrid duplex d(GTGAACTT):r(AAGUUCAC). Eur. J. Biochem. 215:1993;297-306.
34. Leroy J.-L., Broseta D., Gueron M. Proton exchange and base-pair kinetics of poly(rA):poly(rU) and poly(rI):poly(rC). J. Mol. Biol. 184:1985;165-178.
35. Lesnik. E. A., Freier S. M. Relative thermodynamic stability of DNA, RNA and DNA:RNA hybrids: relationship with base composition and structure. Biochemistry. 34:1995;10807-10815.
36. Luo G., Sharmeen L., Taylor J. Specificities involved in the initiation of retroviral plus-strand DNA. J. Virol. 64:1990;592-597.
37. Metzger W., Hermann T., Schatz O., LeCrice S. F. J., Heumann H. Hydroxyl radical footprint analysis of HIV reverse transcriptase-template:primer complexes. Proc. Natl Acad. Sci USA. 90:1993;5909-5913.
38. Maltseva T. V., Agback P., Repkova M. N., Venyaminova A. G., Ivanova E. M., Sandström A., Zarytova V. F., Chattopadhyaya J. The solution structure of a 3′-phenazinium (Pzn) tethered DNA-RNA duplex with a dangling adenosine: r(5′GAUUGAA3′):d(5′TCAATC3′-Pzn). Nucl. Acids Res. 22:1994;5590-5599.
39. Mitra S. W., Chow M., Champoux J. J., Baltimore D. Synthesis of murine leukemia virus plus strong stop DNA initiates at a unique site. J. Biol. Chem. 257:1982;5983-5986.
40. Muesing M. A., Smith D. H., Cabradilla C. D., Benton C., Lasky L., Capon D. Nucleic acid structure and expression of the human AIDS/lymphanedopathy retrovirus. Nature. 313:1985;450-458.
41. Nakamura H., Oda S., Iwai S., Inoue H., Ohtsuka E., Kanaya S., Kimura S., Katsuda C., Katayanagi K., Morikawa K., Miyaashiro H., Ikehara M. How does RNase H recognize a DNA:RNA hybrid? Proc. Natl Acad. Sci. USA. 88:1991;11535-11539.
42. Nishizaki T., Iwai S., Ohkudo T., Kojima C., Nakamura H., Kyogoku Y., Ohtsuka E. Solution structures of DNA duplexes containing a DNA:RNA hybrid region, d(GG)r(AGAU)d(GAC):d(GTCATCTCC) and d(GGAGA)r(UGAC):d(GTCATCTCC). Biochemistry. 35:1996;4016-4025.
43. Trp. Cell. 30:1982;797-805.
44. Pearlman D. A., Kollman P. A. Are time-averaged restraints necessary for nuclear magnetic refinement? A model study for DNA. J. Mol. Biol. 220:1991;457-479.
45. Pearlman, D. A. Case, D. A. Caldwell, J. C. Seibel. G. L. Singh, U. C. Weiner, P. Kollman, P. A. 1990, Amber (UCSF), version 4.0, University of California, San Francisco.
46. Pelletier H., Sawaya M. R., Kumar A., Wilson S. H., Kraut J. Structures of ternary complexes of rat DNA polymerase β, a DNA template-primer and ddCTP. Science, 264:1994;1891-1903.
47. Piotto M., Saudek V., Sklenár, V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR. 2:1992;661-665.
48. Powell M. D., Levin J. G. Sequence and structural determinants required for priming of plus-strand DNA synthesis by the HIV-1 polypurine tract. J. Virol. 70:1996;5288-5296.
49. Pullen K. A., Champoux J. J. Plus-strand origin for human immunodeficiency virus type 1: Implications for integration. J. Virol. 64:1990;6274-6277.
50. Pullen K. A., Rattray A. J., Champoux J. J. The sequence features important for plus strand priming by HIV-1 reverse transcriptase. J. Biol. Chem. 268:1993;6221-6227.
51. Ratmeyer L., Vinayak R., Zhong Y. Y., Zon G., Wilson W. D. Sequence specific thermodynamic and structural properties for DNA:RNA duplexes. Biochemistry. 33:1994;5298-5304.
52. Rattray A. J., Champoux J. J. The role of Moloney murine leukemia virus RNase H activity in the formation of plus-strand primers. J. Virol. 61:1987;2843-2851.
53. Rattray A. J., Champoux J. J. Plus-strand priming by M-MuLV: the sequence features important for cleavage by RNase H. J. Mol. Biol. 208:1989;445-456.
54. Reid B. R., Banks K., Flynn P., Nerdal W. NMR distance measurements in DNA duplexes: sugars and bases have the same correlation times. Biochemistry. 28:1989;10001-10007.
55. Resnick R., Omer C. A., Faras A. J. Involvement of retrovirus reverse transcriptase-associated RNase H in the initiation of strong-stop (+) DNA synthesis and the generation of the long terminal repeat. J. Virol. 51:1984;813-821.
56. Roberts R. W., Crothers D. M. Stability and properties of double and triple helices: dramatic effects of RNA and DNA backbone composition. Science. 258:1992;1463-1466.
57. Saenger W. Principles of Nucleic Acid Structure. 1984;Springer, New York.
58. Salazar M., Fedoroff O. Y., Miller J. M., Ribeiro N. S., Reid B. R. The DNA strand in DNA:RNA hybrid duplexes is neitherBA. Biochemistry. 32:1993;4207-4215.
59. Salazar M., Fedoroff O. Y., Zhu L., Reid B. R. The solution structure of the r(gcg)d(TATACCC):d(GGGTATACGC) Okazaki fragment contains two distinct duplex morphologies connected by a junction. J. Mol. Biol. 241:1994;440-455.
60. Salazar M., Fedoroff O. Y., Reid B. R. Structure of chimeric duplex junctions in retroviral fragments: the solution structure of r(ccca)d(AATGA):d(TCATTTGGG). Biochemistry. 35:1996;8126-8135.
61. 311. FEBS Letters. 208:1986;94-98.
62. Lys. J. Biol. Chem. 267:1992;15071-15079.
63. Smith J. K., Cywinski A., Taylor J. M. Specificity of initiation of plus-strand DNA by Rous sarcoma virus. J. Virol. 52:1984;314-319.
64. States D. J., Haberkorn R. A., Reuben D. J. A two-dimensional nuclear Overhauser experiment with pure absorption phase in four quadrants. J. Magn. Reson. 48:1982;286-292.
65. Steely H. T. Jr, Gray D. M., Ratliff R. L. CD of homopolymer DNA:RNA hybrid duplexes and triplexes containing A:T or A:U base pairs. Nucl. Acids Res. 24:1986;10071-10090.
66. Torda A. E., Scheek R. M., van Gunsteren W. F. Time-averaged nuclear Overhauser effect distance restraints applied to tendamistat. J. Mol. Biol. 214:1990;223-235.
67. Varmus H., Brown P. Retroviruses. Mobile DNA. 1989;American Society for Microbiology, Washington DC.
68. Wang A. C., Kim S.-G., Chou S.-H., Orban J., Flynn P., Reid B. R. Errors in RNA NOESY distance measurements in chimeric and hybrid duplexes; differences in RNA and DNA proton relaxation. Biochemistry. 31:1992;3940-3946.
69. Weiner S. J., Kollman P. A., Nguyen D. T., Case D. A. An all atom force field for simulations of proteins and nucleic acids. J. Comput. Chem. 7:1986;230-252.
70. Wöhrl B., Moelling K. Interaction of HIV-1 RNase H with polypurine tract containing RNA-DNA hybrids. Biochemistry. 29:1990;10141-10147.
71. Zhu L., Reid B. R. An improved NOESY simulation program for partially relaxed spectra: BIRDER. J. Magn. Reson. ser. B. 106:1995;227-235.
72. Zhu L., Reid B. R., Kennedy M., Drobny G. P. Modulation ofJ. J. Magn. Reson. ser. A. 111:1994;195-202.
73. Zimmerman S. B., Pheiffer B. H. A RNA:DNA hybrid that can adopt two conformations: an X-ray diffraction study of poly(rA):poly(dT) in concentrated solution or in fibers. Proc. Natl Acad. Sci. USA. 78:1981;78-82.