The structure of an RNA/DNA hybrid: A substrate of the ribonuclease activity of HIV-1 reverse transcriptase

Journal of Molecular Biology

Volumn 264, Issue 3, 1996, Pages 521-533

  Horton, Nancy C ^a,b   Finzel, Barry C ^a  

^a PFIZER INC   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Drug target; HIV reverse transcriptase; RNA DNA hybrid; RNase H; X ray structure

Indexed keywords

RIBONUCLEASE; RNA DIRECTED DNA POLYMERASE;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA CONFORMATION; DNA RNA HYBRIDIZATION; DNA SEQUENCE; DRUG TARGETING; ENZYME ACTIVITY; ENZYME SUBSTRATE; HUMAN IMMUNODEFICIENCY VIRUS 1; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

EID: 0030572981     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0658     Document Type: Article

References (44)

1. Arnott, S., Chandrasekaran, R., Millane, R. P. & Park, H.-S. (1986). DNA-RNA hybrid secondary structures. J. Mol. Biol. 188, 631-640.
2. Babcock, M. S., Pednault, E. P. D. & Olson, W. K. (1993). Nucleic acid structure analysis: a users guide to a collection of new analysis programs. J. Biomol. Struct. Dynam. 11, 596-628.
3. Babcock, M. S., Pednault, E. P. D. & Olson, W. K. (1994). Nucleic acid structure analysis, mathematics for local Cartesian and helical structure parameters that are truly comparable between structures. J. Mol. Biol. 237, 125-156.
4. Brünger, A. T. (1990). X-PLOR (Version 2.2) Manual, Howard Hughes Medical Institute, Yale University, CT.
5. Chandrasekaran, R., Wang, M., He, R. G., Puigjaner, L. C., Byler, M. A., Millane, R. P. & Arnott, S. (1989). A re-examination of the crystal structure of A-DNA using fiber diffraction data. J. Biomol. Struct. Dynam. 6, 1189-1202.
6. Chen, X., Ramakrishnan, B., Fao, S. T. & Sundaralingam, M. (1993). Binding of two distamycin A molecules in the minor groove of an alternating B-DNA duplex. Nature Struct. Biol. 1, 169-175.
7. Chou, S. H., Flynn, P. & Reid, B. (1989). High-resolution NMR study of a synthetic DNA-RNA hybrid dodecamer containing the consensus pribnow promoter sequence: d(CGTTATAATGCG)r(CGCA-UUAUAACG). Biochemistry, 28, 2435-2443.
8. Coffin, J. M. (1996). Retroviridae: the viruses and their replication. In Virology (Fields, B. N., Knipe, D. M., Howley, P. M., Chanock, R. M., Melnick, J. L., Monath, T. P., Roizman, B. & Straus, S. E., eds), 3rd edit., pp. 1767-1847, Lippincott-Raven Publishers, New York.
9. DeStefano, J. J., Buiser, R. G., Mallaber, L. M., Bambara, R. & Fay, P. J. (1991). Human immunodeficiency virus reverse transcriptase displays a partially processive 3′ to 5′ endonuclease activity. J. Biol. Chem. 266, 24295-24301.
10. Dickerson, R. E. (1992). DNA structure from A to Z. Methods Enzymol. 211, 67-111.
11. Dickerson, R. E., Goodsell, D. S., Kopka, M. L. & Pjura, P. E. (1987). The effect of crystal packing on oligonucleotide double helix structure. J. Biomol. Struct. Dynam. 5, 557-579.
12. 2. J. Mol. Biol. 209, 459-474.
13. Egli, M., Usman, N., Zhang, S. & Rich, A. (1992). Crystal structure of an Okazaki fragment at 2 Å resolution. Proc. Natl Acad. Sci. USA, 89, 534-538.
14. Egli, M., Usman, N. & Rich, A. (1993). Conformational influence of the ribose 2′-hydroxyl group: crystal structures of DNA-RNA chimeric duplexes. Biochemistry, 32, 3221-3237.
15. Fedoroff, O. Y., Salazar, M. & Reid, B. R. (1993). Structure of a DNA:RNA hybrid duplex why RNase H does not cleave pure RNA. J. Mol. Biol. 233, 509-523.
16. Fu, T. & Taylor, J. (1992). When retroviral reverse transcriptases reach the end of their RNA templates. J. Virol. 66, 406-412.
17. Furfine, E. S. & Reardon, J. E. (1991). Human immunodeficiency virus reverse transcriptase ribonuclease H: specificity of tRNA (Lys3)-primer excision. J. Biol. Chem. 266, 406-412.
18. Goodsell, D. S., Kaczor-Grzeskowiak, M. & Dickerson, R. E. (1994). The crystal structure of C-C-A-T-T-A-A-T-G-G. Implications for bending of B-DNA at T-A steps. J. Mol. Biol. 239, 79-96.
19. Gopalakrishnan, V., Peliska, J. A. & Benkovic, S. J. (1992). Human immunodeficiency virus type 1 reverse transcriptase: spatial and temporal relationship between the polymerase and RNase H activities. Proc. Natl Acad. Sci. USA, 89, 10763-10767.
20. Hall, S. R., Flack, H. D. & Stewart, J. M. (1992). Editors of XTAL3.2 Reference Manual, Universities of Western Australia, Geneva and Maryland, Lamb, Perth.
21. Happ, C. S., Happ, E., Clore, G. M. & Gronenborn, A. M. (1988). Refinement of the solution structure of the RNA-DNA hybrid 5′-[r(GCA)d(TGC)]2. FEBS Letters, 236, 62-70.
22. Holbrook, S. R., Cheong, C., Tinoco, I. & Kim, S.-H. (1991). Crystal structure of an RNA double helix incorporating non-Watson-Crick base-pairs. Nature, 353, 579-581.
23. Howard, A. J., Gilliland, G. L, Finzel, B. C., Poulos, T. L., Ohlendorf, D. H. & Salemme, F. R. (1987). The use of an imaging proportional counter in macromolecular crystallography. J. Appl. Crystallog. 20, 383-387.
24. 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. (1993). Crystal structure of human immunodeficiency virus type I reverse transcriptase complexed with double-stranded DNA at 3.0 Å resolution shows bent DNA. Proc. Natl Acad. Sci. USA, 90, 6320-6324.
25. Jain, S. & Sundaralingam, M. (1989). Effect of crystal packing environment on conformation of the DNA duplex. J. Biol. Chem. 264, 12780-12784.
26. Kennard, O. & Hunter, W. N. (1991). Single-crystal X-ray diffraction studies of oligonucleotides and oligonucleotide-drug complexes. Angew. Chem. Int. Ed. Engl. 30, 1254-1277.
27. Kennard, O. & Salisbury, S. A. (1993). Oligonucleotide X-ray structures in the study of conformation and interactions of nucleic acids. J. Biol. Chem. 268, 10701-10704.
28. Leonard, G. A., McAuley-Hecht, K. E., Ebel, S., Lough, D. M., Brown, T. & Hunter, W. N. (1994). Crystal and molecular structure of r(CGCGAAUUAGCG): and RNA duplex containing two G(anti)-A(anti) base-pairs. Stucture, 2, 483-494.
29. Milman, G., Langridge, R. & Chamberlin, M. J. (1967). The structure of a DNA-RNA hybrid. Proc. Natl. Acad. Sci. USA, 57, 1804-1810.
30. O'Brien, E. J. & MacEwan, A. W. (1970). Molecular and crystal structure of the polynucleotide complex: polyinosinic acid plus polydeoxycytidylic acid. J. Mol. Biol. 48, 243-261.
31. Parkinson, G., Vojtechovsky, J., Clowney, L., Brünger, A. & Berman, H. (1996). New parameters for the refinement of nucleic acid containing structures. Acta Crystallog. sect D, 57, 57-64.
32. Pley, H. W., Flaherty, K. M. & McKay, D. B. (1994). Three-dimensional structure of a hammerhead ribozyme. Nature, 372, 68-74.
33. Salazar, M., Fedoroff, O. Y., Leiming, A. & Reid, B. R. (1994). 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, 440-455.
34. Schatz, O., Mous, J. & LeGrice, S. F. J. (1990). HIV-1 RT-associated ribonuclease H displays both endonuclease and 3′-5′ exonuclease activity. EMBO J. 9, 1171-1176.
35. Shakked, Z. Guerstein-Guzikevich, G., Eisenstein, M., Frolow, F. & Rabinovich, D. (1989). The conformation of the DNA double helix in the crystal is dependent on its environment. Nature, 342, 456-460.
36. Smith, J. S. & Roth, M. J. (1992). Specificity of human immunodeficiency virus-1 reverse transcriptase associated ribonuclease H in removal of the minus strand primer, tRNA(Lys3). J. Biol. Chem. 267, 15071.
37. Smith, J. S. & Roth, M. J. (1993). Purification and characterization of an active human immunodeficiency virus type 1 RNase H domain. J. Virol. 67, 4037-4049.
38. Takahara, P. M., Rosenzweig, A. C., Frederick, C. A. & Lippard, S. J. (1995). Crystal structure of a double stranded DNA containing the major adduct of the anticaner drug cisplatin. Nature, 377, 649-652.
39. Timsit, Y., Westhof, E., Fuchs, R. P. & Moras, D. (1989). Unusual helical packing in crystals of DNA bearing a mutation hot spot. Nature, 341, 459-462.
40. Wang, A. H.-J., Fujii, S. van Boom, J. H. & Rich, A. (1982a). Molecular structure of the octamer d(GGC-CGGCC): modified A-DNA. Proc. Natl Acad. Sci. USA, 79, 3968-3972.
41. Wang, A. H.-J., Fuji, S. vanBoom, J. H., vanderMarel, G. A., vanBoekel, S. A. A. & Rich, A. (1982b). Molecular structure of r(GCG)d(TATACGC): a DNA-RNA hybrid helix joined to double helical DNA. Nature, 299, 601-604.
42. Watenpaugh, K. (1992). MIR. In XTAL3.2 Reference Manual (Hall, S. R., Flack, H. D. & Stewart, J. M., eds), Universities of Western Australia, Geneva and Maryland, Lamb, Perth.
43. Woehrl, B. M. & Moelling, K. (1990). Interaction of HIV-1 ribonuclease H with polypurine tract containing RNA-DNA hybrids. Biochemistry, 29, 10141-10147.
44. Zimmerman, S. B. & Pheiffer, B. H. (1981). A RNA-DNA hybrid that can adopt two conformations: an xray diffraction study of poly(rA)-poly(dT) in concentrated solution or in fibers. Proc. Natl Acad. Sci. USA, 78, 78-82.