Ribonuclease H: Properties, substrate specificity and roles in retroviral reverse transcription

FEBS Journal

Volumn 276, Issue 6, 2009, Pages 1506-1516

  Champoux, James J ^a   Schultz, Sharon J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Catalytic mechanism; DNA RNA hybrids; Endonuclease; Human immunodeficiency virus, type 1; Moloney murine leukemia virus; Polypurine tract; Reverse transcriptase; Reverse transcription; RNA cleavage; RNase H

Indexed keywords

DNA POLYMERASE; ENDONUCLEASE; RIBONUCLEASE H; VIRUS RNA;

DNA RNA HYBRIDIZATION; DNA STRUCTURE; DNA SYNTHESIS; ENZYME SPECIFICITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; MINUS STRAND SYNTHESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLUS STRAND SYNTHESIS; PRIORITY JOURNAL; RETROVIRUS; REVERSE TRANSCRIPTION; RNA GENE; RNA STRUCTURE; SHORT SURVEY; STRUCTURE ACTIVITY RELATION;

BIOCATALYSIS; MODELS, MOLECULAR; PROTEIN CONFORMATION; RETROVIRIDAE; RIBONUCLEASE H; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC;

HUMAN IMMUNODEFICIENCY VIRUS 1; MOLONEY MURINE LEUKEMIA VIRUS;

EID: 61349157313     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.06909.x     Document Type: Short Survey

References (102)

1. Baltimore D (1970) RNA-dependent DNA polymerase in virions of RNA tumour viruses. Nature 226, 1209 1211.
2. Temin HM Mizutani S (1970) RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature 226, 1211 1213.
3. Molling K, Bolognesi DP, Bauer H, Busen W, Plassmann HW Hausen P (1971) Association of viral reverse transcriptase with an enzyme degrading the RNA moiety of RNA-DNA hybrids. Nat New Biol 234, 240 243.
4. Champoux JJ (1993) Roles of ribonuclease H in reverse transcription. In Reverse Transcriptase (Skalka AM Goff SP, eds), pp. 103 118. Cold Spring Harbor Laboratory Press, Plain View, NY.
5. Telesnitsky A Goff SP (1993) Strong-stop strand transfer during reverse transcription. In Reverse Transcriptase (Skalka AM Goff SP, eds), pp. 49 83. Cold Spring Harbor Laboratory Press, Plainview, NY.
6. Arts EJ LeGrice SFJ (1998) Interaction of retroviral reverse transcriptase with template-primer duplexes during replication. Prog Nucleic Acid Res Mol Biol 58, 339 393.
7. Rausch JW Le Grice SF (2004) 'Binding, bending and bonding': polypurine tract-primed initiation of plus-strand DNA synthesis in human immunodeficiency virus. Int J Biochem Cell Biol 36, 1752 1766.
8. Schultz SJ Champoux JJ (2008) RNase H activity: structure, specificity, and function in reverse transcription. Virus Res 134, 86 103.
9. Tanese N Goff SP (1988) Domain structure of the Moloney murine leukemia virus reverse transcriptase: mutational analysis and separate expression of the DNA polymerase and RNase H activities. Proc Natl Acad Sci USA 85, 1777 1781.
10. Schultz SJ Champoux JJ (1996) RNase H domain of Moloney murine leukemia virus reverse transcriptase retains activity but requires the polymerase domain for specificity. J Virol 70, 8630 8638.
11. Zhan X Crouch RJ (1997) The isolated RNase H domain of murine leukemia virus reverse transcriptase. Retention of activity with concomitant loss of specificity. J Biol Chem 272, 22023 22029.
12. Evans DB, Brawn K, Deibel MR Jr., Tarpley WG Sharma SK (1991) A recombinant ribonuclease H domain of HIV-1 reverse transcriptase that is enzymatically active. J Biol Chem 266, 20583 20585.
13. Hostomsky Z, Hostomska Z, Hudson GO, Moomaw EW Nodes BR (1991) Reconstitution in vitro of RNase H activity by using purified N-terminal and C-terminal domains of human immunodeficiency virus type 1 reverse transcriptase. Proc Natl Acad Sci USA 88, 1148 1152.
14. Smith JS Roth MJ (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 15079.
15. Smith JS Roth MJ (1993) Purification and characterization of an active human immunodeficiency virus type 1 RNase H domain. J Virol 67, 4037 4049.
16. Smith JS, Gritsman K Roth MJ (1994) Contributions of DNA polymerase subdomains to the RNase H activity of human immunodeficiency virus type 1 reverse transcriptase. J Virol 68, 5721 5729.
17. Smith CM, Potts WB III., Smith JS Roth MJ (1997) RNase H cleavage of tRNAPro mediated by M-MuLV and HIV-1 reverse transcriptases. Virology 229, 437 446.
18. Smith CM, Leon O, Smith JS Roth MJ (1998) Sequence requirements for removal of tRNA by an isolated human immunodeficiency virus type 1 RNase H domain. J Virol 72, 6805 6812.
19. Sarafianos SG, Das K, Tantillo C, Clark AD Jr., Ding J, Whitcomb JM, Boyer PL, Hughes SH Arnold E (2001) Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA. EMBO J 20, 1449 1461.
20. Gao HQ, Boyer PL, Arnold E Hughes SH (1998) Effects of mutations in the polymerase domain on the polymerase, RNase H and strand transfer activities of human immunodeficiency virus type 1 reverse transcriptase. J Mol Biol 277, 559 572.
21. Powell MD, Beard WA, Bebenek K, Howard KJ, Le Grice SF, Darden TA, Kunkel TA, Wilson SH Levin JG (1999) Residues in the alphaH and alphaI helices of the HIV-1 reverse transcriptase thumb subdomain required for the specificity of RNase H-catalyzed removal of the polypurine tract primer. J Biol Chem 274, 19885 19893.
22. Mandal D, Dash C, Le Grice SF Prasad VR (2006) Analysis of HIV-1 replication block due to substitutions at F61 residue of reverse transcriptase reveals additional defects involving the RNase H function. Nucleic Acids Res 34, 2853 2863.
23. Yang W, Hendrickson WA, Crouch RJ Satow Y (1990) Structure of ribonuclease H phased at 2 Å resolution by MAD analysis of the selenomethionyl protein. Science 249, 1398 1405.
24. Davies JF II., Hostomska Z, Hostomsky Z, Jordan SR Matthews DA (1991) Crystal structure of the ribonuclease H domain of HIV-1 reverse transcriptase. Science 252, 88 95.
25. Jacobo-Molina A, Ding J, Nanni RG, Clark AD Jr., Lu X, Tantillo C, Williams RL, Kamer G, Ferris AL, Clark P et al. (1993) Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 Å resolution shows bent DNA. Proc Natl Acad Sci USA 90, 6320 6324.
26. 2+at 2.8 Å resolution: proof for a single Mg(2 +)-binding site. Proteins 17, 337 346.
27. Huang H, Chopra R, Verdine GL Harrison SC (1998) Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282, 1669 1675.
28. Das D Georgiadis MM (2004) The crystal structure of the monomeric reverse transcriptase from Moloney murine leukemia virus. Structure (Camb) 12, 819 829.
29. Nowotny M, Gaidamakov SA, Crouch RJ Yang W (2005) Crystal structures of RNase H bound to an RNA/DNA hybrid: substrate specificity and metal-dependent catalysis. Cell 121, 1005 1016.
30. Nowotny M, Gaidamakov SA, Ghirlando R, Cerritelli SM, Crouch RJ Yang W (2007) Structure of human RNase H1 complexed with an RNA/DNA hybrid: insight into HIV reverse transcription. Mol Cell 28, 264 276.
31. Kanaya S, Katsuda-Nakai C Ikehara M (1991) Importance of the positive charge cluster in Escherichia coli ribonuclease HI for the effective binding of the substrate. J Biol Chem 266, 11621 11627.
32. Telesnitsky A, Blain SW Goff SP (1992) Defects in Moloney murine leukemia virus replication caused by a reverse transcriptase mutation modeled on the structure of Escherichia coli RNase H. J Virol 66, 615 622.
33. Lim D, Orlova M Goff SP (2002) Mutations of the RNase H C helix of the Moloney murine leukemia virus reverse transcriptase reveal defects in polypurine tract recognition. J Virol 76, 8360 8373.
34. Lim D, Gregorio GG, Bingman C, Martinez-Hackert E, Hendrickson WA Goff SP (2006) Crystal structure of the moloney murine leukemia virus RNase H domain. J Virol 80, 8379 8389.
35. Julias JG, McWilliams MJ, Sarafianos SG, Alvord WG, Arnold E Hughes SH (2003) Mutation of amino acids in the connection domain of human immunodeficiency virus type 1 reverse transcriptase that contact the template-primer affects RNase H activity. J Virol 77, 8548 8554.
36. Puglia J, Wang T, Smith-Snyder C, Cote M, Scher M, Pelletier JN, John S, Jonsson CB Roth MJ (2006) Revealing domain structure through linker-scanning analysis of the murine leukemia virus (MuLV) RNase H and MuLV and human immunodeficiency virus type 1 integrase proteins. J Virol 80, 9497 9510.
37. Arion D, Sluis-Cremer N, Min KL, Abram ME, Fletcher RS Parniak MA (2002) Mutational analysis of Tyr-501 of HIV-1 reverse transcriptase. J Biol Chem 277, 1370 1374.
38. Julias JG, McWilliams MJ, Sarafianos SG, Arnold E Hughes SH (2002) Mutations in the RNase H domain of HIV-1 reverse transcriptase affect the initiation of DNA synthesis and the specificity of RNase H cleavage in vivo. Proc Natl Acad Sci USA 99, 9515 9520.
39. Rausch JW, Lener D, Miller JT, Julias JG, Hughes SH Le Grice SF (2002) Altering the RNase H primer grip of human immunodeficiency virus reverse transcriptase modifies cleavage specificity. Biochemistry 41, 4856 4865.
40. McWilliams MJ, Julias JG, Sarafianos SG, Alvord WG, Arnold E Hughes SH (2006) Combining mutations in HIV-1 reverse transcriptase with mutations in the HIV-1 polypurine tract affects RNase H cleavages involved in PPT utilization. Virol 348, 378 388.
41. Zhang WH, Svarovskaia ES, Barr R Pathak VK (2002) Y586F mutation in murine leukemia virus reverse transcriptase decreases fidelity of DNA synthesis in regions associated with adenine-thymine tracts. Proc Natl Acad Sci USA 99, 10090 10095.
42. Mbisa JL, Nikolenko GN Pathak VK (2005) Mutations in the RNase H primer grip domain of murine leukemia virus reverse transcriptase decrease efficiency and accuracy of plus-strand DNA transfer. J Virol 79, 419 427.
43. Krug MS Berger SL (1989) Ribonuclease H activities associated with viral reverse transcriptases are endonucleases. Proc Natl Acad Sci USA 86, 3539 3543.
44. DeStefano JJ, Buiser RG, Mallaber LM, Bambara RA Fay PJ (1991) Human immunodeficiency virus reverse transcriptase displays a partially processive 3′ to 5′ endonuclease activity. J Biol Chem 266, 24295 24301.
45. Ben-Artzi H, Zeelon E, Le-Grice SF, Gorecki M Panet A (1992) Characterization of the double stranded RNA dependent RNase activity associated with recombinant reverse transcriptases. Nucleic Acids Res 20, 5115 5118.
46. Blain SW Goff SP (1993) Nuclease activities of Moloney murine leukemia virus reverse transcriptase. Mutants with altered substrate specificities. J Biol Chem 268, 23585 23592.
47. Hostomsky Z, Hughes SH, Goff SP Le Grice SF (1994) Redesignation of the RNase D activity associated with retroviral reverse transcriptase as RNase H. J Virol 68, 1970 1971.
48. Schultz SJ, Zhang M, Kelleher CD Champoux JJ (2000) Analysis of plus-strand primer selection, removal, and reutilization by retroviral reverse transcriptases. J Biol Chem 275, 32299 32309.
49. Furfine ES Reardon JE (1991) Human immunodeficiency virus reverse transcriptase ribonuclease H: specificity of tRNA(Lys3)-primer excision. Biochemistry 30, 7041 7046.
50. Pullen KA, Ishimoto LK Champoux JJ (1992) Incomplete removal of the RNA primer for minus-strand DNA synthesis by human immunodeficiency virus type 1 reverse transcriptase. J Virol 66, 367 373.
51. Rattray AJ Champoux JJ (1989) Plus-strand priming by Moloney murine leukemia virus. The sequence features important for cleavage by RNase H. J Mol Biol 208, 445 456.
52. Huber HE Richardson CC (1990) Processing of the primer for plus strand DNA synthesis by human immunodeficiency virus 1 reverse transcriptase. J Biol Chem 265, 10565 10573.
53. Nowotny M Yang W (2006) Stepwise analyses of metal ions in RNase H catalysis from substrate destabilization to product release. EMBO J 25, 1924 1933.
54. 2+-ion catalysis and substrate specificity. Mol Cell 22, 5 13.
55. Schultz SJ, Zhang M Champoux JJ (2004) Recognition of internal cleavage sites by retroviral RNases H. J Mol Biol 344, 635 652.
56. Wohrl BM, Georgiadis MM, Telesnitsky A, Hendrickson WA Le Grice SF (1995) Footprint analysis of replicating murine leukemia virus reverse transcriptase. Science 267, 96 99.
57. Wohrl BM, Tantillo C, Arnold E Le Grice SF (1995) An expanded model of replicating human immunodeficiency virus reverse transcriptase. Biochemistry 34, 5343 5356.
58. Winshell J Champoux JJ (2001) Structural alterations in the DNA ahead of the primer terminus during displacement synthesis by reverse transcriptases. J Mol Biol 306, 931 943.
59. Furfine ES Reardon JE (1991) Reverse transcriptase.RNase H from the human immunodeficiency virus. Relationship of the DNA polymerase and RNA hydrolysis activities. J Biol Chem 266, 406 412.
60. Gopalakrishnan V, Peliska JA Benkovic SJ (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.
61. Kati WM, Johnson KA, Jerva LF Anderson KS (1992) Mechanism and fidelity of HIV reverse transcriptase. J Biol Chem 267, 25988 25997.
62. DeStefano JJ, Mallaber LM, Fay PJ Bambara RA (1994) Quantitative analysis of RNA cleavage during RNA-directed DNA synthesis by human immunodeficiency and avian myeloblastosis virus reverse transcriptases. Nucleic Acids Res 22, 3793 3800.
63. Suo Z Johnson KA (1997) Effect of RNA secondary structure on RNA cleavage catalyzed by HIV-1 reverse transcriptase. Biochemistry 36, 12468 12476.
64. Suo Z Johnson KA (1997) Effect of RNA secondary structure on the kinetics of DNA synthesis catalyzed by HIV-1 reverse transcriptase. Biochemistry 36, 12459 12467.
65. Schatz O, Mous J Le Grice SF (1990) HIV-1 RT-associated ribonuclease H displays both endonuclease and 3′ → 5′ exonuclease activity. EMBO J 9, 1171 1176.
66. Wohrl BM Moelling K (1990) Interaction of HIV-1 ribonuclease H with polypurine tract containing RNA-DNA hybrids. Biochemistry 29, 10141 10147.
67. DeStefano JJ, Mallaber LM, Fay PJ Bambara RA (1993) Determinants of the RNase H cleavage specificity of human immunodeficiency virus reverse transcriptase. Nucleic Acids Res 21, 4330 4338.
68. Gotte M, Fackler S, Hermann T, Perola E, Cellai L, Gross HJ, Le Grice SF Heumann H (1995) HIV-1 reverse transcriptase-associated RNase H cleaves RNA/RNA in arrested complexes: implications for the mechanism by which RNase H discriminates between RNA/RNA and RNA/DNA. EMBO J 14, 833 841.
69. Palaniappan C, Fuentes GM, Rodriguez-Rodriguez L, Fay PJ Bambara RA (1996) Helix structure and ends of RNA/DNA hybrids direct the cleavage specificity of HIV-1 reverse transcriptase RNase H. J Biol Chem 271, 2063 2070.
70. Gao G, Orlova M, Georgiadis MM, Hendrickson WA Goff SP (1997) Conferring RNA polymerase activity to a DNA polymerase: a single residue in reverse transcriptase controls substrate selection. Proc Natl Acad Sci USA 94, 407 411.
71. Gao G Goff SP (1998) Replication defect of moloney murine leukemia virus with a mutant reverse transcriptase that can incorporate ribonucleotides and deoxyribonucleotides. J Virol 72, 5905 5911.
72. Schultz SJ, Zhang M Champoux JJ (2006) Sequence, distance, and accessibility are determinants of 5′-end-directed cleavages by retroviral RNases H. J Biol Chem 281, 1943 1955.
73. Fu TB Taylor J (1992) When retroviral reverse transcriptases reach the end of their RNA templates. J Virol 66, 4271 4278.
74. Ben-Artzi H, Zeelon E, Amit B, Wortzel A, Gorecki M Panet A (1993) RNase H activity of reverse transcriptases on substrates derived from the 5′ end of retroviral genome. J Biol Chem 268, 16465 16471.
75. DeStefano JJ (1995) The orientation of binding of human immunodeficiency virus reverse transcriptase on nucleic acid hybrids. Nucleic Acids Res 23, 3901 3908.
76. Wisniewski M, Balakrishnan M, Palaniappan C, Fay PJ Bambara RA (2000) Unique progressive cleavage mechanism of HIV reverse transcriptase RNase H. Proc Natl Acad Sci USA 97, 11978 11983.
77. Wisniewski M, Balakrishnan M, Palaniappan C, Fay PJ Bambara RA (2000) The sequential mechanism of HIV reverse transcriptase RNase H. J Biol Chem 275, 37664 37671.
78. Wisniewski M, Chen Y, Balakrishnan M, Palaniappan C, Roques BP, Fay PJ Bambara RA (2002) Substrate requirements for secondary cleavage by HIV-1 reverse transcriptase RNase H. J Biol Chem 277, 28400 28410.
79. Gilboa E, Mitra SW, Goff S Baltimore D (1979) A detailed model of reverse transcription and tests of crucial aspects. Cell 18, 93 100.
80. Telesnitsky A Goff SP (1997) Reverse transcriptase and the generation of retroviral DNA. In Retroviruses (Coffin JM, Hughes SH Varmus HE, eds), pp. 121 160. Cold Spring Harbor Laboratory Press, Plainview, NY.
81. Telesnitsky A Goff SP (1993) Two defective forms of reverse transcriptase can complement to restore retroviral infectivity. EMBO J 12, 4433 4438.
82. Kelleher CD Champoux JJ (2000) RNA degradation and primer selection by Moloney murine leukemia virus reverse transcriptase contribute to the accuracy of plus strand initiation. J Biol Chem 275, 13061 13070.
83. Driscoll MD, Golinelli MP Hughes SH (2001) In vitro analysis of human immunodeficiency virus type 1 minus-strand strong-stop DNA synthesis and genomic RNA processing. J Virol 75, 672 686.
84. Gao HQ, Sarafianos SG, Arnold E Hughes SH (2001) RNase H cleavage of the 5′ end of the human immunodeficiency virus type 1 genome. J Virol 75, 11874 11880.
85. Kelleher CD Champoux JJ (1998) Characterization of RNA strand displacement synthesis by Moloney murine leukemia virus reverse transcriptase. J Biol Chem 273, 9976 9986.
86. Finston WI Champoux JJ (1984) RNA-primed initiation of Moloney murine leukemia virus plus strands by reverse transcriptase in vitro. J Virol 51, 26 33.
87. Luo GX, Sharmeen L Taylor J (1990) Specificities involved in the initiation of retroviral plus-strand DNA. J Virol 64, 592 597.
88. Wohrl BM Moelling K (1991) Coupling of reverse transcriptase and RNase H during HIV-1 replication. Behring Inst Mitt, 89, 100 107.
89. Pullen KA, Rattray AJ Champoux JJ (1993) The sequence features important for plus strand priming by human immunodeficiency virus type 1 reverse transcriptase. J Biol Chem 268, 6221 6227.
90. Fuentes GM, Rodriguez-Rodriguez L, Fay PJ Bambara RA (1995) Use of an oligoribonucleotide containing the polypurine tract sequence as a primer by HIV reverse transcriptase. J Biol Chem 270, 28169 28176.
91. Powell MD Levin JG (1996) Sequence and structural determinants required for priming of plus-strand DNA synthesis by the human immunodeficiency virus type 1 polypurine tract. J Virol 70, 5288 5296.
92. Klarmann GJ, Yu H, Chen X, Dougherty JP Preston BD (1997) Discontinuous plus-strand DNA synthesis in human immunodeficiency virus type 1-infected cells and in a partially reconstituted cell-free system. J Virol 71, 9259 9269.
93. Schultz SJ, Zhang M, Kelleher CD Champoux JJ (1999) Polypurine tract primer generation and utilization by Moloney murine leukemia virus reverse transcriptase. J Biol Chem 274, 34547 34555.
94. Rattray AJ Champoux JJ (1987) The role of Moloney murine leukemia virus RNase H activity in the formation of plus-strand primers. J Virol 61, 2843 2851.
95. Robson ND Telesnitsky A (2000) Selection of optimal polypurine tract region sequences during Moloney murine leukemia virus replication. J Virol 74, 10293 10303.
96. Julias JG, McWilliams MJ, Sarafianos SG, Alvord WG, Arnold E Hughes SH (2004) Effects of mutations in the G tract of the human immunodeficiency virus type 1 polypurine tract on virus replication and RNase H cleavage. J Virol 78, 13315 13324.
97. Jones FD Hughes SH (2007) In vitro analysis of the effects of mutations in the G-tract of the human immunodeficiency virus type 1 polypurine tract on RNase H cleavage specificity. Virol 360, 341 349.
98. Rausch JW Le Grice SF (2007) Purine analog substitution of the HIV-1 polypurine tract primer defines regions controlling initiation of plus-strand DNA synthesis. Nucleic Acids Res 35, 256 268.
99. Schultz SJ, Zhang M Champoux JJ (2003) Specific cleavages by RNase H facilitate initiation of plus-strand RNA synthesis by Moloney murine leukemia virus. J Virol 77, 5275 5285.
100. Schultz SJ, Whiting SH Champoux JJ (1995) Cleavage specificities of Moloney murine leukemia virus RNase H implicated in the second strand transfer during reverse transcription. J Biol Chem 270, 24135 24145.
101. Randolph CA Champoux JJ (1994) The use of DNA and RNA oligonucleotides in hybrid structures with longer polynucleotide chains to probe the structural requirements for Moloney murine leukemia virus plus strand priming. J Biol Chem 269, 19207 19215.
102. Whiting SH Champoux JJ (1994) Strand displacement synthesis capability of Moloney murine leukemia virus reverse transcriptase. J Virol 68, 4747 4758.