Targeting the retroviral ribonuclease H by rational drug design

AIDS

Volumn 26, Issue 16, 2012, Pages 1983-1993

  Moelling, Karin ^a,b,c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

Author keywords

cellular ribonucleases H; HIV; inhibitors; microbicide

Indexed keywords

MICROBICIDE; NUCLEIC ACID; RIBONUCLEASE H; RNA DIRECTED DNA POLYMERASE;

ANTIVIRAL THERAPY; DNA REPLICATION; DRUG DESIGN; DRUG TARGETING; ENZYME STRUCTURE; GENE EXPRESSION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RETROVIRUS; REVIEW; STRUCTURE ANALYSIS; SUICIDE; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANTI-INFECTIVE AGENTS; DNA REPLICATION; DRUG DESIGN; GENE EXPRESSION REGULATION, VIRAL; GENE SILENCING; HIV REVERSE TRANSCRIPTASE; HIV-1; HUMANS; MUTATION; NUCLEIC ACID AMPLIFICATION TECHNIQUES; RIBONUCLEASE H; RNA, VIRAL; VIRUS REPLICATION;

EID: 84867741977     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e32835537d3     Document Type: Review

References (76)

1. Coffin JM, Hughes SH, Varmus H. Retroviruses. Plainview, New York: Cold Spring Harbor Laboratory Press; 1997.
2. Molling K, Bolognesi DP, Bauer H, Busen W, Plassmann HW, Hausen P. Association of viral reverse transcriptase with an enzyme degrading the RNA moiety of RNA-DNA hybrids. Nat New Biol 1971; 234:240-243.
3. Hansen J, Schulze T, Mellert W, Moelling K. Identification and characterization of HIV-specific RNase H by monoclonal antibody. EMBO J 1988; 7:239-243.
4. Tadokoro T, Kanaya S. Ribonuclease H molecular diversities, substrate binding domains, and catalytic mechanism of the prokaryotic enzymes. FEBS J 2009; 276:1482-1493.
5. Ma BG, Chen L, Ji HF, Chen ZH, Yang FR, Wang L, et al. Characters of very ancient proteins. Biochem Biophys Res Commun 2008; 366:607-611.
6. Nowotny M. Retroviral integrase superfamily: the structural perspective. EMBO Rep 2009; 10:144-151.
7. Cerritelli SM, Crouch RJ. Ribonuclease H: the enzymes in eukaryotes. FEBS J 2009; 276:1494-1505.
8. Song JJ, Smith SK, Hannon GJ, Joshua-Tor L. Crystal structure of Argonaute and its implications for RISC slicer activity. Science 2004; 305:1434-1437.
9. Kochiwa H, Tomita M, Kanai A. Evolution of ribonuclease H genes in prokaryotes to avoid inheritance of redundant genes. BMC Evol Biol 2007; 7:128.
10. Kochiwa H, Itaya M, Tomita M, Kanai A. Stage-specific expression of Caenorhabditis elegans ribonuclease H1 enzymes with different substrate specificities and bivalent cation requirements. FEBS J 2006; 273:420-429.
11. Jozwiakowski SK, Connolly BA. A modified family-B archaeal DNA polymerase with reverse transcriptase activity. Chem-biochem 2011; 12:35-37.
12. Cerritelli SM, Frolova EG, Feng C, Grinberg A, Love PE, Crouch RJ. Failure to produce mitochondrial DNA results in embryonic lethality in Rnaseh1 null mice. Mol Cell 2003; 11:807-815.
13. Crow YJ, Leitch A, Hayward BE, Garner A, Parmar R, Griffith E, et al. Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutieres syndrome and mimic congenital viral brain infection. Nat Genet 2006; 38:910-916.
14. Kwok T, Heinrich J, Jung-Shiu J, Meier MG, Mathur S, Moelling K. Reduction of gene expression by a hairpin-loop structured oligodeoxynucleotide: alternative to siRNA and antisense. Biochim Biophys Acta 2009; 1790:1170-1178.
15. Cerritelli SM, Chon H, Crouch RJ. Molecular biology. A new twist for topoisomerase. Science 2011; 332:1510-1511.
16. Matskevich AA, Moelling K. Dicer is involved in protection against influenza A virus infection. J Gen Virol 2007; 88:2627-2635.
17. Matskevich AA, Moelling K. Stimuli-dependent cleavage of Dicer during apoptosis. Biochem J 2008; 412:527-534.
18. Moelling K, Matskevich A, Jung JS. Relationship between retro-viral replication and RNA interference machineries. Cold Spring Harb Symp Quant Biol 2006; 71:365-368.
19. Flint SJ. American Society for Microbiology. Principles of virology. 3rd ed. Washington, District of Columbia: ASM Press; 2009.
20. Schulze T, Nawrath M, Moelling K. Cleavage of the HIV-1 p66 reverse transcriptase/RNase H by the p9 protease in vitro generates active p15 RNase H. Arch Virol 1991; 118:179-188.
21. Moelling K. Reverse transcriptase and RNase H: present in a murine virus and in both subunits of an avian virus. Cold Spring Harb Symp Quant Biol 1975; 39 (Pt 2):969-973.
22. Sarafianos SG, Das K, Tantillo C, Clark AD Jr, Ding J, Whitcomb JM, et al. Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA. EMBO J 2001; 20:1449-1461.
23. Wohrl BM, Volkmann S, Moelling K. Mutations of a conserved residue within HIV-1 ribonuclease H affect its exo-and en-donuclease activities. J Mol Biol 1991; 220:801-818.
24. Volkmann S, Jendis J, Frauendorf A, Moelling K. Inhibition of HIV-1 reverse transcription by triple-helix forming oligonucleo-tides with viral RNA. Nucleic Acids Res 1995; 23:1204-1212.
25. Mougel M, Cimarelli A, Darlix JL. Implications of the nucleo-capsid and the microenvironment in retroviral reverse transcription. Viruses 2010; 2:939-960.
26. Muller G, Strack B, Dannull J, Sproat BS, Surovoy A, Jung G, et al. Amino acid requirements of the nucleocapsid protein of HIV-1 for increasing catalytic activity of a Ki-ras ribozyme in vitro. J Mol Biol 1994; 242:422-429.
27. Levin JG, Mitra M, Mascarenhas A, Musier-Forsyth K. Role of HIV-1 nucleocapsid protein in HIV-1 reverse transcription. RNA Biol 2010; 7:754-774.
28. Dannull J, Surovoy A, Jung G, Moelling K. Specific binding of HIV-1 nucleocapsid protein to PSI RNA in vitro requires N-terminal zinc finger and flanking basic amino acid residues. EMBO J 1994; 13:1525-1533.
29. Wohrl BM, Moelling K. Interaction of HIV-1 ribonuclease H with polypurine tract containing RNA-DNA hybrids. Biochemistry 1990; 29:10141-10147.
30. Brinson RG, Turner KB, Yi-Brunozzi HY, Le Grice SF, Fabris D, Marino JP. Probing anomalous structural features in polypurine tract-containing RNA-DNA hybrids with neomycin B. Biochemistry 2009; 48:6988-6997.
31. Beilhartz GL, Wendeler M, Baichoo N, Rausch J, Le Grice S, Gotte M. HIV-1 reverse transcriptase can simultaneously engage its DNA/RNA substrate at both DNA polymerase and RNase H active sites: implications for RNase H inhibition. J Mol Biol 2009; 388:462-474.
32. Gotte M, Rausch JW, Marchand B, Sarafianos S, Le Grice SF. Reverse transcriptase in motion: conformational dynamics of enzyme-substrate interactions. Biochim Biophys Acta 2010; 1804:1202-1212.
33. Tisdale M, Schulze T, Larder BA, Moelling K. Mutations within the RNase H domain of human immunodeficiency virus type 1 reverse transcriptase abolish virus infectivity. J Gen Virol 1991; 72 (Pt 1):59-66.
34. Volkmann S, Wohrl BM, Tisdale M, Moelling K. Enzymatic analysis of two HIV-1 reverse transcriptase mutants with mutations in carboxyl-terminal amino acid residues conserved among retroviral ribonucleases H. J Biol Chem 1993; 268: 2674-2683.
35. Champoux JJ, Schultz SJ. Ribonuclease H: properties, substrate specificity and roles in retroviral reverse transcription. FEBS J 2009; 276:1506-1516.
36. Blackburn EH. Telomeres and telomerase: their mechanisms of action and the effects of altering their functions. FEBS Lett 2005; 579:859-862.
37. Bushman FD, Malani N, Fernandes J, D'Orso I, Cagney G, Diamond TL, et al. Host cell factors in HIV replication: meta-analysis of genome-wide studies. PLoS Pathog 2009; 5:e1000437.
38. van den Boorn JG, Schlee M, Coch C, Hartmann G. SiRNA delivery with exosome nanoparticles. Nat Biotechnol 2011; 29:325-326.
39. Eekels JJ, Berkhout B. Toward a durable treatment of HIV-1 infection using RNA interference. Prog Mol Biol Transl Sci 2011; 102:141-163.
40. Westerhout EM, Berkhout B. A systematic analysis of the effect of target RNA structure on RNA interference. Nucleic Acids Res 2007; 35:4322-4330.
41. Volkmann S, Dannull J, Moelling K. The polypurine tract, PPT, of HIV as target for antisense and triple-helix-forming oligo-nucleotides. Biochimie 1993; 75:71-78.
42. Giovannangeli C, Helene C. Progress in developments of triplex-based strategies. Antisense Nucleic Acid Drug Dev 1997; 7:413-421.
43. Postel EH, Berberich SJ, Flint SJ, Ferrone CA. Human c-myc transcription factor PuF identified as nm23-H2 nucleoside diphosphate kinase, a candidate suppressor of tumor metastasis. Science 1993; 261:478-480.
44. Huppert JL. Structure, location and interactions of G-quadru-plexes. FEBS J 2010; 277:3452-3458.
45. Ditzler MA, Bose D, Shkriabai N, Marchand B, Sarafianos SG, Kvaratskhelia M, et al. Broad-spectrum aptamer inhibitors of HIV reverse transcriptase closely mimic natural substrates. Nucleic Acids Res 2011; 39:8237-8247.
46. Hutter G, Nowak D, Mossner M, Ganepola S, Mussig A, Allers K, et al. Long-term control of HIV by CCR5 delta32/delta32 stem-cell transplantation. N Engl J Med 2009; 360:692-698.
47. Su HP, Yan Y, Prasad GS, Smith RF, Daniels CL, Abeywickrema PD, Reid JC, et al. The development of antiviral therapy and its impact on the HIV-1/AIDS pandemic [review]. Antiviral Res 2010; 85:1-18.
48. Su HP, Yan Y, Prasad GS, Smith RF, Daniels CL, Abeywickrema PD, et al. Structural basis for the inhibition of RNase H activity of HIV-1 reverse transcriptase by RNase H active site-directed inhibitors. J Virol 2010; 84:7625-7633.
49. Chung S, Wendeler M, Rausch JW, Beilhartz G, Gotte M, O'Keefe BR, et al. Structure-activity analysis ofvinylogous urea inhibitors of human immunodeficiency virus-encoded ribonuclease H. Antimicrob Agents Chemother 2010; 54:3913-3921.
50. Moelling K, Schulze T, Diringer H. Inhibition of human immunodeficiency virus type 1 RNase H by sulfated polyanions. J Virol 1989; 63:5489-5491.
51. Tramontano E, Di Santo R. HIV-1 RT-associated RNase H function inhibitors: recent advances in drug development. Curr Med Chem 2010; 17:2837-2853.
52. Matskevich AA, Ziogas A, Heinrich J, Quast SA, Moelling K. Short partially double-stranded oligodeoxynucleotide induces reverse transcriptase/RNase H-mediated cleavage of HIV RNA and contributes to abrogation of infectivity of virions. AIDS Res Hum Retroviruses 2006; 22:1220-1230.
53. Himmel DM, Sarafianos SG, Dharmasena S, Hossain MM, McCoy-Simandle K, Ilina T, et al. HIV-1 reverse transcriptase structure with RNase H inhibitor dihydroxy benzoyl naphthyl hydrazone bound at a novel site. ACS Chem Biol 2006; 1:702-712.
54. Himmel DM, Maegley KA, Pauly TA, Bauman JD, Das K, Dharia C, et al. Structure of HIV-1 reverse transcriptase with the inhibitor beta-Thujaplicinol bound at the RNase H active site. Structure 2009; 17:1625-1635.
55. Lansdon EB, Liu Q, Leavitt SA, Balakrishnan M, Perry JK, Lan-caster-Moyer C, et al. Structural and binding analysis of pyr-imidinol carboxylic acid and N-hydroxy quinazolinedione HIV-1 RNase H inhibitors. Antimicrob Agents Chemother 2011; 55:2905-2915.
56. Shaw-Reid CA, Munshi V, Graham P, Wolfe A, Witmer M, Danzeisen R, et al. Inhibition of HIV-1 ribonuclease H by a novel diketo acid, 4-[5-(benzoylamino) thien-2-yl.]-2,4-dioxo-butanoic acid. J Biol Chem 2003; 278:2777-2780.
57. Eigen M. Error catastrophe and antiviral strategy. Proc Natl Acad Sci USA 2002; 99:13374-13376.
58. Matzen K, Elzaouk L, Matskevich AA, Nitzsche A, Heinrich J, Moelling K. RNase H-mediated retrovirus destruction in vivo triggered by oligodeoxynucleotides. Nat Biotechnol 2007; 25:669-674.
59. Johnson WE. Assisted suicide for retroviruses. Nat Biotechnol 2007; 25:643-644.
60. Moelling K, Abels S, Jendis J, Matskevich A, Heinrich J. Silencing of HIV by hairpin-loop-structured DNA oligonucleotide. FEBS Lett 2006; 580:3545-3550.
61. Jendis J, Strack B, Volkmann S, Boni J, Molling K. Inhibition of replication of fresh HIV type 1 patient isolates by a polypurine tract-specific self-complementary oligodeoxynucleotide. AIDS Res Hum Retroviruses 1996; 12:1161-1168.
62. Jendis J, Strack B, Moelling K. Inhibition of replication of drug-resistant HIV type 1 isolates by polypurine tract-specific oli-godeoxynucleotide TFO A. AIDS Res Hum Retroviruses 1998; 14:999-1005.
63. Heinrich J, Mathur S, Matskevich AA, Moelling K. Oligonucleo-tide- mediated retroviral RNase H activation leads to reduced HIV-1 titer in patient-derived plasma. AIDS 2009; 23:213-221.
64. Wittmer-Elzaouk L, Jung-Shiu J, Heinrich J, Moelling K. Retro-viral self-inactivation in the mouse vagina induced by short DNA. Antiviral Res 2009; 82:22-28.
65. Heinrich J, Schols D, Moelling K. A short hairpin loop-structured oligodeoxynucleotide targeting the virion-associated RNase H of HIV inhibits HIV production in cell culture and in huPBL-SCID mice. Intervirology 2012; 55:242-246.
66. Noreen F, Heinrich J, Moelling K. Antitumor activity of small double-stranded oligodeoxynucleotides targeting telomerase RNA in malignant melanoma cells. Oligonucleotides 2009; 19:169-178.
67. Moelling K, Broecker F, Karrigan JE. Methods and protocols. In: Poli G, Vicenzi E, editors. Human retroviruses. RNase H: Specificity, Mechanism of Action and Antiviral Target. New York: Springer Science and Business Media, LLC.
68. Nowotny M, Gaidamakov SA, Crouch RJ, Yang W. Crystal structures of RNase Hboundto an RNA/DNA hybrid: substrate specificity and metal-dependent catalysis. Cell 2005; 121: 1005-1016.
69. Malik HS, Eickbush TH. Phylogenetic analysis of ribonuclease H domains suggests a late, chimeric origin of LTR retrotran-sposable elements and retroviruses. Genome Res 2001; 11:1187-1197.
70. Felts AK, Labarge K, Bauman JD, Patel DV, Himmel DM, Arnold E, et al. Identification of alternative binding sites for inhibitors of HIV-1 ribonuclease H through comparative analysis of virtual enrichment studies. J Chem Inf Model 2011; 51: 1986-1998.
71. Dunn LL, McWilliams MJ, Das K, Arnold E, Hughes SH. Mutations in the thumb allow human immunodeficiency virus type 1 reverse transcriptase to be cleaved by protease in virions. J Virol 2009; 83:12336-12344.
72. Takada K, Bermingham A, O'Keefe BR, Wamiru A, Beutler JA, Le Grice SF, et al. An HIV RNase H inhibitory 1,3,4,5-tetra-galloylapiitol from the African plant Hylodendron gabunensis. J Nat Prod 2007; 70:1647-1649.
73. Kirschberg TA, Balakrishnan M, Squires NH, Barnes T, Brendza KM, Chen X, et al. RNase H active site inhibitors of human immunodeficiency virus type 1 reverse transcriptase: design, biochemical activity, and structural information. J Med Chem 2009; 52:5781-5784.
74. Budihas SR, Gorshkova I, Gaidamakov S, Wamiru A, Bona MK, Parniak MA, et al. Selective inhibition of HIV-1 reverse tran-scriptase-associated ribonuclease H activity by hydroxylated tropolones. Nucleic Acids Res 2005; 33:1249-1256.
75. Dat NT, Bae K, Wamiru A, McMahon JB, Le Grice SF, Bona M, et al. A dimeric lactone from Ardisia japonica with inhibitory activity for HIV-1 and HIV-2 ribonuclease H. J Nat Prod 2007; 70:839-841.
76. Bokesch HR, Wamiru A, Le Grice SF, Beutler JA, McKee TC, McMahon JB. HIV-1 ribonuclease H inhibitory phenolic glyco-sides from Eugenia hyemalis. J Nat Prod 2008; 71:1634-1636.