FRET-based assay to screen inhibitors of HIV-1 reverse transcriptase and nucleocapsid protein

Nucleic Acids Research

Volumn 44, Issue 8, 2016, Pages e74-

  Sharma, Kamal K ^a   Przybilla, Frédéric ^a   Restle, Tobias ^b   Godet, Julien ^a,c   Mély, Yves ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^c UNIVERSITY HOSPITAL OF STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOCAPSID PROTEIN; PROTEIN NCP7; RNA DIRECTED DNA POLYMERASE; UNCLASSIFIED DRUG; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; GAG PROTEIN; NCP7 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; NEVIRAPINE; REVERSE TRANSCRIPTASE, HUMAN IMMUNODEFICIENCY VIRUS 1; RNA DIRECTED DNA POLYMERASE INHIBITOR; VIRUS DNA; VIRUS RNA; ZIDOVUDINE;

ANTIVIRAL THERAPY; ARTICLE; CONTROLLED STUDY; DNA TEMPLATE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HIGH THROUGHPUT SCREENING; HUMAN IMMUNODEFICIENCY VIRUS 1; IC50; IN VITRO STUDY; MUTANT; PRIORITY JOURNAL; PROTEIN FUNCTION; REVERSE TRANSCRIPTION; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; HUMAN; PRECLINICAL STUDY; PROCEDURES;

ANTI-HIV AGENTS; DNA, VIRAL; DRUG EVALUATION, PRECLINICAL; FLUORESCENCE RESONANCE ENERGY TRANSFER; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIGH-THROUGHPUT SCREENING ASSAYS; HIV REVERSE TRANSCRIPTASE; HIV-1; HUMANS; NEVIRAPINE; REVERSE TRANSCRIPTASE INHIBITORS; RNA, VIRAL; ZIDOVUDINE;

EID: 84966440899     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1532     Document Type: Article

References (80)

1. Le Grice,S.F. (2012) Human immunodeficiency virus reverse transcriptase: 25 years of research, drug discovery, and promise. J. Biol. Chem., 287, 40850-40857.
2. 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. et al. (1993) Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A resolution shows bent DNA. Proc. Natl. Acad. Sci. U.S.A., 90, 6320-6324.
3. Kohlstaedt,L.A., Wang,J., Friedman,J.M., Rice,P.A. and Steitz,T.A. (1992) Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science, 256, 1783-1790.
4. Hachiya,A., Shimane,K., Sarafianos,S.G., Kodama,E.N., Sakagami,Y., Negishi,F., Koizumi,H., Gatanaga,H., Matsuoka,M., Takiguchi,M. et al. (2009) Clinical relevance of substitutions in the connection subdomain and RNase H domain of HIV-1 reverse transcriptase from a cohort of antiretroviral treatment-naive patients. Antiviral Res., 82, 115-121.
5. Barber,A.M., Hizi,A., Maizel,J.V. Jr and Hughes,S.H. (1990) HIV-1 reverse transcriptase: structure predictions for the polymerase domain. AIDS Res. Hum. Retroviruses, 6, 1061-1072.
6. Li,X., Zhang,L., Tian,Y., Song,Y., Zhan,P. and Liu,X. (2014) Novel HIV-1 non-nucleoside reverse transcriptase inhibitors: a patent review (2011-2014). Expert Opin. Ther. Pat., 24, 1199-1227.
7. Paydary,K., Khaghani,P., Emamzadeh-Fard,S., Alinaghi,S.A. and Baesi,K. (2013) The emergence of drug resistant HIV variants and novel anti-retroviral therapy. AsianPac.J.Trop.Biomed., 3, 515-522.
8. Althaus,I.W., Chou,J.J., Gonzales,A.J., Deibel,M.R., Chou,K.C., Kezdy,F.J., Romero,D.L., Aristoff,P.A., Tarpley,W.G. and Reusser,F. (1993) Steady-state kinetic studies with the non-nucleoside HIV-1 reverse transcriptase inhibitor U-87201E. J. Biol. Chem., 268, 6119-6124.
9. Althaus,I.W., Chou,J.J., Gonzales,A.J., Deibel,M.R., Chou,K.C., Kezdy,F.J., Romero,D.L., Palmer,J.R., Thomas,R.C., Aristoff,P.A. et al. (1993) Kinetic studies with the non-nucleoside HIV-1 reverse transcriptase inhibitor U-88204E. Biochemistry, 32, 6548-6554.
10. Domaoal,R.A. and Demeter,L.M. (2004) Structural and biochemical effects of human immunodeficiency virus mutants resistant to non-nucleoside reverse transcriptase inhibitors. Int. J. Biochem. Cell Biol., 36, 1735-1751.
11. Sarafianos,S.G., Das,K., Hughes,S.H. and Arnold,E. (2004) Taking aim at a moving target: designing drugs to inhibit drug-resistant HIV-1 reverse transcriptases. Curr. Opin. Struct. Biol., 14, 716-730.
12. Sarafianos,S.G., Hughes,S.H. and Arnold,E. (2004) Designing anti-AIDS drugs targeting the major mechanism of HIV-1 RT resistance to nucleoside analog drugs. Int. J. Biochem. Cell Biol., 36, 1706-1715.
13. Darlix,J.L., Garrido,J.L., Morellet,N., Mély,Y. and de Rocquigny,H. (2007) Properties, functions, and drug targeting of the multifunctional nucleocapsid protein of the human immunodeficiency virus. Adv. Pharmacol., 55, 299-346.
14. Goldschmidt,V., Jenkins,L.M.M., de Rocquigny,H., Darlix,J.-L. and Mély,Y. (2010) The nucleocapsid protein of HIV-1 as a promising therapeutic target for antiviral drugs. HIV Ther., 4, 179-198.
15. Mori,M., Kovalenko,L., Lyonnais,S., Antaki,D., Torbett,B.E., Botta,M., Mirambeau,G. and Mely,Y. (2015) Nucleocapsid protein: a desirable target for future therapies against HIV-1. Curr. Top. Microbiol. Immunol., 389, 53-92.
16. Darlix,J.L., Godet,J., Ivanyi-Nagy,R., Fosse,P., Mauffret,O. and Mely,Y. (2011) Flexible nature and specific functions of the HIV-1 nucleocapsid protein. J. Mol. Biol., 410, 565-581.
17. Godet,J. and Mely,Y. (2010) Biophysical studies of the nucleic acid chaperone properties of the HIV-1 nucleocapsid protein. RNA Biol., 7, 687-699.
18. Levin,J.G., Mitra,M., Mascarenhas,A. and Musier-Forsyth,K. (2010) Role of HIV-1 nucleocapsid protein in HIV-1 reverse transcription. RNA Biol., 7, 754-774.
19. Thomas,J.A. and Gorelick,R.J. (2008) Nucleocapsid protein function in early infection processes. Virus Res., 134, 39-63.
20. Anthony,R.M. and Destefano,J.J. (2007) In vitro synthesis of long DNA products in reactions with HIV-RT and nucleocapsid protein. J. Mol. Biol., 365, 310-324.
21. Levin,J.G., Guo,J., Rouzina,I. and Musier-Forsyth,K. (2005) Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog. Nucleic Acid Res. Mol. Biol., 80, 217-286.
22. Bampi,C., Bibillo,A., Wendeler,M., Divita,G., Gorelick,R.J., Le Grice,S.F. and Darlix,J.L. (2006) Nucleotide excision repair and template-independent addition by HIV-1 reverse transcriptase in the presence of nucleocapsid protein. J. Biol. Chem., 281, 11736-11743.
23. Grohmann,D., Godet,J., Mely,Y., Darlix,J.L. and Restle,T. (2008) HIV-1 nucleocapsid traps reverse transcriptase on nucleic acid substrates. Biochemistry, 47, 12230-12240.
24. Tanchou,V., Delaunay,T., Bodeus,M., Roques,B., Darlix,J.L. and Benarous,R. (1995) Conformational changes between human immunodeficiency virus type 1 nucleocapsid protein NCp7 and its precursor NCp15 as detected by anti-NCp7 monoclonal antibodies. J. Gen. Virol., 76, 2457-2466.
25. Druillennec,S., Caneparo,A., de Rocquigny,H. and Roques,B.P. (1999) Evidence of interactions between the nucleocapsid protein NCp7 and the reverse transcriptase of HIV-1. J. Biol. Chem., 274, 11283-11288.
26. Kim,J., Roberts,A., Yuan,H., Xiong,Y. and Anderson,K.S. (2012) Nucleocapsid protein annealing of a primer-template enhances (+)-strand DNA synthesis and fidelity by HIV-1 reverse transcriptase. J. Mol. Biol., 415, 866-880.
27. Lener,D., Tanchou,V., Roques,B.P., Le Grice,S.F. and Darlix,J.L. (1998) Involvement of HIV-I nucleocapsid protein in the recruitment of reverse transcriptase into nucleoprotein complexes formed in vitro. J. Biol. Chem., 273, 33781-33786.
28. Antoun,M.D., Rios,Y.R., Mendoza,N.T. and Proctor,G. (1994) Reverse transcriptase inhibition as prescreen for potential antiviral bioactives. P.R. Health Sci. J., 13, 17-18.
29. Chang,A., Ostrove,J.M. and Bird,R.E. (1997) Development of an improved product enhanced reverse transcriptase assay. J. Virol. Methods, 65, 45-54.
30. Hizi,A., Tal,R., Shaharabany,M., Currens,M.J., Boyd,M.R., Hughes,S.H. and McMahon,J.B. (1993) Specific inhibition of the reverse transcriptase of human immunodeficiency virus type 1 and the chimeric enzymes of human immunodeficiency virus type 1 and type 2 by nonnucleoside inhibitors. Antimicrob. Agents Chemother., 37, 1037-1042.
31. Kanyara,J.N. and Njagi,E.N. (2005) Anti-HIV-1 activities in extracts from some medicinal plants as assessed in an in vitro biochemical HIV-1 reverse transcriptase assay. Phytother. Res., 19, 287-290.
32. Krebs,J.F. and Kore,A.R. (2008) Novel FRET-based assay to detect reverse transcriptase activity using modified dUTP analogues. Bioconjug. Chem., 19, 185-191.
33. Lovatt,A., Black,J., Galbraith,D., Doherty,I., Moran,M.W., Shepherd,A.J., Griffen,A., Bailey,A., Wilson,N. and Smith,K.T. (1999) High throughput detection of retrovirus-associated reverse transcriptase using an improved fluorescent product enhanced reverse transcriptase assay and its comparison to conventional detection methods. J. Virol. Methods, 82, 185-200.
34. Odawara,F., Abe,H., Kohno,T., Nagai-Fujii,Y., Arai,K., Imamura,S., Misaki,H., Azuma,H., Ikebuchi,K., Ikeda,H. et al. (2002) A highly sensitive chemiluminescent reverse transcriptase assay for human immunodeficiency virus. J. Virol. Methods, 106, 115-124.
35. Porstmann,T., Meissner,K., Glaser,R., Dopel,S.H. and Sydow,G. (1991) A sensitive non-isotopic assay specific for HIV-1 associated reverse transcriptase. J. Virol. Methods, 31, 181-188.
36. Silver,J., Maudru,T., Fujita,K. and Repaske,R. (1993) An RT-PCR assay for the enzyme activity of reverse transcriptase capable of detecting single virions. Nucleic Acids Res., 21, 3593-3594.
37. Suzuki,K., Craddock,B.P., Kano,T. and Steigbigel,R.T. (1993) Colorimetric reverse transcriptase assay for HIV-1. J. Virol. Methods, 41, 21-28.
38. Suzuki,K., Craddock,B.P., Kano,T. and Steigbigel,R.T. (1993) Chemiluminescent enzyme-linked immunoassay for reverse transcriptase, illustrated by detection of HIV reverse transcriptase. Anal. Biochem., 210, 277-281.
39. Suzuki,K., Craddock,B.P., Okamoto,N., Kano,T. and Steigbigel,R.T. (1993) Poly A-linked colorimetric microtiter plate assay for HIV reverse transcriptase. J. Virol. Methods, 44, 189-198.
40. Suzuki,K., Craddock,B.P., Okamoto,N., Kano,T. and Steigbigel,R.T. (1993) Detection of human immunodeficiency virus (HIV) by colorimetric assay for reverse transcriptase activity on magnetic beads. Biotechnol. Appl. Biochem., 18 37-44.
41. Urabe,T., Sano,K., Tanno,M., Mizoguchi,J., Otani,M., Lee,M.H., Takasaki,T., Kusakabe,H., Imagawa,D.T. and Nakai,M. (1992) A non-radioisotopic reverse transcriptase assay using biotin-11-deoxyuridinetriphosphate on primer-immobilized microtiter plates. J. Virol. Methods, 40, 145-154.
42. Vassiliou,W., Epp,J.B., Wang,B.B., Del Vecchio,A.M., Widlanski,T. and Kao,C.C. (2000) Exploiting polymerase promiscuity: a simple colorimetric RNA polymerase assay. Virology, 274, 429-437.
43. Abbondanzieri,E.A., Bokinsky,G., Rausch,J.W., Zhang,J.X., Le Grice,S.F. and Zhuang,X. (2008) Dynamic binding orientations direct activity of HIV reverse transcriptase. Nature, 453, 184-189.
44. Kellinger,M.W. and Johnson,K.A. (2011) Role of induced fit in limiting discrimination against AZT by HIV reverse transcriptase. Biochemistry, 50, 5008-5015.
45. Kirmizialtin,S., Nguyen,V., Johnson,K.A. and Elber,R. (2012) How conformational dynamics of DNA polymerase select correct substrates: experiments and simulations. Structure, 20, 618-627.
46. Liu,S., Abbondanzieri,E.A., Rausch,J.W., Le Grice,S.F. and Zhuang,X. (2008) Slide into action: dynamic shuttling of HIV reverse transcriptase on nucleic acid substrates. Science, 322, 1092-1097.
47. Schauer,G.D., Huber,K.D., Leuba,S.H. and Sluis-Cremer,N. (2014) Mechanism of allosteric inhibition of HIV-1 reverse transcriptase revealed by single-molecule and ensemble fluorescence. Nucleic Acids Res., 42, 11687-11696.
48. Sharma,K.K., Przybilla,F., Restle,T., Boudier,C., Godet,J. and Mely,Y. (2015) Reverse transcriptase in action: FRET-based assay for monitoring flipping and polymerase activity in real time. Anal. Chem., 87, 7690-7697.
49. Muller,B., Restle,T., Weiss,S., Gautel,M., Sczakiel,G. and Goody,R.S. (1989) Co-expression of the subunits of the heterodimer of HIV-1 reverse transcriptase in Escherichia coli. J. Biol. Chem., 264, 13975-13978.
50. Schatz,O., Cromme,F.V., Gruninger-Leitch,F. and Le Grice,S.F. (1989) Point mutations in conserved amino acid residues within the C-terminal domain of HIV-1 reverse transcriptase specifically repress RNase H function. FEBS Lett., 257, 311-314.
51. Shvadchak,V., Sanglier,S., Rocle,S., Villa,P., Haiech,J., Hibert,M., Van Dorsselaer,A., Mely,Y. and de Rocquigny,H. (2009) Identification by high throughput screening of small compounds inhibiting the nucleic acid destabilization activity of the HIV-1 nucleocapsid protein. Biochimie, 91, 916-923.
52. Klarmann,G.J., Schauber,C.A. and Preston,B.D. (1993) Template-directed pausing of DNA synthesis by HIV-1 reverse transcriptase during polymerization of HIV-1 sequences in vitro. J. Biol. Chem., 268, 9793-9802.
53. Kati,W.M., Johnson,K.A., Jerva,L.F. and Anderson,K.S. (1992) Mechanism and fidelity of HIV reverse transcriptase. J. Biol. Chem., 267, 25988-25997.
54. Sarafianos,S.G., Pandey,V.N., Kaushik,N. and Modak,M.J. (1995) Site-directed mutagenesis of arginine 72 of HIV-1 reverse transcriptase. Catalytic role and inhibitor sensitivity. J. Biol. Chem., 270, 19729-19735.
55. Sarafianos,S.G., Pandey,V.N., Kaushik,N. and Modak,M.J. (1995) Glutamine 151 participates in the substrate dNTP binding function of HIV-1 reverse transcriptase. Biochemistry, 34, 7207-7216.
56. Chi,Q., Wang,G. and Jiang,J. (2013) The persistence length and length per base of single-stranded DNA obtained from fluorescence correlation spectroscopy measurements using mean field theory. Phys. A Stat. Mech. Appl., 392, 1072-1079.
57. Wright,K. (1986) AIDS therapy. First tentative signs of therapeutic promise. Nature, 323, 283.
58. Martin,L. (2009) Benchmark Dose Software (BMDS) Version 2.1 User's Manual Version 2.0. United States Environmental Protection Agency, Office of Environmental Information., Washington, DC.
59. Caliendo,A.M., Savara,A., An,D., DeVore,K., Kaplan,J.C. and D'Aquila,R.T. (1996) Effects of zidovudine-selected human immunodeficiency virus type 1 reverse transcriptase amino acid substitutions on processive DNA synthesis and viral replication. J. Virol., 70, 2146-2153.
60. Richman,D., Rosenthal,A.S., Skoog,M., Eckner,R.J., Chou,T.C., Sabo,J.P. and Merluzzi,V.J. (1991) BI-RG-587 is active against zidovudine-resistant human immunodeficiency virus type 1 and synergistic with zidovudine. Antimicrob. Agents Chemother., 35, 305-308.
61. Zhang,J.H., Chung,T.D. and Oldenburg,K.R. (1999) A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J. Biomol. Screen., 4, 67-73.
62. Cohen,J. (1997) HIV suppressed long after treatment. Science, 277, 1927.
63. Cohen,J. (1997) Novel campaign to test live HIV vaccine. Science, 277, 1035.
64. Cohen,J. (1997) The daunting challenge of keeping HIV suppressed. Science, 277, 32-33.
65. Finzi,D., Hermankova,M., Pierson,T., Carruth,L.M., Buck,C., Chaisson,R.E., Quinn,T.C., Chadwick,K., Margolick,J., Brookmeyer,R. et al. (1997) Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science, 278, 1295-1300.
66. Gulnik,S.V., Suvorov,L.I., Liu,B., Yu,B., Anderson,B., Mitsuya,H. and Erickson,J.W. (1995) Kinetic characterization and cross-resistance patterns of HIV-1 protease mutants selected under drug pressure. Biochemistry, 34, 9282-9287.
67. Wong,J.K., Gunthard,H.F., Havlir,D.V., Zhang,Z.Q., Haase,A.T., Ignacio,C.C., Kwok,S., Emini,E. and Richman,D.D. (1997) Reduction of HIV-1 in blood and lymph nodes following potent antiretroviral therapy and the virologic correlates of treatment failure. Proc. Natl. Acad. Sci. U.S.A., 94, 12574-12579.
68. Wong,J.K., Hezareh,M., Gunthard,H.F., Havlir,D.V., Ignacio,C.C., Spina,C.A. and Richman,D.D. (1997) Recovery of replication-competent HIV despite prolonged suppression of plasma viremia. Science, 278, 1291-1295.
69. Vercruysse,T., Basta,B., Dehaen,W., Humbert,N., Balzarini,J., Debaene,F., Sanglier-Cianferani,S., Pannecouque,C., Mely,Y. and Daelemans,D. (2012) A phenyl-thiadiazolylidene-amine derivative ejects zinc from retroviral nucleocapsid zinc fingers and inactivates HIV virions. Retrovirology, 9, 95-109.
70. Green,L.M. and Berg,J.M. (1990) Retroviral nucleocapsid protein-metal ion interactions: folding and sequence variants. Proc. Natl. Acad. Sci. U.S.A., 87, 6403-6407.
71. Beltz,H., Clauss,C., Piemont,E., Ficheux,D., Gorelick,R.J., Roques,B., Gabus,C., Darlix,J.L., de Rocquigny,H. and Mely,Y. (2005) Structural determinants of HIV-1 nucleocapsid protein for cTAR DNA binding and destabilization, and correlation with inhibition of self-primed DNA synthesis. J. Mol. Biology, 348, 1113-1126.
72. Griep,M.A. (1995) Fluorescence recovery assay: a continuous assay for processive DNA polymerases applied specifically to DNA polymerase III holoenzyme. Anal. Biochem., 232, 180-189.
73. Ma,C.B., Comerford,L., Wilson,J. and Puttlitz,C.M. (2006) Biomechanical evaluation of arthroscopic rotator cuff repairs: double-row compared with single-row fixation. J. Bone Joint Surg. Am., 88, 403-410.
74. Schwartz,J.J. and Quake,S.R. (2009) Single molecule measurement of the 'speed limit' of DNA polymerase. Proc. Natl. Acad. Sci. U.S.A., 106, 20294-20299.
75. Seville,M., West,A.B., Cull,M.G. and McHenry,C.S. (1996) Fluorometric assay for DNA polymerases and reverse transcriptase. Biotechniques, 21, 664-672.
76. Tveit,H. and Kristensen,T. (2001) Fluorescence-based DNA polymerase assay. Anal. Biochem., 289, 96-98.
77. Joyce,C.M. (2010) Techniques used to study the DNA polymerase reaction pathway. Biochim. Biophys. Acta, 1804, 1032-1040.
78. Horowitz,R.W., Zhang,H., Schwartz,E.L., Ladner,R.D. and Wadler,S. (1997) Measurement of deoxyuridine triphosphate and thymidine triphosphate in the extracts of thymidylate synthase-inhibited cells using a modified DNA polymerase assay. Biochem. Pharmacol., 54, 635-638.
79. Sherman,P.A. and Fyfe,J.A. (1989) Enzymatic assay for deoxyribonucleoside triphosphates using synthetic oligonucleotides as template primers. Anal. Biochem., 180, 222-226.
80. Smid,K., Van Moorsel,C.J., Noordhuis,P., Voorn,D.A. and Peters,G.J. (2001) Interference of gemcitabine triphosphate with the measurements of deoxynucleotides using an optimized DNA polymerase elongation assay. Int. J. Oncol., 19, 157-162.