A stably expressed llama single-domain intrabody targeting Rev displays broad-spectrum anti-HIV activity

Antiviral Research

Volumn 112, Issue , 2014, Pages 91-102

  Boons, Eline ^a   Li, Guangdi ^a   Vanstreels, Els ^a   Vercruysse, Thomas ^a   Pannecouque, Christophe ^a   Vandamme, Anne Mieke ^a,b   Daelemans, Dirk ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

Author keywords

HIV 1; Intrabody; Rev; Single domain antibody

Indexed keywords

AMINO ACID; EPITOPE; EXPORTIN 1; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HYBRID PROTEIN; KARYOPHERIN; NANOBODY; PLASMID DNA; REV PROTEIN; SINGLE DOMAIN INTRABODY NB 190; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN; VIRUS MESSENGER RNA; RECOMBINANT PROTEIN; REV PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS-1;

AMINO ACID SEQUENCE; ANTIVIRAL ACTIVITY; ARTICLE; BINDING AFFINITY; CELL NUCLEUS; CELL SURVIVAL; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; CYTOPLASM; DIMERIZATION; DNA POLYMORPHISM; EXPRESSION VECTOR; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENETIC VARIABILITY; HEK293 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 (STRAIN IIIB); HUMAN IMMUNODEFICIENCY VIRUS 1 GROUP M; HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 SUBTYPE B; INTRON; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN MULTIMERIZATION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; STABLE EXPRESSION; STOP CODON; VIRUS REPLICATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; DRUG EFFECTS; GENE EXPRESSION; GENETICS; METABOLISM; NEW WORLD CAMELID; PHYSIOLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; LAMA (MAMMAL);

ANIMALS; CAMELIDS, NEW WORLD; CELL LINE; CYTOPATHOGENIC EFFECT, VIRAL; GENE EXPRESSION; GENETIC VARIATION; HIV ANTIBODIES; HIV-1; HUMANS; RECOMBINANT PROTEINS; REV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; SINGLE-DOMAIN ANTIBODIES; VIRUS REPLICATION;

EID: 84910007132     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2014.10.007     Document Type: Article

References (47)

1. A.B. Abecasis, A.M. Wensing, D. Paraskevis, J. Vercauteren, K. Theys, D.A. Van de Vijver, J. Albert, B. Asjo, C. Balotta, D. Beshkov, R.J. Camacho, B. Clotet, C. De Gascun, A. Griskevicius, Z. Grossman, O. Hamouda, A. Horban, T. Kolupajeva, K. Korn, L.G. Kostrikis, C. Kucherer, K. Liitsola, M. Linka, C. Nielsen, D. Otelea, R. Paredes, M. Poljak, E. Puchhammer-Stockl, J.C. Schmit, A. Sonnerborg, D. Stanekova, M. Stanojevic, D. Struck, C.A. Boucher, and A.M. Vandamme HIV-1 subtype distribution and its demographic determinants in newly diagnosed patients in Europe suggest highly compartmentalized epidemics Retrovirology 10 2013 7
2. J. Anderson, and R. Akkina Human immunodeficiency virus type 1 restriction by human-rhesus chimeric tripartite motif 5alpha (TRIM 5alpha) in CD34(+) cell-derived macrophages in vitro and in T cells in vivo in severe combined immunodeficient (SCID-hu) mice transplanted with human fetal tissue Human Gene Ther. 19 2008 217 228
3. Barre-Sinoussi, F., Ross, A.L., Delfraissy, J.F., 2013. Past, present and future: 30 years of HIV research. Nature reviews. Microbiology.
4. M. Bray, S. Prasad, J.W. Dubay, E. Hunter, K.T. Jeang, D. Rekosh, and M.L. Hammarskjold A small element from the Mason-Pfizer monkey virus genome makes human immunodeficiency virus type 1 expression and replication Rev-independent Proc. Natl. Acad. Sci. U.S.A. 91 1994 1256 1260
5. F. Callewaert, J. Roodt, H. Ulrichts, T. Stohr, W.J. van Rensburg, S. Lamprecht, S. Rossenu, S. Priem, W. Willems, and J.B. Holz Evaluation of efficacy and safety of the anti-VWF nanobody ALX-0681 in a preclinical baboon model of acquired thrombotic thrombocytopenic purpura Blood 120 2012 3603 3610
6. D. Daelemans, S.V. Costes, E.H. Cho, R.A. Erwin-Cohen, S. Lockett, and G.N. Pavlakis In vivo HIV-1 Rev multimerization in the nucleolus and cytoplasm identified by fluorescence resonance energy transfer J. Biol. Chem. 279 2004 50167 50175
7. D. Daelemans, S.V. Costes, S. Lockett, and G.N. Pavlakis Kinetic and molecular analysis of nuclear export factor CRM1 association with its cargo in vivo Mol. Cell. Biol. 25 2005 728 739
8. T.J. Daly, K.S. Cook, G.S. Gray, T.E. Maione, and J.R. Rusche Specific binding of HIV-1 recombinant Rev protein to the Rev-responsive element in vitro Nature 342 1989 816 819
9. M.D. Daugherty, I. D'Orso, and A.D. Frankel A solution to limited genomic capacity: using adaptable binding surfaces to assemble the functional HIV Rev oligomer on RNA Mol. Cell 31 2008 824 834
10. M.D. Daugherty, B. Liu, and A.D. Frankel Structural basis for cooperative RNA binding and export complex assembly by HIV Rev Nat. Struct. Mol. Biol. 17 2010 1337 1342
11. M.A. DiMattia, N.R. Watts, S.J. Stahl, C. Rader, P.T. Wingfield, D.I. Stuart, A.C. Steven, and J.M. Grimes Implications of the HIV-1 Rev dimer structure at 3.2 A resolution for multimeric binding to the Rev response element Proc. Natl. Acad. Sci. U.S.A. 107 2010 5810 5814
12. U. Fischer, J. Huber, W.C. Boelens, I.W. Mattaj, and R. Luhrmann The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs Cell 82 1995 475 483
13. U. Fischer, V.W. Pollard, R. Luhrmann, M. Teufel, M.W. Michael, G. Dreyfuss, and M.H. Malim Rev-mediated nuclear export of RNA is dominant over nuclear retention and is coupled to the Ran-GTPase cycle Nucleic Acids Res. 27 1999 4128 4134
14. M. Gouy, S. Guindon, and O. Gascuel SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building Mol. Biol. Evol. 27 2010 221 224
15. S. Heaphy, C. Dingwall, I. Ernberg, M.J. Gait, S.M. Green, J. Karn, A.D. Lowe, M. Singh, and M.A. Skinner HIV-1 regulator of virion expression (Rev) protein binds to an RNA stem-loop structure located within the Rev response element region Cell 60 1990 685 693
16. J. Hemelaar, E. Gouws, P.D. Ghys, S. Osmanov, and W.-U.N.F.H. Isolation Characterisation: global trends in molecular epidemiology of HIV-1 during 2000-2007 Aids 25 2011 679 689
17. J.B. Holz The TITAN trial-assessing the efficacy and safety of an anti-von willebrand factor nanobody in patients with acquired thrombotic thrombocytopenic purpura Transfus Apher. Sci. 46 2012 343 346
18. C. Jain, and J.G. Belasco Structural model for the cooperative assembly of HIV-1 Rev multimers on the RRE as deduced from analysis of assembly-defective mutants Mol. Cell 7 2001 603 614
19. K.H. Kalland, A.M. Szilvay, K.A. Brokstad, W. Saetrevik, and G. Haukenes The human immunodeficiency virus type 1 Rev protein shuttles between the cytoplasm and nuclear compartments Mol. Cell. Biol. 14 1994 7436 7444
20. G. Li, J. Verheyen, S.Y. Rhee, A. Voet, A.M. Vandamme, and K. Theys Functional conservation of HIV-1 Gag: implications for rational drug design Retrovirology 10 2013 126
21. M.H. Malim, and B.R. Cullen HIV-1 structural gene expression requires the binding of multiple Rev monomers to the viral RRE: implications for HIV-1 latency Cell 65 1991 241 248
22. M.H. Malim, J. Hauber, S.Y. Le, J.V. Maizel, and B.R. Cullen The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA Nature 338 1989 254 257
23. J.G. McNally Quantitative FRAP in analysis of molecular binding dynamics in vivo Methods Cell Biol. 85 2008 329 351
24. B.E. Meyer, and M.H. Malim The HIV-1 Rev trans-activator shuttles between the nucleus and the cytoplasm Gene Dev. 8 1994 1538 1547
25. S. Muyldermans, C. Cambillau, and L. Wyns Recognition of antigens by single-domain antibody fragments: the superfluous luxury of paired domains Trends Biochem. Sci. 26 2001 230 235
26. M. Neville, F. Stutz, L. Lee, L.I. Davis, and M. Rosbash The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export Curr. Biol. 7 1997 767 775
27. S. Oliveira, R. Heukers, J. Sornkom, R.J. Kok, and P.M. van Bergen En Henegouwen Targeting tumors with nanobodies for cancer imaging and therapy J. Controlled Release 172 2013 607 617
28. C. Pannecouque, D. Daelemans, and E. De Clercq Tetrazolium-based colorimetric assay for the detection of HIV replication inhibitors: revisited 20 years later Nat. Protoc. 3 2008 427 434
29. E. Pardon, T. Laeremans, S. Triest, S.G. Rasmussen, A. Wohlkonig, A. Ruf, S. Muyldermans, W.G. Hol, B.K. Kobilka, and J. Steyaert A general protocol for the generation of nanobodies for structural biology Nat. Protoc. 9 2014 674 693
30. R. Pauwels, J. Balzarini, M. Baba, R. Snoeck, D. Schols, P. Herdewijn, J. Desmyter, and E. De Clercq Rapid and automated tetrazolium-based colorimetric assay for the detection of anti-HIV compounds J. Virol. Methods 20 1988 309 321
31. A.C. Pineda-Pena, N.R. Faria, S. Imbrechts, P. Libin, A.B. Abecasis, K. Deforche, A. Gomez-Lopez, R.J. Camacho, T. de Oliveira, and A.M. Vandamme Automated subtyping of HIV-1 genetic sequences for clinical and surveillance purposes: performance evaluation of the new REGA version 3 and seven other tools Infect. Genet. Evol.: J. Mol. Epidemiol. Evol. Genet. Infect. Dis. 19 2013 337 348
32. V.W. Pollard, and M.H. Malim The HIV-1 Rev protein Annu. Rev. Microbiol. 52 1998 491 532
33. P.P. Rose, and B.T. Korber Detecting hypermutations in viral sequences with an emphasis on G A hypermutation Bioinformatics 16 2000 400 401
34. C.G. Siontorou Nanobodies as novel agents for disease diagnosis and therapy Int. J. Nanomed. 8 2013 4215 4227
35. J. Sodroski, W.C. Goh, C. Rosen, A. Dayton, E. Terwilliger, and W. Haseltine A second post-transcriptional trans-activator gene required for HTLV-III replication Nature 321 1986 412 417
36. P. Sonigo, C. Barker, E. Hunter, and S. Wain-Hobson Nucleotide sequence of Mason-Pfizer monkey virus: an immunosuppressive D-type retrovirus Cell 45 1986 375 385
37. S.J. Stahl, N.R. Watts, C. Rader, M.A. DiMattia, R.G. Mage, I. Palmer, J.D. Kaufman, J.M. Grimes, D.I. Stuart, A.C. Steven, and P.T. Wingfield Generation and characterization of a chimeric rabbit/human Fab for co-crystallization of HIV-1 Rev J. Mol. Biol. 397 2010 697 708
38. S.L. Thomas, M. Oft, H. Jaksche, G. Casari, P. Heger, M. Dobrovnik, D. Bevec, and J. Hauber Functional analysis of the human immunodeficiency virus type 1 Rev protein oligomerization interface J. Virol. 72 1998 2935 2944
39. J.W. Ulm, M. Perron, J. Sodroski, and C.M. R Complex determinants within the moloney murine leukemia virus capsid modulate susceptibility of the virus to Fv1 and Ref1-mediated restriction Virology 363 2007 245 255
40. T. Venken, D. Daelemans, M. De Maeyer, and A. Voet Computational investigation of the HIV-1 Rev multimerization using molecular dynamics simulations and binding free energy calculations Proteins 80 2012 1633 1646
41. Vercruysse, T., Daelemans, D., 2014. HIV-1 Rev Multimerization: Mechanism and Insights. Curr. HIV Res.
42. T. Vercruysse, E. Pardon, E. Vanstreels, J. Steyaert, and D. Daelemans An intrabody based on a llama single-domain antibody targeting the N-terminal alpha-helical multimerization domain of HIV-1 rev prevents viral production J. Biol. Chem. 285 2010 21768 21780
43. T. Vercruysse, S. Pawar, W. De Borggraeve, E. Pardon, G.N. Pavlakis, C. Pannecouque, J. Steyaert, J. Balzarini, and D. Daelemans Measuring cooperative Rev protein-protein interactions on Rev responsive RNA by fluorescence resonance energy transfer RNA Biol. 8 2011 316 324
44. T. Vercruysse, E. Boons, T. Venken, E. Vanstreels, A. Voet, J. Steyaert, M. De Maeyer, and D. Daelemans Mapping the binding interface between an HIV-1 inhibiting intrabody and the viral protein Rev PLoS One 8 2013 e60259
45. M.L. Zapp, T.J. Hope, T.G. Parslow, and M.R. Green Oligomerization and RNA binding domains of the type 1 human immunodeficiency virus Rev protein: a dual function for an arginine-rich binding motif Proc. Nat. Acad. Sci. U.S.A. 88 1991 7734 7738
46. A. Zhen, and S. Kitchen Stem-cell-based gene therapy for HIV infection Viruses 6 2014 1 12
47. A.S. Zolotukhin, A. Valentin, G.N. Pavlakis, and B.K. Felber Continuous propagation of RRE(-) and Rev(-)RRE(-) human immunodeficiency virus type 1 molecular clones containing a cis-acting element of simian retrovirus type 1 in human peripheral blood lymphocytes J. Virol. 68 1994 7944 7952