Development of RNA aptamers targeting Ebola virus VP35

Biochemistry

Volumn 52, Issue 47, 2013, Pages 8406-8419

  Binning, Jennifer M ^a,b   Wang, Tianjiao ^b,f   Luthra, Priya ^c   Shabman, Reed S ^c   Borek, Dominika M ^d,e   Liu, Gai ^a   Xu, Wei ^a   Leung, Daisy W ^a   Basler, Christopher F ^c   Amarasinghe, Gaya K ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b IOWA STATE UNIVERSITY   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^f UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEINS; FUNCTIONAL VALIDATION; INHIBITORY DOMAINS; INTERACTION PROPERTIES; MULTIFUNCTIONAL PROTEIN; POLYMERASE COMPLEX; PROTEIN INHIBITORS; VIRAL REPLICATION;

DISEASES; NUCLEIC ACIDS; VIRUSES;

PROTEINS;

ANTIVIRUS AGENT; APTAMER; DOUBLE STRANDED RNA; INTERFERON; NUCLEOPROTEIN; PROTEIN INHIBITOR; PROTEIN VP35; RNA APTAMER; RNA POLYMERASE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING COMPETITION; CARBOXY TERMINAL DOUBLE STRANDED RNA BINDING INTERFERON INHIBITORY DOMAIN; CONTROLLED STUDY; DRUG IDENTIFICATION; DRUG MECHANISM; DRUG PROTEIN BINDING; DRUG SPECIFICITY; DRUG TARGETING; EBOLA VIRUS; ENZYME INHIBITION; IMMUNE EVASION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANTIVIRAL AGENTS; APTAMERS, NUCLEOTIDE; BINDING, COMPETITIVE; CONSERVED SEQUENCE; EBOLAVIRUS; HEMORRHAGIC FEVER, EBOLA; KINETICS; MOLECULAR TARGETED THERAPY; MUTANT PROTEINS; NUCLEIC ACID CONFORMATION; NUCLEOPROTEINS; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS; RNA; RNA, DOUBLE-STRANDED; SELEX APTAMER TECHNIQUE; SPECIES SPECIFICITY; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84888632822     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400704d     Document Type: Article

References (67)

1. Bray, M. and Murphy, F. A. (2007) Filovirus research: knowledge expands to meet a growing threat J. Infect. Dis. 196 (Suppl 2) S438-S443
2. Negredo, A., Palacios, G., Vazquez-Moron, S., Gonzalez, F., Dopazo, H., Molero, F., Juste, J., Quetglas, J., Savji, N., de la Cruz Martinez, M., Herrera, J. E., Pizarro, M., Hutchison, S. K., Echevarria, J. E., Lipkin, W. I., and Tenorio, A. (2011) Discovery of an ebolavirus-like filovirus in europe PLoS Pathog. 7, e1002304
3. Kuhn, J. H., Becker, S., Ebihara, H., Geisbert, T. W., Johnson, K. M., Kawaoka, Y., Lipkin, W. I., Negredo, A. I., Netesov, S. V., Nichol, S. T., Palacios, G., Peters, C. J., Tenorio, A., Volchkov, V. E., and Jahrling, P. B. (2010) Proposal for a revised taxonomy of the family Filoviridae: classification, names of taxa and viruses, and virus abbreviations Arch. Virol. 155, 2083-2103
4. Groseth, A., Stroher, U., Theriault, S., and Feldmann, H. (2002) Molecular characterization of an isolate from the 1989/90 epizootic of Ebola virus Reston among macaques imported into the United States Virus Res. 87, 155-163
5. Jahrling, P. B., Geisbert, T. W., Dalgard, D. W., Johnson, E. D., Ksiazek, T. G., Hall, W. C., and Peters, C. J. (1990) Preliminary report: isolation of Ebola virus from monkeys imported to USA Lancet 335, 502-505
6. Barrette, R. W., Metwally, S. A., Rowland, J. M., Xu, L., Zaki, S. R., Nichol, S. T., Rollin, P. E., Towner, J. S., Shieh, W. J., Batten, B., Sealy, T. K., Carrillo, C., Moran, K. E., Bracht, A. J., Mayr, G. A., Sirios-Cruz, M., Catbagan, D. P., Lautner, E. A., Ksiazek, T. G., White, W. R., and McIntosh, M. T. (2009) Discovery of swine as a host for the Reston ebolavirus Science 325, 204-206
7. Leung, D. W., Prins, K. C., Basler, C. F., and Amarasinghe, G. K. (2010) Ebolavirus VP35 is a multifunctional virulence factor Virulence 1, 526-531
8. Basler, C. F., Mikulasova, A., Martinez-Sobrido, L., Paragas, J., Muhlberger, E., Bray, M., Klenk, H. D., Palese, P., and Garcia-Sastre, A. (2003) The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3 J. Virol. 77, 7945-7956
9. Basler, C. F., Wang, X., Muhlberger, E., Volchkov, V., Paragas, J., Klenk, H. D., Garcia-Sastre, A., and Palese, P. (2000) The Ebola virus VP35 protein functions as a type I IFN antagonist Proc. Natl. Acad. Sci. U.S.A. 97, 12289-12294
10. Hartman, A. L., Dover, J. E., Towner, J. S., and Nichol, S. T. (2006) Reverse genetic generation of recombinant Zaire Ebola viruses containing disrupted IRF-3 inhibitory domains results in attenuated virus growth in vitro and higher levels of IRF-3 activation without inhibiting viral transcription or replication J. Virol. 80, 6430-6440
11. Cardenas, W. B., Loo, Y. M., Gale, M., Jr., Hartman, A. L., Kimberlin, C. R., Martinez-Sobrido, L., Saphire, E. O., and Basler, C. F. (2006) Ebola virus VP35 protein binds double-stranded RNA and inhibits alpha/beta interferon production induced by RIG-I signaling J. Virol. 80, 5168-5178
12. Enterlein, S., Warfield, K. L., Swenson, D. L., Stein, D. A., Smith, J. L., Gamble, C. S., Kroeker, A. D., Iversen, P. L., Bavari, S., and Muhlberger, E. (2006) VP35 knockdown inhibits Ebola virus amplification and protects against lethal infection in mice Antimicrob. Agents Chemother. 50, 984-993
13. Feng, Z., Cerveny, M., Yan, Z., and He, B. (2007) The VP35 protein of Ebola virus inhibits the antiviral effect mediated by double-stranded RNA-dependent protein kinase PKR J. Virol. 81, 182-192
14. Haasnoot, J., de Vries, W., Geutjes, E. J., Prins, M., de Haan, P., and Berkhout, B. (2007) The Ebola virus VP35 protein is a suppressor of RNA silencing PLoS Pathog. 3, e86
15. Hartman, A. L., Bird, B. H., Towner, J. S., Antoniadou, Z. A., Zaki, S. R., and Nichol, S. T. (2008) Inhibition of IRF-3 activation by VP35 is critical for the high level of virulence of ebola virus J. Virol. 82, 2699-2704
16. Hartman, A. L., Towner, J. S., and Nichol, S. T. (2004) A C-terminal basic amino acid motif of Zaire ebolavirus VP35 is essential for type I interferon antagonism and displays high identity with the RNA-binding domain of another interferon antagonist, the NS1 protein of influenza A virus Virology 328, 177-184
17. Leung, D. W., Shabman, R. S., Farahbakhsh, M., Prins, K. C., Borek, D. M., Wang, T., Muhlberger, E., Basler, C. F., and Amarasinghe, G. K. (2010) Structural and functional characterization of Reston Ebola virus VP35 interferon inhibitory domain J. Mol. Biol. 399, 347-357
18. Leung, D. W., Prins, K. C., Borek, D. M., Farahbakhsh, M., Tufariello, J. M., Ramanan, P., Nix, J. C., Helgeson, L. A., Otwinowski, Z., Honzatko, R. B., Basler, C. F., and Amarasinghe, G. K. (2010) Structural basis for dsRNA recognition and interferon antagonism by Ebola VP35 Nat. Struct. Mol. Biol. 17, 165-172
19. Luthra, P., Ramanan, P., Mire, C. E., Weisend, C., Tsuda, Y., Yen, B., Liu, G., Leung, D. W., Geisbert, T. W., Ebihara, H., Amarasinghe, G. K., and Basler, C. F. (2013) Mutual antagonism between the Ebola virus VP35 protein and the RIG-I activator PACT determines infection outcome Cell Host Microbe 14, 74-84
20. Prins, K. C., Cardenas, W. B., and Basler, C. F. (2009) Ebola virus protein VP35 impairs the function of interferon regulatory factor-activating kinases IKKepsilon and TBK-1 J. Virol. 83, 3069-3077
21. Schumann, M., Gantke, T., and Muhlberger, E. (2009) Ebola virus VP35 antagonizes PKR activity through its C-terminal interferon inhibitory domain J. Virol. 83, 8993-8997
22. Fabozzi, G., Nabel, C. S., Dolan, M. A., and Sullivan, N. J. (2011) Ebolavirus proteins suppress the effects of small interfering RNA by direct interaction with the mammalian RNA interference pathway J. Virol. 85, 2512-2523
23. Prins, K. C., Binning, J. M., Shabman, R. S., Leung, D. W., Amarasinghe, G. K., and Basler, C. F. (2010) Basic residues within the ebolavirus VP35 protein are required for its viral polymerase cofactor function J. Virol. 84, 10581-10591
24. Huang, Y., Xu, L., Sun, Y., and Nabel, G. J. (2002) The assembly of Ebola virus nucleocapsid requires virion-associated proteins 35 and 24 and posttranslational modification of nucleoprotein Mol. Cell 10, 307-316
25. Johnson, R. F., McCarthy, S. E., Godlewski, P. J., and Harty, R. N. (2006) Ebola virus VP35-VP40 interaction is sufficient for packaging 3E-5E minigenome RNA into virus-like particles J. Virol. 80, 5135-5144
26. Noda, T., Sagara, H., Suzuki, E., Takada, A., Kida, H., and Kawaoka, Y. (2002) Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP J. Virol. 76, 4855-4865
27. Shi, W., Huang, Y., Sutton-Smith, M., Tissot, B., Panico, M., Morris, H. R., Dell, A., Haslam, S. M., Boyington, J., Graham, B. S., Yang, Z. Y., and Nabel, G. J. (2008) A filovirus-unique region of Ebola virus nucleoprotein confers aberrant migration and mediates its incorporation into virions J. Virol. 82, 6190-6199
28. Prins, K. C., Delpeut, S., Leung, D. W., Reynard, O., Volchkova, V. A., Reid, S. P., Ramanan, P., Cardenas, W. B., Amarasinghe, G. K., Volchkov, V. E., and Basler, C. F. (2010) Mutations abrogating VP35 interaction with double-stranded RNA render Ebola virus avirulent in guinea pigs J. Virol. 84, 3004-3015
29. Kimberlin, C. R., Bornholdt, Z. A., Li, S., Woods, V. L., Jr., MacRae, I. J., and Saphire, E. O. (2010) Ebolavirus VP35 uses a bimodal strategy to bind dsRNA for innate immune suppression Proc. Natl. Acad. Sci. U.S.A. 107, 314-319
30. Leung, D. W., Ginder, N. D., Fulton, D. B., Nix, J., Basler, C. F., Honzatko, R. B., and Amarasinghe, G. K. (2009) Structure of the Ebola VP35 interferon inhibitory domain Proc. Natl. Acad. Sci. U.S.A. 106, 411-416
31. Muhlberger, E., Weik, M., Volchkov, V. E., Klenk, H. D., and Becker, S. (1999) Comparison of the transcription and replication strategies of marburg virus and Ebola virus by using artificial replication systems J. Virol. 73, 2333-2342
32. Feldmann, H. and Geisbert, T. W. (2011) Ebola haemorrhagic fever Lancet 377, 849-862
33. Wilson, J. A., Bray, M., Bakken, R., and Hart, M. K. (2001) Vaccine potential of Ebola virus VP24, VP30, VP35, and VP40 proteins Virology 286, 384-390
34. Geisbert, T. W. and Jahrling, P. B. (2003) Towards a vaccine against Ebola virus Expert Rev. Vaccines 2, 777-789
35. Geisbert, T. W., Lee, A. C., Robbins, M., Geisbert, J. B., Honko, A. N., Sood, V., Johnson, J. C., de Jong, S., Tavakoli, I., Judge, A., Hensley, L. E., and Maclachlan, I. (2010) Postexposure protection of non-human primates against a lethal Ebola virus challenge with RNA interference: a proof-of-concept study Lancet 375, 1896-1905
36. Hensley, L. E., Jones, S. M., Feldmann, H., Jahrling, P. B., and Geisbert, T. W. (2005) Ebola and Marburg viruses: pathogenesis and development of countermeasures Curr. Mol. Med. 5, 761-772
37. Hartman, A. L., Towner, J. S., and Nichol, S. T. (2010) Ebola and marburg hemorrhagic fever Clin. Lab. Med. 30, 161-177
38. Fausther-Bovendo, H., Mulangu, S., and Sullivan, N. J. (2012) Ebolavirus vaccines for humans and apes Curr. Opin. Virol. 2, 324-329
39. Warfield, K. L. and Aman, M. J. (2011) Advances in virus-like particle vaccines for filoviruses J. Infect. Dis. 204 (Suppl 3) S1053-S1059
40. Geisbert, T. W., Hensley, L. E., Kagan, E., Yu, E. Z., Geisbert, J. B., Daddario-DiCaprio, K., Fritz, E. A., Jahrling, P. B., McClintock, K., Phelps, J. R., Lee, A. C., Judge, A., Jeffs, L. B., and MacLachlan, I. (2006) Postexposure protection of guinea pigs against a lethal ebola virus challenge is conferred by RNA interference J. Infect. Dis. 193, 1650-1657
41. Groseth, A., Hoenen, T., Alimonti, J. B., Zielecki, F., Ebihara, H., Theriault, S., Stroher, U., Becker, S., and Feldmann, H. (2007) In vitro evaluation of antisense RNA efficacy against filovirus infection, by use of reverse genetics J. Infect. Dis. 196 (Suppl 2) S382-389
42. Warfield, K. L., Swenson, D. L., Olinger, G. G., Nichols, D. K., Pratt, W. D., Blouch, R., Stein, D. A., Aman, M. J., Iversen, P. L., and Bavari, S. (2006) Gene-specific countermeasures against Ebola virus based on antisense phosphorodiamidate morpholino oligomers PLoS Pathog. 2, e1
43. Kang, K. N. and Lee, Y. S. (2012) RNA aptamers: a review of recent trends and applications Adv. Biochem. Eng. Biotechnol. 131, 153-169
44. Lee, J. F., Stovall, G. M., and Ellington, A. D. (2006) Aptamer therapeutics advance Curr. Opin. Chem. Biol. 10, 282-289
45. Bunka, D. H., Platonova, O., and Stockley, P. G. (2010) Development of aptamer therapeutics Curr. Opin. Pharmacol. 10, 557-562
46. Soontornworajit, B. and Wang, Y. (2011) Nucleic acid aptamers for clinical diagnosis: cell detection and molecular imaging Anal. Bioanal. Chem. 399, 1591-1599
47. Wang, T. (2009) Function and Dynamics of Aptamers: A Case Study on the Malachite Green Aptamer, p 156, Iowa State University, Ames, IA.
48. Binning, J. M., Leung, D. W., and Amarasinghe, G. K. (2012) Aptamers in virology: recent advances and challenges Front. Microbiol. 3, 29
49. Ellington, A. D. and Szostak, J. W. (1990) In vitro selection of RNA molecules that bind specific ligands Nature 346, 818-822
50. Tuerk, C. and Gold, L. (1990) Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase Science 249, 505-510
51. Ramanan, P., Edwards, M. R., Shabman, R. S., Leung, D. W., Endlich-Frazier, A. C., Borek, D. M., Otwinowski, Z., Liu, G., Huh, J., Basler, C. F., and Amarasinghe, G. K. (2012) Structural basis for Marburg virus VP35-mediated immune evasion mechanisms Proc.Natl. Acad. Sci. U.S.A. 109, 20661-20666
52. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscilation mode Methods Enzymol. 276, 307-326
53. Collaborative Computational Project, N. (1994) The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D 50, 760-763
54. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D 53, 240-255
55. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D 66, 213-221
56. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D 60, 2126-2132
57. Painter, J. and Merritt, E. A. (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion Acta Crystallogr., Sect. D 62, 439-450
58. Chen, V. B., Arendall, W. B., III, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D 66, 12-21
59. Jhaveri, S. D. and Ellington, A. D. (2001) In vitro selection of RNA aptamers to a protein target by filter immobilization, Curr. Protoc. Mol. Biol. Chapter 24, Unit 24 23.
60. Fitzwater, T. and Polisky, B. (1996) A SELEX primer Methods Enzymol. 267, 275-301
61. Peters, G. A., Li, S., and Sen, G. C. (2006) Phosphorylation of specific serine residues in the PKR activation domain of PACT is essential for its ability to mediate apoptosis J. Biol. Chem. 281, 35129-35136
62. Ramalingam, D., Duclair, S., Datta, S. A., Ellington, A., Rein, A., and Prasad, V. R. (2011) RNA aptamers directed to human immunodeficiency virus type 1 Gag polyprotein bind to the matrix and nucleocapsid domains and inhibit virus production J. Virol. 85, 305-314
63. Gruber, A. R., Lorenz, R., Bernhart, S. H., Neubock, R., and Hofacker, I. L. (2008) The Vienna RNA websuite Nucleic Acids Res. 36, W70-74
64. Mathews, D. H., Sabina, J., Zuker, M., and Turner, D. H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure J. Mol. Biol. 288, 911-940
65. Ding, Y., Chan, C. Y., and Lawrence, C. E. (2005) RNA secondary structure prediction by centroids in a Boltzmann weighted ensemble RNA 11, 1157-1166
66. McCaskill, J. S. (1990) The equilibrium partition function and base pair binding probabilities for RNA secondary structure Biopolymers 29, 1105-1119
67. Darty, K., Denise, A., and Ponty, Y. (2009) VARNA: Interactive drawing and editing of the RNA secondary structure Bioinformatics 25, 1974-1975