The silencing suppressor (NSs) protein of the plant virus Tomato spotted wilt virus enhances heterologous protein expression and baculovirus pathogenicity in cells and lepidopteran insects

Archives of Virology

Volumn 160, Issue 11, 2015, Pages 2873-2879

  de Oliveira, Virgínia Carla ^a   da Silva Morgado, Fabricio ^a   Ardisson Araújo, Daniel Mendes Pereira ^a   Resende, Renato Oliveira ^a   Ribeiro, Bergmann Morais ^a  

^a UNIVERSITY OF BRASILIA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS PROTEIN;

ANIMAL; BACULOVIRIDAE; CELL LINE; GENE EXPRESSION; GENE SILENCING; GENETICS; METABOLISM; MOTH; PATHOGENICITY; SPODOPTERA; TOSPOVIRUS; VIROLOGY; VIRULENCE;

ANIMALS; CELL LINE; GENE EXPRESSION; GENE SILENCING; MOTHS; NUCLEOPOLYHEDROVIRUS; SPODOPTERA; TOSPOVIRUS; VIRAL PROTEINS; VIRULENCE;

EID: 84946491690     PISSN: 03048608     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00705-015-2580-2     Document Type: Article

References (47)

1. Anandalakshmi R, Pruss GJ, Ge X, Marathe R, Mallory AC, Smith TH, Vance VB (1998) A viral suppressor of gene silencing in plants. P Natl Acad Sci USA 95:13079–13084
2. Ardisson-Araujo DMP, Morgado FS, Schwarts EF, Corzo G, Ribeiro BM (2013) A new theraphosid spider toxin causes early insect cell death by necrosis when expressed in vitro during recombinant baculovirus infection. Plos One 8:e84404
3. Bucher E, Hemmes H, de Haan P, Goldbach R, Prins M (2004) The influenza A virus NS1 protein binds small interfering RNAs and suppresses RNA silencing in plants. J Gen Virol 85:983–991
4. Burden JP, Hails RS, Windass JD, Suner MM, Cory JS (2000) Infectivity, speed of kill, and productivity of a baculovirus expressing the itch mite toxin txp-1 in second and fourth instar larvae of Trichoplusia ni. J Invertebr Pathol 75:226–236
5. Blakqori G, Delhaye S, Habjan M, Blair CD, Sanchez-VargasI Olson KE, Attarzadeh-Yazdi G, Fragkoudis R, Kohl A, Kalinke U, Weiss S, Michiels T, Staeheli P, Weber F (2007) La Crosse bunyavirus nonstructural protein NSs serves to suppress the type interferon system of mammalian hosts. J Virol 81:4991–4999
6. Chen Y, Zhong S, Fei Z, Hashimoto Y, Xiang JZ, Zhang S, Blissard GW (2013) The transcriptome of the baculovirus Autographa californica multiple nucleopolyhedrovirus in Trichoplusiani cells. J Virol 87:6391–6405
7. Chikhalya A, Luu DD, Carrera M, De La Cruz A, Torres M, Martinez EN, Chen T, Stephens KD, Haas-Stapleton EJ (2009) Pathogenesis of Autographa californica multiple nucleopolyhedrovirus in fifth-instar Anticarsia gemmatalis larvae. J Gen Virol 90:2023–2032
8. Clarke TE, Clem RJ (2002) Lack of involvement of haemocytes in the establishment and spread of infection in Spodoptera frugiperda larvae infected with the baculovirus Autographa californica M nucleopolyhedrovirus by intrahaemocoelic injection. J Gen Virol 83:1565–1572
9. Cordeiro BA, Tibúrcio VH, Hallwass M, Paes HC, Ribeiro BM, Báo SN (2008) Structural and ultrastructural alterations of Malpighian tubules of Anticarsia gemmatalis (Hübner) (Lepidoptera: Noctuidae) larvae infected with different Anticarsia gemmatalis multiple nucleopolyhedrovirus (AgMNPV) recombinant viruses. J Invertebr Pathol 98:7–19
10. Fath-Goodin A, Kroemer J, Martin S, Reeves K, Webb BA (2006) Polydnavirus genes that enhance the baculovirus expression vector system. Adv Virus Res 68:75–90
11. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811
12. Finney DJ (1971) Probit analysis. Cambridge University Press, New York, p 333
13. Flores-Jasso CF, Valdes VJ, Sampieri A, Valadez-Graham V, Recillas-Targa F, Vaca L (2004) Silencing structural and nonstructural genes in baculovirus by RNA interference. Virus Res 102:75–84
14. Friesen PD, Miller LK (1985) Temporal regulation of baculovirus RNA: overlapping early and late transcripts. J Virol 54:392–400
15. Garcia S, Billecocq A, Crance JM, Prins M, Garin D (2006) Viral suppressors of RNA interference impair RNA silencing induced by a Semliki Forest virus replicon in tick cells. J Gen Virol 87:1985–1989
16. Gershburg E, Stockholm D, Froy O, Rashi S, Gurevitz M, Chejanovsky N (1998) Baculovirus-mediated expression of a scorpion depressant toxin improves the insecticidal efficacy achieved with excitatory toxins. FEBS Lett 422:132–136
17. Granados RR, Li GX, Derksen ACG, McKenna KA (1994) A new insect-cell line from Trichoplusia ni (BTI-Tn-5B1-4) susceptible to Trichoplusia ni single enveloped nuclear polyhedrosis virus. J Invertebr Pathol 64:260–266
18. Gramkow AW, Perecmanis S, Sousa RL, Noronha EF, Felix R, Nagata T, Ribeiro BM (2010) Insecticidal activity of two proteases against Spodoptera frugiperda larvae infected with recombinant baculoviruses. Virol J 7:143
19. Greene GL, Leppla NC, Dickerson WA (1976) Velvetbean caterpillar: a rearing procedure and artificial medium. J Econ Entomol 69:487–548
20. Jayachandran B, Hussain M, Asgari S (2012) RNA interference as a cellular defense mechanism against the DNA virus, baculovirus. J Virol 24:13729–13734
21. Jinn T, Tu W, Lu C, Tzen J (2006) Enhancing insecticidal efficacy of baculovirus by early expressing an insect neurotoxin, LqhIT2, in infected Trichoplusia ni larvae. Appl Micro Biochem 72:1247–1253
22. Leora Software (1980) Polo PC: a user guide to probit or logit analysis. LeOra Software, Berkeley
23. Lee HH, Miller LK (1978) Isolation of genotypic variants of Autographa californica nuclear polyhedrosis virus. J Virol 27:754–767
24. Lubbert H, Doerfler W (1984) Transcription of overlapping sets of RNAs from the genome of Autographa californica nuclear polyhedrosis virus: a novel method for mapping RNAs. JVirol 52:255–265
25. Kainulainen M, Habjan M, Hubel P, Busch L, Lau S, Colinge J, Superti-Furga G, Pichlmair A, Weber F (2014) Virulence factor NSs of Rift valley fever firus recruits the F-Box protein FBXO3 to degrade subunit p62 of general transcription factor TFIIH. J Virol 88:3464–3473
26. Margaria P, Bosco L, Vallino M, Ciuffo M, Mautino GC, Tavella L, Turina M (2014) The NSs protein of Tomato spotted wilt virus is required for persistent infection and transmission by Frankliniella occidentalis. J. Virol 88:5788–5802
27. Medeiros RB, de Resende OR, de Avila AC (2004) The plant virus Tomato spotted wilt tospovirus activates the immune system of its main insect vector, Frankliniella occidentalis. J Virol 78:4976–4982
28. Michael RG, Sambrook J (2001) Molecular cloning A laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York
29. Miller LK, Lu A (1997) The molecular basis of baculovirus host range. In: Miller LK (ed) The baculoviruses. Plenum Press, New York, pp 217–235
30. Molnár A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC (2007) MiRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447:1126–1129
31. Morales L, Moscardi F, Sosa-Gómez DR, Paro FE, Soldorio IL (2001) Fluorescent brighteners improve Anticarsia gemmatalis (Lepidoptera: Noctuidae) nucleopolyhedrovirus (AgMNPV) activity on AgMNPV susceptible and resistant strains of the insect. Biol Control 20:247–253
32. Oliveira VC, Bartasson L, de Castro ME, Corrêa JR, Ribeiro BM, Resende RO (2011) A silencing suppressor protein (NSs) of a tospovirus enhances baculovirus replication in permissive and semipermissive insect cell lines. Virus Res 155:259–267
33. O’Reilly DR, Miller LK (1991) Improvement of a baculovirus pesticide by deletion of the egt gene. Biotechnology 9:1086–1089
34. O’Reilly DR (1992) Baculovirus expression vectors. A laboratory manual. Oxford University Press, New York
35. Pinedo FJR, Moscardi F, Luque T, Olszewski JA, Ribeiro BM (2003) Inactivation of the ecdysteroid UDP-glucosyltransferase (egt) gene of Anticarsia gemmatalis nucleopolyhedrovirus (AgMNPV) improves its virulence towards its insect host. Biol Control 27:336–344
36. Ribeiro BM, Gatti CD, Costa MH, Moscardi F, Maruniak JE, Possee RD, Zanotto PM (2001) Construction of a recombinant Anticarsia gemmatalis nucleopolyhedrovirus (AgMNPV-2D) harbouring the β-galactosidase gene. Arch Virol 146:1355–1367
37. Sieburth PJ, Maruniak JE (1988) Susceptibility of an established cell line of Anticarsia gemmatalis (Lepidoptera, Noctuidae) to three nuclear polyhedrosis viruses. J Invertebr Pathol 52:453–458
38. Schmidt O, Theopold U, Beckage NE (2008) Insect and vertebrate immunity: key similarities versus differences. In: Beckage Nancy E (ed) Insect immunology. Academic Press/Elsevier, San Diego
39. Sun XL, Wu D, Sun XC, Jin L, Ma Y, Bonning BC, Peng HY, Hu ZH (2009) Impact of Helicoverpa armigera nucleopolyhedroviruses expressing a cathepsin L-like protease on target and non target insect species on cotton. Biol Control 49:77–83
40. Szemiel AM, Failloux A-B, Elliott RM (2012) Role of Bunyamwera Orthobunyavirus NSs protein in infection of mosquito cells. Plos Negl Trop Dis 6:e1823
41. KnippenbergI Van, Carlton-Smith C, Elliott RM (2002) The N-terminus of Bunyamwera Orthobunyavirus NSs protein is essential for interferon antagonism. J Gen Virol 91:2002–2006
42. Van Mierlo JT, van Cleef KW, van RijR RP (2011) Defense and counter defense in the RNAi-based antiviral immune system in insects. In: Ronald P, van Rij RP (eds) Antiviral RNAi: concepts, methods, and applications, methods in molecular biology. Springer Science Business Media, New Yrok, pp 220–247
43. Venter PA, Schneemann A (2008) Recent insights into the biology and biomedical applications of Flock House virus. Cell Mol Life Sci 17:2675–2687
44. Tang XX, Sun XL, Pu GQ, Wang WB, Zhang CX, Zhu J (2011) Expression of a neurotoxin gene improves the insecticidal activity of Spodoptera litura nucleopolyhedrovirus (SpltNPV). Virus Res 159:51–56
45. Yokoyama N, Hirata M, Ohtsuka K, Nishiyama Y, Fujii K, Fujita M, Kuzushima K, Kiyono T, Tsurumi T (2000) Co-expression of human chaperones Hsp70 and Hsdj or Hsp40 cofactor increases solubility of overexpressed target proteins in insect cells. Biochim Biophys Acta 1493:119–124
46. Wang XH, Aliyari R, Li WX, Li HW, Kim K, Carthew R, Atkinson P, Ding W (2006) RNA interference directs innate immunity against viruses in adult Drosophila. Science 312:452–454
47. Wijkamp I, van Lent J, Kormelink R, Goldbach R, Peters D (1993) Multiplication of Tomato spotted wilt virus in its insect vector, Frankliniella occidentalis. J Gen Virol 74:341–349