1887

Abstract

Many species of tsetse flies (Diptera: Glossinidae) can be infected by a virus that causes salivary gland hypertrophy (SGH). The genomes of viruses isolated from (GpSGHV) and (MdSGHV) have recently been sequenced. Tsetse flies with SGH have reduced fecundity and fertility which cause a serious problem for mass rearing in the frame of sterile insect technique (SIT) programmes to control and eradicate tsetse populations in the wild. A potential intervention strategy to mitigate viral infections in fly colonies is neutralizing of the GpSGHV infection with specific antibodies against virion proteins. Two major GpSGHV virion proteins of about 130 and 50 kDa, respectively, were identified by Western analysis using a polyclonal rabbit antibody raised against whole GpSHGV virions. The proteome of GpSGHV, containing the antigens responsible for the immune-response, was investigated by liquid chromatography tandem mass spectrometry and 61 virion proteins were identified by comparison with the genome sequence. Specific antibodies were produced in rabbits against seven candidate proteins, including the ORF10/C-terminal fragment, ORF47 and ORF96 as well as proteins involved in peroral infectivity PIF-1 (ORF102), PIF-2 (ORF53), PIF-3 (ORF76) and P74 (ORF1). Antiserum against ORF10 specifically reacted to the 130 kDa protein in a Western blot analysis and to the envelope protein of GpSGHV, detected by using immunogold-electron microscopy. This result suggests that immune intervention of viral infections in colonies of is a realistic option.

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2010-12-01
2019-11-14
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References

  1. Abd-Alla, A., Bossin, H., Cousserans, F., Parker, A., Bergoin, M. & Robinson, A. ( 2007; ). Development of a non-destructive PCR method for detection of the salivary gland hypertrophy virus (SGHV) in tsetse flies. J Virol Methods 139, 143–149.[CrossRef]
    [Google Scholar]
  2. Abd-Alla, A. M. M., Cousserans, F., Parker, A. G., Jehle, J. A., Parker, N. J., Vlak, J. M., Robinson, A. S. & Bergoin, M. ( 2008; ). Genome analysis of a Glossina pallidipes salivary gland hypertrophy virus (GpSGHV) reveals a novel large double-stranded circular DNA virus. J Virol 82, 4595–4611.[CrossRef]
    [Google Scholar]
  3. Abd-Alla, A. M. M., Vlak, J. M., Bergoin, M., Maruniak, J. E., Parker, A. G., Burand, J. P., Jehle, J. A. & Boucias, D. G. ( 2009; ). Hytrosaviridae: a proposal for classification and nomenclature of a new insect virus family. Arch Virol 154, 909–918.[CrossRef]
    [Google Scholar]
  4. Abd-Alla, A. M. M., Kariithi, H., Parker, A. G., Robinson, A. S., Kiflom, M., Bergoin, M. & Vreysen, M. J. B. ( 2010; ). Dynamics of the salivary gland hypertrophy virus in laboratory colonies of Glossina pallidipes (Diptera: Glossinidae). Virus Res 150, 103–110.[CrossRef]
    [Google Scholar]
  5. Aksoy, S. & Rio, R. V. M. ( 2005; ). Interactions among multiple genomes: tsetse, its symbionts and trypanosomes. Insect Biochem Mol Biol 35, 691–698.[CrossRef]
    [Google Scholar]
  6. Amargier, A., Lyon, J. P., Vago, C., Meynadier, G. & Veyrunes, J. C. ( 1979; ). Discovery and purification of a virus in gland hyperplasia of insects. Study of Merodon equestris F. (Diptera, Syrphidae). C R Seances Acad Sci D 289, 481–484 (in French ).
    [Google Scholar]
  7. Borodina, T. A., Lehrach, H. & Soldatov, A. V. ( 2003; ). DNA purification on homemade silica spin-columns. Anal Biochem 321, 135–137.[CrossRef]
    [Google Scholar]
  8. Coler, R. R., Boucias, D. G., Frank, J. H., Maruniak, J. E., Garcia-Canedo, A. & Pendland, J. C. ( 1993; ). Characterization and description of a virus causing salivary gland hyperplasia in the housefly, Musca domestica. Med Vet Entomol 7, 275–282.[CrossRef]
    [Google Scholar]
  9. Cox, J. & Mann, M. ( 2008; ). MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26, 1367–1372.[CrossRef]
    [Google Scholar]
  10. Elias, J. E. & Gygi, S. P. ( 2007; ). Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4, 207–214.[CrossRef]
    [Google Scholar]
  11. Ellis, D. S. & Maudlin, I. ( 1987; ). Salivary gland hyperplasia in wild caught tsetse from Zimbabwe. Entomol Exp Appl 45, 167–173.[CrossRef]
    [Google Scholar]
  12. Feldmann, U. ( 2005; ). The sterile insect technique as a component of area-wide integrated pest management of tsetse. In The Trypanosomiases, pp. 565–582. Edited by Maudlin, I., Holmes, P. H. & Wallingford, M. A.. UK. : CABI Publishing.
    [Google Scholar]
  13. Garcia-Maruniak, A., Maruniak, J. E., Farmerie, W. & Boucias, D. G. ( 2008; ). Sequence analysis of a non-classified, non-occluded DNA virus that causes salivary gland hypertrophy of Musca domestica, MdSGHV. Virology 377, 184–196.[CrossRef]
    [Google Scholar]
  14. Garcia-Maruniak, A., Abd-Alla, A. M. M., Salem, T. Z., Parker, A. G., van Oers, M. M., Maruniak, J. E., Kim, W., Burand, J. P., Cousserans, F. & other authors ( 2009; ). Two viruses that cause salivary gland hypertrophy in Glossina pallidipes and Musca domestica are related and form a distinct phylogenetic clade. J Gen Virol 90, 334–346.[CrossRef]
    [Google Scholar]
  15. Hendrichs, J. P., Kenmore, P., Robinson, A. S. & Vreysen, M. J. B. ( 2007; ). Area-wide integrated pest management (AW-IPM): Principles, practice and prospects. In Area-Wide Control of Insect Pests: From Research to Field Implementation, pp. 3–33. Edited by Vreysen, M. J. B., Robinson, A. S. & Hendrichs, J.. Dordrecht, The Netherlands. : Springer.
    [Google Scholar]
  16. Ince, I. A., Boeren, S., van Oers, M. M., Vervoort, J. J. M. & Vlak, J. M. ( 2010; ). Proteomic analysis of Chilo iridescent virus. Virology 405, 253–258.[CrossRef]
    [Google Scholar]
  17. Jaenson, T. G. T. ( 1978; ). Virus-like rods associated with salivary gland hyperplasia in tsetse, Glossina pallidipes. Trans R Soc Trop Med Hyg 72, 234–238.[CrossRef]
    [Google Scholar]
  18. Jordan, A. M. ( 1986; ). Trypanosomiasis control and African rural development. London, UK. : Longman.
    [Google Scholar]
  19. Jura, W. G. Z. O., Odhiambo, T. R., Otieno, L. H. & Tabu, N. O. ( 1988; ). Gonadal lesions in virus-infected male and female tsetse, Glossina pallidipes (Diptera: Glossinidae). J Invertebr Pathol 52, 1–8.[CrossRef]
    [Google Scholar]
  20. Jura, W. G. Z. O., Otieno, L. H. & Chimtawi, M. M. B. ( 1989; ). Ultrastructural evidence for trans-ovum transmission of the DNA virus of tsetse, Glossina pallidipes (Diptera: Glossinidae). Curr Microbiol 18, 1–4.[CrossRef]
    [Google Scholar]
  21. Kikhno, I., Gutierrez, S., Croizier, L., Croizier, G. & Ferber, M. L. ( 2002; ). Characterization of pif, a gene required for the per os infectivity of Spodoptera littoralis nucleopolyhedrovirus. J Gen Virol 83, 3013–3022.
    [Google Scholar]
  22. Kokwaro, E. D., Nyindo, M. & Chimtawi, M. ( 1990; ). Ultrastructural changes in salivary glands of tsetse, Glossina morsitans morsitans, infected with virus and rickettsia-like organisms. J Invertebr Pathol 56, 337–346.[CrossRef]
    [Google Scholar]
  23. Kuzio, J., Jaques, R. & Faulkner, P. ( 1989; ). Identification of p74 a gene essential for virulence of baculovirus occlusion bodies. Virology 173, 759–763.[CrossRef]
    [Google Scholar]
  24. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  25. Lanier, L. M. & Volkman, L. E. ( 1998; ). Actin binding and nucleation by Autographa california M nucleopolyhedrovirus. Virology 243, 167–177.[CrossRef]
    [Google Scholar]
  26. Leu, J.-H., Tsai, J.-M., Wang, H.-C., Wang, A. H. J., Wang, C.-H., Kou, G.-H. & Lo, C. F. ( 2005; ). The unique stacked rings in the nucleocapsid of the white spot syndrome virus virion are formed by the major structural protein VP664, the largest viral structural protein ever found. J Virol 79, 140–149.[CrossRef]
    [Google Scholar]
  27. Li, X., Song, J., Jiang, T., Liang, C. & Chen, X. ( 2007; ). The N-terminal hydrophobic sequence of Autographa californica nucleopolyhedrovirus PIF-3 is essential for oral infection. Arch Virol 152, 1851–1858.[CrossRef]
    [Google Scholar]
  28. Long, M., Thornton, K., Zhang, L., Gaut, B. S., Vision, T. J., Lynch, M. & Conery, J. C. ( 2001; ). Gene duplication and evolution. Science 293, 1551.[CrossRef]
    [Google Scholar]
  29. Odindo, M. O., Payne, C. C., Crook, N. E. & Jarret, P. ( 1986; ). Properties of a novel DNA virus from the tsetse fly, Glossina pallidipes. J Gen Virol 67, 527–536.[CrossRef]
    [Google Scholar]
  30. Ohkawa, T., Washburn, J. O., Sitapara, R., Sid, E. & Volkman, L. E. ( 2005; ). Specific binding of Autographa californica M nucleopolyhedrovirus occlusion-derived virus to midgut cells of Heliothis virescens larvae is mediated by products of pif genes Ac119 and Ac022 but not by Ac115. J Virol 79, 15258–15264.[CrossRef]
    [Google Scholar]
  31. Peng, J., Elias, J. E., Thoreen, C. C., Licklider, L. J. & Gygi, S. P. ( 2003; ). Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J Proteome Res 2, 43–50.[CrossRef]
    [Google Scholar]
  32. Peng, K., Van Oers, M. M., Hu, Z. H., Van Lent, J. W. M. & Vlak, J. M. ( 2010; ). Baculovirus per os infectivity factors form a complex on the surface of occlusion-derived virus. J Virol doi:.
    [Google Scholar]
  33. Pijlman, G. P., Pruijssers, A. J. & Vlak, J. M. ( 2003; ). Identification of pif-2, a third conserved baculovirus gene required for per os infection of insects. J Gen Virol 84, 2041–2049.[CrossRef]
    [Google Scholar]
  34. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY. : Cold Spring Harbor Laboratory.
    [Google Scholar]
  35. Sang, R. C., Jura, W. G. Z. O., Otieno, L. H. & Ogaja, P. ( 1996; ). Ultrastructural changes in the milk gland of tsetse Glossina morsitans centralis (Diptera; Glissinidae) female infected by a DNA virus. J Invertebr Pathol 68, 253–259.[CrossRef]
    [Google Scholar]
  36. Sang, R. C., Jura, W. G. Z. O., Otieno, L. H. & Mwangi, R. W. ( 1998; ). The effects of a DNA virus infection on the reproductive potential of female tsetse flies, Glossina morsitans centralis and Glossina morsitans morsitans (Diptera: Glossinidae). Mem Inst Oswaldo Cruz 93, 861–864.[CrossRef]
    [Google Scholar]
  37. Sang, R. C., Jura, W. G. Z. O., Otieno, L. H., Mwangi, R. W. & Ogaja, P. ( 1999; ). The effects of a tsetse DNA virus infection on the functions of the male accessory reproductive gland in the host fly Glossina morsitans centralis (Diptera: Glossinidae). Curr Microbiol 38, 349–354.[CrossRef]
    [Google Scholar]
  38. Slack, J. & Arif, B. M. ( 2007; ). The baculoviruses occlusion-derived virus: virion structure and function. Adv Virus Res 69, 99–165.
    [Google Scholar]
  39. Slack, J. M., Lawrence, S. D., Krell, P. J. & Arif, B. M. ( 2010; ). A soluble form of P74 can act as a per os infectivity factor to the Autographa californica multiple nucleopolyhedrovirus. J Gen Virol 91, 915–918.[CrossRef]
    [Google Scholar]
  40. Song, J., Wang, R., Deng, F., Wang, H. & Hu, Z. ( 2008; ). Functional studies of per os infectivity factors of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus. J Gen Virol 89, 2331–2338.[CrossRef]
    [Google Scholar]
  41. Steelman, C. D. ( 1976; ). Effects of external and internal arthropod parasites on domestic livestock production. Annu Rev Entomol 21, 155–178.[CrossRef]
    [Google Scholar]
  42. van Hulten, M. C. W., Witteveldt, J., Peters, S., Kloosterboer, N., Tarchini, R., Fiers, M., Sandbrink, H., Lankhorst, R. K. & Vlak, J. M. ( 2001; ). The white spot syndrome virus DNA genome sequence. Virology 286, 7–22.[CrossRef]
    [Google Scholar]
  43. Vreysen, M. J. B., Saleh, K. M., Ali, M. Y., Abdulla, A. M., Zhu, Z.-R., Juma, K. G., Dyck, V. A., Msangi, A. R., Mkonyi, P. A. & Feldmann, H. U. ( 2000; ). Glossina austeni (Diptera: Glossinidae) eradicated on the island of Unguja, Zanzibar, using the sterile insect technique. J Econ Entomol 93, 123–135.[CrossRef]
    [Google Scholar]
  44. Wang, R., Deng, F., Houm, D., Zhao, Y., Gua, L., Wang, H. & Hu, Z. H. ( 2010; ). Proteomics of the Autographa californica nucleopolyhedrovirus budded virions. J Virol 84, 7233–7242.[CrossRef]
    [Google Scholar]
  45. WHO ( 2001; ). Report on African trypanosomiasis (sleeping sickness), WHO/TDR Committee Report TDR/SWG/01. Geneva, Switzerland: World Health Organization.
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vol. , part 12, pp. 3065 - 3074

Primer sequences used for the amplification of the candidate GpSGHV genes* [PDF](54 KB)



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