Comprehensive annotation of glossina pallidipes salivary gland hypertrophy virus from ethiopian tsetse flies: A proteogenomics approach

Journal of General Virology

Volumn 97, Issue 4, 2016, Pages 1010-1031

  Abd Alla, Adly M M ^a   Kariithi, Henry M ^a,b,c   Cousserans, FranÇois ^d   Parker, Nicolas J ^e   İnce, İkbal Agah ^f   Scully, Erin D ^g   Boeren, Sjef ^c   Geib, Scott M ^h   Mekonnen, Solomon ⁱ   Vlak, Just M ^c   Parker, Andrew G ^a   Vreysen, Marc J B ^a   Bergoin, Max ^d  

^a INTERNATIONAL ATOMIC ENERGY AGENCY   (Austria)

^b KENYA AGRICULTURAL AND LIVESTOCK RESEARCH ORGANIZATION   (Kenya)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d UNIV MONTPELLIER   (France)

^e Acibadem University ^*  (United Kingdom)

^f ACIBADEM UNIVERSITY   (Turkey)

^g UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^h U S DEPARTMENT OF AGRICULTURE   (United States)

ⁱ National Institute for Control and Eradication of Tsetse and Trypanosomosis (NICETT)   (Ethiopia)

Author keywords

[No Author keywords available]

Indexed keywords

REGULATOR PROTEIN; RNA POLYMERASE; RNA POLYMERASE LEF4; RNA POLYMERASE LEF5; RNA POLYMERASE LEF8; RNA POLYMERASE LEF9; TRANSCRIPTOME; UNCLASSIFIED DRUG; VIRUS PROTEIN; CORE PROTEIN; DNA VIRUS; VIRULENCE FACTOR; VIRUS DNA;

ARTICLE; ENVIRONMENTAL FACTOR; GENETIC DIFFERENCE; GENETIC HETEROGENEITY; GLOSSINA PALLIDIPES SALIVARY GLAND HYPERTROPHY VIRUS; GLOSSINIDAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VIRUS; VIRUS GENOME; VIRUS ISOLATION; ANIMAL; CHROMOSOMAL MAPPING; CLASSIFICATION; DNA BASE COMPOSITION; GENETICS; GENOME SIZE; INSECT VIRUS; MOLECULAR GENETICS; OPEN READING FRAME; PATHOGENICITY; PROCEDURES; PROTEOMICS; SALIVARY GLAND; VIROLOGY;

ANIMALS; BASE COMPOSITION; BASE SEQUENCE; CHROMOSOME MAPPING; DNA VIRUSES; DNA, VIRAL; GENOME SIZE; GENOME, VIRAL; INSECT VIRUSES; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PROTEOMICS; SALIVARY GLANDS; TRANSCRIPTOME; TSETSE FLIES; VIRAL CORE PROTEINS; VIRULENCE FACTORS;

EID: 84963724317     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000409     Document Type: Article

References (76)

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.
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 reveals a novel, large, double-stranded circular DNA virus. J Virol 82, 4595–4611.
3. Abd-Alla, A. M. M., Kariithi, H. M., 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.
4. Abd-Alla, A. M. M., Parker, A. G., Vreysen, M. J. B. & Bergoin, M. (2011). Tsetse salivary gland hypertrophy virus: hope or hindrance for tsetse control? PLoS Negl Trop Dis 5, e1220.
5. Abd-Alla, A. M. M., Kariithi, H. M., Mohamed, A. H., Lapiz, E., Parker, A. G. & Vreysen, M. J. B. (2013). Managing hytrosavirus infections in Glossina pallidipes colonies: feeding regime affects the prevalence of salivary gland hypertrophy syndrome. PLoS One 8, e61875.
6. Abd-Alla, A. M. M., Marin, C., Parker, A. G. & Vreysen, M. J. B. (2014). Antiviral drug valacyclovir treatment combined with a clean feeding system enhances the suppression of salivary gland hypertrophy in laboratory colonies of Glossina pallidipes. Parasit Vectors 7, 214.
7. Armengaud, J. (2009). A perfect genome annotation is within reach with the proteomics and genomics alliance. Curr Opin Microbiol 12, 292–300.
8. Aronesty, E. (2013). Comparison of sequencing utility programs. Open Bioinform J 7, 1–8.
9. Asser-Kaiser, S., Heckel, D. G. & Jehle, J. A. (2010). Sex linkage of CpGV resistance in a heterogeneous field strain of the codling moth Cydia pomonella (L.). J Invertebr Pathol 103, 59–64.
10. Asser-Kaiser, S., Radtke, P., El-Salamouny, S., Winstanley, D. & Jehle, J. A. (2011). Baculovirus resistance in codling moth (Cydia pomonella L.) caused by early block of virus replication. Virology 410, 360–367.
11. Barrera, G., Williams, T., Villamizar, L., Caballero, P. & Simón, O. (2013). Deletion genotypes reduce occlusion body potency but increase occlusion body production in a Colombian Spodoptera frugiperda nucleopolyhedrovirus population. PLoS One 8, e77271.
12. Barrett, M. P., Vincent, I. M., Burchmore, R. J., Kazibwe, A. J. & Matovu, E. (2011). Drug resistance in human African trypanosomiasis. Future Microbiol 6, 1037–1047.
13. Bernal, A., Williams, T., Muñoz, D., Caballero, P. & Simón, O. (2013). Complete genome sequences of five Chrysodeixis chalcites nucleopolyhedrovirus genotypes from a Canary Islands isolate. Genome Announc 1, e00873–e00813.
14. Bolger, A. M., Lohse, M. & Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.
15. Boucias, D. G., Kariithi, H. M., Bourtzis, K., Schneider, D. I., Kelley, K., Miller, W. J., Parker, A. G. & Abd-Alla, A. M. M. (2013). Transgenerational transmission of the Glossina pallidipes hytrosavirus depends on the presence of a functional symbiome. PLoS One 8, e61150.
16. Carver, T. J., Rutherford, K. M., Berriman, M., Rajandream, M. A., Barrell, B. G. & Parkhill, J. (2005). ACT: the Artemis comparison tool. Bioinformatics 21, 3422–3423.
17. Chen, Y. R., Zhong, S., Fei, Z., Hashimoto, Y., Xiang, J. Z., Zhang, S. & Blissard, G. W. (2013). The transcriptome of the baculovirus Autographa californica multiple nucleopolyhedrovirus in Trichoplusia ni cells. J Virol 87, 6391–6405.
18. Clavijo, G., Williams, T., Muñoz, D., Caballero, P. & López-Ferber, M. (2010). Mixed genotype transmission bodies and virions contribute to the maintenance of diversity in an insect virus. Proc Biol Sci 277, 943–951.
19. Cochran, M. A. & Faulkner, P. (1983). Location of homologous DNA sequences interspersed at five regions in the baculovirus AcMNPV genome. J Virol 45, 961–970.
20. Conesa, A., Götz, S., García-Gómez, J. M., Terol, J., Talón, M. & Robles, M. (2005). Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676.
21. Corcelette, S., Massé, T. & Madjar, J. J. (2000). Initiation of translation by non-AUG codons in human T-cell lymphotropic virus type I mRNA encoding both Rex and Tax regulatory proteins. Nucleic Acids Res 28, 1625–1634.
22. 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.
23. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V. & Mann, M. (2011). Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 10, 1794–1805.
24. Cui, L., Cheng, X., Li, L. & Li, J. (2007). Identification of Trichoplusia ni ascovirus 2c virion structural proteins. J Gen Virol 88, 2194–2197.
25. den Dunnen, J. T. & Antonarakis, S. E. (2001). Nomenclature for the description of human sequence variations. Hum Genet 109, 121–124.
26. Doi, H. (1991). Importance of purine and pyrimidine content of local nucleotide sequences (six bases long) for evolution of the human immunodeficiency virus type 1. Proc Natl Acad Sci U S A 88, 9282–9286.
27. Dresang, L. R., Teuton, J. R., Feng, H., Jacobs, J. M., Camp, D. G. II, Purvine, S. O., Gritsenko, M. A., Li, Z., Smith, R. D. & other authors (2011). Coupled transcriptome and proteome analysis of human lymphotropic tumor viruses: insights on the detection and discovery of viral genes. BMC Genomics 12, 625.
28. Feldmann, U., Dyck, V. A., Mattioli, R. C. & Jannin, J. (2005). Potential impact of tsetse fly control involving the sterile insect technique. In Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management, pp. 701–723. Edited by V. A. Dyck, J. Hendrichs & A. S. Robinson. Dordrecht: Springer.
29. Finn, R. D., Tate, J., Mistry, J., Coggill, P. C., Sammut, S. J., Hotz, H. R., Ceric, G., Forslund, K., Eddy, S. R. & other authors (2008). The Pfam protein families database. Nucleic Acids Res 36 (Database), D281–D288.
30. Garcia-Maruniak, A., Abd-Alla, A. M. M., Salem, T. Z., Parker, A. G., Lietze, V. U., van Oers, M. M., Maruniak, J. E., Kim, W., Burand, J. P. & 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
31. Gupta, K. C., Ono, E., Ariztia, E. V. & Inaba, M. (1994). Translation initiation from non-AUG codons in COS1 cells is mRNA species dependent. Biochem Biophys Res Commun 201, 567–573.
32. Heler, R., Samai, P., Modell, J. W., Weiner, C., Goldberg, G. W., Bikard, D. & Marraffini, L. A. (2015). Cas9 specifies functional viral targets during CRISPR-Cas adaptation. Nature 519, 199–202.
33. Jaenson, T. G. T. (1978a). Mating behaviour of Glossina pallidipes Austen (Diptera, Glossinidae): genetic differences in copulation time between allopatric populations. Entomol Exp Appl 24, 100–108.
34. Jaenson, T. G. T. (1978b). Reproductive biology of the tsetse Glossina pallidipes Austen (Diptera, Glossinidae) with special reference to mating behaviour. PhD thesis, Uppsala University, Uppsala, Sweden.
35. Jehle, J. A., Abd-Alla, A. M. & Wang, Y. (2013). Phylogeny and evolution of Hytrosaviridae. J Invertebr Pathol 112 (Suppl), S62–S67.
36. Joannin, N., Abhiman, S., Sonnhammer, E. L. & Wahlgren, M. (2008). Sub-grouping and sub-functionalization of the RIFIN multi-copy protein family. BMC Genomics 9, 19.
37. Jordan, A. M. (1986). Trypanosomiasis Control and African Rural Development. London: Longman Higher Education.
38. Kariithi, H. M., Ince, I. A., Boeren, S., Vervoort, J., Bergoin, M., van Oers, M. M., Abd-Alla, A. M. M. & Vlak, J. M. (2010). Proteomic analysis of Glossina pallidipes salivary gland hypertrophy virus virions for immune intervention in tsetse fly colonies. J Gen Virol 91, 3065–3074.
39. Kariithi, H. M., Ince, I. A., Boeren, S., Abd-Alla, A. M. M., Parker, A. G., Aksoy, S., Vlak, J. M. & van Oers, M. M. (2011). The salivary secretome of the tsetse fly Glossina pallidipes (Diptera: Glossinidae) infected by salivary gland hypertrophy virus. PLoS Negl Trop Dis 5, e1371.
40. Kariithi, H. M., Ahmadi, M., Parker, A. G., Franz, G., Ros, V. I. D., Haq, I., Elashry, A. M., Vlak, J. M., Bergoin, M. & other authors (2013a). Prevalence and genetic variation of salivary gland hypertrophy virus in wild populations of the tsetse fly Glossina pallidipes from southern and eastern Africa. J Invertebr Pathol 112 (Suppl), S123–S132.
41. Kariithi, H. M., van Lent, J. W., Boeren, S., Abd-Alla, A. M., Ìnce, I. A., van Oers, M. M. & Vlak, J. M. (2013b). Correlation between structure, protein composition, morphogenesis and cytopathology of Glossina pallidipes salivary gland hypertrophy virus. J Gen Virol 94, 193–208.
42. Kariithi, H. M., van Oers, M. M., Vlak, J. M., Vreysen, M. J., Parker, A. G. & Abd-Alla, A. M. (2013c). Virology, epidemiology and pathology of Glossina hytrosavirus, and its control prospects in laboratory colonies of the tsetse fly, Glossina pallidipes (Diptera; Glossinidae). Insects 4, 287–319.
43. Kariithi, H. M., Ince, A. I., Boeren, S., Murungi, E. K., Meki, I. K., Otieno, E. A., Nyanjom, S. R. G., van Oers, M. M., Vlak, J. M. & other authors (2016). Comparative analysis of salivary gland proteomes of two Glossina species that exhibit differential hytrosavirus pathologies. Front Microbiol 7, 89.
44. Korber, B. T. M. (2000). HIV signature and sequence variation analysis. In Computational Analysis of HIV Molecular Sequences, pp. 55–72. Edited by A. G. Rodrigo & G. H. Learn. Dordrecht: Kluwer Academic.
45. Kreitman, M. & Akashi, H. (1995). Molecular evidence for natural selection. Annu Rev Ecol Syst 26, 403–422.
46. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10, R25.
47. López-Ferber, M., Simón, O., Williams, T. & Caballero, P. (2003). Defective or effective? Mutualistic interactions between virus genotypes. Proc Biol Sci 270, 2249–2255.
48. Magoc, T., Wood, D. & Salzberg, S. L. (2013). EDGE-pro: estimated degree of gene expression in prokaryotic genomes. Evol Bioinform Online 9, 127–136.
49. Marchler-Bauer, A., Derbyshire, M. K., Gonzales, N. R., Lu, S., Chitsaz, F., Geer, L. Y., Geer, R. C., He, J., Gwadz, M. & other authors (2015). CDD: NCBI’s conserved domain database. Nucleic Acids Res 43 (D1), D222–D226.
50. Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J., Braverman, M. S., Chen, Y. J. & other authors (2005). Genome sequencing in microfabricated highdensity picolitre reactors. Nature 437, 376–380.
51. McCarthy, C. B. & Theilmann, D. A. (2008). AcMNPV ac143 (odv-e18) is essential for mediating budded virus production and is the 30th baculovirus core gene. Virology 375, 277–291.
52. Miele, S. A., Garavaglia, M. J., Belaich, M. N. & Ghiringhelli, P. D. (2011). Baculovirus: molecular insights on their diversity and conservation. Int J Evol Biol 2011, 379424.
53. Mitchell, A., Chang, H. Y., Daugherty, L., Fraser, M., Hunter, S., López, R., McAnulla, C., McMenamin, C., Nuka, G. & other authors (2015). InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res 43 (D1), D213–D221.
54. Nei, M. & Gojobori, T. (1986). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3, 418–426.
55. Nesvizhskii, A. I. (2014). Proteogenomics: concepts, applications and computational strategies. Nat Methods 11, 1114–1125.
56. Niang, M., Yan Yam, X. & Preiser, P. R. (2009). The Plasmodium falciparum STEVOR multigene family mediates antigenic variation of the infected erythrocyte. PLoS Pathog 5, e1000307.
57. Nielsen, R. & Yang, Z. (1998). Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148, 929–936.
58. Parker, N. J. & Parker, A. G. (2008). Simple tools for assembling and searching high-density picolitre pyrophosphate sequence data. Source Code Biol Med 3, 5.
59. Rohrmann, G. F. (2013). The AcMNPV genome: gene content, conservation, and function. In Baculovirus Molecular Biology, 3rd edn, pp. 153–193. Bethesda, MD: National Center for Biotechnology Information.
60. Sanders, W. S., Wang, N., Bridges, S. M., Malone, B. M., Dandass, Y. S., McCarthy, F. M., Nanduri, B., Lawrence, M. L. & Burgess, S. C. (2011). The proteogenomic mapping tool. BMC Bioinformatics 12, 115.
61. Schnitzler, P., Delius, H., Scholz, J., Touray, M., Orth, E. & Darai, G. (1987). Identification and nucleotide sequence analysis of the repetitive DNA element in the genome of fish lymphocystis disease virus. Virology 161, 570–578.
62. Schofield, C. J. & Kabayo, J. P. (2008). Trypanosomiasis vector control in Africa and Latin America. Parasit Vectors 1, 24.
63. Simón, O., Williams, T., López-Ferber, M. & Caballero, P. (2004). Genetic structure of a Spodoptera frugiperda nucleopolyhedrovirus population: high prevalence of deletion genotypes. Appl Environ Microbiol 70, 5579–5588.
64. Simón, O., Williams, T., López-Ferber, M. & Caballero, P. (2005). Functional importance of deletion mutant genotypes in an insect nucleopolyhedrovirus population. Appl Environ Microbiol 71, 4254–4262.
65. Slack, J. & Arif, B. M. (2007). The baculoviruses occlusion-derived virus: virion structure and function. Adv Virus Res 69, 99–165.
66. Sokal, R. R. & Rohlf, F. J. (2012). Biometry: The Principles and Practice of Statistics in Biological Research. New York, NY: Freeman.
67. Steelman, C. D. (1976). Effects of external and internal arthropod parasites on domestic livestock production. Annu Rev Entomol 21, 155–178.
68. Syed Musthaq, S., Sudhakaran, R., Ishaq Ahmed, V. P., Balasubramanian, G. & Sahul Hameed, A. S. (2006). Variability in the tandem repetitive DNA sequences of white spot syndrome virus (WSSV) genome and suitability of VP28 gene to detect different isolates of WSSV from India. Aquaculture 256, 34–41.
69. van der Ende, A., Pan, Z. J., Bart, A., van der Hulst, R. W. M., Feller, M., Xiao, S. D., Tytgat, G. N. J. & Dankert, J. (1998). cagA-positive Helicobacter pylori populations in China and The Netherlands are distinct. Infect Immun 66, 1822–1826.
70. Virto, C., Navarro, D., Tellez, M. M., Herrero, S., Williams, T., Murillo, R. & Caballero, P. (2014). Natural populations of Spodoptera exigua are infected by multiple viruses that are transmitted to their offspring. J Invertebr Pathol 122, 22–27.
71. Vreysen, M. J. B., Seck, M. T., Sall, B. & Bouyer, J. (2013). Tsetse flies: their biology and control using area-wide integrated pest management approaches. J Invertebr Pathol 112 (Suppl), S15–S25.
72. Wang, Y., Kleespies, R. G., Huger, A. M. & Jehle, J. A. (2007). The genome of Gryllus bimaculatus nudivirus indicates an ancient diversification of baculovirus-related nonoccluded nudiviruses of insects. J Virol 81, 5395–5406.
73. Wang, Y., Bininda-Emonds, O. R., van Oers, M. M., Vlak, J. M. & Jehle, J. A. (2011). The genome of Oryctes rhinoceros nudivirus provides novel insight into the evolution of nuclear arthropodspecific large circular double-stranded DNA viruses. Virus Genes 42, 444–456.
74. Whitnall, A. B. M. (1934). The trypanosome infections of Glossina pallidipes in the Umfolosi Game Reserve, Zululand. Onderstepoort J Vet Sci Anim Ind 2, 2–21.
75. Wilson, A. C., Carlson, S. S. & White, T. J. (1977). Biochemical evolution. Annu Rev Biochem 46, 573–639.
76. Wolf, Y. I., Viboud, C., Holmes, E. C., Koonin, E. V. & Lipman, D. J. (2006). Long intervals of stasis punctuated by bursts of positive selection in the seasonal evolution of influenza A virus. Biol Direct 1, 34.