Hytrosaviridae

Hytrosaviridae
Schematic drawing
Virus classification
(unranked): Virus
Realm: incertae sedis
Kingdom: incertae sedis
Phylum: incertae sedis
Class: Naldaviricetes
Order: Lefavirales
Family: Hytrosaviridae
Genera

Glossinavirus
Muscavirus

Hytrosaviridae is a family of double-stranded DNA viruses that infect insects.[1][2][3] The name is derived from Hytrosa, sigla from the Greek Hypertrophia for 'hypertrophy' and 'sialoadenitis' for 'salivary gland inflammation.'

Description

The viruses in this family are non occluded, enveloped, rod-shaped virions measuring 500–1,000 nanometers (nm) in length and 50–80 nm in diameter.[4] The virions contain a thin, dense central nucleocapsid that encases the DNA-protein core. The nucleocapsid core is surrounded by an amorphous proteinaceous tegument layer.[5] The outer surface of the virions is studded with helical polymeric structure composed of virally-encoded and host-derived protein dimers. The virions contain at least 35 polypeptides which range in size from 10 to 200 kiloDaltons.

The genome is a supercoiled, circular double stranded DNA (dsDNA) molecule ranging in size from 120 to 190 kilobases with 108-174 putative non-overlapping genes that are equally distributed over the genome in unidirectional clusters.[6] The G+C ratio varies between 28% and 44%.

Species in this family cause overt salivary gland hypertrophy symptoms in dipteran adults. Infection and replication in non-salivary gland cells induce partial in tsetse flies and complete shutdown of vitellogenesis in the houseflies,.[7][8]

Replication occurs in the nucleus of secretory epithelial cells of the salivary gland. The viral DNA synthesis and transcription occurs within the nuclear replication complexes. Replication involved temporal expression of immediate early, early and late genes. The nucleocapsids exit the nucleus into the cytoplasm through the nuclear pore complex, after which they associate with the Golgi apparatus that culminates in cytoplasmic envelopment and virion assembly.

Transmission is either horizontally (per os) through feeding or vertically (transovarially) from mother to offspring,.[9][10] Mechanical transmission (trans-cuticular though wounds) has been suggested in the houseflies.[11]

Taxonomy

Two genera, each containing one species, are assigned to this family:[12]

  • Glossinavirus
    • Glossina hytrosavirus, also called Glossina pallidipes salivary gland hypertrophy virus (GpSGHV)[13][14]
  • Muscavirus
    • Musca hytrosavirus, also called Musca domestica salivary gland hypertrophy virus (MdSGHV)[15]

Host Range

  • Glossina pallidipes. This is the natural host of Glossina pallidipes salivary gland hypertrophy virus (GpSGHV), in which the virus predominantly causes chronic asymptomatic (covert) SGH infections. GpSGHV is highly specific to Glossina species. There is no available evidence for GpSGHV infections or replication in heterologous host species such as the housefly. The susceptibility of the tsetse fly to GpSGHV infections differ widely in different Glossina species, of which Glossina pallidipes is the most susceptible. Up to 15 different GpSGHV haplotypes with varying prevalence rates have been reported in the wild populations of tsetse flies in East, Central and West Africa,.[16][17]
  • Musca domestica. The common housefly is the natural host of Musca domestica salivary gland hypertrophy virus (MdSGHV), in which the virus causes only acute symptomatic (overt) SGH infections,.[18][19] Under laboratory setting, MdSGHV can infect other insects, including the obligate hemato phagous stable flies (Stomoxys calcitrans), the autumn housefly (Musca autumnalis), and the larvae predator of the housefly, the black dump fly (Hydrotaea aenescens).[20] However, MdSGHV does not induce overt SGH symptoms in hosts other than the housefly, but it does significantly affect ovarian development and cause mortalities in some of the muscids such as the stable fly and dump fly.
  • Merodon equestris. The hytrosavirus infecting this phytophagous syrphid fly [21] is yet to be characterized.

Morphologically and symptomologically similar virus to SGHVs has been reported to cause SGH symptoms in the male accessory gland filaments of the solitary braconid wasp, Diachasmimorpha longicuadata Ashmed (Hymenoptera. Braconidae),[22] which suggests existence of other Hytrosaviridae family members.

Virology

Prevalence of this virus is high (80%) in Glossina pallidipes. Within the housefly populations, MdSGHV induces variable rates of overt SGH symptoms (0-40%), which is related to the fly's seasonal densities at various sampling sites.[23]

Pathogenesis and Tissue Tropism

Hytrosaviruses (SGHVs) induce similar gross pathology (SGH symptoms) in the salivary glands of their respective adult insect hosts, but the cytopathogies are distinct for the each of the two known genera (Glossinavirus and Muscavirus). Both pairs of the salivary gland tissue are equally affected (swollen up to four times their normal sizes) with the enlargement extending the entire lengths of the distal regions of the salivary glands. Infections of tissues other than the salivary glands is associated with various pathologies such as reproductive dysfunctions, infertility in females and distorted mating behaviors.

Pathogenesis in the Salivary Glands

GpSGHV causes salivary gland hyperplasia in the infected tsetse flies, i.e. only the cytoplasmic but not the nuclear compartment of the glands are enlarged.[24] However, the hyperplastic salivary gland cells are capable of dividing. This pathology is thought to be due to the virus-induced reprogramming of the differentiated salivary gland cells. Overall, the induction of overt SGH symptoms is typically the exemption rather than the rule. It is only under some unknown conditions that the asymptomatic infection state is triggered to the symptomatic infection state.[25] When GpSGHV is artificially inoculated (intrahemocoelic) into adult stages of the tsetse fly Glossina pallidipes, overt SGH symptoms develop in the F1 offsprings produced by the injected mothers, but not in the parental generation.[26] MdSGHV induces salivary gland hypertrophy in the housefly, i.e. both the cytoplasmic and nuclear compartments of the salivary gland tissue proliferate, but are incapable of dividing. When MdSGHV suspensions are artificially infected into adult houseflies, the virus induces overt SGH symptoms in 100% of the infected flies within three days post infection.[27] Adult housefly develops increased resistance to MdSGHV infections with age, which is partially attributed to the development of the PM barrier in the fly's midguts.

Pathogenesis in non-Salivary Gland Tissues

Infections of non-salivary gland tissues in the tsetse flies by GpSGHV is associated with testicular degeneration, ovarian abnormalities, severe necrosis, degeneration of germinaria, and a reduction of the fly's development, survival and fecundity. Infections of the milk glands cause necrosis and depletion of the milk reservoir organelles.

In the housefly, MdSGHV in non-salivary gland tissues blocks the production of sesquiterpenoids, which in turn induces complete shutdown of vitellogenesis. The ovaries of viremic housefly females become arrested at the pre-vitellogenic stages. MdSGHV induces behavioral alterations in infected females, which refuse to copulate with either healthy or viremic males.[28]

Viral Latency

The asymptomatic GpSGHV infection state represents either a sub-lethal persistence or latency. Host's RNA interference (RNAi) machineries such as the small interfering RNA (siRNA) and micro RNA (miRNA) pathways have been implicated in keeping GpSGHV infections under control,.[29][30]

Similarities with other Virus Taxa

Structurally, hytrosaviruses are similar to members of other arthropod-infecting virus families such as Baculoviridae, Nudiviridae and Nimaviridae. Hytrosaviruses share 12 of the 38 core genes that have been described in baculoviruses, nudiviruses, nimaviruses and some bracoviruses. Some of the structural and genomic features shared between hytrosaviruses and other large, dsDNA viruses include the possession of enveloped, rod-shaped virions, circular dsDNA genomes and replication in the nucleus of infected cells. However, hytrosaviruses differ functionally with baculoviruses by the lack of occlusion bodies and lower lethality.[31]

The viral DNA polymerase encoded is type B, which is present and conserved in all large dsDNA viruses. At the amino acid level, the best match of the DNA polB of hytrosaviruses is to the DNA polB found in the Alcelaphine gammaherpesvirus,.[32][33][34] Based on the DNA polB gene, hytrosaviruses relate more closely with invertebrate viruses with large linear dsDNA compared to viruses with circular dsDNA genomes. Some of the linear dsDNA viruses that cluster together with hytrosaviruses include members of families Herpesviridae (120-240 kp), Iridoviridae (140-303 bp), Poxviridae (130–375 kb), Phycodnaviridae (100–560 kb) and Mimiviridae (1200 kb).[35] Hytrosaviruses encode homologs to the core and highly conserved oral infectivity factor (PIF) genes found in other dsDNA viruses (PIFs o/P74, 1,2 and 3), and occlusion-derived virus (ODV) envelope of epidopteran baculoviruses (OVD-E66). Also found in hytrosaviruses are homologs to some of the subunits of the DNA-dependent RNA polymerase (DdRp) complex found in baculoviruses and nudivuses. The DdRp complex components present in the hytrosaviruses include the late expression factors 4, 5, 8 and 9 (LEF-4, LEF-5, LEF-8 and LEF-9).[36]

Diagnosis and Management of Hytrosavirus Infections

In mass rearing facilities, infections of tsetse flies by hytrosavirus causes reduction in colony productivity, which can cause collapse of the colonies.[37] The virus is introduced into the mass rearing facilities from asymptomatic, field-collected materials, or material derived from already existing colonies, that are used to establish new or replenish existing colonies. The virus is then spread and maintained in the colonies through vertical transmission. Unknown factors (e.g. stress or genetic) can trigger expression of overt SGH symptoms, shich culminate in fly mortalities, reduced fecundity and eventual colony collapse. There are no obvious external clinical signs for hytrosavirus infections. The hytrosavirus infecting the tsetse flies can be diagnosed using a simple, sensitive and reliable non-destructive PCR-based assay, which allows the screening of the virus in individual live flies.[38] Hytrosavirus infections in mass-reared tsetse flies can be effectively managed by an integrated approach involving a "clean feeding system" (CFS), which is based on strict sanitation, regular and routing monitoring of viral infections and the occurrence of overt SGH symptoms.[39] The CFS can be combined with supplementation of bloodmeals with antiviral drugs such as valacyclovir, which are administered at low doses that are non-detrimental to the fly's DNA synthesis.[40] When administered, the antiviral drug is converted into active metabolites by the virally-encoded thymidylate synthase. The active metabolites subsequently block viral replication resulting in the reduction of viral titers and shedding.

References

  1. ↑ Abd-Alla A, Vlak J, Bergoin M, Maruniak J, Parker A, Burand J, Jehle J, Boucias D and Hytrosavirus Study Group of the ICTV (2009) Hytrosaviridae: a proposal for classification and nomenclature of a new insect virus family. Arch Virol 154:909–918
  2. ↑ Kariithi, HM; Vlak, JM; Jehle, JA; Bergoin, M; Boucias, DG; Abd-Alla, AMM; ICTV Report, Consortium (September 2019). "ICTV Virus Taxonomy Profile: Hytrosaviridae". The Journal of General Virology. 100 (9): 1271–1272. doi:10.1099/jgv.0.001300. PMID 31389783.
  3. ↑ "ICTV Report Hytrosaviridae".
  4. ↑ Kariithi, Henry M.; Meki, Irene K. (January 2021). "Hytrosaviruses (Hytrosaviridae: Glossinavirus and Muscavirus)". Reference Module in Life Sciences (4 ed.). [Place of publication not identified]: Elsevier. pp. 780–791. doi:10.1016/B978-0-12-809633-8.21553-7. ISBN 978-0-12-809633-8. S2CID 226478284.
  5. ↑ Kariithi, Henry M.; van Lent, Jan W. M.; Boeren, Sjef; Abd-Alla, Adly M. M.; İnce, İkbal Agah; van Oers, Monique M.; Vlak, Just M. (2013). "Correlation between structure, protein composition, morphogenesis and cytopathology of Glossina pallidipes salivary gland hypertrophy virus". Journal of General Virology. 94 (1): 193–208. doi:10.1099/vir.0.047423-0. PMID 23052395.
  6. ↑ Abd-Alla, Adly M. M.; Kariithi, Henry M.; Cousserans, François; Parker, Nicolas J.; İnce, İkbal Agah; Scully, Erin D.; Boeren, Sjef; Geib, Scott M.; Mekonnen, Solomon; Vlak, Just M.; Parker, Andrew G.; Vreysen, Marc J. B.; Bergoin, Max (2016). "Comprehensive annotation of Glossina pallidipes salivary gland hypertrophy virus from Ethiopian tsetse flies: a proteogenomics approach". Journal of General Virology. 97 (4): 1010–1031. doi:10.1099/jgv.0.000409. PMC 4854362. PMID 26801744.
  7. ↑ Kariithi, Henry M; Meki, Irene K; Boucias, Drion G; Abd-Alla, Adly MM (1 August 2017). "Hytrosaviruses: current status and perspective". Current Opinion in Insect Science. 22: 71–78. doi:10.1016/j.cois.2017.05.009. ISSN 2214-5745. PMID 28805642.
  8. ↑ Kariithi, Henry M.; Yao, Xu; Yu, Fahong; Teal, Peter E.; Verhoeven, Chelsea P.; Boucias, Drion G. (5 April 2017). "Responses of the Housefly, Musca domestica, to the Hytrosavirus Replication: Impacts on Host's Vitellogenesis and Immunity". Frontiers in Microbiology. 8 (583): 583. doi:10.3389/fmicb.2017.00583. ISSN 1664-302X. PMC 5380684. PMID 28424677.
  9. ↑ Boucias, Drion G.; Kariithi, Henry M.; Bourtzis, Kostas; Schneider, Daniela I.; Kelley, Karen; Miller, Wolfgang J.; Parker, Andrew G.; Abd-Alla, Adly M. M. (2013). "Transgenerational transmission of the Glossina pallidipes hytrosavirus depends on the presence of a functional symbiome". PLOS ONE. 8 (4): e61150. Bibcode:2013PLoSO...861150B. doi:10.1371/journal.pone.0061150. ISSN 1932-6203. PMC 3632566. PMID 23613801.
  10. ↑ Abd-Alla, Adly M. M.; Kariithi, Henry M.; Parker, Andrew G.; Robinson, Alan S.; Kiflom, Musie; Bergoin, Max; Vreysen, Marc J. B. (1 June 2010). "Dynamics of the salivary gland hypertrophy virus in laboratory colonies of Glossina pallidipes (Diptera: Glossinidae)". Virus Research. 150 (1): 103–110. doi:10.1016/j.virusres.2010.03.001. ISSN 0168-1702. PMID 20214934.
  11. ↑ Vallejo, Celeste R.; Lee, Jo Ann; Keesling, James E.; Geden, Christopher J.; Lietze, Verena-Ulrike; Boucias, Drion G. (20 November 2013). "A Mathematic Model That Describes Modes of MdSGHV Transmission within House Fly Populations". Insects. 4 (4): 683–693. doi:10.3390/insects4040683. ISSN 2075-4450. PMC 4553510. PMID 26462530.
  12. ↑ "Virus Taxonomy: 2020 Release". International Committee on Taxonomy of Viruses (ICTV). March 2021. Retrieved 12 May 2021.
  13. ↑ Abd-Alla, Adly M. M.; Cousserans, François; Parker, Andrew G.; Jehle, Johannes A.; Parker, Nicolas J.; Vlak, Just M.; Robinson, Alan S.; Bergoin, Max (2008). "Genome analysis of a Glossina pallidipes salivary gland hypertrophy virus reveals a novel, large, double-stranded circular DNA virus". Journal of Virology. 82 (9): 4595–4611. doi:10.1128/JVI.02588-07. ISSN 1098-5514. PMC 2293021. PMID 18272583.
  14. ↑ Abd-Alla, Adly M. M.; Kariithi, Henry M.; Cousserans, François; Parker, Nicolas J.; İnce, İkbal Agah; Scully, Erin D.; Boeren, Sjef; Geib, Scott M.; Mekonnen, Solomon; Vlak, Just M.; Parker, Andrew G.; Vreysen, Marc J. B.; Bergoin, Max (2016). "Comprehensive annotation of Glossina pallidipes salivary gland hypertrophy virus from Ethiopian tsetse flies: a proteogenomics approach". The Journal of General Virology. 97 (4): 1010–1031. doi:10.1099/jgv.0.000409. ISSN 1465-2099. PMC 4854362. PMID 26801744.
  15. ↑ Garcia-Maruniak, Alejandra; Maruniak, James E.; Farmerie, William; Boucias, Drion G. (20 July 2008). "Sequence analysis of a non-classified, non-occluded DNA virus that causes salivary gland hypertrophy of Musca domestica, MdSGHV". Virology. 377 (1): 184–196. doi:10.1016/j.virol.2008.04.010. ISSN 0042-6822. PMC 2583363. PMID 18495197.
  16. ↑ Kariithi, H. M.; Ahmadi, M.; Parker, A. G.; Franz, G.; Ros, V. I. D.; Haq, I.; Elashry, A. M.; Vlak, J. M.; Bergoin, M.; Vreysen, M. J. B.; Abd-Alla, A. M. M. (1 March 2013). "Prevalence and genetic variation of salivary gland hypertrophy virus in wild populations of the tsetse fly Glossina pallidipes from southern and eastern Africa". Journal of Invertebrate Pathology. 112: S123–S132. doi:10.1016/j.jip.2012.04.016. ISSN 0022-2011. PMID 22634094.
  17. ↑ Meki, Irene K.; Kariithi, Henry M.; Ahmadi, Mehrdad; Parker, Andrew G.; Vreysen, Marc J. B.; Vlak, Just M.; van Oers, Monique M.; Abd-Alla, Adly M. M. (2018). "Hytrosavirus genetic diversity and eco-regional spread in Glossina species". BMC Microbiology. 18 (Suppl 1): 143. doi:10.1186/s12866-018-1297-2. ISSN 1471-2180. PMC 6251127. PMID 30470191.
  18. ↑ 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". Medical and Veterinary Entomology. 7 (3): 275–282. doi:10.1111/j.1365-2915.1993.tb00688.x. ISSN 0269-283X. PMID 8369563. S2CID 20825786.
  19. ↑ Garcia-Maruniak, Alejandra; Maruniak, James E.; Farmerie, William; Boucias, Drion G. (20 July 2008). "Sequence analysis of a non-classified, non-occluded DNA virus that causes salivary gland hypertrophy of Musca domestica, MdSGHV". Virology. 377 (1): 184–196. doi:10.1016/j.virol.2008.04.010. ISSN 0042-6822. PMC 2583363. PMID 18495197.
  20. ↑ Geden, C.; Garcia-Maruniak, A.; Lietze, V. U.; Maruniak, J.; Boucias, D. G. (November 2011). "Impact of house fly salivary gland hypertrophy virus (MdSGHV) on a heterologous host, Stomoxys calcitrans". Journal of Medical Entomology. 48 (6): 1128–1135. doi:10.1603/me11021. ISSN 0022-2585. PMID 22238871.
  21. ↑ Amargier, A.; Lyon, J. P.; Vago, C.; Meynadier, G.; Veyrunes, J. C. (24 September 1979). "[Discovery and purification of a virus in gland hyperplasia of insects. Study of Merodon equistris F. (Diptera, Syrphidae)]". Comptes Rendus de l'Académie des Sciences, Série D. 289 (5): 481–484. ISSN 0567-655X. PMID 117940.
  22. ↑ Luo, Li; Zeng, Ling (2010). "A new rod-shaped virus from parasitic wasp Diachasmimorpha longicaudata (Hymenoptera: Braconidae)". Journal of Invertebrate Pathology. 103 (3): 165–169. doi:10.1016/j.jip.2009.08.008. ISSN 1096-0805. PMID 19682456.
  23. ↑ Geden, Christopher J.; Lietze, Verena-Ulrike; Boucias, Drion G. (2008). "Seasonal prevalence and transmission of salivary gland hypertrophy virus of house flies (Diptera: Muscidae)". Journal of Medical Entomology. 45 (1): 42–51. doi:10.1603/0022-2585(2008)45[42:spatos]2.0.co;2. ISSN 0022-2585. PMID 18283941.
  24. ↑ Kariithi, Henry M; Meki, Irene K; Boucias, Drion G; Abd-Alla, Adly MM (1 August 2017). "Hytrosaviruses: current status and perspective". Current Opinion in Insect Science. 22: 71–78. doi:10.1016/j.cois.2017.05.009. ISSN 2214-5745. PMID 28805642.
  25. ↑ Kariithi, Henry M. "Glossina hytrosavirus control strategies in tsetse fly factories: application of infectomics in virus management | Wda". library.wur.nl. Wageningen University and Research.
  26. ↑ Boucias, Drion G.; Kariithi, Henry M.; Bourtzis, Kostas; Schneider, Daniela I.; Kelley, Karen; Miller, Wolfgang J.; Parker, Andrew G.; Abd-Alla, Adly M. M. (2013). "Transgenerational transmission of the Glossina pallidipes hytrosavirus depends on the presence of a functional symbiome". PLOS ONE. 8 (4): e61150. Bibcode:2013PLoSO...861150B. doi:10.1371/journal.pone.0061150. ISSN 1932-6203. PMC 3632566. PMID 23613801.
  27. ↑ Lietze, Verena-Ulrike; Keesling, James E.; Lee, Jo Ann; Vallejo, Celeste R.; Geden, Christopher J.; Boucias, Drion G. (1 March 2013). "Muscavirus (MdSGHV) disease dynamics in house fly populations – How is this virus transmitted and has it potential as a biological control agent?". Journal of Invertebrate Pathology. 112: S40–S43. doi:10.1016/j.jip.2012.07.017. ISSN 0022-2011. PMID 22841946.
  28. ↑ Kariithi, Henry M.; Yao, Xu; Yu, Fahong; Teal, Peter E.; Verhoeven, Chelsea P.; Boucias, Drion G. (5 April 2017). "Responses of the Housefly, Musca domestica, to the Hytrosavirus Replication: Impacts on Host's Vitellogenesis and Immunity". Frontiers in Microbiology. 8: 583. doi:10.3389/fmicb.2017.00583. ISSN 1664-302X. PMC 5380684. PMID 28424677.
  29. ↑ Meki, Irene K.; Kariithi, Henry M.; Parker, Andrew G.; Vreysen, Marc J B; Ros, Vera I D; Vlak, Just M; van Oers, Monique M; Abd-Alla, Adly M. M. (23 November 2018). "RNA interference-based antiviral immune response against the salivary gland hypertrophy virus in Glossina pallidipes". BMC Microbiology. 18 (Suppl 1): 170. doi:10.1186/s12866-018-1298-1. ISSN 1471-2180. PMC 6251114. PMID 30470195.
  30. ↑ Meki, Irene K.; İnce, İkbal A.; Kariithi, Henry M.; Boucias, Drion G.; Ozcan, Orhan; Parker, Andrew G.; Vlak, Just M.; van Oers, Monique M.; Abd-Alla, Adly M. M. (3 September 2018). "Expression Profile of Glossina pallidipes MicroRNAs During Symptomatic and Asymptomatic Infection With Glossina pallidipes Salivary Gland Hypertrophy Virus (Hytrosavirus)". Frontiers in Microbiology. 9: 2037. doi:10.3389/fmicb.2018.02037. ISSN 1664-302X. PMC 6129597. PMID 30233523.
  31. ↑ Kariithi, Henry M; Meki, Irene K; Boucias, Drion G; Abd-Alla, Adly MM (1 August 2017). "Hytrosaviruses: current status and perspective". Current Opinion in Insect Science. 22: 71–78. doi:10.1016/j.cois.2017.05.009. ISSN 2214-5745. PMID 28805642.
  32. ↑ aka Alcelaphine herpesvirus, likely misspelled as Acephaline herpesvirus or Acelaphine herpesvirus
  33. ↑ Abd-Alla, Adly M. M.; Kariithi, Henry M.; Cousserans, François; Parker, Nicolas J.; İnce, İkbal Agah; Scully, Erin D.; Boeren, Sjef; Geib, Scott M.; Mekonnen, Solomon; Vlak, Just M.; Parker, Andrew G.; Vreysen, Marc J. B.; Bergoin, Max (2016). "Comprehensive annotation of Glossina pallidipes salivary gland hypertrophy virus from Ethiopian tsetse flies: a proteogenomics approach". Journal of General Virology. 97 (4): 1010–1031. doi:10.1099/jgv.0.000409. PMC 4854362. PMID 26801744.
  34. ↑ Abd-Alla, Adly M. M.; Cousserans, François; Parker, Andrew G.; Jehle, Johannes A.; Parker, Nicolas J.; Vlak, Just M.; Robinson, Alan S.; Bergoin, Max (2008). "Genome analysis of a Glossina pallidipes salivary gland hypertrophy virus reveals a novel, large, double-stranded circular DNA virus". Journal of Virology. 82 (9): 4595–4611. doi:10.1128/JVI.02588-07. ISSN 1098-5514. PMC 2293021. PMID 18272583.
  35. ↑ Jehle, Johannes A.; Abd-Alla, Adly M. M.; Wang, Yongjie (2013). "Phylogeny and evolution of Hytrosaviridae". Journal of Invertebrate Pathology. 112 Suppl: S62–67. doi:10.1016/j.jip.2012.07.015. ISSN 1096-0805. PMID 22841640.
  36. ↑ Abd-Alla, Adly M. M.; Kariithi, Henry M.; Cousserans, François; Parker, Nicolas J.; İnce, İkbal Agah; Scully, Erin D.; Boeren, Sjef; Geib, Scott M.; Mekonnen, Solomon; Vlak, Just M.; Parker, Andrew G.; Vreysen, Marc J. B.; Bergoin, Max (2016). "Comprehensive annotation of Glossina pallidipes salivary gland hypertrophy virus from Ethiopian tsetse flies: a proteogenomics approach". Journal of General Virology. 97 (4): 1010–1031. doi:10.1099/jgv.0.000409. PMC 4854362. PMID 26801744.
  37. ↑ Abd-Alla, Adly M. M.; Kariithi, Henry M.; Parker, Andrew G.; Robinson, Alan S.; Kiflom, Musie; Bergoin, Max; Vreysen, Marc J. B. (1 June 2010). "Dynamics of the salivary gland hypertrophy virus in laboratory colonies of Glossina pallidipes (Diptera: Glossinidae)". Virus Research. 150 (1): 103–110. doi:10.1016/j.virusres.2010.03.001. ISSN 0168-1702. PMID 20214934.
  38. ↑ Abd-Alla, Adly; Bossin, Hervé; Cousserans, François; Parker, Andrew; Bergoin, Max; Robinson, Alan (2007). "Development of a non-destructive PCR method for detection of the salivary gland hypertrophy virus (SGHV) in tsetse flies". Journal of Virological Methods. 139 (2): 143–149. doi:10.1016/j.jviromet.2006.09.018. ISSN 0166-0934. PMID 17070938.
  39. ↑ Abd-Alla, Adly M. M.; Kariithi, Henry M.; Mohamed, Abdul Hasim; Lapiz, Edgardo; Parker, Andrew G.; Vreysen, Marc J. B. (2013). "Managing hytrosavirus infections in Glossina pallidipes colonies: feeding regime affects the prevalence of salivary gland hypertrophy syndrome". PLOS ONE. 8 (5): e61875. Bibcode:2013PLoSO...861875A. doi:10.1371/journal.pone.0061875. ISSN 1932-6203. PMC 3646844. PMID 23667448.
  40. ↑ Abd-Alla, Adly M.M.; Adun, Henry; Parker, Andrew G.; Vreysen, Marc J.B.; Bergoin, Max (5 June 2012). "The Antiviral Drug Valacyclovir Successfully Suppresses Salivary Gland Hypertrophy Virus (SGHV) in Laboratory Colonies of Glossina pallidipes". PLOS ONE. 7 (6): e38417. Bibcode:2012PLoSO...738417A. doi:10.1371/journal.pone.0038417. ISSN 1932-6203. PMC 3367962. PMID 22679503.
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