Virology, Epidemiology and Pathology of Glossina Hytrosavirus, and Its Control Prospects in Laboratory Colonies of the Tsetse Fly, Glossina pallidipes (Diptera; Glossinidae)
The Glossina hytrosavirus (family Hytrosaviridae) is a double-stranded DNA virus with rod-shaped, enveloped virions. Its 190 kbp genome encodes 160 putative open reading frames. The virus replicates in the nucleus, and acquires a fragile envelope in the cell cytoplasm. Glossina hytrosavirus was first isolated from hypertrophied salivary glands of the tsetse fly, Glossina pallidipes Austen (Diptera; Glossinidae) collected in Kenya in 1986. A certain proportion of laboratory G. pallidipes flies infected by Glossina hytrosavirus develop hypertrophied salivary glands and midgut epithelial cells, gonadal anomalies and distorted sex-ratios associated with reduced insemination rates, fecundity and lifespan. These symptoms are rare in wild tsetse populations. In East Africa, G. pallidipes is one of the most important vectors of African trypanosomosis, a debilitating zoonotic disease that afflicts 37 sub-Saharan African countries. There is a large arsenal of control tactics available to manage tsetse flies and the disease they transmit. The sterile insect technique (SIT) is a robust control tactic that has shown to be effective in eradicating tsetse populations when integrated with other control tactics in an area-wide integrated approach. The SIT requires production of sterile male flies in large production facilities. To supply sufficient numbers of sterile males for the SIT component against G. pallidipes, strategies have to be developed that enable the management of the Glossina hytrosavirus in the colonies. This review provides a historic chronology of the emergence and biogeography of Glossina hytrosavirus, and includes researches on the infectomics (defined here as the functional and structural genomics and proteomics) and pathobiology of the virus. Standard operation procedures for viral management in tsetse mass-rearing facilities are proposed and a future outlook is sketched.
References
[1]
Gooding, R.H.; Krafsur, E.S. Tsetse genetics: Contributions to biology, systematics, and control of tsetse flies. Annu. Rev. Entomol. 2005, 50, 101–123, doi:10.1146/annurev.ento.50.071803.130443.
[2]
Mattioli, R.C.; Feldmann, U.; Hendrickx, G.; Wint, W.; Jannin, J.; Slingenbergh, J. Tsetse and trypanosomiasis intervention policies supporting sustainable animal-agricultural development. J. Food Agric. Environ. 2004, 2, 310–314.
[3]
Mamoudou, A.; Zoli, A.; Hamadama, H.; Abah, S.; Geerts, S.; Clausen, P.H.; Zessin, K.H.; Kyule, M.; van den Bossche, P. Seasonal distribution and abundance of tsetse flies (Glossina spp.) in the Faro and Deo Division of the Adamaoua Plateau in Cameroon. Med. Vet. Entomol. 2008, 22, 32–36, doi:10.1111/j.1365-2915.2008.00711.x.
[4]
Smith, D.H.; Pepin, J.; Stich, A.H. Human African trypanosomiasis: An emerging public health crisis. Br. Med. Bull. 1998, 54, 341–355, doi:10.1093/oxfordjournals.bmb.a011692.
[5]
Cockerell, T.D.A. A fossil tsetse-fly in Colorado. Nature 1907, 76, 414, doi:10.1038/076414b0.
[6]
Elsen, P.; Amoudi, M.A.; Leclercq, M. First record of Glossina fuscipes fuscipes Newstead, 1910 and Glossina morsitans submorsitans Newstead, 1910 in southwestern Saudi Arabia. Ann. Soc. Bel. Med. Trop. 1990, 70, 281–287.
[7]
Hotez, P.J.; Kamath, A. Neglected tropical diseases in sub-saharan Africa: Review of their prevalence, distribution, and disease burden. PLoS Negl. Trop. Dis. 2009, 3, e412, doi:10.1371/journal.pntd.0000412.
[8]
Hotez, P.J.; Molyneux, D.H.; Fenwick, A.; Kumaresan, J.; Sachs, S.E.; Sachs, J.D.; Savioli, L. Control of neglected tropical diseases. N. Engl. J. Med. 2007, 357, 1018–1027, doi:10.1056/NEJMra064142.
[9]
Cecchi, G.; Mattioli, R.C.; Slingenbergh, J.; de la Rocque, S. Land cover and tsetse fly distributions in sub-Saharan Africa. Med. Vet. Entomol. 2008, 22, 364–373, doi:10.1111/j.1365-2915.2008.00747.x.
[10]
Vreysen, M.J.B. Prospects for area-wide integrated control of tsetse flies (Diptera: Glossinidae) and trypanosomosis in sub-Saharan Africa. Rev. Soc. Entomol. Argent 2006, 65, 1–21.
[11]
Otte, M.J.; Chilonda, P. Classification of cattle and small ruminant production systems in sub-Saharan Africa. Outlook Agr. 2003, 32, 183–190, doi:10.5367/000000003101294451.
[12]
Budd, L.T. DFID-funded Tsetse and Trypanosomosis Research and Development Since 1980; Department of International Development: Aylesford, UK, 1999; Volume 2.
[13]
Matovu, E.; Seebeck, T.; Enyaru, J.C.K.; Kaminsky, R. Drug resistance in Trypanosoma brucei spp., the causative agents of sleeping sickness in man and nagana in cattle. Microb. Infect. 2001, 3, 763–770, doi:10.1016/S1286-4579(01)01432-0.
[14]
Oberholzer, M.; Lopez, M.A.; McLelland, B.T.; Hill, K.L. Social motility in african trypanosomes. PLoS Pathog. 2010, 6, e1000739.
[15]
Vickerman, K. Developmental cycles and biology of pathogenic trypanosomes. Br. Med. Bull. 1985, 41, 105–114.
[16]
Brun, R.; Blum, J.; Chappuis, F.; Burri, C. Human African trypanosomiasis. Lancet 2010, 375, 148–159, doi:10.1016/S0140-6736(09)60829-1.
[17]
Chappuis, F.; Loutan, L.; Simarro, P.; Lejon, V.; Büscher, P. Options for field diagnosis of human african trypanosomiasis. Clin. Microbiol. Rev. 2005, 18, 133–146, doi:10.1128/CMR.18.1.133-146.2005.
[18]
Friedheim, E.A.H. Mel B in the treatment of human trypanosomiasis. Am. J. Trop. Med. Hyg. 1949, 29, 173–180.
[19]
Burri, C.; Nkunku, S.; Merolle, A.; Smith, T.; Blum, J.; Brun, R. Efficacy of new, concise schedule for melarsoprol in treatment of sleeping sickness caused by Trypanosoma brucei gambiense: A randomised trial. Lancet 2000, 355, 1419–1425, doi:10.1016/S0140-6736(00)02141-3.
[20]
Burri, C. Chemotherapy against human African trypanosomiasis: Is there a road to success? Parasitology 2010, 137, 1987–1994, doi:10.1017/S0031182010001137.
[21]
Barrett, M.P.; Vincent, I.M.; Burchmore, R.J.; Kazibwe, A.J.; Matovu, E. Drug resistance in human African trypanosomiasis. Future Microbiol. 2011, 6, 1037–1047, doi:10.2217/fmb.11.88.
[22]
Geerts, S.; Holmes, P.H. Drug Management and Parasite Resistance in Bovine Trypanosomiasis in Africa; FAO: Rome, Italy, 1998.
[23]
Schofield, C.J.; Kabayo, J.P. Trypanosomiasis vector control in Africa and Latin America. Parasit Vectors 2008, 1, 24, doi:10.1186/1756-3305-1-24.
[24]
Vreysen, M.J.B.; Seck, M.T.; Sall, B.; Bouyer, J. Tsetse flies: Their biology and control using area-wide integrated pest management approaches. J. Invertebr. Pathol. 2013, 112, S15–S25, doi:10.1016/j.jip.2012.07.026.
[25]
Abd-Alla, A.; Cousserans, F.; Parker, A.; Parker, N.; Robinson, A.; Bergoin, M. Characterization of a Novel virus from the Mass-reared Tsetse Fly Glossina pallidipes. In Proceedings of 11th meeting of the Working Group Arthropod Mass Rearing and Quality Control, Montreal, Canada, 28 October–1 November 2007; pp. 1–4.
[26]
Abd-Alla, A.M.M.; Cousserans, F.; Parker, A.G.; Jehle, J.A.; Parker, N.J.; Vlak, J.M.; Robinson, A.S.; Bergoin, M. Genome analysis of a Glossina pallidipes salivary gland hypertrophy virus reveals a novel large double-stranded circular DNA virus. J. Virol. 2008, 82, 4595–4611, doi:10.1128/JVI.02588-07.
[27]
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. Hytrosavirus Study Group of the ICTV Hytrosaviridae: A proposal for classification and nomenclature of a new insect virus family. Arch. Virol. 2009, 154, 909–918, doi:10.1007/s00705-009-0398-5.
[28]
Abd-Alla, A.; Bossin, H.; Cousserans, F.; Parker, A.; Bergoin, M.; Robinson, A. Development of a non-destructive PCR method for detection of the salivary gland hypertrophy virus (SGHV) in tsetse flies. J. Virol. Methods 2007, 139, 143–149, doi:10.1016/j.jviromet.2006.09.018.
[29]
Leak, S.G.A. Tsetse Biology and Ecology: Their Role in the Epidemiology and Control of Trypanosomosis; CABI Publishing: Wallingford, CT, USA, 1998.
[30]
Matthews, E.G.; Clyne, D.; Kitching, R.L. Insect Ecology, 2nd ed.; University of Queensland Press: St. Lucia, Qld, Australia, 1984; Volume 6.
[31]
Dujardin, J.-P.; Schofield, C.J. Triatominae: Systematics, morphology and population biology. In The Trypanosomiases; Maudlin, I., Holmes, P.H., Miles, M.A., Eds.; CABI Publishing: Wallingford, CT, USA, 2004; pp. 181–201.
[32]
Allsopp, R. Options for vector control against trypanonomiasis in Africa. Trends Parasitol. 2001, 17, 15–19, doi:10.1016/S1471-4922(00)01828-6.
[33]
Brightwell, B.; Dransfield, R. Odour attractants for tsetse: Glossina austeni, G. brevipalpis and G. swynnertoni. Med. Vet. Entomol. 1997, 11, 297–299, doi:10.1111/j.1365-2915.1997.tb00410.x.
[34]
Thomson, J.W.; Wilson, A. The Control of Tsetse Flies and Trypanosomiasis by the Application of Deltamethrin to Cattle. In proceedings of the 20th Meeting of the International Scientific Coubcil for the Trypanosomiasis Research and Control (ISCTRC), Mombasa, Kenya, 10–14 April 1989; pp. 450–454.
[35]
Brightwell, B.; Dransfield, R.D.; Stevenson, P.; Williams, B. Changes over twelve years in populations of Glossina pallidipes and Glossina longipennis (Diptera: Glossinidae) subject to varying trapping pressure at Nguruman, sourth-west Kenya. Bull. Entomol. Res. 1997, 87, 349–370, doi:10.1017/S0007485300037378.
[36]
Knipling, E.F. Possibilities of insect control or eradication through the use of sexually sterile males. J. Econ. Entomol. 1955, 48, 459–469.
[37]
Knipling, E.F. Sterile-male method of population control. Science 1959, 130, 902–904.
[38]
Robinson, A.S. Mutations and their use in insect control. Mutat. Res. 2002, 511, 113–132, doi:10.1016/S1383-5742(02)00006-6.
[39]
Robinson, A.S. Genetic Basis of the Sterile Insect Technique. In Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management; Dyck, V.A., Hendrichs, J., Robinson, A.S., Eds.; Springer: Dordrecht, The Netherlands, 2005; pp. 95–114.
[40]
Abila, P.P.; Kiendrebeogo, M.; Mutika, G.N.; Parker, A.G.; Robinson, A.S. The effect of age on the mating competitiveness of male Glossina fuscipes fuscipes and G. palpalis palpalis. J. Insect Sci. 2003, 3, 13.
[41]
Enkerlin, W.R. Impact of Fruit Fly Control Programmes Using the Sterile Insect Technique. In Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management; Dyck, V.A., Hendrichs, J., Robinson, A.S., Eds.; Springer: Dordrecht, The Netherlands, 2005; pp. 651–676.
[42]
Franz, G. Genetic Sexing Strains in Mediterranean Fruit Fly, An Example for Other Species Amenable to Large-scale Rearing as Required for the Sterile Insect Technique. In Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management; Dyck, V.A., Hendrichs, J., Robinson, A.S., Eds.; Springer: Dordrecht, The Netherlands, 2005; pp. 427–451.
[43]
Dyck, V.A.; Graham, S.H.; Bloem, K.A. Implementation of the Sterile Insect Release Programme to Eradicate the Codling Moth, Cydia pomonella (L.) (Lepidoptera: Olethreutidae), in British Columbia, Canada. In Proceedings of Management of Insect Pests: Nuclear and Related Molecular and Genetic Techniques, Vienna, Austria, 19–23 October 1992; pp. 285–297.
[44]
Carpenter, J.; Bloem, S.; Hofmeyr, H. Area-wide Control Tactics for the False Codling Moth Thaumatotibia leucotreta in South Africa: A Potential Invasive Species. In Area-wide Control of Insect Pests: From Research to Field Implementation, 1st; Vreysen, M.J.B., Robinson, A.S., Hendrichs, J., Eds.; Springer: Dordrecht, The Netherlands, 2007; pp. 351–359.
[45]
Daly, J.M.; Barrington, A.M.; Hackett, J.K.; Suckling, D.M. Sterilisation of painted apple moth Teia anartoides (Lepidoptera: Lymantridae) by irradiation. N. Z. Plant Prot. 2002, 55, 7–11.
[46]
Koyama, J.; Kakinohana, H.; Miyatake, T. Eradication of the melon fly, Bactrocera cucurbitae, in Japan: Importance of behaviour, ecology, genetics and evolution. Ann. Rev. Entomol. 2004, 49, 331–349, doi:10.1146/annurev.ento.49.061802.123224.
[47]
Vreysen, M.J.; 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. Glossina austeni (Diptera: Glossinidae) eradicated on the island of Unguja, Zanzibar, using the sterile insect technique. J. Econ. Entomol. 2000, 93, 123–135, doi:10.1603/0022-0493-93.1.123.
[48]
Vreysen, M.J.; Saleh, K.M.; Lancelot, R.; Bouyer, J. Factory tsetse flies must behave like wild flies: A prerequisite for the sterile insect technique. PLoS Negl. Trop. Dis. 2011, 5, e907, doi:10.1371/journal.pntd.0000907.
[49]
Politzar, H.; Merot, P.; Brandl, F.E. Experimental aerial release of sterile males of Glossina palpalis gambiensis and Glossina tachinoides in a biological control operation. Rev. élev. Méd. Vét. Pays Trop. 1984, 37, 198–202.
[50]
Olandunmade, M.A.; Feldmann, U.; Takken, W.; Tanabe, S.O.; Hamann, H.J.; Onah, J.; Dengwat, L.; Vloedt, A.M.V.V.D.; Gingrich, R.E. Eradication of Glossina palpalis palpalis (Robineau-Desvoidy) (Diptera: Glossinidae) from agropastoral land in central Nigeria by means of the sterile insect technique. In Proceedings of the final research co-ordination meeting, Vom, Plateau State, Nigeria, 6–10 June 1988; pp. 5–23.
[51]
Alemu, T.; Kapitano, B.; Mekonnen, S.; Aboset, G.; Kiflom, M.; Bancha, B.; Woldeyes, G.; Bekele, K.; Feldmann, U. Area-wide Control of Tsetse and Trypanosomosis: Ethiopian Experience in the Southern Rift Valley. In Area-Wide Control of Insect Pests: From Research to Field Implementation; Vreysen, M.J.B., Robinson, A.S., Hendrichs, J., Eds.; Springer: Dordrecht, The Netherlands, 2007; pp. 325–335.
[52]
Abd-Alla, A.M.M.; Kariithi, H.M.; Parker, A.G.; Robinson, A.S.; Kiflom, M.; Bergoin, M.; Vreysen, M.J.B. Dynamics of the salivary gland hypertrophy virus in laboratory colonies of Glossina pallidipes (Diptera: Glossinidae). Virus Res. 2010, 150, 103–110, doi:10.1016/j.virusres.2010.03.001.
[53]
Abd-Alla, A.M.M.; Parker, A.G.; Vreysen, M.J.B.; Bergoin, M. Tsetse salivary gland hypertrophy virus: Hope or hindrance for tsetse control? PLoS Negl. Trop. Dis. 2011, 5, e1220, doi:10.1371/journal.pntd.0001220.
[54]
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.; et al. 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. 2013, 112, S123–S132, doi:10.1016/j.jip.2012.04.016.
[55]
Whitnall, A.B.M. The trypanosome infections of Glossina pallidipes in the Umfolosi Game Reserve, Zululand. Onderstepoort J. Vet. Sci. Anim. Ind. 1934, 2, 2–21.
[56]
Whitnall, A.B.M. The trypanosome infections of Glossina pallidipes in the Umfolosi Game Reserve, Zululand(Preliminary Report). In 18th Report of the Director of Veterinary Services and Animal Industry; Union of South Africa: Onderstepoort, South Africa, 1932; pp. 7–21.
[57]
Burtt, E. Hypertrophied salivary glands in Glossina: Evidence that G. pallidipes with this abnormality is particularly suited to trypanosome infection. Ann. Trop. Med. Parasitol. 1945, 39, 11–13.
[58]
Jenni, L. Virus like particles in a strain of G. morsitans centralis, Machado 1970. Trans. R. Soc. Trop. Med. Hyg. 1973, 67, 295, doi:10.1016/0035-9203(73)90220-4.
[59]
Jenni, L.; Steiger, R.F. Virus like particles in the tsetse fly, Glossina morsitans sspp. Preliminary results. Rev. Suisse Zool. 1974, 81, 663–666.
[60]
Jenni, L.; Steiger, R. Virus like particles of Glossina fuscipes fuscipes Newst. 1910. Acta Trop. 1974, 31, 177–180.
[61]
Jenni, L.; B?hringer, S. Nuclear coat and virus like particles in the midgut epithelium of Glossina morsitans sspp. Acta Trop. 1976, 33, 380–389.
[62]
Lyon, J.P. La mouche des Narcisses (Merodon equestris F., Diptere Syrphidae). I. Identification de l'insecte et de ses degats et biologie dans le sud-est de la France. Rev. Zool. Agr. Pathol. Veg. 1973, 72, 65–92.
[63]
Jaenson, T.G.T. Virus-like rods associated with salivary gland hyperplasia in tsetse, Glossina pallidipes. Trans. R. Soc. Trop. Med. Hyg. 1978, 72, 234–238, doi:10.1016/0035-9203(78)90200-6.
[64]
Amargier, A.; Lyon, J.P.; Vago, C.; Meynadier, G.; Veyrunes, J.C. Mise en evidence et purification d'un virus dans la proliferation monstrueuse glandulaire d'insectes. Etude sur Merodon equestris F. (Diptere: Syrphidae). C. R. Acad. Sci. D 1979, 289, 481–484.
[65]
Otieno, L.H.; Kokwaro, E.D.; Chimtawi, M.; Onyango, P. Prevalence of enlarged salivary glands in wild populations of Glossina pallidipes in Kenya, with a note on the ultrastructure of the affected organ. J. Invertebr. Pathol. 1980, 36, 113–118, doi:10.1016/0022-2011(80)90142-1.
[66]
Opiyo, E.A.; Okumu, I. The KETRI Glossina pallidipes Colony: Further Observations. In Diseases of the Tropics; Tukei, P.M., Njogu, A.R., Eds.; Africa Book Services: Nairobi, Kenya, 1983; pp. 52–54.
[67]
Odindo, M.O.; Sabwa, D.M.; Amutalla, P.A.; Otieno, W.A. Preliminary tests on the transmission of virus-like particles to the tsetse Glossina pallidipes. Insect Sci. Appl. 1981, 2, 219–221.
[68]
Odindo, M.O. Incidence of salivary gland hypertrophy in field populations of the tsetse Glossina pallidipes on the South Kenya coast. Insect Sci. Appl. 1982, 3, 59–64.
[69]
Odindo, M.O.; Payne, C.C.; Crook, N.E.; Jarret, P. Properties of a novel DNA virus from the tsetse fly, Glossina pallidipes. J. Gen. Virol. 1986, 67, 527–536, doi:10.1099/0022-1317-67-3-527.
[70]
Odindo, M.O.; Amutalla, P.A. Distribution pattern of the virus of Glossina pallidipes Austen in a forest ecosystem. Insect Sci. Appl. 1986, 7, 79–84.
[71]
Jaenson, T.G.T. Sex ratio distortion and reduced lifespan of Glossina pallidipes infected with the virus causing salivary gland hyperplasia. Entomol. Exp. Appl. 1986, 41, 256–271.
[72]
Ellis, D.S.; Maudlin, I. Salivary gland hyperplasia in wild caught tsetse from Zimbabwe. Entomol. Exp. Appl. 1987, 45, 167–173, doi:10.1111/j.1570-7458.1987.tb01077.x.
[73]
Gouteux, J.P. Prevalence of enlarged salivary glands in Glossina palpalis, G. pallicera, and G. nigrofusca (Diptera: Glossinidae) from the Vavoua area, Ivory Coast. J. Med. Entomol. 1987, 24, 268.
[74]
Odindo, M.O. Glossina pallidipes virus: Its potential for use in biological control of tsetse. Insect Sci. Appl. 1988, 9, 399–403.
[75]
Jura, W.G.Z.O.; Odhiambo, T.R.; Otieno, L.H.; Tabu, N.O. Gonadal lesions in virus-infected male and female tsetse, Glossina pallidipes (Diptera: Glossinidae). J. Invertebr. Pathol. 1988, 52, 1–8, doi:10.1016/0022-2011(88)90095-X.
[76]
Jura, W.G.Z.O.; Zdarek, J.; Otieno, L.H. A simple method for artificial infection of tsetse, Glossina morsitans morsitans larvae with the DNA virus of G. pallidipes. Int. J. Trop. Insect Sci. 1993, 14, 383–387, doi:10.1017/S1742758400014909.
[77]
Jura, W.G.Z.O.; Davies-Cole, J.O.A. Some aspects of mating behavior of Glossina morsitans morsitans males infected with a DNA virus. Biol. Control 1992, 2, 188–192, doi:10.1016/1049-9644(92)90058-L.
[78]
Jura, W.; Otieno, L.; Chimtawi, M. Ultrastructural evidence for trans-ovum transmission of the DNA virus of tsetse, Glossina pallidipes (Diptera: Glossinidae). Curr. Microbiol. 1989, 18, 1–4, doi:10.1007/BF01568821.
[79]
Kokwaro, E.D.; Nyindo, M.; Chimtawi, M. Ultrastructural changes in salivary glands of tsetse, Glossina morsitans morsitans, infected with virus and rickettsia-like organisms. J. Invertebr. Pathol. 1990, 56, 337–346, doi:10.1016/0022-2011(90)90120-U.
[80]
Kokwaro, E.D.; Otieno, L.H.; Chimtawi, M. Salivary glands of the tsetse Glossina pallidipes Austen infected with Trypanosoma brucei and virus particles: Ultrastructural study. Int. J. Trop. Insect Sci. 1991, 12, 661–669.
[81]
Shaw, M.K.; Moloo, S.K. Virus-like particles in Rickettsia within the midgut epithelial cells of Glossina morsitans centralis and Glossina brevipalpis. J. Invertebr. Pathol. 1993, 61, 162–166, doi:10.1006/jipa.1993.1029.
[82]
Coler, R.R.; Boucias, D.G.; Frank, J.H.; Maruniak, J.E.; Garcia-Canedo, A.; Pendland, J.C. Characterization and description of a virus causing salivary gland hyperplasia in the housefly, Musca domestica. Med. Vet. Entomol. 1993, 7, 275–282, doi:10.1111/j.1365-2915.1993.tb00688.x.
[83]
Sang, R.C.; Jura, W.G.Z.O.; Otieno, L.H.; Ogaja, P. Ultrastructural changes in the milk gland of tsetse Glossina morsitans centralis (Diptera; Glissinidae) female infected by a DNA virus. J. Invertebr. Pathol. 1996, 68, 253–259, doi:10.1006/jipa.1996.0093.
[84]
Sang, R.C.; Jura, W.G.Z.O.; Otieno, L.H.; Tukei, P.M.; Mwangi, R.W. Effects of tsetse DNA virus infection on the survival of a host fly Glossina morsitans centralis (Diptera: Glossinidae). J. Invertebr. Pathol. 1997, 69, 253–260, doi:10.1006/jipa.1996.4629.
[85]
Sang, R.C.; Jura, W.G.Z.O.; Otieno, L.H.; Mwangi, R.W. 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. 1998, 93, 861–864, doi:10.1590/S0074-02761998000600030.
[86]
Sang, R.C.; Jura, W.G.Z.O.; Otieno, L.H.; Mwangi, R.W.; Ogaja, P. 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. 1999, 38, 349–354.
[87]
Kokwaro, E.D. Virus particles in male accessory reproductive glands of tsetse, Glossina morsitans morsitans (Diptera: Glossinidae) and associated tissue changes. Int. J. Trop. Insect Sci. 2006, 26, 266–272, doi:10.1017/S1742758406668458.
[88]
Salem, T.Z.; Garcia-Maruniak, A.; Lietze, V.U.; Maruniak, J.E.; Boucias, D.G. Analysis of transcripts from predicted open reading frames of Musca domestica salivary gland hypertrophy virus. J. Gen. Virol. 2009, 90, 1270–1280, doi:10.1099/vir.0.009613-0.
[89]
Kariithi, H.M.; van Lent, J.W.; Boeren, S.; Abd-Alla, A.M.; Ince, I.A.; van Oers, M.M.; Vlak, J.M. Correlation between structure, protein composition, morphogenesis and cytopathology of Glossina pallidipes salivary gland hypertrophy virus. J Gen. Virol. 2013, 94, 193–208, doi:10.1099/vir.0.047423-0.
[90]
Kariithi, H.M.; Ince, I.A.; Boeren, S.; Vervoort, J.; Bergoin, M.; van Oers, M.M.; Abd-Alla, A.M.M.; Vlak, J.M. Proteomic analysis of Glossina pallidipes salivary gland hypertrophy virus virions for immune intervention in tsetse fly colonies. J. Gen. Virol. 2010, 91, 3065–3074, doi:10.1099/vir.0.023671-0.
Luo, L.; Zeng, L. A new rod-shaped virus from parasitic wasp Diachasmimorpha longicaudata (Hymenoptera: Braconidae). J. Invertebr. Pathol. 2010, 103, 165–169, doi:10.1016/j.jip.2009.08.008.
[93]
Boucias, D.G.; Kariithi, H.M.; Bourtzis, K.; Schneider, D.I.; Kelley, K.; Miller, W.J.; Parker, A.G.; Abd-Alla, A.M.M. Trans-generational transmission of the Glossina pallidipes hytrosavirus depends on the presence of a functional symbiome. PLoS One 2013, 8, e61150.
[94]
Abd-Alla, A.M.M.; Kariithi, H.M.; Mohamed, A.H.; Lapiz, E.; Parker, A.G.; Vreysen, M.J.B. Managing hytrosavirus infections in Glossina pallidipes colonies: Feeding regime affects the prevalence of salivary gland hypertrophy syndrome. PLoS One 2013, 8, e61875.
[95]
Howatson, A.; Whitmore, G. The development and structure of vesicular stomatitis virus. Virology 1962, 16, 466–478, doi:10.1016/0042-6822(62)90228-3.
[96]
Mussgay, M.; Weibel, J. Electron microscopic studies on the development oof vesicular stomatis virus in KB cells. J. Cell Biol. 1963, 16, 119–129, doi:10.1083/jcb.16.1.119.
Janzen, H.G.; Rhodes, A.J.; Doane, F.W. Chikungunya virus in salivary glands of Aedes aegypti (L.): An electron microscope study. Can. J. Microbiol. 1970, 16, 581–586, doi:10.1139/m70-097.
[99]
Lamotte, L.C., Jr. Japanese B encephalitis virus in the organs of infected mosquitoes. Am. J. Epidemiol. 1960, 72, 73–87.
[100]
Mims, C.A.; Day, M.F.; Marshall, I.D. Cytopathic effect of Semliki Forest virus in the mosquito, Aedes aegypti. Am. J. Trop. Med. Hyg. 1966, 15, 775–784.
[101]
Longdon, B.; Wilfert, L.; Obbard, D.J.; Jiggins, F.M. Rhabdoviruses in two species of Drosophila: Vertical transmission and a recent sweep. Genetics 2011, 188, 141–150, doi:10.1534/genetics.111.127696.
[102]
L'Heritier, P.H. The Hereditary virus of Drosophila. In Advances in Virus Research; Kenneth, M.S., Lauffer, M.A., Eds.; Academic Press Inc.: New York, NY, USA, 1958; Volume 5, pp. 195–245.
[103]
Anderson, R.M.; May, R.M. Infectious diseases and population cycles of forest insects. Science 1980, 210, 658–661.
[104]
Geden, C.J.; Lietze, V.U.; Boucias, D.G. Seasonal prevalence and transmission of salivary gland hypertrophy virus of house flies (Diptera: Muscidae). J. Med. Entomol. 2008, 45, 42–51, doi:10.1603/0022-2585(2008)45[42:SPATOS]2.0.CO;2.
[105]
Lietze, V.U.; Geden, C.J.; Blackburn, P.; Boucias, D.G. Effects of salivary gland hypertrophy virus on the reproductive behavior of the housefly, Musca domestica. Appl. Environ. Microbiol. 2007, 73, 6811–6818, doi:10.1128/AEM.02694-06.
[106]
Geden, C.; Garcia-Maruniak, A.; Lietze, V.U.; Maruniak, J.; Boucias, D.G. Impact of house fly salivary gland hypertrophy virus (MdSGHV) on a heterologous host, Stomoxys calcitrans. J. Med. Entomol. 2011, 48, 1128–1135, doi:10.1603/ME11021.
[107]
Chou, M.-Y.; Haymer, D.S.; Feng, H.-Y.; Mau, R.F.L.; Hsu, J.-C. Potential for insecticide resistance in populations of Bactrocera dorsalis in Hawaii: Spinosad susceptibility and molecular characterization of a gene associated with organophosphate resistance. Entomol. Exp. Appl. 2010, 134, 296–303.
[108]
Lawrence, P.O.; Akin, D. Virus-like particles from the poison glands of the parasitic wasp Biosteres longicaudatus (Hymenoptera: Braconidae). Can. J. Zool. 1990, 68, 539–546, doi:10.1139/z90-079.
[109]
Lawrence, P.O. Morphogenesis and cytopathic effects of the Diachasmimorpha longicaudata entomopoxvirus in host haemocytes. J. Insect Physiol. 2005, 51, 221–233, doi:10.1016/j.jinsphys.2004.12.003.
[110]
Abd-Alla, A.; Cousserans, F.; Parker, A.; Bergoin, M.; Chiraz, J.; Robinson, A. Quantitative PCR analysis of the salivary gland hypertrophy virus (GpSGHV) in a laboratory colony of Glossina pallidipes. Virus Res. 2009, 139, 48–53, doi:10.1016/j.virusres.2008.10.006.
[111]
Lietze, V.-U.; Abd-Alla, A.; Vreysen, M.; Geden, C.C.; Boucias, D.G. Salivary gland hypertrophy viruses: A novel group of insect pathogenic viruses. Annu. Rev. Entomol. 2011, 56, 63–80, doi:10.1146/annurev-ento-120709-144841.
[112]
Duron, O.; Bouchon, D.; Boutin, S.; Bellamy, L.; Zhou, L.; Engelstadter, J.; Hurst, G.D. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol. 2008, 6, 27, doi:10.1186/1741-7007-6-27.
[113]
Engelstadter, J.; Hurst, G.D.D. The ecology and evolution of microbes that manipulate host reproduction. Annu. Rev. Ecol. Evol. Syst. 2009, 40, 127–149, doi:10.1146/annurev.ecolsys.110308.120206.
[114]
Hilgenboecker, K.; Hammerstein, P.; Schlattmann, P.; Telschow, A.; Werren, J.H. How many species are infected with Wolbachia?—A statistical analysis of current data. FEMS Microbiol. Lett. 2008, 281, 215–220, doi:10.1111/j.1574-6968.2008.01110.x.
[115]
Doudoumis, V.; Tsiamis, G.; Wamwiri, F.; Brelsfoard, C.; Alam, U.; Aksoy, E.; Dalaperas, S.; bd-Alla, A.; Ouma, J.; Takac, P.; et al. Detection and characterization of Wolbachia infections in laboratory and natural populations of different species of tsetse flies (genus Glossina). BMC Microbiol. 2012, 12, S3, doi:10.1186/1471-2180-12-S1-S3.
[116]
Alam, U.; Hyseni, C.; Symula, R.E.; Brelsfoard, C.; Wu, Y.; Kruglov, O.; Wang, J.; Echodu, R.; Alioni, V.; Okedi, L.M.; et al. Implications of microfauna-host interactions for trypanosome transmission dynamics in Glossina fuscipes fuscipes in Uganda. Appl. Environ. Microbiol. 2012, 78, 4627–4637, doi:10.1128/AEM.00806-12.
Moreira, L.A.; Iturbe-Ormaetxe, I.; Jeffery, J.A.; Lu, G.; Pyke, A.T.; Hedges, L.M.; Rocha, B.C.; Hall-Mendelin, S.; Day, A.; Riegler, M.; et al. A Wolbachia symbiont in Aedes aegypti limits infection with Dengue, Chikungunya, and Plasmodium. Cell 2009, 139, 1268–1278, doi:10.1016/j.cell.2009.11.042.
[119]
Song, J.; Wang, R.; Deng, F.; Wang, H.; Hu, Z. Functional studies of per os infectivity factors of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus. J. Gen. Virol. 2008, 89, 2331–2338, doi:10.1099/vir.0.2008/002352-0.
[120]
Garcia-Maruniak, A.; Maruniak, J.E.; Farmerie, W.; Boucias, D.G. Sequence analysis of a non-classified, non-occluded DNA virus that causes salivary gland hypertrophy of Musca domestica, MdSGHV. Virology 2008, 377, 184–196, doi:10.1016/j.virol.2008.04.010.
[121]
Cheng, C.H.; Liu, S.M.; Chow, T.Y.; Hsiao, Y.Y.; Wang, D.P.; Huang, J.J.; Chen, H.H. Analysis of the complete genome sequence of the Hz-1 virus suggests that it is related to members of the Baculoviridae. J. Virol. 2002, 76, 9024–9034, doi:10.1128/JVI.76.18.9024-9034.2002.
[122]
Wang, Y.; Kleespies, R.G.; Huger, A.M.; Jehle, J.A. The genome of Gryllus bimaculatus nudivirus indicates an ancient diversification of baculovirus-related nonoccluded nudiviruses of insects. J. Virol. 2007, 81, 5395–5406, doi:10.1128/JVI.02781-06.
[123]
Wang, Y.; van Oers, M.M.; Crawford, A.M.; Vlak, J.M.; Jehle, J.A. Genomic analysis of Oryctes rhinoceros virus reveals genetic relatedness to Heliothis zea virus 1. Arch. Virol. 2006, 152, 519–531.
[124]
Wang, Y.; Bininda-Emonds, O.; van Oers, M.; Vlak, J.; Jehle, J. The genome of Oryctes rhinoceros nudivirus provides novel insight into the evolution of nuclear arthropod-specific large circular double-stranded DNA viruses. Virus Genes 2011, 42, 444–456, doi:10.1007/s11262-011-0589-5.
[125]
Ohkawa, T.; Washburn, J.O.; Sitapara, R.; Sid, E.; Volkman, L.E. 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. 2005, 79, 15258–15264, doi:10.1128/JVI.79.24.15258-15264.2005.
[126]
Blissard, G.W.; Rohrmann, G.F. Baculovirus diversity and molecular biology. Ann. Rev. Entomol. 1990, 35, 127–155, doi:10.1146/annurev.en.35.010190.001015.
[127]
Tidona, C.A.; Darai, G. Iridovirus homologues of cellular genes—Implications for the molecular evolution of large DNA viruses. Virus Genes 2000, 21, 77–81, doi:10.1023/A:1008192616923.
[128]
Invertebrate Virus Subcommittee, Hytrosavirus Study Group. Available online: http://www.ictvonline.org/taxonomyHistory.asp?taxnode_id=20125369&taxa_name=Glossinavirus/ (accessed on 19 June 2013).
[129]
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.; Robinson, A.S.; et al. Two viruses that cause salivary gland hypertrophy in Glossina pallidipes and Musca domestica are related and form a distinct phylogenetic clade. J. Gen. Virol. 2009, 90, 334–346, doi:10.1099/vir.0.006783-0.
[130]
Jaenson, T.G.T. Reproductive Biology of the Tsetse Glossina pallidipes Austen (Diptera, Glossinidae) with Special Reference to Mating Behaviour; Department of entomology, University of Uppsala: Uppsala, Sweden, 1978; p. 39.
[131]
Lietze, V.U.; Sims, K.R.; Salem, T.Z.; Geden, C.J.; Boucias, D.G. Transmission of MdSGHV among adult house flies, Musca domestica (Diptera: Muscidae), occurs via oral secretions and excreta. J. Invertebr. Pathol. 2009, 101, 49–55, doi:10.1016/j.jip.2009.02.007.
[132]
Mutika, G.N.; Marin, C.; Parker, A.G.; Boucias, D.G.; Vreysen, M.J.; Abd-Alla, A.M. Impact of salivary gland hypertrophy virus infection on the mating success of male Glossina pallidipes: Consequences for the sterile insect technique. PLoS One 2012, 7, e42188.
[133]
Boucias, D.G.; Deng, F.; Hu, Z.; Garcia-Maruniak, A.; Lietze, V.U. Analysis of the structural proteins from the Musca domestica hytrosavirus with an emphasis on the major envelope protein. J. Invertebr. Pathol. 2013, 112, S44–S52, doi:10.1016/j.jip.2012.03.016.
[134]
Lietze, V.U.; Abd-Alla, A.M.M.; Boucias, D.G. Two hytrosaviruses, MdSGHV and GpSGHV, induce distinct cytopathologies in their respective host insects. J. Invertebr. Pathol. 2011, 107, 161–163, doi:10.1016/j.jip.2011.03.006.
[135]
Gao, Y.; Luo, L. Genome-based phylogeny of dsDNA viruses by a novel alignment-free method. Gene 2012, 492, 309–314, doi:10.1016/j.gene.2011.11.004.
[136]
Wu, G.A.; Jun, S.R.; Sims, G.E.; Kim, S.H. Whole-proteome phylogeny of large dsDNA virus families by an alignment-free method. Proc. Natl. Acad. Sci. USA 2009, 106, 12826–12831, doi:10.1073/pnas.0905115106.
[137]
Yu, Z.G.; Chu, K.H.; Li, C.P.; Anh, V.; Zhou, L.Q.; Wang, R.W. Whole-proteome phylogeny of large dsDNA viruses and parvoviruses through a composition vector method related to dynamical language model. BMC Evol. Biol. 2010, 10, 192.
[138]
Wang, Y.; Jehle, J.A. Nudiviruses and other large, double-stranded circular DNA viruses of invertebrates: New insights on an old topic. J. Invertebr. Pathol. 2009, 101, 187–193, doi:10.1016/j.jip.2009.03.013.
[139]
Jehle, J.A.; Abd-Alla, A.M.; Wang, Y. Phylogeny and evolution of Hytrosaviridae. J. Invertebr. Pathol. 2013, 112, S62–S67, doi:10.1016/j.jip.2012.07.015.
[140]
Lodish, H.; Berk, A.; Zipursky, S.L.; Matsudaira, P.; Baltimore, D.; Darnell, J. Mutations: Types and Causes. In Molecular Cell Biology, 4th ed.; W. H. Freeman and Company: New York, NY, USA, 2000.
[141]
Joyce, A.R.; Palsson, B.O. The model organism as a system: Integrating “omics” data sets. Nat. Rev. Mol. Cell Biol. 2006, 7, 198–210, doi:10.1038/nrm1857.
[142]
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. The salivary secretome of the tsetse fly, Glossina pallidipes (Diptera: Glossinidae) infected by salivary gland hypertrophy virus. PLoS Negl. Trop. Dis. 2011, 5, e1371, doi:10.1371/journal.pntd.0001371.
[143]
Lee, J.C.; Chen, H.H.; Chao, Y.C. Persistent baculovirus infection results from deletion of the apoptotic suppressor gene p35. J. Virol. 1998, 72, 9157–9165.
[144]
Geden, C.J.; Steenberg, T.; Lietze, V.U.; Boucias, D.G. Salivary gland hypertrophy virus of house flies in Denmark: Prevalence, host range, and comparison with a Florida isolate. J. Vector. Ecol. 2011, 36, 231–238, doi:10.1111/j.1948-7134.2011.00163.x.
[145]
Fuxa, J.R.; Weidner, E.H.; Richter, A.R. Polyhedra without virions in a vertically transmitted nuclear polyhedrosis virus. J. Invertebr. Pathol. 1992, 60, 53–58.
[146]
Hughes, D.S.; Possee, R.D.; King, L.A. Activation and detection of a latent baculovirus resembling Mamestra brassicae nuclear polyhedrosis virus in M. brassicae insects. Virology 1993, 194, 608–615, doi:10.1006/viro.1993.1300.
[147]
Hughes, D.S.; Possee, R.D.; King, L.A. Evidence for the presence of a low-level, persistent baculovirus infection of Mamestra brassicae insects. J. Gen. Virol. 1997, 78, 1801–1805.
[148]
Murillo, R.; Hussey, M.S.; Possee, R.D. Evidence for covert baculovirus infections in a Spodoptera exigua laboratory culture. J. Gen. Virol. 2011, 92, 1061–1070, doi:10.1099/vir.0.028027-0.
[149]
Bronkhorst, A.W.; van Cleef, K.W.; Vodovar, N.; Ince, I.A.; Blanc, H.; Vlak, J.M.; Saleh, M.C.; van Rij, R.P. The DNA virus invertebrate iridescent virus 6 is a target of the Drosophila RNAi machinery. Proc. Natl. Acad. Sci. USA. 2012, 109, E3604–E3613.
[150]
Jayachandran, B.; Hussain, M.; Asgari, S. RNA interference as a cellular defense mechanism against the DNA virus baculovirus. J. Virol. 2012, 86, 13729–13734, doi:10.1128/JVI.02041-12.
[151]
Wu, Y.L.; Wu, C.P.; Liu, C.Y.; Hsu, P.W.; Wu, E.C.; Chao, Y.C. A non-coding RNA of insect HzNV-1 virus establishes latent viral infection through microRNA. Sci. Rep. 2011, 1, 1–10.
[152]
Van Den Abbeele, J.; Bourtzis, K.; Weiss, B.; Cord?n-Rosales, C.; Miller, W.; Abd-Alla, A.M.M.; Parker, A. Enhancing tsetse fly refractoriness to trypanosome infection—A new IAEA coordinated research project. J. Invertebr. Pathol. 2013, 112, S142–S147, doi:10.1016/j.jip.2012.07.020.
[153]
Strand, M.R. Polydnaviruses. In Insect Virology; Asgari, S., Johnson, K.N., Eds.; Caister Academic Press: Norfolk, UK, 2010; pp. 171–197.
[154]
Terzian, C.; Pelisson, A.; Bucheton, A. When Drosophila Meets Retrovirology: The Gypsy Case. In Transposons and the Dynamic Genome; Lankenau, D.H., Volff, J.N., Eds.; Springer-Verlag Berlin Heidelberg: London, UK, 2009; pp. 95–107.
[155]
Varaldi, J.; Ravallec, M.; Labrosse, C.; Lopez-Ferber, M.; Bouletreau, M.; Fleury, F. Artifical transfer and morphological description of virus particles associated with superparasitism behaviour in a parasitoid wasp. J. Insect Physiol. 2006, 52, 1202–1212, doi:10.1016/j.jinsphys.2006.09.002.
[156]
Varaldi, J.; Fouillet, P.; Ravallec, M.; Lopez-Ferber, M.; Bouletreau, M.; Fleury, F. Infectious behavior in a parasitoid. Science 2003, 302, 1930, doi:10.1126/science.1088798.
[157]
Rosen, L. Mechanism of vertical transmission of the dengue virus in mosquitoes. C. R. Acad. Sci. III 1987, 304, 347–350.
[158]
Capinera, J.L. Habita. In Encyclopedia of Entomology, 2nd; Capinera, J.L., Ed.; Springer Science: Dordrecht, The Netherlands, 2008; pp. 1761–1906.
[159]
Lietze, V.U.; Geden, C.J.; Doyle, M.A.; Boucias, D.G. Disease dynamics and persistence of Musca domestica salivary gland hypertrophy virus infections in laboratory house fly (Musca domestica) populations. Appl. Environ. Microbiol. 2012, 78, 311–317, doi:10.1128/AEM.06500-11.
[160]
Walshe, D.P.; Lehane, M.J.; Haines, L.R. Post eclosion age predicts the prevalence of midgut trypanosome infections in Glossina. PLoS One 2011, 6, e26984, doi:10.1371/journal.pone.0026984.
[161]
Bignell, D.E. The Arthropod Gut as an Environment for Microorganisms. In Microbial Ecology of the Gut; Clarke, R.T.J., Bauchop, T., Eds.; Academic Press Inc.: New York, NY, USA, 1983; pp. 205–227.
[162]
Zhuzhikov, D.P. Function of the peritrophic membrane in Musca domestica L. and Calliphora erythrocephala Meig. J. Insect Physiol. 1964, 10, 273–278, doi:10.1016/0022-1910(64)90011-3.
[163]
Chapman, R.F. Circulatory System, Blood and Immune Systems. In The Insects: Structure and Functions, 4th; Simpson, S.J., Douglas, A.E., Eds.; Cambridge University Press: Cambridge, NY, USA, 1998; pp. 94–127.
[164]
Feng, L.C. The role of the peritrophic membrane in Leishmania and Trypanosome infections of sandflies. Peking Nat. Hist. Bull. 1951, 19, 327–334.
[165]
Hegedus, D.; Erlandson, M.; Gillott, C.; Toprak, U. New insights into peritrophic matrix synthesis, architecture, and function. Annu. Rev. Entomol. 2009, 54, 285–302, doi:10.1146/annurev.ento.54.110807.090559.
[166]
Blackburn, K.; Wallbanks, K.R.; Molyneux, D.H.; Lavin, D.R.; Winstanley, S.L. The peritrophic membrane of the female sandfly Phlebotomus papatasi. Ann. Trop. Med. Parasitol. 1988, 82, 613–619.
[167]
Bertram, D.S.; Bird, R.G. Studies on mosquito-borne viruses in their vector. I. The normal fine structure of the midgut epithelium of the adult female Aedes aegypti (L). and the functional significance of its modifications following a bloodmeal. Trans. R. Soc. Trop. Med. Hyg. 1961, 55, 404–423, doi:10.1016/0035-9203(61)90085-2.
[168]
Chamberlain, R.W.; Sudia, W.D. Mechanism of transmission of viruses by mosquitoes. Annu. Rev. Entomol. 1961, 6, 371–390, doi:10.1146/annurev.en.06.010161.002103.
[169]
Gemetchu, T. The morphology and fine structure of the midgut and peritrophic membrane of the adult female, Phlebotomus longipes Parrot and Martin (Diptera: Psychodidae). Ann. Trop. Med. Parasitol. 1974, 68, 111–124.
[170]
Mitsuhashi, W.; Kawakita, H.; Murakami, R.; Takemoto, Y.; Saiki, T.; Miyamoto, K.; Wada, S. Spindles of an entomopoxvirus facilitate its infection of the host insect by disrupting the peritrophic membrane. J. Virol. 2007, 81, 4235–4243, doi:10.1128/JVI.02300-06.
[171]
Wang, P.; Granados, R.R. Molecular structure of the peritrophic membrane (PM): Identification of potential PM target sites for insect control. Arch. Insect Biochem. Physiol. 2001, 47, 110–118, doi:10.1002/arch.1041.
Li, F.; Patra, K.P.; Vinetz, J.M. An anti-Chitinase malaria transmission-blocking single-chain antibody as an effector molecule for creating a Plasmodium falciparum-refractory mosquito. J. Infect. Dis. 2005, 192, 878–887, doi:10.1086/432552.
[174]
Ejezie, G.C.; Davey, K.G. Some effects of mating in female tsetse, Glossina austeni Newst. J. Exp. Zool. 1977, 200, 303–310, doi:10.1002/jez.1402000211.
[175]
Harrison, R.; Hoover, K. Baculoviruses and other occluded viruses. In Insect Pathology, 2nd; Vega, E.F., Kaya, H.K., Eds.; Elsevier: New York, NY, USA, 2012; pp. 73–131.
[176]
Moscardi, F. Assessment of the application of baculoviruses for control of Lepidoptera. Annu. Rev. Entomol. 1999, 44, 257–289, doi:10.1146/annurev.ento.44.1.257.
[177]
Horton, H.M.; Burand, J.P. Saturable attachment sites for polyhedron-derived baculovirus on insect cells and evidence for entry via direct membrane fusion. J. Virol. 1993, 67, 1860–1868.
[178]
Sparks, W.O.; Rohlfing, A.; Bonning, B.C. A peptide with similarity to baculovirus ODV-E66 binds the gut epithelium of Heliothis virescens and impedes infection with Autographa californica multiple nucleopolyhedrovirus. J. Gen. Virol. 2011, 92, 1051–1060, doi:10.1099/vir.0.028118-0.
[179]
Sparks, W.O.; Harrison, R.L.; Bonning, B.C. Autographa californica multiple nucleopolyhedrovirus ODV-E56 is a per os infectivity factor, but is not essential for binding and fusion of occlusion-derived virus to the host midgut. Virology 2011, 409, 69–76, doi:10.1016/j.virol.2010.09.027.
[180]
Abd-Alla, A.M.; Adun, H.; Parker, A.G.; Vreysen, M.J.; Bergoin, M. The antiviral drug valacyclovir successfully suppresses salivary gland hypertrophy virus (SGHV) in laboratory colonies of Glossina pallidipes. PLoS One 2012, 7, e38417.
[181]
Feldmann, U. Guidelines for the rearing of tsetse flies using the membrane feeding technique. In Techniques of Insect Rearing for the Development of Integrated Pest and Vector Management Strategies; Ochieng'-Odero, J.P.R., Ed.; ICIPE Science Press: Nairobi, Kenya, 1994; pp. 449–471.
[182]
Enserink, M. Welcome to Ethiopia’s fly factory. Science 2007, 317, 310–313, doi:10.1126/science.317.5836.310.
[183]
Malele, I.I.; Manangwa, O.; Nyingilili, H.H.; Kitwika, W.A.; Lyaruu, E.A.; Msangi, A.R.; Ouma, J.O.; Nkwangulila, G.; Abd-Alla, A.M.M. Prevalence of SGHV among tsetse species of economic importance in Tanzania and their implication for SIT application. J. Invertebr. Pathol. 2013, 112, S133–S137, doi:10.1016/j.jip.2012.07.018.
[184]
Abd-Alla, A.M.M.; Arif, B. Foreword. J. Invertebr. Pathol. 2013, 112, S1, doi:10.1016/j.jip.2012.07.008.