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The Salivary Secretome of the Tsetse Fly Glossina pallidipes (Diptera: Glossinidae) Infected by Salivary Gland Hypertrophy Virus  [PDF]
Henry M. Kariithi,Ikbal A. Ince,Sjef Boeren,Adly M. M. Abd-Alla,Andrew G. Parker,Serap Aksoy,Just M. Vlak ,Monique M. van Oers
PLOS Neglected Tropical Diseases , 2011, DOI: 10.1371/journal.pntd.0001371
Abstract: Background The competence of the tsetse fly Glossina pallidipes (Diptera; Glossinidae) to acquire salivary gland hypertrophy virus (SGHV), to support virus replication and successfully transmit the virus depends on complex interactions between Glossina and SGHV macromolecules. Critical requisites to SGHV transmission are its replication and secretion of mature virions into the fly's salivary gland (SG) lumen. However, secretion of host proteins is of equal importance for successful transmission and requires cataloging of G. pallidipes secretome proteins from hypertrophied and non-hypertrophied SGs. Methodology/Principal Findings After electrophoretic profiling and in-gel trypsin digestion, saliva proteins were analyzed by nano-LC-MS/MS. MaxQuant/Andromeda search of the MS data against the non-redundant (nr) GenBank database and a G. morsitans morsitans SG EST database, yielded a total of 521 hits, 31 of which were SGHV-encoded. On a false discovery rate limit of 1% and detection threshold of least 2 unique peptides per protein, the analysis resulted in 292 Glossina and 25 SGHV MS-supported proteins. When annotated by the Blast2GO suite, at least one gene ontology (GO) term could be assigned to 89.9% (285/317) of the detected proteins. Five (~1.8%) Glossina and three (~12%) SGHV proteins remained without a predicted function after blast searches against the nr database. Sixty-five of the 292 detected Glossina proteins contained an N-terminal signal/secretion peptide sequence. Eight of the SGHV proteins were predicted to be non-structural (NS), and fourteen are known structural (VP) proteins. Conclusions/Significance SGHV alters the protein expression pattern in Glossina. The G. pallidipes SG secretome encompasses a spectrum of proteins that may be required during the SGHV infection cycle. These detected proteins have putative interactions with at least 21 of the 25 SGHV-encoded proteins. Our findings opens venues for developing novel SGHV mitigation strategies to block SGHV infections in tsetse production facilities such as using SGHV-specific antibodies and phage display-selected gut epithelia-binding peptides.
Tsetse Salivary Gland Hypertrophy Virus: Hope or Hindrance for Tsetse Control?  [PDF]
Adly M. M. Abd-Alla ,Andrew G. Parker,Marc J. B. Vreysen,Max Bergoin
PLOS Neglected Tropical Diseases , 2011, DOI: 10.1371/journal.pntd.0001220
Abstract: Many species of tsetse flies (Diptera: Glossinidae) are infected with a virus that causes salivary gland hypertrophy (SGH), and flies with SGH symptoms have a reduced fecundity and fertility. The prevalence of SGH in wild tsetse populations is usually very low (0.2%–5%), but higher prevalence rates (15.2%) have been observed occasionally. The successful eradication of a Glossina austeni population from Unguja Island (Zanzibar) using an area-wide integrated pest management approach with a sterile insect technique (SIT) component (1994–1997) encouraged several African countries, including Ethiopia, to incorporate the SIT in their national tsetse control programs. A large facility to produce tsetse flies for SIT application in Ethiopia was inaugurated in 2007. To support this project, a Glossina pallidipes colony originating from Ethiopia was successfully established in 1996, but later up to 85% of adult flies displayed symptoms of SGH. As a result, the colony declined and became extinct by 2002. The difficulties experienced with the rearing of G. pallidipes, epitomized by the collapse of the G. pallidipes colony originating from Ethiopia, prompted the urgent need to develop management strategies for the salivary gland hypertrophy virus (SGHV) for this species. As a first step to identify suitable management strategies, the virus isolated from G. pallidipes (GpSGHV) was recently sequenced and research was initiated on virus transmission and pathology. Different approaches to prevent virus replication and its horizontal transmission during blood feeding have been proposed. These include the use of antiviral drugs such as acyclovir and valacyclovir added to the blood for feeding or the use of antibodies against SGHV virion proteins. In addition, preliminary attempts to silence the expression of an essential viral protein using RNA interference will be discussed.
Managing Hytrosavirus Infections in Glossina pallidipes Colonies: Feeding Regime Affects the Prevalence of Salivary Gland Hypertrophy Syndrome  [PDF]
Adly M. M. Abd-Alla, Henry M. Kariithi, Abdul Hasim Mohamed, Edgardo Lapiz, Andrew G. Parker, Marc J. B. Vreysen
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0061875
Abstract: Many species of tsetse flies are infected by a virus that causes salivary gland hypertrophy (SGH) syndrome and the virus isolated from Glossina pallidipes (GpSGHV) has recently been sequenced. Flies with SGH have a reduced fecundity and fertility. Due to the deleterious impact of SGHV on G. pallidipes colonies, several approaches were investigated to develop a virus management strategy. Horizontal virus transmission is the major cause of the high prevalence of the GpSGHV in tsetse colonies. Implementation of a “clean feeding” regime (fresh blood offered to each set of flies so that there is only one feed per membrane), instead of the regular feeding regime (several successive feeds per membrane), was among the proposed approaches to reduce GpSGHV infections. However, due to the absence of disposable feeding equipment (feeding trays and silicone membranes), the implementation of a clean feeding approach remains economically difficult. We developed a new clean feeding approach applicable to large-scale tsetse production facilities using existing resources. The results indicate that implementing this approach is feasible and leads to a significant reduction in virus load from 109 virus copies in regular colonies to an average of 102.5 and eliminates the SGH syndrome from clean feeding colonies by28 months post implementation of this approach. The clean feeding approach also reduced the virus load from an average of 108 virus copy numbers to an average of 103 virus copies and SGH prevalence of 10% to 4% in flies fed after the clean fed colony. Taken together, these data indicate that the clean feeding approach is applicable in large-scale G. pallidipes production facilities and eliminates the deleterious effects of the virus and the SGH syndrome in these colonies.
Virology, Epidemiology and Pathology of Glossina Hytrosavirus, and Its Control Prospects in Laboratory Colonies of the Tsetse Fly, Glossina pallidipes (Diptera; Glossinidae)  [PDF]
Henry M. Kariithi,Monique M. van Oers,Just M. Vlak,Marc J. B. Vreysen,Andrew G. Parker,Adly M. M. Abd-Alla
Insects , 2013, DOI: 10.3390/insects4030287
Abstract: 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.
Impact of Salivary Gland Hypertrophy Virus Infection on the Mating Success of Male Glossina pallidipes: Consequences for the Sterile Insect Technique  [PDF]
Gratian N. Mutika, Carmen Marin, Andrew G. Parker, Drion G. Boucias, Marc J. B. Vreysen, Adly M. M. Abd-Alla
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0042188
Abstract: Many species of tsetse flies are infected by a virus (GpSGHV) that causes salivary gland hypertrophy (SGH). Female Glossina pallidipes (Austen) with SGH symptoms (SGH+) have reduced fecundity and SGH+ male G. pallidipes are unable to inseminate female flies. Consequently, G. pallidipes laboratory colonies with a high prevalence of SGH have been difficult to maintain and have collapsed on several occasions. To assess the potential impact of the release of SGH+ sterile male G. pallidipes on the efficacy of an integrated control programme with a sterile insect technique (SIT) component, we examined the mating efficiency and behaviour of male G. pallidipes in field cages in relation to SGH prevalence. The results showed in a field cage setting a significantly reduced mating frequency of 19% for a male G. pallidipes population with a high prevalence of SGH (83%) compared to 38% for a male population with a low prevalence of SGH (7%). Premating period and mating duration did not vary significantly with SGH status. A high percentage (>80%) of females that had mated with SGH+ males had empty spermathecae. The remating frequency of female G. pallidipes was very low irrespective of the SGH status of the males in the first mating. These results indicate that a high prevalence of SGH+ in G. pallidipes not only affects colony stability and performance but, in view of their reduced mating propensity and competitiveness, releasing SGH+ sterile male G. pallidipes will reduce the efficiency of a sterile male release programme.
Transgenerational Transmission of the Glossina pallidipes Hytrosavirus Depends on the Presence of a Functional Symbiome  [PDF]
Drion G. Boucias, Henry M. Kariithi, Kostas Bourtzis, Daniela I. Schneider, Karen Kelley, Wolfgang J. Miller, Andrew G. Parker, Adly M. M. Abd-Alla
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0061150
Abstract: The vertically transmitted endosymbionts (Sodalis glossinidius and Wigglesworthia glossinidia) of the tsetse fly (Diptera: Glossinidae) are known to supplement dietary deficiencies and modulate the reproductive fitness and the defense system of the fly. Some tsetse fly species are also infected with the bacterium, Wolbachia and with the Glossina hytrosavirus (GpSGHV). Laboratory-bred G. pallidipes exhibit chronic asymptomatic and acute symptomatic GpSGHV infection, with the former being the most common in these colonies. However, under as yet undefined conditions, the asymptomatic state can convert to the symptomatic state, leading to detectable salivary gland hypertrophy (SGH+) syndrome. In this study, we investigated the interplay between the bacterial symbiome and GpSGHV during development of G. pallidipes by knocking down the symbionts with antibiotic. Intrahaemocoelic injection of GpSGHV led to high virus titre (109 virus copies), but was not accompanied by either the onset of detectable SGH+, or release of detectable virus particles into the blood meals during feeding events. When the F1 generations of GpSGHV-challenged mothers were dissected within 24 h post-eclosion, SGH+ was observed to increase from 4.5% in the first larviposition cycle to >95% in the fourth cycle. Despite being sterile, these F1 SGH+ progeny mated readily. Removal of the tsetse symbiome, however, suppressed transgenerational transfer of the virus via milk secretions and blocked the ability of GpSGHV to infect salivary glands of the F1 progeny. Whereas GpSGHV infects and replicates in salivary glands of developing pupa, the virus is unable to induce SGH+ within fully differentiated adult salivary glands. The F1 SGH+ adults are responsible for the GpSGHV-induced colony collapse in tsetse factories. Our data suggest that GpSGHV has co-evolved with the tsetse symbiome and that the symbionts play key roles in the virus transmission from mother to progeny.
Identification of landing Site Preference of Fully-fed Glossina pallidipes and Glossina morsitans (diptera: glossinidae)  [PDF]
Nyengerai, T.,Gori, E.,Mwandiringana, E.,Mushayi, W.
Journal of Environmental Issues and Agriculture in Developing Countries , 2012,
Abstract: An experiment to identify landing sites of fully fed Glossina pallidipes and Glossina morsitans was set up at the end of the winter season in Zimbabwe at Rukomichi Research Station. Five experiments subjected to three treatments differing in duration of catch, interval of catch and landing position were performed. A mean catch of 13 was recorded for 15-minute interval catches on logs wrapped in black cloth for the same species. Site and treatment had a significant effect on mean catch levels for Glossina morsitans (LSD=0.0979) and Glossina pallidipes (LSD=0, 1409). The mean catch (1644) for both fully fed Glossina morsitans and Glossina pallidipes was highest for 15-minute interval catches on unwrapped upright logs. This was twice higher than the overall mean catch recorded for continuous catch on unwrapped upright logs indicating the repellent effect of man on Glossina morsitans and Glossina pallidipes. Unwrapped upright logs could alternatively be used to catch Glossina pallidipes and Glossina morsitans after feeding for the purpose of biological and chemical assays to determine the effectiveness of chemicals on trials. This could also avoid the rubbing effect on the animal body and hence eliminating contamination on the hand-nets.
Genetic diversity and population structure of Glossina pallidipes in Uganda and western Kenya
Johnson O Ouma, Jon S Beadell, Chaz Hyseni, Loyce M Okedi, Elliot S Krafsur, Serap Aksoy, Adalgisa Caccone
Parasites & Vectors , 2011, DOI: 10.1186/1756-3305-4-122
Abstract: AMOVA indicated that differences among sampling sites explained a significant proportion of the genetic variation. Principal component analysis and Bayesian assignment of microsatellite genotypes identified three distinct clusters: western Uganda, southeastern Uganda/Lambwe Valley, and Nguruman in central-southern Kenya. Analyses of mtDNA confirmed the results of microsatellite analysis, except in western Uganda, where Kabunkanga and Murchison Falls populations exhibited haplotypes that differed despite homogeneous microsatellite signatures. To better understand possible causes of the contrast between mitochondrial and nuclear markers we tested for sex-biased dispersal. Mean pairwise relatedness was significantly higher in females than in males within populations, while mean genetic distance was lower and relatedness higher in males than females in between-population comparisons. Two populations sampled on the Kenya/Uganda border, exhibited the lowest levels of genetic diversity. Microsatellite alleles and mtDNA haplotypes in these two populations were a subset of those found in neighboring Lambwe Valley, suggesting that Lambwe was the source population for flies in southeastern Uganda. The relatively high genetic diversity of G. pallidipes in Lambwe Valley suggest large relict populations remained even after repeated control efforts.Our research demonstrated that G. pallidipes populations in Kenya and Uganda do not form a contiguous tsetse belt. While Lambwe Valley appears to be a source population for flies colonizing southeastern Uganda, this dispersal does not extend to western Uganda. The complicated phylogeography of G. pallidipes warrants further efforts to distinguish the role of historical and modern gene flow and possible sex-biased dispersal in structuring populations.Glossina pallidipes is a major vector of animal African trypanosomiasis. The vector has also been implicated in the transmission of Human African Trypanosomiasis (HAT). For example, the expa
Laboratory Colonisation and Genetic Bottlenecks in the Tsetse Fly Glossina pallidipes  [PDF]
Marc Ciosi ,Daniel K. Masiga equal contributor,Charles M. R. Turner equal contributor
PLOS Neglected Tropical Diseases , 2014, DOI: 10.1371/journal.pntd.0002697
Abstract: Background The IAEA colony is the only one available for mass rearing of Glossina pallidipes, a vector of human and animal African trypanosomiasis in eastern Africa. This colony is the source for Sterile Insect Technique (SIT) programs in East Africa. The source population of this colony is unclear and its genetic diversity has not previously been evaluated and compared to field populations. Methodology/Principal Findings We examined the genetic variation within and between the IAEA colony and its potential source populations in north Zimbabwe and the Kenya/Uganda border at 9 microsatellites loci to retrace the demographic history of the IAEA colony. We performed classical population genetics analyses and also combined historical and genetic data in a quantitative analysis using Approximate Bayesian Computation (ABC). There is no evidence of introgression from the north Zimbabwean population into the IAEA colony. Moreover, the ABC analyses revealed that the foundation and establishment of the colony was associated with a genetic bottleneck that has resulted in a loss of 35.7% of alleles and 54% of expected heterozygosity compared to its source population. Also, we show that tsetse control carried out in the 1990's is likely reduced the effective population size of the Kenya/Uganda border population. Conclusions/Significance All the analyses indicate that the area of origin of the IAEA colony is the Kenya/Uganda border and that a genetic bottleneck was associated with the foundation and establishment of the colony. Genetic diversity associated with traits that are important for SIT may potentially have been lost during this genetic bottleneck which could lead to a suboptimal competitiveness of the colony males in the field. The genetic diversity of the colony is lower than that of field populations and so, studies using colony flies should be interpreted with caution when drawing general conclusions about G. pallidipes biology.
An insight into the sialome of Glossina morsitans morsitans
Juliana Alves-Silva, José MC Ribeiro, Jan Abbeele, Geoffrey Attardo, Zhengrong Hao, Lee R Haines, Marcelo B Soares, Matthew Berriman, Serap Aksoy, Michael J Lehane
BMC Genomics , 2010, DOI: 10.1186/1471-2164-11-213
Abstract: As part of the effort to sequence the genome of Glossina morsitans morsitans, several organ specific, high quality normalized cDNA libraries have been constructed, from which over 20,000 ESTs from an adult salivary gland library were sequenced. These ESTs have been assembled using previously described ESTs from the fat body and midgut libraries of the same fly, thus totaling 62,251 ESTs, which have been assembled into 16,743 clusters (8,506 of which had one or more EST from the salivary gland library). Coding sequences were obtained for 2,509 novel proteins, 1,792 of which had at least one EST expressed in the salivary glands. Despite library normalization, 59 transcripts were overrepresented in the salivary library indicating high levels of expression. This work presents a detailed analysis of the salivary protein families identified. Protein expression was confirmed by 2D gel electrophoresis, enzymatic digestion and mass spectrometry. Concurrently, an initial attempt to determine the immunogenic properties of selected salivary proteins was undertaken.The sialome of G. m. morsitans contains over 250 proteins that are possibly associated with blood feeding. This set includes alleles of previously described gene products, reveals new evidence that several salivary proteins are multigenic and identifies at least seven new polypeptide families unique to Glossina. Most of these proteins have no known function and thus, provide a discovery platform for the identification of novel pharmacologically active compounds, innovative vector-based vaccine targets, and immunological markers of vector exposure.The superfamily Hippoboscoidea comprises higher flies (Suborder Brachycera Schizophora: Calyptrate), which includes the tsetse, louse flies, and the bird and bat flies [1]. These flies have in common the unusual ovoviviparous reproductive process. All adults are exclusively blood feeders on mammals or other vertebrates, suggesting that hematophagy is a monophyletic trait in t
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