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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.
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.
The Effects of a DNA Virus Infection on the Reproductive Potential of Female Tsetse Flies, Glossina morsitans centralis and Glossina morsitans morsitans (Diptera: Glossinidae)
Sang, Rosemary C;Jura, Walter GZO;Otieno, Leonard H;Mwangi, Richard W;
Memórias do Instituto Oswaldo Cruz , 1998, DOI: 10.1590/S0074-02761998000600030
Abstract: reproductive anomalies associated with the tsetse dna virus infection in the female tsetse hosts, glossina morsitans centralis machado and glossina morsitans morsitans westwood, inoculated with the virus during the 3rd instar larval stage were studied and the data compared to those obtained from the control females injected with sterile physiological saline. virus infected flies had significantly longer first and second pregnancy cycles (p<0.0001) and produced pupae that were of significantly less weight in milligrams (p<0.0001) compared to controls. transmission of the virus to progeny was not absolute and only 21% of g. m. centralis and 48% of g. m. morsitans first progeny flies from infected females developed salivary gland hypertrophy as a result of transmission from mother to progeny. the virus infected females produced significantly fewere pupae compared to the controls during the experimental period (p<0.00001).
The Effects of a DNA Virus Infection on the Reproductive Potential of Female Tsetse Flies, Glossina morsitans centralis and Glossina morsitans morsitans (Diptera: Glossinidae)  [cached]
Sang Rosemary C,Jura Walter GZO,Otieno Leonard H,Mwangi Richard W
Memórias do Instituto Oswaldo Cruz , 1998,
Abstract: Reproductive anomalies associated with the tsetse DNA virus infection in the female tsetse hosts, Glossina morsitans centralis Machado and Glossina morsitans morsitans Westwood, inoculated with the virus during the 3rd instar larval stage were studied and the data compared to those obtained from the control females injected with sterile physiological saline. Virus infected flies had significantly longer first and second pregnancy cycles (P<0.0001) and produced pupae that were of significantly less weight in milligrams (P<0.0001) compared to controls. Transmission of the virus to progeny was not absolute and only 21% of G. m. centralis and 48% of G. m. morsitans first progeny flies from infected females developed salivary gland hypertrophy as a result of transmission from mother to progeny. The virus infected females produced significantly fewere pupae compared to the controls during the experimental period (P<0.00001).
Age prevalence of trypanosomal infections in female Glossina morsitans morsitans (Diptera : Glossinidae) on the plateau area of eastern Zambia  [cached]
C. Kubi,M. Billiouw,P. Van den Bossche
Onderstepoort Journal of Veterinary Research , 2010, DOI: 10.4102/ojvr.v74i3.125
Abstract: Trypanosomal infections in female Glossina morsitans morsitans were investigated in an area in the Eastern Province of Zambia between 1992 and 1994. A total of 4 416 flies were captured, aged using the ovarian ageing method and screened for trypanosomal infections in both the mouthparts, salivary glands and the midgut. Congolense-type infections were identified in 4.8 % of the flies. Vivax-type and immature infections were identified in 1.8 % and 6.8 % of the flies, respectively. The prevalence of con golense-type, vivax-type and immature infections increased with age. For vivax-type infections the age-prevalence relationship could be described by a model assuming a constant per capita rate of infection. For congolense-type and midgut infections, a polynomial term was added to the model significantly improving the fit. The per capita at which flies become infected was significantly higher for immature compared to mature infections. Observations strongly suggest that tsetse acquire new midgut infections at any age and that maturation of these infections is not limited to those obtained during the first blood meal.
Phylogeny of genus Glossina (Diptera: Glossinidae) according to ITS2 sequences
CHEN XiaoaiLI Song LI ChangbenZHAO ShouyuanAksoy Serap,
陈小爱
,李嵩,李昌本,赵寿元,Aksoy Serap

中国科学C辑(英文版) , 1999,
Abstract: The flies of genus Glossina (Diptera: Glossinidae) are an important vector of African trypanosomiases which cause diseases in humans and animals. The ribosomal DNA Internal Transcribed Spacer-2 (ITS-2) region sequences from different Glossina species were PCR-amplified and analyzed in order to construct a molecular phylogeny for genus Glossina. Trees generated by parsimony confirmed the monophyletic taxonomic placement of genus Glossina where fusca group species formed the deepest branch followed by morsitans and palpalis groups, respectively. The placement of Glossina austeni by both the traditional morphological and biochemical criteria has been controversial. Results presented here, based on ITS-2 locus sequence analysis, suggest that Glossina austeni can be placed into a separate sub-generus which forms a sister-group relationship with the morsitans group species.
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
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.
Odorant and Gustatory Receptors in the Tsetse Fly Glossina morsitans morsitans  [PDF]
George F. O. Obiero,Paul O. Mireji,Steven R. G. Nyanjom,Alan Christoffels,Hugh M. Robertson,Daniel K. Masiga
PLOS Neglected Tropical Diseases , 2014, DOI: 10.1371/journal.pntd.0002663
Abstract: Tsetse flies use olfactory and gustatory responses, through odorant and gustatory receptors (ORs and GRs), to interact with their environment. Glossina morsitans morsitans genome ORs and GRs were annotated using homologs of these genes in Drosophila melanogaster and an ab initio approach based on OR and GR specific motifs in G. m. morsitans gene models coupled to gene ontology (GO). Phylogenetic relationships among the ORs or GRs and the homologs were determined using Maximum Likelihood estimates. Relative expression levels among the G. m. morsitans ORs or GRs were established using RNA-seq data derived from adult female fly. Overall, 46 and 14 putative G. m. morsitans ORs and GRs respectively were recovered. These were reduced by 12 and 59 ORs and GRs respectively compared to D. melanogaster. Six of the ORs were homologous to a single D. melanogaster OR (DmOr67d) associated with mating deterrence in females. Sweet taste GRs, present in all the other Diptera, were not recovered in G. m. morsitans. The GRs associated with detection of CO2 were conserved in G. m. morsitans relative to D. melanogaster. RNA-sequence data analysis revealed expression of GmmOR15 locus represented over 90% of expression profiles for the ORs. The G. m. morsitans ORs or GRs were phylogenetically closer to those in D. melanogaster than to other insects assessed. We found the chemoreceptor repertoire in G. m. morsitans smaller than other Diptera, and we postulate that this may be related to the restricted diet of blood-meal for both sexes of tsetse flies. However, the clade of some specific receptors has been expanded, indicative of their potential importance in chemoreception in the tsetse.
Adult midgut expressed sequence tags from the tsetse fly Glossina morsitans morsitans and expression analysis of putative immune response genes
M J Lehane, S Aksoy, W Gibson, A Kerhornou, M Berriman, J Hamilton, M B Soares, M F Bonaldo, S Lehane, N Hall
Genome Biology , 2003, DOI: 10.1186/gb-2003-4-10-r63
Abstract: A total of 21,427 ESTs were produced from the midgut of adult Glossina morsitans morsitans and grouped into 8,876 clusters or singletons potentially representing unique genes. Putative functions were ascribed to 4,035 of these by homology. Of these, a remarkable 3,884 had their most significant matches in the Drosophila protein database. We selected 68 genes with putative immune-related functions, macroarrayed them and determined their expression profiles following bacterial or trypanosome challenge. In both infections many genes are downregulated, suggesting a malaise response in the midgut. Trypanosome and bacterial challenge result in upregulation of different genes, suggesting that different recognition pathways are involved in the two responses. The most notable block of genes upregulated in response to trypanosome challenge are a series of Toll and Imd genes and a series of genes involved in oxidative stress responses.The project increases the number of known Glossina genes by two orders of magnitude. Identification of putative immunity genes and their preliminary characterization provides a resource for the experimental dissection of tsetse-trypanosome interactions.The African trypanosomes that cause sleeping sickness in humans and nagana in livestock are cyclically transmitted by tsetse flies (Glossinidae). Tsetse flies are obligate blood feeders and ingest trypanosomes along with the blood meal from infected animals. In the fly, the trypanosomes undergo complex cycles of growth and development all of which occur within the lumen of the alimentary canal of the fly and, in the case of the brucei group trypanosomes, the salivary glands [1]. Tsetse flies are normally refractory to trypanosome infection with typically less than half the fly population becoming infected, even under ideal conditions in the laboratory. This is reflected in field infection rates which often fail to exceed 10% of the fly population. In addition, many of those that become infected fai
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