Insights into the Trypanosome-Host Interactions Revealed through Transcriptomic Analysis of Parasitized Tsetse Fly Salivary Glands

Telleria, Erich Loza; Benoit, Joshua B.; Zhao, Xin; Savage, Amy F.; Regmi, Sandesh; Silva, Thiago Luiz Alves e; O’Neill, Michelle; Aksoy, Serap

doi:10.1371/journal.pntd.0002649

Cited by 69 publications

(87 citation statements)

References 94 publications

(151 reference statements)

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“…RNA-seq analysis of salivary gland gene expression during parasite infection confirmed the reduction of transcript abundance for previously identified genes, such as ada , tsal1 , tsal2 , and 5 ′ nucleotidase , as well as of many other putative secreted salivary protein genes (12). Additionally, genes involved in stress tolerance and cell repair showed increased expression, indicating that considerable salivary gland tissue damage is caused by trypanosome infections.…”

Section: Blood Feeding and Nutritionsupporting

confidence: 68%

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Genome Sequence of the Tsetse Fly ( Glossina morsitans ): Vector of African Trypanosomiasis

Watanabe¹,

Hattori²,

Berriman³

et al. 2014

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Tsetse flies are the sole vectors of human African trypanosomiasis throughout sub-Saharan Africa. Both sexes of adult tsetse feed exclusively on blood and contribute to disease transmission. Notable differences between tsetse and other disease vectors include obligate microbial symbioses, viviparous reproduction, and lactation. Here, we describe the sequence and annotation of the 366-megabase Glossina morsitans morsitans genome. Analysis of the genome and the 12,308 predicted protein–encoding genes led to multiple discoveries, including chromosomal integrations of bacterial (Wolbachia) genome sequences, a family of lactation-specific proteins, reduced complement of host pathogen recognition proteins, and reduced olfaction/chemosensory associated genes. These genome data provide a foundation for research into trypanosomiasis prevention and yield important insights with broad implications for multiple aspects of tsetse biology.

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Section: Blood Feeding and Nutritionsupporting

confidence: 68%

“…( Bottom ) Glossina digestive physiology and the infection process by trypanosomes. Associated satellite references for these findings are listed within the figure as numbers in parentheses and correspond to the reference list (8, 11, 12). …”

Section: Figmentioning

confidence: 99%

Genome Sequence of the Tsetse Fly ( Glossina morsitans ): Vector of African Trypanosomiasis

Watanabe¹,

Hattori²,

Berriman³

et al. 2014

Science

Self Cite

220

146

View full text Add to dashboard Cite

show abstract

“…It was recently shown that this parasite infection led to a drastic change in the abundance of major saliva proteins resulting in a less efficient tsetse fly feeding process [5]. This reduced expression of saliva proteins was later confirmed in a transcriptome analysis on trypanosome-infected flies [6]. In our study we used an extensive RNA-seq approach in which we compared the whole transcriptome profiles of different age-matched experimental groups of T. brucei -infected tsetse flies i.e.…”

Section: Introductionmentioning

confidence: 98%

Tsetse fly tolerance to T. brucei infection: transcriptome analysis of trypanosome-associated changes in the tsetse fly salivary gland

2016

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BackgroundFor their transmission, African trypanosomes rely on their blood feeding insect vector, the tsetse fly (Glossina sp.). The ingested Trypanosoma brucei parasites have to overcome a series of barriers in the tsetse fly alimentary tract to finally develop into the infective metacyclic forms in the salivary glands that are transmitted to a mammalian host by the tsetse bite. The parasite population in the salivary gland is dense with a significant number of trypanosomes tightly attached to the epithelial cells. Our current knowledge on the impact of the infection on the salivary gland functioning is very limited. Therefore, this study aimed to gain a deeper insight into the global gene expression changes in the salivary glands of Glossina morsitans morsitans in response to an infection with the T. brucei parasite. A detailed whole transcriptome comparison of midgut-infected tsetse with and without a mature salivary gland infection was performed to study the impact of a trypanosome infection on different aspects of the salivary gland functioning and the mechanisms that are induced in this tissue to tolerate the infection i.e. to control the negative impact of the parasite presence. Moreover, a transcriptome comparison with age-matched uninfected flies was done to see whether gene expression in the salivary glands is already affected by a trypanosome infection in the tsetse midgut.ResultsBy a RNA-sequencing (RNA-seq) approach we compared the whole transcriptomes of flies with a T. brucei salivary gland/midgut infection versus flies with only a midgut infection or versus non-infected flies, all with the same age and feeding history. More than 7500 salivary gland transcripts were detected from which a core group of 1214 differentially expressed genes (768 up- and 446 down-regulated) were shared between the two transcriptional comparisons. Gene Ontology enrichment analysis and detailed gene expression comparisons showed a diverse impact at the gene transcript level. Increased expression was observed for transcripts encoding for proteins involved in immunity (like several genes of the Imd-signaling pathway, serine proteases, serpins and thioester-containing proteins), detoxification of reactive species, cell death, cytoskeleton organization, cell junction and repair. Decreased expression was observed for transcripts encoding the major secreted proteins such as 5′-nucleotidases, adenosine deaminases and the nucleic acid binding proteins Tsals. Moreover, expression of some gene categories in the salivary glands were found to be already affected by a trypanosome midgut infection, before the parasite reaches the salivary glands.ConclusionsThis study reveals that the T. brucei population in the tsetse salivary gland has a negative impact on its functioning and on the integrity of the gland epithelium. Our RNA-seq data suggest induction of a strong local tissue response in order to control the epithelial cell damage, the ROS intoxication of the cellular environment and the parasite infection, resulting in the fly tolera...

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“…2 A tight control of gene expression occurs during tsetse colonization by T. brucei, where unique transcripts from parasites infecting midgut, cardia, and salivary glands have been reported. 3,4 Lipid phosphate phosphatases (LPPs) are members of the phosphatidic acid phosphatase superfamily. 5 LPP enzymes catalyze the dephosphorylation of phosphorous lipids, important in a broad range of physiological functions including cell migration, proliferation, and differentiation.…”

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confidence: 99%

Transcript Abundance of Putative Lipid Phosphate Phosphatases During Development of Trypanosoma brucei in the Tsetse Fly

Silva

Savage

Aksoy

2016

The American Journal of Tropical Medicine and Hygiene

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Abstract. African trypanosomes (Trypanosoma brucei spp.) cause devastating diseases in sub-Saharan Africa. Trypanosomes differentiate repeatedly during development in tsetse flies before gaining mammalian infectivity in fly salivary glands. Lipid phosphate phosphatases (LPPs) are involved in diverse biological processes, such as cell differentiation and cell migration. Gene sequences encoding two putative T. brucei LPP proteins were used to search the T. brucei genome, revealing two additional putative family members. Putative structural features and transcript abundance during parasite development in tsetse fly were characterized. Three of the four LPP proteins are predicted to have six transmembrane domains, while the fourth shows only one. Semiquantitative gene expression revealed differential regulation of LPPs during parasite development. Transcript abundance for three of the four putative LPP genes was elevated in parasites infecting salivary glands, but not mammalian-infective metacyclic cells in fly saliva, indicating a potential role of this family in parasite establishment in tsetse salivary glands.Trypanosoma brucei spp. cause human African trypanosomiasis and animal African trypanosomiasis in sub-Saharan Africa.

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Insights into the Trypanosome-Host Interactions Revealed through Transcriptomic Analysis of Parasitized Tsetse Fly Salivary Glands

Cited by 69 publications

References 94 publications

Genome Sequence of the Tsetse Fly ( Glossina morsitans ): Vector of African Trypanosomiasis

Genome Sequence of the Tsetse Fly ( Glossina morsitans ): Vector of African Trypanosomiasis

Tsetse fly tolerance to T. brucei infection: transcriptome analysis of trypanosome-associated changes in the tsetse fly salivary gland

Transcript Abundance of Putative Lipid Phosphate Phosphatases During Development of Trypanosoma brucei in the Tsetse Fly

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