Horizontal gene transfer of a vertebrate vasodilatory hormone into ticks

Iwanaga, Shiro; Isawa, Haruhiko

doi:10.1038/ncomms4373

Cited by 16 publications

(11 citation statements)

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“…The identification of overexpressed transcripts in the haemocyte library matching vertebrate proteins could be due to artefactual contamination of the haemolymph with host blood during the manipulations required for haemolymph extraction. Alternatively, these matches might represent active invasion of the haemocoel by host leukocytes, or, although rare, be derived from the tick genome via a horizontal transfer event, which is known to have occurred at least once in soft ticks [ 75 ].…”

Section: Discussionmentioning

confidence: 99%

Deep Sequencing Analysis of the Ixodes ricinus Haemocytome

et al. 2015

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Background Ixodes ricinus is the main tick vector of the microbes that cause Lyme disease and tick-borne encephalitis in Europe. Pathogens transmitted by ticks have to overcome innate immunity barriers present in tick tissues, including midgut, salivary glands epithelia and the hemocoel. Molecularly, invertebrate immunity is initiated when pathogen recognition molecules trigger serum or cellular signalling cascades leading to the production of antimicrobials, pathogen opsonization and phagocytosis. We presently aimed at identifying hemocyte transcripts from semi-engorged female I. ricinus ticks by mass sequencing a hemocyte cDNA library and annotating immune-related transcripts based on their hemocyte abundance as well as their ubiquitous distribution.Methodology/principal findings De novo assembly of 926,596 pyrosequence reads plus 49,328,982 Illumina reads (148 nt length) from a hemocyte library, together with over 189 million Illumina reads from salivary gland and midgut libraries, generated 15,716 extracted coding sequences (CDS); these are displayed in an annotated hyperlinked spreadsheet format. Read mapping allowed the identification and annotation of tissue-enriched transcripts. A total of 327 transcripts were found significantly over expressed in the hemocyte libraries, including those coding for scavenger receptors, antimicrobial peptides, pathogen recognition proteins, proteases and protease inhibitors. Vitellogenin and lipid metabolism transcription enrichment suggests fat body components. We additionally annotated ubiquitously distributed transcripts associated with immune function, including immune-associated signal transduction proteins and transcription factors, including the STAT transcription factor.Conclusions/significanceThis is the first systems biology approach to describe the genes expressed in the haemocytes of this neglected disease vector. A total of 2,860 coding sequences were deposited to GenBank, increasing to 27,547 the number so far deposited by our previous transcriptome studies that serves as a discovery platform for studies with I. ricinus biochemistry and physiology.

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Section: Discussionmentioning

confidence: 99%

Deep Sequencing Analysis of the Ixodes ricinus Haemocytome

et al. 2015

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“…The repertoire of tick saliva may be complementary to its preferred host’s homeostatic and immune strategies. Ticks can acquire host genes through horizontal gene transfer [ 45 ]; therefore, ticks with different feeding habits may have different repertoires of salivary proteins. A total of six RNA-seq libraries were generated from the salivary glands of nymph and female ticks.…”

Section: Introductionmentioning

confidence: 99%

The sialotranscriptome of Amblyomma triste, Amblyomma parvum and Amblyomma cajennense ticks, uncovered by 454-based RNA-seq

et al. 2014

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BackgroundTick salivary constituents antagonize inflammatory, immune and hemostatic host responses, favoring tick blood feeding and the establishment of tick-borne pathogens in hosts during hematophagy. Amblyomma triste, A. cajennense and A. parvum ticks are very important in veterinary and human health because they are vectors of the etiological agents for several diseases. Insights into the tick salivary components involved in blood feeding are essential to understanding vector-pathogen-host interactions, and transcriptional profiling of salivary glands is a powerful tool to do so. Here, we functionally annotated the sialotranscriptomes of these three Amblyomma species, which allowed comparisons between these and other hematophagous arthropod species.MethodsmRNA from the salivary glands of A. triste, A. cajennense and A. parvum ticks fed on different host species were pyrosequenced on a 454-Roche platform to generate four A. triste (nymphs fed on guinea pigs and females fed on dogs) libraries, one A. cajennense (females fed on rabbits) library and one was A. parvum (females fed on dogs) library. Bioinformatic analyses used in-house programs with a customized pipeline employing standard assembly and alignment algorithms, protein databases and protein servers.ResultsEach library yielded an average of 100,000 reads, which were assembled to obtain contigs of coding sequences (CDSs). The sialotranscriptome analyses of A. triste, A. cajennense and A. parvum ticks produced 11,240, 4,604 and 3,796 CDSs, respectively. These CDSs were classified into over 100 distinct protein families with a wide range of putative functions involved in physiological and blood feeding processes and were catalogued in annotated, hyperlinked spreadsheets. We highlighted the putative transcripts encoding saliva components with critical roles during parasitism, such as anticoagulants, immunosuppressants and anti-inflammatory molecules. The salivary content underwent changes in the abundance and repertoire of many transcripts, which depended on the tick and host species.ConclusionsThe annotated sialotranscriptomes described herein richly expand the biological knowledge of these three Amblyomma species. These comprehensive databases will be useful for the characterization of salivary proteins and can be applied to control ticks and tick-borne diseases.Electronic supplementary materialThe online version of this article (doi:10.1186/1756-3305-7-430) contains supplementary material, which is available to authorized users.

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“…Evidence of gene duplication is common across salivary genes, and it is thought to have greatly contributed to both the specificity of salivary protein function and the evolution of novel functions ( Arca and Ribeiro, 2018 ). Horizontal gene transfer (HGT), too, has provided new tools for blood feeding arthropods; Ornithodoros ticks have acquired a vasodilatory hormone of vertebrate origin by HGT ( Iwanaga et al., 2014 ), and genes originating from Wolbachia have been identified among salivary genes in both Anopheles and Aedes mosquitoes ( Arcà et al., 2005 ; Korochkina et al., 2006 ). Horizontal transfer of a prokaryotic carbohydrate recognition domain to a common dipteran ancestor approximately 250 MYA could explain the divergence of the CWRC proteins across Culicomorpha, including frog-biting midges, Corethrella , and Psorophora mosquitoes ( Fig.…”

Section: Discussionmentioning

confidence: 99%

The structures of two salivary proteins from the West Nile vector Culex quinquefasciatus reveal a beta-trefoil fold with putative sugar binding properties

Kern

Valenzuela-León

Gittis

et al. 2021

Current Research in Structural Biology

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Female mosquitoes require blood meals for egg development. The saliva of blood feeding arthropods contains biochemically active molecules, whose anti-hemostatic and anti-inflammatory properties facilitate blood feeding on vertebrate hosts. While transcriptomics has presented new opportunities to investigate the diversity of salivary proteins from hematophagous arthropods, many of these proteins remain functionally undescribed. Previous transcriptomic analysis of female salivary glands from Culex quinquefasciatus, an important vector of parasitic and viral infections, uncovered a 12-member family of putatively secreted proteins of unknown function, named the Cysteine and Tryptophan-Rich (CWRC) proteins. Here, we present advances in the characterization of two C. quinquefasciatus CWRC family members, CqDVP-2 and CqDVP-4, including their enrichment in female salivary glands, their specific localization within salivary gland tissues, evidence that these proteins are secreted into the saliva, and their native crystal structures, at 2.3 Å and 1.87 Å, respectively. The β-trefoil fold common to CqDVP-2 and CqDVP-4 is similar to carbohydrate-binding proteins, including the B subunit of the AB toxin, ricin, from the castor bean Ricinus communis . Further, we used a glycan array approach, which identifies carbohydrate ligands associated with inflammatory processes and signal transduction. Glycan array 300 testing identified 100 carbohydrate moieties with positive binding to CqDVP-2, and 77 glycans with positive binding to CqDVP-4. The glycan with the highest relative fluorescence intensities, which exhibited binding to both CqDVP-2 and CqDVP-4, was used for molecular docking experiments. We hypothesize that these proteins bind to carbohydrates on the surface of cells important to host immunology. Given that saliva is deposited into the skin during a mosquito bite, and acts as the vehicle for arbovirus inoculation, understanding the role of these proteins in pathogen transmission is of critical importance. This work presents the first solved crystal structures of C. quinquefasciatus salivary proteins with unknown function. These two molecules are the second and third structures reported from salivary proteins from C. quinquefasciatus , an important, yet understudied disease vector.

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Horizontal gene transfer of a vertebrate vasodilatory hormone into ticks

Cited by 16 publications

References 36 publications

Deep Sequencing Analysis of the Ixodes ricinus Haemocytome

Deep Sequencing Analysis of the Ixodes ricinus Haemocytome

The sialotranscriptome of Amblyomma triste, Amblyomma parvum and Amblyomma cajennense ticks, uncovered by 454-based RNA-seq

The structures of two salivary proteins from the West Nile vector Culex quinquefasciatus reveal a beta-trefoil fold with putative sugar binding properties

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