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IrSPI, a tick serine protease inhibitor involved in tick feeding and Bartonella henselae infection.

Liu XY, de la Fuente J, Cote M, Galindo RC, Moutailler S, Vayssier-Taussat M, Bonnet SI - PLoS Negl Trop Dis (2014)

Bottom Line: IrSPI silencing impaired tick feeding, as well as resulted in reduced bacterial load in tick SGs.This study provides a comprehensive analysis of I. ricinus SG transcriptome and contributes significant genomic information about this important disease vector.This in-depth knowledge will enable a better understanding of the molecular interactions between ticks and tick-borne pathogens, and identifies IrSPI, a candidate to study now in detail to estimate its potentialities as vaccine against the ticks and the pathogens they transmit.

View Article: PubMed Central - PubMed

Affiliation: USC INRA Bartonella-Tiques, French National Institute of Agricultural Research (UMR BIPAR ENVA-ANSES-UPEC), Maisons-Alfort, France.

ABSTRACT
Ixodes ricinus is the most widespread and abundant tick in Europe, frequently bites humans, and is the vector of several pathogens including those responsible for Lyme disease, Tick-Borne Encephalitis, anaplasmosis, babesiosis and bartonellosis. These tick-borne pathogens are transmitted to vertebrate hosts via tick saliva during blood feeding, and tick salivary gland (SG) factors are likely implicated in transmission. In order to identify such tick factors, we characterized the transcriptome of female I. ricinus SGs using next generation sequencing techniques, and compared transcriptomes between Bartonella henselae-infected and non-infected ticks. High-throughput sequencing of I. ricinus SG transcriptomes led to the generation of 24,539 isotigs. Among them, 829 and 517 transcripts were either significantly up- or down-regulated respectively, in response to bacterial infection. Searches based on sequence identity showed that among the differentially expressed transcripts, 161 transcripts corresponded to nine groups of previously annotated tick SG gene families, while the others corresponded to genes of unknown function. Expression patterns of five selected genes belonging to the BPTI/Kunitz family of serine protease inhibitors, the tick salivary peptide group 1 protein, the salp15 super-family, and the arthropod defensin family, were validated by qRT-PCR. IrSPI, a member of the BPTI/Kunitz family of serine protease inhibitors, showed the highest up-regulation in SGs in response to Bartonella infection. IrSPI silencing impaired tick feeding, as well as resulted in reduced bacterial load in tick SGs. This study provides a comprehensive analysis of I. ricinus SG transcriptome and contributes significant genomic information about this important disease vector. This in-depth knowledge will enable a better understanding of the molecular interactions between ticks and tick-borne pathogens, and identifies IrSPI, a candidate to study now in detail to estimate its potentialities as vaccine against the ticks and the pathogens they transmit.

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Gene ontology assignments of transcripts expressed in B. henselae-infected and non-infected I. ricinus female salivary glands: A) Biological progresses, B) Cellular components, C) Molecular functions.
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pntd-0002993-g003: Gene ontology assignments of transcripts expressed in B. henselae-infected and non-infected I. ricinus female salivary glands: A) Biological progresses, B) Cellular components, C) Molecular functions.

Mentions: The database of Blast results was then used to annotate the isotigs with GO terms. Isotigs were classified according to the categories of biological processes (BP) in which they may be implicated, the cellular components (CC) with which they may be linked, or a related molecular function (MF). One or more GO IDs were assigned to 10,859 (44.3%) isotigs. The number of isotigs that could be annotated as belonging to either BP, CC and MF categories were 5,308, 7,213 and 9,283, respectively. In the BP category, ‘oxidation reduction’ (12.8%) was the most abundant GO term, followed by ‘proteolysis’ (9.7%) (Figure 3A). In the CC category, the most abundant term was ‘integral to membrane’ (11.4%), followed by ‘nucleus’ (8.1%), ‘cytosol’ (7.7%) and ‘cytoplasm localization’ (7.4%) (Figure 3B). In the MF category, the most abundant term was ‘binding proteins’ (63.2%) (Figure 3C).


IrSPI, a tick serine protease inhibitor involved in tick feeding and Bartonella henselae infection.

Liu XY, de la Fuente J, Cote M, Galindo RC, Moutailler S, Vayssier-Taussat M, Bonnet SI - PLoS Negl Trop Dis (2014)

Gene ontology assignments of transcripts expressed in B. henselae-infected and non-infected I. ricinus female salivary glands: A) Biological progresses, B) Cellular components, C) Molecular functions.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4109860&req=5

pntd-0002993-g003: Gene ontology assignments of transcripts expressed in B. henselae-infected and non-infected I. ricinus female salivary glands: A) Biological progresses, B) Cellular components, C) Molecular functions.
Mentions: The database of Blast results was then used to annotate the isotigs with GO terms. Isotigs were classified according to the categories of biological processes (BP) in which they may be implicated, the cellular components (CC) with which they may be linked, or a related molecular function (MF). One or more GO IDs were assigned to 10,859 (44.3%) isotigs. The number of isotigs that could be annotated as belonging to either BP, CC and MF categories were 5,308, 7,213 and 9,283, respectively. In the BP category, ‘oxidation reduction’ (12.8%) was the most abundant GO term, followed by ‘proteolysis’ (9.7%) (Figure 3A). In the CC category, the most abundant term was ‘integral to membrane’ (11.4%), followed by ‘nucleus’ (8.1%), ‘cytosol’ (7.7%) and ‘cytoplasm localization’ (7.4%) (Figure 3B). In the MF category, the most abundant term was ‘binding proteins’ (63.2%) (Figure 3C).

Bottom Line: IrSPI silencing impaired tick feeding, as well as resulted in reduced bacterial load in tick SGs.This study provides a comprehensive analysis of I. ricinus SG transcriptome and contributes significant genomic information about this important disease vector.This in-depth knowledge will enable a better understanding of the molecular interactions between ticks and tick-borne pathogens, and identifies IrSPI, a candidate to study now in detail to estimate its potentialities as vaccine against the ticks and the pathogens they transmit.

View Article: PubMed Central - PubMed

Affiliation: USC INRA Bartonella-Tiques, French National Institute of Agricultural Research (UMR BIPAR ENVA-ANSES-UPEC), Maisons-Alfort, France.

ABSTRACT
Ixodes ricinus is the most widespread and abundant tick in Europe, frequently bites humans, and is the vector of several pathogens including those responsible for Lyme disease, Tick-Borne Encephalitis, anaplasmosis, babesiosis and bartonellosis. These tick-borne pathogens are transmitted to vertebrate hosts via tick saliva during blood feeding, and tick salivary gland (SG) factors are likely implicated in transmission. In order to identify such tick factors, we characterized the transcriptome of female I. ricinus SGs using next generation sequencing techniques, and compared transcriptomes between Bartonella henselae-infected and non-infected ticks. High-throughput sequencing of I. ricinus SG transcriptomes led to the generation of 24,539 isotigs. Among them, 829 and 517 transcripts were either significantly up- or down-regulated respectively, in response to bacterial infection. Searches based on sequence identity showed that among the differentially expressed transcripts, 161 transcripts corresponded to nine groups of previously annotated tick SG gene families, while the others corresponded to genes of unknown function. Expression patterns of five selected genes belonging to the BPTI/Kunitz family of serine protease inhibitors, the tick salivary peptide group 1 protein, the salp15 super-family, and the arthropod defensin family, were validated by qRT-PCR. IrSPI, a member of the BPTI/Kunitz family of serine protease inhibitors, showed the highest up-regulation in SGs in response to Bartonella infection. IrSPI silencing impaired tick feeding, as well as resulted in reduced bacterial load in tick SGs. This study provides a comprehensive analysis of I. ricinus SG transcriptome and contributes significant genomic information about this important disease vector. This in-depth knowledge will enable a better understanding of the molecular interactions between ticks and tick-borne pathogens, and identifies IrSPI, a candidate to study now in detail to estimate its potentialities as vaccine against the ticks and the pathogens they transmit.

Show MeSH
Related in: MedlinePlus