Expression profiling, gene silencing and transcriptional networking of metzincin metalloproteases in the cattle tick, Rhipicephalus (Boophilus) microplus

Barnard, Annette-Christi; Nijhof, Ard M.; Gaspar, Anabella R. M.; Neitz, A.W.H.; Jongejan, Frans; Maritz-Olivier, Christine

doi:10.1016/j.vetpar.2011.11.026

Cited by 31 publications

(27 citation statements)

References 39 publications

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“…Expression of metalloproteases in tick salivary glands has been widely reported [114–116], with RNAi silencing of some affecting tick feeding efficiency and fertility in R. microplus [117] and I. ricinus [118], while feeding ticks on rabbits immunized with a recombinant tick metalloprotease affected H. longicornis tick feeding efficiency [119]. In a lone study, an I. scapularis recombinant metalloprotease similar to reprolysin had gelatinase and fibrinolytic activities [120].…”

Section: Resultsmentioning

confidence: 99%

A 24-48 h fed Amblyomma americanum tick saliva immuno-proteome

et al. 2014

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BackgroundMultiple tick saliva proteins, the majority of which are unknown, confer tick resistance in repeatedly infested animals. The objective of this study was to identify the 24-48 h fed Amblyomma americanum tick saliva immuno-proteome. The 24-48 h tick-feeding phase is critical to tick parasitism as it precedes important events in tick biology, blood meal feeding and disease agent transmission. Fed male, 24 and 96 h fed female phage display cDNA expression libraries were biopanned using rabbit antibodies to 24 and 48 h fed A. americanum female tick saliva proteins. Biopanned immuno-cDNA libraries were subjected to next generation sequencing, de novo assembly, and bioinformatic analysis.ResultsMore than 800 transcripts that code for 24-48 h fed A. americanum immuno-proteins are described. Of the 895 immuno-proteins, 52% (464/895) were provisionally identified based on matches in GenBank. Of these, ~19% (86/464) show high level of identity to other tick hypothetical proteins, and the rest include putative proteases (serine, cysteine, leukotriene A-4 hydrolase, carboxypeptidases, and metalloproteases), protease inhibitors (serine and cysteine protease inhibitors, tick carboxypeptidase inhibitor), and transporters and/or ligand binding proteins (histamine binding/lipocalin, fatty acid binding, calreticulin, hemelipoprotein, IgG binding protein, ferritin, insulin-like growth factor binding proteins, and evasin). Others include enzymes (glutathione transferase, cytochrome oxidase, protein disulfide isomerase), ribosomal proteins, and those of miscellaneous functions (histamine release factor, selenoproteins, tetraspanin, defensin, heat shock proteins).ConclusionsData here demonstrate that A. americanum secretes a complex cocktail of immunogenic tick saliva proteins during the first 24-48 h of feeding. Of significance, previously validated immunogenic tick saliva proteins including AV422 protein, calreticulin, histamine release factor, histamine binding/lipocalins, selenoproteins, and paramyosin were identified in this screen, supporting the specificity of the approach in this study. While descriptive, this study opens opportunities for in-depth tick feeding physiology studies.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-518) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

A 24-48 h fed Amblyomma americanum tick saliva immuno-proteome

et al. 2014

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“…No implication in a potential biological pathway could be identified for any other isotig in this group. Metalloproteases have been described in the SGs of I. scapularis [53], I. ricinus [54], Haemaphysalis longicornis [55] and R. microplus [56], and have not been described in other hard tick tissues. The role of SG metalloproteinases in tick feeding is thought to be linked to anti-fibrinogen, anti-febrin and anti-hemostatic activities [53].…”

Section: Zinc-dependent Metalloproteases Familymentioning

confidence: 98%

IrSPI, a Tick Serine Protease Inhibitor Involved in Tick Feeding and Bartonella henselae Infection

et al. 2014

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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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“…Metzincin MPs members have been found to participate in tissue development, maintenance, remodeling, and in unspecific protein degradation of intake proteins (Gomis-Ruth, 2009;Rivera et al, 2010). MPs have been identified in various tick species, and are considered crucial for maintenance of blood meal related functions (Francischetti et al, 2003;Harnnoi et al, 2007;Decrem et al, 2008a;Barnard et al, 2012). The up-regulation of MPs transcription in salivary glands has been correlated with tick blood feeding (Francischetti et al, 2003;Harnnoi et al, 2007;Decrem et al, 2008aDecrem et al, , 2008bBarnard et al, 2012;Adamson et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…MPs have been identified in various tick species, and are considered crucial for maintenance of blood meal related functions (Francischetti et al, 2003;Harnnoi et al, 2007;Decrem et al, 2008a;Barnard et al, 2012). The up-regulation of MPs transcription in salivary glands has been correlated with tick blood feeding (Francischetti et al, 2003;Harnnoi et al, 2007;Decrem et al, 2008aDecrem et al, , 2008bBarnard et al, 2012;Adamson et al, 2013). In Ixodes scapularis, MPs are secreted in saliva, playing an essential role in fibrin and fibrinogen breakdown (Francischetti et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

“…Despite the characterization of some tick MPs (Francischetti et al, 2003;Harnnoi et al, 2007;Decrem et al, 2008aDecrem et al, , 2008bBarnard et al, 2012;Adamson et al, 2013), vaccination trials against R. microplus infestation using these proteins as antigen remains to be evaluated. It has been speculated that the cysteine-rich domain in MPs is a limiting factor in the recombinant production of these proteins by prokaryotes (Ramos and SelistreDe-Araujo, 2006), since a native-like conformation of recombinant MPs is supposed to be critical -as far as retaining immunogenic properties is concerned.…”

Section: Introductionmentioning

confidence: 99%

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Immunoprotective potential of a Rhipicephalus (Boophilus) microplus metalloprotease

Ali

Parizi

Guizzo

et al. 2015

Veterinary Parasitology

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Ticks have serious impacts on animal and human health, causing significant economic losses in cattle breeding. Besides damage due to the hematophagous behavior, they transmit several pathogens. Low cost and environmental safety have made vaccines a promising alternative control method against tick infestation. Metalloproteases (MPs) have been shown to be essential for diverse biological functions in hematophagous organisms, inhibiting blood clotting, degrading extracellular matrix proteins, and inhibiting host tissue repair via anti-angiogenic activity. In this study, we analyzed the immunoprotective potential of a recombinant MP against Rhipicephalus (Boophilus) microplus infestation. First, a cDNA encoding R. microplus amino acids sequence with highly conserved regions of the metzincin (reprolysin) group of MP was identified (BrRm-MP4). After expression and purification, recombinant BrRm-MP4 was used as a vaccinal antigen against R. microplus infestation in cattle (Bos taurus taurus). All vaccinated bovines developed immune response to the antigen, resulting in increased antibody level throughout the immunization protocol. Immunization with rBrRm-MP4 reduced tick feeding success, decreasing the number of engorged females and their reproduction potential, representing a 60% overall protection. These results show that rBrRm-MP4 provides protection against tick infestation, placing it is a potential candidate for an anti-tick vaccine.

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Expression profiling, gene silencing and transcriptional networking of metzincin metalloproteases in the cattle tick, Rhipicephalus (Boophilus) microplus

Cited by 31 publications

References 39 publications

A 24-48 h fed Amblyomma americanum tick saliva immuno-proteome

A 24-48 h fed Amblyomma americanum tick saliva immuno-proteome

IrSPI, a Tick Serine Protease Inhibitor Involved in Tick Feeding and Bartonella henselae Infection

Immunoprotective potential of a Rhipicephalus (Boophilus) microplus metalloprotease

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