Knockdown of the Rhipicephalus microplus Cytochrome c Oxidase Subunit III Gene Is Associated with a Failure of Anaplasma marginale Transmission

Bifano, Thaís D.; Ueti, Massaro W.; Esteves, Eliane; Reif, Kathryn E.; Braz, Glória R.C.; Scoles, Glen A.; Bastos, Reginaldo G.; White, Stephen N.; Daffre, Sirlei

doi:10.1371/journal.pone.0098614

Cited by 15 publications

(11 citation statements)

References 56 publications

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“…Clones that code for mitochondrial cytochrome C oxidase subunits I and III appeared at least 10 times. Cytochrome C oxidase, a key mitochondrial enzyme in the respiratory chain, was shown to be important for the transmission of Anaplasma marginale 7 . Several genes coding for the short-chain dehydrogenase family of proteins involved in the metabolism of amino acids, lipids or sugars 8 and for proteins involved in defense responses 9 , bloodmeal digestion 10 , detoxification of endo and xenobiotics 11 , complement inhibition 12 , lipid transport 13 , actin assembly, cell signaling 14 – 16 and for proteins paralogous to secreted salivary proteins including Salp26A 17 were also upregulated by the presence of Borrelia in the tick gut (Supplementary Table 1 ).…”

Section: Resultsmentioning

confidence: 99%

Modulation of the tick gut milieu by a secreted tick protein favors Borrelia burgdorferi colonization

et al. 2017

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The Lyme disease agent, Borrelia burgdorferi, colonizes the gut of the tick Ixodes scapularis, which transmits the pathogen to vertebrate hosts including humans. Here we show that B. burgdorferi colonization increases the expression of several tick gut genes including pixr, encoding a secreted gut protein with a Reeler domain. RNA interference-mediated silencing of pixr, or immunity against PIXR in mice, impairs the ability of B. burgdorferi to colonize the tick gut. PIXR inhibits bacterial biofilm formation in vitro and in vivo. Abrogation of PIXR function in vivo results in alterations in the gut microbiome, metabolome and immune responses. These alterations influence the spirochete entering the tick gut in multiple ways. PIXR abrogation also impairs larval molting, indicative of its role in tick biology. This study highlights the role of the tick gut in actively managing its microbiome, and how this impacts B. burgdorferi colonization of its arthropod vector.

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Section: Resultsmentioning

confidence: 99%

Modulation of the tick gut milieu by a secreted tick protein favors Borrelia burgdorferi colonization

et al. 2017

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“…Intriguingly, the knockdown of CYP by RNAi reduced the infection of the mosquito Anopheles gambiae by Plasmodium berghei (Felix and Silveira, 2011). GSTs, which are involved in the detoxification of xenobiotics and oxidative stress (Pavlidi et al, 2018), were also previously reported to be upregulated by infection in arthropods, such as ticks (Mulenga et al, 2003; Mercado-Curiel et al, 2011; Bifano et al, 2014). For instance, one CDS of glutathione S -transferase was upregulated in the cell line BME26 of R. microplus and also in both MG and SG adult males by infection with Anaplasma marginale , the causative agent of bovine anaplasmosis.…”

Section: Discussionmentioning

confidence: 99%

“…For instance, one CDS of glutathione S -transferase was upregulated in the cell line BME26 of R. microplus and also in both MG and SG adult males by infection with Anaplasma marginale , the causative agent of bovine anaplasmosis. However, GST knockdown induced by RNAi presented no effect in either the acquisition of A. marginale by ticks or transmission to calves (Bifano et al, 2014). On the other hand, GST-knockdown reduced the acquisition of A. marginale by the tick D. variabilis , suggesting that the susceptibility response obtained by GST-silencing depends on the tick species and/or the pathogen strain (Kocan et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

The Transcriptome of the Salivary Glands of Amblyomma aureolatum Reveals the Antimicrobial Peptide Microplusin as an Important Factor for the Tick Protection Against Rickettsia rickettsii Infection

et al. 2019

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The salivary glands (SG) of ixodid ticks play a pivotal role in blood feeding, producing both the cement and the saliva. The cement is an adhesive substance that helps the attachment of the tick to the host skin, while the saliva contains a rich mixture of antihemostatic, anti-inflammatory, and immunomodulatory substances that allow ticks to properly acquire the blood meal. The tick saliva is also a vehicle used by several pathogens to be transmitted to the vertebrate host, including various bacterial species from the genus Rickettsia . Rickettsia rickettsii is a tick-borne obligate intracellular bacterium that causes the severe Rocky Mountain spotted fever. In Brazil, the dog yellow tick Amblyomma aureolatum is a vector of R. rickettsii . In the current study, the effects of an experimental infection with R. rickettsii on the global gene expression profile of A. aureolatum SG was determined by next-generation RNA sequencing. A total of 260 coding sequences (CDSs) were modulated by infection, among which 161 were upregulated and 99 were downregulated. Regarding CDSs in the immunity category, we highlight one sequence encoding one microplusin-like antimicrobial peptide (AMP) (Ambaur-69859). AMPs are important effectors of the arthropod immune system, which lack the adaptive response of the immune system of vertebrates. The expression of microplusin was confirmed to be significantly upregulated in the SG as well as in the midgut (MG) of infected A. aureolatum by a quantitative polymerase chain reaction preceded by reverse transcription. The knockdown of the microplusin expression by RNA interference caused a significant increase in the prevalence of infected ticks in relation to the control. In addition, a higher rickettsial load of one order of magnitude was recorded in both the MG and SG of ticks that received microplusin-specific dsRNA. No effect of microplusin knockdown was observed on the R. rickettsii transmission to rabbits. Moreover, no significant differences in tick engorgement and oviposition were recorded in ticks that received dsMicroplusin, demonstrating that microplusin knockdown has no effect on tick fitness. Further studies must be performed to determine the mechanism of action of this AMP against R. rickettsii .

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“…The total number of A. marginale in tick midguts and salivary glands was quantified by qPCR using genomic DNA as template, specific primers ( Supplementary Table 1), and a TaqMan probe that targeted msp5, as detailed by (Bifano et al, 2014).…”

Section: Quantitative Pcr (Qpcr)mentioning

confidence: 99%

The transcription factor Relish controls Anaplasma marginale infection in the bovine tick Rhipicephalus microplus

Capelli-Peixoto

Carvalho²,

Johnson

et al. 2017

Developmental & Comparative Immunology

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Rhipicephalus microplus is an important biological vector of Anaplasma marginale, the etiological agent of bovine anaplasmosis. The knowledge of tick immune responses to control bacterial infections remains limited. In this study, we demonstrate that transcription factor Relish from the IMD signaling pathway has an important role in the control of A. marginale infection in ticks. We found that RNA-mediated silencing of Relish caused a significant increase in the number of A. marginale in the midgut and salivary glands of R. microplus. In addition, the IMD pathway regulates the expression of the gene that encodes the antimicrobial peptide (AMP) microplusin. Moreover, microplusin expression was up-regulated in the midgut (2×) and salivary glands (8×) of A. marginale infected R. microplus. Therefore, it is plausible to hypothesize that microplusin may be involved in the A. marginale control. This study provides the first evidence of IMD signaling pathway participation on the A. marginale control in R. microplus.

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Knockdown of the Rhipicephalus microplus Cytochrome c Oxidase Subunit III Gene Is Associated with a Failure of Anaplasma marginale Transmission

Cited by 15 publications

References 56 publications

Modulation of the tick gut milieu by a secreted tick protein favors Borrelia burgdorferi colonization

Modulation of the tick gut milieu by a secreted tick protein favors Borrelia burgdorferi colonization

The Transcriptome of the Salivary Glands of Amblyomma aureolatum Reveals the Antimicrobial Peptide Microplusin as an Important Factor for the Tick Protection Against Rickettsia rickettsii Infection

The transcription factor Relish controls Anaplasma marginale infection in the bovine tick Rhipicephalus microplus

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