Immune and biochemical responses in skin differ between bovine hosts genetically susceptible and resistant to the cattle tick Rhipicephalus microplus

Abstract

BackgroundTicks attach to and penetrate their hosts’ skin and inactivate multiple components of host responses in order to acquire a blood meal. Infestation loads with the cattle tick, Rhipicephalus microplus, are heritable: some breeds carry high loads of reproductively successful ticks, whereas in others, few ticks feed and reproduce efficiently.MethodsIn order to elucidate the mechanisms that result in the different outcomes of infestations with cattle ticks, we examined global gene expression and inflammation induced by tick bites in skins from one resistant and one susceptible breed of cattle that underwent primary infestations with larvae and nymphs of R. microplus. We also examined the expression profiles of genes encoding secreted tick proteins that mediate parasitism in larvae and nymphs feeding on these breeds.ResultsFunctional analyses of differentially expressed genes in the skin suggest that allergic contact-like dermatitis develops with ensuing production of IL-6, CXCL-8 and CCL-2 and is sustained by HMGB1, ISG15 and PKR, leading to expression of pro-inflammatory chemokines and cytokines that recruit granulocytes and T lymphocytes. Importantly, this response is delayed in susceptible hosts. Histopathological analyses of infested skins showed inflammatory reactions surrounding tick cement cones that enable attachment in both breeds, but in genetically tick-resistant bovines they destabilized the cone. The transcription data provided insights into tick-mediated activation of basophils, which have previously been shown to be a key to host resistance in model systems. Skin from tick-susceptible bovines expressed more transcripts encoding enzymes that detoxify tissues. Interestingly, these enzymes also produce volatile odoriferous compounds and, accordingly, skin rubbings from tick-susceptible bovines attracted significantly more tick larvae than rubbings from resistant hosts. Moreover, transcripts encoding secreted modulatory molecules by the tick were significantly more abundant in larval and in nymphal salivary glands from ticks feeding on susceptible bovines.ConclusionsCompared with tick-susceptible hosts, genes encoding enzymes producing volatile compounds exhibit significantly lower expression in resistant hosts, which may render them less attractive to larvae; resistant hosts expose ticks to an earlier inflammatory response, which in ticks is associated with significantly lower expression of genes encoding salivary proteins that suppress host immunity, inflammation and coagulation.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1945-z) contains supplementary material, which is available to authorized users.

Cattle Tick Rhipicephalus microplus-Host Interface: A Review of Resistant and Susceptible Host Responses

“…This finding is consistent with the theory associated with odor (Osterkamp et al, 1999 ) described above. The study also reported that resistant hosts when exposed to ticks mount an earlier inflammatory response than susceptible cattle (gene expression studies undertaken at 2 days post larval infestation using tick naïve cattle) (Franzin et al, 2017 ) which appears to disappear later (feeding nymphs at 9 days) but lingers in susceptible cattle.…”

“…Conversely, in susceptible cattle ( B. t. taurus Holstein) the acute phase response appeared impaired but this study confirmed the up-regulation of calcium ion control genes which correlates with the calcium binding proteins reported by Nascimento et al ( 2010 ). Franzin et al ( 2017 ) also report the up-regulation of protein S100G, another calcium binding protein, in susceptible cattle. An earlier qPCR study showed higher up-regulation of calcium signaling genes in a tick resistant composite breed in response to ticks most predominantly at 24 h post-infestation with larvae (Belmont Red) (Bagnall et al, 2009 ).…”

“…Another host gene expression study was reported recently demonstrating that resistant cattle ( B. t. indicus Nelore breed) up-regulated the expression of fewer genes encoding enzymes producing volatile compounds that render them less “attractive” to ticks compared with susceptible cattle ( B. t. taurus Holstein breed) (Franzin et al, 2017 ). This finding is consistent with the theory associated with odor (Osterkamp et al, 1999 ) described above.…”

Gene Expression in the Salivary Gland of Rhipicephalus (Boophilus) microplus Fed on Tick-Susceptible and Tick-Resistant Hosts

“…In this way, bovine European breeds (Bos taurus) and their industrial crossbreeds are more susceptible to tick infestations than B. indicus. This resistance is associated with the immune systems of the hosts, since in the first infestation, the number of ticks completing the cycle is similar in all races (Hewetson, 1972;Mattioli et al, 1993;Ghosh et al, 1999), and with the absence of transcripts of genes encoding enzymes producing volatile compounds, which may render the host less attractive to larvae (Franzin et al, 2017). Franzin et al (2017) concluded that resistant hosts expose ticks to an earlier inflammatory response, which in ticks is associated with significantly lower expression of genes encoding salivary proteins that suppress host immunity, inflammation and coagulation.…”

Vacina multicomponente recombinante baseada em antígenos secretados por Rhipicephalus microplus induz imunidade protetora contra carrapatos em bovinos e cães

“…cada ponto representa o peso das larvas eclodidas por alíquota de 1g de ovos. A ocorrência de moléculas ligantes de imunoglobulinas na saliva dos carrapatos capazes de sequestrar e remover anticorpos da hemolinfa 86 Franzin e colaboradores 144 50,159 . O uso de bases de dados de carrapatos relacionados apresenta-se como uma alternativa para a seleção de antígenos vacinais para R. sanguineus através da função predita in silico.…”