Tick host immunity: vector immunomodulation and acquired tick resistance

Kitsou, Chrysoula; Fikrig, Erol; Pal, Utpal

doi:10.1016/j.it.2021.05.005

Cited by 34 publications

(23 citation statements)

References 171 publications

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“…Female cattle ticks have an average parasitic phase of ~ 21 days on the host. During this period, the ticks secrete a diverse range of bioactive molecules to modulate host responses in order to achieve feeding success and survival [ 11 ]. This complex range of secreted protein and non-protein tick salivary molecules has been reviewed elsewhere [ 12 ].…”

Section: Introductionmentioning

confidence: 99%

“…Some of the host processes that are known to be disrupted by the hematophagy of cattle ticks include blood coagulation, cytokine secretion, cell adhesion, as well as leukocyte recruitment to the feeding site. Conversely, host resistance in cattle manifests by preventing attachment of tick larvae, which results in early larval death, as well as limiting hematophagy, thus reducing the reproductive success of the female adult ticks [ 11 ].…”

Section: Introductionmentioning

confidence: 99%

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Transcriptional changes in the peripheral blood leukocytes from Brangus cattle before and after tick challenge with Rhipicephalus australis

et al. 2022

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Background Disease emergence and production loss caused by cattle tick infestations have focused attention on genetic selection strategies to breed beef cattle with increased tick resistance. However, the mechanisms behind host responses to tick infestation have not been fully characterised. Hence, this study examined gene expression profiles of peripheral blood leukocytes from tick-naive Brangus steers (Bos taurus x Bos indicus) at 0, 3, and 12 weeks following artificial tick challenge experiments with Rhipicephalus australis larvae. The aim of the study was to investigate the effect of tick infestation on host leukocyte response to explore genes associated with the expression of high and low host resistance to ticks. Results Animals with high (HR, n = 5) and low (LR, n = 5) host resistance were identified after repeated tick challenge. A total of 3644 unique differentially expressed genes (FDR < 0.05) were identified in the comparison of tick-exposed (both HR and LR) and tick-naive steers for the 3-week and 12-week infestation period. Enrichment analyses showed genes were involved in leukocyte chemotaxis, coagulation, and inflammatory response. The IL-17 signalling, and cytokine-cytokine interactions pathways appeared to be relevant in protection and immunopathology to tick challenge. Comparison of HR and LR phenotypes at timepoints of weeks 0, 3, and 12 showed there were 69, 8, and 4 differentially expressed genes, respectively. Most of these genes were related to immune, tissue remodelling, and angiogenesis functions, suggesting this is relevant in the development of resistance or susceptibility to tick challenge. Conclusions This study showed the effect of tick infestation on Brangus cattle with variable phenotypes of host resistance to R. australis ticks. Steers responded to infestation by expressing leukocyte genes related to chemotaxis, cytokine secretion, and inflammatory response. The altered expression of genes from the bovine MHC complex in highly resistant animals at pre- and post- infestation stages also supports the relevance of this genomic region for disease resilience. Overall, this study offers a resource of leukocyte gene expression data on matched tick-naive and tick-infested steers relevant for the improvement of tick resistance in composite cattle.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Transcriptional changes in the peripheral blood leukocytes from Brangus cattle before and after tick challenge with Rhipicephalus australis

et al. 2022

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“…We previously found that mammalian IFN-γ acquired during a tick’s blood meal can trigger a potent antimicrobial response within the vector ( 21 ). As hematophagy in ticks originated with primeval vertebrates and evolved to include modern mammals ( 4 ), we explored whether the I. scapularis genome acquired a cytokine receptor that binds IFN-γ, such as through lateral gene transfer ( 22 ), with the ability to trigger immune signaling in ticks. We adopted an unbiased approach using coimmunoprecipitation (Co-IP) assay with whole tick lysates and mammalian IFN-γ as bait, coupled with mass spectrometry.…”

Section: Resultsmentioning

confidence: 99%

“…Blood meal ingestion is aided by bursts of cellular proliferation, differentiation, and hypertrophy, which are central to organ development. Host specialization in ticks ( 3 ), including highly evolved hematophagy, supports the tick’s unique physiological adaptations, particularly blood meal ingestion and storage, survivability through extended intermolt periods, and the maintenance of complex reproductive and developmental programs ( 4 ), the molecular aspects of which remain unknown.…”

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confidence: 99%

Dome1–JAK–STAT signaling between parasite and host integrates vector immunity and development

Rana

Kitsou

Dutta

et al. 2023

Science

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Ancestral signaling pathways serve critical roles in metazoan development, physiology, and immunity. We report an evolutionary interspecies communication pathway involving a central Ixodes scapularis tick receptor termed Dome1, which acquired a mammalian cytokine receptor motif exhibiting high affinity for interferon-gamma (IFN-γ). Host-derived IFN-γ facilitates Dome1-mediated activation of the Ixodes JAK–STAT pathway. This accelerates tick blood meal acquisition and development while upregulating antimicrobial components. The Dome1–JAK–STAT pathway, which exists in most Ixodid tick genomes, regulates the regeneration and proliferation of gut cells—including stem cells—and dictates metamorphosis through the Hedgehog and Notch–Delta networks, ultimately affecting Ixodes vectorial competence. We highlight the evolutionary dependence of I. scapularis on mammalian hosts through cross-species signaling mechanisms that dually influence arthropod immunity and development.

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“…There are various parallel proteins which directly or indirectly contribute to the natural cycle of B. burgdorfer iinfection. There is a need to identify discrete molecular interactions between spirochetes and tick components, which play critical roles in pathogen persistence and transmission by the arthropod vector [81] (table 4).…”

Section: Lyme Diseasementioning

confidence: 99%

Tick-Borne Zoonotic Diseases and Its Control

Yadav

Upadhyay

2022

Int J Pharm Pharm Sci

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The present review article explains different zoonotic diseases transmitted by various species of ticks. This article emphasizes various animal hosts, transmission and prevalence of various zoonotic diseases caused by a virus, bacteria, protozoans in different eco-climatic regions of the world. This article also explains various diagnostic methods applied for the detection of disease pathogens, treatment methods and prophylactic measures. It recommends tick saliva antigen-based oral vaccines and antibiotics as treatment methods. It also suggests use of various bait formulations and cultural control methods for deterring ticks from blood feeding. This article signifies the need of pesticides for control of ticks and tick-borne diseases.

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Tick host immunity: vector immunomodulation and acquired tick resistance

Cited by 34 publications

References 171 publications

Transcriptional changes in the peripheral blood leukocytes from Brangus cattle before and after tick challenge with Rhipicephalus australis

Transcriptional changes in the peripheral blood leukocytes from Brangus cattle before and after tick challenge with Rhipicephalus australis

Dome1–JAK–STAT signaling between parasite and host integrates vector immunity and development

Tick-Borne Zoonotic Diseases and Its Control

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