Tick–Host–Pathogen Interactions: Conflict and Cooperation

Fuente, José de la; Villar, Margarita; Cabezas-Cruz, Alejandro; Estrada-Peña, Agustı́n; Ayllón, Nieves; Alberdi, Pilar

doi:10.1371/journal.ppat.1005488

Cited by 89 publications

(89 citation statements)

References 26 publications

(58 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…These results suggested that a compensatory mechanism might exist by which A. phagocytophilum manipulates tick HMEs to regulate transcription and apoptosis in a tissue-specific manner to facilitate infection but preserving tick fitness to guarantee survival of both pathogens and ticks. 69 Similar to other biological processes involved in A. phagocytophilum infection, 14 these results also suggested that the pathogen manipulates arthropod and vertebrate host cell epigenetics in similar ways to inhibit host responses and facilitate infection. Investigating gene expression by epigenetic regulation and the relevance of HMEs in tick biology and pathogen infection is essential to advance our knowledge of tick-pathogen molecular interactions with possible implications for the identification of new targets for anti-tick drug and vaccine development.…”

Section: Discussionmentioning

confidence: 66%

“…14,18,19 However, the mechanisms by which A. phagocytophilum modifies gene expression or protein levels to inhibit apoptosis are not known but likely involve secreted bacterial effector proteins or the effect of tick response to infection that also results in apoptosis inhibition facilitating pathogen infection and multiplication. 69 It has been established that HMEs affect cell apoptosis. [60][61][62] The results obtained here showed that IsHDAC8 is involved in the regulation of apoptosis in tick cells (Fig.…”

Section: Functional Characterization Of Selected I Scapularis Hme Prmentioning

confidence: 99%

See 1 more Smart Citation

Anaplasma phagocytophilumincreases the levels of histone modifying enzymes to inhibit cell apoptosis and facilitate pathogen infection in the tick vectorIxodes scapularis

Cabezas-Cruz¹,

Alberdi²,

Ayllón³

et al. 2016

Epigenetics

Self Cite

View full text Add to dashboard Cite

Epigenetic mechanisms have not been characterized in ticks despite their importance as vectors of human and animal diseases worldwide. The objective of this study was to characterize the histones and histone modifying enzymes (HMEs) of the tick vector Ixodes scapularis and their role during Anaplasma phagocytophilum infection. We first identified 5 histones and 34 HMEs in I. scapularis in comparison with similar proteins in model organisms. Then, we used transcriptomic and proteomic data to analyze the mRNA and protein levels of I. scapularis histones and HMEs in response to A. phagocytophilum infection of tick tissues and cultured cells. Finally, selected HMEs were functionally characterized by pharmacological studies in cultured tick cells. The results suggest that A. phagocytophilum manipulates tick cell epigenetics to increase I. scapularis p300/CBP, histone deacetylase, and Sirtuin levels, resulting in an inhibition of cell apoptosis that in turn facilitates pathogen infection and multiplication. These results also suggest that a compensatory mechanism might exist by which A. phagocytophilum manipulates tick HMEs to regulate transcription and apoptosis in a tissue-specific manner to facilitate infection, but preserving tick fitness to guarantee survival of both pathogens and ticks. Our study also indicates that the pathogen manipulates arthropod and vertebrate cell epigenetics in similar ways to inhibit the host response to infection. Epigenetic regulation of tick biological processes is an essential element of the infection by A. phagocytophilum and the study of the mechanisms and principal actors involved is likely to provide clues for the development of anti-tick drugs and vaccines.

show abstract

Section: Discussionmentioning

confidence: 66%

Section: Functional Characterization Of Selected I Scapularis Hme Prmentioning

confidence: 99%

Anaplasma phagocytophilumincreases the levels of histone modifying enzymes to inhibit cell apoptosis and facilitate pathogen infection in the tick vectorIxodes scapularis

Cabezas-Cruz¹,

Alberdi²,

Ayllón³

et al. 2016

Epigenetics

Self Cite

View full text Add to dashboard Cite

show abstract

“…The conflict between ticks and hosts includes host local and systemic reactions to tick bite [31]. The comparative proteomics analysis showed the presence of tick proteins that react with IgE in patients but not control sera.…”

Section: Discussionmentioning

confidence: 99%

Tick-host conflict: immunoglobulin E antibodies to tick proteins in patients with anaphylaxis to tick bite

et al. 2017

Self Cite

View full text Add to dashboard Cite

Tick-borne infectious diseases and allergies are a growing problem worldwide. Tick bite allergy has been associated with the direct effect of immunoglobulin E (IgE) response to tick salivary antigens, or secondary to the induction of allergy to red meat consumption through IgE antibodies against the carbohydrate α-Gal (Gal α 1-3Gal β 1-(3)4GlcNAc-R). However, despite the growing burden of this pathology, the proteins associated with anaphylaxis to tick bite have not been characterized. To address this question, a comparative proteomics approach was used to characterize tick proteins producing an IgE antibody response in a healthy individual with record of tick bites, which had not resulted in any allergic reactions, and two patients with anaphylactic reactions to Rhipicephalus bursa or Hyalomma marginatum tick bites. Both patients and the healthy individual were red meat tolerant. The results supported a patient-specific IgE antibody response to tick species responsible for the anaphylaxis to tick bite. Both patients and the healthy individual serologically recognized tick proteins with and without α-Gal modifications, with proteins differentially recognized by patients but not control sera. These proteins could be used as potential antigens for diagnostics, treatment and prevention of tick bite-induced allergies.

show abstract

“…Given their overlapping life history strategies, vectors and pathogens form intimate relationships [85]. These tight relationships can evolve into positive [86][87][88][89][90][91][92] or negative [93][94][95][96][97][98] associations, with outcomes often varying based on the degree and duration of evolutionary association [89]. In laboratory experiments, B. burgdorferi infection has been shown to promote nymphal survival and host-seeking under suboptimal environmental conditions [99,100], suggesting a co-evolved mutualistic relationship.…”

Section: Discussionmentioning

confidence: 99%

Comparative vector competence of North American Lyme disease vectors

Couper

Yang

et al. 2020

Parasites Vectors

View full text Add to dashboard Cite

Background: Understanding the drivers of Lyme disease incidence at broad spatial scales is critical for predicting and mitigating human disease risk. Previous studies have identified vector phenology and behavior, host community composition, and landscape features as drivers of variable Lyme disease risk. However, while the Lyme disease transmission cycles in the eastern and western USA involve different vector species (Ixodes scapularis and Ixodes pacificus, respectively), the role of vector-specific differences in transmission efficiency has not been directly examined. By comparing the performance of traits involved in vector competence between these two species, this study aims to identify how vector competence contributes to variable Lyme disease risk. Methods:We used a suite of laboratory experiments to compare the performance of traits related to vector competence for the two USA Lyme disease vectors. For each species, we measured the rate of attachment to a common rodent host, the engorgement weight, and the efficiency of pathogen acquisition (host to tick) and pathogen transmission (tick to host) from laboratory mice. In measuring pathogen acquisition and transmission, we used two different pathogen strains, one sympatric with I. scapularis and one sympatric with I. pacificus, to assess the importance of vector-pathogen coevolutionary history in transmission dynamics. Results:We found I. pacificus had significantly higher host attachment success and engorgement weights, but significantly lower pathogen transmission efficiency relative to I. scapularis. Molting success and pathogen acquisition did not differ between these two species. However, pathogen acquisition efficiency was significantly higher for both sympatric vector and pathogen strains than the allopatric pairings. Conclusions:This study identified species-specific vector traits as a potential driver of broad scale variation in Lyme disease risk in the USA. In particular, the exceedingly low rates of pathogen transmission from tick to host observed for I. pacificus may limit Lyme disease transmission efficiency in the western USA. Further, observed variation in pathogen acquisition between sympatric and allopatric vector-pathogen strains indicate that vector-pathogen coevolutionary history may play a key role in transmission dynamics. These findings underscore the need to consider vector traits and vector-pathogen coevolution as important factors governing regional Lyme disease risk.

show abstract

Tick–Host–Pathogen Interactions: Conflict and Cooperation

Cited by 89 publications

References 26 publications

Anaplasma phagocytophilumincreases the levels of histone modifying enzymes to inhibit cell apoptosis and facilitate pathogen infection in the tick vectorIxodes scapularis

Anaplasma phagocytophilumincreases the levels of histone modifying enzymes to inhibit cell apoptosis and facilitate pathogen infection in the tick vectorIxodes scapularis

Tick-host conflict: immunoglobulin E antibodies to tick proteins in patients with anaphylaxis to tick bite

Comparative vector competence of North American Lyme disease vectors

Contact Info

Product

Resources

About