Tick-susceptible Bos taurus cattle display an increased cellular response at the site of larval Rhipicephalus (Boophilus) microplus attachment, compared with tick-resistant Bos indicus cattle
Introduction
Cattle demonstrate divergent and heritable phenotypes of resistance and susceptibility to infestation with the cattle tick Rhipicephalus (Boophilus) microplus (formerly Boophilus microplus) (Wharton et al., 1970, Utech et al., 1978b). It is well documented that Bos indicus breeds are generally more resistant to tick infestation than Bos taurus breeds; however, large variations in resistance can occur within breed (Seifert, 1970). Although it is known that the expression of tick resistance can be affected by many factors including age, sex and season (Utech et al., 1978a, Doube and Wharton, 1980, Sutherst et al., 1983), the processes responsible for conferring high levels of tick resistance in B. indicus breeds are yet to be fully described. Elucidating the mechanisms by which resistant animals prevent heavy tick infestation is a crucial step in the development of predictive biomarkers for tick resistance for use in selective breeding programs, and is also potentially useful for the development of anti-tick vaccines.
Previous research concerning immune responses in the skin of tick-infested cattle has associated a strong hypersensitivity reaction with increased tick resistance in B. taurus cattle (Schleger et al., 1976, Schleger et al., 1981, Kemp et al., 1983), involving the infiltration of eosinophils and concentration of histamine at the tick-attachment site. Kemp and Bourne (1980) demonstrated a direct effect of histamine on larval attachment by injecting it underneath attached larvae; however, it was noted that the sensitivity of larvae to histamine injection decreases as larval attachments stabilise. Tatchell and Moorhouse (1968) conducted a comprehensive histological study of skin sections from B. taurus and B. indicus hosts to which different instars (larvae, nymph and adult) of R. microplus were attached. This study showed that although the feeding lesion beneath nymphal and adult tick stages were similar in resistant and susceptible hosts, the early eosinophil response to larval attachment developed to a much greater extent in the majority of B. taurus hosts than in B. indicus cattle. The authors suggested that this vigorous response by the susceptible animals functioned to create a more favourable environment for the tick, through the increase of available tissue fluids, mediated by increased capillary permeability (Tatchell and Moorhouse, 1968).
Wang et al. (2007) employed an in-house microarray constructed from a bovine skin cDNA library to analyse changes in gene expression in the skin of high-resistance and low-resistance B. taurus (Hereford × Shorthorn) cattle following tick exposure. The number of cattle used in this study was low, as was the difference between designated high- and low-resistance groups (95–99% resistant); however, the authors were able to document differential gene expression between high- and low-resistance groups following larval R. microplus infestation. The authors reported that many differentially expressed genes indicated a suppression of the cell-mediated inflammatory response and restriction of blood flow in resistant animals (Wang et al., 2007).
We have previously reported on gene expression in the skin of highly tick-resistant Brahman (B. indicus) and tick-susceptible Holstein–Friesian (B. taurus) cattle using quantitative PCR (qPCR) (Piper et al., 2008). Forty-four genes were chosen for study including those involved in innate immune responses and some genes suggested to be involved in tick resistance by Wang et al. (2007). Fifteen genes were more highly expressed in skin samples from Holstein–Friesian animals compared with samples from Brahman animals, suggesting an increased cell-mediated inflammatory response at the tick-attachment site in the susceptible Holstein–Friesian animals (Piper et al., 2008). We concluded from this study that the mechanism by which resistant B. indicus animals acquire and sustain high levels of tick resistance is different from the cell-mediated hypersensitivity-type reaction considered to be important for resistance to infestation in B. taurus breeds.
We report herein the results of a study examining global gene expression in the skin of tick-naïve and tick-infested Holstein–Friesian and Brahman cattle using the commercially available Affymetrix bovine whole-genome microarray platform, together with histological examination of skin sections taken from tick-infested animals.
Section snippets
Animals and treatment
Methods regarding the artificial infestations and tick counting procedures undertaken on the tick-infested Holstein–Friesian (B. taurus) and Brahman (B. indicus) cattle used in this study have been described in detail elsewhere (Piper et al., 2008). Briefly, six Holstein–Friesian and six Brahman heifers aged 6 months (±1 month) with previous exposure to R. microplus were artificially infested with 10,000 R. microplus larvae each, weekly for 7 weeks. The larvae used to artificially infest the
Tick counts
Weekly tick counts demonstrated that the tick-infested Brahman heifers carried significantly fewer ticks (P < 0.001) than the tick-infested Holstein–Friesian heifers throughout the duration of the trial (Piper et al., 2008). The mean number of ticks carried by the infested Brahman animals was 15 ticks per side (±14) while the mean number of ticks carried by the infested Holstein–Friesian animals was 151 per side (±36). The three Brahman animals used in the microarray analysis carried average tick
Discussion
The present study demonstrates that the expression of many genes is differentially regulated in the skin of cattle following infestation with the cattle tick, R. microplus. The cattle in this study demonstrated divergent phenotypes with respect to host resistance to tick infestation, and changes in gene expression and cell populations in the skin following tick infestation. The skin was chosen as the subject of this experiment as it is the immediate interface between the tick and the host;
Acknowledgements
The authors gratefully acknowledge funding by the Cooperative Research Centre for Beef Genetic Technologies (Beef CRC). The authors thank Tom Connolly and Mathew Verri (The University of Queensland) for their care of the animals in this project and assistance with sample collection, and Laercio Porto-Neto (The University of Queensland) for assistance with sample collection. Thanks are also extended to Ralph Stutchbury (QPIF) for preparation of tick larvae, and the Animal Genetics Laboratory at
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Tick host immunity: vector immunomodulation and acquired tick resistance
2021, Trends in ImmunologyCitation Excerpt :Furthermore, some animals display hereditary resistance to ticks, as seen in Bos taurus indicus cattle when infested with R. microplus or other ticks, as evidenced from tick counts on naturally exposed animals, serum complement amounts, and delayed skin hypersensitivity [122]; however, the precise genetic or immunological basis for such resistance remains unknown [99–101,123,124]. Moreover, differential infiltration of immune cells such as eosinophils, mast cells, macrophages, and plasma cells has been reported in the skin of sensitive versus resistant cattle [100], including inflammatory episodes such as cutaneous basophil hypersensitivity [98], skin degradation, and cytokine signaling [99]; in addition, major events of skin remodeling, particularly involving components of the dermal extracellular matrix, have also been noted [100]. However, research has yet to identify the specific tick proteins that can trigger the inflammatory reactions associated with ATR in incidental hosts or genetically resistant cows; nevertheless, it is reasonable to speculate that these antigens might include saliva components, as highlighted by recent studies showing that immunization of guinea pigs with isolated I. scapularis saliva [102], or even one of its fractions containing 24 identified proteins, induced partial ATR against subsequent challenge with nymphal ticks [102,104].
Distinct immune response profile during rhipicephalus (boophilus) microplus infestations of guzerat dairy herd according to the maternal lineage ancestry (mitochondrial DNA)
2019, Veterinary ParasitologyCitation Excerpt :Our results that clearly showed that B. indicus developed an immune response more efficient and earlier than B. taurus, corroborate their findings. On the other hand, Piper et al. (2010) and Tatchell and Moorhouse (1968), showed from both histological and whole genome expression studies of skin sections from these animals that the B. taurus host elicits a more vigorous cellular response at the site of tick attachment. Differences between the present data set and the results of others may be attributed to the time post tick exposure that the cells are isolated from the host and also that the majority of the studies were evaluating the tick-attachment site (skin), while the present work evaluated the peripheral blood.