Abstract
The porin gene is widely disseminated in various organisms and has a pivotal role in the regulation of pathogen infection in blood-sucking arthropods. However, to date, information on the porin gene from the Haemaphysalis longicornis tick, an important vector of human and animal diseases, remains unknown. In this study, we identified the porin gene from H. longicornis and evaluated its expression levels in Babesia microti-infected and -uninfected H. longicornis ticks at developmental stages. We also analyzed porin functions in relation to both tick blood feeding and Babesia infection and the relationship between porin and porin-related apoptosis genes such as B-cell lymphoma (Bcl), cytochrome complex (Cytc), caspase 2 (Cas2), and caspase 8 (Cas8). The coding nucleotide sequence of H. longicornis porin cDNA was found to be 849 bp in length and encoded 282 amino acids. Domain analysis showed the protein to contain six determinants of voltage gating and two polypeptide binding sites. Porin mRNA levels were not significantly different between 1-day-laid and 7-day-laid eggs. In the nymphal stage, higher porin expression levels were found in unfed, 12-h-partially-fed (12 hPF), 1-day-partially-fed (1 dPF), 2 dPF nymphs and nymphs at 0 day post-engorgement (0 dAE) vs. nymphs at 2 dAE. Cytc and Cas2 mRNA levels were higher in 2 dPF nymphs in contrast to nymphs at 2 dAE. Porin expression levels appeared to be higher in the infected vs. uninfected nymphs during blood feeding except at 1 dPF and 0–1 dAE. Especially, the highest B. microti burden negatively affected porin mRNA levels in both nymphs and female adults. Porin knockdown affected body weight and Babesia infection levels and significantly downregulated the expression levels of Cytc and Bcl in H. longicornis female ticks. In addition, this study showed that infection levels of the B. microti Gray strain in nymphal and female H. longicornis peaked at or around engorgement from blood feeding to post engorgement. Taken together, the research conducted in this study suggests that H. longicornis porin might interfere with blood feeding and B. microti infection.
Highlights
The Asian longhorned tick, Haemaphysalis longicornis, is widely distributed in eastern Asia, Australia, and New Zealand and was recently found in the US (Heath, 2016; Rainey et al, 2018; Raghavan et al, 2019; Wormser et al, 2019; Zheng et al, 2019)
Our study showed that determinants of voltage gating and polypeptide binding sites in porin protein are conserved among tick species (Figure 2), suggesting that they play a primary role in the regulation of ion and molecular flow and in metabolism inside and outside the mitochondrial membrane among ticks
Porin mRNA levels of I. scapularis increased from egg to adult stages and from the non-feeding to feeding periods of female ticks
Summary
The Asian longhorned tick, Haemaphysalis longicornis, is widely distributed in eastern Asia, Australia, and New Zealand and was recently found in the US (Heath, 2016; Rainey et al, 2018; Raghavan et al, 2019; Wormser et al, 2019; Zheng et al, 2019). It is speculated that porin, termed a voltage-dependent anion-selective channel (VDAC), plays paramount roles in modulating pathogen infection in vectors, including bacteria and protozoa in ticks, and viruses in mosquitoes (Fongsaran et al, 2014; Alberdi et al, 2015; Rodríguez-Hernández et al, 2015; Jitobaom et al, 2016). Porin has been described in at least three tick species, including Ixodes scapularis, Rhipicephalus microplus, and Amblyomma variegatum (Ribeiro et al, 2011; RodríguezHernández et al, 2011; Alberdi et al, 2015). Porin in R. microplus was identified when it was exposed to Babesia bigemina infection (Rodríguez-Hernández et al, 2011)
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