Tick-Host Range Adaptation: Changes in Protein Profiles in Unfed Adult Ixodes scapularis and Amblyomma americanum Saliva Stimulated to Feed on Different Hosts.

Lucas Tirloni,John R Yates,Itabajara Da Silva Vaz,Tae K Kim,Albert Mulenga,Antônio F M Pinto

doi:10.3389/fcimb.2017.00517

Abstract

Understanding the molecular basis of how ticks adapt to feed on different animal hosts is central to understanding tick and tick-borne disease (TBD) epidemiology. There is evidence that ticks differentially express specific sets of genes when stimulated to start feeding. This study was initiated to investigate if ticks such as Ixodes scapularis and Amblyomma americanum that are adapted to feed on multiple hosts utilized the same sets of proteins to prepare for feeding. We exposed I. scapularis and A. americanum to feeding stimuli of different hosts (rabbit, human, and dog) by keeping unfed adult ticks enclosed in a perforated microfuge in close contact with host skin, but not allowing ticks to attach on host. Our data suggest that ticks of the same species differentially express tick saliva proteins (TSPs) when stimulated to start feeding on different hosts. SDS-PAGE and silver staining analysis revealed unique electrophoretic profiles in saliva of I. scapularis and A. americanum that were stimulated to feed on different hosts: rabbit, human, and dog. LC-MS/MS sequencing and pairwise analysis demonstrated that I. scapularis and A. americanum ticks expressed unique protein profiles in their saliva when stimulated to start feeding on different hosts: rabbit, dog, or human. Specifically, our data revealed TSPs that were unique to each treatment and those that were shared between treatments. Overall, we identified a total of 276 and 340 non-redundant I. scapularis and A. americanum TSPs, which we have classified into 28 functional classes including: secreted conserved proteins (unknown functions), proteinase inhibitors, lipocalins, extracellular matrix/cell adhesion, heme/iron metabolism, signal transduction and immunity-related proteins being the most predominant in saliva of unfed ticks. With exception of research on vaccines against Rhipicephalus microplus, which its natural host, cattle, research on vaccine against other ticks relies feeding ticks on laboratory animals. Data here suggest that relying on lab animal tick feeding data to select target antigens could result in prioritizing irrelevant anti-tick vaccine targets that are expressed when ticks feed on laboratory animals. This study provides the platform that could be utilized to identify relevant target anti-tick vaccine antigens, and will facilitate early stage tick feeding research.

Highlights

Ticks and tick-borne diseases (TBD) cause significant problems to global and veterinary health, impacting huge losses in the livestock industry (Jongejan and Uilenberg, 2004; Grisi et al, 2014)
We provide evidence that protein profiles in saliva of ticks that are stimulated to start feeding on different change, as suggested by differential protein profiles in saliva of both A. americanum and I. scapularis ticks, which were stimulated to start feeding on different hosts
Findings that 83 of the 165 proteins found in start feeding on rabbits (SR) I. scapularis tick saliva were identified in the saliva of I. scapularis ticks that were fed on rabbits (Table S3) gives us confidence these proteins are injected into the host during feeding

Summary

Introduction

Ticks and tick-borne diseases (TBD) cause significant problems to global and veterinary health, impacting huge losses in the livestock industry (Jongejan and Uilenberg, 2004; Grisi et al, 2014). Their impact on public health has been on a steady climb since the 1980s (Dantas-Torres et al, 2012). A deeper understanding of tick feeding is needed as a mean to find molecular targets that can be useful for development of novel tick control methods. From this perspective, tick-feeding physiology continues to receive significant research attention

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