Differential Tick Salivary Protein Profiles and Human Immune Responses to Lone Star Ticks (Amblyomma americanum) From the Wild vs. a Laboratory Colony.

L Paulina Maldonado-Ruiz,Berlin Londono-Renteria,Sapna Menghwar,Brittany Blattner,Ludek Zurek,Lidia Montenegro-Cadena

doi:10.3389/fimmu.2019.01996

Abstract

Ticks are a growing concern to human and animal health worldwide and they are leading vectors of arthropod-borne pathogens in the United States. Ticks are pool blood feeders that can attach to the host skin for days to weeks using their saliva to counteract the host defenses. Tick saliva, as in other hematophagous arthropods, contains pharmacological and immunological active compounds, which modulate local and systemic immune responses and induce antibody production. In the present study, we explore differences in the salivary gland extract (SGE) protein content of Amblyomma americanum ticks raised in a laboratory colony (CT) vs. those collected in the field (FT). First, we measured the IgG antibody levels against SGE in healthy volunteers residing in Kansas. ELISA test showed higher IgG antibody levels when using the SGE from CT as antigen. Interestingly, antibody levels against both, CT-SGE and FT-SGE, were high in the warm months (May–June) and decreased in the cold months (September–November). Immunoblot testing revealed a set of different immunogenic bands for each group of ticks and mass spectrometry data revealed differences in at 19 proteins specifically identified in the CT-SGE group and 20 from the FT-SGE group. Our results suggest that differences in the salivary proteins between CT-SGE and FT-SGE may explain the differential immune responses observed in this study.

Highlights

Ticks are obligate blood-feeding ectoparasites of a wide range of vertebrates and are important vectors of human and animal pathogens [1]
To evaluate human immune responses against tick saliva, we collected blood samples from 36 volunteers living in Manhattan, KS, who reported no current illness at the time of sampling
Comparison of the IgG antibody levels against each salivary gland extract (SGE) type (FT vs. CT) showed significantly higher antibody levels against the CT-SGE than against the female adult ticks (FT)-SGE (Mann-Whitney test, p = 0.0094). Antibody levels against both SGE antigens were significantly higher in the summer months than in the Fall (Mann-Whitney test, p < 0.05), but no significant differences were observed when comparing antibody levels between males and females, or after comparing people using repellent or not (Mann-Whitney test, p > 0.05) (Figures 2A–D)

Summary

Introduction

Ticks are obligate blood-feeding ectoparasites of a wide range of vertebrates and are important vectors of human and animal pathogens [1]. Hard ticks (Ixodidae) feed once in each developmental stage for a prolonged period by deeply penetrating the epidermis, forming a pool of blood, and causing great damage to the host skin that could last from several days to weeks [2, 3]. Arthropods use saliva to counteract the response against injury caused during the process of blood feeding (piercing and tearing) that trigger host defense mechanisms as well as to facilitate the process of obtaining the blood. Arthropod saliva modulates the transmission of pathogens either directly by enhancing pathogen invasion [10, 11] or indirectly by modulating host immune responses [12, 13]

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