Abstract
In North America, the black-legged tick, Ixodes scapularis, an obligate haematophagus arthropod, is a vector of several human pathogens including Borrelia burgdorferi, the Lyme disease agent. In this report, we show that the tick salivary gland transcriptome and proteome is dynamic and changes during the process of engorgement. We demonstrate, using a guinea pig model of I. scapularis feeding and B. burgdorferi transmission, that immunity directed against salivary proteins expressed in the first 24 h of tick attachment — and not later — is sufficient to evoke all the hallmarks of acquired tick-immunity, to thwart tick feeding and also to impair Borrelia transmission. Defining this subset of proteins will promote a mechanistic understanding of novel I. scapularis proteins critical for the initiation of tick feeding and for Borrelia transmission.
Highlights
The black-legged tick Ixodes scapularis is a vector of Borrelia burgdorferi, the agent of Lyme disease [1] and of pathogens responsible for anaplasmosis [2], babesiosis [3], and tick-borne encephalitis [4]
We examined Borrelia transmission in the context of immunity against 24 h tick salivary proteins. 24 h tick-immune guinea pigs were each challenged with 5–6 B. burgdorferi-infected I. scapularis nymphs
In 1939 Trager showed that [26] repeated tick infestations provoked guinea pig immunity against D. variabilis salivary proteins characterized by cutaneous reactions at tick feeding sites that resulted in tick rejection within 24–48 h of attachment
Summary
The black-legged tick Ixodes scapularis is a vector of Borrelia burgdorferi, the agent of Lyme disease [1] and of pathogens responsible for anaplasmosis [2], babesiosis [3], and tick-borne encephalitis [4]. Defining tick proteins critical for feeding and transmission is essential for a molecular basis of new vaccines against tick-borne pathogens Towards this goal, research efforts focused on salivary gland proteins expressed in ticks that fed for 3–4 days or longer, primarily due to the ease of obtaining protein and RNA from fed, compared with unfed, ticks [10,11,12]. Several tick salivary proteins with pharmacological activities that block host haemostatic cascades and immune responses have been identified in this way [11,12,13,14,15,16,17,18,19,20,21] The potential of these proteins to serve as efficient vaccines to block feeding, has not yet been demonstrated. Immunity against 64TRP, a potential broad-spectrum vaccine candidate was shown to decrease the transmission efficiency of TBE by I. ricinus nymphs [25]
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