Abstract
BackgroundNew candidate protective antigens for tick vaccine development may be identified by selecting and testing antigen candidates that play key biological functions. After blood-feeding, tick midgut overexpresses proteins that play essential functions in tick survival and disease transmission. Herein, Ornithodoros erraticus midgut transcriptomic and proteomic data were examined in order to select functionally significant antigens upregulated after feeding to be tested as vaccine candidate antigens.MethodsTranscripts annotated as chitinases, tetraspanins, ribosomal protein P0 and secreted proteins/peptides were mined from the recently published O. erraticus midgut transcriptome and filtered in a second selection step using criteria based on upregulation after feeding, predicted antigenicity and expression in the midgut proteome. Five theoretical candidate antigens were selected, obtained as recombinant proteins and used to immunise rabbits: one chitinase (CHI), two tetraspanins (TSPs), the ribosomal protein P0 (RPP0) and one secreted protein PK-4 (PK4).ResultsRabbit vaccination with individual recombinant candidates induced strong humoral responses that mainly reduced nymph moulting and female reproduction, providing 30.2% (CHI), 56% (TSPs), 57.5% (RPP0) and 57.8% (PK4) protection to O. erraticus infestations and 19.6% (CHI), 11.1% (TSPs), 0% (RPP0) and 8.1% (PK4) cross-protection to infestations by the African tick Ornithodoros moubata. The joint vaccine efficacy of the candidates was assessed in a second vaccine trial reaching 66.3% protection to O. erraticus and 25.6% cross-protection to O. moubata.ConclusionsThese results (i) indicate that argasid chitinases and RPP0 are promising protective antigens, as has already been demonstrated for ixodid chitinases and RPP0, and could be included in vaccines targeting multiple tick species; (ii) reveal novel protective antigens tetraspanins and secreted protein PK-4, never tested before as protective antigens in ticks; and (iii) demonstrate that multi-antigenic vaccines increased vaccine efficacy compared with individual antigens. Lastly, our data emphasize the value of the tick midgut as a source of protective candidate antigens in argasids for tick control.
Highlights
New candidate protective antigens for tick vaccine development may be identified by selecting and testing antigen candidates that play key biological functions
Uniprot and National Center for Biotechnology Information non redundant (NCBInr) databases searching for tick orthologues of OeCHI retrieved 12 top matches, comprising 3 argasid and 9 ixodid chitinases belonging to the GH-18 family
We focused on midgut chitinases, tetraspanins and ribosomal protein P0 (RPP0) because these proteins are involved in important midgut physiological processes; several publications highlight their potential as vaccine candidates to control parasite infections [28, 29, 33, 42]
Summary
New candidate protective antigens for tick vaccine development may be identified by selecting and testing antigen candidates that play key biological functions. O. erraticus is the typespecies of the “O. erraticus complex”, and several species in this complex, including O. asperus, O. lahorensis, O. tartakovsky and O. tholozani, are distributed through the Middle East, the Caucasus, the Russian Federation and the Far East, where they transmit different species of TBRF-causing borreliae [5,6,7] and where the ASF virus has penetrated and spread out of control in the last decade [8,9,10,11] This has not been experimentally proven hitherto, if these tick species in the “O. erraticus complex” were competent vectors of the ASF virus, their presence in anthropic environments would significantly increase the transmission and long-term persistence of ASF in this wide region. While chemical acaricide agents are not effective against these Ornithodoros ticks [12], alternative methods for the control of ticks are urgently required and tick vaccines have been validated as an effective sustainable method for the control of tick infestations and tick-borne diseases [13,14,15]
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