Abstract
In human and porcine cysticercosis caused by the tapeworm Taenia solium, the larval stage (cysts) can infest several tissues including the central nervous system (CNS) and the skeletal muscles (SM). The cyst’s proteomics changes associated with the tissue localization in the host tissues have been poorly studied. Quantitative multiplexed proteomics has the power to evaluate global proteome changes in response to different conditions. Here, using a TMT-multiplexed strategy we identified and quantified over 4,200 proteins in cysts obtained from the SM and CNS of pigs, of which 891 were host proteins. To our knowledge, this is the most extensive intermixing of host and parasite proteins reported for tapeworm infections.Several antigens in cysticercosis, i.e., GP50, paramyosin and a calcium-binding protein were enriched in skeletal muscle cysts. Our results suggested the occurrence of tissue-enriched antigen that could be useful in the improvement of the immunodiagnosis for cysticercosis. Using several algorithms for epitope detection, we selected 42 highly antigenic proteins enriched for each tissue localization of the cysts. Taking into account the fold changes and the antigen/epitope contents, we selected 10 proteins and produced synthetic peptides from the best epitopes. Nine peptides were recognized by serum antibodies of cysticercotic pigs, suggesting that those peptides are antigens. Mixtures of peptides derived from SM and CNS cysts yielded better results than mixtures of peptides derived from a single tissue location, however the identification of the ‘optimal’ tissue-enriched antigens remains to be discovered. Through machine learning technologies, we determined that a reliable immunodiagnostic test for porcine cysticercosis required at least five different antigenic determinants.
Highlights
Human and porcine cysticercosis caused by the larval stage of Taenia solium, is acquired by the ingestion of this parasite’s eggs
The protein changes observed between parasites obtained from different hosts and tissues were relatively discrete; the large majority of the identified and quantified cyst proteins remained at similar levels of expression, i.e., more than 3,200 proteins were found within a fold change of -1:1 (Fig 1B and 1C) for the skeletal muscles (SM) and central nervous system (CNS) cysts of the five pigs analyzed
Nine of 10 peptides were significantly recognized by the sera from cysticercotic, in comparison with the sera from non cysticercotic pigs (Fig 7). These data, suggest that the proteins from which the peptides were originated are immunologically recognized in porcine cysticercosis; we have identified several tissueenriched antigens; interestingly, a peptide that was enriched for SM (p165800) and other for CNS (p223100) cysts, produced the highest difference between the cysticercotic and non cysticercotic pig sera (Fig 7A and 7B)
Summary
Human and porcine cysticercosis caused by the larval stage of Taenia solium, is acquired by the ingestion of this parasite’s eggs. Establishment of cysts in the central nervous system (CNS) causes neurocysticercosis (NC), a serious and pleomorphic disease that can become highly debilitating [1]. Heterogeneity of human NC has been associated, at least in part, with the number and localization of the cysts in the CNS [2], as well as to many other factors including a complex immune response directed to a number of cyst’s antigens [3, 4, 5, 6]. The molecular factors associated with the tissue localization of the T. solium cysts remain poorly understood [7]. Other pathogenic microorganisms (S. pneumoniae, Campylobacter jejuni, Escherichia coli, Trypanosoma brucei, etc.), show tissue preference linked to a number of specific pathogen’s proteins [8, 9, 10, 11, 12]
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