Comparative Proteomic Analysis of Hymenolepis diminuta Cysticercoid and Adult Stages

Abstract

Cestodiases are common parasitic diseases of animals and humans. As cestodes have complex lifecycles, hexacanth larvae, metacestodes (including cysticercoids), and adults produce proteins allowing them to establish invasion and to survive in the hostile environment of the host. Hymenolepis diminuta is the most commonly used model cestode in experimental parasitology. The aims of the present study were to perform a comparative proteomic analysis of two consecutive developmental stages of H. diminuta (cysticercoid and adult) and to distinguish proteins which might be characteristic for each of the stages from those shared by both stages. Somatic proteins of H. diminuta were isolated from 6-week-old cysticercoids and adult tapeworms. Cysticercoids were obtained from experimentally infected beetles, Tenebrio molitor, whereas adult worms were collected from experimentally infected rats. Proteins were separated by GeLC-MS/MS (one dimensional gel electrophoresis coupled with liquid chromatography and tandem mass spectrometry). Additionally protein samples were digested in-liquid and identified by LC-MS/MS. The identified proteins were classified according to molecular function, cellular components and biological processes. Our study showed a number of differences and similarities in the protein profiles of cysticercoids and adults; 233 cysticercoid and 182 adult proteins were identified. From these proteins, 131 were present only in the cysticercoid and 80 only in the adult stage samples. Both developmental stages shared 102 proteins; among which six represented immunomodulators and one is a potential drug target. In-liquid digestion and LC-MS/MS complemented and confirmed some of the GeLC-MS/MS identifications. Possible roles and functions of proteins identified with both proteomic approaches are discussed.

Immunoproteomics and Surfaceomics of the Adult Tapeworm Hymenolepis diminuta

“…These included actin, paramyosin and several moonlighters such as enolase (ENO), malate dehydrogenase (MDH), TPI as well as the stress-related HSP60 and HSP70 proteins. Two other proteins, namely, calreticulin and superoxide dismutase (SOD) were previously identified in H. diminuta cysticercoids ( 11 ), but they have not been recognized as immunogenic ( 57 ). The revealed immunoproteome of the H. diminuta indicated potential vaccine candidates against echinococcosis, such as ENO, calpain, and GAPDH and the stress proteins HSP60 and HSP70 ( 51 ).…”

“…For as much as HSPs are considered as potential vaccine target proteins ( 66 ), their presence throughout the cestode life cycle suggests their importance in cestode biology and survival in the host. The balanced interplay between structural and stress molecules is probably one of the survival factors adopted by parasites during coevolution with their hosts ( 11 ). Comparative proteomic analyses of adult and metacestode stages suggest stage-specific mechanisms engaged in the parasite's survival at different life-cycle stages ( 11 , 67 ).…”

“…The balanced interplay between structural and stress molecules is probably one of the survival factors adopted by parasites during coevolution with their hosts ( 11 ). Comparative proteomic analyses of adult and metacestode stages suggest stage-specific mechanisms engaged in the parasite's survival at different life-cycle stages ( 11 , 67 ). In H. diminuta , proteins with antigenic potential, common for these two stages are structural proteins (actins, annexin, lamin, myosin, paramyosin, tubulin), enzymes (calpain, NADP dependent malic enzyme, phosphoenolpyruvate carboxykinase, succinyl co-A), HSPs, and major egg antigen ( 57 ).…”

“…In a number of cases, this mechanical contact between the parasite and host intestinal tissue can irritate the intestinal mucosa, which may finally result in inflammatory processes leading to ulceration and intestinal dysfunctions ( 8 ). In this way parasite-derived molecules interact with the host immune system as antigens associated with three sources: excretory-secretory, surface, and tegumental proteins ( 9 – 11 ). Many of these molecules are proteins involved in the parasite's metabolism and survival strategies.…”

Selected Molecular Mechanisms Involved in the Parasite–Host System Hymenolepis diminuta–Rattus norvegicus

“…The proteomic analysis of two invasive forms, tapeworm cysticercoid and adult stages, by Sulima (2017), found a very large number of proteins responsible for the invasion, development, and adaptation of H. diminuta , including thioredoxin, at both stages of parasite development [97]. …”