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      Comparative dynamics of peritoneal cell immunophenotypes in sheep during the early and late stages of the infection with Fasciola hepatica by flow cytometric analysis

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          Abstract

          Background

          The peritoneal cell populations (PCP) are thought to play a crucial role during the early immune response in Fasciola hepatica infection while newly excysted juveniles (NEJ) are migrating in the peritoneal cavity (PC) towards the liver. In this study, we aimed to determine the immunophenotypes of the PCP and to analyse the dynamics of the recruitment of the PCP during the early and late stage of the infection in sheep infected with F. hepatica.

          Methods

          Thirty-seven sheep were divided into three groups: Group 1 ( n = 20) and 2 ( n = 10) were challenged with F. hepatica, Group 3 ( n = 7) was not infected and remained as uninfected control (UC). After the slaughtering, peritoneal lavages were carried out to isolate peritoneal cell populations at 1, 3, 9 and 18 days post-infection (dpi) for Group 1 and at 14 weeks post-infection (wpi) for Group 2 and 3. Flow cytometry was conducted to assess the dynamics of peritoneal cavity cell populations.

          Results

          TCD4 cells showed a significant decrease at 1 and 18 dpi when compared to UC; no statistical differences were detected for TCD8 and WC1 +γδ during the early stage of the infection with respect to the UC. CD14 cells exhibited a decreasing trend, with a significant decrease at 9 and 18 dpi when compared to the UC. The dynamics of MHCII and CD83 cells showed a similar increasing pattern from 3 to 18 dpi. During the chronic stage, both TCD4 and TCD8 cells showed no significant differences when compared to the UC, although a slight but statistically significant higher level of WC1 +γδ cells was observed. A lower percentage of antigen-presenting cells (APCs) was detected with respect to the UC.

          Conclusions

          The recruitment of the lymphocytes subsets did not show a significant increase during the course of the infection and only WC1 +γδ cells displayed a significant increase at the chronic stage. For the CD14, a decreasing trend was observed during the early stage, which was statistically significant at the chronic stage of the infection. Peritoneal CD83 and MHCII cells developed an increasing trend during the early stage of infection, and showed a significant decrease at the late stage of the infection.

          Electronic supplementary material

          The online version of this article (10.1186/s13071-018-3250-5) contains supplementary material, which is available to authorized users.

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          Most cited references39

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          Fascioliasis and other plant-borne trematode zoonoses.

          Fascioliasis and other food-borne trematodiases are included in the list of important helminthiases with a great impact on human development. Six plant-borne trematode species have been found to affect humans: Fasciola hepatica, Fasciola gigantica and Fasciolopsis buski (Fasciolidae), Gastrodiscoides hominis (Gastrodiscidae), Watsonius watsoni and Fischoederius elongatus (Paramphistomidae). Whereas F. hepatica and F. gigantica are hepatic, the other four species are intestinal parasites. The fasciolids and the gastrodiscid cause important zoonoses distributed throughout many countries, while W. watsoni and F. elongatus have been only accidentally detected in humans. Present climate and global changes appear to increasingly affect snail-borne helminthiases, which are strongly dependent on environmental factors. Fascioliasis is a good example of an emerging/re-emerging parasitic disease in many countries as a consequence of many phenomena related to environmental changes as well as man-made modifications. The ability of F. hepatica to spread is related to its capacity to colonise and adapt to new hosts and environments, even at the extreme inhospitality of very high altitude. Moreover, the spread of F. hepatica from its original European range to other continents is related to the geographic expansion of its original European lymnaeid intermediate host species Galba truncatula, the American species Pseudosuccinea columella, and its adaptation to other lymnaeid species authochthonous in the newly colonised areas. Although fasciolopsiasis and gastrodiscoidiasis can be controlled along with other food-borne parasitoses, fasciolopsiasis still remains a public health problem in many endemic areas despite sustained WHO control programmes. Fasciolopsiasis has become a re-emerging infection in recent years and gastrodiscoidiasis, initially supposed to be restricted to Asian countries, is now being reported in African countries.
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            Immunomodulatory molecules of Fasciola hepatica: candidates for both vaccine and immunotherapeutic development.

            The liver fluke, Fasciola hepatica, causes fascioliasis in domestic animals (sheep, cattle), a global disease that is also an important infection of humans. As soon as the parasite invades the gut wall its interaction with various host immune cells (e.g. dendritic cells, macrophages and mast cells) is complex. The parasite secretes a myriad of molecules that direct the immune response towards a favourable non-protective Th2-mediate/regulatory environment. These immunomodulatory molecules, such as cathepsin L peptidase (FhCL1), are under development as the first generation of fluke vaccines. However, this peptidase and other molecules, such as peroxiredoxin (FhPrx) and helminth defence molecule (FhHDM-1), exhibit various immunomodulatory properties that could be harnessed to help treat immune-related conditions in humans and animals. Copyright © 2013 Elsevier B.V. All rights reserved.
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              Fasciola hepatica vaccine: We may not be there yet but we’re on the right road

              Major advances have been made in identifying potential vaccine molecules for the control of fasciolosis in livestock but we have yet to reach the level of efficacy required for commercialisation. The pathogenesis of fasciolosis is associated with liver damage that is inflicted by migrating and feeding immature flukes as well as host inflammatory immune responses to parasite-secreted molecules and tissue damage alarm signals. Immune suppression/modulation by the parasites prevents the development of protective immune responses as evidenced by the lack of immunity observed in naturally and experimentally infected animals. In our opinion, future efforts need to focus on understanding how parasites invade and penetrate the tissues of their hosts and how they potentiate and control the ensuing immune responses, particularly in the first days of infection. Emerging ‘omics’ data employed in an unbiased approach are helping us understand liver fluke biology and, in parallel with new immunological data, to identify molecules that are essential to parasite development and accessible to vaccine-induced immune responses.
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                Author and article information

                Contributors
                v72pecar@uco.es
                fjmartinez@uco.es
                v62zafle@uco.es
                b62mohev@uco.es
                ilpl0510@gmail.com
                mtrcampillo@gmail.com
                jandromilla@hotmail.com
                an1pearj@uco.es
                amm@uco.es
                h12bupel@uco.es
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                14 December 2018
                14 December 2018
                2018
                : 11
                : 640
                Affiliations
                [1 ]ISNI 0000 0001 2183 9102, GRID grid.411901.c, Animal Health Department (Parasitology and Parasitic Diseases), Faculty of Veterinary Medicine, , University of Córdoba, Campus de Rabanales, ; Ctra. Madrid-Cádiz, km 396, 14014 Córdoba, Spain
                [2 ]ISNI 0000 0001 2183 9102, GRID grid.411901.c, Anatomy and Comparative Pathology Department, Faculty of Veterinary Medicine, , University of Córdoba, Campus de Rabanales, ; Ctra. Madrid-Cádiz, km 396, 14014 Córdoba, Spain
                Article
                3250
                10.1186/s13071-018-3250-5
                6295066
                30547823
                6b75edac-10c8-485c-931f-e3fa204770f0
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 24 September 2018
                : 2 December 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100010661, Horizon 2020 Framework Programme;
                Award ID: H2020-635408
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003176, Ministerio de Educación, Cultura y Deporte;
                Award ID: AGL2015-67023-C2-1-R
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Parasitology
                flow cytometry,nej,fasciola hepatica,peritoneal cells,recruitment
                Parasitology
                flow cytometry, nej, fasciola hepatica, peritoneal cells, recruitment

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