Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-28T04:01:18.094Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunization with adult Schistosoma mansoni tegument, treated with sub-curative praziquantel, partially protects mice against the infection

Published online by Cambridge University Press:  31 January 2019

B.E.W. El-Aswad Open the ORCID record for B.E.W. El-Aswad [Opens in a new window] ,
N.M. Harba ,
I.M. Moharm  and
S.F. Mahmoud
B.E.W. El-Aswad*
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Menoufia University, Egypt
N.M. Harba
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Menoufia University, Egypt
I.M. Moharm
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Menoufia University, Egypt
S.F. Mahmoud
Affiliation:
Department of Pathology, Faculty of Medicine, Menoufia University, Egypt
*
Author for correspondence: B.E.W. El-Aswad; E-mail: [email protected], [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The tegument of schistosomes is a source of many potential anti-Schistosoma vaccine molecules. This work aimed to assess the protective effects of the adult Schistosoma mansoni tegument treated (TT) with sub-curative praziquantel (PZQ), whether in vivo (in vivo TT) or in vitro (in vitro TT), in murine schistosomiasis. In vitro TT and in vivo TT showed great similarity, and they differed from untreated tegument antigen (Teg) in terms of quantity and quality of protein bands on SDS–PAGE. Two immunization trials were performed, each with 50 mice, divided randomly into five groups of 10 mice each: (1) uninfected control mice (UC), (2) infected mice given phosphate buffer saline + adjuvant (PBS + adjuvant), (3) infected, Teg vaccinated, (4) infected, in vivo TT vaccinated, and (5) infected, in vitro TT vaccinated. All the immunizations with antigens induced mixed Th1/Th2 immune responses, as indicated by significantly high (P < 0.001) specific IgG2a and IgG1 levels, with Th1 predominating, as shown by a diminished IgG1/IgG2a ratio, as well as a high serum concentration of IFN-γ, an absence of IL-4 and increased IL-10. In vitro TT gave the most pronounced response. With respect to reduction of total worm burden, relative to PBS + adjuvant mice, in vitro TT achieved the highest significant (P < 0.001) results, followed by in vivo TT and Teg (51.8–57.04%, 44.6–50.2% and 35.2–39.3%, respectively). In scanning electron microscopy studies, all the tested antigens caused tegumental changes in adult worms, with the worst occurring with in vitro TT, such as retracted ventral sucker, an effect on the gynaecophoric canal, and changes to tubercles. In conclusion, in vitro TT, which is cheap to prepare, could be a potential vaccine against S. mansoni.

Keywords

praziquantelSchistosomategumentvaccine
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e26
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abath, FG and Werkhauser, RC (1996) The tegument of Schistosoma mansoni: functional and immunological features. Parasite Immunology 18, 15–20.Google Scholar
Araujo, JM et al. (2012) Schistosoma mansoni schistosomula tegument (Smteg) immunization in absence of adjuvant induce IL10 production by CD4+ cells and failed to protect mice against challenge infection. Acta Tropica 124, 140–146.Google Scholar
Bergquist, R et al. (2002) Blue print for schistosomiasis vaccine development. Acta Tropica 82, 183–192.Google Scholar
Brindley, PJ et al. (1989) Role of host antibody in the chemotherapeutic action of praziquantel against Schistosoma mansoni: identification of target antigens. Molecular and Biochemical Parasitology 34, 99–108.Google Scholar
Capron, M and Capron, A (1994) Immunoglobulin E and effector cells in schistosomiasis. Science 264, 1876–1877.Google Scholar
Capron, A, Capron, M and Rivaeau, G (2002) Vaccine developed against schistosomiasis from concepts to clinical trials. British Medical Bulletin 62, 139–148.Google Scholar
Cioli, D et al. (2014) Schistosomiasis control: praziquantel forever? Molecular & Biochemical Parasitology 195, 23–29.Google Scholar
Cheever, AW (1968) Conditions affecting the accuracy of potassium hydroxide digestion techniques for counting Schistosoma mansoni eggs in tissues. Bulletin of the World Health Organization 39, 328–331.Google Scholar
David, JR, Butterworth, AE and Vadas, MA (1980) Mechanism of the interaction mediating killing of Schistosoma mansoni by human eosinophils. The American Journal of Tropical Medicine and Hygiene 29, 842–848.Google Scholar
DeKruyff, RH, Mosmann, RR and Umetsu, DT (1990) Induction of antibody synthesis by CD4+ T cells: IL-5 is essential for induction of antigen specific antibody response by Th2 but not Th1 clones. European Journal of Immunology 20, 2219–2222.Google Scholar
Dias, SR et al. (2014) Evaluation of the Schistosoma mansoni Y-box-binding protein (SMYB1) potential as a vaccine candidate against schistosomiasis. Frontiers in Genetics 5, 174.Google Scholar
Doenhoff, MJ et al. (1987) Evidence for an immune-dependent action of praziquantel on Schistosoma mansoni in mice. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 947–951.Google Scholar
Doenhoff, MJ, Modha, J and Lambertucci, JR (1988) Antischistosome chemotherapy enhanced by antibodies specific for a parasite esterase. Immunology 65, 507–510.Google Scholar
Dunne, DW et al. (1992) Human IgE responses to Schistosoma mansoni and resistance to reinfection. Memórias do Instituto Oswaldo Cruz 87, 99–103.Google Scholar
Duvall, RH and DeWitt, WB (1967) An improved perfusion technique for recovering adult schistosomes from laboratory animals. The American Journal of Tropical Medicine and Hygiene 16, 483–486.Google Scholar
El Azzouni, MZ et al. (2017) Protective capacity of cercarial transformation fluid alone or in combination with crude cercarial antigen against challenge infections of Schistosoma mansoni in mice. Journal of Helminthology 91, 35–42.Google Scholar
El-Shabasy, EA et al. (2015) Transmission electron microscopic observations on ultrastructural alterations in Schistosoma mansoni adult worms recovered from C57BL/6 mice treated with radiation attenuated vaccine and/or praziquantel in addition to passive immunization with normal and vaccinated rabbit sera against infection. Parasitology Research 114, 1563–1580.Google Scholar
Fallon, PG and Doenhooff, MJ (1995) Active immunization of mice with Schistosoma mansoni worm membrane antigens enhances efficacy of praziquantel. Parasite Immunology 17, 261–268.Google Scholar
Fallon, PG et al. (1994) Praziquantel-induced exposure of Schistosoma mansoni alkaline phosphatase: drug-antibody synergy which acts preferentially against female worms. Parasite Immunology 16, 529–535.Google Scholar
Finkelman, FD et al. (1988) IFN gamma regulates the isotypes of Ig secreted during in vivo humoral immune responses. The Journal of Immunology 140, 1022–1027.Google Scholar
Flores-Villanueva, PO et al. (1996) Recombinant IL-10 and IL-10/Fc treatment down regulate egg antigen-specific delayed hypersensitivity reactions and egg granuloma formation in schistosomiasis. The Journal of Immunology 156, 3315–3320.Google Scholar
Gupta, BC and Basch, PF (1987) The role of Schistosoma mansoni males in feeding and development of female worms. Journal of Parasitology 73, 481–486.Google Scholar
Heegaard, PM et al. (2011) Adjuvants and delivery systems in veterinary vaccinology: current state and future developments. Archives of Virology 156,183–202.Google Scholar
Hockley, DJ and McLaren, DJ (1973) Schistosoma mansoni: changes in the outer membrane of the tegumental during development from cercaria to adult worm. International Journal of Parasitology 3, 13–25.Google Scholar
Jankovic, D et al. (1999) Optimal vaccination against Schistosoma mansoni requires the induction of both B cell- and IFN- gamma-dependent effector mechanisms. Journal of Immunology 162, 345–351.Google Scholar
Joseph, M et al. (1983) A new function for platelets: IgE dependent killing of schistosomules. Nature 303, 810–812.Google Scholar
Laemmli, VK (1970) Cleavage of structural proteins during assembly of the head of the bacteriophage T4. Nature 277, 630–634.Google Scholar
Loukas, A, Tran, M and Pearson, MS (2007) Schistosome membrane proteins as vaccines. International Journal for Parasitology 37, 257–263.Google Scholar
Martins, VP et al. (2012) Vaccination with enzymatically cleaved GPI-anchored proteins from Schistosoma mansoni induces protection against challenge infection. Clinical and Developmental Immunology 2012, 962538.Google Scholar
Modha, J et al. (1990) Immune dependence of schistosomicidal chemotherapy: an ultrastructural study of Schistosoma mansoni infected adult worms exposed to praziquantel and immune serum in vivo. Parasite Immunology 12, 321–334.Google Scholar
Mossallam, SF et al. (2015) Fusion protein comprised of the two schistosomal antigens, Sm14 and Sm29, provides significant protection against Schistosoma mansoni in murine infection model. BMC Infectious Diseases 15, 147.Google Scholar
Oliveira, RR et al. (2012) Factors associated with resistance to Schistosoma mansoni infection in an endemic area of Bahia, Brazil. The American Journal of Tropical Medicine and Hygiene 86, 296–305.Google Scholar
Pinot de Moira, A et al. (2010) Analysis of complex patterns of human exposure and immunity to Schistosomiasis mansoni the influence of age, sex, ethnicity and IgE. PLoS Neglected Tropical Diseases 4, e820.Google Scholar
Ranasinghe, SL et al. (2018) Kunitz-type protease inhibitor as a vaccine candidate against schistosomiasis mansoni. International Journal of Infectious Diseases 66, 26–32.Google Scholar
Roberts, SM et al. (1983) Tegument surface membranes of adult Schistosoma mansoni: development of a method for their isolation. Molecular and Biochemical Parasitology 9, 105–128.Google Scholar
Roberts, SM, Boot, C and Wilson, RA (1988) Antibody responses of rodents to a tegument membrane preparation from adult Schistosoma mansoni. Parasitology 97, 425–435.Google Scholar
Rofatto, HK et al. (2013) Immunization with tegument nucleotidases associated with a subcurative praziquantel treatment reduces worm burden following Schistosoma mansoni challenge. PeerJ 1, e58.Google Scholar
Sadler, CH et al. (2003) IL-10 is crucial for the transition from acute to chronic disease state during infection of mice with Schistosoma mansoni. European Journal of Immunology 33, 880–888.Google Scholar
Siddiqui, AA and Siddiqui, SZ (2017) Sm-p80-based schistosomiasis vaccine: preparation for human clinical trials. Trends in Parasitology 33, 194–201.Google Scholar
Skelly, PJ and Wilson, RA (2006) Making sense of the schistosome surface. Advances in Parasitology 63, 185–284.Google Scholar
Smithers, SR and Terry, RJ (1965) The infection of laboratory hosts with cercariae of S. mansoni and the recovery of adult worms. Parasitology 55, 695–700.Google Scholar
Smithers, SR et al. (1989) Protective immunization of mice against Schistosoma mansoni with purified adult worm surface membranes. Parasite Immunology 11, 301–318.Google Scholar
Smythies, LE, Coulson, PS and Wilson, RA (1992) Monoclonal antibody to IFN gamma modifies pulmonary inflammatory responses and abrogates immunity to Schistosoma mansoni in mice vaccinated with attenuated cercariae. The Journal of Immunology 149, 3654–3658.Google Scholar
Spellberg, B and Edwards, JE Jr (2001) Type 1/Type 2 immunity in infectious diseases. Clinical Infectious Diseases 32, 76–102.Google Scholar
Sulbaran, G et al. (2013) Immunoprotection of mice against Schistosomiasis mansoni using solubilized membrane antigens. PLOS Neglected Tropical Diseases 7, e2254.Google Scholar
Sundstedt, A et al. (1997) Immunoregulatory role of IL-10 during superantigen-induced hyporesponsiveness in vivo. The Journal of Immunology 158, 180–186.Google Scholar
Teixeira de Melo, T et al. (2010) Immunization with newly transformed Schistosoma mansoni schistosomula tegument elicits tegument damage, reduction in egg and parasite burden. Parasite Immunology 32, 749–759.Google Scholar
Teixeira de Melo, T et al. (2013) Evaluation of the protective immune response induced in mice by immunization with Schistosoma mansoni schistosomula tegument (Smteg) in association with CpG-ODN. Microbes and Infection 15, 28–36.Google Scholar
Tendler, M et al. (1986) Schistosoma mansoni: vaccination with adult worm antigens. Internatinal Journal of Parasitology 16, 347–352.Google Scholar
von Lichtenberg, F (1962) Host response to eggs of S. mansoni. I. Granuloma formation in the unsensitized laboratory mouse. American Journal of Pathology 41, 711–731.Google Scholar
WHO (2016) Schistosomiasis. WHO Media Centre, Fact sheet No. 115. Available at: http://www.who.int/mediacentre/factsheets/fs115/en/.Google Scholar
Wilson, RA et al. (1996) Impaired immunity and altered pulmonary responses in mice with a disrupted interferon-γ receptor gene exposed to the irradiated Schistosoma mansoni vaccine. Immunology 87, 275–282.Google Scholar
Wilson, RA and Coulson, PS (2009) Immune effector mechanisms against schistosomiasis: looking for a chink in the parasite's armour. Trends in Parasitology 25, 423–431.Google Scholar
Xiao, S et al. (2000) Tegumental changes in 21-day-old Schistosoma mansoni harboured in mice treated with artemether. Acta Tropica 75, 341–348.Google Scholar