Immune Events Associated with High Level Protection Against Schistosoma Japonicum Infection in Pigs Immunized with UV-attenuated Cercariae

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2010 Oct 27

PMID 20976218

Citations 23

Authors

Fang Tian

Dandan Lin

Jingjiao Wu

Yanan Gao

Donghui Zhang

Minjun Ji

Guanling Wu

Affiliations

Soon will be listed here.

Abstract

Background: The vaccination of radiation-attenuated Schistosoma japonicum cercariae can induce effective protection in artiodactyl, but the immune events related to protective immunity are not fully understood. To provide a paradigm for a human recombinant antigen vaccine, we have undertaken a vaccination and challenge experiment in pigs, which was recognized as an appropriate animal model in this type of study because of their similarity to human in immunology, and investigated the relative immune events induced by the radiation-attenuated S. japonicum cercariae.

Methods And Findings: We found that pigs immunized once with 400 µw UV-irradiated cercariae exhibited 63.84% and 71.82% reductions in worm burden and hepatic eggs respectively. Protective immunity in vaccinated pigs was associated with high level productions of IgM, total IgG, IgG1 and IgG2; IgG2 was significantly increased in the acute infection. IFN-γ levels could be elicited by immunization. At week 6 post-infection, IFN-γ, IL-4 and IL-10 levels also showed a dramatic rise synchronously in vaccinated pigs. Moreover, the granzyme b, nk-lysin, ifnγ, il4 and il10 mRNA levels in early skin-draining lymph nodes of immunized pigs were higher than those in pigs with non-irradiated cercariae infection. In addition, cytotoxicity-related genes in the mesenteric lymph nodes were significantly upregulated in vaccinated pigs in the acute infection.

Conclusion/significance: Our results demonstrated that IFN-γ and IgG2 antibody production, as well as genes related to cytotoxicity are associated with the high level protection induced by UV-irradiated Schistosoma japonicum vaccine. These findings indicated that optimal vaccination against S. japonicum required the induction of IFN-γ, IgG2 antibody related to Th1 responses and cytotoxicity effect.

Citing Articles

Co-expression gene module analysis in response to attenuated cercaria vaccine reveals a critical role for NK cells in protection against Schistosoma mansoni.

Neto A, Vitoriano-Souza J, Khouri M, Favaro R, Wilson R, Leite L Parasit Vectors. 2024; 17(1):476.

PMID: 39563428 PMC: 11575109. DOI: 10.1186/s13071-024-06505-0.

Skin-Based Vaccination: A Systematic Mapping Review of the Types of Vaccines and Methods Used and Immunity and Protection Elicited in Pigs.

Co-Rives I, Chen A, Moore A Vaccines (Basel). 2023; 11(2).

PMID: 36851328 PMC: 9962282. DOI: 10.3390/vaccines11020450.

Systematic review of animal-based indicators to measure thermal, social, and immune-related stress in pigs.

Guevara R, Pastor J, Manteca X, Tedo G, Llonch P PLoS One. 2022; 17(5):e0266524.

PMID: 35511825 PMC: 9070874. DOI: 10.1371/journal.pone.0266524.

Ultraviolet disinfection of Schistosoma mansoni cercariae in water.

Hazell L, Allan F, Emery A, Templeton M PLoS Negl Trop Dis. 2021; 15(7):e0009572.

PMID: 34228750 PMC: 8284627. DOI: 10.1371/journal.pntd.0009572.

Systems Biology Analysis of the Radiation-Attenuated Schistosome Vaccine Reveals a Role for Growth Factors in Protection and Hemostasis Inhibition in Parasite Survival.

Farias L, Vitoriano-Souza J, Cardozo L, Gama L, Singh Y, Miyasato P Front Immunol. 2021; 12:624191.

PMID: 33777004 PMC: 7996093. DOI: 10.3389/fimmu.2021.624191.

References

Yuan H . Epidemiological features and control strategies of schistosomiasis japonica in China. Chin Med J (Engl). 1993; 106(8):563-8. View

Kumar P, Ramaswamy K . Vaccination with irradiated cercariae of Schistosoma mansoni preferentially induced the accumulation of interferon-gamma producing T cells in the skin and skin draining lymph nodes of mice. Parasitol Int. 2001; 48(2):109-19. DOI: 10.1016/s1383-5769(99)00008-2. View

Techau M, Johansen M, Aasted B, Lind P, Ornbjerg N, Oswald I . Cytokine mRNA profiles in pigs exposed prenatally and postnatally to Schistosoma japonicum. Vet Res. 2006; 38(1):25-36. DOI: 10.1051/vetres:2006042. View

Lu F, Gui M, Filsinger S, Hansch G, Ruppel A . Comparative phenotypic analysis of lymph node cells in mice after infection or vaccination with normal or ultraviolet-attenuated cercariae of Schistosoma japonicum or S. mansoni. Parasite Immunol. 1995; 17(8):435-40. DOI: 10.1111/j.1365-3024.1995.tb00911.x. View

Ribeiro de Jesus A, Araujo I, Bacellar O, Magalhaes A, Pearce E, Harn D . Human immune responses to Schistosoma mansoni vaccine candidate antigens. Infect Immun. 2000; 68(5):2797-803. PMC: 97490. DOI: 10.1128/IAI.68.5.2797-2803.2000. View

Eberl M, Langermans J, Frost P, Vervenne R, van Dam G, Deelder A . Cellular and humoral immune responses and protection against schistosomes induced by a radiation-attenuated vaccine in chimpanzees. Infect Immun. 2001; 69(9):5352-62. PMC: 98645. DOI: 10.1128/IAI.69.9.5352-5362.2001. View

Ruppel A, Shi Y, Moloney N . Schistosoma mansoni and S. japonicum: comparison of levels of ultraviolet irradiation for vaccination of mice with cercariae. Parasitology. 1990; 101 Pt 1:23-6. DOI: 10.1017/s0031182000079701. View

Buzza M, Bird P . Extracellular granzymes: current perspectives. Biol Chem. 2006; 387(7):827-37. DOI: 10.1515/BC.2006.106. View

Coulson P, Wilson R . Pulmonary T helper lymphocytes are CD44hi, CD45RB- effector/memory cells in mice vaccinated with attenuated cercariae of Schistosoma mansoni. J Immunol. 1993; 151(7):3663-71. View

10.

Johansen M, Bogh H, Nansen P, CHRISTENSEN N . Schistosoma japonicum infection in the pig as a model for human schistosomiasis japonica. Acta Trop. 2000; 76(2):85-99. DOI: 10.1016/s0001-706x(00)00103-0. View

11.

Shi Y, Jiang C, Han J, Li Y, Ruppel A . Immunization of pigs against infection with Schistosoma japonicum using ultraviolet-attenuated cercariae. Parasitology. 1993; 106 ( Pt 5):459-62. DOI: 10.1017/s0031182000076745. View

12.

Crawley A, Wilkie B . Porcine Ig isotypes: function and molecular characteristics. Vaccine. 2003; 21(21-22):2911-22. DOI: 10.1016/s0264-410x(03)00142-7. View

13.

Bickle Q, Bogh H, Johansen M, Zhang Y . Comparison of the vaccine efficacy of gamma-irradiated Schistosoma japonicum cercariae with the defined antigen Sj62(IrV-5) in pigs. Vet Parasitol. 2001; 100(1-2):51-62. DOI: 10.1016/s0304-4017(01)00483-6. View

14.

Willingham 3rd A, Hurst M, Bogh H, Johansen M, Lindberg R, CHRISTENSEN N . Schistosoma japonicum in the pig: the host-parasite relationship as influenced by the intensity and duration of experimental infection. Am J Trop Med Hyg. 1998; 58(2):248-56. DOI: 10.4269/ajtmh.1998.58.248. View

15.

Abdel-Hafeez E, Kikuchi M, Watanabe K, Ito T, Yu C, Chen H . Proteome approach for identification of schistosomiasis japonica vaccine candidate antigen. Parasitol Int. 2008; 58(1):36-44. DOI: 10.1016/j.parint.2008.09.004. View

16.

Shi Y, Jiang C, Han J, Li Y, Ruppel A . Schistosoma japonicum: an ultraviolet-attenuated cercarial vaccine applicable in the field for water buffaloes. Exp Parasitol. 1990; 71(1):100-6. DOI: 10.1016/0014-4894(90)90012-2. View

17.

Bartley P, Glanfield A, Li Y, Stanisic D, Duke M, Jones M . Artemether treatment of prepatent Schistosoma japonicum induces resistance to reinfection in association with reduced pathology. Am J Trop Med Hyg. 2008; 78(6):929-35. PMC: 2756499. View

18.

Zhang Y, Taylor M, Bickle Q, Wang H, Ge J . Vaccination of mice with gamma-irradiated Schistosoma japonicum cercariae. Parasite Immunol. 1999; 21(2):111-7. DOI: 10.1046/j.1365-3024.1999.00208.x. View

19.

Willingham 3rd A, Hurst M . The pig as a unique host model for Schistosoma japonicum infection. Parasitol Today. 1996; 12(4):132-4. DOI: 10.1016/0169-4758(96)20001-8. View

20.

Zhou X, Wang L, Chen M, Wu X, Jiang Q, Chen X . The public health significance and control of schistosomiasis in China--then and now. Acta Trop. 2005; 96(2-3):97-105. DOI: 10.1016/j.actatropica.2005.07.005. View