Open Access
Research (Published online: 30-11-2018)
19. Antibody immunoglobulin G1 and immunoglobulin G2a responses against some cystic fluid proteins of Cysticercus bovis in Balb/c mice
I Nyoman Mantik Astawa, Ida Bagus Made Oka and I Made Dwinata
Veterinary World, 11(11): 1641-1647

I Nyoman Mantik Astawa: Laboratory of Immunology, Faculty of Veterinary Medicine, Udayana University, Denpasar Bali 80232, Indonesia.
Ida Bagus Made Oka: Laboratory of Parasitology, Faculty of Veterinary Medicine, Udayana University, Bali 80232, Indonesia.
I Made Dwinata: Laboratory of Parasitology, Faculty of Veterinary Medicine, Udayana University, Bali 80232, Indonesia.

doi: 10.14202/vetworld.2018.1641-1647

Share this article on [Facebook] [LinkedIn]

Article history: Received: 17-07-2018, Accepted: 11-10-2018, Published online: 30-11-2018

Corresponding author: I Nyoman Mantik Astawa

E-mail: mantik.astawa@unud.ac.id

Citation: Astawa, INM, Oka IBM, Dwinata IM (2018) Antibody immunoglobulin G1 and immunoglobulin G2a responses against some cystic fluid proteins of Cysticercus bovis in Balb/c mice. Veterinary World, 11(11): 1641-1647.
Abstract

Background and Aim: Immunoglobulin (Ig) G1 and IgG2a are the surrogate markers respectively for humoral and cellular immune responses of hosts against antigens including cystic fluid proteins of Cysticercus bovis. A study was conducted to investigate the IgG1 and IgG2a responses of Balb/c mice against some individual cystic fluid proteins of C. bovis in an effort to determine the roles of each protein in inducing the humoral and cellular immune responses in host.

Materials and Methods: Individual p71, p31, and p14 proteins of C. bovis were purified by separation of the proteins using sodium dodecyl sulfate-polyacrylamide gel electrophoresis and elution of individual proteins from the gel. Six female Balb/c mice were immunized 4 times at 10-day intervals with the crude cystic fluid proteins, and sera were collected for the measurement of IgG1 and IgG2a levels against the individual proteins. Sera samples collected before the first immunization were used as negative antibody control, sera samples collected after the fourth immunization were used as positive antibody control, and crude cystic fluid protein was used as positive antigen control.

Results: All immunized mice were immune to p71, p31, p14, and crude cystic fluid proteins of C. bovis. The crude cystic fluid proteins of C. bovis induced a higher IgG2a than IgG1 level following the first and the second immunizations but switched into a higher IgG1 than IgG2a level following the fourth immunization. Protein 71 kDa (p71) induced a higher IgG2a than IgG1 level following the fourth immunization. In contrast, p14 induced a higher IgG1 than IgG2a level following the fourth immunization. Low and balance IgG1 and IgG2a levels against p31 were observed following the first to the fourth immunizations.

Conclusion: Using IgG1 and IgG2a levels as the surrogate markers, it appears that cystic fluid antigens of C. bovis induce both humoral and cellular immune responses in Balb/c mice. The p71 appears to be a better inducer of cellular immune response, whereas p14 is a better inducer of humoral immune response of mice.

Keywords: Cystic fluid, Cysticercus bovis, immunoglobulin G1, immunoglobulin G2a, proteins.

References

1. Lopes, W.D.Z., Santos, T.R., Soares, V.E., Nunes, J.L., Mendonca, R.P., de Lima, R.C., Sakamoto, C.A., Costa, G.H., Thomaz-Soccol, V., Oliveira, G.P. and Costa, A.J. (2011) Preferential infection sites of Cysticercus bovis in cattle experimentally infected with Taenia saginata eggs. Res. Vet. Sci., 90(1): 84-88. [Crossref] [PubMed]

2. Schmid-Hempel, P. (2009) Immune defense, parasite evasion strategies and their relevance for "macroscopic phenomena" such as virulence. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 364(1513): 85-98. [Crossref] [PubMed] [PMC]

3. Amit, P., Prasad, K.N., Kumar, G.R., Shweta, T., Sanjeev, J., Kumar, P.V. and Mukesh, T. (2011) Immune response to different fractions of Taenia solium cyst fluid antigens in patients with neurocysticercosis. Exp. Parasitol., 127(3): 687-692. [Crossref] [PubMed]

4. Vielma, J.R., Urdaneta-Romero, H., Villarreal, J.C., Paz, L.A., Gutierrez, L.V., Mora, M. and Chacin-Bonilla, L. (2014) Neurocysticercosis: Clinical aspects, immunopathology, diagnosis, treatment and vaccine development. Epidemiol, 4: 156.

5. Terrazas, L.I., Bojalil, R., Govezensky, T. and Larralde, C. (1998) Shift from an early protective Th1-type immune response to a late permissive Th2-type response in murine cysticercosis (Taenia crassiceps). J. Parasitol., 84(1): 74-81. [Crossref]

6. Nimmerjahn, F. and Ravetch, J.V. (2008) Fcgamma receptors as regulator of immune responses. Nat. Rev. Immunol., 8(1): 34-47. [Crossref] [PubMed]

7. Gurish, M.F., Paul, J., Bryce, P.J., Kisselgof, A.B., Thornton, E.M., Miller, H.R., Friend, D.S. and Oettgen, H.C. (2004) IgE enhances parasite clearance and regulates mast cell responses in mice infected with Trichinella spiralis. J. Immunol., 172(2): 1139-1145. [Crossref]

8. Chavarria, A., Fleury, A., Bobes, R.J., Morales, J., Fragoso, G. and Sciutto, E. (2006) A depressed peripheral cellular immune response is related to symptomatic neurocysticercosis. Microbes Infect., 8(4): 1082-1089. [Crossref] [PubMed]

9. Sciutto, E., Chavarria, A., Fragoso, G., Fleury, A. and Larralde, C. (2007) The immune response in Taenia solium cysticercosis: Protection and injury. Parasite Immunol., 29(12): 621-636. [Crossref] [PubMed]

10. Abuseir, S., Nagel-Kohl, U., Wolken, S. and Strube, C. (2013) An immunoblot for detection of Taenia saginata cysticercosis. Parasitol. Res., 112(5): 2069-2073. [Crossref] [PubMed]

11. Dharmawan, N.S., Dwinata, I.M., Swastika, K., Damriyasa, I.M., Oka, I.B.M. and Astawa, I.N.M. (2013) Specific protein of Cysticercus bovis cyst fluid on Bali cattle experimentally infected with Taenia saginata. J. Vet., 14(1): 78-84.

12. Wang, G., Zhao, J., Liu, J., Huang, Y., Zhong, J.J. and Tang, W. (2007) Enhancement of IL-2 and IFN-gamma expression and NK cells activity involved in the anti-tumor effect of ganoderic acid me in vivo. Int. Immunopharmacol., 7(6): 864-870. [Crossref] [PubMed]

13. Stevens, T.L., Bossie, A., Sanders, V.M., Fernandez-Botran, R., Coffman, R.L., Mosmann, T.R. and Vitetta, E.S. (1988) Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells. Nature, 334(6179): 255-258. [Crossref] [PubMed]

14. Herbst, S., Schaible, U.E. and Schneider, B.E. (2011). Interferon-gamma activated macrophages kill mycobacteria by nitric oxide-induced apoptosis. PLoS One, 6(5): e19105. [Crossref] [PubMed] [PMC]

15. Yu, T.K., Caudel, E.G., Smid, C. and Grimm, E.A. (2000) IL-2 activation of NK cells: Involvement of MKK1/2/ERK but not p38 kinase pathway. J. Immunol., 164(12): 6244-6251. [Crossref]

16. Cho, J., Kim, H., Kim, K., Yang, D.H., Surh, C.D. and Sprent, J. (2013) Unique features of naive CD8+ T cell activation by IL-2. J. Immunol., 191(11): 5559-5573. [Crossref] [PubMed]

17. Laemli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227(5259): 680-685. [Crossref]

18. Puchades, M., Westman, A., Blennow, K. and Davidson, P. (1999) Removal of sodium dodecyl sulfate from protein samples prior to matrix-assisted laser desorption/ionization mass spectrometry. Rapid Commun. Mass Spectrom., 13(5): 344-349. [Crossref]

19. Dunn, S.D. (1986) Effects of the modification of transfer buffer composition and the renaturation of proteins in gels on the recognition of proteins on Western blots by monoclonal antibodies. Anal. Biochem., 157(1): 144-153. [Crossref]

20. Ramadass, P., Parthiban, M., Thiagarajan, V., Chandrasekar, M., Vidhya, M.N. and Raj, G.D. (2008) Development of single serum dilution ELISA for detection of infectious bursal disease virus. Veterinarski Arhiv 78 (1): 23-30.

21. Sabry, M.A., Taher, E.S., Allah, N.F. and Mahgoub, A.M. (2014) Diagnosis of Fasciola infection by SDS-PAGE eluted excretory-secretory (ES) protein fractions using dot-ELISA. Int. J. Vet. Sci. Med., 2(2): 130-135. [Crossref]

22. Kaplan, C., Valde, J.C., Chandrasekaran, R., Eibel, H., Mikecz, K., Glant, T.T. and Finnegan, A. (2002) Th1 and Th2 cytokines regulate proteoglycan-specific autoantibody isotypes and arthritis. Arthritis Res., 4(1): 54-58. [Crossref] [PubMed] [PMC]

23. Khan, T.A., Mazhar, H., Saleha, S., Tipu, H.N., Muhammad, N. and Abbas, M.N. (2016) Interferon-gamma improves macrophages function against M. tuberculosis in multidrug-resistant tuberculosis patients. Chemother. Res. Pract., 2016: 7295390. [Crossref] [PubMed] [PMC]

24. Becker, P.S., Suck, G., Nowakowska, P., Ullrich, E., Seifried, E., Bader, P., Tonn, T. and Seid, C. (2016) Selection and expansion of natural killer cells for NK cell-based immunotherapy. Cancer Immunol. Immunother., 65(4): 477-484. [Crossref] [PubMed] [PMC]

25. Liao, W., Lin, J.X. and Leonard, W.J. (2013) Interleukin-2 at the crossroads of effector responses, tolerance, and immunotherapy. Immunity, 38(1): 13-25. [Crossref] [PubMed] [PMC]

26. Hurdayal, R., Ndlovu, H.H., Revaz-Breton, M., Parihar, S.P., Nono, J.K., Govender, M. and Brombacher. F (2017) IL-4-producing B cells regulate T helper cell dichotomy in Type 1- and Type 2-controlled diseases. Proc. Natl. Acad. Sci. U. S. A., 114(40): E8430-E8439. [Crossref]

27. Carneiro, P.P., Conceicao, J., Macedo, M., Magalhaes, V., Carvalho, E.M. and Bacellar, O. (2016) The role of nitric oxide and reactive oxygen species in the killing of Leishmania braziliensis by monocytes from patients with cutaneous leishmaniasis. PLoS One, 11(2): e0148084. [Crossref]

28. Wang, Z.E., Reiner, S.L., Zheng, S., Dalton, D.K. and Locksley, R.M. (1994) CD4+ effector cells default to the Th2 pathway in interferon gamma-deficient mice infected with Leishmania major. J. Exp. Med., 179(4): 1367e71. [Crossref]

29. Kim, H.P., Imbert, J. and Leonard, W.J. (2006) Both integrated and differential regulation of components of the IL-2/IL-2 receptor system. Cytokine Growth Factor Rev. 17(5): 49-66. [Crossref]

30. Ekkens, M.J., Shedlock, D.J., Jung, E., Troy, A., Pearce, E.L., Shen, H. and Pearce, E.J. (2007) Th1 and Th2 cells help CD8 T-cell responses. Infect. Immun., 75(5): 2291-2296. [Crossref] [PubMed] [PMC]

31. Nutman, T.B. (2015) Looking beyond the induction of Th2 responses to explain immunomodulation by helminths. Parasite Immunol., 37(6): 304-313. [Crossref] [PubMed] [PMC]

32. Osier, F.H.A., Feng, G. and Boyle, M.J. (2014) Opsonic phagocytosis of Plasmodium falciparum merozoites : Mechanism in human immunity and correlate of protection against malaria. BMC Med., 12(1): 108. [Crossref] [PubMed] [PMC]

33. Hill, D.L., Wilson, D.W., Sampaio, N.G., Ryg-Cornejo, V., Harrison, G.L.A., Uboldi, A.D., Robinson, L.J., Beeson, J.G., Siba, P., Cowman, A.F., Diana, S., Hansen, D.S., Mueller, I. and Schofield, L. (2016) Merozoite antigens of Plasmodium falciparum elicit strain-transcending opsonizing immunity. Infect. Immun., 84(8): 2175-2184. [Crossref] [PubMed] [PMC]