Immunological characterization of a chimeric form of Schistosoma mansoni aquaporin in the murine model

Parasitology

Volumn 141, Issue 10, 2014, Pages 1277-1288

  Figueiredo, Barbara Castro Pimentel ^a,b   De Assis, Natan Raimundo Gonçalves ^a,b   De Morais, Suellen Batistoni ^a,b   Martins, Vicente Paulo ^b,c   Ricci, Natasha Delaqua ^a,b   Bicalho, Rodrigo Marques ^a,b   Pinheiro, Carina Da Silva ^b,d   Oliveira, Sergio Costa ^a,b  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b Instituto Nacional de Ciência e Tecnologia de Vacinas   (Brazil)

^c INSTITUTO DE CIÊNCIAS BIOLÓGICAS   (Brazil)

^d FEDERAL UNIVERSITY OF BAHIA   (Brazil)

Author keywords

aquaporin; Schistosoma mansoni; tegument; Th1 Th17 response; vaccine

Indexed keywords

AQUAPORIN; CHIMERIC PROTEIN; GAMMA INTERFERON; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A ANTIBODY; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 5; SCHISTOSOMA VACCINE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; HELMINTH ANTIBODY; HELMINTH PROTEIN; IMMUNOLOGICAL ADJUVANT; RECOMBINANT PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HELMINTHIASIS; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; MOUSE; NONHUMAN; OSMOREGULATION; PARASITE SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; ANIMAL; C57BL MOUSE; DISEASE MODEL; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; LIVER; PARASITOLOGY; VACCINATION; VALIDATION STUDY; ANIMAL TISSUE; MALE; TH1 CELL; TH17 CELL;

MURINAE; MUS; SCHISTOSOMA MANSONI;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, HELMINTH; AQUAPORINS; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; HELMINTH PROTEINS; IMMUNIZATION; LIVER; MICE; MICE, INBRED C57BL; RECOMBINANT PROTEINS; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; VACCINATION;

EID: 84938573067     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182014000468     Document Type: Article

References (40)

1. Amiri, P., Locksley, R. M., Parslow, T. G., Sadick, M., Rector, E., Ritter, D. and McKerrow, J. H. (1992). Tumour necrosis factor alpha restores granulomas and induces parasite egg-laying in schistosome-infected SCID mice. Nature 356, 604-607. doi: 10.1038/356604a0.
2. Bazzone, L. E., Smith, P. M., Rutitzky, L. I., Shainheit, M. G., Urban, J. F., Setiawan, T., Blum, A. M., Weinstock, J. V. and Stadecker, M. J. (2008). Coinfection with the intestinal nematode Heligmosomoides polygyrus markedly reduces hepatic egg-induced immuno-pathology and proinflammatory cytokines in mouse models of severe schistosomiasis. Infection and Immunity 76, 5164-5172. doi: 10.1128/IAI.00673-08.
3. Bergquist, N. R., Leonardo, L. R. and Mitchell, G. F. (2005). Vaccine-linked chemotherapy: can schistosomiasis control benefit from an integrated approach? Trends in Parasitology 21, 112-117. doi: 10.1016/j. pt.2005.01.001.
4. Braschi, S. and Wilson, R. A. (2006). Proteins exposed at the adult schistosome surface revealed by biotinylation. Molecular and Cellular Proteomics 5, 347-356. doi: 10.1074/mcp.M500287-MCP200.
5. Braschi, S., Curwen, R. S., Ashton, P. D., Verjovski-Almeida, S. and Wilson, A. (2006). The tegument surface membranes of the human blood parasite Schistosoma mansoni: a proteomic analysis after differential extraction. Proteomics 6, 1471-1482. doi: 10.1002/pmic.200500368.
6. Brito, C. F., Fonseca, C. T., Goes, A. M., Azevedo, V., Simpson, A. J. and Oliveira, S. C. (2000). Human IgG1 and IgG3 recognition of Schistosoma mansoni 14 kDa fatty acid-binding recombinant protein. Parasite Immunology 22, 41-48.
7. Capron, A., Bazin, H., Dessaint, J. P. and Capron, M. (1975). The role of specific IgE antibodies in the immune adherence of normal macrophages to schistosomes of Schistosoma mansoni. Comptes Rendus Hebdomadaires des Seances de l'Academie des Sciences D: Sciences Naturelles 280, 927-930.
8. Cardoso, F. C., Pacifico, R.N., Mortara, R. A. and Oliveira, S. C. (2006). Human antibody responses of patients living in endemic areas for schistosomiasis to the tegumental protein Sm29 identified through genomic studies. Clinical and Experimental Immunology (Oxford) 144, 382-391. doi: 10.1111/j.1365-2249.2006.03081.x.
9. Cardoso, L. S., Araujo, M. I., Goes, A. M., Pacifico, L. G., Oliveira, R. R. and Oliveira, S. C. (2007). Polymyxin B as inhibitor of LPS contamination of Schistosoma mansoni recombinant proteins in human cytokine analysis. Microbial Cell Factories 6, 1. doi: 10.1186/1475-2859-6-1.
10. Cardoso, F.C., Macedo, G. C., Gava, E., Kitten, G. T., Mati, V.L., de Melo, A. L., Caliari, M. V., Almeida, G. T., Venancio, T.M., Verjovski-Almeida, S. and Oliveira, S. C. (2008). Schistosoma mansoni tegument protein Sm29 is able to induce a Th1-type of immune response and protection against parasite infection. PLoS Neglected Tropical Diseases 2, e308. doi: 10.1371/journal.pntd.0000308.
11. Castro-Borges, W., Simpson, D. M., Dowle, A., Curwen, R. S., Thomas-Oates, J., Beynon, R. J. and Wilson, R. A. (2011). Abundance of tegument surface proteins in the human blood fluke Schistosoma mansoni determined by QconCAT proteomics. Journal of Proteomics 74, 1519-1533. doi: 10.1016/j.jprot.2011.06.011.
12. Cheever, A. W., Poindexter, R. W.and Wynn, T. A.(1999). Egg laying is delayed but worm fecundity is normal in SCID mice infected with Schistosoma japonicum and S. mansoni with or without recombinant tumor necrosis factor alpha treatment. Infection and Immunity 67, 2201-2208.
13. Delgado, V. and McLaren, D. J. (1990). Evidence for enhancement of IgG1 subclass expression in mice polyvaccinated with radiation-attenuated cercariae of Schistosoma mansoni and the role of this isotype in serum-transferred immunity. Parasite Immunology 12, 15-32.
14. Faghiri, Z. and Skelly, P. J.(2009). The roleoftegumental aquaporin from the human parasitic worm, Schistosoma mansoni, in osmoregulation and drug uptake. FASEB Journal 23, 2780-2789. doi: 10.1096/fj.09-130757.
15. Faghiri, Z., Camargo, S. M., Huggel, K., Forster, I. C., Ndegwa, D., Verrey, F. and Skelly, P. J. (2010). The tegument of the human parasitic worm Schistosoma mansoni as an excretory organ: the surface aquaporin SmAQP is a lactate transporter. PLoS One 5, e10451. doi: 10.1371/journal.pone.0010451.
16. Fonseca, C. T., Brito, C. F., Alves, J.B. and Oliveira, S. C. (2004). IL-12 enhances protective immunity in mice engendered by immunization with recombinant 14 kDa Schistosoma mansoni fatty acid-binding protein through an IFN-gamma and TNF-alpha dependent pathway. Vaccine 22, 503-510.
17. Fonseca, C. T., Pacifico, L. G., Barsante, M. M., Rassi, T., Cassali, G. D. and Oliveira, S.C. (2006). Co-administration of plasmid expressing IL-12 with 14-kDa Schistosoma mansoni fatty acid-binding protein cDNA alters immune response profiles and fails to enhance protection induced by Sm14 DNA vaccine alone. Microbes and Infection 8, 2509-2516. doi: 10.1016/j.micinf.2006.06.008.
18. Gonen, T. and Walz, T. (2006). The structure of aquaporins. Quarterly Reviews of Biophysics 39, 361-396. doi: 10.1017/S0033583506004458.
19. Gray, D. J., McManus, D. P., Li, Y., Williams, G. M., Bergquist, R. and Ross, A. G. (2010). Schistosomiasis elimination: lessons from the past guide the future. Lancet Infectious Diseases 10, 733-736. doi: 10.1016/S1473-3099(10)70099-2.
20. Jankovic, D., Wynn, T. A., Kullberg, M. C., Hieny, S., Caspar, P., James, S., Cheever, A. W. and Sher, A. (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.
21. Khalife, J., Dunne, D. W., Richardson, B. A., Mazza, G., Thorne, K. J., Capron, A. and Butterworth, A. E. (1989). Functional role of human IgG subclasses in eosinophil-mediated killing of schistosomula of Schistosoma mansoni. Journal of Immunology 142, 4422-4427.
22. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
23. Loukas, A., Tran, M. and Pearson, M.S. (2007). Schistosome membrane proteins as vaccines. International Journal for Parasitology 37, 257-263. doi: 10.1016/j.ijpara.2006.12.001.
24. Lustigman, S., Prichard, R. K., Gazzinelli, A., Grant, W. N., Boatin, B. A., McCarthy, J. S. and Basanez, M. G. (2012). A research agenda for helminth diseases of humans: the problem of helminthiases. PLoS Neglected Tropical Diseases 6, e1582. doi: 10.1371/journal.pntd.0001582.
25. McManus, D. P. (2012). Schistosomiasis in 2012: current status and key research priorities required for control leading to elimination. Expert Review of Anti-infective Therapy 10, 1233-1236. doi: 10.1586/eri.12.121.
26. McManus, D. P. and Loukas, A. (2008). Current status of vaccines for schistosomiasis. Clinical Microbiology Reviews 21, 225-242. doi: 10.1128/CMR.00046-07.
27. Medzhitov, R.(2007). Recognition of microorganisms and activationofthe immune response. Nature 449, 819-826. doi: 10.1038/nature06246.
28. Pacifico, L. G., Fonseca, C. T., Chiari, L. and Oliveira, S.C. (2006). Immunization with Schistosoma mansoni 22·6 kDa antigen induces partial protection against experimental infection in a recombinant protein form but not as DNA vaccine. Immunobiology 211, 97-104. doi: 10.1016/j.imbio.2005.06.004.
29. Pearce, E.J. and MacDonald, A. S. (2002). The immunobiology of schistosomiasis. Nature Reviews Immunology 2, 499-511. doi: 10.1038/nri843.
30. Pearson, M. S., Pickering, D. A., McSorley, H. J., Bethony, J. M., Tribolet, L., Dougall, A.M., Hotez, P. J. and Loukas, A. (2012). Enhanced protective efficacy of a chimeric form of the schistosomiasis vaccine antigen Sm-TSP-2. PLOS Neglected Tropical Diseases 6, e1564. doi: 10.1371/journal.pntd.0001564.
31. Pinheiro, C. S., Martins, V.P., Assis, N. R., Figueiredo, B. C., Morais, S. B., Azevedo, V. and Oliveira, S. C. (2011). Computational vaccinology: an important strategy to discover new potential S. mansoni vaccine candidates. Journal of Biomedicine and Biotechnology 2011, 503068. doi: 10.1155/2011/503068.
32. Prichard, R. K., Basanez, M. G., Boatin, B. A., McCarthy, J. S., Garcia, H. H., Yang, G. J., Sripa, B. and Lustigman, S. (2012). A research agenda for helminth diseases of humans: intervention for control and elimination. PLOS Neglected Tropical Diseases 6, e1549. doi: 10.1371/journal.pntd.0001549.
33. Romeih, M. H., Hassan, H. M., Shousha, T.S. and Saber, M. A. (2008). Immunization against Egyptian Schistosoma mansoni infection by multivalent DNA vaccine. Acta Biochimica et Biophysica Sinica (Shanghai) 40, 327-338.
34. Rutitzky, L. I. and Stadecker, M. J. (2011). Exacerbated egg-induced immunopathology in murine Schistosoma mansoni infection is primarily mediated by IL-17 and restrained by IFN-gamma. European Journal of Immunology 41, 2677-2687. doi: 10.1002/eji.201041327.
35. Steinmann, P., Keiser, J., Bos, R., Tanner, M. and Utzinger, J. (2006). Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infectious Diseases 6, 411-425. doi: 10.1016/S1473-3099(06)70521-7.
36. Towbin, H., Staehelin, T.and Gordon, J.(1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences USA 76, 4350-4354.
37. Tran, M.H., Pearson, M. S., Bethony, J. M., Smyth, D. J., Jones, M. K., Duke, M., Don, T.A., McManus, D. P., Correa-Oliveira, R. and Loukas, A. (2006). Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nature Medicine 12, 835-840. doi: 10.1038/nm1430.
38. van der Werf, M. J., de Vlas, S. J., Brooker, S., Looman, C. W., Nagelkerke, N. J., Habbema, J. D.and Engels, D. (2003). Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Tropica 86, 125-139.
39. Wilson, R.A., Coulson, P.S., Betts, C., Dowling, M.A. and Smythies, L. E. (1996). Impaired immunity and altered pulmonary responses in mice with a disrupted interferon-gamma receptor gene exposed to the irradiated Schistosoma mansoni vaccine. Immunology 87, 275-282.
40. World Health Organization (2010). Working to Overcome the Global Impact of Neglected Tropical Diseases. First WHO Report on Neglected Tropical Diseases. World Health Organization, Geneva, Switzerland.