Immunization with tegument nucleotidases associated with a subcurative praziquantel treatment reduces wormburden following Schistosoma mansoni challenge

PeerJ

Volumn 2013, Issue 1, 2013, Pages

  Rofatto, Henrique K ^a   Araujo Montoya, Bogar O ^a   Miyasato, Patrícia A ^a   Levano Garcia, Julio ^b   Rodriguez, Dunia ^a   Nakano, Eliana ^a   Verjovski Almeida, Sergio ^b   Farias, Leonardo P ^a   Leite, Luciana C C ^a  

^a INSTITUTO BUTANTAN   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Alkaline phosphatase; Nucleotidases; Nucleotide pyrophosphatase phosphodiesterase smNPP NPP; Praziquantel; Schistosoma mansoni; SmNTPDase Apyrase ATPDase; Tegument; Vaccine

Indexed keywords

ALKALINE PHOSPHATASE; APYRASE; CYTOKINE; FREUND ADJUVANT; HEXAHISTIDINE; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; INTERLEUKIN 17; NUCLEOTIDASE; PHOSPHODIESTERASE; PRAZIQUANTEL; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR IMMUNITY; CERCARIA; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DRUG POTENTIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HELMINTHIASIS; HUMORAL IMMUNITY; IMMUNIZATION; IMMUNOGENICITY; INFECTION CONTROL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHISTOSOMIASIS; SCHISTOSOMIASIS MANSONI; SPLEEN CELL; TH2 CELL;

EID: 84877124369     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.58     Document Type: Article

References (40)

1. Araujo-Montoya BO, Rofatto HK, Tararam CA, Farias LP, Oliveira KC, Verjovski-Almeida S, Wilson RA, Leite LC. 2011. Schistosoma mansoni: molecular characterization of Alkaline Phosphatase and expression patterns across life cycle stages. Experimental Parasitology 129:284-291 DOI 10.1016/j.exppara.2011.07.008.
2. Bergquist NR. 2002. Schistosomiasis: from risk assessment to control. Trends in Parasitology 18:309-314 DOI 10.1016/S1471-4922(02)02301-2.
3. Berriman M, Haas BJ, LoVerde PT,Wilson RA, Dillon GP, Cerqueira GC,Mashiyama ST, Al-Lazikani B, Andrade LF, Ashton PD, Aslett MA, Bartholomeu DC, Blandin G, Caffrey CR, Coghlan A, Coulson R, Day TA, Delcher A, DeMarco R, Djikeng A, Eyre T, Gamble JA, Ghedin E, Gu Y, Hertz-Fowler C, Hirai H, Hirai Y, Houston R, Ivens A, Johnston DA, Lacerda D,Macedo CD,McVeigh P, Ning Z, Oliveira G, Overington JP, Parkhill J, Pertea M, Pierce RJ, Protasio AV, Quail MA, Rajandream MA, Rogers J, Sajid M, Salzberg SL, Stanke M, Tivey AR,White O,Williams DL,Wortman J,Wu W, Zamanian M, Zerlotini A, Fraser-Liggett CM, Barrell BG, El-Sayed NM. 2009. The genome of the blood fluke Schistosoma mansoni. Nature 460:352-358 DOI 10.1038/nature08160.
4. Bhardwaj R, Krautz-Peterson G, Da'dara A, Tzipori S, Skelly PJ. 2011. Tegumental phosphodiesterase SmNPP-5 is a virulence factor for schistosomes. Infection and Immunity 79:4276-4284 DOI 10.1128/IAI.05431-11.
5. Bhardwaj R, Skelly PJ. 2009. Purinergic signaling and immune modulation at the schistosome surface? Trends in Parasitology 25:256-260 DOI 10.1016/j.pt.2009.03.004.
6. Bhardwaj R, Skelly PJ. 2011. Characterization of schistosome tegumental alkaline phosphatase (SmAP). PLoS Neglected Tropical Diseases 5:e1011 DOI 10.1371/journal.pntd.0001011.
7. Braschi S, Curwen RS, Ashton PD, Verjovski-Almeida S,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.
8. Braschi S,Wilson RA. 2006. Proteins exposed at the adult schistosome surface revealed by biotinylation. Molecular and Cellular Proteomics 5:347-356 DOI 10.1074/mcp.M500287-MCP200.
9. Brindley PJ, Sher A. 1987. The chemotherapeutic effect of Praziquantel against Schistosoma mansoni is dependent on host antibody response. Journal of Immunology 139:215-220.
10. Brindley PJ, Strand M, Norden AP, Sher A. 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 DOI 10.1016/0166-6851(89)90001-7.
11. Cardoso FC,Macedo GC, Gava E, Kitten GT,Mati VL, deMelo AL, Caliari MV, Almeida GT, Venancio TM, Verjovski-Almeida S, Oliveira SC. 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.
12. Castro-Borges W, Dowle A, Curwen RS, Thomas-Oates J,Wilson RA. 2011a. Enzymatic shaving of the tegument surface of live schistosomes for proteomic analysis: a rational approach to select vaccine candidates. PLoS Neglected Tropical Diseases 5:e993 DOI 10.1371/journal.pntd.0000993.
13. Castro-Borges W, Simpson DM, Dowle A, Curwen RS, Thomas-Oates J, Beynon RJ,Wilson RA. 2011b. 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.
14. Curwen RS, Ashton PD, Johnston DA,Wilson RA. 2004. The Schistosoma mansoni soluble proteome: a comparison across four life-cycle stages. Molecular and Biochemical Parasitology 138:57-66 DOI 10.1016/j.molbiopara.2004.06.016.
15. DeMarco R, Kowaltowski AT,Mortara RA, Verjovski-Almeida S. 2003. Molecular characterization and immunolocalization of Schistosoma mansoni ATP-diphosphohydrolase. Biochemical and Biophysical Research Communications 307:831-838 DOI 10.1016/S0006-291X(03)01268-3.
16. Doenhoff MJ,Modha J, Lambertucci JR. 1988. Anti-schistosome chemotherapy enhanced by antibodies specific for a parasite esterase. Immunology 65:507-510.
17. El Ridi R, Tallima H. 2012. Vaccine-induced protection against murine Schistosomiasis mansoni with larval excretory-secretory antigens and papain or type-2 cytokines. Journal of Parasitology (in press).
18. Engels D, Chitsulo L,Montresor A, Savioli L. 2002. The global epidemiological situation of schistosomiasis and new approaches to control and research. ACTA Tropica 82:139-146 DOI 10.1016/S0001-706X(02)00045-1.
19. Fallon PG, Doenhoff MJ. 1995. Active immunization of mice with Schistosoma mansoni worm membrane antigens enhances efficacy of Praziquantel. Parasite Immunology 17:261-268 DOI 10.1111/j.1365-3024.1995.tb01024.x.
20. Fallon PG, Smith P, Nicholls T,Modha J, Doenhoff MJ. 1994. Praziquantel-induced exposure of Schistosoma mansoni alkaline phosphatase: drug-antibody synergy which acts preferentially against female worms. Parasite Immunology 16:529-535 DOI 10.1111/j.1365-3024.1994.tb00307.x.
21. Fallon PG, Sturrock RF, Niang AC, Doenhoff MJ. 1995. Short report: diminished susceptibility to Praziquantel in a Senegal isolate of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 53:61-62.
22. Hoffmann KF, James SL, Cheever AW,Wynn TA. 1999. Studies with double cytokine-deficient mice reveal that highly polarized Th1- and Th2-type cytokine and antibody responses contribute equally to vaccine-induced immunity to Schistosoma mansoni. Journal of Immunology 163:927-938.
23. Hu W, Yan Q, Shen DK, Liu F, Zhu ZD, Song HD, Xu XR,Wang ZJ, Rong YP, Zeng LC,Wu J, Zhang X,Wang JJ, Xu XN,Wang SY, Fu G, Zhang XL,Wang ZQ, Brindley PJ,McManus DP, Xue CL, Feng Z, Chen Z, Han ZG. 2003. Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nature Genetics 35:139-147 DOI 10.1038/ng1236.
24. Ismail M, Botros S,Metwally A,William S, Farghally A, Tao LF, Day TA, Bennett JL. 1999. Resistance to Praziquantel: direct evidence from Schistosoma mansoni isolated from Egyptian villagers. American Journal of Tropical Medicine and Hygiene 60:932-935.
25. Levano-Garcia J,Mortara RA, Verjovski-Almeida S, DeMarco R. 2007. Characterization of Schistosoma mansoni ATPDase2 gene, a novel apyrase family member. Biochemical and Biophysical Research Communications 352:384-389 DOI 10.1016/j.bbrc.2006.11.023.
26. Liang YS, Coles GC, Dai JR, Zhu YC, Doenhoff MJ. 2002. Adult worm tegumental damage and egg-granulomas in Praziquantel-resistant and -susceptible Schistosoma mansoni treated in vivo. Journal of Helminthology 76:327-333 DOI 10.1079/JOH2002135.
27. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408 DOI 10.1006/meth.2001.1262.
28. Martins VP, Pinheiro CS, Figueiredo BC, Assis NR,Morais SB, Caliari MV, Azevedo V, Castro-Borges W,Wilson RA, Oliveira SC. 2012. Vaccination with enzymatically cleaved GPI-anchored proteins from Schistosoma mansoni induces protection against challenge infection. Clinics in Developmental Immunology 2012:01-11 DOI 10.1155/2012/962538.
29. Moraes J, Nascimento C, Lopes PO, Nakano E, Yamaguchi LF, Kato MJ, Kawano T. 2011. Schistosoma mansoni: in vitro schistosomicidal activity of piplartine. Experimental Parasitology 127:357-364 DOI 10.1016/j.exppara.2010.08.021.
30. Roberts SM,MacGregor AN, Vojvodic M,Wells E, Crabtree JE,Wilson RA. 1983. Tegument surface membranes of adult Schistosoma mansoni: development of a method for their isolation. Molecular and Biochemical Parasitology 9:105-127 DOI 10.1016/0166-6851(83)90104-4.
31. Rofatto HK, Tararam CA, BorgesWC,Wilson RA, Leite LC, Farias LP. 2009. Characterization of phosphodiesterase-5 as a surface protein in the tegument of Schistosoma mansoni. Molecular and Biochemical Parasitology 166:32-41 DOI 10.1016/j.molbiopara.2009.02.006.
32. Skelly PJ,Wilson RA. 2006. Making sense of the schistosome surface. Advances in Parasitology 63:185-284 DOI 10.1016/S0065-308X(06)63003-0.
33. Steinmann P, Keiser J, Bos R, Tanner M, 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.
34. Teixeira de Melo T, Michel de Araujo J, Do Valle Duraes F, Caliari MV, Oliveira SC, Coelho PM, Fonseca CT. 2010. Immunization with newly transformed Schistosoma mansoni schistosomula tegument elicits tegument damage, reduction in egg and parasite burden. Parasite Immunology 32:749-759 DOI 10.1111/j.1365-3024.2010.01244.x.
35. van BalkomBW, van Gestel RA, Brouwers JF, Krijgsveld J, Tielens AG, Heck AJ, van Hellemond JJ. 2005. Mass spectrometric analysis of the Schistosoma mansoni tegumental sub-proteome. Journal of Proteome Research 4:958-966 DOI 10.1021/pr050036w.
36. Verjovski-Almeida S, DeMarco R,Martins EA, Guimaraes PE, Ojopi EP, Paquola AC, Piazza JP, Nishiyama MY Jr, Kitajima JP, Adamson RE, Ashton PD, Bonaldo MF, Coulson PS, Dillon GP, Farias LP, Gregorio SP, Ho PL, Leite RA,Malaquias LC,Marques RC, Miyasato PA, Nascimento AL, Ohlweiler FP, Reis EM, Ribeiro MA, Sa RG, Stukart GC, Soares MB, Gargioni C, Kawano T, Rodrigues V,Madeira AM,Wilson RA,Menck CF, Setubal JC, Leite LC, Dias-Neto E. 2003. Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nature Genetics 35:148-157 DOI 10.1038/ng1237.
37. Wilson RA, Coulson PS. 1999. Strategies for a schistosome vaccine: can we manipulate the immune response effectively? Microbes and Infection 1:535-543 DOI 10.1016/S1286-4579(99)80093-8.
38. Zhang M, Han Y, Zhu Z, Li D, Hong Y,Wu X, Fu Z, Lin J. 2012a. Cloning, expression, and characterization of Schistosoma japonicum tegument protein phosphodiesterase-5. Parasitology Research 110(2):775-786 DOI 10.1007/s00436-011-2552-8.
39. Zhang Z, Xu H, Gan W, Zeng S, Hu X. 2012b. Schistosoma japonicum calcium-binding tegumental protein SjTP22.4 immunization confers praziquantel schistosomulumicide and antifecundity effect in mice. Vaccine 30:5141-5150 DOI 10.1016/j.vaccine.2012.05.056.
40. Zhou Y, Zheng H, Chen Y, Zhang L,Wang K, Guo J, Huang Z, Zhang B, Huang W, Jin K, Dou T, Hasegawa M,Wang L, Zhang Y, Zhou J, Tao L, Cao Z, Li Y, Vinar T, Brejova B, Brown D, Li M,Miller DJ, Hu W,Wang ZQ, Zhang QH, Song HD, Chen S, Xu X, Xu B, Ju C, Huang Y, Feng Z, Ren S,Wang Y, Gu W, Kang H, Chen J, Chen X, Yan J,Wang B, Lv X, Jin L, Pu S, Zhang X, Zhang W, Hu Q, Zhu G,Wang J, Yu J, Yang H, Ning Z, Beriman M,Wei CL, Ruan Y, Zhao G, Liu F, Lu G, Brindley PJ,McManus DP, Blair D, Zhong Y,Wang S, Han ZG, Chen Z. 2009. The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460:345-351 DOI 10.1038/nature08140.