Schistosome Syntenin Partially Protects Vaccinated Mice against Schistosoma mansoni Infection

PLoS Neglected Tropical Diseases

Volumn 8, Issue 8, 2014, Pages

  Figueiredo, Barbara C ^a,b,c   Assis, Natan R G ^a,b   Morais, Suellen B ^a,b   Ricci, Natasha D ^a,b   Pinheiro, Carina S ^a,b,d   Martins, Vicente P ^a,b,e   Bicalho, Rodrigo M ^a,b   Da'dara, Akram A ^c   Skelly, Patrick J ^c   Oliveira, Sergio C ^a,b  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b CNPq/MCT   (Brazil)

^c TUFTS UNIVERSITY   (United States)

^d FEDERAL UNIVERSITY OF BAHIA   (Brazil)

^e INSTITUTO DE CIÊNCIAS BIOLÓGICAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CONCANAVALIN A; GAMMA INTERFERON; RECOMBINANT VACCINE; SCHISTOSOME SYNTENIN; SMALL INTERFERING RNA; SYNTENIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; PARASITE ANTIGEN; VACCINE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE; GENE SILENCING; HELMINTHIASIS; HISTOPATHOLOGY; IMMUNIZATION; IMMUNOLOCALIZATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHISTOSOMIASIS MANSONI; SERIAL ANALYSIS OF GENE EXPRESSION; SMSYNT GENE; TH1 CELL; WESTERN BLOTTING; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; CHEMISTRY; CLASSIFICATION; GENETICS; IMMUNOLOGY; MOLECULAR GENETICS; PARASITOLOGY; SCHISTOSOMA MANSONI; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, HELMINTH; FEMALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SEQUENCE ALIGNMENT; SYNTENINS; VACCINES;

EID: 84926632696     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003107     Document Type: Article

References (52)

1. van der Werf MJ, de Vlas SJ, Brooker S, Looman CW, Nagelkerke NJ, et al. (2003) Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop 86: 125–139.
2. Lustigman S, Prichard RK, Gazzinelli A, Grant WN, Boatin BA, et al. (2012) A research agenda for helminth diseases of humans: the problem of helminthiases. PLoS Negl Trop Dis 6: e1582.
3. 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 Infect Dis 6: 411–425.
4. WHO (2010) Working to overcome the global impact of neglected tropical diseases. First WHO report on neglected tropical diseases 129–135.
5. Prichard RK, Basanez MG, Boatin BA, McCarthy JS, Garcia HH, et al. (2012) A research agenda for helminth diseases of humans: intervention for control and elimination. PLoS Negl Trop Dis 6: e1549.
6. McManus DP, Loukas A, (2008) Current status of vaccines for schistosomiasis. Clin Microbiol Rev 21: 225–242.
7. Harder A, (2002) Chemotherapeutic approaches to trematodes (except schistosomes) and cestodes: current level of knowledge and outlook. Parasitol Res 88: 587–590.
8. Mahmoud A, Zerhouni E, (2009) Neglected tropical diseases: moving beyond mass drug treatment to understanding the science. Health Aff (Millwood) 28: 1726–1733.
9. Gryseels B, (2012) Schistosomiasis. Infect Dis Clin North Am 26: 383–397.
10. McManus DP, (2012) Schistosomiasis in 2012: current status and key research priorities required for control leading to elimination. Expert Rev Anti Infect Ther 10: 1233–1236.
11. Gray DJ, McManus DP, Li Y, Williams GM, Bergquist R, et al. (2010) Schistosomiasis elimination: lessons from the past guide the future. Lancet Infect Dis 10: 733–736.
12. Bergquist NR, (2002) Schistosomiasis: from risk assessment to control. Trends Parasitol 18: 309–314.
13. Chitsulo L, Loverde P, Engels D, (2004) Schistosomiasis. Nat Rev Microbiol 2: 12–13.
14. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, et al. (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460: 352–358.
15. Cardoso FC, Macedo GC, Gava E, Kitten GT, Mati VL, et al. (2008) Schistosoma mansoni tegument protein Sm29 is able to induce a Th1-type of immune response and protection against parasite infection. PLoS Negl Trop Dis 2: e308.
16. Zimmermann P, Tomatis D, Rosas M, Grootjans J, Leenaerts I, et al. (2001) Characterization of syntenin, a syndecan-binding PDZ protein, as a component of cell adhesion sites and microfilaments. Mol Biol Cell 12: 339–350.
17. Zimmermann P, Zhang Z, Degeest G, Mortier E, Leenaerts I, et al. (2005) Syndecan recycling [corrected] is controlled by syntenin-PIP2 interaction and Arf6. Dev Cell 9: 377–388.
18. Beekman JM, Coffer PJ, (2008) The ins and outs of syntenin, a multifunctional intracellular adaptor protein. J Cell Sci 121: 1349–1355.
19. Grootjans JJ, Zimmermann P, Reekmans G, Smets A, Degeest G, et al. (1997) Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc Natl Acad Sci U S A 94: 13683–13688.
20. Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, et al. (2012) Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol 14: 677–685.
21. Sales AD, Brito IR, de Lima LF, Lobo CH, Duarte AB, et al. (2014) Expression and localization of Aquaporin 3 (AQP3) in folliculogenesis of ewes. Acta Histochem 116: 831–837.
22. Boukerche H, Su ZZ, Emdad L, Baril P, Balme B, et al. (2005) mda-9/Syntenin: a positive regulator of melanoma metastasis. Cancer Res 65: 10901–10911.
23. Helmke BM, Polychronidis M, Benner A, Thome M, Arribas J, et al. (2004) Melanoma metastasis is associated with enhanced expression of the syntenin gene. Oncol Rep 12: 221–228.
24. Enz R, Croci C, (2003) Different binding motifs in metabotropic glutamate receptor type 7b for filamin A, protein phosphatase 1C, protein interacting with protein kinase C (PICK) 1 and syntenin allow the formation of multimeric protein complexes. Biochem J 372: 183–191.
25. Koroll M, Rathjen FG, Volkmer H, (2001) The neural cell recognition molecule neurofascin interacts with syntenin-1 but not with syntenin-2, both of which reveal self-associating activity. J Biol Chem 276: 10646–10654.
26. Basch PF, (1981) Cultivation of Schistosoma mansoni in vitro. I. Establishment of cultures from cercariae and development until pairing. J Parasitol 67: 179–185.
27. Pinheiro CS, Martins VP, Assis NR, Figueiredo BC, Morais SB, et al. (2011) Computational vaccinology: an important strategy to discover new potential S. mansoni vaccine candidates. J Biomed Biotechnol 2011: 503068.
28. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725–2729.
29. 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.
30. Krautz-Peterson G, Simoes M, Faghiri Z, Ndegwa D, Oliveira G, et al. (2010) Suppressing glucose transporter gene expression in schistosomes impairs parasite feeding and decreases survival in the mammalian host. PLoS Pathog 6: e1000932.
31. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254.
32. Fonseca CT, Brito CF, Alves JB, Oliveira SC, (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.
33. Figueiredo BC, NR DEA, SB DEM, Martins VP, Ricci ND, et al. (2014) Immunological characterization of a chimeric form of Schistosoma mansoni aquaporin in the murine model. Parasitology 1–12.
34. Drummond MG, Calzavara-Silva CE, D'Astolfo DS, Cardoso FC, Rajao MA, et al. (2009) Molecular characterization of the Schistosoma mansoni zinc finger protein SmZF1 as a transcription factor. PLoS Negl Trop Dis 3: e547.
35. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.
36. Towbin H, Staehelin T, Gordon J, (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76: 4350–4354.
37. Faghiri Z, Skelly PJ, (2009) The role of tegumental aquaporin from the human parasitic worm, Schistosoma mansoni, in osmoregulation and drug uptake. FASEB J 23: 2780–2789.
38. Lopes DO, Paiva LF, Martins MA, Cardoso FC, Rajao MA, et al. (2009) Sm21.6 a novel EF-hand family protein member located on the surface of Schistosoma mansoni adult worm that failed to induce protection against challenge infection but reduced liver pathology. Vaccine 27: 4127–4135.
39. Pinho JM, Cardoso FC, Lopes DO, Pinheiro CS, Caliari MV, et al. (2010) Immunization with SmIg, a novel tegument protein from Schistosoma mansoni, fails to induce protection in mice but reduces liver pathology. Parasitology 137: 1079–1088.
40. Martins VP, Pinheiro CS, Figueiredo BC, Assis NR, Morais SB, et al. (2012) Vaccination with enzymatically cleaved GPI-anchored proteins from Schistosoma mansoni induces protection against challenge infection. Clin Dev Immunol 2012: 962538.
41. Farias LP, Cardoso FC, Miyasato PA, Montoya BO, Tararam CA, et al. (2010) Schistosoma mansoni Stomatin like protein-2 is located in the tegument and induces partial protection against challenge infection. PLoS Negl Trop Dis 4: e597.
42. Garcia TC, Fonseca CT, Pacifico LG, Duraes Fdo V, Marinho FA, et al. (2008) Peptides containing T cell epitopes, derived from Sm14, but not from paramyosin, induce a Th1 type of immune response, reduction in liver pathology and partial protection against Schistosoma mansoni infection in mice. Acta Trop 106: 162–167.
43. Ponting CP, (1997) Evidence for PDZ domains in bacteria, yeast, and plants. Protein Sci 6: 464–468.
44. Nourry C, Grant SG, Borg JP, (2003) PDZ domain proteins: plug and play!. Sci STKE 2003: RE7.
45. Livak F, Petrie HT, (2001) Somatic generation of antigen-receptor diversity: a reprise. Trends Immunol 22: 608–612.
46. Slack JL, Bi W, Livak KJ, Beaubier N, Yu M, et al. (2001) Pre-clinical validation of a novel, highly sensitive assay to detect PML-RARalpha mRNA using real-time reverse-transcription polymerase chain reaction. J Mol Diagn 3: 141–149.
47. Latif S, Bauer-Sardina I, Ranade K, Livak KJ, Kwok PY, (2001) Fluorescence polarization in homogeneous nucleic acid analysis II: 5′-nuclease assay. Genome Res 11: 436–440.
48. Martins VP, Morais SB, Pinheiro CS, Assis NR, Figueiredo BC, et al. (2014) Sm10.3, a Member of the Micro-Exon Gene 4 (MEG-4) Family, Induces Erythrocyte Agglutination In Vitro and Partially Protects Vaccinated Mice against Schistosoma mansoni Infection. PLoS Negl Trop Dis 8: e2750.
49. Jankovic D, Wynn TA, Kullberg MC, Hieny S, Caspar P, et al. (1999) Optimal vaccination against Schistosoma mansoni requires the induction of both B cell- and IFN-gamma-dependent effector mechanisms. J Immunol 162: 345–351.
50. Smythies LE, Coulson PS, Wilson RA, (1992) Monoclonal antibody to IFN-gamma modifies pulmonary inflammatory responses and abrogates immunity to Schistosoma mansoni in mice vaccinated with attenuated cercariae. J Immunol 149: 3654–3658.
51. Pearce EJ, MacDonald AS, (2002) The immunobiology of schistosomiasis. Nat Rev Immunol 2: 499–511.
52. Sadler CH, Rutitzky LI, Stadecker MJ, Wilson RA, (2003) IL-10 is crucial for the transition from acute to chronic disease state during infection of mice with Schistosoma mansoni. Eur J Immunol 33: 880–888.