Tegumental phosphodiesterase SmNPP-5 is a virulence factor for schistosomes

Infection and Immunity

Volumn 79, Issue 10, 2011, Pages 4276-4284

  Bhardwaj, Rita ^a   Krautz Peterson, Greice ^a   Da'dara, Akram ^a   Tzipori, Saul ^a   Skelly, Patrick J ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELMINTH PROTEIN; PHOSPHODIESTERASE; SMNPP 5 PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLONING; CONTROLLED STUDY; FEMALE; GENE SILENCING; HUMAN; HYDROLYSIS; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE TEST; IMMUNOGOLD LABELING; MALE; MOUSE; NONHUMAN; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SCHISTOSOMA; SCHISTOSOMULUM; WESTERN BLOTTING; WORM TEGUMENT;

AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; FEMALE; HELMINTH PROTEINS; MALE; MICE; MICROSCOPY, IMMUNOELECTRON; MOLECULAR SEQUENCE DATA; PHOSPHORIC DIESTER HYDROLASES; POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SEQUENCE ANALYSIS, DNA; VIRULENCE; VIRULENCE FACTORS;

EID: 80855127601     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05431-11     Document Type: Article

References (35)

1. Bartlett, D. W., and M. E. Davis. 2006. Insights into the kinetics of siRNAmediated gene silencing from live-cell and live-animal bioluminescent imaging. Nucleic Acids Res. 34:322-333.
2. Basch, P. F. 1981. Cultivation of Schistosoma mansoni in vitro. I. Establishment of cultures from cercariae and development until pairing. J. Parasitol. 67:179-185.
3. Basch, P. F. 1990. Why do schistosomes have separate sexes? Parasitol. Today 6:160-163.
4. Bhardwaj, R., and P. J. Skelly. 2011. Characterization of Schistosome Tegumental Alkaline Phosphatase (SmAP). PLoS Negl. Trop. Dis. 5:e1011.
5. Bhardwaj, R., and P. J. Skelly. 2009. Purinergic signaling and immune modulation at the schistosome surface? Trends Parasitol. 25:256-260.
6. Braschi, S., W. C. Borges, and R. A. Wilson. 2006. Proteomic analysis of the schistosome tegument and its surface membranes. Mem. Inst. Oswaldo Cruz 101(Suppl. 1):205-212.
7. Braschi, S., R. S. Curwen, P. D. Ashton, S. Verjovski-Almeida, and A. Wilson. 2006. The tegument surface membranes of the human blood parasite Schistosoma mansoni: a proteomic analysis after differential extraction. Proteomics 6:1471-1482.
8. Braschi, S., and R. A. Wilson. 2006. Proteins exposed at the adult schistosome surface revealed by biotinylation. Mol. Cell Proteomics 5:347-356.
9. Castro-Borges, W., A. Dowle, R. S. Curwen, J. Thomas-Oates, and R. A. Wilson. 2011. Enzymatic shaving of the tegument surface of live schistosomes for proteomic analysis: a rational approach to select vaccine candidates. PLoS Negl. Trop. Dis. 5:e993.
10. Cesari, I. M. 1974. Schistosoma mansoni: distribution and characteristics of alkaline and acid phosphatase. Exp. Parasitol. 36:405-414.
11. Cesari, I. M., A. J. Simpson, and W. H. Evans. 1981. Properties of a series of tegumental membrane-bound phosphohydrolase activities of Schistosoma mansoni. Biochem. J. 198:467-473.
12. Correnti, J. M., P. J. Brindley, and E. J. Pearce. 2005. Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth. Mol. Biochem. Parasitol. 143:209-215.
13. Faghiri, Z., et al. 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.
14. Gryseels, B., K. Polman, J. Clerinx, and L. Kestens. 2006. Human schistosomiasis. Lancet 368:1106-1118.
15. Hackett, F. 1993. The culture of Schistosoma mansoni and production of life cycle stages. Methods Mol. Biol. 21:89-99.
16. Jiang, J., P. J. Skelly, C. B. Shoemaker, and J. P. Caulfield. 1996. Schistosoma mansoni: the glucose transport protein SGTP4 is present in tegumental multilamellar bodies, discoid bodies, and the surface lipid bilayers. Exp. Parasitol. 82:201-210.
17. Krautz-Peterson, G., et al. 2007. Amino Acid Transport in Schistosomes: Characterization of the Permease Heavy Chain SPRM1hc. J. Biol. Chem. 282:21767-21775.
18. Krautz-Peterson, G., M. Radwanska, D. Ndegwa, C. B. Shoemaker, and P. J. Skelly. 2007. Optimizing gene suppression in schistosomes using RNA interference. Mol. Biochem. Parasitol. 153:194-202.
19. Krautz-Peterson, 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.
20. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408.
21. Mclaren, D. J., and D. J. Hockley. 1977. Blood flukes have a double outer membrane. Nature 269:147-149.
22. Ndegwa, D., G. Krautz-Peterson, and P. J. Skelly. 2007. Protocols for gene silencing in schistosomes. Exp. Parasitol. 117:284-291.
23. Payares, G., D. J. McLaren, W. H. Evans, and S. R. Smithers. 1985. Antigenicity and immunogenicity of the tegumental outer membrane of adult Schistosoma mansoni. Parasite Immunol. 7:45-61.
24. Pinheiro, C. S., et al. 2009. Characterization and binding affinities of SmLANP: a new Schistosoma mansoni member of the ANP32 family of regulatory proteins. Mol. Biochem. Parasitol. 165:95-102.
25. Roberts, S. M., R. Aitken, M. Vojvodic, E. Wells, and R. A. Wilson. 1983. Identification of exposed components on the surface of adult Schistosoma mansoni by lactoperoxidase-catalysed iodination. Mol. Biochem. Parasitol. 9:129-143.
26. Rofatto, H. K., et al. 2009. Characterization of phosphodiesterase-5 as a surface protein in the tegument of Schistosoma mansoni. Mol. Biochem. Parasitol. 166:32-41.
27. Skelly, P., and R. Wilson. 2006. Making Sense of the Schistosome Surface. Advances in Parasitology 63:185-284.
28. Skelly, P. J., and C. B. Shoemaker. 1996. Rapid appearance and asymmetric distribution of glucose transporter SGTP4 at the apical surface of intramammalian-stage Schistosoma mansoni. Proc. Natl. Acad. Sci. U. S. A. 93:3642-3646.
29. Skelly, P. J., and C. B. Shoemaker. 2001. Schistosoma mansoni proteases Sm31 (cathepsin B) and Sm32 (legumain) are expressed in the cecum and protonephridia of cercariae. J. Parasitol. 87:1218-1221.
30. Stefan, C., S. Jansen, and M. Bollen. 2005. NPP-type ectophosphodiesterases: unity in diversity. Trends Biochem. Sci. 30:542-550.
31. Terkeltaub, R. 2006. Physiologic and pathologic functions of the NPP nucleotide pyrophosphatase/phosphodiesterase family focusing on NPP1 in calcification. Purinergic Signal. 2:371-377.
32. Tran, M. H., et al. 2010. Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover. PLoS Pathog. 6:e1000840.
33. van Balkom, B. W., et al. 2005. Mass spectrometric analysis of the Schistosoma mansoni tegumental sub-proteome. J. Proteome Res. 4:958-966.
34. Vennervald, B. J., and D. W. Dunne. 2004. Morbidity in schistosomiasis: an update. Curr. Opin. Infect. Dis. 17:439-447.
35. Wilson, R. A., and P. E. Barnes. 1974. The tegument of Schistosoma mansoni: observations on the formation, structure and composition of cytoplasmic inclusions in relation to tegument function. Parasitology 68:239-258.