Table of Contents
ISRN Parasitology
Volume 2013, Article ID 247036, 10 pages
http://dx.doi.org/10.5402/2013/247036
Review Article

Applications of RNA Interference in Schistosomiasis: Gene Function Identification and Development of New Therapies

1Department of Biology, Faculty of Philosophy, Sciences and Languages of Ribeirao Preto, University of Sao Paulo (USP), 14040 901 Ribeirao Preto, SP, Brazil
2Department of Animal Biology, Institute of Biology, University of Campinas (UNICAMP), 13083-862 Campinas, SP, Brazil
3Department of Medical Genetics, School of Medical Sciences, University of Campinas (UNICAMP), 13083-887 Campinas, SP, Brazil

Received 17 October 2012; Accepted 1 November 2012

Academic Editors: C. Araujo, G. Lochnit, and G. Mkoji

Copyright © 2013 Tiago Campos Pereira et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. M. Merrick, A. Osman, J. Tsai, J. Quackenbush, P. T. LoVerde, and N. H. Lee, “The Schistosoma mansoni gene index: gene discovery and biology by reconstruction and analysis of expressed gene sequences,” Journal of Parasitology, vol. 89, no. 2, pp. 261–269, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Verjovski-Almeida, R. DeMarco, E. A. L. Martins et al., “Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni,” Nature Genetics, vol. 35, no. 2, pp. 148–157, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. R. S. Curwen, P. D. Ashton, D. A. Johnston, and R. A. Wilson, “The Schistosoma mansoni soluble proteome: a comparison across four life-cycle stages,” Molecular and Biochemical Parasitology, vol. 138, no. 1, pp. 57–66, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Berriman, B. J. Haas, P. T. LoVerde et al., “The genome of the blood fluke Schistosoma mansoni,” Nature, vol. 460, pp. 352–358, 2009. View at Google Scholar
  5. The Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium, “The Schistosoma japonicum genome reveals features of host-parasite interplay,” Nature, vol, vol. 460, pp. 345–351, 2009. View at Google Scholar
  6. N. D. Young, A. R. Jex, B. Li et al., “Whole-genome sequence of Schistosoma haematobium,” Nature Genetics, vol. 44, pp. 221–225, 2012. View at Google Scholar
  7. A. Fire, S. Xu, M. K. Montgomery, S. A. Kostas, S. E. Driver, and C. C. Mello, “Potent and specific genetic interference by double-stranded RNA in caenorhabditis elegans,” Nature, vol. 391, no. 6669, pp. 806–811, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. E. Check, “RNA therapy beckons as firms prepare for clinical trials,” Nature, vol. 429, no. 6994, p. 792, 2004. View at Google Scholar · View at Scopus
  9. R. Osborne, “Companies jostle for lead in RNAi, despite uncertainties,” Nature Biotechnology, vol. 25, no. 11, pp. 1191–1192, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Bonetta, “Three researchers developing therapies based on RNA interference talk about their experiences leaving academia for biotech companies,” BioTechniques, vol. 42, supplement 4, pp. S10–S16, 2007. View at Google Scholar · View at Scopus
  11. P. Lundin, “Is silence still golden? Mapping the RNAi patent landscape,” Nature Biotechnology, vol. 29, no. 6, pp. 493–497, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Goto, S. Blandin, J. Royet, J. M. Reichhart, and E. A. Levashina, “Silencing of Toll pathway components by direct injection of double-stranded RNA into Drosophila adult flies,” Nucleic Acids Research, vol. 31, no. 22, pp. 6619–6623, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. R. S. Kamath, M. Martinez-Campos, P. Zipperlen, A. G. Fraser, and J. Ahringer, “Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans,” Genome Biology, vol. 2, no. 1, Article ID RESEARCH0002, 2001. View at Google Scholar · View at Scopus
  14. C. F. Chuang and E. M. Meyerowitz, “Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 9, pp. 4985–4990, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. S. M. Elbashir, J. Harborth, W. Lendeckel, A. Yalcin, K. Weber, and T. Tuschl, “Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells,” Nature, vol. 411, no. 6836, pp. 494–498, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Yang, Y. Jin, P. Liu et al., “RNAi silencing of type V collagen in Schistosoma japonicumaffects parasite morphology, spawning, and hatching,” Parasitology Research, vol. 111, pp. 1251–1257, 2012. View at Google Scholar
  17. X. Zou, Y. M. Jin, P. P. Liu, Q. J. Wu, J. M. Liu, and J. J. Lin, “RNAi silencing of calcium-regulated heat-stable protein of 24 kDa in Schistosoma japonicum affects parasite growth,” Parasitology Research, vol. 108, no. 3, pp. 567–572, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Beckmann, T. Quack, C. Burmeister et al., “Schistosoma mansoni: signal transduction processes during the development of the reproductive organs,” Parasitology, vol. 137, no. 3, pp. 497–520, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Beckmann, C. Buro, C. Dissous, J. Hirzmann, and C. G. Grevelding, “The Syk kinase SmTK4 of Schistosoma mansoni is involved in the regulation of spermatogenesis and oogenesis,” PLoS Pathogens, vol. 6, no. 2, Article ID e1000769, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Grimm, K. L. Streetz, C. L. Jopling et al., “Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways,” Nature, vol. 441, no. 7092, pp. 537–541, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. M. D. White, M. Farmer, I. Mirabile, S. Brandner, J. Collinge, and G. R. Mallucci, “Single treatment with RNAi against prion protein rescues early neuronal dysfunction and prolongs survival in mice with prion disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 29, pp. 10238–10243, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. E. Herker, C. Harris, C. Hernandez et al., “Efficient hepatitis C virus particle formation requires diacylglycerol acyltransferase-1,” Nature Medicine, vol. 16, no. 11, pp. 1295–1298, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Luo and J. W. McBride, “Ehrlichia chaffeensis TRP32 interacts with host cell targets that influence intracellular survival,” Infection an Immunity, vol. 80, pp. 2297–2306, 2012. View at Google Scholar
  24. M. Moazeni, M. R. Khoramizadeh, P. Kordbacheh et al., “RNA-mediated gene silencing in Candida albicans: inhibition of hyphae formation by use of RNAi technology,” Mycopathologia, vol. 174, pp. 177–185, 2012. View at Google Scholar
  25. E. L. Telleria, M. R. Sant'Anna, J. R. Ortigão-Farias et al., “Caspar-like gene depletion reduces Leishmania infection in sand fly host Lutzomyia longipalpis,” The Journal of Biological Chemistry, vol. 287, pp. 12985–12993, 2012. View at Google Scholar
  26. G. Rinaldi, T. I. Okatcha, A. Popratiloff et al., “Genetic manipulation of Schistosoma haematobium, the neglected schistosome,” PLoS Neglected Tropical Diseases, vol. 5, Article ID e1348, 2011. View at Google Scholar
  27. G. Rinaldi, M. E. Morales, Y. N. Alrefaei et al., “RNA interference targeting leucine aminopeptidase blocks hatching of Schistosoma mansoni eggs,” Molecular and Biochemical Parasitology, vol. 167, no. 2, pp. 118–126, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. M. M. Mourão, N. Dinguirard, G. R. Franco, and T. P. Yoshino, “Phenotypic screen of early-developing larvae of the blood fluke, Schistosoma mansoni, using RNA interference,” PLoS Neglected Tropical Diseases, vol. 3, no. 8, article e502, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. N. Dinguirard and T. P. Yoshino, “Potential role of a CD36-like class B scavenger receptor in the binding of modified low-density lipoprotein (acLDL) to the tegumental surface of Schistosoma mansoni sporocysts,” Molecular and Biochemical Parasitology, vol. 146, no. 2, pp. 219–230, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. J. P. Boyle, X. J. Wu, C. B. Shoemaker, and T. P. Yoshino, “Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts,” Molecular and Biochemical Parasitology, vol. 128, no. 2, pp. 205–215, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. M. H. Tran, T. C. Freitas, L. Cooper et al., “Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover,” PLoS Pathogens, vol. 6, no. 4, Article ID e1000840, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. R. S. Kasinathan, W. M. Morgan, and R. M. Greenberg, “Genetic knockdown and pharmacological inhibition of parasite multidrug resistance transporters disrupts egg production in Schistosoma mansoni,” PLoS Neglected Tropical Diseases, vol. 5, article e1425, 2011. View at Google Scholar
  33. M. E. Morales, G. Rinaldi, G. N. Gobert, K. J. Kines, J. F. Tort, and P. J. Brindley, “RNA interference of Schistosoma mansoni cathepsin D, the apical enzyme of the hemoglobin proteolysis cascade,” Molecular and Biochemical Parasitology, vol. 157, no. 2, pp. 160–168, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. T. C. Pereira, V. D. B. Pascoal, R. B. Marchesini et al., “Schistosoma mansoni: evaluation of an RNAi-based treatment targeting HGPRTase gene,” Experimental Parasitology, vol. 118, no. 4, pp. 619–623, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. G. Krautz-Peterson, M. Simoes, Z. Faghiri et al., “Suppressing glucose transporter gene expression in schistosomes impairs parasite feeding and decreases survival in the mammalian host,” PLoS Pathogens, vol. 6, no. 6, Article ID e1000932, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. R. Bhardwaj, G. Krautz-Peterson, A. Da'dara, S. Tzipori, and P. J. Skelly, “Tegumental phosphodiesterase SmNPP-5 is a virulence factor for schistosomes,” Infection an Immunity, vol. 79, pp. 4276–4284, 2011. View at Google Scholar
  37. T. C. Freitas, E. Jung, and E. J. Pearce, “TGF-beta signaling controls embryo development in the parasitic flatworm Schistosoma mansoni,” PLoS Pathogens, vol. 3, no. 4, article e52, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. A. N. Kuntz, E. Davioud-Charvet, A. A. Sayed et al., “Thioredoxin glutathione reductase from Schistosoma mansoni: an essential parasite enzyme and a key drug target,” PLoS Medicine, vol. 4, article e206, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. B. E. Swierczewski and S. J. Davies, “A schistosome cAMP-dependent protein kinase catalytic subunit is essential for parasite viability,” PLoS Neglected Tropical Diseases, vol. 3, no. 8, article e505, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. M. D. M. Mourão, N. Dinguirard, G. R. Franco, and T. P. Yoshino, “Role of the endogenous antioxidant system in the protection of Schistosoma mansoni primary sporocysts against exogenous oxidative stress,” PLoS Neglected Tropical Diseases, vol. 3, no. 11, article e550, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. E. B. Tchoubrieva, P. C. Ong, R. N. Pike, P. J. Brindley, and B. H. Kalinna, “Vector-based RNA interference of cathepsin B1 in Schistosoma mansoni,” Cellular and Molecular Life Sciences, vol. 67, no. 21, pp. 3739–3748, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. He, G. Cai, Y. Ni, Y. Li, H. Zong, and L. He, “siRNA-mediated knockdown of two tyrosinase genes from Schistosoma japonicum cultured in vitro,” Experimental Parasitology, vol. 132, pp. 394–402, 2012. View at Google Scholar
  43. J. M. Correnti, P. J. Brindley, and E. J. Pearce, “Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth,” Molecular and Biochemical Parasitology, vol. 143, no. 2, pp. 209–215, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. J. F. Nabhan, F. El-Shehabi, N. Patocka, and P. Ribeiro, “The 26S proteasome in Schistosoma mansoni: bioinformatics analysis, developmental expression, and RNA interference (RNAi) studies,” Experimental Parasitology, vol. 117, no. 3, pp. 337–347, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. Z. Faghiri, S. M. R. Camargo, K. Huggel et al., “The tegument of the human parasitic worm Schistosoma mansoni as an excretory organ: the surface aquaporin SmAQP is a lactate transporter,” PLoS ONE, vol. 5, no. 5, Article ID e10451, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Knight, A. Miller, Y. Liu, P. Scaria, M. Woodle, and W. Ittiprasert, “Polyethyleneimine (pei) mediated sirna gene silencing in the Schistosoma mansoni snail host, biomphalaria glabrata,” PLoS Neglected Tropical Diseases, vol. 5, no. 7, Article ID e1212, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. P. C. Hanington, M. A. Forys, and E. S. Loker, “A somatically diversified defense factor, FREP3, is a determinant of snail resistance to schistosome infection,” PLoS Neglected Tropical Diseases, vol. 6, article e1591, 2012. View at Google Scholar
  48. J. J. Taylor, C. M. Krawczyk, M. Mohrs, and E. J. Pearce, “Th2 cell hyporesponsiveness during chronic murine schistosomiasis is cell intrinsic and linked to GRAIL expression,” The Journal of Clinical Investigation, vol. 119, no. 4, pp. 1019–1028, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. D. Shirane, K. Sugao, S. Namiki, M. Tanabe, M. Iino, and K. Hirose, “Enzymatic production of RNAi libraries from cDNAs,” Nature Genetics, vol. 36, no. 2, pp. 190–196, 2004. View at Publisher · View at Google Scholar · View at Scopus