Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T01:14:26.581Z Has data issue: false hasContentIssue false
  • English
  • Français

In vitro manipulation of gene expression in larval Schistosoma: a model for postgenomic approaches in Trematoda

Published online by Cambridge University Press:  07 December 2009

TIMOTHY P. YOSHINO ,
NATHALIE DINGUIRARD  and
MARINA DE MORAES MOURÃO
TIMOTHY P. YOSHINO*
Affiliation:
Department of Pathobiological Sciences, University of Wisconsin, Madison, WI53706, USA
NATHALIE DINGUIRARD
Affiliation:
Department of Pathobiological Sciences, University of Wisconsin, Madison, WI53706, USA
MARINA DE MORAES MOURÃO
Affiliation:
Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG – Brazil
*
*Corresponding author: Timothy P. Yoshino, PhD, Department of Pathobiological Sciences, University of Wisconsin, School of Veterinary Medicine, 2115 Observatory Drive, Madison, WI53706USA. Tel.: (608) 263-6002; Fax: (608) 262-7871; E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

With rapid developments in DNA and protein sequencing technologies, combined with powerful bioinformatics tools, a continued acceleration of gene identification in parasitic helminths is predicted, potentially leading to discovery of new drug and vaccine targets, enhanced diagnostics and insights into the complex biology underlying host-parasite interactions. For the schistosome blood flukes, with the recent completion of genome sequencing and comprehensive transcriptomic datasets, there has accumulated massive amounts of gene sequence data, for which, in the vast majority of cases, little is known about actual functions within the intact organism. In this review we attempt to bring together traditional in vitro cultivation approaches and recent emergent technologies of molecular genomics, transcriptomics and genetic manipulation to illustrate the considerable progress made in our understanding of trematode gene expression and function during development of the intramolluscan larval stages. Using several prominent trematode families (Schistosomatidae, Fasciolidae, Echinostomatidae), we have focused on the current status of in vitro larval isolation/cultivation as a source of valuable raw material supporting gene discovery efforts in model digeneans that include whole genome sequencing, transcript and protein expression profiling during larval development, and progress made in the in vitro manipulation of genes and their expression in larval trematodes using transgenic and RNA interference (RNAi) approaches.

Keywords

Trematodalarval stagesSchistosomain vitro culturegenometranscriptomegene manipulationtransgenesisRNA interference
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 3: Development and applications of cestode and trematode laboratory models , March 2010 , pp. 463 - 483
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adema, C. M., Léonard, P. M., DeJong, R. J., Day, H. L., Edwards, D. J., Burgett, G., Hertel, L. A. and Loker, E. S. (2000). Analysis of messages expressed by Echinostoma paraensei miracidia and sporocysts, obtained by random EST sequencing. Journal of Parasitology 86, 60–65.CrossRefGoogle ScholarPubMed
Ataev, G., Fournaier, A. and Coustau, C. (1998). Comparison of Echinostoma caproni mother sporocyst development in vivo and in vitro using Biomphalaria glabrata snails and a B. glabrata embryonic cell line. Journal of Parasitology 84, 227–235.CrossRefGoogle Scholar
Barakat, A., DiLoreto, D. S., Zhang, Y., Smith, C., Baier, K., Powell, W. A., Wheeler, N., Sederoff, R. and Carlson, J. E. (2009). Comparison of the transcriptomes of American chestnut (Castanea dentata) and Chinese chestnut (Castanea mollissima) in response to the chestnut blight infection. BMC Plant Biology 9, 51.CrossRefGoogle Scholar
Basch, P. F. (1991). Schistosomes – Development, Reproduction and Host Relations. Oxford University Press, New York and Oxford. 248 p.Google Scholar
Beckmann, S., Wippersteg, V., El-Bahay, A., Hirzmann, J., Oliveria, G. and Grevelding, C. G. (2007). Schistosoma mansoni: germ-line transformation approaches and actin-promoter analysis. Experimental Parasitology 117, 292–303.CrossRefGoogle ScholarPubMed
Bender, R. C., Bixler, L. M., Lerner, J. P. and Bayne, C. J. (2002). Schistosoma mansoni sporocysts in culture: host plasma hemoglobin contributes to in vitro oxidative stress. Journal of Parasitology 88, 14–18.CrossRefGoogle ScholarPubMed
Berriman, M., Haas, B. J., Loverde, P. T., Wilson, R. A., Dillon, G. P., Cerqueira, G. C., Mashiyama, S. T., Al-Lazikani, B., Andrade, L. F., Ashton, P. D., Aslett, M. A., Bartholomeu, D. C., Blandin, G., Caffrey, C. R., Coghlan, A., Coulson, R., Day, T. A., Delcher, A., Demarco, R., Djikeng, A., Eyre, T., Gamble, J. A., Ghedin, E., Gu, Y., Hertz-Fowler, C., Hirai, H., Hirai, Y., Houston, R., Ivens, A., Johnston, D. A., Lacerda, D., Macedo, C. D., McVeigh, P., Ning, Z., Oliveira, G., Overington, J. P., Parkhill, J., Pertea, M., Pierce, R. J., Protasio, A. V., Quail, M. A., Rajandream, M.A, Rogers, J., Sajid, M., Salzberg, S. L., Stanke, M., Tivey, A. R., White, O., Williams, D. L., Wortman, J., Wu, W., Zamanian, M., Zerlotini, A., Fraser-Liggett, C. M., Barrell, B. G., El-Sayed, N. M. (2009). The genome of the blood fluke Schistosoma mansoni. Nature 460, 352–358.CrossRefGoogle ScholarPubMed
Boyle, J. P., Wu, X. J., Shoemaker, C. B. and Yoshino, T. P. (2003). Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts. Molecular and Biochemical Parasitology 128, 205–215.CrossRefGoogle ScholarPubMed
Brindley, P. J. and Pearce, E. J. (2007). Genetic manipulation of schistosomes. International Journal for Parasitology 37, 465–473.CrossRefGoogle ScholarPubMed
Campbell, W. C. and Todd, A. C. (1955). In vitro metamorphosis of the miracidium of Fascioloides magna (Bassi, 1851) Ward, 1917. Transactions of the Americian Microscopical Society 74, 225–228.CrossRefGoogle Scholar
Chernin, E. (1963). Observations on hearts explanted in vitro from the snail Australorbis glabratus. Journal of Parasitology 49, 353–364.CrossRefGoogle ScholarPubMed
Coppin, J. F., Lefebvre, C., Caby, S., Cocquerelle, C., Vicogne, J., Coustau, C. and Dissous, C. (2002). Gene expression changes in Schistosoma mansoni sporocysts induced by Biomphalaria glabrata embryonic cells. Parasitology Research 89, 113–119.CrossRefGoogle ScholarPubMed
Correnti, J. M., Brindley, P. J. and Pearce, E. J. (2005). Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth. Molecular and Biochemical Parasitology 143, 209–215.CrossRefGoogle ScholarPubMed
Coustau, C., Ataev, G., Jourdane, J. and Yoshino, T. P. (1997). Schistosoma japonicum: in vitro cultivation of miracidium to daughter sporocyst using a Biomphalaria glabrata embryonic cell line. Experimental Parasitology 87, 77–87.CrossRefGoogle ScholarPubMed
Coustau, C. and Yoshino, T. P. (2000). Flukes without snails: advances in the in vitro cultivation of intramolluscan stages of trematodes. Experimental Parasitology 94, 62–66.CrossRefGoogle ScholarPubMed
Curwen, R. S., Ashton, P. D., Johnston, D. A. and Wilson, R. A. (2004). The Schistosoma mansoni soluble proteome: a comparison across four life-cycle stages. Molecular and Biochemistry Parasitology 138, 57–66.CrossRefGoogle ScholarPubMed
Curwen, R. S., Ashton, P. D., Sundaralingam, S. and Wilson, R. A. (2006). Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Molecular and Cellular Proteomics 5, 835–844.CrossRefGoogle ScholarPubMed
Diatchenko, L., Lau, Y. F., Campbell, A. P., Chenchik, A., Moqadam, F., Huang, B., Lukyanov, S., Lukyanov, K., Gurskaya, N., Sverdlov, E. D. and Siebert, P. D. (1996). Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proceedings of the National Academy of Sciences, USA 93, 6025–6030.CrossRefGoogle ScholarPubMed
Dillon, G. P., Illes, J. C., Isaacs, H. V. and Wilson, R. A. (2007). Patterns of gene expression in schistosomes: localization by whole mount in situ hybridization. Parasitology. 134, 1589–1597.CrossRefGoogle ScholarPubMed
Dinguirard, N. and Yoshino, T. P. (2006). 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 146, 219–230.CrossRefGoogle Scholar
El-Sayed, N. M., Bartholomeu, D., Ivens, A., Johnston, D. A. and LoVerde, P. T. (2004). Advances in schistosome genomics. Trends in Parasitolology 20, 154–157.CrossRefGoogle ScholarPubMed
Fitzpatrick, J. M., Johnston, D. A., Williams, G. W., Williams, D. J., Freeman, T. C., Dunne, D. W. and Hoffmann, K. F. (2005). An oligonucleotide microarray for transcriptome analysis of Schistosoma mansoni and its application/use to investigate gender-associated gene expression. Molecular and Biochemical Parasitology 141, 1–13.CrossRefGoogle ScholarPubMed
Fitzpatrick, J. M., Protasio, A. V., McArdle, A. J., Williams, G. A., Johnston, D. A. and Hoffmann, K. F. (2008). Use of genomic DNA as an indirect reference for identifying gender-associated transcripts in morphologically identical, but chromosomally distinct, Schistosoma mansoni cercariae. PLoS Negected Tropical Diseases 2, e323.CrossRefGoogle ScholarPubMed
Franco, G. R., Adams, M. D., Soares, M. B., Simpson, A. J., Venter, J. C. and Pena, S. D. (1995). Identification of new Schistosoma mansoni genes by the EST strategy using a directional cDNA library. Gene 23, 141–147.CrossRefGoogle Scholar
Franco, G. R., Rabelo, E. M., Azevedo, V., Pena, H. B., Ortega, J. M., Santos, T. M., Meira, W. S., Rodrigues, N. A., Dias, C. M., Harrop, R., Wilson, A., Saber, M., Abdel-Hamid, H., Faria, M. S., Margutti, M. E., Parra, J. C. and Pena, S. D. (1997). Evaluation of cDNA libraries from different developmental stages of Schistosoma mansoni for production of expressed sequence tags (ESTs). DNA Research. 30, 231–240.CrossRefGoogle Scholar
Franco, G. R., Valadão, A. F., Azevedo, V. and Rabelo, E. M. (2000). The Schistosoma gene discovery program: state of the art. International Journal of Parasitology 30, 453–463.CrossRefGoogle ScholarPubMed
Freitas, T. C., Jung, E. and Pearce, E. J. (2007). TGF-ß signaling controls embryo development in the parasitic flatworm Schistosoma mansoni. PLoS Pathogens 3, e52.CrossRefGoogle Scholar
Geldhof, P., Visser, A., Clark, D., Saunders, G., Britton, C., Gilleard, J., Berriman, M. and Knox, D. (2007). RNA interference in parasitic helminths: current situation, potential pitfalls and future prospects. Parasitology 134, 609–619.CrossRefGoogle ScholarPubMed
Gobert, G. N., Moertel, L., Brindley, P. J. and McManus, D. P. (2009). Developmental gene expression profiles of the human pathogen Schistosoma japonicum. BMC Genomics 10:128.CrossRefGoogle ScholarPubMed
Gomes, M. S., Cabral, F. J., Jannotti-Passos, L. K., Carvalho, O., Rodriques, V., Baba, E. H. and Sa, R. G. (2009). Preliminary analysis of miRNA pathway in Schistosoma mansoni. Parasitology International 58, 61–68.CrossRefGoogle ScholarPubMed
Gourbal, B. E. F., Guillou, F., Mitta, G., Sibille, P., Theron, A., Pointier, J. P. and Coustau, C. (2008). Excretory–secretory products of larval Fasciola hepatica investigated using a two-dimensional proteomic approach. Molecular and Biochemical Parasitology 161, 63–66.CrossRefGoogle ScholarPubMed
Grevelding, C. G. (2006). Transgenic flatworms. In Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology, and Physiology (ed. Maule, A. G. and Marks, N. J.), pp. 149–173. CABI, Oxfordshire, UK.CrossRefGoogle Scholar
Guillou, F., Roger, E., Mone, Y., Rognon, A., Grunau, C., Theron, A., Mitta, G., Coustau, C. and Gourbal, B. E. F. (2007). Excretory–secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Molecular and Biochemical Parasitology 155, 45–56.CrossRefGoogle ScholarPubMed
Gunasekera, A. M., Patankar, S., Schug, J., Eisen, G., Kissinger, J., Roos, D. and Wirth, D. F. (2004). Widespread distribution of antisense transcripts in the Plasmodium falciparum genome. Molecular and Biochemical Parasitology 136, 35–42.CrossRefGoogle ScholarPubMed
Haas, B. J., Berriman, M., Hirai, H., Cerqueira, G. G., LoVerde, P. T. and El-Sayed, N. M. (2007). Schistosoma mansoni genome: closing in on a final gene set. Experimental Parasitology 117, 225–228.CrossRefGoogle Scholar
Han, Z. G., Brindley, P. J., Wang, S. Y. and Chen, Z. (2009). Schistosome genomics: new perspectives on schistosome biology and host-parasite interactions. Annual Review of Genomics and Human Genetics 10, 10.1–10.30.CrossRefGoogle Scholar
Hastings, M. L., Ingle, H. A., Lazar, M. A. and Munroe, S. H. (2000). Post-transcriptional regulation of thyroid hormone receptor expression by cis-acting sequences and a naturally occurring antisense RNA. Journal of Biological Chemistry 275, 11507–11153.CrossRefGoogle Scholar
Heyers, O., Walduck, A. K., Brindley, P. J., Bleizß, W., Lucius, R., Dorbic, T., Wittig, B. and Kalinna, B. H. (2003). Schistosoma mansoni miracidia transformed by particle bombardment infect Biomphalaria glabrata snails and develop into transgenic sporocysts. Experimental Parasitology 105, 174–178.CrossRefGoogle ScholarPubMed
Hokke, C. H., Fitzpatrick, J. M. and Hoffmann, K. F. (2007). Integrating transcriptome, proteome and glycome analyses of Schistosoma biology. Trends in Parasitology 23, 165–174.CrossRefGoogle ScholarPubMed
Hu, W., Yan, Q., Shen, D. K., Liu, F., Zhu, Z. D., Song, H. D., Xu, X. R., Wang, Z. J., Rong, Y. P., Zeng, L. C., Wu, J., Zhang, X., Wang, J. J., Xu, X. N., Wang, S. Y., Fu, G., Zhang, X. L., Wang, Z. Q., Brindley, P. J., McManus, D., Zue, C. L., Feng, Z., Chen, Z. and Han, Z. G. (2003). Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nature Genetics 35, 139–147.CrossRefGoogle ScholarPubMed
Ivanchenko, M. G., Lerner, J. P., McCormick, R. S., Toumadje, A., Allen, B., Fischer, K., Hedstrom, O., Helmrich, A., Barnes, D. W. and Bayne, C. J. (1999). Continuous in vitro propagation and differentiation of cultures of the intramolluscan stages of the human parasite Schistosoma mansoni. Proceedings of the National Academy of Sciences, USA 96, 4965–4970.CrossRefGoogle ScholarPubMed
Jolly, E. R., Chin, C. S., Miller, S., Baghat, M. M., Lim, K. C., DeRisi, J. and McKerrow, J. H. (2007). Gene expression patterns during adaptation of a helminth parasite to different environmental niches. Genome Biology 8, R65.CrossRefGoogle ScholarPubMed
Kapp, K.Coustau, C., Wippersteg, V., Jourdane, J., Kunz, W. and Grevelding, C. G. (2003). Transplantation of in vitro-generated Schistosoma mansoni mother sporocysts into Biomphalaria glabrata. Parasitology Research 91, 482–485.Google ScholarPubMed
Kalinna, B. H. and Brindley, P. J. (2007). Manipulating the manipulators: advances in parasitic helminth transgenesis. Trends in Parasitology 23, 197–204.CrossRefGoogle ScholarPubMed
Kines, K. J., Mann, V. H., Morales, M. E., Shelby, B. D., Kalinna, B. H., Gobert, G. N., Chirgwin, S. R. and Brindley, P. J. (2006). Transduction of Schistosoma mansoni by vesicular stomatitis virus glycoprotein-pseudotyped Moloney murine leukemia retrovirus. Experimental Parasitology 112, 209–220.CrossRefGoogle ScholarPubMed
Knox, D. P., Geldhof, P., Visser, A. and Britton, C. (2007). RNA interference in parasitic nematodes of animals: a reality check? Trends in Parasitology 23, 105–107.CrossRefGoogle ScholarPubMed
Knudsen, G. M., Medzihradszky, K. F., Lim, K. C., Hansell, E. and McKerrow, J. H. (2005). Proteomic analysis of Schistosoma mansoni cercarial secretions. Molecular and Cellular Proteomics 4, 1862–1875.CrossRefGoogle ScholarPubMed
Krautz-Peterson, G., Bhardwaj, R., Faghiri, Z., Tararam, C. A. and Skelly, P. J. (2009). RNA interference in schistosomes: machinery and methodology. Parasitology 137. doi:10.1017/S0031182009991168Google ScholarPubMed
Krautz-Peterson, G., Radwanska, M., Ndegwa, D., Shoemaker, C. B. and Skelly, P. J. (2007). Optimizing gene suppression in schistosomes using RNA interference. Molecular and Biochemical Parasitology 153, 194–202.CrossRefGoogle ScholarPubMed
Krautz-Peterson, G. and Skelly, P. J. (2008). Schistosoma mansoni: the dicer gene and its expression. Experimental Parasitology 118, 122–128.CrossRefGoogle ScholarPubMed
Kulkarni, M. M., Booker, M., Silver, S. J., Friedman, A., Hong, P., Perrimon, N. and Mathey-Prevot, B. (2006). Evidence of off-target effects associated with long dsRNAs in Drosophila melanogaster cell-based assays. Nature Methods 3, 833–838.CrossRefGoogle ScholarPubMed
Laursen, J. R. and Yoshino, T. P. (1999). Biomphalaria glabrata embryonic (Bge) cell line supports in vitro miracidial transformation and early larval development of the deer liver fluke, Fascioloides magna. Journal of Parasitology 118, 187–194.CrossRefGoogle ScholarPubMed
Lehr, T., Beuerlein, K., Doenhoff, M. J., Grevelding, C. G. and Geyer, R. (2008). Localization of carbohydrate determinants common to Biomphalaria glabrata as well as to sporocysts and miracidia of Schistosoma mansoni. Parasitology 135, 931–942.CrossRefGoogle ScholarPubMed
Liang, P. and Pardee, A. B. (1992). Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257, 967–971.CrossRefGoogle ScholarPubMed
Liu, F., Lu, J., Hu, W., Wang, S. Y., Cui, S. J., Chi, M., Yan, Q., Wang, X. R., Song, H. D., Xu, X. N., Wang, J. J., Zhang, X. L., Zhang, X., Wang, Z. Q., Xue, C. L., Brindley, P. J., McManus, D. P., Yang, P. Y., Feng, Z., Chen, Z. and Han, Z. G. (2006). New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. PLoS Pathogens 2, e29.CrossRefGoogle ScholarPubMed
Loker, E. S., Cimino, D. F. and Hertel, L. A. (1992). Excretory-secretory products of Echinostoma paraensei sporocysts mediate interference with Biomphalaria glabrata hemocyte function. Journal of Parasitology 78, 104–115.CrossRefGoogle Scholar
LoVerde, P. T., Hirai, H., Merrick, J. M., Lee, N. H. and El-Sayed, N. (2004). Schistosoma mansoni genome project: an update. Parasitology International 53, 183–192.CrossRefGoogle ScholarPubMed
Luther, H. P., Haase, H., Hohaus, A., Beckmann, G., Reich, J. and Morano, I. (1998). Characterization of naturally occurring myosin heavy chain antisense mRNA in rat heart. Journal of Cellular Biochemistry 70, 110–120.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Mann, V. H., Morales, M. E., Kines, K. J. and Brindley, P. J. (2008). Transgenesis of schistosomes: approaches employing mobile genetic elements. Parasitology 135, 141–153.CrossRefGoogle ScholarPubMed
McManus, D. P. and Dalton, J. P. (2006). Vaccines against the zoonotic trematodes Schistosoma japonicum, Fasciola hepatica and Fasciola gigantica. Parasitology 133, S43–61.CrossRefGoogle ScholarPubMed
McManus, D. P., Hu, W., Brindley, P. J., Feng, Z. and Han, Z. G. (2004). Schistosome transcriptome analysis at the cutting edge. Trends in Parasitology 20, 301–304.CrossRefGoogle ScholarPubMed
Morales, M. E., Rinaldi, G., Gobert, G. N., Kines, K. J., Tort, J. F., and Brindley, P. J. (2008). RNA interference of Schistosoma mansoni cathepsin D, the apical enzyme of the hemoglobin proteolysis cascade. Molecular and Biochemical Parasitology 157, 160–168.CrossRefGoogle ScholarPubMed
Mourão, M. M., Dinguirard, N., Franco, G. R. and Yoshino, T. P. (2009). Phenotypic screen of early-developing larvae of the blood fluke, Schistosoma mansoni,using RNA interference. PLoS Neglected Tropical Diseases 3, e502. doi:10.1371/journal.pntd.0000502.CrossRefGoogle ScholarPubMed
Ndegwa, D., Krautz-Peterson, G. and Skelly, P. J. (2007). Protocols for gene silencing in schistosomes. Experimental Parasitology 117, 284–291.CrossRefGoogle ScholarPubMed
Nickel, W. (2005). Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 6, 607–614.CrossRefGoogle ScholarPubMed
Nordstrom, T., Gharizadeh, B., Pourmand, N., Nyren, P. and Ronaghi, M. (2001). Method enabling fast partial sequencing of cDNA clones. Analytical Biochemistry 15, 266–271.CrossRefGoogle Scholar
Nowak, T. S. and Loker, E. S. (2005). Echinostoma paraensei: differential gene transcription in the sporocyst stage. Expimental Parasitology 109, 94–105.CrossRefGoogle ScholarPubMed
Osman, A., Niles, E. G., Verjovski-Almeida, S. and LoVerde, P. T. (2006). Schistosoma mansoni TGF-ß receptor II: role in host ligand-induced regulation of a schistosome target gene. PLoS Pathogen 2, e54.CrossRefGoogle Scholar
Oliveira, G. C., Franco, G. and Verjovski-Almeida, S. (2008). The Brazilian contribution to the study of the Schistosoma mansoni transcriptome. Acta Tropica 108, 179–182.CrossRefGoogle Scholar
Oliveira, G. C., Rodrigues, N. B., Romanha, A. and Bahia, D. (2004). Genome and genomics of schistosomes. Canadian Journal of Zoology 82, 375–390.CrossRefGoogle Scholar
Patankar, S., Munasinghe, A., Shoaibi, A., Cummings, L. M. and Wirth, D. F. (2001). Serial analysis of gene expression in Plasmodium falciparum reveals the global expression profile of erythrocytic stages and the presence of anti-sense transcripts in the malarial parasite. Molecular Biology of the Cell 12, 3114–1325.CrossRefGoogle ScholarPubMed
Pearce, E. J. and Freitas, T. C. (2008). Reverse genetics and the study of the immune response to schistosomes. Parasite Immunology 30, 215–221.CrossRefGoogle Scholar
Peng, H. J., Chen, X. G., Wang, X. Z. and Lun, Z. R. (2003). Analysis of the gene expression profile of Schistosoma japonicum cercariae by a strategy based on expressed sequence tags. Parasitology Research. 90, 287–293.CrossRefGoogle ScholarPubMed
Pereira, T. C., Pascoal, V. D. B., Marchesini, R. B., Maia, I. G., Magalhaes, L. A., Zanotti-Magalhaes, E. M. and Lopes-Cendes, I. (2008). Schistosoma mansoni: Evaluation of an RNAi-based treatment targeting HGPRTase gene. Experimental Parasitology 118, 619–623.CrossRefGoogle ScholarPubMed
Petalidis, L., Bhattacharyya, S., Morris, G. A., Collins, V. P., Freeman, T. C. and Lyon, P. A. (2003). Global amplification of mRNA by template-switching PCR: linearity and application to microarray analysis. Nucleic Acids Research 25, 402–408.Google Scholar
Peterson, N. A., Hokke, C. H., Deelder, A. M. and Yoshino, T. P. (2009). Glycotope analysis in miracidia and primary sporocysts of Schistosoma mansoni: differential expression during the miracidium-to-sporocyst transformation. International Journal for Parasitology 39, 1331–1344.CrossRefGoogle ScholarPubMed
Ramaswamy, K., Salafsky, B., Potluri, S., He, Y. X., Li, J. W. and Shibuya, T. (1995). Secretion of an anti-inflammatory, immunomodulatory factor by Schistosomulae of Schistosoma mansoni. Journal of Inflammation 46, 13–22.Google ScholarPubMed
Radke, J. R., Behnke, M. S., Mackey, A. J., Radke, J. B., Roos, D. S. and White, M. W. (2005). The transcriptome of Toxoplasma gondii. BMC biology 2, 3–26.Google Scholar
Reynolds, A., Leake, D., Boese, Q., Scaringe, S., Marshall, W. S., and Khvorova, A. (2004). Rational siRNA design for RNA interference. Nature Biotechnology 22, 326–330.CrossRefGoogle ScholarPubMed
Rinaldi, G., Morales, M. E., Alrefaei, Y. N., Cancela, M., Castillo, E., Dalton, J. P., Tort, J. F. and Brindley, P. J. (2009). RNA interference targeting leucine aminopeptidase blocks hatching of Schisotosoma mansoni eggs. Molecular and Biochemical Parasitology 167, 118–126.CrossRefGoogle Scholar
Rinaldi, G., Morales, M. E., Cancela, M., Castillo, E., Brindley, P. J., Jose, F. and Tort, J. F. (2008). Development of functional genomic tools in trematodes: RNA interference and luciferase reporter gene activity in Fasciola hepatica. PLoS Neglected Tropical Diseases 2, e260.CrossRefGoogle ScholarPubMed
Robijn, M. L., Wujrer, M., Kornelis, D., Deelder, A. M., Geyer, R. and Hokke, C. H. (2005). Mapping fucosylated epitopes on glycoproteins and glycolipids of Schistosoma mansoni cercariae, adult worms and eggs. Parasitology 130, 67–77.CrossRefGoogle ScholarPubMed
Roger, E., Gourbal, B., Grunau, C., Pierce, R. J., Galinier, R. and Mitta, G. (2008 b). Expression analysis of highly polymorphic mucin proteins (Sm PoMuc) from the parasite Schistosoma mansoni. Molecular and Biochemical Parasitology 157, 217–227.CrossRefGoogle ScholarPubMed
Roger, E., Grunau, C., Pierce, R. J., Hirai, H., Gourbal, B., Galinier, R., Emans, R., Cesari, I. M., Cosseau, C. and Mitta, G. (2008 c). Controlled chaos of polymorphic mucins in a metazoan parasite (Schistosoma mansoni) interacting with its invertebrate host (Biomphalaria glabrata). PLoS Neglected Tropical Diseases 2(11), e330.CrossRefGoogle Scholar
Roger, E., Mitta, G., Mone, Y., Bouchut, A., Rognon, A., Grunau, C., Boissier, J., Theron, A. and Gourbal, B. E. F. (2008 a). Molecular determinants of compatibility polymorphism in the Biomphalaria glabrata/Schistosoma mansoni model: New candidates identified by a global comparative proteomics approach. Molecular and Biochemical Parasitology 157, 205–216.CrossRefGoogle ScholarPubMed
Saha, S., Sparks, A. B., Rago, C., Akmaev, V., Wang, C. J., Vogelstein, B., Kinzler, K. W. and Velculescu, V. E. (2002). Using the transcriptome to annotate the genome. Nature Biotechnology 20, 508–512.CrossRefGoogle ScholarPubMed
Santos, T. M., Johnston, D. A., Azevedo, V., Ridgers, I. L., Martinez, M. F., Marotta, G. B., Santos, R. L., Fonseca, S. J., Ortega, J. M., Rabelo, E. M., Saber, M., Ahmed, H. M., Romeih, M. H., Franco, G. R., Rollinson, D. and Pena, S. D. (1999). Analysis of the gene expression profile of Schistosoma mansoni cercariae using the expressed sequence tag approach, Molecular and Biochemistry Parasitology 20, 79–97.CrossRefGoogle Scholar
Sargent, T. D. and Dawid, I. B. (1983). Differential gene expression in the gastrula of Xenopus laevis. Science 222, 135–139.CrossRefGoogle ScholarPubMed
Sayed, A. H., Cook, S. K. and Williams, D. L. (2006). Redox balance mechanisms in Schistosoma mansoni rely on peroxiredoxins and albumin and implicate peroxiredoxins as novel drug targets. Journal of Biological Chemistry 281, 17001–17010.CrossRefGoogle ScholarPubMed
Simpson, A. J., Sher, A. and McCutchan, T. F. (1982). The genome of Schistosoma mansoni: isolation of DNA, its size, bases and repetitive sequences. Molecular and Biochemistry Parasitology 6, 125–137.CrossRefGoogle ScholarPubMed
Skelly, P. J. (2006). Gene silencing in flatworms using RNA interference. In Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology, and Physiology (ed. Maule, A. G. and Marks, N. J.), pp. 423–434. CABI, Oxfordshire, UK.CrossRefGoogle Scholar
Skelly, P. J., Da'dara, A. and Harn, D. A. (2003). Suppression of cathepsin B expression in Schistosoma mansoni by RNA interference. International Journal for Parasitology 33, 363–369.CrossRefGoogle ScholarPubMed
Skelly, P. J., Kim, J. W., Cunningham, J. and Shoemaker, C. B. (1994). Cloning, characterization, and functional expression of cDNAs encoding glucose transporter proteins from the human parasite Schistosoma mansoni. Journal of Biological Chemistry 269, 4247–4253.CrossRefGoogle ScholarPubMed
Taft, A. S., Vermeire, J. J., Bernier, J., Birkeland, S. R., Cipriano, M. J., Papa, A. R., McArthur, A. G. and Yoshino, T. P. (2009). Transcriptome analysis of Schistosoma mansoni larval development using serial analysis of gene expression (SAGE). Parasitology 136, 469–485.CrossRefGoogle ScholarPubMed
Tang, F., Barbacioru, C., Wang, Y., Nordman, E., Lee, C., Xu, N., Wang, X., Bodeau, J., Tuch, B. B., Siddiqui, A., Lao, K. and Surani, M. A. (2009). mRNA-seq whole-transcriptome analysis of a single cell. Nature Methods 6, 377–382.CrossRefGoogle ScholarPubMed
Theodoropoulos, G., Hicks, S. J., Corfield, A. P., Miller, B. G., Carrington, S. D. (2001). The role of mucins in host-parasite interactions. Part II. Helminth parasites. Trends in Parasitology 17, 130–135.CrossRefGoogle ScholarPubMed
The Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium; Genome annotation and evolution analysis: 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, D. J., Blair, D., Zhong, Y., Chen, Z.; Functional genomics analysis: Liu, F., Hu, W., Wang, Z. Q., Zhang, Q. H., Song, H. D., Chen, S., Xu, X., Xu, B., Ju, C., Huang, Y., Brindley, P. J., McManus, D. P., Feng, Z., Han, Z. G.; Sequencing and assembly: Lu, G., Ren, S., Wang, Y., Gu, W., Kang, H., Chen, J., Chen, X., Chen, S., Wang, L., Yan, J., Wang, B., Li, X., Jin, L., Wang, B., Pu, S., Zhang, X., Zhang, W., Hu, Q., Zhu, G., Wang, J., Yu, J., Wang, J., Yang, H., Ning, Z., Berriman, M., Wei, C. L., Ruan, Y., Zhao, G., Wang, S.; Paper writing: Liu, F., Zhou, Y., Wang, Z. Q., Lu, G., Zheng, H., Brindley, P. J., McManus, D. P., Blair, D., Zhang, Q. H., Zhong, Y., Wang, S., Han, Z. G, Chen, Z.; Project leaders: Wang, S., Han, Z. G. and Chen, Z. (2009). The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460, 345–351.Google Scholar
Valentim, C. L., LoVerde, P. T., Anderson, T. J. and Criscione, C. D. (2009). Efficient genotyping of Schistosoma mansoni miracidia following whole genome amplification. Molecular and Biochemistry Parasitology 166, 81–84.CrossRefGoogle ScholarPubMed
Velculescu, V. E., Zhang, L., Vogelstein, B. and Kinzler, K. W. (1995). Serial analysis of gene expression. Science 270, 484–487.CrossRefGoogle ScholarPubMed
Vera, J. C., Wheat, C W., Fescemyer, H. W., Frilander, M. J., Crawford, D. L., Hanski, I., and Marden, J. H. (2008). Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Molecular Ecology 17, 1636–1647.CrossRefGoogle Scholar
Verjovski-Almeida, S., DeMarco, R., Martins, E. A., Guimarães, P. E., Ojopi, E. P., Paquola, A. C., Piazza, J. P., Nishiyama, M. Y. Jr., Kitajima, J. P., Adamson, R. E., Ashton, P. D., Bonaldo, M. F., Coulson, P. S., Dillon, G. P., Farias, L. P., Gregorio, S. P., Ho, P. L., Leite, R. A., Malaquias, L. C., Marques, R. C., Miyasato, P. A., Nascimento, A. L., Ohlweiler, F. P., Reis, E. M., Ribeiro, M. A., Sá, R. G., Stukart, G. C., Soares, M. B., Gargioni, C., Kawano, T., Rodrigues, V., Madeira, A. M., Wilson, R. A., Menck, C. F., Setubal, J. C., Leite, L. C. and Dias-Neto, E. (2003). Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nature Genetics 35, 148–157.CrossRefGoogle ScholarPubMed
Vermeire, J. J., Taft, A. S., Hoffmann, K. F., Fitzpatrick, J. M. and Yoshino, T. P. (2006). Schistosoma mansoni: DNA microarray gene expression profiling during the miracidium-to-mother sporocyst transformation. Molecular and Biochemical Parasitology 147, 39–47.CrossRefGoogle ScholarPubMed
Vermeire, J. J. and Yoshino, T. P. (2007). Antioxidant gene expression and function in in vitro-developing Schistosoma mansoni mother sporocysts: possible role in self-protection. Parasitology 134, 1369–1378.CrossRefGoogle ScholarPubMed
Viney, M. E. and Thompson, F. J. (2008). Two hypotheses to explain why RNA interference does not work in animal parasitic nematodes. International Journal for Parasitology 38, 43–47.CrossRefGoogle Scholar
Williams, D. L., Sayed, A. A., Bernier, J., Birkeland, S. R., Cipriano, M. J., Papa, A. R., McArthur, A. G., Taft, A., Vermeire, J. J. and Yoshino, T. P. (2007). Profiling Schistosoma mansoni development using Serial Analysis of Gene Expression (SAGE). Experimental Parasitology 117, 246–258.CrossRefGoogle ScholarPubMed
Wilson, R. A., Ashton, P. D., Braschi, S., Dillion, G. P., Berriman, M. and Ivens, A. (2006). ‘Oming in on schistosomes: prospects and limitations for post-genomics. Trends in Parasitology 23, 14–20.CrossRefGoogle Scholar
Wippersteg, V., Kapp, K., Kunz, W. and Grevelding, C. G. (2002 b). Characterization of the cysteine protease ER60 in transgenic Schistosoma mansoni larvae. International Journal for Parasitology 32, 1219–1224.CrossRefGoogle ScholarPubMed
Wippersteg, V., Kapp, K., Kunz, W., Jackstadt, W. P., Zahner, H. and Grevelding, C. G. (2002 a). HSP70-controlled GFP expression in transiently transformed schistosomes. Molecular and Biochemical Parasitology 120, 141–150.CrossRefGoogle ScholarPubMed
Wippersteg, V., Ribeiro, F., Liedtke, S., Kunz, W. and Grevelding, C. G. (2003). The uptake of Texas red bovine serum albumin in the excretory system of schistosomes, and its colocalization with ER60 promoter-induced GFP in transiently transformed adult males. International Journal for Parasitology 33, 1139–1143.CrossRefGoogle Scholar
Wu, X. J., Sabat, G., Brown, J. F., Zhang, M., Taft, A., Peterson, N. P., Harms, A. and Yoshino, T. P. (2009). Proteomic analysis of Schistosoma mansoni proteins released during in vitro miracidium-to-sporocyst transformation. Molecular and Biochemical Parasitology 164, 32–44.CrossRefGoogle ScholarPubMed
Xu, Y. Z. and Dresden, M. H. (1986). Leucine aminopeptidase and hatching of Schistosoma mansoni eggs. Journal of Parasitology 72, 507–511.CrossRefGoogle ScholarPubMed
Xue, X., Sun, J., Zhang, Q., Wang, Z., Huang, Y. and Pan, W. (2008). Identification and characterization of novel microRNAs from Schistosoma japonicum. PLoS One 3, e4034.CrossRefGoogle ScholarPubMed
Yang, L. L., Lu, Z. Y., Hu, S. M., He, S. J., Li, Z. Y., Zhang, S. M., Zheng, H. Q., Li, M. T., Yu, X. B., Fung, M. C. and Wu, Z. D. (2009). Schistosoma japonicum: proteomics analysis of differentially expressed proteins from ultraviolet-attenuated cercariae compared to normal cercariae. Parasitology Research 105, 237–248.CrossRefGoogle ScholarPubMed
Yoshino, T. P. and Boswell, C. A. (1986). Antigen sharing between larval trematodes and their snail hosts: how real a phenomenon in immune evasion? In Immune Mechanisms in Invertebrate Vectors (ed., Lackie, A. M.), pp. 221–238. Clarendon Press, Oxford.Google Scholar
Yoshino, T. P. and Laursen, J. R. (1995). Production of Schistosoma mansoni daughter sporocysts from mother sporocysts maintained in synxenic culture with Biomphalaria glabrata embryonic (Bge) cells. Journal of Parasitology 81, 714–722.CrossRefGoogle ScholarPubMed
Zhao, Z.-R., Lei, L., Liu, M., Zhu, S.-C., Ren, C.-P., Wang, X.-N., and Shen, J.-J. (2008). Schistosoma japonicum: inhibition of mago nashi gene expression by shRNA-mediated RNA interference. Experimental Parasitology 119, 379–384.CrossRefGoogle ScholarPubMed
Zelck, U. E. and Von Janowsky, B. (2004). Antioxidant enzymes in intramolluscan Schistosoma mansoni and ROS-induced changes in expression. Parasitology 128, 493–501.CrossRefGoogle ScholarPubMed