Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-28T03:26:07.933Z Has data issue: false hasContentIssue false
  • English
  • Français

Transcriptome analysis of Schistosoma mansoni larval development using serial analysis of gene expression (SAGE)

Published online by Cambridge University Press:  05 March 2009

A. S. TAFT ,
J. J. VERMEIRE ,
J. BERNIER ,
S. R. BIRKELAND ,
M. J. CIPRIANO ,
A. R. PAPA ,
A. G. McARTHUR  and
T. P. YOSHINO
A. S. TAFT
Affiliation:
Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2115 Observatory Drive, Madison, WI, USA
J. J. VERMEIRE
Affiliation:
Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2115 Observatory Drive, Madison, WI, USA Current address: Department of Pediatrics, Yale University School of Medicine, New Haven, CT, USA.
J. BERNIER
Affiliation:
Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, MA, USA
S. R. BIRKELAND
Affiliation:
Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, MA, USA
M. J. CIPRIANO
Affiliation:
Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, MA, USA
A. R. PAPA
Affiliation:
Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, MA, USA
A. G. McARTHUR
Affiliation:
Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, MA, USA
T. P. YOSHINO*
Affiliation:
Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2115 Observatory Drive, Madison, WI, USA
*
*Corresponding author: Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2115 Observatory Drive, Madison, WI, 53726, USA. Tel: +608 263 6002. Fax: +608 265 8122. E_mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Infection of the snail, Biomphalaria glabrata, by the free-swimming miracidial stage of the human blood fluke, Schistosoma mansoni, and its subsequent development to the parasitic sporocyst stage is critical to establishment of viable infections and continued human transmission. We performed a genome-wide expression analysis of the S. mansoni miracidia and developing sporocyst using Long Serial Analysis of Gene Expression (LongSAGE). Five cDNA libraries were constructed from miracidia and in vitro cultured 6- and 20-day-old sporocysts maintained in sporocyst medium (SM) or in SM conditioned by previous cultivation with cells of the B. glabrata embryonic (Bge) cell line. We generated 21 440 SAGE tags and mapped 13 381 to the S. mansoni gene predictions (v4.0e) either by estimating theoretical 3′ UTR lengths or using existing 3′ EST sequence data. Overall, 432 transcripts were found to be differentially expressed amongst all 5 libraries. In total, 172 tags were differentially expressed between miracidia and 6-day conditioned sporocysts and 152 were differentially expressed between miracidia and 6-day unconditioned sporocysts. In addition, 53 and 45 tags, respectively, were differentially expressed in 6-day and 20-day cultured sporocysts, due to the effects of exposure to Bge cell-conditioned medium.

Keywords

Schistosoma mansoniBiomphalaria glabrataSAGEmiracidiasporocystdevelopment
Type
Research Article
Information
Parasitology , Volume 136 , Issue 5 , April 2009 , pp. 469 - 485
Copyright
Copyright © 2009 Cambridge University Press

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

Basch, P. F. (1991) Schistosomes-Development, Reproduction and Host Relations. Oxford University Press, New York and Oxford.Google Scholar
Basch, P. F. and DiConza, J. J. (1974). The miracidium-sporocyst transition in Schistosoma mansoni, surface changes in vitro with ultrastructural correlation. Journal of Parasitology 60, 935–941.CrossRefGoogle ScholarPubMed
Bender, R. C., Broderick, E. J., Goodall, C. P. and Bayne, C. J. (2005). Respiratory burst of Biomphalaria glabrata hemocytes, Schistosoma mansoni-resistant snails produce more extracellular H2O2 than susceptible snails. Journal of Parasitology 91, 275–279.CrossRefGoogle ScholarPubMed
Bers, D. M. and Guo, T. (2005). Calcium signaling in cardiac ventricular myocytes. Annals of the New York Academy of Sciences 1047, 86–98.CrossRefGoogle ScholarPubMed
Bhattacharya, A., Padhan, N., Jain, R. and Bhattacharya, S. (2006). Calcium-binding proteins of Entamoeba histolytica. Archives of Medical Research 37, 221–225.CrossRefGoogle ScholarPubMed
Binder, R. J., Vatner, R. and Srivastava, P. (2004). The heat-shock protein receptors, some answers and more questions. Tissue Antigens 64, 442–451.CrossRefGoogle ScholarPubMed
Bonnet, C., Petter, E., Dumont, X., Picard, A., Caput, D. and Lenaers, G. (2000). Identification and transcription control of fission yeast genes repressed by and ammonium starvation growth arrest. Yeast 16, 23–33.3.0.CO;2-A>CrossRefGoogle ScholarPubMed
Brown, M. A., Zhu, L., Schmidt, C. and Tucker, P. W. (2007). Hsp90-from signal transduction to cell transformation. Biochemical and Biophysical Research Communications 363, 241–246.CrossRefGoogle ScholarPubMed
Cai, Y., Langley, J. G., Smith, D. I. and Boros, D. L. (1996). A cloned major Schistosoma mansoni egg antigen with homologies to small heat shock proteins elicits Th1 responsiveness. Infection and Immunity 64, 1750–1755.CrossRefGoogle ScholarPubMed
Cass, C. L., Johnson, J. R., Califf, L. L., Xu, T., Hernandez, H. J., Stadecker, M. J., Yates, J. R. 3RD. and Williams, D. L. (2007). Proteomic analysis of Schistosoma mansoni egg secretions. Molecular and Biochemical Parasitology 155, 84–93.CrossRefGoogle ScholarPubMed
Conesa, A., Gotz, S., Garcia-Gomez, J. M., Terol, J., Talon, M. and Robles, M. (2005). Blast2GO, a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676.CrossRefGoogle ScholarPubMed
Coppin, J. F., Lefebvre, C., Caby, S., Cocquerelle, C., Vicogne, J., Coustau, C. and Dissous, C. (2003). Gene expression changes in Schistosoma mansoni sporocysts induced by Biomphalaria glabrata embryonic cells. Parasitology Research 89, 113–119.CrossRefGoogle ScholarPubMed
Craig, H., Wastling, J. M. and Knox, D. P. (2006). A preliminary proteomic survey of the in vitro excretory-secretory products of fourth-stage larval and adult Teladorsagia circumcincta. Parasitology 132, 535–543.CrossRefGoogle ScholarPubMed
de Waard, V., van den Berg, B. M., Veken, J., Schultz-Heienbrok, R., Pannekoek, H. and van Zonneveld, A. J. (1999). Serial analysis of gene expression to assess the endothelial cell response to an atherogenic stimulus. Gene 226, 1–8.CrossRefGoogle Scholar
Dresden, M. H. and Edlin, E. M. (1975). Schistosoma mansoni, calcium content of cercariae and its effects on protease activity in vitro. Journal of Parasitology 61, 398–402.CrossRefGoogle Scholar
Dumas, C., Chow, C., Muller, M. and Papadopoulou, B. (2006). A novel class of developmentally regulated noncoding RNAs in Leishmania. Eukaryotic Cell 5, 2033–2046.CrossRefGoogle ScholarPubMed
El Ridi, R., Velupillai, P. and Harn, D. A. (1996). Regulation of schistosome egg granuloma formation, host-soluble L-selectin enters tissue-trapped eggs and binds to carbohydrate antigens on surface membranes of miracidia. Infection and Immunity 64, 4700–4705.CrossRefGoogle ScholarPubMed
Emmersen, J. (2008 a). Duplicate ditag analysis in LongSAGE. Methods in Molecular Biology 387, 143–150.CrossRefGoogle ScholarPubMed
Emmersen, J. (2008 b). Extraction and annotation of SAGE tags using sequence quality values. Methods in Molecular Biology 387, 123–132.CrossRefGoogle ScholarPubMed
Erttmann, K. D., Buttner, D. W. and Gallin, M. Y. (1995). A putative protein related to human chemokines encoded antisense to the cDNA of an Onchocerca volvulus antigen. Tropical Medicine and Parasitology 46, 123–130.Google Scholar
Ewing, B. and Green, P. (1998). Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Research 8, 186–194.CrossRefGoogle ScholarPubMed
Ewing, B., Hillier, L., Wendl, M. C. and Green, P. (1998). Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Research 8, 175–185.CrossRefGoogle ScholarPubMed
Farrell, C. M. and Lukens, L. N. (1995). Naturally occurring antisense transcripts are present in chick embryo chondrocytes simultaneously with the down-regulation of the alpha 1 (I) collagen gene. Journal of Biological Chemistry 270, 3400–3408.CrossRefGoogle ScholarPubMed
Fisher, R. A. (1922). On the interpretation of χ2 from contingency tables, and the calculation of P. Journal of the Royal Statistical Society 85, 87–94.CrossRefGoogle Scholar
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
Fusco, A. C., Salafsky, B., Vanderkooi, G. and Shibuya, T. (1991). Schistosoma mansoni, the role of calcium in the stimulation of cercarial proteinase release. Journal of Parasitology 77, 649–657.CrossRefGoogle ScholarPubMed
Gelebart, P., Opas, M. and Michalak, M. (2005). Calreticulin, a Ca2+-binding chaperone of the endoplasmic reticulum. International Journal of Biochemistry and Cell Biology 37, 260–266.CrossRefGoogle ScholarPubMed
Gnanasekar, M. and Ramaswamy, K. (2007). Translationally controlled tumor protein of Brugia malayi functions as an antioxidant protein. Parasitology Research 101, 1533–1540.CrossRefGoogle ScholarPubMed
Granath, W. O. and Yoshino, T. P. (1984). Schistosoma mansoni: passive transfer of resistance by serum in the vector snail, Biomphalaria glabrata. Experimental Parasitology 58, 188–193.CrossRefGoogle ScholarPubMed
Guillou, F., Roger, E., Mone, Y., Rognon, A., Grunau, C., Theron, A., Mitta, G., Coustau, C. and Gourbal, B. E. (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
Hahn, U. K., Bender, R. C. and Bayne, C. J. (2001 a). Involvement of nitric oxide in killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata. Journal of Parasitology 87, 778–785.CrossRefGoogle ScholarPubMed
Hahn, U. K., Bender, R. C. and Bayne, C. J. (2001 b). Killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata, role of reactive oxygen species. Journal of Parasitology 87, 292–299.CrossRefGoogle ScholarPubMed
Hansen, E. L. (1976). A cell line from embryos of Biomphalaria glabrata (Pulmonata): establishment and characteristics. In Invertebrate Tissue Culture, Research Applications (ed. Kurstak, E. and Maramorosch, K.), pp. 75–99. Academic Press, New York, USA.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, 11507–11513.CrossRefGoogle Scholar
Hoffmann, K. F., Johnston, D. A. and Dunne, D. W. (2002). Identification of Schistosoma mansoni gender-associated gene transcripts by cDNA microarray profiling. Genome Biology 3, 1–12.CrossRefGoogle ScholarPubMed
Ikeda, T. (2004). Effects of blockers of Ca2+ channels and other ion channels on in vitro excystment of Paragonimus ohirai metacercariae induced by sodium cholate. Parasitology Research 94, 329–331.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 Science, USA 96, 4965–4970.CrossRefGoogle ScholarPubMed
Jolly, E. R., Chin, C. S., Miller, S., Bahgat, 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
Katsumata, T., Kohno, S., Yamaguchi, K., Hara, K. and Aoki, Y. (1989). Hatching of Schistosoma mansoni eggs is a Ca2+/calmodulin-dependent process. Parasitology Research 76, 90–91.CrossRefGoogle ScholarPubMed
Katsumata, T., Shimada, M., Sato, K. and Aoki, Y. (1988). Possible involvement of calcium ions in the hatching of Schistosoma mansoni eggs in water. Journal of Parasitology 74, 1040–1041.CrossRefGoogle ScholarPubMed
Kawamoto, F., Shozawa, A., Kumada, N. and Kojima, K. (1989). Possible roles of cAMP and Ca2+ in the regulation of miracidial transformation in Schistosoma mansoni. Parasitology Research 75, 368–374.CrossRefGoogle ScholarPubMed
Knabe, E., Gilbertson, D. E. and Plorin, G. G. (1982). The effect of concentrations of external sodium and calcium on the swimming speed of Schistosoma mansoni miracidia. Journal of Parasitology 68, 507–508.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
Kronstad, J. W. (2006). Serial analysis of gene expression in eukaryotic pathogens. Infectious Disorders – Drug Targets 6, 281–297.CrossRefGoogle ScholarPubMed
Lee, S., Bao, J., Zhou, G., Shapiro, J., Xu, J., Shi, R. Z., Lu, X., Clark, T., Johnson, D., Kim, Y. C., Wing, C., Tseng, C., Sun, M., Lin, W., Wang, J., Yang, H., Wang, J., Du, W., Wu, C. I., Zhang, X. and Wang, S. M. (2005). Detecting novel low-abundance transcripts in Drosophila. RNA 11, 939–946.CrossRefGoogle Scholar
Lewert, R. M., Hopkins, D. R. and Mandlowitz, S. (1966). The role of calcium and magnesium ions in invasiveness of schistosome cercariae. American Journal of Tropical Medicine and Hygiene 15, 314–323.CrossRefGoogle ScholarPubMed
Liniger, M., Bodenmüller, K., Pays, E., Gallati, S. and Roditi, I. (2001). Overlapping sense and antisense transcription units in Trypanosoma brucei. Molecular Microbiology 40, 869–878.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
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 Cell Biochemistry 70, 110–120.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Mei, H., Thakur, A., Schwartz, J. and Lo Verde, P. T. (1996). Expression and characterization of glutathione peroxidase activity in the human blood fluke Schistosoma mansoni. Infection and Immunity 64, 4299–4306.CrossRefGoogle ScholarPubMed
Messerli, S. M., Morgan, W., Birkeland, S. R., Bernier, J., Cipriano, M. J., McArthur, A. G. and Greenberg, R. M. (2006). Nitric oxide-dependent changes in Schistosoma mansoni gene expression. Molecular and Biochemical Parasitology 2, 367–370.CrossRefGoogle Scholar
Moser, D., Doenhoff, M. J. and Klinkert, M. Q. (1992). A stage-specific calcium-binding protein expressed in eggs of Schistosoma mansoni. Molecular and Biochemical Parasitology 51, 229–238.CrossRefGoogle ScholarPubMed
Neill, P. J., Smith, J. H., Doughty, B. L. and Kemp, M. (1988). The ultrastructure of the Schistosoma mansoni egg. American Journal of Tropical Medicine and Hygiene 39, 52–65.CrossRefGoogle ScholarPubMed
Nene, V., Dunne, D. W., Johnson, K. S., Taylor, D. W. and Cordingley, J. S. (1986). Sequence and expression of a major egg antigen from Schistosoma mansoni. Homologies to heat shock proteins and alpha-crystallins. Molecular and Biochemical Parasitology 21, 179–188.CrossRefGoogle Scholar
Noel, F., Cunha, V. M., Silva, C. L. and Mendonca-Silva, D. L. (2001). Control of calcium homeostasis in Schistosoma mansoni. Memórias do Instituto Oswaldo Cruz 96, 85–88.CrossRefGoogle ScholarPubMed
Ojopi, E. P., Oliveira, P. S., Nunes, D. N., Paquola, A., DeMarco, R., Gregório, S. P., Aires, K. A., Menck, C. F., Leite, L. C., Verjovski-Almeida, S. and Dias-Neto, E. (2007). A quantitative view of the transcriptome of Schistosoma mansoni adult-worms using SAGE. BMC Genomics 8, 186–191.CrossRefGoogle ScholarPubMed
Palm, D., Weiland, M., McArthur, A. G., Winiecka-Krusnell, J., Cipriano, M. J., Birkeland, S. R., Pacocha, S. E., Davids, B., Gillin, F., Linder, E. and Svard, S. (2005). Developmental changes in the adhesive disk during Giardia differentiation. Molecular and Biochemical Parasitology 141, 199–207.CrossRefGoogle ScholarPubMed
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, 3114–3125.CrossRefGoogle 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 Genomics 3, 26–34.Google 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
Skuce, P. J., Yaga, R., Lainson, F. A. and Knox, D. P. (2005). An evaluation of serial analysis of gene expression (SAGE) in the parasitic nematode, Haemonchus contortus. Parasitology 130, 553–559.CrossRefGoogle ScholarPubMed
Song, K. J., Song, K. H., Na, B. K., Kim, J. H., Kwon, D., Park, S., Pak, J. H., Im, K. I. and Shin, H. J. (2007). Molecular cloning and characterization of a cytosolic heat shock protein 70 from Naegleria fowleri. Parasitology Research 100, 1083–1089.CrossRefGoogle ScholarPubMed
Sponholtz, G. M. and Short, R. B. (1976). Schistosoma mansoni miracidia, stimulation by calcium and magnesium. Journal of Parasitology 62, 155–157.CrossRefGoogle ScholarPubMed
St-Croix, B., Rago, C., Velculescu, V., Traverso, G., Romans, K. E., Montgomery, E., Lal, A., Riggins, G. J., Lengauer, C., Vogelstein, B. and Kinzler, K. W. (2000). Genes expressed in human tumor endothelium. Science 289, 1197–1202.CrossRefGoogle ScholarPubMed
Stekel, D. J., Git, Y. and Falciani, F. (2000). The comparison of gene expression from multiple cDNA libraries. Genome Research 10, 2055–2061.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
Verjovski-Almeida, S., Venancio, T. M., Oliveira, K. C., Almeida, G. T. and Demarco, R. (2007). Use of a 44 k oligoarray to explore the transcriptome of Schistosoma mansoni adult worms. Experimental Parasitology 117, 236–245.CrossRefGoogle Scholar
Vermeire, J. J., Boyle, J. P. and Yoshino, T. P. (2004). Differential gene expression and the effects of Biomphalaria glabrata embryonic (Bge) cell factors during larval Schistosoma mansoni development. Molecular and Biochemical Parasitology 135, 153–157.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
Voge, M. and Seidel, J. S. (1972). Transformation in vitro of miracidia of Schistosoma mansoni and S. japonicum into young sporocysts. Journal of Parasitology 58, 699–704.CrossRefGoogle ScholarPubMed
Wahl, S. M., Frazier-Jessen, M., Jin, W. W., Kopp, J. B., Sher, A. and Cheever, A. W. (1997). Cytokine regulation of schistosome-induced granuloma and fibrosis. Kidney International 51, 1370–1375.CrossRefGoogle ScholarPubMed
Waisberg, M., Lobo, F. P., Cerqueira, G. C., Passo, L. K., Carvalho, O. S., Franco, G. R. and El-Sayed, N. M. (2007). Microarray analysis of gene expression induced by sexual contact in Schistosoma mansoni. BMC Genomics 8, 181–195.CrossRefGoogle ScholarPubMed
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 146, 246–257.CrossRefGoogle Scholar
Winder, S. J., Allen, B. G., Clément-Chomienne, O. and Walsh, M. P. (1998). Regulation of smooth muscle actin-myosin interaction and force by calponin. Acta Physiologica Scandinavia 164, 415–426.CrossRefGoogle ScholarPubMed
Wu, X. J., Sabat, G., Brown, J. F., Zhang, M., Taft, A. S., Peterson, N. A., Harms, A. and Yoshino, T. P. (2008). Proteomic analysis of Schistosoma mansoni proteins released during in vitro miracidium-to-sporocyst transformation. Molecular and Biochemical Parasitology doi:10.1016/j.molbiopara.2008.11.005 (Epub ahead of print).Google ScholarPubMed
Yoshihara, M. and Montana, E. S. (2004). The synaptotagmins: calcium sensors for vesicular trafficking. Neuroscientist 10, 566–574.CrossRefGoogle ScholarPubMed
Yoshino, T. P. (1981). Concanavalin A-induced receptor redistribution on Biomphalaria glabrata hemocytes, characterization of capping and patching responses. Journal of Invertebrate Pathology 38, 102–112.CrossRefGoogle ScholarPubMed
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
Young, J. C., Agash, V. R., Siegers, K. and Hartl, F. U. (2004). Pathways of chaperone mediated protein folding in the cytosol. Nature Reviews Molecular Cell Biology 5, 781–791.CrossRefGoogle ScholarPubMed
Zhang, G., Schmidt, O. and Asgari, S. (2006). A calreticulin-like protein from endoparasitoid venom fluid is involved in host hemocyte inactivation. Developmental and Comparative Immunology 30, 756–764.CrossRefGoogle ScholarPubMed