Skip to main content
    • Aa
    • Aa

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

  • A. S. TAFT (a1), J. J. VERMEIRE (a1) (a2), J. BERNIER (a3), S. R. BIRKELAND (a3), M. J. CIPRIANO (a3), A. R. PAPA (a3), A. G. McARTHUR (a3) and T. P. YOSHINO (a1)...

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.

Corresponding author
*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:
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

P. F. Basch and J. J. DiConza (1974). The miracidium-sporocyst transition in Schistosoma mansoni, surface changes in vitro with ultrastructural correlation. Journal of Parasitology 60, 935941.

R. C. Bender , E. J. Broderick , C. P. Goodall and C. J. Bayne (2005). Respiratory burst of Biomphalaria glabrata hemocytes, Schistosoma mansoni-resistant snails produce more extracellular H2O2 than susceptible snails. Journal of Parasitology 91, 275279.

D. M. Bers and T. Guo (2005). Calcium signaling in cardiac ventricular myocytes. Annals of the New York Academy of Sciences 1047, 8698.

A. Bhattacharya , N. Padhan , R. Jain and S. Bhattacharya (2006). Calcium-binding proteins of Entamoeba histolytica. Archives of Medical Research 37, 221225.

R. J. Binder , R. Vatner and P. Srivastava (2004). The heat-shock protein receptors, some answers and more questions. Tissue Antigens 64, 442451.

C. Bonnet , E. Petter , X. Dumont , A. Picard , D. Caput and G. Lenaers (2000). Identification and transcription control of fission yeast genes repressed by and ammonium starvation growth arrest. Yeast 16, 2333.

M. A. Brown , L. Zhu , C. Schmidt and P. W. Tucker (2007). Hsp90-from signal transduction to cell transformation. Biochemical and Biophysical Research Communications 363, 241246.

C. L. Cass , J. R. Johnson , L. L. Califf , T. Xu , H. J. Hernandez , M. J. Stadecker , J. R. Yates 3RD. and D. L. Williams (2007). Proteomic analysis of Schistosoma mansoni egg secretions. Molecular and Biochemical Parasitology 155, 8493.

A. Conesa , S. Gotz , J. M. Garcia-Gomez , J. Terol , M. Talon and M. Robles (2005). Blast2GO, a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 36743676.

J. F. Coppin , C. Lefebvre , S. Caby , C. Cocquerelle , J. Vicogne , C. Coustau and C. Dissous (2003). Gene expression changes in Schistosoma mansoni sporocysts induced by Biomphalaria glabrata embryonic cells. Parasitology Research 89, 113119.

V. de Waard , B. M. van den Berg , J. Veken , R. Schultz-Heienbrok , H. Pannekoek and A. J. van Zonneveld (1999). Serial analysis of gene expression to assess the endothelial cell response to an atherogenic stimulus. Gene 226, 18.

M. H. Dresden and E. M. Edlin (1975). Schistosoma mansoni, calcium content of cercariae and its effects on protease activity in vitro. Journal of Parasitology 61, 398402.

C. Dumas , C. Chow , M. Muller and B. Papadopoulou (2006). A novel class of developmentally regulated noncoding RNAs in Leishmania. Eukaryotic Cell 5, 20332046.

J. Emmersen (2008 a). Duplicate ditag analysis in LongSAGE. Methods in Molecular Biology 387, 143150.

J. Emmersen (2008 b). Extraction and annotation of SAGE tags using sequence quality values. Methods in Molecular Biology 387, 123132.

B. Ewing , L. Hillier , M. C. Wendl and P. Green (1998). Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Research 8, 175185.

R. A. Fisher (1922). On the interpretation of χ2 from contingency tables, and the calculation of P. Journal of the Royal Statistical Society 85, 8794.

J. M. Fitzpatrick , D. A. Johnston , G. W. Williams , D. J. Williams , T. C. Freeman , D. W. Dunne and K. F. Hoffmann (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, 113.

A. C. Fusco , B. Salafsky , G. Vanderkooi and T. Shibuya (1991). Schistosoma mansoni, the role of calcium in the stimulation of cercarial proteinase release. Journal of Parasitology 77, 649657.

P. Gelebart , M. Opas and M. Michalak (2005). Calreticulin, a Ca2+-binding chaperone of the endoplasmic reticulum. International Journal of Biochemistry and Cell Biology 37, 260266.

M. Gnanasekar and K. Ramaswamy (2007). Translationally controlled tumor protein of Brugia malayi functions as an antioxidant protein. Parasitology Research 101, 15331540.

W. O. Granath and T. P. Yoshino (1984). Schistosoma mansoni: passive transfer of resistance by serum in the vector snail, Biomphalaria glabrata. Experimental Parasitology 58, 188193.

F. Guillou , E. Roger , Y. Mone , A. Rognon , C. Grunau , A. Theron , G. Mitta , C. Coustau and B. E. Gourbal (2007). Excretory-secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Molecular and Biochemical Parasitology 155, 4556.

A. M. Gunasekera , S. Patankar , J. Schug , G. Eisen , J. Kissinger , D. Roos and D. F. Wirth (2004). Widespread distribution of antisense transcripts in the Plasmodium falciparum genome. Molecular and Biochemical Parasitology 136, 3542.

U. K. Hahn , R. C. Bender and C. J. Bayne (2001 a). Involvement of nitric oxide in killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata. Journal of Parasitology 87, 778785.

E. L. Hansen (1976). A cell line from embryos of Biomphalaria glabrata (Pulmonata): establishment and characteristics. In Invertebrate Tissue Culture, Research Applications (ed. E. Kurstak and K. Maramorosch ), pp. 7599. Academic Press, New York, USA.

M. L. Hastings , H. A. Ingle , M. A. Lazar and S. H. Munroe (2000). Post-transcriptional regulation of thyroid hormone receptor expression by cis-acting sequences and a naturally occurring antisense RNA. Journal of Biological Chemistry 275, 1150711513.

T. Ikeda (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, 329331.

M. G. Ivanchenko , J. P. Lerner , R. S. McCormick , A. Toumadje , B. Allen , K. Fischer , O. Hedstrom , A. Helmrich , D. W. Barnes and C. J. Bayne (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, 49654970.

E. R. Jolly , C. S. Chin , S. Miller , M. M. Bahgat , K. C. Lim , J. DeRisi and J. H. McKerrow (2007). Gene expression patterns during adaptation of a helminth parasite to different environmental niches. Genome Biology 8, R65.

T. Katsumata , S. Kohno , K. Yamaguchi , K. Hara and Y. Aoki (1989). Hatching of Schistosoma mansoni eggs is a Ca2+/calmodulin-dependent process. Parasitology Research 76, 9091.

T. Katsumata , M. Shimada , K. Sato and Y. Aoki (1988). Possible involvement of calcium ions in the hatching of Schistosoma mansoni eggs in water. Journal of Parasitology 74, 10401041.

F. Kawamoto , A. Shozawa , N. Kumada and K. Kojima (1989). Possible roles of cAMP and Ca2+ in the regulation of miracidial transformation in Schistosoma mansoni. Parasitology Research 75, 368374.

E. Knabe , D. E. Gilbertson and G. G. Plorin (1982). The effect of concentrations of external sodium and calcium on the swimming speed of Schistosoma mansoni miracidia. Journal of Parasitology 68, 507508.

G. M. Knudsen , K. F. Medzihradszky , K. C. Lim , E. Hansell and J. H. McKerrow (2005). Proteomic analysis of Schistosoma mansoni cercarial secretions. Molecular and Cellular Proteomics 4, 18621875.

J. W. Kronstad (2006). Serial analysis of gene expression in eukaryotic pathogens. Infectious Disorders – Drug Targets 6, 281297.

S. Lee , J. Bao , G. Zhou , J. Shapiro , J. Xu , R. Z. Shi , X. Lu , T. Clark , D. Johnson , Y. C. Kim , C. Wing , C. Tseng , M. Sun , W. Lin , J. Wang , H. Yang , J. Wang , W. Du , C. I. Wu , X. Zhang and S. M. Wang (2005). Detecting novel low-abundance transcripts in Drosophila. RNA 11, 939946.

M. Liniger , K. Bodenmüller , E. Pays , S. Gallati and I. Roditi (2001). Overlapping sense and antisense transcription units in Trypanosoma brucei. Molecular Microbiology 40, 869878.

F. Liu , J. Lu , W. Hu , S. Y. Wang , S. J. Cui , M. Chi , Q. Yan , X. R. Wang , H. D. Song , X. N. Xu , J. J. Wang , X. L. Zhang , X. Zhang , Z. Q. Wang , C. L. Xue , P. J. Brindley , D. P. McManus , P. Y. Yang , Z. Feng , Z. Chen and Z. G. Han (2006). New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. PLoS Pathogens 2, e29.

H. P. Luther , H. Haase , A. Hohaus , G. Beckmann , J. Reich and I. Morano (1998). Characterization of naturally occurring myosin heavy chain antisense mRNA in rat heart. Journal of Cell Biochemistry 70, 110120.

D. Moser , M. J. Doenhoff and M. Q. Klinkert (1992). A stage-specific calcium-binding protein expressed in eggs of Schistosoma mansoni. Molecular and Biochemical Parasitology 51, 229238.

V. Nene , D. W. Dunne , K. S. Johnson , D. W. Taylor and J. S. Cordingley (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, 179188.

F. Noel , V. M. Cunha , C. L. Silva and D. L. Mendonca-Silva (2001). Control of calcium homeostasis in Schistosoma mansoni. Memórias do Instituto Oswaldo Cruz 96, 8588.

E. P. Ojopi , P. S. Oliveira , D. N. Nunes , A. Paquola , R. DeMarco , S. P. Gregório , K. A. Aires , C. F. Menck , L. C. Leite , S. Verjovski-Almeida and E. Dias-Neto (2007). A quantitative view of the transcriptome of Schistosoma mansoni adult-worms using SAGE. BMC Genomics 8, 186191.

D. Palm , M. Weiland , A. G. McArthur , J. Winiecka-Krusnell , M. J. Cipriano , S. R. Birkeland , S. E. Pacocha , B. Davids , F. Gillin , E. Linder and S. Svard (2005). Developmental changes in the adhesive disk during Giardia differentiation. Molecular and Biochemical Parasitology 141, 199207.

S. Patankar , A. Munasinghe , A. Shoaibi , L. M. Cummings and D. F. Wirth (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, 31143125.

S. Saha , A. B. Sparks , C. Rago , V. Akmaev , C. J. Wang , B. Vogelstein , K. W. Kinzler and V. E. Velculescu (2002). Using the transcriptome to annotate the genome. Nature Biotechnology 20, 508512.

K. J. Song , K. H. Song , B. K. Na , J. H. Kim , D. Kwon , S. Park , J. H. Pak , K. I. Im and H. J. Shin (2007). Molecular cloning and characterization of a cytosolic heat shock protein 70 from Naegleria fowleri. Parasitology Research 100, 10831089.

G. M. Sponholtz and R. B. Short (1976). Schistosoma mansoni miracidia, stimulation by calcium and magnesium. Journal of Parasitology 62, 155157.

B. St-Croix , C. Rago , V. Velculescu , G. Traverso , K. E. Romans , E. Montgomery , A. Lal , G. J. Riggins , C. Lengauer , B. Vogelstein and K. W. Kinzler (2000). Genes expressed in human tumor endothelium. Science 289, 11971202.

D. J. Stekel , Y. Git and F. Falciani (2000). The comparison of gene expression from multiple cDNA libraries. Genome Research 10, 20552061.

V. E. Velculescu , L. Zhang , B. Vogelstein and K. W. Kinzler (1995). Serial analysis of gene expression. Science 270, 484487.

S. Verjovski-Almeida , T. M. Venancio , K. C. Oliveira , G. T. Almeida and R. Demarco (2007). Use of a 44 k oligoarray to explore the transcriptome of Schistosoma mansoni adult worms. Experimental Parasitology 117, 236245.

J. J. Vermeire , J. P. Boyle and T. P. Yoshino (2004). Differential gene expression and the effects of Biomphalaria glabrata embryonic (Bge) cell factors during larval Schistosoma mansoni development. Molecular and Biochemical Parasitology 135, 153157.

J. J. Vermeire , A. S. Taft , K. F. Hoffmann , J. M. Fitzpatrick and T. P. Yoshino (2006). Schistosoma mansoni, DNA microarray gene expression profiling during the miracidium-to-mother sporocyst transformation. Molecular and Biochemical Parasitology 147, 3947.

M. Voge and J. S. Seidel (1972). Transformation in vitro of miracidia of Schistosoma mansoni and S. japonicum into young sporocysts. Journal of Parasitology 58, 699704.

S. M. Wahl , M. Frazier-Jessen , W. W. Jin , J. B. Kopp , A. Sher and A. W. Cheever (1997). Cytokine regulation of schistosome-induced granuloma and fibrosis. Kidney International 51, 13701375.

M. Waisberg , F. P. Lobo , G. C. Cerqueira , L. K. Passo , O. S. Carvalho , G. R. Franco and N. M. El-Sayed (2007). Microarray analysis of gene expression induced by sexual contact in Schistosoma mansoni. BMC Genomics 8, 181195.

S. J. Winder , B. G. Allen , O. Clément-Chomienne and M. P. Walsh (1998). Regulation of smooth muscle actin-myosin interaction and force by calponin. Acta Physiologica Scandinavia 164, 415426.

M. Yoshihara and E. S. Montana (2004). The synaptotagmins: calcium sensors for vesicular trafficking. Neuroscientist 10, 566574.

T. P. Yoshino (1981). Concanavalin A-induced receptor redistribution on Biomphalaria glabrata hemocytes, characterization of capping and patching responses. Journal of Invertebrate Pathology 38, 102112.

T. P. Yoshino and J. R. Laursen (1995). Production of Schistosoma mansoni daughter sporocysts from mother sporocysts maintained in synxenic culture with Biomphalaria glabrata embryonic (Bge) cells. Journal of Parasitology 81, 714722.

J. C. Young , V. R. Agash , K. Siegers and F. U. Hartl (2004). Pathways of chaperone mediated protein folding in the cytosol. Nature Reviews Molecular Cell Biology 5, 781791.

G. Zhang , O. Schmidt and S. Asgari (2006). A calreticulin-like protein from endoparasitoid venom fluid is involved in host hemocyte inactivation. Developmental and Comparative Immunology 30, 756764.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 6
Total number of PDF views: 6 *
Loading metrics...

Abstract views

Total abstract views: 113 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 25th June 2017. This data will be updated every 24 hours.