Abstract
Schistosoma japonicum causes schistosomiasis in humans and livestock in the Asia-Pacific region. Knowledge of the genome of this parasite should improve understanding of schistosome-host interactions, biomedical aspects of schistosomiasis and invertebrate evolution. We assigned 43,707 expressed sequence tags (ESTs) derived from adult S. japonicum and their eggs to 13,131 gene clusters. Of these, 35% shared no similarity with known genes and 75% had not been reported previously in schistosomes. Notably, S. japonicum encoded mammalian-like receptors for insulin, progesterone, cytokines and neuropeptides, suggesting that host hormones, or endogenous parasite homologs, could orchestrate schistosome development and maturation and that schistosomes modulate anti-parasite immune responses through inhibitors, molecular mimicry and other evasion strategies.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Ross, A.G. et al. Schistosomiasis in the People's Republic of China: prospects and challenges for the 21st century. Clin. Microbiol. Rev. 14, 270–295 (2001).
Holland, P.W. The future of evolutionary developmental biology. Nature 402, C41–C44 (1999).
Dacks, J.B. & Doolittle, W.F. Reconstructing/deconstructing the earliest eukaryotes: how comparative genomics can help. Cell 107, 419–425 (2001).
Morand, S. & Muller-Graf, C.D. Muscles or testes? Comparative evidence for sexual competition among dioecious blood parasites (Schistosomatidae) of vertebrates. Parasitology 120, 45–56 (2000).
Boag, P.R., Newton, S.E. & Gasser, R.B. Molecular aspects of sexual development and reproduction in nematodes and schistosomes. Adv. Parasitol. 50, 153–198 (2001).
Ross, A.G. et al. Schistosomiasis. N. Engl. J. Med. 346, 1212–1220 (2002).
Salzet, M., Capron, A. & Stefano, G.B. Molecular crosstalk in host-parasite relationships: schistosome- and leech-host interactions. Parasitol. Today 16, 536–540 (2000).
Davies, S.J. et al. Modulation of blood fluke development in the liver by hepatic CD4+ lymphocytes. Science 294, 1358–1361 (2001).
Johnston, D.A. et al. Genomics and the biology of parasites. Bioessays 21, 131–147 (1999).
Rubin, G.M. et al. A Drosophila complementary DNA resource. Science 287, 2222–2224 (2000).
Thornton, J.W. & DeSalle, R. Gene family evolution and homology: genomics meets phylogenetics. Annu. Rev. Genomics Hum. Genet. 1, 41–73 (2000).
Venter, J.C. et al. The sequence of the human genome. Science 291, 1304–1351 (2001).
Lander, E.S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001).
Ashburner, M. et al. Gene Ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25–29 (2000).
The Gene Ontology Consortium. Creating the gene ontology resource: design and implementation. Genome Res. 11, 1425–1433 (2001).
Brindley, P.J. et al. Proteolytic degradation of host hemoglobin by schistosomes. Mol. Biochem. Parasitol. 89, 1–9 (1997).
Halton, D.W. Nutritional adaptations to parasitism within the platyhelminthes. Int. J. Parasitol. 27, 693–704 (1997).
Camacho, M. & Agnew, A. Glucose uptake rates by Schistosoma mansoni, S. haematobium, and S. bovis adults using a flow in vitro culture system. J. Parasitol. 81, 637–640 (1995).
Skelly, P.J., Kim, J.W., Cunningham, J. & Shoemaker, C.B. Cloning, characterization, and functional expression of cDNAs encoding glucose transporter proteins from the human parasite Schistosoma mansoni. J. Biol. Chem. 269, 4247–4253 (1994).
Skelly, P.J. & Shoemaker, C.B. Rapid appearance and asymmetric distribution of glucose transporter SGTP4 at the apical surface of intramammalian-stage Schistosoma mansoni. Proc. Natl. Acad. Sci. USA 93, 3642–3646 (1996).
Bueding, E. & Fisher, J. Metabolic requirements of schistosomes. J. Parasitol. 68, 208–212 (1982).
Hoffmann, K.F., Johnston, D.A. & Dunne, D.W. Identification of Schistosoma mansoni gender-associated gene transcripts by cDNA microarray profiling. Genome Biol. 3, RESEARCH0041 (2002).
Gorman, M., Kuroda, M.I. & Baker, B.S. Regulation of the sex-specific binding of the maleless dosage compensation protein to the male X chromosome in Drosophila. Cell 72, 39–49 (1993).
Pultz, M.A. & Baker, B.S. The dual role of hermaphrodite in the Drosophila sex determination regulatory hierarchy. Development 121, 99–111 (1995).
Sokol, S.B. & Kuwabara, P.E. Proteolysis in Caenorhabditis elegans sex determination: cleavage of TRA-2A by TRA-3. Genes Dev. 14, 901–906 (2000).
Kuwabara, P.E., Okkema, P.G. & Kimble, J. Germ-line regulation of the Caenorhabditis elegans sex-determining gene tra-2. Dev. Biol. 204, 251–262 (1998).
Lum, D.H., Kuwabara, P.E., Zarkower, D. & Spence, A.M. Direct protein-protein interaction between the intracellular domain of TRA-2 and the transcription factor TRA-1A modulates feminizing activity in C. elegans. Genes Dev. 14, 3153–3165 (2000).
Bostic, J.R. & Strand, M. Molecular cloning of a Schistosoma mansoni protein expressed in the gynecophoral canal of male worms. Mol. Biochem. Parasitol. 79, 79–89 (1996).
Ravindran, B. Are inflammation and immunological hyperactivity needed for filarial parasite development? Trends Parasitol. 17, 70–73 (2001).
Amiri, P. et al. Tumour necrosis factor alpha restores granulomas and induces parasite egg-laying in schistosome-infected SCID mice. Nature 356, 604–607 (1992).
Pearce, E.J. & MacDonald, A.S. The immunobiology of schistosomiasis. Nat. Rev. Immunol. 2, 499–511 (2002).
Gardner, M.J. et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498–511 (2002).
Santos, T.M. et al. Analysis of the gene expression profile of Schistosoma mansoni cercariae using the expressed sequence tag approach. Mol. Biochem. Parasitol. 103, 79–97 (1999).
Li, L. et al. Gene discovery in the apicomplexa as revealed by EST sequencing and assembly of a comparative gene database. Genome Res. 13, 443–454 (2003).
Blair, J.E., Ikeo, K., Gojobori, T. & Hedges, S.B. The evolutionary position of nematodes. BMC Evol. Biol. 2, 7 (2002).
Adoutte, A. et al. The new animal phylogeny: reliability and implications. Proc. Natl. Acad. Sci. USA 97, 4453–4456 (2000).
Le, T.H., Blair, D. & McManus, D.P. Mitochondrial genomes of parasitic flatworms. Trends Parasitol. 18, 206–213 (2002).
Rubin, G.M. et al. Comparative genomics of the eukaryotes. Science 287, 2204–2215 (2000).
Li, W.H., Gu, Z., Wang, H. & Nekrutenko, A. Evolutionary analyses of the human genome. Nature 409, 847–849 (2001).
Lipman, D.J., Souvorov, A., Koonin, E.V., Panchenko, A.R. & Tatusova, T.A. The relationship of protein conservation and sequence length. BMC Evol. Biol. 2, 20 (2002).
de Mendonca, R.L., Escriva, H., Bouton, D., Laudet, V. & Pierce, R.J. Hormones and nuclear receptors in schistosome development. Parasitol. Today 16, 233–240 (2000).
Imase, A., Kobayashi, K., Ohmae, H., Matsuda, H. & Iwamura, Y. Horizontal and vertical transmission of mouse class I MHC sequence in Schistosoma mansoni. Parasitology 123, 163–168 (2001).
Xu, X.R. et al. Insight into hepatocellular carcinogenesis at transcriptome level by comparing gene expression profiles of hepatocellular carcinoma with those of corresponding noncancerous liver. Proc. Natl. Acad. Sci. USA 98, 15089–15094 (2001).
Kumar, S., Tamura, K., Jakobsen, I.B. & Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245 (2001).
Mei, H. & LoVerde, P.T. Schistosoma mansoni: the developmental regulation and immunolocalization of antioxidant enzymes. Exp. Parasitol. 86, 69–78 (1997).
Audic, S. & Claverie, J.M. The significance of digital gene expression profiles. Genome Res. 7, 986–995 (1997).
Acknowledgements
The Chinese High-Tech Research and Development Program, Chinese National Key Program on Basic Research, National Foundation for Excellence Doctoral Project, National Natural Science Foundation of China, Shanghai Commission for Science and Technology, and National Institute of Allergy and Infectious Diseases, National Institutes of Health, USA, supported this work.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Rights and permissions
About this article
Cite this article
Hu, W., Yan, Q., Shen, DK. et al. Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nat Genet 35, 139–147 (2003). https://doi.org/10.1038/ng1236
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ng1236
This article is cited by
-
Identification of Schistosoma japonicum GSK3β interacting partners by yeast two-hybrid screening and its role in parasite survival
Parasitology Research (2020)
-
A novel progesterone receptor membrane component (PGRMC) in the human and swine parasite Taenia solium: implications to the host-parasite relationship
Parasites & Vectors (2018)
-
Identification and validation of a Schistosoma japonicum U6 promoter
Parasites & Vectors (2017)
-
A next-generation microarray further reveals stage-enriched gene expression pattern in the blood fluke Schistosoma japonicum
Parasites & Vectors (2017)
-
Suppression of VAMP2 Alters Morphology of the Tegument and Affects Glucose uptake, Development and Reproduction of Schistosoma japonicum
Scientific Reports (2017)