Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-12-01T02:01:10.203Z Has data issue: false hasContentIssue false
  • English
  • Français

An historical and genomic view of schistosome conjugal biology with emphasis on sex-specific gene expression

Published online by Cambridge University Press:  12 May 2005

K. F. HOFFMANN
K. F. HOFFMANN
Affiliation:
University of Cambridge, Department of Pathology, Tennis Court Road, Cambridge, CB2 1QP, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

The genetic programmes associated with the sexual biology of dioecious schistosomes remain a critically important but significantly understudied area of parasitology. Throughout the last four decades, progress has been slow in describing the gross antigenic and proteomic differences linked to sexually mature schistosomes and in characterizing some of the sex-associated transcripts and regulatory mechanisms induced during developmental maturation. These investigations have been severely hindered by the lack of complete EST/genomic information, as well as corresponding post- and functional-genomic tools for studying these pathogenic parasites. As near complete transcriptomes for Schistosoma japonicum and S. mansoni have recently been reported, and both DNA microarrays and post-transcriptional gene silencing have been applied to schistosomes, the tools and techniques for the high-throughput identification and characterization of transcripts involved in conjugal biology are now readily available. Here, an historical review is presented that summarizes some of the most significant findings associated with schistosome sex and sexual maturation during the last several decades. Following this discussion is a current overview of some modern day genomic approaches used to study schistosomes, which illustrates how major advances in the field of conjugal biology will be achieved.

Keywords

Schistosomesexual-biologytranscriptiongenomicstranscriptomeDNA microarray
Type
Research Article
Information
Parasitology , Volume 128 , Issue S1 , October 2004 , pp. S11 - S22
Copyright
© 2004 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

AJIOKA, J. W., BOOTHROYD, J. C., BRUNK, B. P., HEHL, A., HILLIER, L., MANGER, I. D., MARRA, M., OVERTON, G. C., ROOS, D. S., WAN, K. L., WATERSTON, R. & SIBLEY, L. D. ( 1998). Gene discovery by EST sequencing in Toxoplasma gondii reveals sequences restricted to the Apicomplexa. Genome Research 8, 18–28.CrossRefGoogle Scholar
ARMSTRONG, J. ( 1965). Mating behavior and development of schistosomes in the mouse. Journal of Parasitology 51, 605–616.CrossRefGoogle Scholar
ARONSTEIN, W. S. & STRAND, M. ( 1983). Identification of species-specific and gender-specific proteins and glycoproteins of three human schistosomes. Journal of Parasitology 69, 1006–1017.CrossRefGoogle Scholar
ARONSTEIN, W. S. & STRAND, M. ( 1984). Gender-specific and pair-dependent glycoprotein antigens of Schistosoma mansoni. Journal of Parasitology 70, 545–557.CrossRefGoogle Scholar
ARONSTEIN, W. S. & STRAND, M. ( 1985). A glycoprotein antigen of Schistosoma mansoni expressed on the gynecophoral canal of mature male worms. American Journal of Tropical Medicine Hygiene 34, 508–512.CrossRefGoogle Scholar
ATKINSON, B. G. & ATKINSON, K. H. ( 1982). Schistosoma mansoni: one- and two-dimensional electrophoresis of proteins synthesized in vitro by males, females, and juveniles. Experimental Parasitology 53, 26–38.CrossRefGoogle Scholar
ATKINSON, K. H. ( 1980). Chromosome analysis of Schistosoma rodhaini (Trematoda: Schistosomatidae). Canadian Journal of Genetics and Cytology 22, 143–147.CrossRefGoogle Scholar
BASCH, P. F. ( 1990). Why do schistosomes have separate sexes? Parasitology Today 6, 160–163.Google Scholar
BASCH, P. F. ( 1991). Schistosomes: Development, Reproduction, and Host Relations. New York, Oxford University Press, Inc.
BASCH, P. F. & BASCH, N. ( 1984). Intergeneric reproductive stimulation and parthenogenesis in Schistosoma mansoni. Parasitology 89, 369–376.CrossRefGoogle Scholar
BEALL, M. J., McGONIGLE, S. & PEARCE, E. J. ( 2000). Functional conservation of Schistosoma mansoni Smads in TGF-beta signaling. Molecular and Biochemical Parasitology 111, 131–142.CrossRefGoogle Scholar
BECKER, W. ( 1977). [The activation of miracidia of Schistosoma mansoni in the eggshell: uptake of water and the metabolic changes connected with it (author's transl)]. Zeitschrif für Parasitenkunde 52, 69–79.CrossRefGoogle Scholar
BENNETT, J. L., SEED, J. L. & BOFF, M. ( 1978). Fluorescent histochemical localization of phenol oxidase in female Schistosoma mansoni. Journal of Parasitology 64, 941–944.CrossRefGoogle Scholar
BERGQUIST, N. R. & COLLEY, D. G. ( 1998). Schistosomiasis vaccines: research to development. Parasitology Today 14, 99–104.CrossRefGoogle Scholar
BOAG, P. R., NEWTON, S. E. & GASSER, R. B. ( 2001). Molecular aspects of sexual development and reproduction in nematodes and schistosomes. Advances in Parasitology 50, 153–198.CrossRefGoogle Scholar
BOBEK, L., REKOSH, D. M., VAN KEULEN, H. & LOVERDE, P. T. ( 1986). Characterization of a female-specific cDNA derived from a developmentally regulated mRNA in the human blood fluke Schistosoma mansoni. Proceedings of the National Academy of Sciences, USA 83, 5544–5548.CrossRefGoogle Scholar
BOBEK, L. A., REKOSH, D. M. & LOVERDE, P. T. ( 1988). Small gene family encoding an eggshell (chorion) protein of the human parasite Schistosoma mansoni. Molecular and Cell Biology 8, 3008–3016.CrossRefGoogle Scholar
BOOTH, M., MWATHA, J. K., JOSEPH, S., JONES, F. J., KADZO, H., IRERI, E., KAZIBWE, F., KEMIJUMBI, J., KARIUKI, C., KIMANI, G., OUMA, J. H., KABATEREINE, N. B., VENNERVELD, B. J. & DUNNE, D. W. ( 2004). Periportal fibrosis in human Schistosoma mansoni infection is associated with low IL-10, low IFN gamma, high TNF-alpha or low RANTES, depending on age and gender. Journal of Immunology 172, 1295–1303.CrossRefGoogle Scholar
BOSTIC, J. R. & STRAND, M. ( 1996). Molecular cloning of a Schistosoma mansoni protein expressed in the gynecophoral canal of male worms. Molecular and Biochemical Parasitology 79, 79–89.CrossRefGoogle Scholar
BOYLE, J. P., WU, X. J., SHOEMAKER, C. B. & YOSHINO, T. P. ( 2003). Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts. Molecular and Biochemical Parasitology 128, 205–215.CrossRefGoogle Scholar
BOYLE, J. P. & YOSHINO, T. P. ( 2003). Gene manipulation in parasitic helminths. International Journal for Parasitology 33, 1259–1268.CrossRefGoogle Scholar
BRAGA, V. M., TAVARES, C. A. & RUMJANEK, F. D. ( 1989). Protein characterization of sexually mature and immature forms of Schistosoma mansoni. Comparative Biochemistry and Physiology B 94, 427–433.CrossRefGoogle Scholar
CAFFREY, C. R., SALTER, J. P., LUCAS, K. D., KHIEM, D., HSIEH, I., LIM, K., RUPPEL, A., McKERROW, J. H. & SAJID, M. ( 2002). SmCB2, a novel tegumental cathepsin B from adult Schistosoma mansoni. Molecular and Biochemical Parasitology 121, 49–61.CrossRefGoogle Scholar
CHAN, M. S., GUYATT, H. L., BUNDY, D. A. & MEDLEY, G. F. ( 1996). Dynamic models of schistosomiasis morbidity. American Journal of Tropical Medicine and Hygiene 55, 52–62.CrossRefGoogle Scholar
CHEN, L. L., REKOSH, D. M. & LOVERDE, P. T. ( 1992). Schistosoma mansoni p48 eggshell protein gene: characterization, developmentally regulated expression and comparison to the p14 eggshell protein gene. Molecular and Biochemical Parasitology 52, 39–52.CrossRefGoogle Scholar
COLHOUN, L. M., FAIRWEATHER, I. & BRENNAN, G. P. ( 1998). Observations on the mechanism of eggshell formation in the liver fluke, Fasciola hepatica. Parasitology 116, 555–567.CrossRefGoogle Scholar
CORDEIRO, M. N. & GAZZINELLI, G. ( 1979). Schistosoma mansoni: resolution and molecular weight estimates of tegument glycoproteins by polyacrylamide gel electrophoresis. Experimental Parasitology 48, 337–344.CrossRefGoogle Scholar
DALTON, J. P., CLOUGH, K. A., JONES, M. K. & BRINDLEY, P. J. ( 1996). Characterization of the cathepsin-like cysteine proteinases of Schistosoma mansoni. Infection and Immunity 64, 1328–1334.Google Scholar
DESSEIN, A. J., HILLAIRE, D., ELWALI, N. E., MARQUET, S., MOHAMED-ALI, Q., MIRGHANI, A., HENRI, S., ABDELHAMEED, A. A., SAEED, O. K., MAGZOUB, M. M. & ABEL, L. ( 1999). Severe hepatic fibrosis in Schistosoma mansoni infection is controlled by a major locus that is closely linked to the interferon-gamma receptor gene. American Journal of Human Genetics 65, 709–721.CrossRefGoogle Scholar
DIETZEL, J., HIRZMANN, J., PREIS, D., SYMMONS, P. & KUNZ, W. ( 1992). Ferritins of Schistosoma mansoni: sequence comparison and expression in female and male worms. Molecular and Biochemal Parasitology 50, 245–254.CrossRefGoogle Scholar
ERASMUS, D. A. & DAVIES, T. W. ( 1979). Schistosoma mansoni and S. haematobium: calcium metabolism of the vitelline cell. Experimental Parasitology 47, 91–106.Google Scholar
ESHETE, F. & LOVERDE, P. T. ( 1993). Characteristics of phenol oxidase of Schistosoma mansoni and its functional implications in eggshell synthesis. Journal of Parasitology 79, 309–317.CrossRefGoogle Scholar
FANTAPPIE, M. R., FREEBERN, W. J., OSMAN, A., LADUCA, J., NILES, E. G. & LOVERDE, P. T. ( 2001). Evaluation of Schistosoma mansoni retinoid X receptor (SmRXR1 and SmRXR2) activity and tissue distribution. Molecular and Biochemical Parasitology 115, 87–99.CrossRefGoogle Scholar
FANTAPPIE, M. R., OSMAN, A., ERICSSON, C., NILES, E. G. & LOVERDE, P. T. ( 2003). Cloning of Schistosoma mansoni Seven in Absentia (SmSINA)(+) homologue cDNA, a gene involved in ubiquitination of SmRXR1 and SmRXR2. Molecular and Biochemical Parasitology 131, 45–54.CrossRefGoogle Scholar
FITZPATRICK, J. M., JOHANSEN, M. V., JOHNSTON, D. A., DUNNE, D. W. & HOFFMANN, K. F. ( 2004). Gender-associated gene expression in two related strains of Schistosoma japonicum. Molecular and Biochemical Parasitology 136, 191–209.CrossRefGoogle Scholar
FOULK, B. W., PAPPAS, G., HIRAI, Y., HIRAI, H. & WILLIAMS, D. L. ( 2002). Adenylosuccinate Lyase of Schistosoma mansoni: gene structure, mRNA expression, and analysis of the predicted peptide structure of a potential chemotherapeutic target. International Journal for Parasitology 32, 1487–1495.CrossRefGoogle Scholar
FREEBERN, W. J., NILES, E. G. & LOVERDE, P. T. ( 1999 a). RXR-2, a member of the retinoid x receptor family in Schistosoma mansoni. Gene 233, 33–38.Google Scholar
FREEBERN, W. J., OSMAN, A., NILES, E. G., CHRISTEN, L. & LOVERDE, P. T. ( 1999 b). Identification of a cDNA encoding a retinoid X receptor homologue from Schistosoma mansoni. Evidence for a role in female-specific gene expression. Journal of Biological Chemistry 274, 4577–4585.Google Scholar
FULFORD, A. J., BUTTERWORTH, A. E., OUMA, J. H. & STURROCK, R. F. ( 1995). A statistical approach to schistosome population dynamics and estimation of the life-span of Schistosoma mansoni in man. Parasitology 110, 307–316.CrossRefGoogle Scholar
GIANNINI, A. L., CARIDE, E. C., BRAGA, V. M. & RUMJANEK, F. D. ( 1995). F-10 nuclear binding proteins of Schistosoma mansoni: structural and functional features. Parasitology 110, 155–161.CrossRefGoogle Scholar
GRANT, C. T. & SENFT, A. W. ( 1971). Schistosome proteolytic enzyme. Comparative Biochemistry and Physiology 38, 663–678.CrossRefGoogle Scholar
GREVELDING, C. G., SOMMER, G. & KUNZ, W. ( 1997). Female-specific gene expression in Schistosoma mansoni is regulated by pairing. Parasitology 115, 635–640.CrossRefGoogle Scholar
GRZYCH, J. M., PEARCE, E. J., CHEEVER, A., CAULADA, Z. A., CASPAR, P., HEINY, S., LEWIS, F. & SHER, A. ( 1991). Egg deposition is the major stimulus for the production of Th2 cytokines in murine schistosomiasis mansoni. Journal of Immunology 146, 1322–1327.Google Scholar
GUPTA, B. C. & BASCH, P. F. ( 1987). The role of Schistosoma mansoni males in feeding and development of female worms. Journal of Parasitology 73, 481–486.CrossRefGoogle Scholar
HANNON, G. J. ( 2002). RNA interference. Nature 418, 244–251.CrossRefGoogle Scholar
HENKLE, K. J., COOK, G. A., FOSTER, L. A., ENGMAN, D. M., BOBEK, L. A., CAIN, G. D. & DONELSON, J. E. ( 1990). The gene family encoding eggshell proteins of Schistosoma japonicum. Molecular and Biochemical Parasitology 42, 69–82.CrossRefGoogle Scholar
HENRI, S., CHEVILLARD, C., MERGANI, A., PARIS, P., GAUDART, J., CAMILLA, C., DESSEIN, H., MONTERO, F., ELWALI, N. M. A., SAEED, O. K., MAGZOUB, M. & DESSEIN, A. J. ( 2002). Cytokine regulation of periportal fibrosis in human Schistosoma mansoni: IFN-gamma is associated with protection against fibrosis and TNF-alpha with aggravation of disease. Journal of Immunology 169, 929–936.CrossRefGoogle Scholar
HOFFMANN, K. F., JOHNSTON, D. A. & DUNNE, D. W. ( 2002 a). Identification of Schistosoma mansoni gender-associated gene transcripts by cDNA microarray profiling. Genome Biology 3, RESEARCH0041.Google Scholar
HOFFMANN, K. F., WYNN, T. A. & DUNNE, D. W. ( 2002 b). Cytokine-mediated host responses during schistosome infections; walking the fine line between immunological control and immunopathology. Advances in Parasitology 52, 265–307.Google Scholar
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. P., XUE, C. L., FENG, Z., CHEN, Z. & HAN, Z. G. ( 2003). Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nature Genetics 35, 139–147.CrossRefGoogle Scholar
JOHNSON, K. S., TAYLOR, D. W. & CORDINGLEY, J. S. ( 1987). Possible eggshell protein gene from Schistosoma mansoni. Molecular and Biochemical Parasitology 22, 89–100.CrossRefGoogle Scholar
KAMPKOTTER, A., RIDGERS, I., JOHNSTON, D. A., ROLLINSON, D., KUNZ, W. & GREVELDING, C. G. ( 1999). Schistosoma mansoni: cloning and characterization of the Ras homologue. Experimental Parasitology 91, 280–283.CrossRefGoogle Scholar
KNOBLOCH, J., WINNEN, R., QUACK, M., KUNZ, W. & GREVELDING, C. G. ( 2002). A novel Syk-family tyrosine kinase from Schistosoma mansoni which is preferentially transcribed in reproductive organs. Gene 294, 87–97.CrossRefGoogle Scholar
KOSTER, B., DARGATZ, H., SCHRODER, J., HIRZMANN, J., HAARMANN, C., SYMMONS, P. & KUNZ, W. ( 1988). Identification and localisation of the products of a putative eggshell precursor gene in the vitellarium of Schistosoma mansoni. Molecular and Biochemical Parasitology 31, 183–198.CrossRefGoogle Scholar
LAWRENCE, J. D. ( 1973). The ingestion of red blood cells by Schistosoma mansoni. Journal of Parasitology 59, 60–63.CrossRefGoogle Scholar
LIBERATOS, J. D. ( 1987). Schistosoma mansoni: male-biased sex ratios in snails and mice. Experimental Parasitology 64, 165–177.CrossRefGoogle Scholar
LIBERATOS, J. D. & SHORT, R. B. ( 1983). Identification of sex of schistosome larval stages. Journal of Parasitology 69, 1084–1089.CrossRefGoogle Scholar
LOEFFLER, I. K. & BENNETT, J. L. ( 1996). A rab-related GTP-binding protein in Schistosoma mansoni. Molecular and Biochemical Parasitology 77, 31–40.CrossRefGoogle Scholar
LOVERDE, P. T., REKOSH, D. M. & BOBEK, L. A. ( 1989). Developmentally regulated gene expression in Schistosoma. Experimental Parasitology 68, 116–120.CrossRefGoogle Scholar
LOVERDE, P. T. & CHEN, L. ( 1991). Schistosome female reproductive development. Parasitology Today 7, 303–308.CrossRefGoogle Scholar
MARQUET, S., ABEL, L., HILLAIRE, D., DESSEIN, H., KALIL, J., FEINGOLD, J., WEISSENBACH, J. & DESSEIN, A. J. ( 1996). Genetic localization of a locus controlling the intensity of infection by Schistosoma mansoni on chromosome 5q31-q33. Nature Genetics 14, 181–184.CrossRefGoogle Scholar
MARSHALL, A. J., BRUNET, L. R., VAN GESSEL, Y., ALCARAZ, A., BLISS, S. K., PEARCE, E. J. & DENKERS, E. Y. ( 1999). Toxoplasma gondii and Schistosoma mansoni synergize to promote hepatocyte dysfunction associated with high levels of plasma TNF-alpha and early death in C57BL/6 mice. Journal of Immunology 163, 2089–2097.Google Scholar
McGONIGLE, S., FEENEY, E. L., BEALL, M. J. & PEARCE, E. J. ( 2001). SIP, a novel SH3 domain-containing protein, interacts with Schistosoma mansoni receptor kinase 1. Molecular and Biochemical Parasitology 114, 119–123.CrossRefGoogle Scholar
McGONIGLE, S., LOSCHIAVO, M. & PEARCE, E. J. ( 2002). 14-3-3 proteins in Schistosoma mansoni; identification of a second epsilon isoform. International Journal for Parasitology 32, 685–693.CrossRefGoogle Scholar
MEI, H. & LOVERDE, P. T. ( 1997). Schistosoma mansoni: the developmental regulation and immunolocalization of antioxidant enzymes. Experimental Parasitology 86, 69–78.CrossRefGoogle Scholar
MENRATH, M., MICHEL, A. & KUNZ, W. ( 1995). A female-specific cDNA sequence of Schistosoma mansoni encoding a mucin-like protein that is expressed in the epithelial cells of the reproductive duct. Parasitology 111, 477–483.CrossRefGoogle Scholar
MITCHELL, G. F., GARCIA, E. G., WOOD, S. M., DIASANTA, R., ALMONTE, R., CALICA, E., DAVERN, K. M. & TIU, W. U. ( 1990). Studies on the sex ratio of worms in schistosome infections. Parasitology 101, 27–34.CrossRefGoogle Scholar
MITSIALIS, S. A., VELETZA, S. & KAFATOS, F. C. ( 1989). Transgenic regulation of moth chorion gene promoters in Drosophila: tissue, temporal, and quantitative control of four bidirectional promoters. Journal of Molecular Evolution 29, 486–495.CrossRefGoogle Scholar
MOHAMEO-ALI, Q., ELWALI, N. E., ABDELHAMEED, A. A., MERGANI, A., RAHOUD, S., ELAGIB, K. E., SAEED, O. K., ABEL, L., MAGZOUB, M. M. & DESSEIN, A. J. ( 1999). Susceptibility to periportal (Symmers) fibrosis in human Schistosoma mansoni infections: evidence that intensity and duration of infection, gender, and inherited factors are critical in disease progression. Journal of Infectious Diseases 180, 1298–1306.CrossRefGoogle Scholar
MOORE, D. V., YOLLES, T. K. & MELENEY, H. E. ( 1954). The relationship of male worms to the sexual development of female Schistosoma mansoni. Journal of Parasitology 40, 166–185.CrossRefGoogle Scholar
MWATHA, J. K., JONES, F. M., MOHAMED, G., NAUS, C. W., RILEY, E. M., BUTTERWORTH, A. E., KIMANI, G., KARIUKI, C. H., OUMA, J. H., KOECH, D. & DUNNE, D. W. ( 2003). Associations between anti-Schistosoma mansoni and anti-Plasmodium falciparum antibody responses and hepatosplenomegaly, in Kenyan schoolchildren. Journal of Infectious Diseases 187, 1337–1341.CrossRefGoogle Scholar
MWINZI, P. N., KARANJA, D. M., COLLEY, D. G., ORAGO, A. S. & SECOR, W. E. ( 2001). Cellular immune responses of schistosomiasis patients are altered by human immunodeficiency virus type 1 coinfection. Journal of Infectious Diseases 184, 488–496.CrossRefGoogle Scholar
NAUS, C. W., JONES, F. M., SATTI, M. Z., JOSEPH, S., RILEY, E. M., KIMANI, G., MWATH, J. K., KARIUKI, C. H., OUMA, J. H., KABATEREINE, N. B., VENNERVALD, B. J. & DUNNE, D. W. ( 2003). Serological responses among individuals in areas where both schistosomiasis and malaria are endemic: cross-reactivity between Schistosoma mansoni and Plasmodium falciparum. Journal of Infectious Diseases 187, 1272–1282.CrossRefGoogle Scholar
OSMAN, A., NILES, E. G. & LOVERDE, P. T. ( 1999). Characterization of the Ras homologue of Schistosoma mansoni. Molecular and Biochemical Parasitology 100, 27–41.CrossRefGoogle Scholar
PANDEY, A. V., BABBARWAL, V. K., OKOYEH, J. N., JOSHI, R. M., PURI, S. K., SINGH, R. L. & CHAUHAN, V. S. ( 2003). Hemozoin formation in malaria: a two-step process involving histidine-rich proteins and lipids. Biochemical and Biophysical Research Communications 308, 736–743.CrossRefGoogle Scholar
PEARCE, E. J., CASPAR, P., GRZYCH, J. M., LEWIS, F. A. & SHER, A. ( 1992). Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. Journal of Experimental Medicine 173, 159–162.Google Scholar
PLATT, T. R. & BROOKS, D. R. ( 1997). Evolution of the schistosomes (Digenea: Schistosomatoidea): the origin of dioecy and colonization of the venous system. Journal of Parasitology 83, 1035–1044.CrossRefGoogle Scholar
POPIEL, I. & BASCH, P. F. ( 1984). Reproductive development of female Schistosoma mansoni (Digenea: Schistosomatidae) following bisexual pairing of worms and worm segments. Journal of Experimental Zoology 232, 141–150.CrossRefGoogle Scholar
PRUGNOLLE, F., DE MEEUS, T., DURAND, P., SIRE, C. & THERON, A. ( 2002). Sex-specific genetic structure in Schistosoma mansoni: evolutionary and epidemiological implications. Molecular Ecology 11, 1231–1238.CrossRefGoogle Scholar
PRUGNOLLE, F., DURAND, P., THERON, A., CHEVILLON, C. & DE MEEUS, T. ( 2003). Sex-specific genetic structure: new trends for dioecious parasites. Trends in Parasitology 19, 171–174.CrossRefGoogle Scholar
REIS, M. G., KUHNS, J., BLANTON, R. & DAVIS, A. H. ( 1989). Localization and pattern of expression of a female specific mRNA in Schistosoma mansoni. Molecular and Biochemical Parasitology 32, 113–119.CrossRefGoogle Scholar
RIBEIRO-PAES, J. T. & RODRIGUES, V. ( 1997). Sex determination and female reproductive development in the genus Schistosoma: a review. Revista do Instituto de Medicina Tropical de Sal Paulo 39, 337–344.CrossRefGoogle Scholar
ROBINSON, D. L. ( 1960). Egg-laying by Schistosoma mansoni in vitro. Annals of Tropical Medicine and Parasitology 54, 112–117.CrossRefGoogle Scholar
ROCHE, C., LIU, J. L., LEPRESLE, T., CAPRON, A. & PIERCE, R. J. ( 1996). Tissue localization and stage-specific expression of the phospholipid hydroperoxide glutathione peroxidase of Schistosoma mansoni. Molecular and Biochemical Parasitology 75, 187–195.CrossRefGoogle Scholar
RODRIGUES, V., CHAUDHRI, M., KNIGHT, M., MEADOWS, H., CHAMBERS, A. E., TAYLOR, W. R., KELLY, C. & SIMPSON, A. J. ( 1989). Predicted structure of a major Schistosoma mansoni eggshell protein. Molecular and Biochemical Parasitology 32, 7–13.CrossRefGoogle Scholar
RODRIGUES, V. Jr., PIPER, K., COUISSINIER-PARIS, P., BACELAR, O., DESSEIN, H. & DESSEIN, A. J. ( 1999). Genetic control of schistosome infections by the SM1 locus of the 5q31-q33 region is linked to differentiation of type 2 helper T lymphocytes. Infection and Immunity 67, 4689–4692.Google Scholar
RUFF, M. D., DAVIS, G. M. & WERNER, J. K. ( 1973). Schistosoma japonicum: disc electrophoretic protein patterns of the Japanese, Philippine, and Formosan strains. Experimental Parasitology 33, 437–446.CrossRefGoogle Scholar
RUPPEL, A. & CIOLI, D. ( 1977). A comparative analysis of various developmental stages of Schistosoma mansoni with respect to their protein composition. Parasitology 75, 339–343.CrossRefGoogle Scholar
SCHECHTMAN, D., WINNEN, R., TARRAB-HAZDAI, R., RAM, D., SHINDER, V., GREVELDING, C. G., KUNZ, W. & ARNON, R. ( 2001). Expression and immunolocalization of the 14-3-3 protein of Schistosoma mansoni. Parasitology 123, 573–582.CrossRefGoogle Scholar
SCHENA, M., SHALON, D., DAVIS, R. W. & BROWN, P. O. ( 1995). Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270, 467–470.CrossRefGoogle Scholar
SCHUSSLER, P., GREVELDING, C. G. & KUNZ, W. ( 1997). Identification of Ras, MAP kinases, and a GAP protein in Schistosoma mansoni by immunoblotting and their putative involvement in male–female interaction. Parasitology 115, 629–634.CrossRefGoogle Scholar
SCHUSSLER, P., KOHRER, K., FINKEN-EIGEN, M., MICHEL, A., GREVELDING, C. G. & KUNZ, W. ( 1998). A female-specific cDNA sequence of Schistosoma mansoni encoding an amidase that is expressed in the gastrodermis. Parasitology 116, 131–137.CrossRefGoogle Scholar
SCHUSSLER, P., POTTERS, E., WINNEN, R., BOTTKE, W. & KUNZ, W. ( 1995). An isoform of ferritin as a component of protein yolk platelets in Schistosoma mansoni. Molecular Reproduction and Development 41, 325–330.CrossRefGoogle Scholar
SEED, J. L. & BENNETT, J. L. ( 1980). Schistosoma mansoni: phenol oxidase's role in eggshell formation. Experimental Parasitology 49, 430–441.CrossRefGoogle Scholar
SEED, J. L., KILTS, C. D. & BENNETT, J. L. ( 1980). Schistosoma mansoni: tyrosine, a putatuve in vivo substrate of phenol oxidase. Experimental Parasitology 50, 33–44.CrossRefGoogle Scholar
SHALON, D., SMITH, S. J. & BROWN, P. O. ( 1996). A DNA microarray system for analyzing complex DNA samples using two-color fluorescent probe hybridization. Genome Research 6, 639–645.CrossRefGoogle Scholar
SHAW, J. R. & ERASMUS, D. A. ( 1981). Schistosoma mansoni: an examination of the reproductive status of females from single sex infections. Parasitology 82, 121–124.CrossRefGoogle Scholar
SHAW, M. K. ( 1987). Schistosoma mansoni: vitelline gland development in females from single sex infections. Journal of Helminthology 61, 253–259.CrossRefGoogle Scholar
SHEA, M. J., KING, D. L., CONBOY, M. J., MARIANI, B. D. & KAFATOS, F. C. ( 1990). Proteins that bind to Drosophila chorion cis-regulatory elements: a new C2H2 zinc finger protein and a C2C2 steroid receptor-like component. Genes and Development 4, 1128–1140.CrossRefGoogle Scholar
SHORT, R. B. ( 1948). Hermaphrodites in a Puerto Rican strain of Schistosoma mansoni in vitro. Journal of Parasitology 34, 240–242.CrossRefGoogle Scholar
SHORT, R. B. ( 1957). Chromosome and sex in Schistosomatium douthitti. Journal of Heredity 48, 2–6.CrossRefGoogle Scholar
SIMPSON, A. J. & KNIGHT, M. ( 1986). Cloning of a major developmentally regulated gene expressed in mature females of Schistosoma mansoni. Molecular and Biochemical Parasitology 18, 25–35.CrossRefGoogle Scholar
SKELLY, P. J., DA'DARA, A. & HARN, D. A. ( 2003). Suppressions of cathepsin B expression in Schistosoma mansoni by RNA interference. International Journal for Parasitology 33, 363–369.CrossRefGoogle Scholar
SMYTH, D., McMANUS, D. P., SMOUT, M. J., LAHA, T., ZHANG, W. & LOUKAS, A. ( 2003). Isolation of cDNAs encoding secreted and transmembrane proteins from Schistosoma mansoni by a signal sequence trap method. Infection and Immunity 71, 2548–2554.CrossRefGoogle Scholar
SMYTH, J. D. & CLEGG, J. A. ( 1959). Egg-shell formation in trematodes and cestodes. Experimental Parasitology 8, 286–323.CrossRefGoogle Scholar
STURROCK, R. F. ( 1966). Daily egg output of schistosomes. Transactions of the Royal Society of Tropical Medicine and Hygiene 60, 139–140.Google Scholar
TEMPONE, A. J., AFONSO, A. O., NASCIMENTO, D. & RUMJANEK, F. D. ( 1999). Dolichol phosphate is a rate-limiting factor in mannosyl transferase activity of adult male worms of Schistosoma mansoni. Molecular and Cellular Biochemistry 198, 187–191.CrossRefGoogle Scholar
TEMPONE, A. J., FURTADO, D. R., GIMBA, E. R., OLIVEIRA, F. M. & RUMJANEK, F. D. ( 2002). Dolichol phosphate mannose synthase is differentially expressed in male and female worms of Schistosoma mansoni. Comparative Biochemistry and Physiology B Biochemistry and Molecular Biology 131, 465–474.CrossRefGoogle Scholar
VERJOVSKI-ALMEIDA, S., DEMARCO, R., MARTINS, E. A., GUIMARAES, 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., SA, 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. & DIAS-NETO, E. ( 2003). Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nature Genetics 35, 148–157.CrossRefGoogle Scholar
VERMEIRE, J. J., OSMAN, A., LOVERDE, P. T. & WILLIAMS, D. L. ( 2003). Characterisation of a Rho homologue of Schistosoma mansoni. International Journal for Parasitology 33, 721–731.CrossRefGoogle Scholar
VOGEL, H. ( 1947). Hermaphrodites of Schistosoma mansoni. Annals of Tropical Medicine and Parasitology 4, 266–277.CrossRefGoogle Scholar
WARREN, K. S. ( 1978). The pathology, pathobiology and pathogenesis of schistosomiasis. Nature 273, 609–612.CrossRefGoogle Scholar
WELLS, K. E. & CORDINGLEY, J. S. ( 1991). Schistosoma mansoni: eggshell formation is regulated by pH and calcium. Experimental Parasitology 73, 295–310.CrossRefGoogle Scholar
WELLS, K. E. & CORDINGLEY, J. S. ( 1992). The cell and molecular biology of eggshell formation in Schistosoma mansoni. Results and Problems in Cell Differentiation 19, 97–114.CrossRefGoogle Scholar