The Relationship of Male Worms to the Sexual Development of Female Schistosoma mansoni

Moore, Donald V.; Yolles, Tamarath K.; Meleney, Henry E.

doi:10.2307/3274297

Cited by 66 publications

(20 citation statements)

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“…The identification of a specific gene in female schistosomes that seems to be activated in response to the presence of males provides the first clear confirmation at the molecular level of a classical morphological observation: female schistosomes do not complete physical or reproductive development unless worm pairing takes place (3,4). Since the changes that occur as a result of pairing are many, it seems likely that several genes could be regulated in this manner.…”

Section: (Upper)mentioning

confidence: 78%

“…Earlier studies dealing with female maturation and development demonstrated that the presence of the male worm is necessary for full growth and complete sexual maturation of the female (3,4). Female worms obtained from single-sex infections are stunted and not sexually developed (3,5), although male worms from single-sex infections appear normal (6,7).…”

mentioning

confidence: 99%

“…When sexually mature female worms are removed from their male partners, they stop laying eggs and regress to a condition morphologically resembling immature female parasites, until they are reunited with mature male worms. The stimulus from the male schistosome responsible for female growth, maturation, and fecundity is independent of sperm transfer (6,7,9), but its exact nature is unresolved (4,(10)(11)(12).…”

mentioning

confidence: 99%

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Characterization of a female-specific cDNA derived from a developmentally regulated mRNA in the human blood fluke Schistosoma mansoni.

Bobek

Rekosh

Keulen

et al. 1986

Proc. Natl. Acad. Sci. U.S.A.

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We have isolated and characterized a cDNA clone that is derived from a developmentally regulated mRNA found only in mature female schistosomes. The mRNA is approximately 950 nucleotides in length and is not detectable in immature female schistosomes isolated from single-sex infections, in male worms, or in eggs. During normal bisexual infections, the mRNA species is first detected 28 days after infection (the time of worm pairing) and increases to a high level 35 days after infection, coinciding with the start of egg production. The nucleotide sequence of the cDNA shows two large open reading frames in the coding strand. Several features of the clone, including the deduced sequence of the polypeptide encoded by one of the reading frames, suggest a relationship to the silk moth chorion (egg shell) gene family.The isolation of this clone provides us with a probe for further studies of female schistosome development and is a first step toward a detailed understanding of this process at the molecular level.Schistosomes are multicellular parasites whose life cycle includes both human and snail hosts. Schistosoma mansoni, as the other species that infect humans, inhabits the bloodstream of man. Infection begins when cercariae penetrate unbroken skin of humans who are in contact with fresh water containing Schistosoma. Once the skin is penetrated, the transformed parasite, termed a schistosomule, remains in the interstitial tissue for 2 days, then enters the circulation, and migrates to the lungs. By day 7-14 the parasites leave the lungs and migrate to the liver where male and female worms mate (approximately day 28), and encopula move to their final niche in the mesenteries. Egg laying commences about day 35 (1).Unlike most trematode parasites, schistosomes are dioecious. S. mansoni has 8 pairs of chromosomes, and the female schistosome is heterogametic (2). Sex is determined in the zygote, which develops into an embryonated egg.Earlier studies dealing with female maturation and development demonstrated that the presence of the male worm is necessary for full growth and complete sexual maturation of the female (3, 4). Female worms obtained from single-sex infections are stunted and not sexually developed (3, 5), although male worms from single-sex infections appear normal (6, 7). Moreover, Clough (8) showed that male worms are necessary to maintain, as well as to initiate, female maturation and fecundity. When sexually mature female worms are removed from their male partners, they stop laying eggs and regress to a condition morphologically resembling immature female parasites, until they are reunited with mature male worms. The stimulus from the male schistosome responsible for female growth, maturation, and fecundity is independent of sperm transfer (6, 7, 9), but its exact nature is unresolved (4, 10-12).The unusual interplay between male and female schistosomes in the regulation of female development provides a unique system to study sexual differentiation. Moreover, since the production of eggs by mature ...

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Section: (Upper)mentioning

confidence: 78%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Characterization of a female-specific cDNA derived from a developmentally regulated mRNA in the human blood fluke Schistosoma mansoni.

Bobek

Rekosh

Keulen

et al. 1986

Proc. Natl. Acad. Sci. U.S.A.

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“…Female schistosome physical and reproductive development is dependent on the presence of mature male worms (Armstrong, 1965, Erasmus, 1973, Michaels, 1969, Moore, et al, 1954, Shaw, 1977, Vogel, 1941. Females from single sex infections are underdeveloped in that they are stunted and exhibit an immature reproductive system.…”

Section: Biological Interplay Between Male and Female Parasitementioning

confidence: 99%

Schistosoma mansoni: TGF-β signaling pathways

LoVerde

Osman

Hinck

2007

Experimental Parasitology

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Schistosome parasites have co-evolved an intricate relationship with their human and snail hosts as well as a novel interplay between the adult male and female parasites. We review the role of the TGF-β signaling pathway in parasite development, host-parasite interactions and male-female interactions. The data to date supports multiple roles for the TGF-β signaling pathway throughout schistosome development, in particular in the tegument which is at the interface with the host and between the male and female schistosome, development of vitelline cells in female worms whose genes and development are regulated by a stimulus from the male schistosome and embryogenesis of the egg. The human ligand TGF-β1 has been demonstrated to regulate the expression of a schistosome target gene that encodes a gynecophoric canal protein in the schistosome worm itself. Studies on signaling in schistosomes opens a new era for investigation of host-parasite and malefemale interactions. Index DescriptorsHost-parasite interactions; Male-female interactions; Schistosoma mansoni; Smad; TGF-β Schistosome parasites are muticellular eukaryotic organisms with a complex life cycle that involves mammalian and snail hosts. The vertebrate endoparasitic life cycle begins when a schistosome parasite (cercariae) penetrates the skin of a host, it transforms into a schistosomule and begins its life as an endoparasite. To continue its development it must take advantage of signals from the host. Schistosome parasites stay in the skin and after two days enter the circulation and move to the lungs where they remain for further development. About day 8-15, the parasites leave the lungs and move to the portal circulation of the liver where the male and female worms mate. The male worm, through a set of unknown signals, stimulates female gene expression that results in reproductive development and subsequent egg production. The worm pairs move against the flow of blood into their final niche in the mesenteric veins. This stage of the parasite life cycle takes place in a milieu of host signaling molecules. Co-evolution has allowed the schistosome parasite to sense and respond to host mediators. As with all multicellular eucaryotic organisms, development proceeds through the elaboration and response to extracellular signals. In the case of an endoparasite such as the schistosomes, one must consider both external and internal signaling mechanisms in parasite-host and malefemale signaling pathways.

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“…This possibility has been suggested by previous studies including those of Severinghaus (1928) and Moore, Yolles & Meleney (1954). In a more recent study, Shaw (1977) found in a short-term in vitro study that only those S. mansoni females held in the gynecophoral canal of males showed normal vitelline cell development.…”

Section: Mating Behaviour Of Schistosomesmentioning

confidence: 74%

Patterns of sexual reproduction among parasitic platyhelminths

Nollen

1983

Parasitology

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Previous studies on the spermatogenesis and oogenesis of digeneans, monogeneans and cestodes are reviewed, including those in which isotopic labelling techniques have been utilized in order to determine the temporal duration of spermatogenic development stages. Similar labelling experiments have also provided information on the development and movement of oocytes in the female reproductive tract as well as indicating patterns of cell division and development in vitelline glands. The literature relating to the inseminative behaviour of parasitic platyhelminths is considered from a number of viewpoints including the patterns of cross- and self-insemination that occur in hermaphroditic digeneans, the mating behaviour of dioecious schistosomes, spermatophore production and insemination among monogeneans and the inseminative behaviour of polyzoic cestodes. The implications of selfing among parasitic platyhelminths are considered with respect to possible genetically deleterious consequences. In addition, consideration is given to the mechanisms underlying the fact that some species require cross-insemination or at least the presence of another worm in order to undergo normal growth and sexual development. Finally, experimental studies are reviewed which shed light on the strength of the barriers against hybridization that exist between well-defined species of parasitic platyhelminths.

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The Relationship of Male Worms to the Sexual Development of Female Schistosoma mansoni

Cited by 66 publications

References 4 publications

Characterization of a female-specific cDNA derived from a developmentally regulated mRNA in the human blood fluke Schistosoma mansoni.

Characterization of a female-specific cDNA derived from a developmentally regulated mRNA in the human blood fluke Schistosoma mansoni.

Schistosoma mansoni: TGF-β signaling pathways

Patterns of sexual reproduction among parasitic platyhelminths

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