Cell Death and Reproductive Regression in Female Schistosoma mansoni

The vitellarium is a highly proliferative organ, producing cells which are incorporated along with a fertilized ovum into the schistosome egg. Vitellarial growth fails to occur in virgin female schistosomes in single sex (female-only) infections, and involution of this tissue, which is accompanied b...

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Main Authors: Galanti, Sarah E., Huang, Stanley Ching-Cheng, Pearce, Edward J.
Format: Online
Language:English
Published: Public Library of Science 2012
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3283563/
id pubmed-3283563
recordtype oai_dc
spelling pubmed-32835632012-02-23 Cell Death and Reproductive Regression in Female Schistosoma mansoni Galanti, Sarah E. Huang, Stanley Ching-Cheng Pearce, Edward J. Research Article The vitellarium is a highly proliferative organ, producing cells which are incorporated along with a fertilized ovum into the schistosome egg. Vitellarial growth fails to occur in virgin female schistosomes in single sex (female-only) infections, and involution of this tissue, which is accompanied by physical shrinkage of the entire worm, occurs when mature females sexually regress upon removal from their male partners. We have found that upon removal from their hosts into tissue culture, female parasites regress whether they are mated or not, but that cessation of egg production and a decline in expression of the vitelline gene p14 is delayed by mating. We used BrdU labeling to investigate whether there was a loss of proliferation in the vittelarium that might account for regression and found that the proliferation rate declined equally in paired and singled females once placed into culture. However, TUNEL staining and Caspase 3 activity measurements indicate that the loss of vitrellarial cellularity associated with regression is associated with profound apoptotic vitelline cell death, which is not apparent in the vitellaria of paired females immediately ex vivo, and which develops in vitro regardless of whether males are present or not. Furthermore, primordial vitellaria in virgin females have a high frequency of apoptotic cells but are characterized by a proliferation rate that is indistinguishable from that in fully developed vitellaria in mature paired females. Taken together, our data suggest that the vitelline proliferation rate is independent of pairing status. In contrast, the survival of vitelline cells, and therefore the development of the vitellarium, is highly male-dependent. Both processes are negatively affected by removal from the host regardless of whether male worms are present or not, and are unsustainable using standard tissue culture approaches. Public Library of Science 2012-02-21 /pmc/articles/PMC3283563/ /pubmed/22363825 http://dx.doi.org/10.1371/journal.pntd.0001509 Text en Galanti et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Galanti, Sarah E.
Huang, Stanley Ching-Cheng
Pearce, Edward J.
spellingShingle Galanti, Sarah E.
Huang, Stanley Ching-Cheng
Pearce, Edward J.
Cell Death and Reproductive Regression in Female Schistosoma mansoni
author_facet Galanti, Sarah E.
Huang, Stanley Ching-Cheng
Pearce, Edward J.
author_sort Galanti, Sarah E.
title Cell Death and Reproductive Regression in Female Schistosoma mansoni
title_short Cell Death and Reproductive Regression in Female Schistosoma mansoni
title_full Cell Death and Reproductive Regression in Female Schistosoma mansoni
title_fullStr Cell Death and Reproductive Regression in Female Schistosoma mansoni
title_full_unstemmed Cell Death and Reproductive Regression in Female Schistosoma mansoni
title_sort cell death and reproductive regression in female schistosoma mansoni
description The vitellarium is a highly proliferative organ, producing cells which are incorporated along with a fertilized ovum into the schistosome egg. Vitellarial growth fails to occur in virgin female schistosomes in single sex (female-only) infections, and involution of this tissue, which is accompanied by physical shrinkage of the entire worm, occurs when mature females sexually regress upon removal from their male partners. We have found that upon removal from their hosts into tissue culture, female parasites regress whether they are mated or not, but that cessation of egg production and a decline in expression of the vitelline gene p14 is delayed by mating. We used BrdU labeling to investigate whether there was a loss of proliferation in the vittelarium that might account for regression and found that the proliferation rate declined equally in paired and singled females once placed into culture. However, TUNEL staining and Caspase 3 activity measurements indicate that the loss of vitrellarial cellularity associated with regression is associated with profound apoptotic vitelline cell death, which is not apparent in the vitellaria of paired females immediately ex vivo, and which develops in vitro regardless of whether males are present or not. Furthermore, primordial vitellaria in virgin females have a high frequency of apoptotic cells but are characterized by a proliferation rate that is indistinguishable from that in fully developed vitellaria in mature paired females. Taken together, our data suggest that the vitelline proliferation rate is independent of pairing status. In contrast, the survival of vitelline cells, and therefore the development of the vitellarium, is highly male-dependent. Both processes are negatively affected by removal from the host regardless of whether male worms are present or not, and are unsustainable using standard tissue culture approaches.
publisher Public Library of Science
publishDate 2012
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3283563/
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