Long non-coding RNAs are essential for Schistosoma mansoni pairing-dependent adult worm homeostasis and fertility

The trematode parasite Schistosoma mansoni causes schistosomiasis, which affects over 200 million people worldwide. Schistosomes are dioecious, with egg laying depending on the females' obligatory pairing with males. Long non-coding RNAs (lncRNAs) are transcripts longer than 200 nucleotides wit...

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Bibliographic Details
Published in:PLoS pathogens 2023-05, Vol.19 (5), p.e1011369-e1011369
Main Authors: Silveira, Gilbert O, Coelho, Helena S, Pereira, Adriana S A, Miyasato, Patrícia A, Santos, Daisy W, Maciel, Lucas F, Olberg, Giovanna G G, Tahira, Ana C, Nakano, Eliana, Oliveira, Maria Leonor S, Amaral, Murilo S, Verjovski-Almeida, Sergio
Format: Article
Language:English
Subjects:
Analysis
Animals
Biological properties
Biological samples
Biology and life sciences
Causes of
Cell growth
Cell proliferation
Drug resistance
Egg laying
Eggs
Female
Females
Fertility
Fertility - genetics
Gene expression
Gene loci
Gonads
Homeostasis
Hybridization
Infections
Maintenance
Male
Males
Mammals
Medicine and Health Sciences
Mice
Non-coding RNA
Nucleotides
Ovaries
Parasites
Parasites - genetics
Proteins
Reproduction
RNA
RNA sequencing
RNA, Long Noncoding - genetics
Schistosoma mansoni
Schistosoma mansoni - genetics
Schistosomiasis
Schistosomiasis mansoni - parasitology
Sex
Stem cells
Testes
Therapeutic targets
Tropical diseases
Worms
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Summary:The trematode parasite Schistosoma mansoni causes schistosomiasis, which affects over 200 million people worldwide. Schistosomes are dioecious, with egg laying depending on the females' obligatory pairing with males. Long non-coding RNAs (lncRNAs) are transcripts longer than 200 nucleotides with low or no protein-coding potential that have been involved in other species with reproduction, stem cell maintenance, and drug resistance. In S. mansoni, we recently showed that the knockdown of one lncRNA affects the pairing status of these parasites. Here, we re-analyzed public RNA-Seq data from paired and unpaired adult male and female worms and their gonads, obtained from mixed-sex or single-sex cercariae infections, and found thousands of differentially expressed pairing-dependent lncRNAs among the 23 biological samples that were compared. The expression levels of selected lncRNAs were validated by RT-qPCR using an in vitro unpairing model. In addition, the in vitro silencing of three selected lncRNAs showed that knockdown of these pairing-dependent lncRNAs reduced cell proliferation in adult worms and their gonads, and are essential for female vitellaria maintenance, reproduction, and/or egg development. Remarkably, in vivo silencing of each of the three selected lncRNAs significantly reduced worm burden in infected mice by 26 to 35%. Whole mount in situ hybridization experiments showed that these pairing-dependent lncRNAs are expressed in reproductive tissues. These results show that lncRNAs are key components intervening in S. mansoni adult worm homeostasis, which affects pairing status and survival in the mammalian host, thus presenting great potential as new therapeutic target candidates.
ISSN:1553-7374
1553-7366
1553-7374
DOI:10.1371/journal.ppat.1011369