De Novo Transcriptome Analysis of Oncomelania hupensis after Molluscicide Treatment by Next-Generation Sequencing: Implications for Biology and Future Snail Interventions

Zhao, Qin; Xiong, Tingting; Xu, Xin; Jiang, Ming; Dong, Hui

doi:10.1371/journal.pone.0118673

Cited by 26 publications

(24 citation statements)

References 31 publications

(36 reference statements)

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“…Based on Illumina RNA-seq analysis, Zhao et al (2015) described the responses of the amphibious snail, Oncomelania hupensis , after challenge with two different niclosamide-based molluscicides. They showed that two CYP genes and one GST gene were upregulated following molluscicide exposure [ 51 ]. This observation coupled with our results suggests that both enzyme families are a common component of the snail transcriptomic response to molluscicides.…”

Section: Discussionmentioning

confidence: 99%

Altered Gene Expression in the Schistosome-Transmitting Snail Biomphalaria glabrata following Exposure to Niclosamide, the Active Ingredient in the Widely Used Molluscicide Bayluscide

et al. 2015

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In view of the call by the World Health Organization (WHO) for elimination of schistosomiasis as a public health problem by 2025, use of molluscicides in snail control to supplement chemotherapy–based control efforts is likely to increase in the coming years. The mechanisms of action of niclosamide, the active ingredient in the most widely used molluscicides, remain largely unknown. A better understanding of its toxicology at the molecular level will both improve our knowledge of snail biology and may offer valuable insights into the development of better chemical control methods for snails. We used a recently developed Biomphalaria glabrata oligonucleotide microarray (31K features) to investigate the effect of sublethal exposure to niclosamide on the transcriptional responses of the snail B. glabrata relative to untreated snails. Most of the genes highly upregulated following exposure of snails to niclosamide are involved in biotransformation of xenobiotics, including genes encoding cytochrome P450s (CYP), glutathione S-transferases (GST), and drug transporters, notably multi-drug resistance protein (efflux transporter) and solute linked carrier (influx transporter). Niclosamide also induced stress responses. Specifically, six heat shock protein (HSP) genes from three super-families (HSP20, HSP40 and HSP70) were upregulated. Genes encoding ADP-ribosylation factor (ARF), cAMP response element-binding protein (CREB) and coatomer, all of which are involved in vesicle trafficking in the Golgi of mammalian cells, were also upregulated. Lastly, a hemoglobin gene was downregulated, suggesting niclosamide may affect oxygen transport. Our results show that snails mount substantial responses to sublethal concentrations of niclosamide, at least some of which appear to be protective. The topic of how niclosamide’s lethality at higher concentrations is determined requires further study. Given that niclosamide has also been used as an anthelmintic drug for decades and has been found to have activity against several types of cancer, our findings may be of relevance in understanding how both parasites and neoplastic cells respond to this compound.

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Section: Discussionmentioning

confidence: 99%

Altered Gene Expression in the Schistosome-Transmitting Snail Biomphalaria glabrata following Exposure to Niclosamide, the Active Ingredient in the Widely Used Molluscicide Bayluscide

et al. 2015

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“…Zhao et al [15] undertook an Illumina-based study of the molluscicide-induced transcriptome of Oncomelania hupensis, the pomatiopsid snail host of S. japonicum. The response of B. pfeifferi to simultaneous exposure to schistosome infection and niclosamide exposure is the first glimpse we have for how snails respond transcriptionally to simultaneous exposure to these two relevant stressors.…”

Section: Resultsmentioning

confidence: 99%

“…CYPs are also up-regulated in B. pfeifferi in response to niclosamide exposure, including two in common with B. glabrata ( Table 1) Glutathione-S-transferase 7-like (GST) was up-regulated 5-fold following niclosamide exposure in B. glabrata [16]. In addition to CYPs, GST has also been shown to be upregulated following niclosamide-based molluscicide exposure in Oncomelania hupensis [15].…”

Section: Shared Response Of Two Biomphalaria Species To a Sublethal Dmentioning

confidence: 99%

Transcriptional responses ofBiomphalaria pfeifferiandSchistosoma mansonifollowing exposure to niclosamide, with evidence for a synergistic effect on snails following exposure to both stressors

Buddenborg¹,

Kamel²,

Zhang³

et al. 2018

Preprint

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BackgroundSchistosomiasis is one of the world's most common NTDs. Successful control operations often target snail vectors with the molluscicide niclosamide. Little is known about how niclosamide affects snails, including for Biomphalaria pfeifferi, the most important vector for Schistosoma mansoni in Africa. We used Illumina technology to explore how field-derived B. pfeifferi, either uninfected or harboring cercariae-producing S. mansoni sporocysts, respond to a sublethal exposure of niclosamide. This study afforded the opportunity to determine if snails respond differently to biotic or abiotic stressors, and if they reserve unique responses for when presented with both stressors in combination. We also examined how sporocysts respond when their snail host is exposed to niclosamide. Principal FindingsCercariae-producing sporocysts within snails exposed to niclosamide express ~68% of the genes in the S. mansoni genome, as compared to 66% expressed by intramolluscan stages of S. mansoni in snails not exposed to niclosamide. Niclosamide does not disable sporocysts nor does it seem to provoke from them distinctive responses associated with detoxifying a xenobiotic. For B. pfeifferi, niclosamide treatment alone increases expression of several features not up-regulated in infected snails including particular cytochrome p450s and heat shock proteins, glutathione-S-transferases, antimicrobial factors like LBP/BPI and protease inhibitors, and also provokes strong down regulation of proteases. Exposure of infected snails to niclosamide resulted in numerous up-regulated responses associated with apoptosis along with down-regulated ribosomal and defense functions, indicative of a distinctive, compromised state not achieved with either stimulus alone. Conclusions/SignificanceThis study helps define the transcriptomic responses of an important and under-studied schistosome vector to S. mansoni sporocysts, to niclosamide, and to both in combination. It suggests the response of S. mansoni sporocysts to niclosamide is minimal and not reflective of a distinct repertoire of genes to handle xenobiotics while in the snail host. It also offers new insights for how niclosamide affects snails. AUTHOR'S SUMMARYSchistosomaisis control programs often employ the use of chemical molluscicides, such as niclosamide, to control the obligatory intermediate snail hosts. Despite its widespread use, we know little about how niclosamide affects snails like Biomphalaria pfeifferi, the most important vector Schistosoma mansoni in Africa. By sequencing the transcriptomes of uninfected and S. mansoni-infected B. pfeifferi exposed to niclosamide, we analyze the snail's response to both biotic and abiotic stressors. We can also examine the response of S. mansoni to niclosamide exposure during intramolluscan development. Biomphalaria pfeifferi snails exposed only to niclosamide showed unique up-regulation of stress and defense-related transcripts not seen in snails infected with a biotic, like S. mansoni infection, alone. Schistosoma mansoni-infected B. ...

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“…By contrast, only a few study focused on the transcriptomic studies in the snail O. hupensis, for instance, Zhao et al have characterized the transcriptome profiling of O. hupensis from the two distinct habitats and identified thousands of genes that show either increased or decreased expression [15]. A RNA-Seq experiment revealed that gene expression of O. hupensis showed significantly effects exposed to two kinds of molluscicides [14]. Together these data demonstrate the highly dynamic nature of transcriptomic profile in response to environment, infection and molluscicide.…”

Section: Discussionmentioning

confidence: 99%

“…For O. hupensis, transcriptomic studies by RNA-seq have been performed after molluscicide treatment. Many genes involved in key processes associated with biological regulation and innate immunity have been identified, which would benefit for elucidating the molluscicidal mechanism [14]. Another study by comparing the differences in gene expression between the hilly and marshland snails revealed that there is a potential relationship between expression profiling and ecological adaptation of the snail that may have implications for schistosomiasis control in future [15].…”

Section: Introductionmentioning

confidence: 99%

Temporal transcriptome change of Oncomelania hupensis revealed by Schistosoma japonicum invasion

et al. 2020

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Background: The freshwater snail Oncomelania hupensis is the obligate intermediate host for Schistosoma japonicum in China. Transcriptomic examination of snail-schistosome interactions can provide valuable information of host response at physiological and immune levels. Methods: To investigate S. japonicum-induced changes in O. hupensis gene expression, we utilized high-throughput sequencing to identify transcripts that were differentially expressed between infected snails and their uninfected controls at two key time-point, Day 7 and Day 30 after challenge. Time-series transcriptomic profiles were analyzed using R package DESeq 2, followed by GO, KEGG and (weighted gene correlation network analysis) WGCNA analysis to elucidate and identify important molecular mechanism, and subsequently understand host-parasite relationship. The identified unigenes was verified by bioinformatics and real-time PCR. Possible adaptation molecular mechanisms of O. hupensis to S. japonicum challenge were proposed. Results: Transcriptomic analyses of O. hupensis by S. japonicum invasion yielded billion reads including 92,144 annotated transcripts. Over 5000 differentially expressed genes (DEGs) were identified by pairwise comparisons of infected libraries from two time points to uninfected libraries in O. hupensis. In total, 6032 gene ontology terms and 149 KEGG pathways were enriched. After the snails were infected with S. japonicum on Day 7 and Day 30, DEGs were shown to be involved in many key processes associated with biological regulation and innate immunity pathways. Gene expression patterns differed after exposure to S. japonicum. Using WGCNA, 16 modules were identified. Module-trait analysis identified that a module involved in RNA binding, ribosome, translation, mRNA processing, and structural constituent of ribosome were strongly associated with S. japonicum invasion. Many of the genes from enriched KEGG pathways were involved in lysosome, spliceosome and ribosome, indicating that S. japonicum invasion may activate the regulation of ribosomes and immune response to infection in O. hupensis. Conclusions: Our analysis provided a temporally dynamic gene expression pattern of O. hupensis by S. japonicum invasion. The identification of gene candidates serves as a foundation for future investigations of S. japonicum infection. Additionally, major DEGs expression patterns and putative key regulatory pathways would provide useful information to construct gene regulatory networks between host-parasite crosstalk.

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De Novo Transcriptome Analysis of Oncomelania hupensis after Molluscicide Treatment by Next-Generation Sequencing: Implications for Biology and Future Snail Interventions

Cited by 26 publications

References 31 publications

Altered Gene Expression in the Schistosome-Transmitting Snail Biomphalaria glabrata following Exposure to Niclosamide, the Active Ingredient in the Widely Used Molluscicide Bayluscide

Altered Gene Expression in the Schistosome-Transmitting Snail Biomphalaria glabrata following Exposure to Niclosamide, the Active Ingredient in the Widely Used Molluscicide Bayluscide

Transcriptional responses ofBiomphalaria pfeifferiandSchistosoma mansonifollowing exposure to niclosamide, with evidence for a synergistic effect on snails following exposure to both stressors

Temporal transcriptome change of Oncomelania hupensis revealed by Schistosoma japonicum invasion

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