Comparative analysis of microRNA expression profiles of adult Schistosoma japonicum isolated from water buffalo and yellow cattle

Abstract

Background Yellow cattle and water buffalo are important natural reservoir hosts and the main transmission sources of Schistosoma japonicum in endemic areas of China. The worms from the two hosts have marked differences in general worm morphology and ultrastructure, gene transcription and protein expression profiles. Results To investigate microRNAs (miRNAs) involved in the regulation of schistosome development and survival, we compared miRNA expression profiles of adult schistosomes derived from yellow cattle and water buffalo by using high-throughput sequencing with Illumina Hiseq Xten. Schistosoma japonicum from water buffalo and yellow cattle yielded 63.78 million and 63.21 million reads, respectively, of which nearly 50% and 49% could be mapped to selected miRNAs in miRbase. A total of 206 miRNAs were identified, namely 79 previously annotated miRNAs of S. japonicum and 127 miRNAs that matched with the S. japonicum genome and were highly similar to the annotated miRNAs from other organisms. Among the 79 miRNAs, five (sja-miR-124-3p, sja-miR-219-5p, sja-miR-2e-3p, sja-miR-7-3p and sja-miR-3490) were significantly upregulated in the schistosomes from water buffalo compared with those from yellow cattle. A total of 268 potential target genes were predicted for these five differentially expressed miRNAs. Eleven differentially expressed targets were confirmed by qRT-PCR among 15 tested targets, one of which was further validated through dual-luciferase reporter assay. Among the 127 ‘possible’ S. japonicum miRNAs, ten were significantly differentially expressed in the schistosomes from these two hosts. Conclusions These results highlight the important roles of miRNAs in regulating the development and survival of schistosomes in water buffalo and yellow cattle and facilitate understanding of the miRNA regulatory mechanisms in schistosomes derived from different susceptible hosts. Electronic supplementary material The online version of this article (10.1186/s13071-019-3450-7) contains supplementary material, which is available to authorized users.

The Potential Role of MicroRNA‐124‐3p in Growth, Development, and Reproduction of Schistosoma japonicum

“…Previous miRNA sequencing studies showed that sja-miR-124-3p in adult schistosomes isolated from water buffalo and 10-day-old schistosomula isolated from Wistar rats was significantly higher than that from yellow cattle and BALB/c mice, respectively ( Han et al., 2015a ; Yu X., et al., 2019 ). Moreover, the sja-miR-124-3p expression level in unisexual and stunted S. japonicum females was significantly higher than in paired females ( Han et al., 2020 ).…”

“…Then, equal amounts of parasites were mixed with RNAlater (Ambion, Carlsbad, CA, USA) in several sterile cryopreservation tubes and stored at −80°C until further use. The 56-day-old adult worms collected from yellow cattle and water buffalo were stored at −80°C in RNAlater and provided by the National Reference Laboratory for Animal Schistosomiasis, Shanghai Veterinary Research Institute, CAAS ( Yu X. et al., 2019 ).…”

“…However, significantly higher sja-miR-124 expressions were detected in immature worms compared with adults ( Huang et al., 2009 ), in males compared with females ( Cai et al., 2011 ; Zhu et al., 2016 ), and in single-sex infecting stunted females compared with bisexual infecting mature females ( Han et al., 2020 ). Moreover, the expression level of sja-miR-124-3p in adult schistosomes from the less suitable host (water buffalo) was always higher than that from the suitable host, yellow cattle ( Yu X., et al., 2019 ). The expression of sja-miR-124-3p in 10-day-old schistosomula from less suitable host Wistar rats was over 10 times than that from BALB/c mice ( Han et al., 2015a ).…”

“…MicroRNAs are considered potential targets for diagnosing and treating parasitic diseases due to their specific and complex regulatory effects ( Mu et al., 2020 ). Schistosoma japonicum miRNA presented differential expression patterns in worms at different developmental stages, sexes, and hosts ( Xue et al., 2008 ; Huang et al., 2009 ; Hao et al., 2010 ; Cai et al., 2011 ; Han et al., 2015a ; Han et al., 2015b ; Zhu et al., 2016 ; Yu X., et al., 2019 ).…”

Multifunctional Roles of MicroRNAs in Schistosomiasis

“…Schistosomes have numerous naturally permissive hosts (such as 46 species for S. japonicum , including cattle, pigs, sheep, goats, and mice) and non-adaptive hosts (such as water buffalo, Rattus norvegicus , Microtus fortis , and immunodeficient mice). Comparative studies elucidating the miRNA expression profiles of different hosts infected different developmental stages of schistosomes were also conducted ( Yu X. et al, 2019 ; Sun et al, 2021 ; Tang et al, 2021 ; Li et al, 2022 ; Liu et al, 2022 ). The characterization of differentially expressed worm-derived or host-derived miRNAs can also be a supplementary tool for grading and diagnosis of schistosomiasis ( Cai et al, 2018 ; Mu et al, 2019 ; Cai et al, 2020 ).…”