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Comparative analysis of transcriptional profiles of Schistosoma japonicum adult worms derived from primary-infected and re-infected water buffaloes

BACKGROUND: Schistosoma japonicum (S. japonicum) is an important zoonotic parasite that is prevalent in China and parts of Southeast Asia. Water buffaloes are an important reservoir and the main transmission sources of S. japonicum. However, self-curing and resistance to re-infection have been obser...

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Autores principales: Mao, Yudan, He, Chuanchuan, Li, Hao, Lu, Ke, Fu, Zhiqiang, Hong, Yang, Jin, Yamei, Lin, Jiaojiao, Zhang, Xin, Liu, Jinming
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6625002/
https://www.ncbi.nlm.nih.gov/pubmed/31296252
http://dx.doi.org/10.1186/s13071-019-3600-y
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author Mao, Yudan
He, Chuanchuan
Li, Hao
Lu, Ke
Fu, Zhiqiang
Hong, Yang
Jin, Yamei
Lin, Jiaojiao
Zhang, Xin
Liu, Jinming
author_facet Mao, Yudan
He, Chuanchuan
Li, Hao
Lu, Ke
Fu, Zhiqiang
Hong, Yang
Jin, Yamei
Lin, Jiaojiao
Zhang, Xin
Liu, Jinming
author_sort Mao, Yudan
collection PubMed
description BACKGROUND: Schistosoma japonicum (S. japonicum) is an important zoonotic parasite that is prevalent in China and parts of Southeast Asia. Water buffaloes are an important reservoir and the main transmission sources of S. japonicum. However, self-curing and resistance to re-infection have been observed in water buffaloes. RESULTS: In this study, we compared the morphometry and differences in transcriptional expression of adult S. japonicum worms recovered from primary-infected and re-infected water buffaloes using Illumina RNA-sequencing (RNA-Seq) technology. Results of morphometry analysis revealed that adult S. japonicum worms recovered from re-infected water buffaloes were runtish with smaller organs. The ventral length of male worms was shorter in re-infected buffaloes (328 ± 13 vs 273 ± 8 µm, P < 0.05), and in female worms the oral sucker length (44 ± 3 vs 33 ± 5 µm, P < 0.05), ovary length (578 ± 23 vs 297 ± 27 µm, P < 0.05) and width (150 ± 8 vs 104 ± 9 µm, P < 0.05) were shorter, with fewer eggs in the uteri (41 ± 2 vs 12 ± 1, P < 0.05). Of 13,605 identified genes, 112 were differentially expressed, including 51 upregulated and 61 downregulated genes, in worms from re-infected compared with primary-infected water buffaloes. Gene ontology (GO) enrichment analysis revealed that GO terms such as “oxidation-reduction process”, “calcium-dependent phospholipid binding”, “lipid binding” and “calcium ion binding” were significantly enriched in downregulated genes, whereas GO terms related to metabolism and biosynthesis were significantly enriched in upregulated genes. The results revealed that the downregulation of some important genes might contribute to a reduction in worm numbers and maldevelopment of surviving worms in re-infected water buffaloes. Furthermore, upregulation of genes related to metabolic processes and biosynthesis might be a compensatory mechanism of worms in disadvantageous environments. CONCLUSIONS: To our knowledge, our results present the first large-scale transcriptional expression study identifying the differences between adult S. japonicum worms from primary-infected and re-infected water buffaloes, and particularly emphasize differential expression that may affect the survival and growth of worms in re-infected water buffalo. This will provide new insight into screening for anti-schistosome targets and vaccine candidates. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-019-3600-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-66250022019-07-23 Comparative analysis of transcriptional profiles of Schistosoma japonicum adult worms derived from primary-infected and re-infected water buffaloes Mao, Yudan He, Chuanchuan Li, Hao Lu, Ke Fu, Zhiqiang Hong, Yang Jin, Yamei Lin, Jiaojiao Zhang, Xin Liu, Jinming Parasit Vectors Research BACKGROUND: Schistosoma japonicum (S. japonicum) is an important zoonotic parasite that is prevalent in China and parts of Southeast Asia. Water buffaloes are an important reservoir and the main transmission sources of S. japonicum. However, self-curing and resistance to re-infection have been observed in water buffaloes. RESULTS: In this study, we compared the morphometry and differences in transcriptional expression of adult S. japonicum worms recovered from primary-infected and re-infected water buffaloes using Illumina RNA-sequencing (RNA-Seq) technology. Results of morphometry analysis revealed that adult S. japonicum worms recovered from re-infected water buffaloes were runtish with smaller organs. The ventral length of male worms was shorter in re-infected buffaloes (328 ± 13 vs 273 ± 8 µm, P < 0.05), and in female worms the oral sucker length (44 ± 3 vs 33 ± 5 µm, P < 0.05), ovary length (578 ± 23 vs 297 ± 27 µm, P < 0.05) and width (150 ± 8 vs 104 ± 9 µm, P < 0.05) were shorter, with fewer eggs in the uteri (41 ± 2 vs 12 ± 1, P < 0.05). Of 13,605 identified genes, 112 were differentially expressed, including 51 upregulated and 61 downregulated genes, in worms from re-infected compared with primary-infected water buffaloes. Gene ontology (GO) enrichment analysis revealed that GO terms such as “oxidation-reduction process”, “calcium-dependent phospholipid binding”, “lipid binding” and “calcium ion binding” were significantly enriched in downregulated genes, whereas GO terms related to metabolism and biosynthesis were significantly enriched in upregulated genes. The results revealed that the downregulation of some important genes might contribute to a reduction in worm numbers and maldevelopment of surviving worms in re-infected water buffaloes. Furthermore, upregulation of genes related to metabolic processes and biosynthesis might be a compensatory mechanism of worms in disadvantageous environments. CONCLUSIONS: To our knowledge, our results present the first large-scale transcriptional expression study identifying the differences between adult S. japonicum worms from primary-infected and re-infected water buffaloes, and particularly emphasize differential expression that may affect the survival and growth of worms in re-infected water buffalo. This will provide new insight into screening for anti-schistosome targets and vaccine candidates. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-019-3600-y) contains supplementary material, which is available to authorized users. BioMed Central 2019-07-11 /pmc/articles/PMC6625002/ /pubmed/31296252 http://dx.doi.org/10.1186/s13071-019-3600-y Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Mao, Yudan
He, Chuanchuan
Li, Hao
Lu, Ke
Fu, Zhiqiang
Hong, Yang
Jin, Yamei
Lin, Jiaojiao
Zhang, Xin
Liu, Jinming
Comparative analysis of transcriptional profiles of Schistosoma japonicum adult worms derived from primary-infected and re-infected water buffaloes
title Comparative analysis of transcriptional profiles of Schistosoma japonicum adult worms derived from primary-infected and re-infected water buffaloes
title_full Comparative analysis of transcriptional profiles of Schistosoma japonicum adult worms derived from primary-infected and re-infected water buffaloes
title_fullStr Comparative analysis of transcriptional profiles of Schistosoma japonicum adult worms derived from primary-infected and re-infected water buffaloes
title_full_unstemmed Comparative analysis of transcriptional profiles of Schistosoma japonicum adult worms derived from primary-infected and re-infected water buffaloes
title_short Comparative analysis of transcriptional profiles of Schistosoma japonicum adult worms derived from primary-infected and re-infected water buffaloes
title_sort comparative analysis of transcriptional profiles of schistosoma japonicum adult worms derived from primary-infected and re-infected water buffaloes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6625002/
https://www.ncbi.nlm.nih.gov/pubmed/31296252
http://dx.doi.org/10.1186/s13071-019-3600-y
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