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A new ferritin SjFer0 affecting the growth and development of Schistosoma japonicum

BACKGROUND: Schistosomiasis, an acute and chronic parasitic disease, causes substantial morbidity and mortality in tropical and subtropical regions of the world. Iron is an essential constituent of numerous macromolecules involving in important cellular reactions in virtually all organisms. Trematod...

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Autores principales: Zeng, Fanyuan, Yi, Cun, Zhang, Wei, Cheng, Shaoyun, Sun, Chengsong, Luo, Fang, Feng, Zheng, Hu, Wei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9128280/
https://www.ncbi.nlm.nih.gov/pubmed/35610663
http://dx.doi.org/10.1186/s13071-022-05247-1
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author Zeng, Fanyuan
Yi, Cun
Zhang, Wei
Cheng, Shaoyun
Sun, Chengsong
Luo, Fang
Feng, Zheng
Hu, Wei
author_facet Zeng, Fanyuan
Yi, Cun
Zhang, Wei
Cheng, Shaoyun
Sun, Chengsong
Luo, Fang
Feng, Zheng
Hu, Wei
author_sort Zeng, Fanyuan
collection PubMed
description BACKGROUND: Schistosomiasis, an acute and chronic parasitic disease, causes substantial morbidity and mortality in tropical and subtropical regions of the world. Iron is an essential constituent of numerous macromolecules involving in important cellular reactions in virtually all organisms. Trematodes of the genus Schistosoma live in iron-rich blood, feed on red blood cells and store abundant iron in vitelline cells. Ferritins are multi-meric proteins that store iron inside cells. Three ferritin isoforms in Schistosoma japonicum are known, namely SjFer0, SjFer1 and SjFer2; however, their impact on the growth and development of the parasites  is still unknown. In this study we report on and characterize the ferritins in S. japonicum. METHODS: A phylogenetic tree of the SjFer0, SjFer1 and SjFer2 genes was constructed to show the evolutionary relationship among species of genus Schistosoma. RNA interference in vivo was used to investigate the impact of SjFer0 on schistosome growth and development.  Immunofluorescence assay was applied  to localize the expression of the ferritins. RNA-sequencing was performed  to characterize the iron transport profile after RNA interference. RESULTS: SjFer0 was found to have low similarity with SjFer1 and SjFer2 and contain an additional signal peptide sequence. Phylogenetic analysis revealed that SjFer0 can only cluster with some ferritins of other trematodes and tapeworms, suggesting that this ferritin branch might be unique to these parasites. RNA interference in vivo showed that SjFer0 significantly affected the growth and development of schistosomula but did not affect egg production of adult female worms. SjFer1 and SjFer2 had no significant impact on growth and development. The immunofluorescence study showed that SjFer0 was widely expressed in the somatic cells and vitelline glands but not in the testicle or ovary. RNA-sequencing indicated  that, in female, the ion transport process and calcium ion binding function were downregulated after SjFer0 RNA interference. Among the differentially downregulated genes, Sj-cpi-2, annexin and insulin-like growth factor-binding protein may be accounted for the suppression of schistosome growth and development. CONCLUSIONS: The results indicate that SjFer0 affects the growth and development of schistosomula but does not affect egg production of adult female worms. SjFer0 can rescue the growth of the fet3fet4 double mutant Saccharomyces cerevisiae (strain DEY1453), suggesting being able to promote iron absorption. The RNA interference of SjFer0 inferred that  the suppression of worm growth and development may via  down-regulating Sj-cpi-2, annexin, and IGFBP. GRAPHIC ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05247-1.
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spelling pubmed-91282802022-05-25 A new ferritin SjFer0 affecting the growth and development of Schistosoma japonicum Zeng, Fanyuan Yi, Cun Zhang, Wei Cheng, Shaoyun Sun, Chengsong Luo, Fang Feng, Zheng Hu, Wei Parasit Vectors Research BACKGROUND: Schistosomiasis, an acute and chronic parasitic disease, causes substantial morbidity and mortality in tropical and subtropical regions of the world. Iron is an essential constituent of numerous macromolecules involving in important cellular reactions in virtually all organisms. Trematodes of the genus Schistosoma live in iron-rich blood, feed on red blood cells and store abundant iron in vitelline cells. Ferritins are multi-meric proteins that store iron inside cells. Three ferritin isoforms in Schistosoma japonicum are known, namely SjFer0, SjFer1 and SjFer2; however, their impact on the growth and development of the parasites  is still unknown. In this study we report on and characterize the ferritins in S. japonicum. METHODS: A phylogenetic tree of the SjFer0, SjFer1 and SjFer2 genes was constructed to show the evolutionary relationship among species of genus Schistosoma. RNA interference in vivo was used to investigate the impact of SjFer0 on schistosome growth and development.  Immunofluorescence assay was applied  to localize the expression of the ferritins. RNA-sequencing was performed  to characterize the iron transport profile after RNA interference. RESULTS: SjFer0 was found to have low similarity with SjFer1 and SjFer2 and contain an additional signal peptide sequence. Phylogenetic analysis revealed that SjFer0 can only cluster with some ferritins of other trematodes and tapeworms, suggesting that this ferritin branch might be unique to these parasites. RNA interference in vivo showed that SjFer0 significantly affected the growth and development of schistosomula but did not affect egg production of adult female worms. SjFer1 and SjFer2 had no significant impact on growth and development. The immunofluorescence study showed that SjFer0 was widely expressed in the somatic cells and vitelline glands but not in the testicle or ovary. RNA-sequencing indicated  that, in female, the ion transport process and calcium ion binding function were downregulated after SjFer0 RNA interference. Among the differentially downregulated genes, Sj-cpi-2, annexin and insulin-like growth factor-binding protein may be accounted for the suppression of schistosome growth and development. CONCLUSIONS: The results indicate that SjFer0 affects the growth and development of schistosomula but does not affect egg production of adult female worms. SjFer0 can rescue the growth of the fet3fet4 double mutant Saccharomyces cerevisiae (strain DEY1453), suggesting being able to promote iron absorption. The RNA interference of SjFer0 inferred that  the suppression of worm growth and development may via  down-regulating Sj-cpi-2, annexin, and IGFBP. GRAPHIC ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05247-1. BioMed Central 2022-05-24 /pmc/articles/PMC9128280/ /pubmed/35610663 http://dx.doi.org/10.1186/s13071-022-05247-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Zeng, Fanyuan
Yi, Cun
Zhang, Wei
Cheng, Shaoyun
Sun, Chengsong
Luo, Fang
Feng, Zheng
Hu, Wei
A new ferritin SjFer0 affecting the growth and development of Schistosoma japonicum
title A new ferritin SjFer0 affecting the growth and development of Schistosoma japonicum
title_full A new ferritin SjFer0 affecting the growth and development of Schistosoma japonicum
title_fullStr A new ferritin SjFer0 affecting the growth and development of Schistosoma japonicum
title_full_unstemmed A new ferritin SjFer0 affecting the growth and development of Schistosoma japonicum
title_short A new ferritin SjFer0 affecting the growth and development of Schistosoma japonicum
title_sort new ferritin sjfer0 affecting the growth and development of schistosoma japonicum
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9128280/
https://www.ncbi.nlm.nih.gov/pubmed/35610663
http://dx.doi.org/10.1186/s13071-022-05247-1
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