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


Journal

Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774

Informations de publication

Date de publication:
24 May 2022
Historique:
received: 08 09 2021
accepted: 21 03 2022
entrez: 24 5 2022
pubmed: 25 5 2022
medline: 27 5 2022
Statut: epublish

Résumé

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. 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. 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. 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.

Sections du résumé

BACKGROUND 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 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 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 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.

Identifiants

pubmed: 35610663
doi: 10.1186/s13071-022-05247-1
pii: 10.1186/s13071-022-05247-1
pmc: PMC9128280
doi:

Substances chimiques

Annexins 0
RNA 63231-63-0
Ferritins 9007-73-2
Iron E1UOL152H7

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

177

Subventions

Organisme : National Outstanding Youth Science Fund Project of National Natural Science Foundation of China
ID : 31725025
Organisme : Program of Shanghai Academic Research Leader
ID : 18XD1400400

Informations de copyright

© 2022. The Author(s).

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Auteurs

Fanyuan Zeng (F)

State Key Laboratory of Genetic Engineering, Ministry of Education Key Laboratory of Contemporary Anthropology, Collaborative Innovation Center for Genetics and Development, School of Life Sciences, Fudan University, 2005 Song Hu Road, Shanghai, 200438, People's Republic of China.

Cun Yi (C)

State Key Laboratory of Genetic Engineering, Ministry of Education Key Laboratory of Contemporary Anthropology, Collaborative Innovation Center for Genetics and Development, School of Life Sciences, Fudan University, 2005 Song Hu Road, Shanghai, 200438, People's Republic of China.

Wei Zhang (W)

State Key Laboratory of Genetic Engineering, Ministry of Education Key Laboratory of Contemporary Anthropology, Collaborative Innovation Center for Genetics and Development, School of Life Sciences, Fudan University, 2005 Song Hu Road, Shanghai, 200438, People's Republic of China.

Shaoyun Cheng (S)

State Key Laboratory of Genetic Engineering, Ministry of Education Key Laboratory of Contemporary Anthropology, Collaborative Innovation Center for Genetics and Development, School of Life Sciences, Fudan University, 2005 Song Hu Road, Shanghai, 200438, People's Republic of China.

Chengsong Sun (C)

State Key Laboratory of Genetic Engineering, Ministry of Education Key Laboratory of Contemporary Anthropology, Collaborative Innovation Center for Genetics and Development, School of Life Sciences, Fudan University, 2005 Song Hu Road, Shanghai, 200438, People's Republic of China.

Fang Luo (F)

State Key Laboratory of Genetic Engineering, Ministry of Education Key Laboratory of Contemporary Anthropology, Collaborative Innovation Center for Genetics and Development, School of Life Sciences, Fudan University, 2005 Song Hu Road, Shanghai, 200438, People's Republic of China.

Zheng Feng (Z)

Key Laboratory of Parasite and Vector Biology of the Chinese Ministry of Health, WHO Collaborating Center for Tropical Diseases, Joint Research Laboratory of Genetics and Ecology on Parasite-Host Interaction, National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, 200025, People's Republic of China.

Wei Hu (W)

State Key Laboratory of Genetic Engineering, Ministry of Education Key Laboratory of Contemporary Anthropology, Collaborative Innovation Center for Genetics and Development, School of Life Sciences, Fudan University, 2005 Song Hu Road, Shanghai, 200438, People's Republic of China. huw@fudan.edu.cn.
Key Laboratory of Parasite and Vector Biology of the Chinese Ministry of Health, WHO Collaborating Center for Tropical Diseases, Joint Research Laboratory of Genetics and Ecology on Parasite-Host Interaction, National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, 200025, People's Republic of China. huw@fudan.edu.cn.
State Key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock, School of Life Sciences, Inner Monglia University, Hohhot, 010030, People's Republic of China. huw@fudan.edu.cn.

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