Proteases and their inhibitors involved in Schistosoma mansoni egg-host interaction revealed by comparative transcriptomics with Fasciola hepatica eggs

Peterkova, Kristyna; Vorel, Jiří; Ilgová, Jana; Ostasov, Pavel; Fajtová, Pavla; Konecny, Lukas; Chanová, Marta; Kašný, Martin; Horn, Martin; Dvořák, Jan

doi:10.1016/j.ijpara.2022.12.007

Cited by 6 publications

(9 citation statements)

References 63 publications

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“…This process involves a multienzymatic network cascade, featuring clan CA (cathepsins B, C and L) and AA (cathepsin D) cysteine peptidases, alongside aminopeptidases [ 62 , 63 ]. So far, they have been identified in Nematoda, Trematoda, Cestoda [ 64 – 66 ], Monopisthocotyla and Polyopisthocotyla [ 9 , 11 , 15 , 16 ].…”

Section: Discussionmentioning

confidence: 99%

An inside out journey: biogenesis, ultrastructure and proteomic characterisation of the ectoparasitic flatworm Sparicotyle chrysophrii extracellular vesicles

Riera-Ferrer,

Mazanec,

Mladineo

et al. 2024

Parasites Vectors

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Background Helminth extracellular vesicles (EVs) are known to have a three-way communication function among parasitic helminths, their host and the host-associated microbiota. They are considered biological containers that may carry virulence factors, being therefore appealing as therapeutic and prophylactic target candidates. This study aims to describe and characterise EVs secreted by Sparicotyle chrysophrii (Polyopisthocotyla: Microcotylidae), a blood-feeding gill parasite of gilthead seabream (Sparus aurata), causing significant economic losses in Mediterranean aquaculture. Methods To identify proteins involved in extracellular vesicle biogenesis, genomic datasets from S. chrysophrii were mined in silico using known protein sequences from Clonorchis spp., Echinococcus spp., Fasciola spp., Fasciolopsis spp., Opisthorchis spp., Paragonimus spp. and Schistosoma spp. The location and ultrastructure of EVs were visualised by transmission electron microscopy after fixing adult S. chrysophrii specimens by high-pressure freezing and freeze substitution. EVs were isolated and purified from adult S. chrysophrii (n = 200) using a newly developed ultracentrifugation-size-exclusion chromatography protocol for Polyopisthocotyla, and EVs were characterised via nanoparticle tracking analysis and tandem mass spectrometry. Results Fifty-nine proteins involved in EV biogenesis were identified in S. chrysophrii, and EVs compatible with ectosomes were observed in the syncytial layer of the haptoral region lining the clamps. The isolated and purified nanoparticles had a mean size of 251.8 nm and yielded 1.71 × 108 particles · mL−1. The protein composition analysis identified proteins related to peptide hydrolases, GTPases, EF-hand domain proteins, aerobic energy metabolism, anticoagulant/lipid-binding, haem detoxification, iron transport, EV biogenesis-related, vesicle-trafficking and other cytoskeletal-related proteins. Several identified proteins, such as leucyl and alanyl aminopeptidases, calpain, ferritin, dynein light chain, 14–3–3, heat shock protein 70, annexin, tubulin, glutathione S-transferase, superoxide dismutase, enolase and fructose-bisphosphate aldolase, have already been proposed as target candidates for therapeutic or prophylactic purposes. Conclusions We have unambiguously demonstrated for the first time to our knowledge the secretion of EVs by an ectoparasitic flatworm, inferring their biogenesis machinery at a genomic and transcriptomic level, and by identifying their location and protein composition. The identification of multiple therapeutic targets among EVs' protein repertoire provides opportunities for target-based drug discovery and vaccine development for the first time in Polyopisthocotyla (sensu Monogenea), and in a fish-ectoparasite model. Graphical Abstract

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Section: Discussionmentioning

confidence: 99%

An inside out journey: biogenesis, ultrastructure and proteomic characterisation of the ectoparasitic flatworm Sparicotyle chrysophrii extracellular vesicles

Riera-Ferrer,

Mazanec,

Mladineo

et al. 2024

Parasites Vectors

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“…Unlike other proteins involved in the haem synthesis cascade, gene-encoding 5aminolevulinic acid synthase (ALAS) is not present in this genome assembly. Among functionally important molecules in the E. nipponicum biology, we have observed four proteins of metalloprotease endothelin-converting enzyme 1 (ECE1, M13 family), which is a highly expressed transcript in immature S. mansoni eggs [70]. ECE1 participates in the disruption of blood vessel wall and helps the eggs penetrate into the intestine and be excreted out of the host body [71].…”

Section: Discussionmentioning

confidence: 99%

An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio

Vorel

Kmentová

Hahn

et al. 2023

Preprint

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Background Monogenea (Platyhelminthes, Neodermata) are the most species-rich class within the Neodermata superclass of primarily fish parasites. Despite their economic and ecological importance, monogenean research tends to focus on their morphological, phylogenetic, and population characteristics, while comprehensive omics analyses aimed at describing functionally important molecules are few and far between. We present a molecular characterisation of monogenean representative Eudiplozoon nipponicum, an obligate haematophagous parasite infecting the gills of the common carp. We report its nuclear and mitochondrial genomes, present a functional annotation of protein molecules relevant to the molecular and biochemical aspect of physiological processes involved in interactions with the fish hosts, and re-examinate the taxonomic position of Eudiplozoonspecies within the Diplozoidae family. Results We have generated 50.81 Gbp of raw sequencing data (Illumina and Oxford Nanopore reads), bioinformatically processed, and de novo assembled them into a genome draft 0.94 Gbp long, consisting of 21,044 contigs (N50 = 87 kbp). The final assembly represents 57% of the estimated total genome size (~1.64 Gbp), whereby repetitive and low-complexity regions account for ~64% of the assembled length. In total, 36,626 predicted genes encode 33,031 protein-coding transcripts. Homology-based annotation of transcripts and proteins characterises 14,785 (44.76%) molecules. We have detected significant representation of functional proteins and known molecular functions. The numbers of peptidases and inhibitors (579 proteins), characterised GO terms (16,016 unique assigned GO terms), and identified KEGG Orthology (4,315 proteins) acting in 378 KEGG pathways demonstrate the variety of mechanisms by which the parasite interacts with hosts on a macromolecular level (immunomodulation, feeding, and development). Comparison between the newly assembled E. nipponicum mitochondrial genome (length of 17,038 bp) and other diplozoid monogeneans confirms the existence of two distinct Eudiplozoon species infecting different fish hosts: Cyprinus carpio and Carassiusspp. Conclusions Although the amount of sequencing data and characterised molecules of monogenean parasites has recently increased, a better insight into their molecular biology is needed. The E. nipponicum nuclear genome presented here, currently the largest described genome within parasitic helminths, represents a milestone in the study of monogeneans and their molecules but further omics research is needed to understand these parasites’ biological nature.

show abstract

“…Unlike other proteins involved in the haem synthesis cascade, gene-encoding 5-aminolevulinic acid synthase (ALAS) is not present in this genome assembly. Among functionally important molecules in the E. nipponicum biology, we have observed four proteins of metalloprotease endothelin-converting enzyme 1 (ECE1, M13 family), which is a highly expressed transcript in immature S. mansoni eggs [ 86 ]. ECE1 participates in the disruption of blood vessel wall and helps the eggs penetrate into the intestine and be excreted out of the host body [ 87 ].…”

Section: Discussionmentioning

confidence: 99%

An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio

et al. 2023

Self Cite

View full text Add to dashboard Cite

Background Monogenea (Platyhelminthes, Neodermata) are the most species-rich class within the Neodermata superclass of primarily fish parasites. Despite their economic and ecological importance, monogenean research tends to focus on their morphological, phylogenetic, and population characteristics, while comprehensive omics analyses aimed at describing functionally important molecules are few and far between. We present a molecular characterisation of monogenean representative Eudiplozoon nipponicum, an obligate haematophagous parasite infecting the gills of the common carp. We report its nuclear and mitochondrial genomes, present a functional annotation of protein molecules relevant to the molecular and biochemical aspect of physiological processes involved in interactions with the fish hosts, and re-examinate the taxonomic position of Eudiplozoon species within the Diplozoidae family. Results We have generated 50.81 Gbp of raw sequencing data (Illumina and Oxford Nanopore reads), bioinformatically processed, and de novo assembled them into a genome draft 0.94 Gbp long, consisting of 21,044 contigs (N50 = 87 kbp). The final assembly represents 57% of the estimated total genome size (~ 1.64 Gbp), whereby repetitive and low-complexity regions account for ~ 64% of the assembled length. In total, 36,626 predicted genes encode 33,031 proteins and homology-based annotation of protein-coding genes (PCGs) and proteins characterises 14,785 (44.76%) molecules. We have detected significant representation of functional proteins and known molecular functions. The numbers of peptidases and inhibitors (579 proteins), characterised GO terms (16,016 unique assigned GO terms), and identified KEGG Orthology (4,315 proteins) acting in 378 KEGG pathways demonstrate the variety of mechanisms by which the parasite interacts with hosts on a macromolecular level (immunomodulation, feeding, and development). Comparison between the newly assembled E. nipponicum mitochondrial genome (length of 17,038 bp) and other diplozoid monogeneans confirms the existence of two distinct Eudiplozoon species infecting different fish hosts: Cyprinus carpio and Carassius spp. Conclusions Although the amount of sequencing data and characterised molecules of monogenean parasites has recently increased, a better insight into their molecular biology is needed. The E. nipponicum nuclear genome presented here, currently the largest described genome of any monogenean parasite, represents a milestone in the study of monogeneans and their molecules but further omics research is needed to understand these parasites’ biological nature.

show abstract

Proteases and their inhibitors involved in Schistosoma mansoni egg-host interaction revealed by comparative transcriptomics with Fasciola hepatica eggs

Cited by 6 publications

References 63 publications

An inside out journey: biogenesis, ultrastructure and proteomic characterisation of the ectoparasitic flatworm Sparicotyle chrysophrii extracellular vesicles

An inside out journey: biogenesis, ultrastructure and proteomic characterisation of the ectoparasitic flatworm Sparicotyle chrysophrii extracellular vesicles

An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio

An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio

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