Evidence of Immune Modulators in the Secretome of the Equine Tapeworm Anoplocephala perfoliata

Boontarikaan Wititkornkul; Benjamin J. Hulme; John J. Tomes; Nathan R. Allen; Chelsea N. Davis; Sarah D. Davey; Alan R. Cookson; Helen C. Phillips; Matthew J. Hegarty; Martin T. Swain; Peter M. Brophy; Ruth E. Wonfor; Russell M. Morphew

doi:10.3390/pathogens10070912

Evidence of Immune Modulators in the Secretome of the Equine Tapeworm Anoplocephala perfoliata

Boontarikaan Wititkornkul, Benjamin J. Hulme, John J. Tomes, Nathan R. Allen, Chelsea N. Davis, Sarah D. Davey, Alan R. Cookson, Helen C. Phillips, Matthew J. Hegarty, Martin T. Swain, Peter M. Brophy, Ruth E. Wonfor^*, Russell M. Morphew^*

^*Corresponding author for this work

Department of Life Sciences

Rajamangala University of Technology, Srivijaya

Research output: Contribution to journal › Article › peer-review

9 Citations (Scopus)

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Abstract

Anoplocephala perfoliata is a neglected gastro-intestinal tapeworm, commonly infecting horses worldwide. Molecular investigation of A. perfoliata is hampered by a lack of tools to better understand the host–parasite interface. This interface is likely influenced by parasite derived immune modulators released in the secretome as free proteins or components of extracellular vesicles (EVs). Therefore, adult RNA was sequenced and de novo assembled to generate the first A. perfoliata transcriptome. In addition, excretory secretory products (ESP) from adult A. perfoliata were collected and EVs isolated using size exclusion chromatography, prior to proteomic analysis of the EVs, the EV surface and EV depleted ESP. Transcriptome analysis revealed 454 sequences homologous to known helminth immune modulators including two novel Sigma class GSTs, five α-HSP90s, and three α-enolases with isoforms of all three observed within the proteomic analysis of the secretome. Furthermore, secretome proteomics identified common helminth proteins across each sample with known EV markers, such as annexins and tetraspanins, observed in EV fractions. Importantly, 49 of the 454 putative immune modulators were identified across the secretome proteomics contained within and on the surface of EVs in addition to those identified in free ESP. This work provides the molecular tools for A. perfoliata to reveal key players in the host–parasite interaction within the horse host.

Original language	English
Article number	e912
Number of pages	30
Journal	Pathogens
Volume	10
Issue number	7
DOIs	https://doi.org/10.3390/pathogens10070912
Publication status	Published - 20 Jul 2021

Keywords

Anoplocephala perfoliata
EV depleted ESP
EV surface
Extracellular vesicles
Parasite–host interaction
Secretome
Transcriptome

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Wititkornkul, B., Hulme, B. J., Tomes, J. J., Allen, N. R., Davis, C. N., Davey, S. D., Cookson, A. R., Phillips, H. C., Hegarty, M. J., Swain, M. T., Brophy, P. M., Wonfor, R. E., & Morphew, R. M. (2021). Evidence of Immune Modulators in the Secretome of the Equine Tapeworm Anoplocephala perfoliata. Pathogens, 10(7), Article e912. https://doi.org/10.3390/pathogens10070912

@article{84c2adb459d948dbab131deb85b76652,

title = "Evidence of Immune Modulators in the Secretome of the Equine Tapeworm Anoplocephala perfoliata",

abstract = "Anoplocephala perfoliata is a neglected gastro-intestinal tapeworm, commonly infecting horses worldwide. Molecular investigation of A. perfoliata is hampered by a lack of tools to better understand the host–parasite interface. This interface is likely influenced by parasite derived immune modulators released in the secretome as free proteins or components of extracellular vesicles (EVs). Therefore, adult RNA was sequenced and de novo assembled to generate the first A. perfoliata transcriptome. In addition, excretory secretory products (ESP) from adult A. perfoliata were collected and EVs isolated using size exclusion chromatography, prior to proteomic analysis of the EVs, the EV surface and EV depleted ESP. Transcriptome analysis revealed 454 sequences homologous to known helminth immune modulators including two novel Sigma class GSTs, five α-HSP90s, and three α-enolases with isoforms of all three observed within the proteomic analysis of the secretome. Furthermore, secretome proteomics identified common helminth proteins across each sample with known EV markers, such as annexins and tetraspanins, observed in EV fractions. Importantly, 49 of the 454 putative immune modulators were identified across the secretome proteomics contained within and on the surface of EVs in addition to those identified in free ESP. This work provides the molecular tools for A. perfoliata to reveal key players in the host–parasite interaction within the horse host.",

keywords = "Anoplocephala perfoliata, EV depleted ESP, EV surface, Extracellular vesicles, Parasite–host interaction, Secretome, Transcriptome",

author = "Boontarikaan Wititkornkul and Hulme, {Benjamin J.} and Tomes, {John J.} and Allen, {Nathan R.} and Davis, {Chelsea N.} and Davey, {Sarah D.} and Cookson, {Alan R.} and Phillips, {Helen C.} and Hegarty, {Matthew J.} and Swain, {Martin T.} and Brophy, {Peter M.} and Wonfor, {Ruth E.} and Morphew, {Russell M.}",

note = "Funding Information: Funding: This research was funded by Rajamangala University of Technology Srivijaya, Thailand. The Institute of Biology, Environmental and Rural Sciences (Aberystwyth University, Wales) receives strategic funding from Biotechnology and Biological Sciences Research that also supported the current work. Publisher Copyright: {\textcopyright} 2021 by the authors. Licensee MDPI, Basel, Switzerland.",

year = "2021",

month = jul,

day = "20",

doi = "10.3390/pathogens10070912",

language = "English",

volume = "10",

journal = "Pathogens",

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AU - Wititkornkul, Boontarikaan

AU - Hulme, Benjamin J.

AU - Tomes, John J.

AU - Allen, Nathan R.

AU - Davis, Chelsea N.

AU - Davey, Sarah D.

AU - Cookson, Alan R.

AU - Phillips, Helen C.

AU - Hegarty, Matthew J.

AU - Swain, Martin T.

AU - Brophy, Peter M.

AU - Wonfor, Ruth E.

AU - Morphew, Russell M.

N1 - Funding Information: Funding: This research was funded by Rajamangala University of Technology Srivijaya, Thailand. The Institute of Biology, Environmental and Rural Sciences (Aberystwyth University, Wales) receives strategic funding from Biotechnology and Biological Sciences Research that also supported the current work. Publisher Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland.

PY - 2021/7/20

Y1 - 2021/7/20

N2 - Anoplocephala perfoliata is a neglected gastro-intestinal tapeworm, commonly infecting horses worldwide. Molecular investigation of A. perfoliata is hampered by a lack of tools to better understand the host–parasite interface. This interface is likely influenced by parasite derived immune modulators released in the secretome as free proteins or components of extracellular vesicles (EVs). Therefore, adult RNA was sequenced and de novo assembled to generate the first A. perfoliata transcriptome. In addition, excretory secretory products (ESP) from adult A. perfoliata were collected and EVs isolated using size exclusion chromatography, prior to proteomic analysis of the EVs, the EV surface and EV depleted ESP. Transcriptome analysis revealed 454 sequences homologous to known helminth immune modulators including two novel Sigma class GSTs, five α-HSP90s, and three α-enolases with isoforms of all three observed within the proteomic analysis of the secretome. Furthermore, secretome proteomics identified common helminth proteins across each sample with known EV markers, such as annexins and tetraspanins, observed in EV fractions. Importantly, 49 of the 454 putative immune modulators were identified across the secretome proteomics contained within and on the surface of EVs in addition to those identified in free ESP. This work provides the molecular tools for A. perfoliata to reveal key players in the host–parasite interaction within the horse host.

AB - Anoplocephala perfoliata is a neglected gastro-intestinal tapeworm, commonly infecting horses worldwide. Molecular investigation of A. perfoliata is hampered by a lack of tools to better understand the host–parasite interface. This interface is likely influenced by parasite derived immune modulators released in the secretome as free proteins or components of extracellular vesicles (EVs). Therefore, adult RNA was sequenced and de novo assembled to generate the first A. perfoliata transcriptome. In addition, excretory secretory products (ESP) from adult A. perfoliata were collected and EVs isolated using size exclusion chromatography, prior to proteomic analysis of the EVs, the EV surface and EV depleted ESP. Transcriptome analysis revealed 454 sequences homologous to known helminth immune modulators including two novel Sigma class GSTs, five α-HSP90s, and three α-enolases with isoforms of all three observed within the proteomic analysis of the secretome. Furthermore, secretome proteomics identified common helminth proteins across each sample with known EV markers, such as annexins and tetraspanins, observed in EV fractions. Importantly, 49 of the 454 putative immune modulators were identified across the secretome proteomics contained within and on the surface of EVs in addition to those identified in free ESP. This work provides the molecular tools for A. perfoliata to reveal key players in the host–parasite interaction within the horse host.

KW - Anoplocephala perfoliata

KW - EV depleted ESP

KW - EV surface

KW - Extracellular vesicles

KW - Parasite–host interaction

KW - Secretome

KW - Transcriptome

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U2 - 10.3390/pathogens10070912

DO - 10.3390/pathogens10070912

M3 - Article

C2 - 34358062

SN - 2076-0817

VL - 10

JO - Pathogens

JF - Pathogens

IS - 7

M1 - e912

ER -

Evidence of Immune Modulators in the Secretome of the Equine Tapeworm Anoplocephala perfoliata

Abstract

Keywords

UN SDGs

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