Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways

Parasitic nematodes cause significant morbidity and mortality globally. Excretory/secretory products (ESPs) such as fatty acid- and retinol- binding proteins (FARs) are hypothesized to suppress host immunity during nematode infection, yet little is known about their interactions with host tissues. L...

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Autores principales:	Sophia C. Parks, Susan Nguyen, Shyon Nasrolahi, Chaitra Bhat, Damian Juncaj, Dihong Lu, Raghavendran Ramaswamy, Harpal Dhillon, Hideji Fujiwara, Anna Buchman, Omar S. Akbari, Naoki Yamanaka, Martin J. Boulanger, Adler R. Dillman
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/7f9dfce116564f459e99b8e22eb3390e
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spelling	oai:doaj.org-article:7f9dfce116564f459e99b8e22eb3390e2021-11-18T06:01:31ZParasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways1553-73661553-7374https://doaj.org/article/7f9dfce116564f459e99b8e22eb3390e2021-10-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8580252/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Parasitic nematodes cause significant morbidity and mortality globally. Excretory/secretory products (ESPs) such as fatty acid- and retinol- binding proteins (FARs) are hypothesized to suppress host immunity during nematode infection, yet little is known about their interactions with host tissues. Leveraging the insect parasitic nematode, Steinernema carpocapsae, we describe here the first in vivo study demonstrating that FARs modulate animal immunity, causing an increase in susceptibility to bacterial co-infection. Moreover, we show that FARs dampen key components of the fly immune response including the phenoloxidase cascade and antimicrobial peptide (AMP) production. Our data also reveal that FARs deplete lipid signaling precursors in vivo as well as bind to these fatty acids in vitro, suggesting that FARs elicit their immunomodulatory effects by altering the availability of lipid signaling molecules necessary for an efficient immune response. Collectively, these data support a complex role for FARs in immunosuppression in animals and provide detailed mechanistic insight into parasitism in phylum Nematoda. Author summary A central aspect of parasitic nematode success is their ability to modify host biology, including evasion and/or subversion of host immunity. Modulation of host biology and the pathology caused by parasitic nematodes is largely effected through the release of proteins and small molecules. There are hundreds of proteins released by nematodes during an infection and few have been studied in detail. Fatty acid- and retinol-binding proteins (FARs) are a unique protein family, found only in nematodes and some bacteria, and are released during nematode infection. We report that nematode FARs from S. carpocapsae, C. elegans and A. ceylanicum dampen fly immunity decreasing resistance to infection. Mechanistically, this is achieved through modulation of the phenoloxidase cascade and antimicrobial peptide production. Furthermore, FARs alter the availability of lipid immune signaling precursors in vivo and show binding specificity in vitro.Sophia C. ParksSusan NguyenShyon NasrolahiChaitra BhatDamian JuncajDihong LuRaghavendran RamaswamyHarpal DhillonHideji FujiwaraAnna BuchmanOmar S. AkbariNaoki YamanakaMartin J. BoulangerAdler R. DillmanPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 17, Iss 10 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Sophia C. Parks Susan Nguyen Shyon Nasrolahi Chaitra Bhat Damian Juncaj Dihong Lu Raghavendran Ramaswamy Harpal Dhillon Hideji Fujiwara Anna Buchman Omar S. Akbari Naoki Yamanaka Martin J. Boulanger Adler R. Dillman Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways
description	Parasitic nematodes cause significant morbidity and mortality globally. Excretory/secretory products (ESPs) such as fatty acid- and retinol- binding proteins (FARs) are hypothesized to suppress host immunity during nematode infection, yet little is known about their interactions with host tissues. Leveraging the insect parasitic nematode, Steinernema carpocapsae, we describe here the first in vivo study demonstrating that FARs modulate animal immunity, causing an increase in susceptibility to bacterial co-infection. Moreover, we show that FARs dampen key components of the fly immune response including the phenoloxidase cascade and antimicrobial peptide (AMP) production. Our data also reveal that FARs deplete lipid signaling precursors in vivo as well as bind to these fatty acids in vitro, suggesting that FARs elicit their immunomodulatory effects by altering the availability of lipid signaling molecules necessary for an efficient immune response. Collectively, these data support a complex role for FARs in immunosuppression in animals and provide detailed mechanistic insight into parasitism in phylum Nematoda. Author summary A central aspect of parasitic nematode success is their ability to modify host biology, including evasion and/or subversion of host immunity. Modulation of host biology and the pathology caused by parasitic nematodes is largely effected through the release of proteins and small molecules. There are hundreds of proteins released by nematodes during an infection and few have been studied in detail. Fatty acid- and retinol-binding proteins (FARs) are a unique protein family, found only in nematodes and some bacteria, and are released during nematode infection. We report that nematode FARs from S. carpocapsae, C. elegans and A. ceylanicum dampen fly immunity decreasing resistance to infection. Mechanistically, this is achieved through modulation of the phenoloxidase cascade and antimicrobial peptide production. Furthermore, FARs alter the availability of lipid immune signaling precursors in vivo and show binding specificity in vitro.
format	article
author	Sophia C. Parks Susan Nguyen Shyon Nasrolahi Chaitra Bhat Damian Juncaj Dihong Lu Raghavendran Ramaswamy Harpal Dhillon Hideji Fujiwara Anna Buchman Omar S. Akbari Naoki Yamanaka Martin J. Boulanger Adler R. Dillman
author_facet	Sophia C. Parks Susan Nguyen Shyon Nasrolahi Chaitra Bhat Damian Juncaj Dihong Lu Raghavendran Ramaswamy Harpal Dhillon Hideji Fujiwara Anna Buchman Omar S. Akbari Naoki Yamanaka Martin J. Boulanger Adler R. Dillman
author_sort	Sophia C. Parks
title	Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways
title_short	Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways
title_full	Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways
title_fullStr	Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways
title_full_unstemmed	Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways
title_sort	parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/7f9dfce116564f459e99b8e22eb3390e
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Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways

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