Nb-FAR-1: A key developmental protein affects lipid droplet accumulation and cuticle formation in Nippostrongylus brasiliensis.

Fatty acid and retinol binding proteins (FARs) are lipid-binding protein that may be associated with modulating nematode pathogenicity to their hosts. However, the functional mechanism of FARs remains elusive. We attempt to study the function of a certain FAR that may be important in the development...

Full description

Saved in:
Bibliographic Details
Main Authors: Wenmin Qi, Fei Shen, Chuyue Wang, Juan Wen, Xi Pan, Zhongying Zhao, Lihua Xiao, Yaoyu Feng, Dongjuan Yuan
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS Neglected Tropical Diseases
Online Access:https://doi.org/10.1371/journal.pntd.0012769
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832540002543730688
author Wenmin Qi
Fei Shen
Chuyue Wang
Juan Wen
Xi Pan
Zhongying Zhao
Lihua Xiao
Yaoyu Feng
Dongjuan Yuan
author_facet Wenmin Qi
Fei Shen
Chuyue Wang
Juan Wen
Xi Pan
Zhongying Zhao
Lihua Xiao
Yaoyu Feng
Dongjuan Yuan
author_sort Wenmin Qi
collection DOAJ
description Fatty acid and retinol binding proteins (FARs) are lipid-binding protein that may be associated with modulating nematode pathogenicity to their hosts. However, the functional mechanism of FARs remains elusive. We attempt to study the function of a certain FAR that may be important in the development of Nippostrongylus brasiliensis. Nb-FAR-1 was highly expressed throughout developmental stages by RNA-seq data and qPCR analyses, and Nb-FAR-1 was a secretory protein and abundant in the excretory-secretory products. Nb-FAR-1 could bind fatty acids and retinol. Fatty acid pattern of parasitic adults was more similar to rat intestine than to free-living L3s, indicating that N. brasiliensis may be dependent on the host to obtain fatty acids. Lentivirus-mediated RNAi was performed on L3s, resulting in a reduction in the expression of Nb-far-1 gene. Furthermore, these RNAi effects could be maintained in several generations. The offspring L3s in Nb-far-1 RNAi group had a reduction in lipid droplets within the subcuticle and the swelling of the perioral epidermis, accompanied with down-regulated expression of enzymes in amino acid and glycerolipid metabolism and glycometabolism for growth by RNA-seq data. Adults in Nb-far-1 RNAi group had the crumpled epidermis loosely attached to the basal membrane of body surface and the breakage of mouth epidermis, accompanied with a decrease in adult egg-shedding and an appearance of abnormal eggs. In vitro culture of eggs showed decreased efficiency of egg hatchability and larval development in the Nb-far-1 RNAi group. Transcriptomic analysis showed that interference with Nb-far-1 expression induced downregulated expression of major sperm protein and serpin for reproduction, and collagen for epidermis formation in adults, most of which were relatively high expression in adults but low expression in L3s in the WT group. Thus, Nb-FAR-1 may affect the reproduction, growth, and development of N. brasiliensis by regulating the level of lipids.
format Article
id doaj-art-dcaafa7ab949419b948a4b8f11394dec
institution Kabale University
issn 1935-2727
1935-2735
language English
publishDate 2025-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Neglected Tropical Diseases
spelling doaj-art-dcaafa7ab949419b948a4b8f11394dec2025-02-05T05:33:27ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352025-01-01191e001276910.1371/journal.pntd.0012769Nb-FAR-1: A key developmental protein affects lipid droplet accumulation and cuticle formation in Nippostrongylus brasiliensis.Wenmin QiFei ShenChuyue WangJuan WenXi PanZhongying ZhaoLihua XiaoYaoyu FengDongjuan YuanFatty acid and retinol binding proteins (FARs) are lipid-binding protein that may be associated with modulating nematode pathogenicity to their hosts. However, the functional mechanism of FARs remains elusive. We attempt to study the function of a certain FAR that may be important in the development of Nippostrongylus brasiliensis. Nb-FAR-1 was highly expressed throughout developmental stages by RNA-seq data and qPCR analyses, and Nb-FAR-1 was a secretory protein and abundant in the excretory-secretory products. Nb-FAR-1 could bind fatty acids and retinol. Fatty acid pattern of parasitic adults was more similar to rat intestine than to free-living L3s, indicating that N. brasiliensis may be dependent on the host to obtain fatty acids. Lentivirus-mediated RNAi was performed on L3s, resulting in a reduction in the expression of Nb-far-1 gene. Furthermore, these RNAi effects could be maintained in several generations. The offspring L3s in Nb-far-1 RNAi group had a reduction in lipid droplets within the subcuticle and the swelling of the perioral epidermis, accompanied with down-regulated expression of enzymes in amino acid and glycerolipid metabolism and glycometabolism for growth by RNA-seq data. Adults in Nb-far-1 RNAi group had the crumpled epidermis loosely attached to the basal membrane of body surface and the breakage of mouth epidermis, accompanied with a decrease in adult egg-shedding and an appearance of abnormal eggs. In vitro culture of eggs showed decreased efficiency of egg hatchability and larval development in the Nb-far-1 RNAi group. Transcriptomic analysis showed that interference with Nb-far-1 expression induced downregulated expression of major sperm protein and serpin for reproduction, and collagen for epidermis formation in adults, most of which were relatively high expression in adults but low expression in L3s in the WT group. Thus, Nb-FAR-1 may affect the reproduction, growth, and development of N. brasiliensis by regulating the level of lipids.https://doi.org/10.1371/journal.pntd.0012769
spellingShingle Wenmin Qi
Fei Shen
Chuyue Wang
Juan Wen
Xi Pan
Zhongying Zhao
Lihua Xiao
Yaoyu Feng
Dongjuan Yuan
Nb-FAR-1: A key developmental protein affects lipid droplet accumulation and cuticle formation in Nippostrongylus brasiliensis.
PLoS Neglected Tropical Diseases
title Nb-FAR-1: A key developmental protein affects lipid droplet accumulation and cuticle formation in Nippostrongylus brasiliensis.
title_full Nb-FAR-1: A key developmental protein affects lipid droplet accumulation and cuticle formation in Nippostrongylus brasiliensis.
title_fullStr Nb-FAR-1: A key developmental protein affects lipid droplet accumulation and cuticle formation in Nippostrongylus brasiliensis.
title_full_unstemmed Nb-FAR-1: A key developmental protein affects lipid droplet accumulation and cuticle formation in Nippostrongylus brasiliensis.
title_short Nb-FAR-1: A key developmental protein affects lipid droplet accumulation and cuticle formation in Nippostrongylus brasiliensis.
title_sort nb far 1 a key developmental protein affects lipid droplet accumulation and cuticle formation in nippostrongylus brasiliensis
url https://doi.org/10.1371/journal.pntd.0012769
work_keys_str_mv AT wenminqi nbfar1akeydevelopmentalproteinaffectslipiddropletaccumulationandcuticleformationinnippostrongylusbrasiliensis
AT feishen nbfar1akeydevelopmentalproteinaffectslipiddropletaccumulationandcuticleformationinnippostrongylusbrasiliensis
AT chuyuewang nbfar1akeydevelopmentalproteinaffectslipiddropletaccumulationandcuticleformationinnippostrongylusbrasiliensis
AT juanwen nbfar1akeydevelopmentalproteinaffectslipiddropletaccumulationandcuticleformationinnippostrongylusbrasiliensis
AT xipan nbfar1akeydevelopmentalproteinaffectslipiddropletaccumulationandcuticleformationinnippostrongylusbrasiliensis
AT zhongyingzhao nbfar1akeydevelopmentalproteinaffectslipiddropletaccumulationandcuticleformationinnippostrongylusbrasiliensis
AT lihuaxiao nbfar1akeydevelopmentalproteinaffectslipiddropletaccumulationandcuticleformationinnippostrongylusbrasiliensis
AT yaoyufeng nbfar1akeydevelopmentalproteinaffectslipiddropletaccumulationandcuticleformationinnippostrongylusbrasiliensis
AT dongjuanyuan nbfar1akeydevelopmentalproteinaffectslipiddropletaccumulationandcuticleformationinnippostrongylusbrasiliensis