An invertebrate-specific miRNA targeted the ancient cholinergic neuroendocrine system of oyster

Acetylcholine (ACh) is the main neurotransmitter in the cholinergic neuroendocrine system and plays an indispensable role in modulating diverse immune responses. As important transporters in choline uptake, choline transporter-like proteins (CTLs) can control ACh synthesis and release indirectly in...

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Main Authors: Hao Chen, Zhi Zhou, Lingling Wang, Hao Wang, Rui Liu, Huan Zhang, Linsheng Song
Format: Article
Language:English
Published: The Royal Society 2016-01-01
Series:Open Biology
Subjects:
Online Access:https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.160059
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spelling doaj-9ed0e860945141029f01e919ec4e08ab2020-11-25T04:00:23ZengThe Royal SocietyOpen Biology2046-24412016-01-016810.1098/rsob.160059160059An invertebrate-specific miRNA targeted the ancient cholinergic neuroendocrine system of oysterHao ChenZhi ZhouLingling WangHao WangRui LiuHuan ZhangLinsheng SongAcetylcholine (ACh) is the main neurotransmitter in the cholinergic neuroendocrine system and plays an indispensable role in modulating diverse immune responses. As important transporters in choline uptake, choline transporter-like proteins (CTLs) can control ACh synthesis and release indirectly in multiple organisms. In this study, cgi-miR-2d, an invertebrate-specific miRNA in oyster Crassostrea gigas, is proved to repress the synthesis/release of ACh by targeting CgCTL1 and choline uptake in haemocytes during the early stage of pathogen infection. In short, an opposite expression pattern between CgCTL1 and cgi-miR-2d is observed during Vibrio splendidus infection, accompanied by changes in haemolymph ACh. In addition, the expression level of CgCTL1 is found to be significantly repressed after cgi-miR-2d overexpression in vivo, while both haemocyte choline and haemolymph ACh are also decreased simultaneously, similar to the finding in CgCTL1 knock-down assay. As a result, the expression of two tumour necrosis factor-like proteins and the bacteriostatic activity of oyster haemocytes are found to be altered significantly by either gain-of-function cgi-miR-2d or knock-down of CgCTL1. To our knowledge, this is the first miRNA identified in invertebrates that can target the ancient cholinergic system and augment immune response during infection.https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.160059mirnamir-2 familycholine transporter-like proteinacetylcholinecholinergic systemimmunomodulation
collection DOAJ
language English
format Article
sources DOAJ
author Hao Chen
Zhi Zhou
Lingling Wang
Hao Wang
Rui Liu
Huan Zhang
Linsheng Song
spellingShingle Hao Chen
Zhi Zhou
Lingling Wang
Hao Wang
Rui Liu
Huan Zhang
Linsheng Song
An invertebrate-specific miRNA targeted the ancient cholinergic neuroendocrine system of oyster
Open Biology
mirna
mir-2 family
choline transporter-like protein
acetylcholine
cholinergic system
immunomodulation
author_facet Hao Chen
Zhi Zhou
Lingling Wang
Hao Wang
Rui Liu
Huan Zhang
Linsheng Song
author_sort Hao Chen
title An invertebrate-specific miRNA targeted the ancient cholinergic neuroendocrine system of oyster
title_short An invertebrate-specific miRNA targeted the ancient cholinergic neuroendocrine system of oyster
title_full An invertebrate-specific miRNA targeted the ancient cholinergic neuroendocrine system of oyster
title_fullStr An invertebrate-specific miRNA targeted the ancient cholinergic neuroendocrine system of oyster
title_full_unstemmed An invertebrate-specific miRNA targeted the ancient cholinergic neuroendocrine system of oyster
title_sort invertebrate-specific mirna targeted the ancient cholinergic neuroendocrine system of oyster
publisher The Royal Society
series Open Biology
issn 2046-2441
publishDate 2016-01-01
description Acetylcholine (ACh) is the main neurotransmitter in the cholinergic neuroendocrine system and plays an indispensable role in modulating diverse immune responses. As important transporters in choline uptake, choline transporter-like proteins (CTLs) can control ACh synthesis and release indirectly in multiple organisms. In this study, cgi-miR-2d, an invertebrate-specific miRNA in oyster Crassostrea gigas, is proved to repress the synthesis/release of ACh by targeting CgCTL1 and choline uptake in haemocytes during the early stage of pathogen infection. In short, an opposite expression pattern between CgCTL1 and cgi-miR-2d is observed during Vibrio splendidus infection, accompanied by changes in haemolymph ACh. In addition, the expression level of CgCTL1 is found to be significantly repressed after cgi-miR-2d overexpression in vivo, while both haemocyte choline and haemolymph ACh are also decreased simultaneously, similar to the finding in CgCTL1 knock-down assay. As a result, the expression of two tumour necrosis factor-like proteins and the bacteriostatic activity of oyster haemocytes are found to be altered significantly by either gain-of-function cgi-miR-2d or knock-down of CgCTL1. To our knowledge, this is the first miRNA identified in invertebrates that can target the ancient cholinergic system and augment immune response during infection.
topic mirna
mir-2 family
choline transporter-like protein
acetylcholine
cholinergic system
immunomodulation
url https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.160059
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