Lineage/species-specific expansion of the Mx gene family in teleosts: Differential expression and modulation of nine Mx genes in rainbow trout Oncorhynchus mykiss

Tingyu Wang; Fuguo Liu; Guangming Tian; Christopher J. Secombes; Tiehui Wang

doi:10.1016/j.fsi.2019.04.303

Lineage/species-specific expansion of the Mx gene family in teleosts: Differential expression and modulation of nine Mx genes in rainbow trout Oncorhynchus mykiss

Tingyu Wang, Fuguo Liu, Guangming Tian, Christopher J. Secombes^* (Corresponding Author), Tiehui Wang^* (Corresponding Author)

^*Corresponding author for this work

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

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Abstract

Myxovirus resistance (Mx) proteins are interferon (IFN)-inducible Dynamin-like GTPases, which play an important role in antiviral immunity. Three Mx genes (Mx1-3) have been cloned previously in rainbow trout. In this study, an additional six Mx genes were cloned that reside in four chromosomal loci. Further bioinformatics analysis suggests the presence of three teleost Mx groups (TMG) each with a characteristic gene organisation. Salmonid Mx belong to TMG1 and TMG2. The increased salmonid Mx gene copies are due mainly to local gene duplications that happened before and after salmonid speciation, in a lineage/species specific manner. Trout Mx molecules have been diversified in the loop 1 and 4 regions, and in the nuclear localisation signal in loop 4. The trout Mx genes were shown to be differentially expressed in tissues, with high levels of expression of TMG1 (Mx1-4) in blood and TMG2 (Mx5-9) in intestine. The expression of the majority of the trout Mx genes was induced by poly IC in vitro and in vivo, and increased during development. In addition, induction by antiviral (IFN) and proinflammatory cytokines was studied, and showed that type I IFN, IFNγ and IL-1β can induce Mx gene expression in an Mx gene-, cytokine- and cell line-dependent manner. These results show that salmonids possess a large number Mx genes as well as complex regulatory pathways, which may contribute to their success in an anadromous life style.

Original language	English
Pages (from-to)	413-430
Number of pages	18
Journal	Fish & Shellfish Immunology
Volume	90
Early online date	4 May 2019
DOIs	https://doi.org/10.1016/j.fsi.2019.04.303
Publication status	Published - 1 Jul 2019

Bibliographical note

This work was partially funded by the Biotechnology and Biological Sciences Research Council (BBSRC, BB/R008442/1). Tingyu Wang was supported by the Ministry of Science and Technology, Republic of China (Taiwan) (MOST 107-2917-I-564-019). Fuguo Liu was supported by a Newton International Fellowship funded by the Academy of Medical Sciences, UK (AMS, NIF004\1036). Guangming Tian was supported financially by the State Scholarship Fund organised by the China Scholarship Council (201808420042).

Keywords

Rainbow trout
Mx
Anti-viral defence
Evolution
Gene expression
Modulation
Type I interferon
IFNγ
IL-1β

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@article{e6730295c82f4f07a5631a8bdcd6110f,

title = "Lineage/species-specific expansion of the Mx gene family in teleosts: Differential expression and modulation of nine Mx genes in rainbow trout Oncorhynchus mykiss",

abstract = "Myxovirus resistance (Mx) proteins are interferon (IFN)-inducible Dynamin-like GTPases, which play an important role in antiviral immunity. Three Mx genes (Mx1-3) have been cloned previously in rainbow trout. In this study, an additional six Mx genes were cloned that reside in four chromosomal loci. Further bioinformatics analysis suggests the presence of three teleost Mx groups (TMG) each with a characteristic gene organisation. Salmonid Mx belong to TMG1 and TMG2. The increased salmonid Mx gene copies are due mainly to local gene duplications that happened before and after salmonid speciation, in a lineage/species specific manner. Trout Mx molecules have been diversified in the loop 1 and 4 regions, and in the nuclear localisation signal in loop 4. The trout Mx genes were shown to be differentially expressed in tissues, with high levels of expression of TMG1 (Mx1-4) in blood and TMG2 (Mx5-9) in intestine. The expression of the majority of the trout Mx genes was induced by poly IC in vitro and in vivo, and increased during development. In addition, induction by antiviral (IFN) and proinflammatory cytokines was studied, and showed that type I IFN, IFNγ and IL-1β can induce Mx gene expression in an Mx gene-, cytokine- and cell line-dependent manner. These results show that salmonids possess a large number Mx genes as well as complex regulatory pathways, which may contribute to their success in an anadromous life style.",

keywords = "Rainbow trout, Mx, Anti-viral defence, Evolution, Gene expression, Modulation, Type I interferon, IFNγ, IL-1β",

author = "Tingyu Wang and Fuguo Liu and Guangming Tian and Secombes, {Christopher J.} and Tiehui Wang",

note = "This work was partially funded by the Biotechnology and Biological Sciences Research Council (BBSRC, BB/R008442/1). Tingyu Wang was supported by the Ministry of Science and Technology, Republic of China (Taiwan) (MOST 107-2917-I-564-019). Fuguo Liu was supported by a Newton International Fellowship funded by the Academy of Medical Sciences, UK (AMS, NIF004\1036). Guangming Tian was supported financially by the State Scholarship Fund organised by the China Scholarship Council (201808420042).",

year = "2019",

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doi = "10.1016/j.fsi.2019.04.303",

language = "English",

volume = "90",

pages = "413--430",

journal = "Fish & Shellfish Immunology",

issn = "1050-4648",

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T1 - Lineage/species-specific expansion of the Mx gene family in teleosts

T2 - Differential expression and modulation of nine Mx genes in rainbow trout Oncorhynchus mykiss

AU - Wang, Tingyu

AU - Liu, Fuguo

AU - Tian, Guangming

AU - Secombes, Christopher J.

AU - Wang, Tiehui

N1 - This work was partially funded by the Biotechnology and Biological Sciences Research Council (BBSRC, BB/R008442/1). Tingyu Wang was supported by the Ministry of Science and Technology, Republic of China (Taiwan) (MOST 107-2917-I-564-019). Fuguo Liu was supported by a Newton International Fellowship funded by the Academy of Medical Sciences, UK (AMS, NIF004\1036). Guangming Tian was supported financially by the State Scholarship Fund organised by the China Scholarship Council (201808420042).

PY - 2019/7/1

Y1 - 2019/7/1

N2 - Myxovirus resistance (Mx) proteins are interferon (IFN)-inducible Dynamin-like GTPases, which play an important role in antiviral immunity. Three Mx genes (Mx1-3) have been cloned previously in rainbow trout. In this study, an additional six Mx genes were cloned that reside in four chromosomal loci. Further bioinformatics analysis suggests the presence of three teleost Mx groups (TMG) each with a characteristic gene organisation. Salmonid Mx belong to TMG1 and TMG2. The increased salmonid Mx gene copies are due mainly to local gene duplications that happened before and after salmonid speciation, in a lineage/species specific manner. Trout Mx molecules have been diversified in the loop 1 and 4 regions, and in the nuclear localisation signal in loop 4. The trout Mx genes were shown to be differentially expressed in tissues, with high levels of expression of TMG1 (Mx1-4) in blood and TMG2 (Mx5-9) in intestine. The expression of the majority of the trout Mx genes was induced by poly IC in vitro and in vivo, and increased during development. In addition, induction by antiviral (IFN) and proinflammatory cytokines was studied, and showed that type I IFN, IFNγ and IL-1β can induce Mx gene expression in an Mx gene-, cytokine- and cell line-dependent manner. These results show that salmonids possess a large number Mx genes as well as complex regulatory pathways, which may contribute to their success in an anadromous life style.

AB - Myxovirus resistance (Mx) proteins are interferon (IFN)-inducible Dynamin-like GTPases, which play an important role in antiviral immunity. Three Mx genes (Mx1-3) have been cloned previously in rainbow trout. In this study, an additional six Mx genes were cloned that reside in four chromosomal loci. Further bioinformatics analysis suggests the presence of three teleost Mx groups (TMG) each with a characteristic gene organisation. Salmonid Mx belong to TMG1 and TMG2. The increased salmonid Mx gene copies are due mainly to local gene duplications that happened before and after salmonid speciation, in a lineage/species specific manner. Trout Mx molecules have been diversified in the loop 1 and 4 regions, and in the nuclear localisation signal in loop 4. The trout Mx genes were shown to be differentially expressed in tissues, with high levels of expression of TMG1 (Mx1-4) in blood and TMG2 (Mx5-9) in intestine. The expression of the majority of the trout Mx genes was induced by poly IC in vitro and in vivo, and increased during development. In addition, induction by antiviral (IFN) and proinflammatory cytokines was studied, and showed that type I IFN, IFNγ and IL-1β can induce Mx gene expression in an Mx gene-, cytokine- and cell line-dependent manner. These results show that salmonids possess a large number Mx genes as well as complex regulatory pathways, which may contribute to their success in an anadromous life style.

KW - Rainbow trout

KW - Mx

KW - Anti-viral defence

KW - Evolution

KW - Gene expression

KW - Modulation

KW - Type I interferon

KW - IFNγ

KW - IL-1β

UR - http://www.mendeley.com/research/lineagespeciesspecific-expansion-mx-gene-family-teleosts-differential-expression-modulation-nine-mx

U2 - 10.1016/j.fsi.2019.04.303

DO - 10.1016/j.fsi.2019.04.303

M3 - Article

C2 - 31063803

SN - 1050-4648

VL - 90

SP - 413

EP - 430

JO - Fish & Shellfish Immunology

JF - Fish & Shellfish Immunology

ER -

Lineage/species-specific expansion of the Mx gene family in teleosts: Differential expression and modulation of nine Mx genes in rainbow trout Oncorhynchus mykiss

Abstract

Bibliographical note

Keywords

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