Two Duplicated Ptpn6 Homeologs Cooperatively and Negatively Regulate RLR-Mediated IFN Response in Hexaploid Gibel Carp

Src homology region 2 domain-containing phosphatase 1 (SHP1), encoded by the protein tyrosine phosphatase nonreceptor type 6 (ptpn6) gene, belongs to the family of protein tyrosine phosphatases (PTPs) and participates in multiple signaling pathways of immune cells. However, the mechanism of SHP1 in...

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Autores principales:	Jin-Feng Tong, Li Zhou, Shun Li, Long-Feng Lu, Zhuo-Cong Li, Zhi Li, Rui-Hai Gan, Cheng-Yan Mou, Qi-Ya Zhang, Zhong-Wei Wang, Xiao-Juan Zhang, Yang Wang, Jian-Fang Gui
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	Gibel carp SHP1 negative regulator autophagy MITA interferon Immunologic diseases. Allergy RC581-607
Acceso en línea:	https://doaj.org/article/c48623879e57447aaf7fb347b836bc28
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spelling	oai:doaj.org-article:c48623879e57447aaf7fb347b836bc282021-12-01T07:56:07ZTwo Duplicated Ptpn6 Homeologs Cooperatively and Negatively Regulate RLR-Mediated IFN Response in Hexaploid Gibel Carp1664-322410.3389/fimmu.2021.780667https://doaj.org/article/c48623879e57447aaf7fb347b836bc282021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fimmu.2021.780667/fullhttps://doaj.org/toc/1664-3224Src homology region 2 domain-containing phosphatase 1 (SHP1), encoded by the protein tyrosine phosphatase nonreceptor type 6 (ptpn6) gene, belongs to the family of protein tyrosine phosphatases (PTPs) and participates in multiple signaling pathways of immune cells. However, the mechanism of SHP1 in regulating fish immunity is largely unknown. In this study, we first identified two gibel carp (Carassius gibelio) ptpn6 homeologs (Cgptpn6-A and Cgptpn6-B), each of which had three alleles with high identities. Then, relative to Cgptpn6-B, dominant expression in adult tissues and higher upregulated expression of Cgptpn6-A induced by polyinosinic-polycytidylic acid (poly I:C), poly deoxyadenylic-deoxythymidylic (dA:dT) acid and spring viremia of carp virus (SVCV) were uncovered. Finally, we demonstrated that CgSHP1-A (encoded by the Cgptpn6-A gene) and CgSHP1-B (encoded by the Cgptpn6-B gene) act as negative regulators of the RIG-I-like receptor (RLR)-mediated interferon (IFN) response via two mechanisms: the inhibition of CaTBK1-induced phosphorylation of CaMITA shared by CgSHP1-A and CgSHP1-B, and the autophagic degradation of CaMITA exclusively by CgSHP1-A. Meanwhile, the data support that CgSHP1-A and CgSHP1-B have sub-functionalized and that CgSHP1-A overwhelmingly dominates CgSHP1-B in the process of RLR-mediated IFN response. The current study not only sheds light on the regulative mechanism of SHP1 in fish immunity, but also provides a typical case of duplicated gene evolutionary fates.Jin-Feng TongJin-Feng TongJin-Feng TongLi ZhouLi ZhouLi ZhouShun LiShun LiLong-Feng LuLong-Feng LuZhuo-Cong LiZhuo-Cong LiZhi LiZhi LiRui-Hai GanRui-Hai GanRui-Hai GanCheng-Yan MouCheng-Yan MouCheng-Yan MouQi-Ya ZhangQi-Ya ZhangZhong-Wei WangZhong-Wei WangZhong-Wei WangXiao-Juan ZhangYang WangYang WangYang WangJian-Fang GuiJian-Fang GuiJian-Fang GuiFrontiers Media S.A.articleGibel carpSHP1negative regulatorautophagyMITAinterferonImmunologic diseases. AllergyRC581-607ENFrontiers in Immunology, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Gibel carp SHP1 negative regulator autophagy MITA interferon Immunologic diseases. Allergy RC581-607
spellingShingle	Gibel carp SHP1 negative regulator autophagy MITA interferon Immunologic diseases. Allergy RC581-607 Jin-Feng Tong Jin-Feng Tong Jin-Feng Tong Li Zhou Li Zhou Li Zhou Shun Li Shun Li Long-Feng Lu Long-Feng Lu Zhuo-Cong Li Zhuo-Cong Li Zhi Li Zhi Li Rui-Hai Gan Rui-Hai Gan Rui-Hai Gan Cheng-Yan Mou Cheng-Yan Mou Cheng-Yan Mou Qi-Ya Zhang Qi-Ya Zhang Zhong-Wei Wang Zhong-Wei Wang Zhong-Wei Wang Xiao-Juan Zhang Yang Wang Yang Wang Yang Wang Jian-Fang Gui Jian-Fang Gui Jian-Fang Gui Two Duplicated Ptpn6 Homeologs Cooperatively and Negatively Regulate RLR-Mediated IFN Response in Hexaploid Gibel Carp
description	Src homology region 2 domain-containing phosphatase 1 (SHP1), encoded by the protein tyrosine phosphatase nonreceptor type 6 (ptpn6) gene, belongs to the family of protein tyrosine phosphatases (PTPs) and participates in multiple signaling pathways of immune cells. However, the mechanism of SHP1 in regulating fish immunity is largely unknown. In this study, we first identified two gibel carp (Carassius gibelio) ptpn6 homeologs (Cgptpn6-A and Cgptpn6-B), each of which had three alleles with high identities. Then, relative to Cgptpn6-B, dominant expression in adult tissues and higher upregulated expression of Cgptpn6-A induced by polyinosinic-polycytidylic acid (poly I:C), poly deoxyadenylic-deoxythymidylic (dA:dT) acid and spring viremia of carp virus (SVCV) were uncovered. Finally, we demonstrated that CgSHP1-A (encoded by the Cgptpn6-A gene) and CgSHP1-B (encoded by the Cgptpn6-B gene) act as negative regulators of the RIG-I-like receptor (RLR)-mediated interferon (IFN) response via two mechanisms: the inhibition of CaTBK1-induced phosphorylation of CaMITA shared by CgSHP1-A and CgSHP1-B, and the autophagic degradation of CaMITA exclusively by CgSHP1-A. Meanwhile, the data support that CgSHP1-A and CgSHP1-B have sub-functionalized and that CgSHP1-A overwhelmingly dominates CgSHP1-B in the process of RLR-mediated IFN response. The current study not only sheds light on the regulative mechanism of SHP1 in fish immunity, but also provides a typical case of duplicated gene evolutionary fates.
format	article
author	Jin-Feng Tong Jin-Feng Tong Jin-Feng Tong Li Zhou Li Zhou Li Zhou Shun Li Shun Li Long-Feng Lu Long-Feng Lu Zhuo-Cong Li Zhuo-Cong Li Zhi Li Zhi Li Rui-Hai Gan Rui-Hai Gan Rui-Hai Gan Cheng-Yan Mou Cheng-Yan Mou Cheng-Yan Mou Qi-Ya Zhang Qi-Ya Zhang Zhong-Wei Wang Zhong-Wei Wang Zhong-Wei Wang Xiao-Juan Zhang Yang Wang Yang Wang Yang Wang Jian-Fang Gui Jian-Fang Gui Jian-Fang Gui
author_facet	Jin-Feng Tong Jin-Feng Tong Jin-Feng Tong Li Zhou Li Zhou Li Zhou Shun Li Shun Li Long-Feng Lu Long-Feng Lu Zhuo-Cong Li Zhuo-Cong Li Zhi Li Zhi Li Rui-Hai Gan Rui-Hai Gan Rui-Hai Gan Cheng-Yan Mou Cheng-Yan Mou Cheng-Yan Mou Qi-Ya Zhang Qi-Ya Zhang Zhong-Wei Wang Zhong-Wei Wang Zhong-Wei Wang Xiao-Juan Zhang Yang Wang Yang Wang Yang Wang Jian-Fang Gui Jian-Fang Gui Jian-Fang Gui
author_sort	Jin-Feng Tong
title	Two Duplicated Ptpn6 Homeologs Cooperatively and Negatively Regulate RLR-Mediated IFN Response in Hexaploid Gibel Carp
title_short	Two Duplicated Ptpn6 Homeologs Cooperatively and Negatively Regulate RLR-Mediated IFN Response in Hexaploid Gibel Carp
title_full	Two Duplicated Ptpn6 Homeologs Cooperatively and Negatively Regulate RLR-Mediated IFN Response in Hexaploid Gibel Carp
title_fullStr	Two Duplicated Ptpn6 Homeologs Cooperatively and Negatively Regulate RLR-Mediated IFN Response in Hexaploid Gibel Carp
title_full_unstemmed	Two Duplicated Ptpn6 Homeologs Cooperatively and Negatively Regulate RLR-Mediated IFN Response in Hexaploid Gibel Carp
title_sort	two duplicated ptpn6 homeologs cooperatively and negatively regulate rlr-mediated ifn response in hexaploid gibel carp
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/c48623879e57447aaf7fb347b836bc28
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Two Duplicated Ptpn6 Homeologs Cooperatively and Negatively Regulate RLR-Mediated IFN Response in Hexaploid Gibel Carp

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