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A Predominant Role of AtEDEM1 in Catalyzing a Rate-Limiting Demannosylation Step of an Arabidopsis Endoplasmic Reticulum-Associated Degradation Process

Endoplasmic reticulum-associated degradation (ERAD) is a key cellular process for degrading misfolded proteins. It was well known that an asparagine (N)-linked glycan containing a free α1,6-mannose residue is a critical ERAD signal created by Homologous to α-mannosidase 1 (Htm1) in yeast and ER-Degr...

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Autores principales: Zhang, Jianjun, Xia, Yang, Wang, Dinghe, Du, Yamin, Chen, Yongwu, Zhang, Congcong, Mao, Juan, Wang, Muyang, She, Yi-Min, Peng, Xinxiang, Liu, Li, Voglmeir, Josef, He, Zuhua, Liu, Linchuan, Li, Jianming
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9302962/
https://www.ncbi.nlm.nih.gov/pubmed/35874007
http://dx.doi.org/10.3389/fpls.2022.952246
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author Zhang, Jianjun
Xia, Yang
Wang, Dinghe
Du, Yamin
Chen, Yongwu
Zhang, Congcong
Mao, Juan
Wang, Muyang
She, Yi-Min
Peng, Xinxiang
Liu, Li
Voglmeir, Josef
He, Zuhua
Liu, Linchuan
Li, Jianming
author_facet Zhang, Jianjun
Xia, Yang
Wang, Dinghe
Du, Yamin
Chen, Yongwu
Zhang, Congcong
Mao, Juan
Wang, Muyang
She, Yi-Min
Peng, Xinxiang
Liu, Li
Voglmeir, Josef
He, Zuhua
Liu, Linchuan
Li, Jianming
author_sort Zhang, Jianjun
collection PubMed
description Endoplasmic reticulum-associated degradation (ERAD) is a key cellular process for degrading misfolded proteins. It was well known that an asparagine (N)-linked glycan containing a free α1,6-mannose residue is a critical ERAD signal created by Homologous to α-mannosidase 1 (Htm1) in yeast and ER-Degradation Enhancing α-Mannosidase-like proteins (EDEMs) in mammals. An earlier study suggested that two Arabidopsis homologs of Htm1/EDEMs function redundantly in generating such a conserved N-glycan signal. Here we report that the Arabidopsis irb1 (reversal of bri1) mutants accumulate brassinosteroid-insensitive 1–5 (bri1–5), an ER-retained mutant variant of the brassinosteroid receptor BRI1 and are defective in one of the Arabidopsis Htm1/EDEM homologs, AtEDEM1. We show that the wild-type AtEDEM1, but not its catalytically inactive mutant, rescues irb1-1. Importantly, an insertional mutation of the Arabidopsis Asparagine-Linked Glycosylation 3 (ALG3), which causes N-linked glycosylation with truncated glycans carrying a different free α1,6-mannose residue, completely nullifies the inhibitory effect of irb1-1 on bri1-5 ERAD. Interestingly, an insertional mutation in AtEDEM2, the other Htm1/EDEM homolog, has no detectable effect on bri1-5 ERAD; however, it enhances the inhibitory effect of irb1-1 on bri1-5 degradation. Moreover, AtEDEM2 transgenes rescued the irb1-1 mutation with lower efficacy than AtEDEM1. Simultaneous elimination of AtEDEM1 and AtEDEM2 completely blocks generation of α1,6-mannose-exposed N-glycans on bri1-5, while overexpression of either AtEDEM1 or AtEDEM2 stimulates bri1-5 ERAD and enhances the bri1-5 dwarfism. We concluded that, despite its functional redundancy with AtEDEM2, AtEDEM1 plays a predominant role in promoting bri1-5 degradation.
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spelling pubmed-93029622022-07-22 A Predominant Role of AtEDEM1 in Catalyzing a Rate-Limiting Demannosylation Step of an Arabidopsis Endoplasmic Reticulum-Associated Degradation Process Zhang, Jianjun Xia, Yang Wang, Dinghe Du, Yamin Chen, Yongwu Zhang, Congcong Mao, Juan Wang, Muyang She, Yi-Min Peng, Xinxiang Liu, Li Voglmeir, Josef He, Zuhua Liu, Linchuan Li, Jianming Front Plant Sci Plant Science Endoplasmic reticulum-associated degradation (ERAD) is a key cellular process for degrading misfolded proteins. It was well known that an asparagine (N)-linked glycan containing a free α1,6-mannose residue is a critical ERAD signal created by Homologous to α-mannosidase 1 (Htm1) in yeast and ER-Degradation Enhancing α-Mannosidase-like proteins (EDEMs) in mammals. An earlier study suggested that two Arabidopsis homologs of Htm1/EDEMs function redundantly in generating such a conserved N-glycan signal. Here we report that the Arabidopsis irb1 (reversal of bri1) mutants accumulate brassinosteroid-insensitive 1–5 (bri1–5), an ER-retained mutant variant of the brassinosteroid receptor BRI1 and are defective in one of the Arabidopsis Htm1/EDEM homologs, AtEDEM1. We show that the wild-type AtEDEM1, but not its catalytically inactive mutant, rescues irb1-1. Importantly, an insertional mutation of the Arabidopsis Asparagine-Linked Glycosylation 3 (ALG3), which causes N-linked glycosylation with truncated glycans carrying a different free α1,6-mannose residue, completely nullifies the inhibitory effect of irb1-1 on bri1-5 ERAD. Interestingly, an insertional mutation in AtEDEM2, the other Htm1/EDEM homolog, has no detectable effect on bri1-5 ERAD; however, it enhances the inhibitory effect of irb1-1 on bri1-5 degradation. Moreover, AtEDEM2 transgenes rescued the irb1-1 mutation with lower efficacy than AtEDEM1. Simultaneous elimination of AtEDEM1 and AtEDEM2 completely blocks generation of α1,6-mannose-exposed N-glycans on bri1-5, while overexpression of either AtEDEM1 or AtEDEM2 stimulates bri1-5 ERAD and enhances the bri1-5 dwarfism. We concluded that, despite its functional redundancy with AtEDEM2, AtEDEM1 plays a predominant role in promoting bri1-5 degradation. Frontiers Media S.A. 2022-07-07 /pmc/articles/PMC9302962/ /pubmed/35874007 http://dx.doi.org/10.3389/fpls.2022.952246 Text en Copyright © 2022 Zhang, Xia, Wang, Du, Chen, Zhang, Mao, Wang, She, Peng, Liu, Voglmeir, He, Liu and Li. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Zhang, Jianjun
Xia, Yang
Wang, Dinghe
Du, Yamin
Chen, Yongwu
Zhang, Congcong
Mao, Juan
Wang, Muyang
She, Yi-Min
Peng, Xinxiang
Liu, Li
Voglmeir, Josef
He, Zuhua
Liu, Linchuan
Li, Jianming
A Predominant Role of AtEDEM1 in Catalyzing a Rate-Limiting Demannosylation Step of an Arabidopsis Endoplasmic Reticulum-Associated Degradation Process
title A Predominant Role of AtEDEM1 in Catalyzing a Rate-Limiting Demannosylation Step of an Arabidopsis Endoplasmic Reticulum-Associated Degradation Process
title_full A Predominant Role of AtEDEM1 in Catalyzing a Rate-Limiting Demannosylation Step of an Arabidopsis Endoplasmic Reticulum-Associated Degradation Process
title_fullStr A Predominant Role of AtEDEM1 in Catalyzing a Rate-Limiting Demannosylation Step of an Arabidopsis Endoplasmic Reticulum-Associated Degradation Process
title_full_unstemmed A Predominant Role of AtEDEM1 in Catalyzing a Rate-Limiting Demannosylation Step of an Arabidopsis Endoplasmic Reticulum-Associated Degradation Process
title_short A Predominant Role of AtEDEM1 in Catalyzing a Rate-Limiting Demannosylation Step of an Arabidopsis Endoplasmic Reticulum-Associated Degradation Process
title_sort predominant role of atedem1 in catalyzing a rate-limiting demannosylation step of an arabidopsis endoplasmic reticulum-associated degradation process
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9302962/
https://www.ncbi.nlm.nih.gov/pubmed/35874007
http://dx.doi.org/10.3389/fpls.2022.952246
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