Cytosolic O-GlcNAcylation and PNG1 maintain Drosophila gut homeostasis by regulating proliferation and apoptosis.

Tissue homeostasis requires a delicate balance between stem cell self-renewal, proliferation, and differentiation. Essential to this process is glycosylation, with both intra-and extra-cellular glycosylation being required for stem cell homeostasis. However, it remains unknown how intracellular glyc...

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Main Authors: Hyun-Jin Na, Lara K Abramowitz, John A Hanover
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-03-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1010128&type=printable
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author Hyun-Jin Na
Lara K Abramowitz
John A Hanover
author_facet Hyun-Jin Na
Lara K Abramowitz
John A Hanover
author_sort Hyun-Jin Na
collection DOAJ
description Tissue homeostasis requires a delicate balance between stem cell self-renewal, proliferation, and differentiation. Essential to this process is glycosylation, with both intra-and extra-cellular glycosylation being required for stem cell homeostasis. However, it remains unknown how intracellular glycosylation, O-GlcNAcylation, interfaces with cellular components of the extracellular glycosylation machinery, like the cytosolic N-glycanase NGLY1. In this study, we utilize the Drosophila gut and uncover a pathway in which O-GlcNAcylation cooperates with the NGLY1 homologue PNG1 to regulate proliferation in intestinal stem cells (ISCs) and apoptosis in differentiated enterocytes. Further, the CncC antioxidant signaling pathway and ENGase, an enzyme involved in the processing of free oligosaccharides in the cytosol, interact with O-GlcNAc and PNG1 through regulation of protein aggregates to contribute to gut maintenance. These findings reveal a complex coordinated regulation between O-GlcNAcylation and the cytosolic glycanase PNG1 critical to balancing proliferation and apoptosis to maintain gut homeostasis.
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publishDate 2022-03-01
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spelling doaj-art-0f4d1de8df93425ea62965bcb2dd47d42025-08-20T02:31:41ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042022-03-01183e101012810.1371/journal.pgen.1010128Cytosolic O-GlcNAcylation and PNG1 maintain Drosophila gut homeostasis by regulating proliferation and apoptosis.Hyun-Jin NaLara K AbramowitzJohn A HanoverTissue homeostasis requires a delicate balance between stem cell self-renewal, proliferation, and differentiation. Essential to this process is glycosylation, with both intra-and extra-cellular glycosylation being required for stem cell homeostasis. However, it remains unknown how intracellular glycosylation, O-GlcNAcylation, interfaces with cellular components of the extracellular glycosylation machinery, like the cytosolic N-glycanase NGLY1. In this study, we utilize the Drosophila gut and uncover a pathway in which O-GlcNAcylation cooperates with the NGLY1 homologue PNG1 to regulate proliferation in intestinal stem cells (ISCs) and apoptosis in differentiated enterocytes. Further, the CncC antioxidant signaling pathway and ENGase, an enzyme involved in the processing of free oligosaccharides in the cytosol, interact with O-GlcNAc and PNG1 through regulation of protein aggregates to contribute to gut maintenance. These findings reveal a complex coordinated regulation between O-GlcNAcylation and the cytosolic glycanase PNG1 critical to balancing proliferation and apoptosis to maintain gut homeostasis.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1010128&type=printable
spellingShingle Hyun-Jin Na
Lara K Abramowitz
John A Hanover
Cytosolic O-GlcNAcylation and PNG1 maintain Drosophila gut homeostasis by regulating proliferation and apoptosis.
PLoS Genetics
title Cytosolic O-GlcNAcylation and PNG1 maintain Drosophila gut homeostasis by regulating proliferation and apoptosis.
title_full Cytosolic O-GlcNAcylation and PNG1 maintain Drosophila gut homeostasis by regulating proliferation and apoptosis.
title_fullStr Cytosolic O-GlcNAcylation and PNG1 maintain Drosophila gut homeostasis by regulating proliferation and apoptosis.
title_full_unstemmed Cytosolic O-GlcNAcylation and PNG1 maintain Drosophila gut homeostasis by regulating proliferation and apoptosis.
title_short Cytosolic O-GlcNAcylation and PNG1 maintain Drosophila gut homeostasis by regulating proliferation and apoptosis.
title_sort cytosolic o glcnacylation and png1 maintain drosophila gut homeostasis by regulating proliferation and apoptosis
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1010128&type=printable
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AT larakabramowitz cytosolicoglcnacylationandpng1maintaindrosophilaguthomeostasisbyregulatingproliferationandapoptosis
AT johnahanover cytosolicoglcnacylationandpng1maintaindrosophilaguthomeostasisbyregulatingproliferationandapoptosis