Negative regulation of autophagy by UBA6-BIRC6–mediated ubiquitination of LC3

Although the process of autophagy has been extensively studied, the mechanisms that regulate it remain insufficiently understood. To identify novel autophagy regulators, we performed a whole-genome CRISPR/Cas9 knockout screen in H4 human neuroglioma cells expressing endogenous LC3B tagged with a tan...

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Published ineLife Vol. 8
Main Authors Jia, Rui, Bonifacino, Juan S
Format Journal Article
LanguageEnglish
Published England eLife Science Publications, Ltd 06.11.2019
eLife Sciences Publications Ltd
eLife Sciences Publications, Ltd
Subjects
Autophagy
BIRC6
Cell Biology
Cell Line
CRISPR
Enzymes
Gene expression
Gene Expression Regulation, Enzymologic
Gene Knockout Techniques
Genetic Testing
Genomes
Genomics
Hippocampus
Humans
Inhibitor of Apoptosis Proteins - metabolism
Kinases
LC3
Ligases
Microtubule-Associated Proteins - metabolism
Nervous system diseases
Neurodegenerative diseases
Neurons
Novels
Phagocytosis
Phosphorylation
Polymerization
Proteasome Endopeptidase Complex - metabolism
Proteasomes
Protein biosynthesis
Protein Interaction Maps
Protein synthesis
Proteins
Proteolysis
Scientific equipment industry
Sedimentation & deposition
Synuclein
UBA6
Ubiquitin
Ubiquitin-Activating Enzymes - metabolism
Ubiquitin-conjugating enzyme
Ubiquitin-protein ligase
Ubiquitination
Variance analysis
United States
United States > US
autophagy
cell biology
rat
UBA6
ubiquitination
BIRC6
LC3
human
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Abstract Although the process of autophagy has been extensively studied, the mechanisms that regulate it remain insufficiently understood. To identify novel autophagy regulators, we performed a whole-genome CRISPR/Cas9 knockout screen in H4 human neuroglioma cells expressing endogenous LC3B tagged with a tandem of GFP and mCherry. Using this methodology, we identified the ubiquitin-activating enzyme UBA6 and the hybrid ubiquitin-conjugating enzyme/ubiquitin ligase BIRC6 as autophagy regulators. We found that these enzymes cooperate to monoubiquitinate LC3B, targeting it for proteasomal degradation. Knockout of UBA6 or BIRC6 increased autophagic flux under conditions of nutrient deprivation or protein synthesis inhibition. Moreover, UBA6 or BIRC6 depletion decreased the formation of aggresome-like induced structures in H4 cells, and α-synuclein aggregates in rat hippocampal neurons. These findings demonstrate that UBA6 and BIRC6 negatively regulate autophagy by limiting the availability of LC3B. Inhibition of UBA6/BIRC6 could be used to enhance autophagic clearance of protein aggregates in neurodegenerative disorders.
AbstractList Although the process of autophagy has been extensively studied, the mechanisms that regulate it remain insufficiently understood. To identify novel autophagy regulators, we performed a whole-genome CRISPR/Cas9 knockout screen in H4 human neuroglioma cells expressing endogenous LC3B tagged with a tandem of GFP and mCherry. Using this methodology, we identified the ubiquitin-activating enzyme UBA6 and the hybrid ubiquitin-conjugating enzyme/ubiquitin ligase BIRC6 as autophagy regulators. We found that these enzymes cooperate to monoubiquitinate LC3B, targeting it for proteasomal degradation. Knockout of UBA6 or BIRC6 increased autophagic flux under conditions of nutrient deprivation or protein synthesis inhibition. Moreover, UBA6 or BIRC6 depletion decreased the formation of aggresome-like induced structures in H4 cells, and α-synuclein aggregates in rat hippocampal neurons. These findings demonstrate that UBA6 and BIRC6 negatively regulate autophagy by limiting the availability of LC3B. Inhibition of UBA6/BIRC6 could be used to enhance autophagic clearance of protein aggregates in neurodegenerative disorders.
Although the process of autophagy has been extensively studied, the mechanisms that regulate it remain insufficiently understood. To identify novel autophagy regulators, we performed a whole-genome CRISPR/Cas9 knockout screen in H4 human neuroglioma cells expressing endogenous LC3B tagged with a tandem of GFP and mCherry. Using this methodology, we identified the ubiquitin-activating enzyme UBA6 and the hybrid ubiquitin-conjugating enzyme/ubiquitin ligase BIRC6 as autophagy regulators. We found that these enzymes cooperate to monoubiquitinate LC3B, targeting it for proteasomal degradation. Knockout of UBA6 or BIRC6 increased autophagic flux under conditions of nutrient deprivation or protein synthesis inhibition. Moreover, UBA6 or BIRC6 depletion decreased the formation of aggresome-like induced structures in H4 cells, and [alpha]-synuclein aggregates in rat hippocampal neurons. These findings demonstrate that UBA6 and BIRC6 negatively regulate autophagy by limiting the availability of LC3B. Inhibition of UBA6/BIRC6 could be used to enhance autophagic clearance of protein aggregates in neurodegenerative disorders.
Although the process of autophagy has been extensively studied, the mechanisms that regulate it remain insufficiently understood. To identify novel autophagy regulators, we performed a whole-genome CRISPR/Cas9 knockout screen in H4 human neuroglioma cells expressing endogenous LC3B tagged with a tandem of GFP and mCherry. Using this methodology, we identified the ubiquitin-activating enzyme UBA6 and the hybrid ubiquitin-conjugating enzyme/ubiquitin ligase BIRC6 as autophagy regulators. We found that these enzymes cooperate to monoubiquitinate LC3B, targeting it for proteasomal degradation. Knockout of UBA6 or BIRC6 increased autophagic flux under conditions of nutrient deprivation or protein synthesis inhibition. Moreover, UBA6 or BIRC6 depletion decreased the formation of aggresome-like induced structures in H4 cells, and α-synuclein aggregates in rat hippocampal neurons. These findings demonstrate that UBA6 and BIRC6 negatively regulate autophagy by limiting the availability of LC3B. Inhibition of UBA6/BIRC6 could be used to enhance autophagic clearance of protein aggregates in neurodegenerative disorders.Although the process of autophagy has been extensively studied, the mechanisms that regulate it remain insufficiently understood. To identify novel autophagy regulators, we performed a whole-genome CRISPR/Cas9 knockout screen in H4 human neuroglioma cells expressing endogenous LC3B tagged with a tandem of GFP and mCherry. Using this methodology, we identified the ubiquitin-activating enzyme UBA6 and the hybrid ubiquitin-conjugating enzyme/ubiquitin ligase BIRC6 as autophagy regulators. We found that these enzymes cooperate to monoubiquitinate LC3B, targeting it for proteasomal degradation. Knockout of UBA6 or BIRC6 increased autophagic flux under conditions of nutrient deprivation or protein synthesis inhibition. Moreover, UBA6 or BIRC6 depletion decreased the formation of aggresome-like induced structures in H4 cells, and α-synuclein aggregates in rat hippocampal neurons. These findings demonstrate that UBA6 and BIRC6 negatively regulate autophagy by limiting the availability of LC3B. Inhibition of UBA6/BIRC6 could be used to enhance autophagic clearance of protein aggregates in neurodegenerative disorders.
Audience Academic
Author Jia, Rui
Bonifacino, Juan S
Author_xml – sequence: 1
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  orcidid: 0000-0002-1797-4069
  surname: Jia
  fullname: Jia, Rui
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  orcidid: 0000-0002-5673-6370
  surname: Bonifacino
  fullname: Bonifacino, Juan S
  organization: Neurosciences and Cellular and Structural Biology Division, Eunice Kennedy Shriver National Institute of Child Health and Human Development National Institutes of Health, Bethesda, United States
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31692446$$D View this record in MEDLINE/PubMed
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Keywords autophagy
cell biology
rat
UBA6
ubiquitination
BIRC6
LC3
human
Language English
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Snippet Although the process of autophagy has been extensively studied, the mechanisms that regulate it remain insufficiently understood. To identify novel autophagy...
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SubjectTerms Autophagy
BIRC6
Cell Biology
Cell Line
CRISPR
Enzymes
Gene expression
Gene Expression Regulation, Enzymologic
Gene Knockout Techniques
Genetic Testing
Genomes
Genomics
Hippocampus
Humans
Inhibitor of Apoptosis Proteins - metabolism
Kinases
LC3
Ligases
Microtubule-Associated Proteins - metabolism
Nervous system diseases
Neurodegenerative diseases
Neurons
Novels
Phagocytosis
Phosphorylation
Polymerization
Proteasome Endopeptidase Complex - metabolism
Proteasomes
Protein biosynthesis
Protein Interaction Maps
Protein synthesis
Proteins
Proteolysis
Scientific equipment industry
Sedimentation & deposition
Synuclein
UBA6
Ubiquitin
Ubiquitin-Activating Enzymes - metabolism
Ubiquitin-conjugating enzyme
Ubiquitin-protein ligase
Ubiquitination
Variance analysis
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Title Negative regulation of autophagy by UBA6-BIRC6–mediated ubiquitination of LC3
URI https://www.ncbi.nlm.nih.gov/pubmed/31692446
https://www.proquest.com/docview/2320050810
https://www.proquest.com/docview/2312555417
https://pubmed.ncbi.nlm.nih.gov/PMC6863627
https://doaj.org/article/5613fd83227d40cf9b03e8ccce1b5ef8
Volume 8
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