The autophagy protein Ambra1 regulates gene expression by supporting novel transcriptional complexes

Ambra1 is considered an autophagy and trafficking protein with roles in neurogenesis and cancer cell invasion. Here, we report that Ambra1 also localizes to the nucleus of cancer cells, where it has a novel nuclear scaffolding function that controls gene expression. Using biochemical fractionation a...

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Published inThe Journal of biological chemistry Vol. 295; no. 34; pp. 12045 - 12057
Main Authors Schoenherr, Christina, Byron, Adam, Griffith, Billie, Loftus, Alexander, Wills, Jimi C., Munro, Alison F., von Kriegsheim, Alex, Frame, Margaret C.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 21.08.2020
American Society for Biochemistry and Molecular Biology
Subjects
A Kinase Anchor Proteins - genetics
A Kinase Anchor Proteins - metabolism
Activating Transcription Factor 2 - genetics
Activating Transcription Factor 2 - metabolism
Active Transport, Cell Nucleus - genetics
Adaptor Proteins, Signal Transducing - genetics
Adaptor Proteins, Signal Transducing - metabolism
Akap8
Ambra1
Angiopoietin-1 - biosynthesis
Angiopoietin-1 - genetics
Atf2
autophagy
Cdk9
Cell Biology
Cell Line
chromatin
Chromatin - genetics
Chromatin - metabolism
DNA Helicases - genetics
DNA Helicases - metabolism
DNA transcription
Focal Adhesion Kinase 1 - genetics
Focal Adhesion Kinase 1 - metabolism
Gene Expression Regulation
Humans
Integrin alpha Chains - biosynthesis
Integrin alpha Chains - genetics
Integrin beta Chains - biosynthesis
Integrin beta Chains - genetics
Multiprotein Complexes - genetics
Multiprotein Complexes - metabolism
Nuclear Proteins - genetics
Nuclear Proteins - metabolism
nucleus
Signal Transduction
trafficking
transcription
Transcription Factors - genetics
Transcription Factors - metabolism
Transforming Growth Factor beta2 - biosynthesis
Transforming Growth Factor beta2 - genetics
Transforming Growth Factor beta3 - biosynthesis
Transforming Growth Factor beta3 - genetics
Atf2
Cdk9
autophagy
transcription
Ambra1
nucleus
Akap8
chromatin
trafficking
DNA transcription
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Abstract Ambra1 is considered an autophagy and trafficking protein with roles in neurogenesis and cancer cell invasion. Here, we report that Ambra1 also localizes to the nucleus of cancer cells, where it has a novel nuclear scaffolding function that controls gene expression. Using biochemical fractionation and proteomics, we found that Ambra1 binds to multiple classes of proteins in the nucleus, including nuclear pore proteins, adaptor proteins such as FAK and Akap8, chromatin-modifying proteins, and transcriptional regulators like Brg1 and Atf2. We identified biologically important genes, such as Angpt1, Tgfb2, Tgfb3, Itga8, and Itgb7, whose transcription is regulated by Ambra1-scaffolded complexes, likely by altering histone modifications and Atf2 activity. Therefore, in addition to its recognized roles in autophagy and trafficking, Ambra1 scaffolds protein complexes at chromatin, regulating transcriptional signaling in the nucleus. This novel function for Ambra1, and the specific genes impacted, may help to explain the wider role of Ambra1 in cancer cell biology.
AbstractList Ambra1 is considered an autophagy and trafficking protein with roles in neurogenesis and cancer cell invasion. Here, we report that Ambra1 also localizes to the nucleus of cancer cells, where it has a novel nuclear scaffolding function that controls gene expression. Using biochemical fractionation and proteomics, we found that Ambra1 binds to multiple classes of proteins in the nucleus, including nuclear pore proteins, adaptor proteins such as FAK and Akap8, chromatin-modifying proteins, and transcriptional regulators like Brg1 and Atf2. We identified biologically important genes, such as Angpt1, Tgfb2, Tgfb3, Itga8, and Itgb7, whose transcription is regulated by Ambra1-scaffolded complexes, likely by altering histone modifications and Atf2 activity. Therefore, in addition to its recognized roles in autophagy and trafficking, Ambra1 scaffolds protein complexes at chromatin, regulating transcriptional signaling in the nucleus. This novel function for Ambra1, and the specific genes impacted, may help to explain the wider role of Ambra1 in cancer cell biology.
Ambra1 is considered an autophagy and trafficking protein with roles in neurogenesis and cancer cell invasion. Here, we report that Ambra1 also localizes to the nucleus of cancer cells, where it has a novel nuclear scaffolding function that controls gene expression. Using biochemical fractionation and proteomics, we found that Ambra1 binds to multiple classes of proteins in the nucleus, including nuclear pore proteins, adaptor proteins such as FAK and Akap8, chromatin-modifying proteins, and transcriptional regulators like Brg1 and Atf2. We identified biologically important genes, such as Angpt1 , Tgfb2 , Tgfb3 , Itga8 , and Itgb7 , whose transcription is regulated by Ambra1-scaffolded complexes, likely by altering histone modifications and Atf2 activity. Therefore, in addition to its recognized roles in autophagy and trafficking, Ambra1 scaffolds protein complexes at chromatin, regulating transcriptional signaling in the nucleus. This novel function for Ambra1, and the specific genes impacted, may help to explain the wider role of Ambra1 in cancer cell biology.
Ambra1 is considered an autophagy and trafficking protein with roles in neurogenesis and cancer cell invasion. Here, we report that Ambra1 also localizes to the nucleus of cancer cells, where it has a novel nuclear scaffolding function that controls gene expression. Using biochemical fractionation and proteomics, we found that Ambra1 binds to multiple classes of proteins in the nucleus, including nuclear pore proteins, adaptor proteins such as FAK and Akap8, chromatin-modifying proteins, and transcriptional regulators like Brg1 and Atf2. We identified biologically important genes, such as , , , , and , whose transcription is regulated by Ambra1-scaffolded complexes, likely by altering histone modifications and Atf2 activity. Therefore, in addition to its recognized roles in autophagy and trafficking, Ambra1 scaffolds protein complexes at chromatin, regulating transcriptional signaling in the nucleus. This novel function for Ambra1, and the specific genes impacted, may help to explain the wider role of Ambra1 in cancer cell biology.
Author Schoenherr, Christina
Byron, Adam
Wills, Jimi C.
Griffith, Billie
Munro, Alison F.
von Kriegsheim, Alex
Loftus, Alexander
Frame, Margaret C.
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Issue 34
Keywords Atf2
Cdk9
autophagy
transcription
Ambra1
nucleus
Akap8
chromatin
trafficking
DNA transcription
Language English
License This is an open access article under the CC BY license.
2020 Schoenherr et al.
Published under exclusive license by The American Society for Biochemistry and Molecular Biology, Inc.
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Snippet Ambra1 is considered an autophagy and trafficking protein with roles in neurogenesis and cancer cell invasion. Here, we report that Ambra1 also localizes to...
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elsevier
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SubjectTerms A Kinase Anchor Proteins - genetics
A Kinase Anchor Proteins - metabolism
Activating Transcription Factor 2 - genetics
Activating Transcription Factor 2 - metabolism
Active Transport, Cell Nucleus - genetics
Adaptor Proteins, Signal Transducing - genetics
Adaptor Proteins, Signal Transducing - metabolism
Akap8
Ambra1
Angiopoietin-1 - biosynthesis
Angiopoietin-1 - genetics
Atf2
autophagy
Cdk9
Cell Biology
Cell Line
chromatin
Chromatin - genetics
Chromatin - metabolism
DNA Helicases - genetics
DNA Helicases - metabolism
DNA transcription
Focal Adhesion Kinase 1 - genetics
Focal Adhesion Kinase 1 - metabolism
Gene Expression Regulation
Humans
Integrin alpha Chains - biosynthesis
Integrin alpha Chains - genetics
Integrin beta Chains - biosynthesis
Integrin beta Chains - genetics
Multiprotein Complexes - genetics
Multiprotein Complexes - metabolism
Nuclear Proteins - genetics
Nuclear Proteins - metabolism
nucleus
Signal Transduction
trafficking
transcription
Transcription Factors - genetics
Transcription Factors - metabolism
Transforming Growth Factor beta2 - biosynthesis
Transforming Growth Factor beta2 - genetics
Transforming Growth Factor beta3 - biosynthesis
Transforming Growth Factor beta3 - genetics
Title The autophagy protein Ambra1 regulates gene expression by supporting novel transcriptional complexes
URI https://dx.doi.org/10.1074/jbc.RA120.012565
https://www.ncbi.nlm.nih.gov/pubmed/32616651
https://search.proquest.com/docview/2420154163
https://pubmed.ncbi.nlm.nih.gov/PMC7443501
Volume 295
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