Metabolic regulation of the proteasome under hypoxia by Poldip2 controls fibrotic signaling in vascular smooth muscle cells
The polymerase delta interacting protein 2 (Poldip2) is a nuclear-encoded mitochondrial protein required for oxidative metabolism. Under hypoxia, Poldip2 expression is repressed by an unknown mechanism. Therefore, low levels of Poldip2 are required to maintain glycolytic metabolism. The Cellular Com...
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Published in | Free radical biology & medicine Vol. 195; pp. 283 - 297 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Inc
01.02.2023
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Abstract | The polymerase delta interacting protein 2 (Poldip2) is a nuclear-encoded mitochondrial protein required for oxidative metabolism. Under hypoxia, Poldip2 expression is repressed by an unknown mechanism. Therefore, low levels of Poldip2 are required to maintain glycolytic metabolism.
The Cellular Communication Network Factor 2 (CCN2, Connective tissue growth factor, CTGF) is a profibrogenic molecule highly expressed in cancer and vascular inflammation in advanced atherosclerosis. Because CCN2 is upregulated under hypoxia and is associated with glycolytic metabolism, we hypothesize that Poldip2 downregulation is responsible for the upregulation of profibrotic signaling under hypoxia. Here, we report that Poldip2 is repressed under hypoxia by a mechanism that requires the activation of the enhancer of zeste homolog 2 repressive complex (EZH2) downstream from the Cyclin-Dependent Kinase 2 (CDK2). Importantly, we found that Poldip2 repression is required for CCN2 expression downstream of metabolic inhibition of the ubiquitin-proteasome system (UPS)-dependent stabilization of the serum response factor. Pharmacological or gene expression inhibition of CDK2 under hypoxia reverses Poldip2 downregulation, the inhibition of the UPS, and the expression of CCN2, collagen, and fibronectin. Thus, our findings connect cell cycle regulation and proteasome activity to mitochondrial function and fibrotic responses under hypoxia.
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•In hypoxia, Poldip2 is repressed by EZH2-mediated signaling downstream of the cell cycle.•Poldip2 expression under hypoxia controls the activity of the Ubiquitin proteasome system.•Cell cycle regulation controls pro-fibrotic signaling under hypoxia.•Poldip2 deficiency exacerbates hypoxia-induced vascular hypoxia. |
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AbstractList | The polymerase delta interacting protein 2 (Poldip2) is a nuclear-encoded mitochondrial protein required for oxidative metabolism. Under hypoxia, Poldip2 expression is repressed by an unknown mechanism. Therefore, low levels of Poldip2 are required to maintain glycolytic metabolism.
The Cellular Communication Network Factor 2 (CCN2, Connective tissue growth factor, CTGF) is a profibrogenic molecule highly expressed in cancer and vascular inflammation in advanced atherosclerosis. Because CCN2 is upregulated under hypoxia and is associated with glycolytic metabolism, we hypothesize that Poldip2 downregulation is responsible for the upregulation of profibrotic signaling under hypoxia. Here, we report that Poldip2 is repressed under hypoxia by a mechanism that requires the activation of the enhancer of zeste homolog 2 repressive complex (EZH2) downstream from the Cyclin-Dependent Kinase 2 (CDK2). Importantly, we found that Poldip2 repression is required for CCN2 expression downstream of metabolic inhibition of the ubiquitin-proteasome system (UPS)-dependent stabilization of the serum response factor. Pharmacological or gene expression inhibition of CDK2 under hypoxia reverses Poldip2 downregulation, the inhibition of the UPS, and the expression of CCN2, collagen, and fibronectin. Thus, our findings connect cell cycle regulation and proteasome activity to mitochondrial function and fibrotic responses under hypoxia. The polymerase delta interacting protein 2 (Poldip2) is a nuclear-encoded mitochondrial protein required for oxidative metabolism. Under hypoxia, Poldip2 expression is repressed by an unknown mechanism. Therefore, low levels of Poldip2 are required to maintain glycolytic metabolism. The Cellular Communication Network Factor 2 (CCN2, Connective tissue growth factor, CTGF) is a profibrogenic molecule highly expressed in cancer and vascular inflammation in advanced atherosclerosis. Because CCN2 is upregulated under hypoxia and is associated with glycolytic metabolism, we hypothesize that Poldip2 downregulation is responsible for the upregulation of profibrotic signaling under hypoxia. Here, we report that Poldip2 is repressed under hypoxia by a mechanism that requires the activation of the enhancer of zeste homolog 2 repressive complex (EZH2) downstream from the Cyclin-Dependent Kinase 2 (CDK2). Importantly, we found that Poldip2 repression is required for CCN2 expression downstream of metabolic inhibition of the ubiquitin-proteasome system (UPS)-dependent stabilization of the serum response factor. Pharmacological or gene expression inhibition of CDK2 under hypoxia reverses Poldip2 downregulation, the inhibition of the UPS, and the expression of CCN2, collagen, and fibronectin. Thus, our findings connect cell cycle regulation and proteasome activity to mitochondrial function and fibrotic responses under hypoxia. The polymerase delta interacting protein 2 (Poldip2) is a nuclear-encoded mitochondrial protein required for oxidative metabolism. Under hypoxia, Poldip2 expression is repressed by an unknown mechanism. Therefore, low levels of Poldip2 are required to maintain glycolytic metabolism. The Cellular Communication Network Factor 2 (CCN2, Connective tissue growth factor, CTGF) is a profibrogenic molecule highly expressed in cancer and vascular inflammation in advanced atherosclerosis. Because CCN2 is upregulated under hypoxia and is associated with glycolytic metabolism, we hypothesize that Poldip2 downregulation is responsible for the upregulation of profibrotic signaling under hypoxia. Here, we report that Poldip2 is repressed under hypoxia by a mechanism that requires the activation of the enhancer of zeste homolog 2 repressive complex (EZH2) downstream from the Cyclin-Dependent Kinase 2 (CDK2). Importantly, we found that Poldip2 repression is required for CCN2 expression downstream of metabolic inhibition of the ubiquitin-proteasome system (UPS)-dependent stabilization of the serum response factor. Pharmacological or gene expression inhibition of CDK2 under hypoxia reverses Poldip2 downregulation, the inhibition of the UPS, and the expression of CCN2, collagen, and fibronectin. Thus, our findings connect cell cycle regulation and proteasome activity to mitochondrial function and fibrotic responses under hypoxia. [Display omitted] •In hypoxia, Poldip2 is repressed by EZH2-mediated signaling downstream of the cell cycle.•Poldip2 expression under hypoxia controls the activity of the Ubiquitin proteasome system.•Cell cycle regulation controls pro-fibrotic signaling under hypoxia.•Poldip2 deficiency exacerbates hypoxia-induced vascular hypoxia. |
Author | Holden, Claire M. Paredes, Felipe Bogan, Bethany Fuentealba, Roberto Suster, Izabela Tejos, Macarena San Martin, Alejandra Williams, Holly C. |
AuthorAffiliation | 1 Department of Medicine, Division of Cardiology, Emory University, Atlanta, GA 30322 2 Institute of Chemistry and Natural Resources, Universidad de Talca, Talca 3460000, Chile |
AuthorAffiliation_xml | – name: 1 Department of Medicine, Division of Cardiology, Emory University, Atlanta, GA 30322 – name: 2 Institute of Chemistry and Natural Resources, Universidad de Talca, Talca 3460000, Chile |
Author_xml | – sequence: 1 givenname: Felipe surname: Paredes fullname: Paredes, Felipe organization: Department of Medicine, Division of Cardiology, Emory University, Atlanta, GA, 30322, USA – sequence: 2 givenname: Holly C. orcidid: 0000-0002-1890-1830 surname: Williams fullname: Williams, Holly C. organization: Department of Medicine, Division of Cardiology, Emory University, Atlanta, GA, 30322, USA – sequence: 3 givenname: Izabela surname: Suster fullname: Suster, Izabela organization: Department of Medicine, Division of Cardiology, Emory University, Atlanta, GA, 30322, USA – sequence: 4 givenname: Macarena surname: Tejos fullname: Tejos, Macarena organization: Department of Medicine, Division of Cardiology, Emory University, Atlanta, GA, 30322, USA – sequence: 5 givenname: Roberto surname: Fuentealba fullname: Fuentealba, Roberto organization: Institute of Chemistry and Natural Resources, Universidad de Talca, Talca, 3460000, Chile – sequence: 6 givenname: Bethany surname: Bogan fullname: Bogan, Bethany organization: Department of Medicine, Division of Cardiology, Emory University, Atlanta, GA, 30322, USA – sequence: 7 givenname: Claire M. surname: Holden fullname: Holden, Claire M. organization: Department of Medicine, Division of Cardiology, Emory University, Atlanta, GA, 30322, USA – sequence: 8 givenname: Alejandra surname: San Martin fullname: San Martin, Alejandra email: asanmartin@emory.edu organization: Department of Medicine, Division of Cardiology, Emory University, Atlanta, GA, 30322, USA |
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Keywords | GFPT2 SRF Poldip2 HK2 CCNA2 Mitochondria PSMC1 Cell cycle CDK2 Hypoxia CCN2 OGT Proteasome EZH2 |
Language | English |
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Snippet | The polymerase delta interacting protein 2 (Poldip2) is a nuclear-encoded mitochondrial protein required for oxidative metabolism. Under hypoxia, Poldip2... |
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SubjectTerms | CCN2 Cell cycle Connective Tissue Growth Factor - genetics Connective Tissue Growth Factor - metabolism Humans Hypoxia Hypoxia - genetics Hypoxia - metabolism Mitochondria Muscle, Smooth, Vascular - metabolism Nuclear Proteins - metabolism Poldip2 Proteasome Proteasome Endopeptidase Complex - genetics Proteasome Endopeptidase Complex - metabolism Signal Transduction |
Title | Metabolic regulation of the proteasome under hypoxia by Poldip2 controls fibrotic signaling in vascular smooth muscle cells |
URI | https://dx.doi.org/10.1016/j.freeradbiomed.2022.12.098 https://www.ncbi.nlm.nih.gov/pubmed/36596387 https://search.proquest.com/docview/2760817934 https://pubmed.ncbi.nlm.nih.gov/PMC10268434 |
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