Modulators of Alpha-2 Macroglobulin Upregulation by High Glucose in Glomerular Mesangial Cells

Up to 40% of patients with diabetes mellitus will develop diabetic kidney disease (DKD), characterized pathologically by the accumulation of extracellular matrix proteins, which leads to the loss of kidney function over time. Our previous studies showed that the pan-protease inhibitor alpha 2-macrog...

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Main Authors: Jackie Trink, Renzhong Li, Bo Gao, Chao Lu, Joan C. Krepinsky
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Biomolecules
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Online Access:https://www.mdpi.com/2218-273X/14/11/1444
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author Jackie Trink
Renzhong Li
Bo Gao
Chao Lu
Joan C. Krepinsky
author_facet Jackie Trink
Renzhong Li
Bo Gao
Chao Lu
Joan C. Krepinsky
author_sort Jackie Trink
collection DOAJ
description Up to 40% of patients with diabetes mellitus will develop diabetic kidney disease (DKD), characterized pathologically by the accumulation of extracellular matrix proteins, which leads to the loss of kidney function over time. Our previous studies showed that the pan-protease inhibitor alpha 2-macroglobulin (A2M) is increased in DKD and is a critical regulator of the fibrotic response in glomerular mesangial cells (MC), an initial site of injury during DKD development. How A2M is regulated by high glucose (HG) has not yet been elucidated and is the focus of this investigation. Using serial deletions of the full A2M promoter, we identified the −405 bp region as HG-responsive in MC. Site-directed mutagenesis, siRNA, and ChIP studies showed that the transcription factor, nuclear factor of activated T cells 5 (NFAT5), regulated A2M promoter activity and protein expression in response to HG. Forkhead box P1 (FOXP1) served as a cooperative binding partner for NFAT5, required for A2M upregulation. Lastly, we showed that Smad3, known for its role in kidney fibrosis, regulated A2M promoter activity and protein production independently of HG. The importance of NFAT5, FOXP1, and Smad3 in A2M regulation was confirmed in ex vivo studies using isolated glomeruli. In conclusion, Smad3 is required for basal and HG-induced A2M expression, while NFAT5 and FOXP1 cooperatively regulate increased A2M transcription in response to HG. Inhibition of NFAT5/FOXP1 will be further evaluated as a potential therapeutic strategy to inhibit A2M production and attenuate profibrotic signaling in DKD.
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spelling doaj-art-71fd79983a0b4e98ab9fed316cae4d822025-08-20T02:28:07ZengMDPI AGBiomolecules2218-273X2024-11-011411144410.3390/biom14111444Modulators of Alpha-2 Macroglobulin Upregulation by High Glucose in Glomerular Mesangial CellsJackie Trink0Renzhong Li1Bo Gao2Chao Lu3Joan C. Krepinsky4Division of Nephrology, McMaster University, Hamilton, ON L8N 1Y3, CanadaDivision of Nephrology, McMaster University, Hamilton, ON L8N 1Y3, CanadaDivision of Nephrology, McMaster University, Hamilton, ON L8N 1Y3, CanadaDivision of Nephrology, McMaster University, Hamilton, ON L8N 1Y3, CanadaDivision of Nephrology, McMaster University, Hamilton, ON L8N 1Y3, CanadaUp to 40% of patients with diabetes mellitus will develop diabetic kidney disease (DKD), characterized pathologically by the accumulation of extracellular matrix proteins, which leads to the loss of kidney function over time. Our previous studies showed that the pan-protease inhibitor alpha 2-macroglobulin (A2M) is increased in DKD and is a critical regulator of the fibrotic response in glomerular mesangial cells (MC), an initial site of injury during DKD development. How A2M is regulated by high glucose (HG) has not yet been elucidated and is the focus of this investigation. Using serial deletions of the full A2M promoter, we identified the −405 bp region as HG-responsive in MC. Site-directed mutagenesis, siRNA, and ChIP studies showed that the transcription factor, nuclear factor of activated T cells 5 (NFAT5), regulated A2M promoter activity and protein expression in response to HG. Forkhead box P1 (FOXP1) served as a cooperative binding partner for NFAT5, required for A2M upregulation. Lastly, we showed that Smad3, known for its role in kidney fibrosis, regulated A2M promoter activity and protein production independently of HG. The importance of NFAT5, FOXP1, and Smad3 in A2M regulation was confirmed in ex vivo studies using isolated glomeruli. In conclusion, Smad3 is required for basal and HG-induced A2M expression, while NFAT5 and FOXP1 cooperatively regulate increased A2M transcription in response to HG. Inhibition of NFAT5/FOXP1 will be further evaluated as a potential therapeutic strategy to inhibit A2M production and attenuate profibrotic signaling in DKD.https://www.mdpi.com/2218-273X/14/11/1444alpha 2-macroglobulinpromoterSmad3NFAT5FOXP1diabetic kidney disease
spellingShingle Jackie Trink
Renzhong Li
Bo Gao
Chao Lu
Joan C. Krepinsky
Modulators of Alpha-2 Macroglobulin Upregulation by High Glucose in Glomerular Mesangial Cells
Biomolecules
alpha 2-macroglobulin
promoter
Smad3
NFAT5
FOXP1
diabetic kidney disease
title Modulators of Alpha-2 Macroglobulin Upregulation by High Glucose in Glomerular Mesangial Cells
title_full Modulators of Alpha-2 Macroglobulin Upregulation by High Glucose in Glomerular Mesangial Cells
title_fullStr Modulators of Alpha-2 Macroglobulin Upregulation by High Glucose in Glomerular Mesangial Cells
title_full_unstemmed Modulators of Alpha-2 Macroglobulin Upregulation by High Glucose in Glomerular Mesangial Cells
title_short Modulators of Alpha-2 Macroglobulin Upregulation by High Glucose in Glomerular Mesangial Cells
title_sort modulators of alpha 2 macroglobulin upregulation by high glucose in glomerular mesangial cells
topic alpha 2-macroglobulin
promoter
Smad3
NFAT5
FOXP1
diabetic kidney disease
url https://www.mdpi.com/2218-273X/14/11/1444
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