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AMPK mediates regulation of glomerular volume and podocyte survival

Herein, we report that Shroom3 knockdown, via Fyn inhibition, induced albuminuria with foot process effacement (FPE) without focal segmental glomerulosclerosis (FSGS) or podocytopenia. Interestingly, knockdown mice had reduced podocyte volumes. Human minimal change disease (MCD), where podocyte Fyn...

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Autores principales: Banu, Khadija, Lin, Qisheng, Basgen, John M., Planoutene, Marina, Wei, Chengguo, Reghuvaran, Anand C., Tian, Xuefei, Shi, Hongmei, Garzon, Felipe, Garzia, Aitor, Chun, Nicholas, Cumpelik, Arun, Santeusanio, Andrew D., Zhang, Weijia, Das, Bhaskar, Salem, Fadi, Li, Li, Ishibe, Shuta, Cantley, Lloyd G., Kaufman, Lewis, Lemley, Kevin V., Ni, Zhaohui, He, John Cijiang, Murphy, Barbara, Menon, Madhav C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Clinical Investigation 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8525649/
https://www.ncbi.nlm.nih.gov/pubmed/34473647
http://dx.doi.org/10.1172/jci.insight.150004
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author Banu, Khadija
Lin, Qisheng
Basgen, John M.
Planoutene, Marina
Wei, Chengguo
Reghuvaran, Anand C.
Tian, Xuefei
Shi, Hongmei
Garzon, Felipe
Garzia, Aitor
Chun, Nicholas
Cumpelik, Arun
Santeusanio, Andrew D.
Zhang, Weijia
Das, Bhaskar
Salem, Fadi
Li, Li
Ishibe, Shuta
Cantley, Lloyd G.
Kaufman, Lewis
Lemley, Kevin V.
Ni, Zhaohui
He, John Cijiang
Murphy, Barbara
Menon, Madhav C.
author_facet Banu, Khadija
Lin, Qisheng
Basgen, John M.
Planoutene, Marina
Wei, Chengguo
Reghuvaran, Anand C.
Tian, Xuefei
Shi, Hongmei
Garzon, Felipe
Garzia, Aitor
Chun, Nicholas
Cumpelik, Arun
Santeusanio, Andrew D.
Zhang, Weijia
Das, Bhaskar
Salem, Fadi
Li, Li
Ishibe, Shuta
Cantley, Lloyd G.
Kaufman, Lewis
Lemley, Kevin V.
Ni, Zhaohui
He, John Cijiang
Murphy, Barbara
Menon, Madhav C.
author_sort Banu, Khadija
collection PubMed
description Herein, we report that Shroom3 knockdown, via Fyn inhibition, induced albuminuria with foot process effacement (FPE) without focal segmental glomerulosclerosis (FSGS) or podocytopenia. Interestingly, knockdown mice had reduced podocyte volumes. Human minimal change disease (MCD), where podocyte Fyn inactivation was reported, also showed lower glomerular volumes than FSGS. We hypothesized that lower glomerular volume prevented the progression to podocytopenia. To test this hypothesis, we utilized unilateral and 5/6th nephrectomy models in Shroom3-KD mice. Knockdown mice exhibited less glomerular and podocyte hypertrophy after nephrectomy. FYN-knockdown podocytes had similar reductions in podocyte volume, implying that Fyn was downstream of Shroom3. Using SHROOM3 or FYN knockdown, we confirmed reduced podocyte protein content, along with significantly increased phosphorylated AMPK, a negative regulator of anabolism. AMPK activation resulted from increased cytoplasmic redistribution of LKB1 in podocytes. Inhibition of AMPK abolished the reduction in glomerular volume and induced podocytopenia in mice with FPE, suggesting a protective role for AMPK activation. In agreement with this, treatment of glomerular injury models with AMPK activators restricted glomerular volume, podocytopenia, and progression to FSGS. Glomerular transcriptomes from MCD biopsies also showed significant enrichment of Fyn inactivation and Ampk activation versus FSGS glomeruli. In summary, we demonstrated the important role of AMPK in glomerular volume regulation and podocyte survival. Our data suggest that AMPK activation adaptively regulates glomerular volume to prevent podocytopenia in the context of podocyte injury.
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spelling pubmed-85256492021-10-26 AMPK mediates regulation of glomerular volume and podocyte survival Banu, Khadija Lin, Qisheng Basgen, John M. Planoutene, Marina Wei, Chengguo Reghuvaran, Anand C. Tian, Xuefei Shi, Hongmei Garzon, Felipe Garzia, Aitor Chun, Nicholas Cumpelik, Arun Santeusanio, Andrew D. Zhang, Weijia Das, Bhaskar Salem, Fadi Li, Li Ishibe, Shuta Cantley, Lloyd G. Kaufman, Lewis Lemley, Kevin V. Ni, Zhaohui He, John Cijiang Murphy, Barbara Menon, Madhav C. JCI Insight Research Article Herein, we report that Shroom3 knockdown, via Fyn inhibition, induced albuminuria with foot process effacement (FPE) without focal segmental glomerulosclerosis (FSGS) or podocytopenia. Interestingly, knockdown mice had reduced podocyte volumes. Human minimal change disease (MCD), where podocyte Fyn inactivation was reported, also showed lower glomerular volumes than FSGS. We hypothesized that lower glomerular volume prevented the progression to podocytopenia. To test this hypothesis, we utilized unilateral and 5/6th nephrectomy models in Shroom3-KD mice. Knockdown mice exhibited less glomerular and podocyte hypertrophy after nephrectomy. FYN-knockdown podocytes had similar reductions in podocyte volume, implying that Fyn was downstream of Shroom3. Using SHROOM3 or FYN knockdown, we confirmed reduced podocyte protein content, along with significantly increased phosphorylated AMPK, a negative regulator of anabolism. AMPK activation resulted from increased cytoplasmic redistribution of LKB1 in podocytes. Inhibition of AMPK abolished the reduction in glomerular volume and induced podocytopenia in mice with FPE, suggesting a protective role for AMPK activation. In agreement with this, treatment of glomerular injury models with AMPK activators restricted glomerular volume, podocytopenia, and progression to FSGS. Glomerular transcriptomes from MCD biopsies also showed significant enrichment of Fyn inactivation and Ampk activation versus FSGS glomeruli. In summary, we demonstrated the important role of AMPK in glomerular volume regulation and podocyte survival. Our data suggest that AMPK activation adaptively regulates glomerular volume to prevent podocytopenia in the context of podocyte injury. American Society for Clinical Investigation 2021-10-08 /pmc/articles/PMC8525649/ /pubmed/34473647 http://dx.doi.org/10.1172/jci.insight.150004 Text en © 2021 Banu et al. https://creativecommons.org/licenses/by/4.0/This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Banu, Khadija
Lin, Qisheng
Basgen, John M.
Planoutene, Marina
Wei, Chengguo
Reghuvaran, Anand C.
Tian, Xuefei
Shi, Hongmei
Garzon, Felipe
Garzia, Aitor
Chun, Nicholas
Cumpelik, Arun
Santeusanio, Andrew D.
Zhang, Weijia
Das, Bhaskar
Salem, Fadi
Li, Li
Ishibe, Shuta
Cantley, Lloyd G.
Kaufman, Lewis
Lemley, Kevin V.
Ni, Zhaohui
He, John Cijiang
Murphy, Barbara
Menon, Madhav C.
AMPK mediates regulation of glomerular volume and podocyte survival
title AMPK mediates regulation of glomerular volume and podocyte survival
title_full AMPK mediates regulation of glomerular volume and podocyte survival
title_fullStr AMPK mediates regulation of glomerular volume and podocyte survival
title_full_unstemmed AMPK mediates regulation of glomerular volume and podocyte survival
title_short AMPK mediates regulation of glomerular volume and podocyte survival
title_sort ampk mediates regulation of glomerular volume and podocyte survival
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8525649/
https://www.ncbi.nlm.nih.gov/pubmed/34473647
http://dx.doi.org/10.1172/jci.insight.150004
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