TY - JOUR
T1 - AMPK mediates regulation of glomerular volume and podocyte survival
AU - Banu, Khadija
AU - Lin, Qisheng
AU - Basgen, John M.
AU - Planoutene, Marina
AU - Wei, Chengguo
AU - Reghuvaran, Anand C.
AU - Tian, Xuefei
AU - Shi, Hongmei
AU - Garzon, Felipe
AU - Garzia, Aitor
AU - Chun, Nicholas
AU - Cumpelik, Arun
AU - Santeusanio, Andrew D.
AU - Zhang, Weijia
AU - Das, Bhaskar
AU - Salem, Fadi
AU - Li, Li
AU - Ishibe, Shuta
AU - Cantley, Lloyd G.
AU - Kaufman, Lewis
AU - Lemley, Kevin V.
AU - Ni, Zhaohui
AU - He, John Cijiang
AU - Murphy, Barbara
AU - Menon, Madhav C.
N1 - Publisher Copyright:
Copyright: © 2021, Banu et al.
PY - 2021/10/8
Y1 - 2021/10/8
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85116756303&partnerID=8YFLogxK
U2 - 10.1172/jci.insight.150004
DO - 10.1172/jci.insight.150004
M3 - Article
C2 - 34473647
AN - SCOPUS:85116756303
SN - 2379-3708
VL - 6
JO - JCI insight
JF - JCI insight
IS - 19
M1 - e150004
ER -