SGLT2 inhibition protects kidney function by SAM-dependent epigenetic repression of inflammatory genes under metabolic stress.
Hiroshi Maekawa, Yalu Zhou, Yuki Aoi, Margaret E Fain, Dorian S Kaminski, Hyewon Kong, Zachary L Sebo, Ram P Chakrabarty, Benjamin C Howard, Grant Andersen, Biliana Marcheva, Peng Gao, Pinelopi Kapitsinou, Joseph Bass, Ali Shilatifard
Abstract
Open AccessClinically, blockade of renal glucose resorption by sodium-glucose cotransporter 2 (SGLT2) inhibitors slows progression of kidney disease, yet the underlying mechanisms are not fully understood. We hypothesized that altered renal metabolites underlie observed kidney protection when SGLT2 function is lost. S-adenosylmethionine (SAM) levels were increased in kidneys from mice lacking SGLT2 function on a diabetogenic high-fat diet (SPHFD) compared with WT mice fed HFD. Elevated SAM in SPHFD was associated with improved kidney function and decreased expression of NF-κB pathway-related genes. Injured proximal tubular cells that emerged under HFD conditions in WT mice and humans consistently showed reduction in expression of the SAM synthetase Mat2a/MAT2A, while MAT2A inhibition, which reduces SAM production, abrogated kidney protection in SPHFD mice. Histone H3 lysine 27 (H3K27) repressive trimethylation of NF-κB-related genes was increased in SPHFD, consistent with SAM's role as a methyl donor. Our data support a model whereby SGLT2 loss enhances SAM levels within the kidney, leading to epigenetic repression of inflammatory genes and kidney protection under metabolic stress.