Off-target effects of sodium-glucose co-transporter 2 blockers: empagliflozin does not inhibit Na+/H+ exchanger-1 or lower [Na+]i in the heart

Cardiovasc Res. 2021 Dec 17;117(14):2794-2806. doi: 10.1093/cvr/cvaa323.

Abstract

Aims: Emipagliflozin (EMPA) is a potent inhibitor of the renal sodium-glucose co-transporter 2 (SGLT2) and an effective treatment for type-2 diabetes. In patients with diabetes and heart failure, EMPA has cardioprotective effects independent of improved glycaemic control, despite SGLT2 not being expressed in the heart. A number of non-canonical mechanisms have been proposed to explain these cardiac effects, most notably an inhibitory action on cardiac Na+/H+ exchanger 1 (NHE1), causing a reduction in intracellular [Na+] ([Na+]i). However, at resting intracellular pH (pHi), NHE1 activity is very low and its pharmacological inhibition is not expected to meaningfully alter steady-state [Na+]i. We re-evaluate this putative EMPA target by measuring cardiac NHE1 activity.

Methods and results: The effect of EMPA on NHE1 activity was tested in isolated rat ventricular cardiomyocytes from measurements of pHi recovery following an ammonium pre-pulse manoeuvre, using cSNARF1 fluorescence imaging. Whereas 10 µM cariporide produced near-complete inhibition, there was no evidence for NHE1 inhibition with EMPA treatment (1, 3, 10, or 30 µM). Intracellular acidification by acetate-superfusion evoked NHE1 activity and raised [Na+]i, reported by sodium binding benzofuran isophthalate (SBFI) fluorescence, but EMPA did not ablate this rise. EMPA (10 µM) also had no significant effect on the rate of cytoplasmic [Na+]i rise upon superfusion of Na+-depleted cells with Na+-containing buffers. In Langendorff-perfused mouse, rat and guinea pig hearts, EMPA did not affect [Na+]i at baseline nor pHi recovery following acute acidosis, as measured by 23Na triple quantum filtered NMR and 31P NMR, respectively.

Conclusions: Our findings indicate that cardiac NHE1 activity is not inhibited by EMPA (or other SGLT2i's) and EMPA has no effect on [Na+]i over a wide range of concentrations, including the therapeutic dose. Thus, the beneficial effects of SGLT2i's in failing hearts should not be interpreted in terms of actions on myocardial NHE1 or intracellular [Na+].

Keywords: Heart failure; Intracellular Na; NMR spectroscopy; Na/H exchanger-1; SGLT2 inhibitor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Benzhydryl Compounds / pharmacology*
  • Glucosides / pharmacology*
  • Guinea Pigs
  • HCT116 Cells
  • HEK293 Cells
  • Humans
  • Hydrogen-Ion Concentration
  • In Vitro Techniques
  • Isolated Heart Preparation
  • Male
  • Membrane Potentials
  • Mice
  • Myocytes, Cardiac / drug effects*
  • Myocytes, Cardiac / metabolism
  • Rats
  • Rats, Wistar
  • Sodium / metabolism*
  • Sodium-Glucose Transporter 2 Inhibitors / pharmacology*
  • Sodium-Hydrogen Exchanger 1 / antagonists & inhibitors*
  • Sodium-Hydrogen Exchanger 1 / metabolism
  • Ventricular Function, Left / drug effects
  • Ventricular Pressure / drug effects

Substances

  • Benzhydryl Compounds
  • Glucosides
  • SLC9A1 protein, human
  • Slc9a1 protein, rat
  • Sodium-Glucose Transporter 2 Inhibitors
  • Sodium-Hydrogen Exchanger 1
  • Sodium
  • empagliflozin