Impact of Diabetes on Cardiomyocyte Stiffness and Beta-Adrenergic Pathways in Heart Failure with Normal LVEF

https://doi.org/10.1007/s00392-024-02526-y

Heidi Budde (Bochum)1, S. Delalat (Bochum)1, I. Sultana (Bochum)1, S. Zhazykbayeva (Bochum)1, M. Herwig (Bochum)1, H. Osman (Bochum)1, M. Begovic (Bochum)1, A. Mügge (Bochum)1, I. El-Battrawy (Bochum)1, L. van Heerebeek (AC Amsterdam)2, N. Hamdani (Bochum)1

1Abteilung für Zelluläre und Translationale Physiologie, Molekulare und Experimentelle Kardiologie, Institut für Physiologie, Institut für Forschung und Lehre (IFL), Ruhr-Universität Bochum, Bochum Bochum, Deutschland; 2Onze Lieve Vrouw Gasthuis Amsterdam Department of Cardiology AC Amsterdam, Niederlande

 

Background: Excessive diastolic left ventricular (LV) stiffness is a major contributor to heart failure in patients with diabetes mellitus. Diabetes increases stiffness by promoting collagen deposition in the myocardium and raising passive stiffness of cardiomyocytes, particularly in heart failure with preserved ejection fraction (HFpEF). This study examines the role of cardiomyocyte passive stiffness and alterations in beta-adrenergic (Beta-AR) pathways in diabetic heart failure patients with normal left ventricular ejection fraction (LVEF) compared to non-failing control tissue.

Methods and Results: Endomyocardial biopsy samples were obtained from 30 patients with normal LVEF (>50%), all of whom did not have coronary artery disease. Sixteen patients had diabetes mellitus. The biopsy samples were analyzed to assess cardiomyocyte function and beta-adrenergic pathway components. Diabetic heart failure patients displayed higher diastolic LV stiffness regardless of LVEF. Diabetes increased cardiomyocyte passive stiffness, calcium sensitivity, and reduced maximal generated force. These changes were reversible with protein kinase A (PKA) treatment. PKA activity was diminished in diabetic HFpEF compared to non-diabetic HFpEF. Furthermore, the levels of Beta1-AR, Beta2-AR, G protein-coupled receptor kinase 2 (GRK2), and GRK5 were lower in diabetic HFpEF compared to non-diabetic HFpEF and controls. G-stimulatory (Gs) protein expression was elevated, while G-inhibitory (Gi) protein expression was reduced in diabetic HFpEF compared to non-diabetic HFpEF and controls. These changes were associated with decreased phosphorylation of myofilament proteins (myosin light chain, troponin I, myosin binding protein C, and titin) and calcium-handling proteins (phospholamban, SERCA2a, and the ryanodine receptor), along with disrupted kinase activities involved in their phosphorylation.

Conclusion: Diabetic heart failure patients with normal LVEF exhibit significant increases in diastolic LV stiffness due to enhanced cardiomyocyte passive stiffness and altered beta-adrenergic signaling. These changes are a result of reduced PKA activity and dysregulated phosphorylation of myofilament and calcium-handling proteins. Targeting these pathways may hold therapeutic potential for enhancing diastolic function in diabetic HFpEF patients.

 

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