The cardiomyocyte origins of diastolic dysfunction: cellular components of myocardial "stiffness"

Am J Physiol Heart Circ Physiol. 2024 Mar 1;326(3):H584-H598. doi: 10.1152/ajpheart.00334.2023. Epub 2024 Jan 5.

Abstract

The impaired ability of the heart to relax and stretch to accommodate venous return is generally understood to represent a state of "diastolic dysfunction" and often described using the all-purpose noun "stiffness." Despite the now common qualitative usage of this term in fields of cardiac patho/physiology, the specific quantitative concept of stiffness as a molecular and biophysical entity with real practical interpretation in healthy and diseased hearts is sometimes obscure. The focus of this review is to characterize the concept of cardiomyocyte stiffness and to develop interpretation of "stiffness" attributes at the cellular and molecular levels. Here, we consider "stiffness"-related terminology interpretation and make links between cardiomyocyte stiffness and aspects of functional and structural cardiac performance. We discuss cross bridge-derived stiffness sources, considering the contributions of diastolic myofilament activation and impaired relaxation. This includes commentary relating to the role of cardiomyocyte Ca2+ flux and Ca2+ levels in diastole, the troponin-tropomyosin complex role as a Ca2+ effector in diastole, the myosin ADP dissociation rate as a modulator of cross bridge attachment and regulation of cross-bridge attachment by myosin binding protein C. We also discuss non-cross bridge-derived stiffness sources, including the titin sarcomeric spring protein, microtubule and intermediate filaments, and cytoskeletal extracellular matrix interactions. As the prevalence of conditions involving diastolic heart failure has escalated, a more sophisticated understanding of the molecular, cellular, and tissue determinants of cardiomyocyte stiffness offers potential to develop imaging and molecular intervention tools.

Keywords: cardiac compliance; cardiomyocyte; diastolic dysfunction; myocardial stiffness; myofilament posttranslational modifications.

Publication types

  • Review

MeSH terms

  • Cardiomyopathies*
  • Connectin
  • Diastole / physiology
  • Humans
  • Myocardium
  • Myocytes, Cardiac* / physiology
  • Myofibrils
  • Myosins

Substances

  • Myosins
  • Connectin