S-glutathiolation impairs phosphoregulation and function of cardiac myosin-binding protein C in human heart failure

FASEB J. 2016 May;30(5):1849-64. doi: 10.1096/fj.201500048. Epub 2016 Feb 2.

Abstract

Cardiac myosin-binding protein C (cMyBP-C) regulates actin-myosin interaction and thereby cardiac myocyte contraction and relaxation. This physiologic function is regulated by cMyBP-C phosphorylation. In our study, reduced site-specific cMyBP-C phosphorylation coincided with increased S-glutathiolation in ventricular tissue from patients with dilated or ischemic cardiomyopathy compared to nonfailing donors. We used redox proteomics, to identify constitutive and disease-specific S-glutathiolation sites in cMyBP-C in donor and patient samples, respectively. Among those, a cysteine cluster in the vicinity of the regulatory phosphorylation sites within the myosin S2 interaction domain C1-M-C2 was identified and showed enhanced S-glutathiolation in patients. In vitro S-glutathiolation of recombinant cMyBP-C C1-M-C2 occurred predominantly at Cys(249), which attenuated phosphorylation by protein kinases. Exposure to glutathione disulfide induced cMyBP-C S-glutathiolation, which functionally decelerated the kinetics of Ca(2+)-activated force development in ventricular myocytes from wild-type, but not those from Mybpc3-targeted knockout mice. These oxidation events abrogate protein kinase-mediated phosphorylation of cMyBP-C and therefore potentially contribute to the reduction of its phosphorylation and the contractile dysfunction observed in human heart failure.-Stathopoulou, K., Wittig, I., Heidler, J., Piasecki, A., Richter, F., Diering, S., van der Velden, J., Buck, F., Donzelli, S., Schröder, E., Wijnker, P. J. M., Voigt, N., Dobrev, D., Sadayappan, S., Eschenhagen, T., Carrier, L., Eaton, P., Cuello, F. S-glutathiolation impairs phosphoregulation and function of cardiac myosin-binding protein C in human heart failure.

Keywords: cardiac disease; contractile function; cross-bridge cycling; post-translational modifications; redox proteomics.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Adult
  • Animals
  • Cardiovascular Agents / therapeutic use
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Female
  • Gene Expression Regulation / physiology*
  • Glutathione / metabolism*
  • Heart Failure / drug therapy
  • Heart Failure / metabolism*
  • Heart Ventricles / metabolism
  • Humans
  • Male
  • Mice
  • Mice, Knockout
  • Middle Aged
  • Oxidation-Reduction
  • Phosphorylation
  • Young Adult

Substances

  • Cardiovascular Agents
  • Carrier Proteins
  • myosin-binding protein C
  • Glutathione