Ninjurin1 regulates striated muscle growth and differentiation

PLoS One. 2019 May 15;14(5):e0216987. doi: 10.1371/journal.pone.0216987. eCollection 2019.

Abstract

Chronic pressure overload due to aortic valve stenosis leads to pathological cardiac hypertrophy and heart failure. Hypertrophy is accompanied by an increase in myocyte surface area, which requires a proportional increase in the number of cell-cell and cell-matrix contacts to withstand enhanced workload. In a proteomic analysis we identified nerve injury-induced protein 1 (Ninjurin1), a 16kDa transmembrane cell-surface protein involved in cell adhesion and nerve repair, to be increased in hypertrophic hearts from patients with aortic stenosis. We hypothesised that Ninjurin1 is involved in myocyte hypertrophy. We analyzed cardiac biopsies from aortic-stenosis patients and control patients undergoing elective heart surgery. We studied cardiac hypertrophy in mice after transverse aortic constriction and angiotensin II infusions, and performed mechanistic analyses in cultured myocytes. We assessed the physiological role of ninjurin1 in zebrafish during heart and skeletal muscle development. Ninjurin1 was increased in hearts of aortic stenosis patients, compared to controls, as well as in hearts from mice with cardiac hypertrophy. Besides the 16kDa Ninjurin1 (Ninjurin1-16) we detected a 24kDa variant of Ninjurin1 (Ninjurin1-24), which was predominantly expressed during myocyte hypertrophy. We disclosed that the higher molecular weight of Ninjurin1-24 was caused by N-glycosylation. Ninjurin1-16 was contained in the cytoplasm of myocytes where it colocalized with stress-fibers. In contrast, Ninjurin1-24 was localized at myocyte membranes. Gain and loss-of-function experiments showed that Ninjurin1-24 plays a role in myocyte hypertrophy and myogenic differentiation in vitro. Reduced levels of ninjurin1 impaired cardiac and skeletal muscle development in zebrafish. We conclude that Ninjurin1 contributes to myocyte growth and differentiation, and that these effects are mainly mediated by N-glycosylated Ninjurin1-24.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aortic Valve Stenosis / genetics*
  • Aortic Valve Stenosis / pathology
  • Cardiomegaly / genetics*
  • Cardiomegaly / pathology
  • Cell Adhesion Molecules, Neuronal / genetics*
  • Cell Differentiation / genetics
  • Disease Models, Animal
  • Female
  • Humans
  • Loss of Function Mutation / genetics
  • Male
  • Mice
  • Muscle Development / genetics
  • Muscle, Striated / growth & development*
  • Muscle, Striated / metabolism
  • Muscle, Striated / pathology
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / pathology
  • Nerve Growth Factors / genetics*
  • Signal Transduction / genetics
  • Zebrafish

Substances

  • Cell Adhesion Molecules, Neuronal
  • NINJ1 protein, human
  • Nerve Growth Factors
  • Ninj1 protein, mouse

Grants and funding

This work was supported by the Deutsche Forschungsgemeinschaft [http://www.dfg.de; grant numbers: FI 965/2-1, FI 965/4-1, FI 965/5-1] to JF, the Marie Curie International Reintegration grant [https://cordis.europa.eu/programme/rcn/7487_de.html; grant number: FP7-PEOPLE-IRG-2008 – 231014; to JF], the Marie Curie Career Integration Grant [https://cordis.europa.eu/programme/rcn/19064_de.html; to DP)], and the Deutsches Zentrum für Herz-Kreislaufforschung, grant number 81Z5400153 to JF. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.