Variants in TRIM55, encoding a myogenic ubiquitin ligase, have been associated with hypertrophic cardiomyopathy (HCM), but the underlying disease mechanism is still unknown, limiting the identification of novel therapeutic interventions.
Aims: This study aims to dissect the molecular function of TRIM55 in cardiomyocytes and to understand how TRIM55 contributes to HCM pathogenesis.
Methods: TRIM55 Knockout (KO) and TRIM55 reporter human induced pluripotent stem cell (hiPSC) lines were generated and differentiated into cardiomyocytes. Full proteome, TRIM55 interactome and cardiac ubiquitinome mass spectrometry analysis, as well as bulk RNA sequencing was performed. Calcium handling analysis, live cell imaging and immunofluorescence imaging was carried out in cardiac monolayer, and the functional phenotype was assessed in 3D cardiac organoids.
Results: TRIM55-KO hiPSC-CMs displayed an HCM-like functional phenotype with abnormal calcium handling and, in 3D cardiac organoid, a prolonged relaxation time in comparison to healthy controls. OMICs profiling revealed dysregulation of both structural sarcomeric components and sarcomere regulators in TRIM55-KO hiPSC-CMs, suggesting a regulatory role of TRIM55 in sarcomere formation. Live cell and immunofluorescence imaging showed TRIM55 has a variegated localisation either at the M-band of the sarcomere or more diffuse punctate cytoplasmic localisation. Investigation of the TRIM55 interactome, confirmed the close interaction with the two close family members, TRIM54 and TRIM63. Further, the TRIM55-dependant ubiquitinome contains 515 proteins, including sarcomeric proteins found at the M-band. These data suggest the HCM phenotype is due to impaired sarcomere protein homeostasis.
Conclusion: Our findings indicate that TRIM55 is vital for cardiac sarcomere maintenance and function.