Evolution of translational control and the emergence of genes and open reading frames in human and non-human primate hearts.

Ruiz-Orera, Jorge; Mbebi, Jeanne; Genehr, Carolin; Schrade, Lisa; Liang, Ning; Hildebrandt, Thomas B; Hübner, Norbert; Zimmermann, Wolfram H; Diecke, Sebastian; Miller, Duncan C; Hummel, Oliver; Kondova, Ivanela; Greiner, Johannes; Blachut, Susanne; Grammatikaki, Aliki; Dewani, Nikita; van Heesch, Sebastiaan; Muecke, Michael B; Adami, Eleonora; Fritsch, Guido; Patone, Giannino; Myronova, Anna

doi:10.1038/s44161-024-00544-7

Journal Article

DZNE-2024-01228

Evolution of translational control and the emergence of genes and open reading frames in human and non-human primate hearts.

Ruiz-Orera, J. ; Miller, D. C. ; Greiner, J. ; Genehr, C. ; Grammatikaki, A. ; Blachut, S. ; Mbebi, J. ; Patone, G. ; Myronova, A. ; Adami, E. ; Dewani, N. ; Liang, N. ; Hummel, O. ; Muecke, M. B. ; Hildebrandt, T. B. ; Fritsch, G. ; Schrade, L. ; Zimmermann, W. H.DZNE* ; Kondova, I. ; Diecke, S. ; van Heesch, S. ; Hübner, N.

2024
Nature Publishing Group UK London

Nature cardiovascular research 3(10), 1217 - 1235 (2024) [10.1038/s44161-024-00544-7]

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Please use a persistent id in citations: doi:10.1038/s44161-024-00544-7

Abstract: Evolutionary innovations can be driven by changes in the rates of RNA translation and the emergence of new genes and small open reading frames (sORFs). In this study, we characterized the transcriptional and translational landscape of the hearts of four primate and two rodent species through integrative ribosome and transcriptomic profiling, including adult left ventricle tissues and induced pluripotent stem cell-derived cardiomyocyte cell cultures. We show here that the translational efficiencies of subunits of the mitochondrial oxidative phosphorylation chain complexes IV and V evolved rapidly across mammalian evolution. Moreover, we discovered hundreds of species-specific and lineage-specific genomic innovations that emerged during primate evolution in the heart, including 551 genes, 504 sORFs and 76 evolutionarily conserved genes displaying human-specific cardiac-enriched expression. Overall, our work describes the evolutionary processes and mechanisms that have shaped cardiac transcription and translation in recent primate evolution and sheds light on how these can contribute to cardiac development and disease.

Keyword(s): Animals (MeSH) ; Humans (MeSH) ; Open Reading Frames: genetics (MeSH) ; Protein Biosynthesis: genetics (MeSH) ; Evolution, Molecular (MeSH) ; Myocytes, Cardiac: metabolism (MeSH) ; Species Specificity (MeSH) ; Transcriptome (MeSH) ; Gene Expression Profiling: methods (MeSH) ; Induced Pluripotent Stem Cells: metabolism (MeSH) ; Ribosomes: metabolism (MeSH) ; Ribosomes: genetics (MeSH) ; Primates: genetics (MeSH) ; Cells, Cultured (MeSH)