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Single cell expression analysis reveals anatomical and cell cycle-dependent transcriptional shifts during heart development.

ABSTRACT: The heart is a complex organ composed of multiple cell and tissue types. Cardiac cells from different regions of the growing embryonic heart exhibit distinct patterns of gene expression, which are thought to contribute to heart development and morphogenesis. Single cell RNA sequencing allows genome-wide analysis of gene expression at the single cell level. Here, we have analyzed cardiac cells derived from early stage developing hearts by single cell RNA-seq and identified cell cycle gene expression as a major determinant of transcriptional variation. Within cell cycle stage-matched CMs from a given heart chamber, we found that CMs in the G2/M phase downregulated sarcomeric and cytoskeletal markers. We also identified cell location-specific signaling molecules that may influence the proliferation of other nearby cell types. Our data highlight how variations in cell cycle activity selectively promote cardiac chamber growth during development, reveal profound chamber-specific cell cycle-linked transcriptional shifts, and open the way to deeper understanding of pathogenesis of congenital heart disease.

SUBMITTER: Li G

PROVIDER: S-EPMC6602356 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Single cell expression analysis reveals anatomical and cell cycle-dependent transcriptional shifts during heart development.

Li Guang G Tian Lei L Goodyer William W Kort Eric J EJ Buikema Jan W JW Xu Adele A Wu Joseph C JC Jovinge Stefan S Wu Sean M SM

Development (Cambridge, England) 20190614 12

The heart is a complex organ composed of multiple cell and tissue types. Cardiac cells from different regions of the growing embryonic heart exhibit distinct patterns of gene expression, which are thought to contribute to heart development and morphogenesis. Single cell RNA sequencing allows genome-wide analysis of gene expression at the single cell level. Here, we have analyzed cardiac cells derived from early stage developing hearts by single cell RNA-seq and identified cell cycle gene express ...[more]

PMID: 31142541

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Project description:The heart is a complex organ composed of multiple cell and tissue types. During early developmental stages, heart cells from different regions of the heart exhibit different patterns of gene expression, which are thought to significantly contribute to heart development and morphogenesis. Until recently, the lack of adequate tools prevented our ability to systematically profile gene expression in a cell type and anatomically-specific manner during heart development. Single cell RNA sequencing has emerged as a powerful approach that allows genome-wide analysis of gene expression in single cells. Using microfluidic-chip and droplet-based single-cell RNA sequencing platforms, we analyze cardiac cells during the early stages of heart development. We found, by principle component analysis, that the expression of cell cycle genes represents a major determinant of transcriptional variation in all analyzed cardiac cell types. Interestingly, when single cardiomyocytes (CMs) from different heart chambers were analyzed, we found that atrial ventricular canal derived CMs have reduced cell cycle activity compare with CMs from the left and right ventricular chambers. In addition, CMs in the trabecular myocardium exhibit reduced cell cycle activity than CMs in the compact myocardium. When CMs within the same chamber were segregated by their cell cycle phase, we found that CMs in the G2/M phase downregulate their sarcomeric and cytoskeletal markers. Finally, we revealed the expression of a signaling ligand from the endocardium that may repress trabecular CM proliferation, and an epicardial-derived ligand that can promote compact CM proliferation. Together these data highlight the variations in cell cycle activity to selectively promote cardiac chamber growth during development and the profound transcriptional shift within the same cell at different phases of cell cycle. Identifying alterations in the expression of key signaling molecules that drive CM proliferation may lead to greater understanding of the onset or progression of congenital heart disease.

Dataset Information

Single cell expression analysis reveals anatomical and cell cycle-dependent transcriptional shifts during heart development.

Publications

Single cell expression analysis reveals anatomical and cell cycle-dependent transcriptional shifts during heart development.

Similar Datasets

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