Extracellular mechanical forces drive endocardial cell volume decrease during zebrafish cardiac valve morphogenesis

Vignes, Hélène; Vagena-Pantoula, Christina; Prakash, Mangal; Fukui, Hajime; Norden, Caren; Mochizuki, Naoki; Jug, Florian; Vermot, Julien

doi:10.1016/j.devcel.2022.02.011

Cited by 31 publications

(17 citation statements)

References 89 publications

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“…The expression of piezo1 and piezo2a are restricted to the AV canal in zebrafish embryos 18 and larvae (our study). Furthermore, other mechanosensor channels, such as Trpv4, show enrichment in the AV region 50 . Therefore, it would be interesting to generate fluorescent fusion lines of the mechanosensors essential for cardiac valve formation in order to track their trafficking within endocardial cells and study the signals required for their activation 51 .…”

Section: Discussionmentioning

confidence: 99%

Multiple pkd and piezo gene family members are required for atrioventricular valve formation

et al. 2023

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Cardiac valves ensure unidirectional blood flow through the heart, and altering their function can result in heart failure. Flow sensing via wall shear stress and wall stretching through the action of mechanosensors can modulate cardiac valve formation. However, the identity and precise role of the key mechanosensors and their effectors remain mostly unknown. Here, we genetically dissect the role of Pkd1a and other mechanosensors in atrioventricular (AV) valve formation in zebrafish and identify a role for several pkd and piezo gene family members in this process. We show that Pkd1a, together with Pkd2, Pkd1l1, and Piezo2a, promotes AV valve elongation and cardiac morphogenesis. Mechanistically, Pkd1a, Pkd2, and Pkd1l1 all repress the expression of klf2a and klf2b, transcription factor genes implicated in AV valve development. Furthermore, we find that the calcium-dependent protein kinase Camk2g is required downstream of Pkd function to repress klf2a expression. Altogether, these data identify, and dissect the role of, several mechanosensors required for AV valve formation, thereby broadening our understanding of cardiac valvulogenesis.

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Section: Discussionmentioning

confidence: 99%

Multiple pkd and piezo gene family members are required for atrioventricular valve formation

et al. 2023

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“…This tissue convergence has recently been linked to a global endocardial cell orientation change directed toward the AVC and a cell clustering event that is associated with decreased AVC cell volume. This process was further found to depend on mechanosensitive TRP channels (TRPP2 and TRPV4) and the ECM component hyaluronan [ 128 ].…”

Section: Endocardial Regulation Of Other Cell Types/processesmentioning

confidence: 99%

Endocardial Regulation of Cardiac Development

Feulner

Vliet

Pucéat

et al. 2022

JCDD

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The endocardium is a specialized form of endothelium that lines the inner side of the heart chambers and plays a crucial role in cardiac development. While comparatively less studied than other cardiac cell types, much progress has been made in understanding the regulation of and by the endocardium over the past two decades. In this review, we will summarize what is currently known regarding endocardial origin and development, the relationship between endocardium and other cardiac cell types, and the various lineages that endocardial cells derive from and contribute to. These processes are driven by key molecular mechanisms such as Notch and BMP signaling. These pathways in particular have been well studied, but other signaling pathways and mechanical cues also play important roles. Finally, we will touch on the contribution of stem cell modeling in combination with single cell sequencing and its potential translational impact for congenital heart defects such as bicuspid aortic valves and hypoplastic left heart syndrome. The detailed understanding of cellular and molecular processes in the endocardium will be vital to further develop representative stem cell-derived models for disease modeling and regenerative medicine in the future.

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“…Their ability to trap fluid and swell by osmotic pressure generates mechanical stress to influence the form and function of the tissue microenvironment (Voutouri and Stylianopoulos, 2018). In zebrafish, HA provides anisotropic extracellular stress to guide otic bud morphogenesis (Munjal et al, 2021) or cardiac valve development (Vignes et al, 2022). In murine adenocarcinoma models, administration of hyaluronidase resulted in tumour relaxation, indicating that HA provides tissue compressive resistance (Stylianopoulos et al, 2012;Voutouri and Stylianopoulos, 2018).…”

Section: Interstitial Extracellular Matrixmentioning

confidence: 99%

Squeezing the eggs to grow: The mechanobiology of mammalian folliculogenesis

Biswas

Prabhakaran

et al. 2022

Front. Cell Dev. Biol.

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The formation of functional eggs (oocyte) in ovarian follicles is arguably one of the most important events in early mammalian development since the oocytes provide the bulk genetic and cytoplasmic materials for successful reproduction. While past studies have identified many genes that are critical to normal ovarian development and function, recent studies have highlighted the role of mechanical force in shaping folliculogenesis. In this review, we discuss the underlying mechanobiological principles and the force-generating cellular structures and extracellular matrix that control the various stages of follicle development. We also highlight emerging techniques that allow for the quantification of mechanical interactions and follicular dynamics during development, and propose new directions for future studies in the field. We hope this review will provide a timely and useful framework for future understanding of mechano-signalling pathways in reproductive biology and diseases.

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Extracellular mechanical forces drive endocardial cell volume decrease during zebrafish cardiac valve morphogenesis

Cited by 31 publications

References 89 publications

Multiple pkd and piezo gene family members are required for atrioventricular valve formation

Multiple pkd and piezo gene family members are required for atrioventricular valve formation

Endocardial Regulation of Cardiac Development

Squeezing the eggs to grow: The mechanobiology of mammalian folliculogenesis

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