Tcf21 regulates the specification and maturation of proepicardial cells

Tandon, Panna; Miteva, Yana; M., Kuchenbrod, Lauren; Cristea, Ileana M.; Conlon, Frank L.

doi:10.1242/dev.093385

Cited by 73 publications

(87 citation statements)

References 151 publications

(117 reference statements)

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“…5A,B). Consistent with the observation that many of these genes are also expressed in non-muscle and non-cardiac tissues (Amin et al, 2013;Tandon et al, 2013;Fu et al, 1998;Hopwood and Gurdon, 1990;Wong et al, 1994;Newman and Krieg, 1998;della Gaspera et al, 2009;Martin and Harland, 2001), we also observe expression of these genes in the non-bound fraction, albeit at significantly lower levels.…”

Section: Enrichment Of Muscle-specific Nucleisupporting

confidence: 92%

Proteomic profiling of cardiac tissue by isolation of nuclei tagged in specific cell types (INTACT)

Amin

Greco

et al. 2014

Development

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The proper dissection of the molecular mechanisms governing the specification and differentiation of specific cell types requires isolation of pure cell populations from heterogeneous tissues and whole organisms. Here, we describe a method for purification of nuclei from defined cell or tissue types in vertebrate embryos using INTACT (isolation of nuclei tagged in specific cell types). This method, previously developed in plants, flies and worms, utilizes in vivo tagging of the nuclear envelope with biotin and the subsequent affinity purification of the labeled nuclei. In this study we successfully purified nuclei of cardiac and skeletal muscle from Xenopus using this strategy. We went on to demonstrate the utility of this approach by coupling the INTACT approach with liquid chromatography-tandem mass spectrometry (LC-MS/MS) proteomic methodologies to profile proteins expressed in the nuclei of developing hearts. From these studies we have identified the Xenopus orthologs of 12 human proteins encoded by genes, which when mutated in human lead to congenital heart disease. Thus, by combining these technologies we are able to identify tissue-specific proteins that are expressed and required for normal vertebrate organ development.

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Section: Enrichment Of Muscle-specific Nucleisupporting

confidence: 92%

Proteomic profiling of cardiac tissue by isolation of nuclei tagged in specific cell types (INTACT)

Amin

Greco

et al. 2014

Development

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“…1K-N, Fig. S3; Tandon et al, 2013). Consistently, we observed a dramatic restriction of lhx9-α expression to the right side of the septum transversum (stages 39-46) (Fig.…”

Section: Introductionsupporting

confidence: 82%

“…We previously reported lhx9 and itga4 are co-regulated in response to loss of the epicardial transcription factor Tcf21 (Tandon et al, 2013). Based on these observations we hypothesized that Lhx9 acts upstream of itga4 to correctly position the PEO.…”

Section: Lhx9 Is Required For Proepicardial Clustering Through An Intmentioning

confidence: 88%

“…1D,N, Fig. S3; Tandon et al, 2013). An identical pattern of expression was obtained with an independent probe recognizing the LIM domains of lhx9-α and lhx9-HD (Fig.…”

Section: Introductionmentioning

confidence: 98%

“…Many vertebrates show a right side clustering of PE cells during epicardial formation (Virágh et al, 1993;Kálmán et al, 1995;Nahirney et al, 2003;Serluca, 2008;Pombal et al, 2008;Jahr et al, 2008). Recently, we have demonstrated that the LIM homeodomain transcription factor family lhx9 is transiently expressed in the Xenopus PEO (Tandon et al, 2013). We therefore conducted a detailed analysis to establish the relationship between Lhx9 expression and formation of the PEO on the septum transversum.…”

Section: Introductionmentioning

confidence: 99%

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The Lhx9-Integrin pathway is essential for positioning of the proepicardial organ

Tandon¹,

Wilczewski²,

Williams³

et al. 2016

Development

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The development of the vertebrate embryonic heart occurs by hyperplastic growth as well as the incorporation of cells from tissues outside of the initial heart field. Amongst these tissues is the epicardium, a cell structure that develops from the precursor proepicardial organ on the right side of the septum transversum caudal to the developing heart. During embryogenesis, cells of the proepicardial organ migrate, adhere and envelop the maturing heart, forming the epicardium. The cells of the epicardium then delaminate and incorporate into the heart giving rise to cardiac derivatives, including smooth muscle cells and cardiac fibroblasts. Here, we demonstrate that the LIM homeodomain protein Lhx9 is transiently expressed in Xenopus proepicardial cells and is essential for the position of the proepicardial organ on the septum transversum. Utilizing a small-molecule screen, we found that Lhx9 acts upstream of integrin-paxillin signaling and consistently demonstrate that either loss of Lhx9 or disruption of the integrin-paxillin pathway results in mis-positioning of the proepicardial organ and aberrant deposition of extracellular matrix proteins. This leads to a failure of proepicardial cell migration and adhesion to the heart, and eventual death of the embryo. Collectively, these studies establish a requirement for the Lhx9-integrin-paxillin pathway in proepicardial organ positioning and epicardial formation.

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Proepicardium: Current Understanding of its Structure, Induction, and Fate

Niderla-Bielińska

Jankowska‐Steifer

Flaht-Zabost

et al. 2018

The Anatomical Record

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The proepicardium (PE) is a transitory extracardiac embryonic structure which plays a crucial role in cardiac morphogenesis and delivers various cell lineages to the developing heart. The PE arises from the lateral plate mesoderm (LPM) and is present in all vertebrate species. During development, mesothelial cells of the PE reach the naked myocardium either as free‐floating aggregates in the form of vesicles or via a tissue bridge; subsequently, they attach to the myocardium and, finally, form the third layer of a mature heart—the epicardium. After undergoing epithelial‐to‐mesenchymal transition (EMT) some of the epicardial cells migrate into the myocardial wall and differentiate into fibroblasts, smooth muscle cells, and possibly other cell types. Despite many recent findings, the molecular pathways that control not only proepicardial induction and differentiation but also epicardial formation and epicardial cell fate are poorly understood. Knowledge about these events is essential because molecular mechanisms that occur during embryonic development have been shown to be reactivated in pathological conditions, for example, after myocardial infarction, during hypertensive heart disease or other cardiovascular diseases. Therefore, in this review we intended to summarize the current knowledge about PE formation and structure, as well as proepicardial cell fate in animals commonly used as models for studies on heart development. Anat Rec, 302:893–903, 2019. © 2018 Wiley Periodicals, Inc.

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Tcf21 regulates the specification and maturation of proepicardial cells

Cited by 73 publications

References 151 publications

Proteomic profiling of cardiac tissue by isolation of nuclei tagged in specific cell types (INTACT)

Proteomic profiling of cardiac tissue by isolation of nuclei tagged in specific cell types (INTACT)

The Lhx9-Integrin pathway is essential for positioning of the proepicardial organ

Proepicardium: Current Understanding of its Structure, Induction, and Fate

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