The role of Zic transcription factors in regulating hindbrain retinoic acid signaling

Drummond, Danna L; Cheng, Caroline S.; Selland, Lyndsay G.; Hocking, Jennifer C.; Prichard, Lisa; Waskiewicz, Andrew J.

doi:10.1186/1471-213x-13-31

Cited by 18 publications

(13 citation statements)

References 70 publications

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“…Of the known aldh1a genes expressed in early zebrafish development, only aldh1a2 is expressed in pre-hematopoietic posterior mesoderm (Fig 1A–1C; [40–42]). Consequently, to determine if RA regulates zebrafish HSC formation, we generated RA-deficient embryos by injecting embryos with aldh1a2 morpholino (hereafter referred to as aldh1a2 -morphants) [41, 43], or by treating them with Diethylaminobenzaldehyde (DEAB), a competitive inhibitor of aldehyde dehydrogenases including Aldh1a2 [31, 32].…”

Section: Resultsmentioning

confidence: 99%

Somite-Derived Retinoic Acid Regulates Zebrafish Hematopoietic Stem Cell Formation

2016

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Hematopoietic stem cells (HSCs) are multipotent progenitors that generate all vertebrate adult blood lineages. Recent analyses have highlighted the importance of somite-derived signaling factors in regulating HSC specification and emergence from dorsal aorta hemogenic endothelium. However, these factors remain largely uncharacterized. We provide evidence that the vitamin A derivative retinoic acid (RA) functions as an essential regulator of zebrafish HSC formation. Temporal analyses indicate that RA is required for HSC gene expression prior to dorsal aorta formation, at a time when the predominant RA synthesis enzyme, aldh1a2, is strongly expressed within the paraxial mesoderm and somites. Previous research implicated the Cxcl12 chemokine and Notch signaling pathways in HSC formation. Consequently, to understand how RA regulates HSC gene expression, we surveyed the expression of components of these pathways in RA-depleted zebrafish embryos. During somitogenesis, RA-depleted embryos exhibit altered expression of jam1a and jam2a, which potentiate Notch signaling within nascent endothelial cells. RA-depleted embryos also exhibit a severe reduction in the expression of cxcr4a, the predominant Cxcl12b receptor. Furthermore, pharmacological inhibitors of RA synthesis and Cxcr4 signaling act in concert to reduce HSC formation. Our analyses demonstrate that somite-derived RA functions to regulate components of the Notch and Cxcl12 chemokine signaling pathways during HSC formation.

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Section: Resultsmentioning

confidence: 99%

Somite-Derived Retinoic Acid Regulates Zebrafish Hematopoietic Stem Cell Formation

2016

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“…Zic2a and 2b are expressed in the gastrula mesoderm (Drummond et al, 2013; Grinblat and Sive, 2001; Toyama et al, 2004), including the prechordal plate, which induces formation of the hypothalamus in the ventral diencephalon (Mathieu et al, 2002; Pera and Kessel, 1997; Rubenstein et al, 1998). The hypothalamus subsequently becomes an important source of Shh and is required for regionalization of the anterior diencephalon and optic fissure (Shimamura and Rubenstein, 1997; Zhao et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

Zebrafish zic2 controls formation of periocular neural crest and choroid fissure morphogenesis

Sedykh

Yoon

Roberson

et al. 2017

Developmental Biology

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The vertebrate retina develops in close proximity to the forebrain and neural crest-derived cartilages of the face and jaw. Coloboma, a congenital eye malformation, is associated with aberrant forebrain development (holoprosencephaly) and with craniofacial defects (frontonasal dysplasia) in humans, suggesting a critical role for cross-lineage interactions during retinal morphogenesis. ZIC2, a zinc-finger transcription factor, is linked to human holoprosencephaly. We have previously used morpholino assays to show zebrafish zic2 functions in the developing forebrain, retina and craniofacial cartilage. We now report that zebrafish with genetic lesions in zebrafish zic2 orthologs, zic2a and zic2b, develop with retinal coloboma and craniofacial anomalies. We demonstrate a requirement for zic2 in restricting pax2a expression and show evidence that zic2 function limits Hh signaling. RNA-seq transcriptome analysis identified an early requirement for zic2 in periocular neural crest as an activator of alx1, a transcription factor with essential roles in craniofacial and ocular morphogenesis in human and zebrafish. Collectively, these data establish zic2 mutant zebrafish as a powerful new genetic model for in-depth dissection of cell interactions and genetic controls during craniofacial complex development.

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“…Categories of a cell type that was positive for a given element are color-coded, with a GFP-expressing cell. 22,23 Therefore, the extended version of CNE12030 was shown to drive expression in the habenula, which coincided with the zic3 expression domain. The percentage of GFPexpressing embryos per CNE is indicated beneath each schematic (EE = %).…”

Section: Cne12030 Drives Gfp Expression In the Habenulamentioning

confidence: 89%

“…Moreover, RNA in situ hybridization using an antisense probe against zic3 ( Figure 3N,O) showed that CNE12030 transgene expression coincided with known sites of zic3 expression. 22,23 Therefore, the extended version of CNE12030 was shown to drive expression in the habenula, which coincided with the zic3 expression domain.…”

Section: Cne12030 Drives Gfp Expression In the Habenulamentioning

confidence: 89%

A novel conserved enhancer at zebrafish zic3 and zic6 loci drives neural expression

Minhas

Paterek

Łapiński

et al. 2019

Developmental Dynamics

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Background Identifying enhancers and deciphering their putative roles represent a major step to better understand the mechanism of metazoan gene regulation, development, and the role of regulatory elements in disease. Comparative genomics and transgenic assays have been used with some success to identify critical regions that are involved in regulating the spatiotemporal expression of genes during embryogenesis. Results We identified two novel tetrapod‐teleost conserved noncoding elements within the vicinity of the zic3 and zic6 loci in the zebrafish genome and demonstrated their ability to drive tissue‐specific expression in a transgenic zebrafish assay. The syntenic analysis and robust green fluorescent expression in the developing habenula in the stable transgenic line were correlated with known sites of endogenous zic3 and zic6 expression. Conclusion This transgenic line that expresses green fluorescent protein in the habenula is a valuable resource for studying a specific population of cells in the zebrafish central nervous system. Our observations indicate that a genomic sequence that is conserved between humans and zebrafish acts as an enhancer that likely controls zic3 and zic6 expression.

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The role of Zic transcription factors in regulating hindbrain retinoic acid signaling

Cited by 18 publications

References 70 publications

Somite-Derived Retinoic Acid Regulates Zebrafish Hematopoietic Stem Cell Formation

Somite-Derived Retinoic Acid Regulates Zebrafish Hematopoietic Stem Cell Formation

Zebrafish zic2 controls formation of periocular neural crest and choroid fissure morphogenesis

A novel conserved enhancer at zebrafish zic3 and zic6 loci drives neural expression

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