Identification of a retinoic acid‐responsive neural enhancer in the <i>Ciona intestinalis Hox1</i> gene

Kanda, Miyuki; Ikeda, Taku; Fujiwara, Shigeki

doi:10.1111/dgd.12033

Cited by 9 publications

(14 citation statements)

References 55 publications

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“…The conservation of ParaHox gene expression in the CNS allows us to dissect ParaHox regulation in Ciona , as the CNS of Ciona shows clear similarities in gene expression to the wider Chordata, perhaps even the Bilateria [ 66 , 67 ]. In addition, the tunicates also retain many of the signalling pathways involved in Hox and ParaHox regulation, such as RA [ 68 – 70 ], FGF [ 71 – 73 ], BMP [ 74 , 75 ], Wnts [ 76 , 77 ] and hedgehog [ 76 , 78 , 79 ]. By using C. intestinalis , we are able to quickly assess hundreds of embryos at a time, allowing the identification of even weak regulatory elements, e.g.…”

Section: Discussionmentioning

confidence: 99%

TCF/Lef regulates the Gsx ParaHox gene in central nervous system development in chordates

Garstang¹,

Osborne²,

Ferrier³

2016

BMC Evol Biol

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BackgroundThe ParaHox genes play an integral role in the anterior-posterior (A-P) patterning of the nervous system and gut of most animals. The ParaHox cluster is an ideal system in which to study the evolution and regulation of developmental genes and gene clusters, as it displays similar regulatory phenomena to its sister cluster, the Hox cluster, but offers a much simpler system with only three genes.ResultsUsing Ciona intestinalis transgenics, we isolated a regulatory element upstream of Branchiostoma floridae Gsx that drives expression within the central nervous system of Ciona embryos. The minimal amphioxus enhancer region required to drive CNS expression has been identified, along with surrounding sequence that increases the efficiency of reporter expression throughout the Ciona CNS. TCF/Lef binding sites were identified and mutagenized and found to be required to drive the CNS expression. Also, individual contributions of TCF/Lef sites varied across the regulatory region, revealing a partial division of function across the Bf-Gsx-Up regulatory element. Finally, when all TCF/Lef binding sites are mutated CNS expression is not only abolished, but a latent repressive function is also unmasked.ConclusionsWe have identified a B. floridae Gsx upstream regulatory element that drives CNS expression within transgenic Ciona intestinalis, and have shown that this CNS expression is dependent upon TCF/Lef binding sites. We examine the evolutionary and developmental implications of these results, and discuss the possibility of TCF/Lef not only as a regulator of chordate Gsx, but as a deeply conserved regulatory factor controlling all three ParaHox genes across the Metazoa.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0614-3) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

TCF/Lef regulates the Gsx ParaHox gene in central nervous system development in chordates

Garstang¹,

Osborne²,

Ferrier³

2016

BMC Evol Biol

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“…Cis ‐regulatory assays of mouse hindbrain enhancers in Ciona and Ciona Hox regulatory modules in mouse and chick embryos revealed that enhancers dependent upon and capable of reading out input from segmental regulators such as Krox20 and Kreisler are specific to the vertebrate lineage . Hox genes are up‐regulated upon RA treatment in Ciona embryos but RA appears to have a less profound influence on neural Hox expression in tunicates than in vertebrates, which is possibly linked to Hox cluster disintegration …”

Section: Insights From Invertebrate Chordates Into the Evolution Of Tmentioning

confidence: 97%

“…Only a modest number of regulatory elements are identifiable by sequence conservation between tunicates and vertebrates (reviewed in), but comprehensive regulatory surveys of Ciona Hox loci have uncovered a number of enhancer sequences . For example, two enhancers proximal to ci‐Hox1 have been implicated in its neural and ectodermal expression, which contain RAREs that may be homologues of those in amphioxus and vertebrate Hox clusters.…”

Section: Insights From Invertebrate Chordates Into the Evolution Of Tmentioning

confidence: 99%

Segmental arithmetic: summing up the Hox gene regulatory network for hindbrain development in chordates

Parker

Krumlauf

2017

WIREs Developmental Biology

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Organization and development of the early vertebrate hindbrain are controlled by a cascade of regulatory interactions that govern the process of segmentation and patterning along the anterior-posterior axis via Hox genes. These interactions can be assembled into a gene regulatory network that provides a framework to interpret experimental data, generate hypotheses, and identify gaps in our understanding of the progressive process of hindbrain segmentation. The network can be broadly separated into a series of interconnected programs that govern early signaling, segmental subdivision, secondary signaling, segmentation, and ultimately specification of segmental identity. Hox genes play crucial roles in multiple programs within this network. Furthermore, the network reveals properties and principles that are likely to be general to other complex developmental systems. Data from vertebrate and invertebrate chordate models are shedding light on the origin and diversification of the network. Comprehensive cis-regulatory analyses of vertebrate Hox gene regulation have enabled powerful cross-species gene regulatory comparisons. Such an approach in the sea lamprey has revealed that the network mediating segmental Hox expression was present in ancestral vertebrates and has been maintained across diverse vertebrate lineages. Invertebrate chordates lack hindbrain segmentation but exhibit conservation of some aspects of the network, such as a role for retinoic acid in establishing nested Hox expression domains. These comparisons lead to a model in which early vertebrates underwent an elaboration of the network between anterior-posterior patterning and Hox gene expression, leading to the gene-regulatory programs for segmental subdivision and rhombomeric segmentation. WIREs Dev Biol 2017, 6:e286. doi: 10.1002/wdev.286 For further resources related to this article, please visit the WIREs website.

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“…). The identification of RA‐responsive Hox enhancers in a urochordate provides further support for this scenario .…”

Section: Insights Into the Evolution Of The Hindbrain Grn From Invertmentioning

confidence: 99%

The vertebrate Hox gene regulatory network for hindbrain segmentation: Evolution and diversification

2016

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Hindbrain development is orchestrated by a vertebrate gene regulatory network that generates segmental patterning along the anterior-posterior axis via Hox genes. Here, we review analyses of vertebrate and invertebrate chordate models that inform upon the evolutionary origin and diversification of this network. Evidence from the sea lamprey reveals that the hindbrain regulatory network generates rhombomeric compartments with segmental Hox expression and an underlying Hox code. We infer that this basal feature was present in ancestral vertebrates and, as an evolutionarily constrained developmental state, is fundamentally important for patterning of the vertebrate hindbrain across diverse lineages. Despite the common ground plan, vertebrates exhibit neuroanatomical diversity in lineage-specific patterns, with different vertebrates revealing variations of Hox expression in the hindbrain that could underlie this diversification. Invertebrate chordates lack hindbrain segmentation but exhibit some conserved aspects of this network, with retinoic acid signaling playing a role in establishing nested domains of Hox expression.

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Identification of a retinoic acid‐responsive neural enhancer in the Ciona intestinalis Hox1 gene

Cited by 9 publications

References 55 publications

TCF/Lef regulates the Gsx ParaHox gene in central nervous system development in chordates

TCF/Lef regulates the Gsx ParaHox gene in central nervous system development in chordates

Segmental arithmetic: summing up the Hox gene regulatory network for hindbrain development in chordates

The vertebrate Hox gene regulatory network for hindbrain segmentation: Evolution and diversification

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