Dissecting early regulatory relationships in the lamprey neural crest gene network

Nikitina, Natalya; Sauka‐Spengler, Tatjana; Bronner‐Fraser, Marianne

doi:10.1073/pnas.0806009105

Cited by 97 publications

(86 citation statements)

References 33 publications

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“…Logically, programmed death of every cell is not consistent with embryonic development or survival. Moreover, alternate assays for apoptosis do not indicate widespread cell death (19) (Fig. S7 and Fig.…”

Section: Discussionmentioning

confidence: 94%

“…The results presented here suggest that considering the germline genome structure and how somatic changes alter this structure when using lamprey as a model for comparative developmental and genomic studies will be especially important. With ongoing progress toward complete sequencing of the lamprey somatic genome (21) and the recent development of several techniques for performing genetic manipulations of lamprey embryos (17)(18)(19)(20), we anticipate that the lamprey genome will prove fertile ground for identifying mechanisms that mediate the differential development of cell lineages and participate in large-scale rearrangement and stabilization of vertebrate genomes.…”

Section: Discussionmentioning

confidence: 99%

“…Experimentally validated computational screens for other germline-limited sequences uncovered several additional sequences that are lost during developmental restructuring of the lamprey genome, including one sequence that is homologous to SPOPL (speckle-type POZ protein-like) genes, which is transcribed in lamprey testes and lost during embryonic development. The presence of predictable and extensive reorganization events within the genome of the lamprey, coupled with its high fecundity (16) and amenable embryology (17)(18)(19)(20), present a uniquely tractable system for understanding the dynamics of genome stability and the consequences of reorganization in the context of ''normal'' vertebrate development and cell biology.…”

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confidence: 99%

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Programmed loss of millions of base pairs from a vertebrate genome

Smith

Antonacci²,

Eichler³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

151

195

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In general, the strict preservation of broad-scale structure is thought to be critical for maintaining the precisely tuned functionality of vertebrate genomes, although nearly all vertebrate species undergo a small number of programmed local rearrangements during development (e.g., remodeling of adaptive immune receptor loci). However, a limited number of metazoan species undergo much more extensive reorganizations as a normal feature of their development. Here, we show that the sea lamprey (Petromyzon marinus), a jawless vertebrate, undergoes a dramatic remodeling of its genome, resulting in the elimination of hundreds of millions of base pairs (and at least one transcribed locus) from many somatic cell lineages during embryonic development. These studies reveal the highly dynamic nature of the lamprey genome and provide the first example of broad-scale programmed rearrangement of a definitively vertebrate genome. Understanding the mechanisms by which this vertebrate species regulates such extensive remodeling of its genome will provide invaluable insight into factors that can promote stability and change in vertebrate genomes.A few species are known to undergo extensive genomic rearrangements during the specification of different cell lineages [e.g., sciarid flies (1, 2), some copepods (3, 4), and some roundworms (5)] or nuclear lineages [e.g., ciliates (6, 7)] (8). These rearrangements result in the selective removal of repetitive sequences (9-11), entire chromosomes (5), or single-copy genes (12, 13). Notably, only one chordate group (hagfish) is thought to undergo similar large-scale rearrangements and possesses certain repetitive elements in its germline that undergo diminution in somatic tissues, sometimes exhibiting a reduction in chromosome number (9-11). The unique genome biologies of these organisms are fascinating because changes that are tightly regulated in these exceptional genomes are reminiscent of the dysregulated structural changes that give rise to cancers or other genomic disorders (14,15). In this context, developmentally regulated rearrangements hold great potential for studying the factors that promote genome stability and change in normally developing somatic cells and the means by which alterations in genome structure contribute to the differentiation of cell lineages (8).Here, we report new data that reveal extensive programmed genome rearrangement in the sea lamprey, an important model system for studying basal vertebrate biology. Several complementary lines of evidence indicate that hundreds of megabases of DNA are specifically removed from somatic cell lineages. Here, we demonstrate the existence of a specific DNA sequence (called Germ1) that is highly abundant in germline but substantially rarer in many, if not all, somatic tissues. Fluorescence in situ hybridization reveals that Germ1 is present at a high copy number on several chromosomes in meiotic germline but dramatically reduced in soma. Estimates of relative copy number indicate that the loss of Germ1 is tightly regulated an...

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Section: Discussionmentioning

confidence: 94%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

Programmed loss of millions of base pairs from a vertebrate genome

Smith

Antonacci²,

Eichler³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

151

195

View full text Add to dashboard Cite

show abstract

“…30,39 BMP and Wnt/b-Catenin signaling functionally interact with Pax3, Zic1 and Ap2a in later phases to induce bona fide NC fate. 19,30,40,41 Likewise, Wnt/b-Catenin signaling is essential for NPB specification in epiblast explants from chick blastulae, where Wnt activity precedes and upregulates bmp4, 17 as well as for expression of NPB genes in hESCs.…”

Section: Wnt Signalingmentioning

confidence: 99%

Signaling pathways and tissue interactions in neural plate border formation

Schille

Schambony

2017

Neurogenesis

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The neural crest is a transient cell population that gives rise to various cell types of multiple tissues and organs in the vertebrate embryo. Neural crest cells arise from the neural plate border, a region localized at the lateral borders of the prospective neural plate. Temporally and spatially coordinated interaction with the adjacent tissues, the non-neural ectoderm, the neural plate and the prospective dorsolateral mesoderm, is required for neural plate border specification. Signaling molecules, namely BMP, Wnt and FGF ligands and corresponding antagonists are derived from these tissues and interact to induce the expression of neural plate border specific genes. The present mini-review focuses on the current understanding of how the NPB territory is formed and accentuates the need for coordinated interaction of BMP and Wnt signaling pathways and precise tissue communication that are required for the definition of the prospective NC in the competent ectoderm.

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“…Conditional disruption of Smad4 in neural crest cells results in AP2α downregulation from embryonic day 9.5 (E9.5) in mouse embryo [29]. AP2α also regulates neural border specification during the neuralization stage in Xenopus and lamprey [30,31]. Mouse AP2γ is expressed in both extraembryonic and embryonic tissues [32,33] and displays multiple functions in extraembryonic development, neural crest induction and terminal epidermal differentiation [26,34,35].…”

Section: Introductionmentioning

confidence: 99%

AP2γ regulates neural and epidermal development downstream of the BMP pathway at early stages of ectodermal patterning

et al. 2012

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Bone morphogenetic protein (BMP) inhibits neural specification and induces epidermal differentiation during ectodermal patterning. However, the mechanism of this process is not well understood. Here we show that AP2γ, a transcription factor activator protein (AP)-2 family member, is upregulated by BMP4 during neural differentiation of pluripotent stem cells. Knockdown of AP2γ facilitates mouse embryonic stem cell (ESC) neural fate determination and impairs epidermal differentiation, whereas AP2γ overexpression inhibits neural conversion and promotes epidermal commitment. In the early chick embryo, AP2γ is expressed in the entire epiblast before HH stage 3 and gradually shifts to the putative epidermal ectoderm during HH stage 4. In the future neural plate AP2γ inhibits excessive neural expansion and it also promotes epidermal development in the surface ectoderm. Moreover, AP2γ knockdown in ESCs and chick embryos partially rescued the neural inhibition and epidermal induction effects of BMP4. Mechanistic studies showed that BMP4 directly regulates AP2γ expression through Smad1 binding to the AP2γ promoter. Taken together, we propose that during the early stages of ectodermal patterning in the chick embryo, AP2γ acts downstream of the BMP pathway to restrict precocious neural expansion in the prospective neural plate and initiates epidermal differentiation in the future epidermal ectoderm.

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Dissecting early regulatory relationships in the lamprey neural crest gene network

Cited by 97 publications

References 33 publications

Programmed loss of millions of base pairs from a vertebrate genome

Programmed loss of millions of base pairs from a vertebrate genome

Signaling pathways and tissue interactions in neural plate border formation

AP2γ regulates neural and epidermal development downstream of the BMP pathway at early stages of ectodermal patterning

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