Oxygen, pH, and oral-aboral axis specification in the sea urchin embryo

Coluccio, Alison; LaCasse, Taylor; Coffman, James A.

doi:10.1002/mrd.21267

Cited by 10 publications

(20 citation statements)

References 3 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Each time point was cultured in a separate dish to minimize oxygenation of subsequent time points. An aliquot of embryos removed from hypoxia at a given time point were allowed to develop to prism stage under normoxia, and scored for radialization by morphological criteria as described in Coluccio et al (2011).…”

Section: Methodsmentioning

confidence: 99%

“…Embryos cultured hypoxically to late blastula stage (18 hrs post-fertilization, hpf) were found to under-express nodal at 18 hpf (and other oral ectoderm genes later in development), which led us to propose that hypoxia suppresses specification of oral ectoderm by blocking nodal expression (Coffman et al, 2004). However, we subsequently found that embryos cultured hypoxically only through late cleavage stage (up to 6 hpf) develop a radialized phenotype (Coluccio et al, 2011). Since nodal is normally activated at ~6 hpf (Nam et al, 2007), we sought to determine how hypoxia affects nodal expression at time points earlier than 18 hpf.…”

Section: Introductionmentioning

confidence: 91%

“…Previous studies have provided evidence that in Strongylocentrotus purpuratus , the side of the embryo that expresses nodal (the prospective oral side) contains a higher than average density of mitochondria, owing to an asymmetric distribution of mitochondria in the unfertilized egg (Coffman et al, 2004, 2009). We have shown that mitochondrial H 2 O 2 is rate-limiting for the initial (pre-feedback) phase of nodal activity (Coffman et al, 2009), and that hypoxic culture of early embryos leads to significantly decreased levels of mitochondrial H 2 O 2 and subsequently to development of radialized larvae lacking an oral-aboral axis (Coffman et al, 2004; Coluccio et al, 2011). Embryos cultured hypoxically to late blastula stage (18 hrs post-fertilization, hpf) were found to under-express nodal at 18 hpf (and other oral ectoderm genes later in development), which led us to propose that hypoxia suppresses specification of oral ectoderm by blocking nodal expression (Coffman et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Oral–aboral axis specification in the sea urchin embryo, IV: Hypoxia radializes embryos by preventing the initial spatialization of nodal activity

Coffman

Wessels

DeSchiffart

et al. 2014

Developmental Biology

Self Cite

View full text Add to dashboard Cite

The oral-aboral axis of the sea urchin embryo is specified conditionally via a regulated feedback circuit involving the signaling gene nodal and its antagonist lefty. In normal development nodal activity becomes localized to the prospective oral side of the blastula stage embryo, a process that requires lefty. In embryos of Strongylocentrotus purpuratus, a redox gradient established by asymmetrically distributed mitochondria provides an initial spatial input that positions the localized domain of nodal expression. This expression is perturbed by hypoxia, leading to development of radialized embryos lacking an oral-aboral axis. Here we show that this radialization is not caused by a failure to express nodal, but rather by a failure to localize nodal activity to one side of the embryo. This occurs even when embryos are removed from hypoxia at late cleavage stage when nodal is first expressed, indicating that the effect involves the initiation phase of nodal activity, rather than its positive feedback-driven amplification and maintenance. Quantitative fluorescence microscopy of MitoTracker Orange-labelled embryos expressing nodal-GFP reporter gene revealed that hypoxia abolishes the spatial correlation between mitochondrial distribution and nodal expression, suggesting that hypoxia eliminates the initial spatial bias in nodal activity normally established by the redox gradient. We propose that absent this bias, the initiation phase of nodal expression is spatially uniform, such that the ensuing Nodal-mediated community effect is not localized, and hence refractory to Lefty-mediated enforcement of localization.

show abstract

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 91%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Oral–aboral axis specification in the sea urchin embryo, IV: Hypoxia radializes embryos by preventing the initial spatialization of nodal activity

Coffman

Wessels

DeSchiffart

et al. 2014

Developmental Biology

Self Cite

View full text Add to dashboard Cite

show abstract

“…Partial repression by Six3 probably accounts for the relatively weak nodal expression in the near-apical animal oral ectoderm. Expression of the nodal gene is the primary transcriptional response to the redox polarization that in causal terms initially generates the future oral/aboral axis (24)(25)(26)(27)(28). Therefore, because much of the oral ectoderm-specific GRN is wired downstream of Nodal response genes (9-11, 29, 30), Foxq2 repression of nodal hierarchically confines the whole oral ectoderm GRN to the region below the foxq2 expression boundary, that is, the "apical/near apical" boundary of Fig.…”

Section: Grn Interactions Controlling the Apical Domain/oral Ectodermmentioning

confidence: 99%

Encoding regulatory state boundaries in the pregastrular oral ectoderm of the sea urchin embryo

Cui

Peter

et al. 2014

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

View full text Add to dashboard Cite

By gastrulation the ectodermal territories of the sea urchin embryo have developed an unexpectedly complex spatial pattern of sharply bounded regulatory states, organized orthogonally with respect to the animal/vegetal and oral/aboral axes of the embryo. Although much is known of the gene regulatory network (GRN) linkages that generate these regulatory states, the principles by which the boundaries between them are positioned and maintained have remained undiscovered. Here we determine the encoded genomic logic responsible for the boundaries of the oral aspect of the embryo that separate endoderm from ectoderm and ectoderm from neurogenic apical plate and that delineate the several further subdivisions into which the oral ectoderm per se is partitioned. Comprehensive regulatory state maps, including all spatially expressed oral ectoderm regulatory genes, were established. The circuitry at each boundary deploys specific repressors of regulatory states across the boundary, identified in this work, plus activation by broadly expressed positive regulators. These network linkages are integrated with previously established interactions on the oral/aboral axis to generate a GRN model encompassing the 2D organization of the regulatory state pattern in the pregastrular oral ectoderm of the embryo.regulatory state boundaries | pattern formation | repression circuitry B y the onset of gastrulation, bilaterian embryos consist of a complex mosaic of sharply bounded regulatory state domains, where "regulatory state" refers to the sum of specifically expressed mRNAs encoding DNA sequence-recognizing transcription factors in each nucleus. The regulatory state domains or territories are organized spatially in respect to the two major axes of the embryo, and they constitute informational specifications that determine the subsequent embryonic fates and functions of the cells descendant from these domains. Although in different modes of pregastrular embryogenesis regional specification functions are accomplished in somewhat different ways (1, 2), the end result is always the same: subdivision of the embryo into (transient) spatial regulatory states. These progressively specified regulatory states, and the boundaries between them, are the output of networks of genomically ordained interactions among regulatory genes. Gene regulatory networks (GRNs) encompass the heritable code for the embryonic development of each species. At present, the best known, experimentally determined, large-scale GRN drives the specification of endoderm and mesoderm in the embryo of the sea urchin Strongylocentrotus purpuratus up to gastrulation (3-6). This GRN model encompasses about half of the embryo, covers 30 h of development (18 h in the nonskeletogenic mesoderm), and all or almost all relevant regionally expressed regulatory genes. A recent study (7) shows that the endomesoderm GRN model contains sufficient regulatory relationships to generate a computational automaton that successfully predicts almost all spatial and temporal regulatory gene expre...

show abstract

“…In fact, quenching mitochondrial H2O2 emissions by clonal overexpression of mitochondrially-targeted catalase entrains DV polarity by under-expression of nodal [26]. Similarly, embryos cultured under hypoxic conditions through early cleavage exhibit significantly decreased levels of H2O2 and develop as radialized larvae lacking DV polarity [25,31]. Worth mentioning, nodal expression is not abolished in these larvae, but rather its spatial localization to one side of the embryo is prevented by hypoxia, revealing that redox anisotropies are not required to activate nodal transcription by itself, but rather to provide an initial spatial bias in the rate of nodal transcription [32].…”

Section: Symmetry Breaking: Subtle Redox Anisotropies Prefiguring Thementioning

confidence: 99%

Symmetry Breaking and Establishment of Dorsal/Ventral Polarity in the Early Sea Urchin Embryo

Cavalieri

Spinelli

2015

Symmetry

View full text Add to dashboard Cite

Abstract:The mechanisms imposing the Dorsal/Ventral (DV) polarity of the early sea urchin embryo consist of a combination of inherited maternal information and inductive interactions among blastomeres. Old and recent studies suggest that a key molecular landmark of DV polarization is the expression of nodal on the future ventral side, in apparent contrast with other metazoan embryos, where nodal is expressed dorsally. A subtle maternally-inherited redox anisotropy, plus some maternal factors such as SoxB1, Univin, and p38-MAPK have been identified as inputs driving the spatially asymmetric transcription of nodal. However, all the mentioned factors are broadly distributed in the embryo as early as nodal transcription occurs, suggesting that repression of the gene in non-ventral territories depends upon negative regulators. Among these, the Hbox12 homeodomain-containing repressor is expressed by prospective dorsal cells, where it acts as a dorsal-specific negative modulator of the p38-MAPK activity. This review provides an overview of the molecular mechanisms governing the establishment of DV polarity in sea urchins, focusing on events taking place in the early embryo. Altogether, these findings provide a framework for future studies aimed to unravel the inceptive mechanisms involved in the DV symmetry breaking.

show abstract

Oxygen, pH, and oral-aboral axis specification in the sea urchin embryo

Cited by 10 publications

References 3 publications

Oral–aboral axis specification in the sea urchin embryo, IV: Hypoxia radializes embryos by preventing the initial spatialization of nodal activity

Oral–aboral axis specification in the sea urchin embryo, IV: Hypoxia radializes embryos by preventing the initial spatialization of nodal activity

Encoding regulatory state boundaries in the pregastrular oral ectoderm of the sea urchin embryo

Symmetry Breaking and Establishment of Dorsal/Ventral Polarity in the Early Sea Urchin Embryo

Contact Info

Product

Resources

About