Amiel Aldine R, Johnston Hereroa, Chock Taylor, Dahlin Paul, Iglesias Marta, Layden Michael, Röttinger Eric, Martindale Mark Q
Université Côte d'Azur, CNRS, INSERM, Institute for Research on Cancer and Aging, Nice, France.
University of Florida, The Whitney Marine Laboratory for Marine Science, St. Augustine, FL, USA.
Dev Biol. 2017 Oct 15;430(2):346-361. doi: 10.1016/j.ydbio.2017.08.015. Epub 2017 Aug 14.
Germ layer formation and axial patterning are biological processes that are tightly linked during embryonic development of most metazoans. In addition to canonical WNT, it has been proposed that ERK-MAPK signaling is involved in specifying oral as well as aboral territories in cnidarians. However, the effector and the molecular mechanism underlying latter phenomenon is unknown. By screening for potential effectors of ERK-MAPK signaling in both domains, we identified a member of the ETS family of transcription factors, Nverg that is bi-polarily expressed prior to gastrulation. We further describe the crucial role of NvERG for gastrulation, endomesoderm as well as apical domain formation. The molecular characterization of the obtained NvERG knock-down phenotype using previously described as well as novel potential downstream targets, provides evidence that a single transcription factor, NvERG, simultaneously controls expression of two different sets of downstream targets, leading to two different embryonic gene regulatory networks (GRNs) in opposite poles of the developing embryo. We also highlight the molecular interaction of cWNT and MEK/ERK/ERG signaling that provides novel insight into the embryonic axial organization of Nematostella, and show a cWNT repressive role of MEK/ERK/ERG signaling in segregating the endomesoderm in two sub-domains, while a common input of both pathways is required for proper apical domain formation. Taking together, we build the first blueprint for a global cnidarian embryonic GRN that is the foundation for additional gene specific studies addressing the evolution of embryonic and larval development.
胚层形成和轴向模式形成是大多数后生动物胚胎发育过程中紧密相连的生物学过程。除了经典的WNT信号通路外,有研究提出ERK-MAPK信号通路参与了刺胞动物口部和反口部区域的特化。然而,这一现象背后的效应分子和分子机制尚不清楚。通过在这两个区域筛选ERK-MAPK信号通路的潜在效应分子,我们鉴定出一种转录因子ETS家族的成员Nverg,它在原肠胚形成之前呈双极性表达。我们进一步描述了NvERG在原肠胚形成、内胚层和顶端区域形成中的关键作用。利用先前描述的以及新发现的潜在下游靶点对获得的NvERG敲低表型进行分子特征分析,结果表明单个转录因子NvERG同时控制两组不同下游靶点的表达,从而在发育胚胎的相对两极形成两个不同的胚胎基因调控网络(GRNs)。我们还强调了cWNT和MEK/ERK/ERG信号通路的分子相互作用,这为星状海葵的胚胎轴向组织提供了新的见解,并表明MEK/ERK/ERG信号通路在将内胚层分隔为两个亚区域时具有cWNT抑制作用,而两个通路的共同输入是顶端区域正常形成所必需的。综上所述,我们构建了第一个刺胞动物胚胎全局GRN蓝图,这为进一步开展针对胚胎和幼虫发育进化的基因特异性研究奠定了基础。