Functional constraints on SoxE proteins in neural crest development: The importance of differential expression for evolution of protein activity.

Functional constraints on SoxE proteins in neural crest development: The importance of differential expression for evolution of protein activity.
复制标题

SoxE 蛋白在神经嵴发育中的功能限制:差异表达对于蛋白质活性进化的重要性。

DOI:
10.1016/j.ydbio.2016.07.022
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发表时间:
2016
影响因子:
2.7
通讯作者:
McCauley,DavidW
McCauley,DavidW
中科院分区:
生物学3区
文献类型:
--
作者:
Lee,EricM;Yuan,Tian;Ballim,ReynaD;Nguyen,Kristy;Kelsh,RobertN;Medeiros,DanielM;McCauley,DavidW

文献摘要

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脊椎动物 SoxE 基因(Sox8、9 和 10)是神经嵴细胞 (NCC) 发育的关键调节因子。这些基因是由脊椎动物祖先中的单个 SoxE 基因复制而来的。尽管 SoxE 旁系同源物在 NCC 发育早期共表达,但后来,Sox9 仅限于头部的骨骼源性谱系,而 Sox10 则仅限于躯干和头部的非骨骼源性 NCC。这种亚功能化何时进化及其在神经嵴进化中可能发挥的作用尚不清楚。海七鳃鳗是基础脊椎动物,也拥有三个 SoxE 基因,而头索类文昌鱼中只存在一个 SoxE 基因。为了解决SoxE基因的功能差异,并确定其生化功能的差异是否可能与神经嵴发育潜力的变化有关,我们研究了七鳃鳗和文昌鱼SoxE基因在缺乏sox10表达的斑马鱼无色(cls)突变体中调节NCC衍生物分化的能力。我们的研究结果表明,原始脊椎动物 SoxE 基因在 SoxE 基因复制之前就具有黑色素生成和神经生成能力。在无颌-颌口分裂后,七鳃鳗SoxE1和SoxE3很大程度上失去了它们的黑色素生成和/或肠神经源性特性,而颌口SoxE旁系同源物保留了功能保守性。我们认为蛋白质亚功能化的这种差异是两个谱系之间 SoxE 旁系同源表达独立调节的直接结果。具体来说,我们提出早期神经嵴中颌骨 SoxE 旁系同源物的重叠表达在很大程度上限制了颌骨 SoxE 蛋白的功能。相比之下,七鳃鳗 SoxE 旁系同源物的基本非重叠表达使它们能够专门化其 DNA 结合和/或蛋白质相互作用特性。七鳃鳗颅骨和躯干神经嵴发育潜力的限制可能与复制品中 SoxE 活性的限制有关,但这种特化似乎并未发生在颌类动物中。这凸显了这两个不同的脊椎动物谱系之间 SoxE 活性进化的重要差异,并为理解不同 NCC 群体中的细胞命运限制如何依赖于 SoxE 复制品之间的亚功能化提供了见解。
Vertebrate SoxE genes (Sox8,9, and10) are key regulators of neural crest cell (NCC) development. These genes arose by duplication from a single SoxE gene in the vertebrate ancestor. Although SoxE paralogs are coexpressed early in NCC development, later,Sox9is restricted to skeletogenic lineages in the head, andSox10to non-skeletogenic NCC in the trunk and head. When this subfunctionalization evolved and its possible role in the evolution of the neural crest are unknown. Sea lampreys are basal vertebrates that also possess three SoxE genes, while only a single SoxE is present in the cephalochordate amphioxus. In order to address the functional divergence of SoxE genes, and to determine if differences in their biochemical functions may be linked to changes in neural crest developmental potential, we examined the ability of lamprey and amphioxus SoxE genes to regulate differentiation of NCC derivatives in zebrafishcolourless(cls) mutants lacking expression ofsox10. Our findings suggest that the proto-vertebrateSoxEgene possessed both melanogenic and neurogenic capabilities prior to SoxE gene duplication. Following the agnathan-gnathostome split, lampreySoxE1andSoxE3largely lost their melanogenic and/or enteric neurogenic properties, while gnathostome SoxE paralogs have retained functional conservation. We posit that this difference in protein subfunctionalization is a direct consequence of the independent regulation of SoxE paralog expression between the two lineages. Specifically, we propose that the overlapping expression of gnathostome SoxE paralogs in early neural crest largely constrained the function of gnathostome SoxE proteins. In contrast, the largely non-overlapping expression of lamprey SoxE paralogs allowed them to specialize with regard to their DNA-binding and/or protein interaction properties. Restriction of developmental potential among cranial and trunk neural crest in lampreys may be related to constraints on SoxE activity among duplicates, but such specialization does not appear to have occurred in gnathostomes. This highlights an important difference in the evolution of SoxE activity between these two divergent vertebrate lineages and provides insights for understanding how cell fate restriction in different NCC populations may be dependent on subfunctionalization among SoxE duplicates.