Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain.
Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain.
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DOI：
10.1371/journal.pbio.2001573
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发表时间：
2017-04
期刊：
影响因子：
9.8
通讯作者：
Ferran JL
中科院分区：
文献类型：
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作者：
Albuixech-Crespo B;López-Blanch L;Burguera D;Maeso I;Sánchez-Arrones L;Moreno-Bravo JA;Somorjai I;Pascual-Anaya J;Puelles E;Bovolenta P;Garcia-Fernàndez J;Puelles L;Irimia M;Ferran JL
所有脊椎动物的大脑发育遵循由前后（AP）和背腹（DV）细分定义的共同的Bauplan，其特征在于基因标记物的大部分保守的差异表达。然而，目前还不清楚这种鲍普兰在进化过程中是如何起源的。我们研究了48个基因的相对表达在脊椎动物神经模式的关键作用，在一个代表性的文昌鱼胚胎阶段。与非脊索动物不同，文昌鱼的中枢神经系统（CNS）是从一个与脊椎动物同源的神经板发展而来的，可以进行直接的拓扑比较。由此产生的genoarchitectonic模型显示，文昌鱼的初期神经管是出乎意料的复杂，由几个AP和DV分子分区。引人注目的是，与脊椎动物的比较表明，脊椎动物丘脑，pretectum，中脑域共同对应于一个单一的文昌鱼区域，我们称之为二中脑原基（DiMes）。这表明，这些领域有一个共同的发展和进化的起源，支持操纵斑马鱼和小鼠的二级组织者的功能实验。根据教科书，脊椎动物的大脑是从一个神经管发展而来的，这个神经管迅速地区域化为前脑（包括次级前脑和间脑）、中脑和后脑。这些区域然后进一步细分;特别是，间脑产生前丘脑，丘脑和前顶盖。然而，对大脑信号中心的胚胎学操作表明，前丘脑的行为与丘脑和前顶盖非常不同，后者在很大程度上与中脑共享其发育潜力。因此，从发展的角度来看，这种经典的分区方案可能并不完全一致。为了更好地理解脊椎动物大脑区域化的起源和进化，我们建立了文昌鱼早期神经管的综合分子模型，文昌鱼是一种无脊椎脊索动物，与其脊椎动物亲属共享多种特征。这个模型表明文昌鱼的神经系统出乎意料地复杂，与脊椎动物共享其基本蓝图。然而，文昌鱼中有一个未分割的区域，我们称之为二中脑原基（DiMes），它明确地对应于脊椎动物中包括丘脑、顶盖前体和中脑的区域，这表明这些区域在进化上也更密切相关。因此，间脑作为一个神经解剖隔间，以及在脊椎动物的前脑和中脑之间的经典分离似乎从进化和发育的角度来看是不一致的。
All vertebrate brains develop following a common Bauplan defined by anteroposterior (AP) and dorsoventral (DV) subdivisions, characterized by largely conserved differential expression of gene markers. However, it is still unclear how this Bauplan originated during evolution. We studied the relative expression of 48 genes with key roles in vertebrate neural patterning in a representative amphioxus embryonic stage. Unlike nonchordates, amphioxus develops its central nervous system (CNS) from a neural plate that is homologous to that of vertebrates, allowing direct topological comparisons. The resulting genoarchitectonic model revealed that the amphioxus incipient neural tube is unexpectedly complex, consisting of several AP and DV molecular partitions. Strikingly, comparison with vertebrates indicates that the vertebrate thalamus, pretectum, and midbrain domains jointly correspond to a single amphioxus region, which we termed Di-Mesencephalic primordium (DiMes). This suggests that these domains have a common developmental and evolutionary origin, as supported by functional experiments manipulating secondary organizers in zebrafish and mice. According to textbooks, vertebrate brains develop from a neural tube that rapidly becomes regionalized into the forebrain (which includes the secondary prosencephalon and diencephalon), midbrain, and hindbrain. These regions are then further subdivided; in particular, the diencephalon gives rise to the prethalamus, thalamus, and pretectum. However, embryological manipulations of brain signaling centers showed that the prethalamus behaves very differently than the thalamus and pretectum, which largely share their developmental potential with the midbrain. Therefore, this classic partition scheme might not be fully consistent from a developmental perspective. To better understand the origin and evolution of the regionalization of the vertebrate brain, we built a comprehensive molecular model of the incipient neural tube of amphioxus, an invertebrate chordate that shares multiple features with its vertebrate relatives. This model shows that the amphioxus nervous system is unexpectedly complex, sharing its basic blueprint with that of vertebrates. However, a single undivided region in amphioxus, which we termed Di-Mesencephalic primordium (DiMes), unambiguously corresponds to the region encompassing the thalamus, pretectum, and midbrain in vertebrates, indicating that these regions are also more closely related evolutionarily. Therefore, the diencephalon as a neuroanatomical compartment as well as the classic separation between forebrain and midbrain in vertebrates seem inconsistent from both an evolutionary and developmental perspective.