Huang Shengfeng, Wang Xin, Yan Qingyu, Guo Lei, Yuan Shaochun, Huang Guangrui, Huang Huiqing, Li Jun, Dong Meiling, Chen Shangwu, Xu Anlong
State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Pharmaceutical Functional Genes, College of Life Sciences, Sun Yat-sen University, Guangzhou 510275, People's Republic of China.
J Immunol. 2011 Feb 15;186(4):2042-55. doi: 10.4049/jimmunol.1001824. Epub 2011 Jan 19.
Both amphioxus and the sea urchin encode a complex innate immune gene repertoire in their genomes, but the composition and mechanisms of their innate immune systems, as well as the fundamental differences between two systems, remain largely unexplored. In this study, we dissect the mucosal immune complexity of amphioxus into different evolutionary-functional modes and regulatory patterns by integrating information from phylogenetic inferences, genome-wide digital expression profiles, time course expression dynamics, and functional analyses. With these rich data, we reconstruct several major immune subsystems in amphioxus and analyze their regulation during mucosal infection. These include the TNF/IL-1R network, TLR and NLR networks, complement system, apoptosis network, oxidative pathways, and other effector genes (e.g., peptidoglycan recognition proteins, Gram-negative binding proteins, and chitin-binding proteins). We show that beneath the superficial similarity to that of the sea urchin, the amphioxus innate system, despite preserving critical invertebrate components, is more similar to that of the vertebrates in terms of composition, expression regulation, and functional strategies. For example, major effectors in amphioxus gut mucous tissue are the well-developed complement and oxidative-burst systems, and the signaling network in amphioxus seems to emphasize signal transduction/modulation more than initiation. In conclusion, we suggest that the innate immune systems of amphioxus and the sea urchin are strategically different, possibly representing two successful cases among many expanded immune systems that arose at the age of the Cambrian explosion. We further suggest that the vertebrate innate immune system should be derived from one of these expanded systems, most likely from the same one that was shared by amphioxus.
文昌鱼和海胆在其基因组中都编码了一套复杂的先天性免疫基因库，但它们先天性免疫系统的组成和机制，以及两个系统之间的根本差异，在很大程度上仍未被探索。在本研究中，我们通过整合系统发育推断、全基因组数字表达谱、时间进程表达动态和功能分析等信息，将文昌鱼的黏膜免疫复杂性解析为不同的进化功能模式和调控模式。利用这些丰富的数据，我们重建了文昌鱼的几个主要免疫子系统，并分析了它们在黏膜感染过程中的调控。这些包括肿瘤坏死因子/白细胞介素-1受体网络、Toll样受体和NOD样受体网络、补体系统、凋亡网络、氧化途径以及其他效应基因（如肽聚糖识别蛋白、革兰氏阴性结合蛋白和几丁质结合蛋白）。我们表明，尽管文昌鱼先天性免疫系统与海胆的表面相似，但尽管保留了关键的无脊椎动物成分，在组成、表达调控和功能策略方面，它与脊椎动物的更为相似。例如，文昌鱼肠道黏液组织中的主要效应器是发育良好的补体和氧化爆发系统，文昌鱼中的信号网络似乎更强调信号转导/调节而非启动。总之，我们认为文昌鱼和海胆的先天性免疫系统在策略上是不同的，可能代表了寒武纪大爆发时期出现的众多扩展免疫系统中的两个成功案例。我们进一步认为，脊椎动物的先天性免疫系统应该源自这些扩展系统之一，很可能来自文昌鱼所共有的同一个系统。
