玻璃海鞘作为模式生物的优势及其应用

doi:10.12300/j.issn.1674-5817.2023.159

实验动物与比较医学 ›› 2024, Vol. 44 ›› Issue (2): 162-179.DOI: 10.12300/j.issn.1674-5817.2023.159

玻璃海鞘作为模式生物的优势及其应用

李睿琪(), 段涵(), 甘罗, 郑媛()(), 杨文()()

上海交通大学医学院基础医学院, 上海 200025

收稿日期:2023-11-13 修回日期:2024-02-09 出版日期:2024-05-09 发布日期:2024-04-25
通讯作者: 杨文（1979—），男，博士，研究员，研究方向：线粒体代谢与衰老。E-mail: yangwen@shsmu.edu.cn。ORCID: 0000-0002-2032-1982；
郑媛（1979—），女，博士，助理研究员，研究方向：玻璃海鞘实验动物模型的构建及其在衰老生物学研究中的应用。E-mail: zhengyuan@shsmu.edu.cn。0009-0007-6016-548X；
作者简介:李睿琪（2001—），女，临床医学八年制在读，研究方向：临床医学。E-mail: lrq.seven@sjtu.edu.cn。ORCID: 0009-0004-1379-0555；
段涵（2002—），女，临床医学八年制在读，研究方向：临床医学。E-mail: dhhhh020606@sjtu.edu.cn。ORCID: 0009-0006-6080-0896
基金资助:
国家自然科学基金项目“基于玻璃海鞘（Ciona intestinalis）的衰老对心肌细胞凋亡作用初步研究”(31900377)

Advantages of Ciona intestinalis as a Model Organism and Its Applications

Ruiqi LI(), Han DUAN(), Luo GAN, Yuan ZHENG()(), Wen YANG()()

Shanghai Jiao Tong University College of Basic Medicine Sciences, Shanghai 200025, China

Received:2023-11-13 Revised:2024-02-09 Published:2024-04-25 Online:2024-05-09
Contact: YANG Wen (ORCID: 0000-0002-2032-1982), E-mail: yangwen@shsmu.edu.cn;
ZHENG Yuan （ORCID：0009-0007-6016-548X）， E-mail： zhengyuan@shsmu.edu.cn;

摘要/Abstract

摘要：

随着实验生物学的持续发展，常用模式生物的应用局限日益凸显。由于实验动物和人类的相关研究之间存在差异，严重影响到动物实验研究结果的转化应用。本文介绍了一种在进化上与脊椎动物亲缘关系最近的无脊椎动物，同时也是脊椎动物的姊妹分支——尾索动物玻璃海鞘（ Ciona intestinalis）。本综述通过总结近年来玻璃海鞘在各领域的研究进展，说明其作为新型模式生物具有的优势与巨大应用前景。玻璃海鞘的研究进展主要包括：（1）玻璃海鞘全基因组测序完成并建立了许多相关数据库，多种胚胎基因编辑技术已经在玻璃海鞘中成功应用，使玻璃海鞘成为易于遗传学操作且能够直观研究目的基因功能和相互作用的动物模型。（2）神经生物学领域，玻璃海鞘具有与脊椎动物相似的中枢神经系统组织结构且拥有众多同源神经肽和激素分子，使其在研究内分泌与神经内分泌相关分子的作用机制、功能进化方面具有优越性。同时，玻璃海鞘幼虫对光刺激的敏感性与习惯性可用于探索行为可塑性相关机制。（3）免疫学领域，玻璃海鞘已有成熟的固有免疫系统，并进化出部分适应性免疫系统相关基因的前体，加之编码免疫相关基因较简单，故而可以作为免疫领域研究较理想的模式生物。（4）发育生物学领域，众多研究聚焦玻璃海鞘的脊索发育过程和其中的表达调控机制，提示脊索动物共同的进化发育策略。另外有关心脏发育方向的研究则对人类心脏发育基因网络的理解做出重要贡献。（5）医学领域中，玻璃海鞘的神经复合体和虹吸管具有再生能力，以及心脏在严重损伤后仍然可以存活并恢复收缩功能，使得玻璃海鞘可作为研究再生问题和心脏受损的动物模型。同时玻璃海鞘作为阿尔茨海默病的研究模型在新药开发方面也有其独特优势。此外，玻璃海鞘的完整生命周期仅5个月左右，便于用其观察记录衰老全过程，探索不同因子的衰老效应。总之，本综述旨在说明玻璃海鞘作为模式动物具有独特的优越性并且有望在更多的科学研究方面发挥重要作用。

关键词: 玻璃海鞘, 模式生物, 神经生物学, 免疫学, 发育生物学

Abstract:

With the continuous development of experimental biology, the limitations of commonly utilized model organisms are becoming increasingly apparent. Discrepancies between research conducted on laboratory animals and humans significantly impede the translational application of findings derived from animal experiments. This review introduces ascidian Ciona intestinalis as a novel model organism, an invertebrate that is evolutionarily closest to vertebrates and is a sister group to vertebrates. The review summarizes recent research progress on Ciona intestinalis in various fields to illustrate the significant advantages and promising application prospects of it as a model organism. The research progress outlined in the review mainly encompasses: (1) The whole-genome sequencing of Ciona intestinalis has been determined and numerous related databases have been established. Various embryonic gene editing technologies have been successfully applied, making it an animal model easy to manipulate genetically and study the functions and interactions of target genes visually. (2) In the field of neurobiology, Ciona intestinalis boasts a central nervous system structure similar to that of vertebrates and possesses numerous homologous neuropeptides and hormone molecules. These features grant it an edge in exploring the mechanisms and functional evolution of endocrine and neuroendocrine-related molecules. Additionally, the sensitivity and habituation of its larvae to light stimulation provide an avenue for exploring mechanisms related to behavioral plasticity. (3) In the field of immunology, Ciona intestinalis possesses a mature innate immune system and has evolved precursor genes to the adaptive immune system, with a relatively simple coding of immune-related genes. These features make it an exemplary model organism for immunological studies. (4) In the field of developmental biology, many studies have focused on the notochord development process in Ciona intestinalis and the regulatory mechanisms of gene expression within it, indicating common evolutionary developmental strategies among chordates. Additionally, insights into its heart development also significantly enhance our comprehension on the genetic network of human heart development. (5) In medical research, the ability of Ciona intestinalis to regenerate its neural complex and siphon, as well as the resilience of its heart to recover contractile function from substantial damage, renders it a valuable animal model for the study of regeneration and heart injury. It also has unique advantages as a research model for Alzheimer's disease and new drug development. Furthermore, its brief five-month lifespan facilitates the observation and recording of the entire aging process and the exploration of the effects of various factors on aging. In summary, this review aims to demonstrate that Ciona intestinalis stands out as a model organism with unique attributes and is expected to play a significant role in a wider range of scientific research areas.

Key words: Ciona intestinalis, Model organism, Neurobiology, Immunology, Developmental biology

中图分类号:

Q95-33

李睿琪, 段涵, 甘罗, 郑媛, 杨文. 玻璃海鞘作为模式生物的优势及其应用[J]. 实验动物与比较医学, 2024, 44(2): 162-179.

Ruiqi LI, Han DUAN, Luo GAN, Yuan ZHENG, Wen YANG. Advantages of Ciona intestinalis as a Model Organism and Its Applications[J]. Laboratory Animal and Comparative Medicine, 2024, 44(2): 162-179.

图/表 6

图1 从系统进化树看玻璃海鞘的进化地位

Figure 1 Evolutionary status of Ciona intestinalis in the phylogenetic tree

图2 玻璃海鞘生活史注：A，受精卵（标尺：50 μm）；B，贴壁的幼虫（标尺：100 μm）；C，变态期稚体（标尺：100 μm）；D，二鳃囊期稚体（标尺：100 μm）；E，四鳃囊期稚体（标尺：100 μm）；F，鳃囊分裂期稚体（标尺：100 μm）；G，性成熟成体（标尺：2 mm）；H，衰老成体（标尺：2 mm）。

Figure 2 Life history of Ciona intestinalisNote：A, Fertilized egg (scale bar: 50 μm); B, Attached larva (scale bar: 100 μm); C, Juvenile during metamorphosis (scale bar: 100 μm); D, Two-branchial sac stage larva (scale bar: 100 μm); E, Four-branchial sac stage larva (scale bar: 100 μm); F, Juvenile during branchial sac division (scale bar: 100 μm); G, Sexually mature adult (scale bar: 2 mm); H, Aged adult (scale bar: 2 mm).

图3 玻璃海鞘幼虫及成体的结构示意图和中枢神经系统示意图注：A，幼虫结构示意图，6种幼虫组织分别为内胚层（蓝色）、间充质（紫色）、中枢神经系统（绿色）、脊索（橙色）、肌肉（红棕色）以及最外层的表皮；B，成体内部结构示意图，中枢神经系统包括感觉囊泡（脑，其中包括眼点和耳石等感觉器官）、神经索和神经节；C，幼虫神经系统的示意图；D，成体的神经系统示意图。

Figure 3 Structural diagrams and central nervous system diagrams of Ciona intestinalis larva and adultNote：A, Schematic diagram of larval structure depicting six tissues: the endoderm (blue), mesenchyma (purple), central nervous system (green), notochord (orange), muscle (reddish-brown), and the outermost layer of epidermis; B, Schematic diagram of the adult's internal structure, showing the central nervous system consisting of sensory vesicles (the brain, which includes sensory organs such as ocellus and otolith), nerve cords, and ganglia; C, Schematic diagram of the larval central nervous system; D, Schematic diagram of the adult central nervous system.

表1 玻璃海鞘生物信息相关的数据库

Table 1 Genome-related databases of Ciona intestinalis

资源名称 Resource names	网址 Website	类型 Type	主要内容 Main content
Joint genome institute	https://genome.jgi.doe.gov/portal/	数据库	基因组
Ghost Database	http://ghost.zool.kyoto-u.ac.jp/cgi-bin/gb2/gbrowse/kh	数据库（日语）	基因组和cDNA
Aniseed genome browser	http://www.aniseed.cnrs.fr/	数据库	基因组
Smith research lab	http://labs.mcdb.ucsb.edu/smith/william	公众号	神经系统发育和功能
UniProt	https://www.uniprot.org/	数据库	蛋白质组
Ensemble	http://asia.ensemble.org	数据库	基因组
NCBI	http://www.ncbi.nlm.nih.gov/dbEST/dbEST_summary.html	数据库	基因的时空表达信息
NBRP	http://nbrp.jp/	数据库（日语）	cDNA
Database of Tunicate Gene Regulation	http://dbtgr.hgc.jp/	数据库	组织特异性基因5'侧翼的顺式调控元件数据库
NCBI	http://www.ncbi.nlm.nih.gov/geo/	数据库	基因表达谱
Tefor	http://crispor.tefor.vet	数据库	CRISPOR引物在线设计
PrimerX	http://www.bioinformatics.org/primerx/cgi-bin/DNA_1.cgi	数据库	基因突变引物在线设计
EDomics	http://edomics.qnlm.ac/#/home	数据库	基因组和转录组等

图4 玻璃海鞘的固有免疫系统对消化道的保护机制注：黏膜免疫包括黏膜上皮细胞分泌黏液，以及帕内特细胞分泌抗菌肽；固有免疫是由Toll样受体（TLR）、含几丁质结合蛋白的可变区（VCBP）和补体系统等机制介导变形细胞吞噬作用。

Figure 4 Protective mechanism of the innate immune system to the digestive tract of Ciona intestinalisNote： Mucosal immunity includes the secretion of mucus by mucosal epithelial cells and the secretion of antimicrobial peptides by Paneth cells. The innate immunity is mediated by Toll-like receptors (TLR), variable region-containing chitin-binding proteins (VCBP), and the complement system, which facilitate the phagocytic activity of amoebocytes.

表2 海鞘免疫系统与人类免疫系统的比较

Table 2 Comparison of immune systems between Ciona intestinalis and human

免疫系统组成 Immune system composition	玻璃海鞘 Ciona intestinalis		人 Homo sapiens		进化差别 Evolutionary difference
免疫系统组成 Immune system composition	分子 Molecules	作用 Function	分子 Molecules	作用 Function	进化差别 Evolutionary difference
免疫识别分子 Immune recognition molecules	TLR	介导免疫应答	TLR	介导免疫应答	人类TLR具有更多亚型
	凝集素	特异性结合糖蛋白	-	-	不存在同源分子
	酚氧化酶	杀死细菌，合成黑色素	-	-	不存在同源分子
	CrPxt	介导细胞-细胞，细胞-细胞外基质之间的黏附	-	-	不存在同源分子
	CrPtx-like	参与体液免疫	C反应蛋白	参与固有免疫反应	同源
	补体系统分子C3、CFB、MASP等	调理作用、炎症反应	补体系统分子C3、CFB、MASP等	调理作用、炎症反应、溶解细胞	同源
细胞因子 Cytokine	TNF-α	参与细菌的免疫反应	TNF-α	识别病原体，激活NF-κB	同源
	IL-17	介导抗真菌和细菌的保护性免疫	IL-17	介导抗真菌和细菌的保护性免疫，也与多种自身免疫性和慢性炎症性疾病相关	同源
	CiTGF-β	参与免疫应答，激活免疫细胞	hTGF-β	调节炎症过程	同源
组织重构与伤口愈合相关因子 Factors related to tissue remodeling and wound healing	MMP-9样分子	胚胎发生、组织重构、血管生成、伤口愈合	MMP-9	胚胎发生、组织重构、血管生成、伤口愈合	同源
	MIF	介导免疫反应	MIF	介导固有免疫和适应性免疫反应	同源
顺式调控元件 Cis-regulatory element	Cr8long、Cr8short	功能尚不明确	RTP	与嗅觉相关	同源
顺式调控元件 Cis-regulatory element	CrCAP	免疫应答调控	GAIT复合物	免疫应答调控	同源
抗菌肽 Antimicrobial peptide	Ci-MAM-A、 Ci-PAP-A	参与初次免疫应答	-	-	不存在同源分子

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玻璃海鞘作为模式生物的优势及其应用

Advantages of Ciona intestinalis as a Model Organism and Its Applications

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