2020, Vol. 50-
李红岩, 张祥敏, 杨帅奇. 海洋生物C型凝集素研究进展[J]. 中国海洋大学学报(自然科学版), 2020, 50(9): 113-119.
LI Hong-Yan, ZHANG Xiang-Min, YANG Shuai-Qi. Research Progress of C-Type Lectin in Marine Organisms[J]. Periodical of Ocean University of China, 2020, 50(9): 113-119.
引用本文 
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基金项目
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国家重点研究发展计划项目(2018YFD0900502)资助
Supported by the National Key Research and Development Program of China (2018YFD0900502)
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作者简介
- 李红岩(1975-)，女，教授。E-mail: hongyanli@ouc.edu.cn
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文章历史
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收稿日期：2020-02-01
修订日期：2020-05-02
C型凝集素(C-type lectins，CTLs)是指一类需要钙离子参与选择性结合糖类物质的蛋白超家族，是凝集素家族中种类和数量最多的一个家族，广泛存在于脊椎动物和无脊椎动物中[1-2]。C型凝集素通常含有一个至多个糖识别结构域(Carbonhydrate-recognition domain，CRD)[2-3]，该结构域一般含有110~130个氨基酸，是典型的双环结构[1, 3-5]。EPN/QPD和WND是该结构域中两个高度保守的氨基酸基序，与糖类物质的特异性识别有关，可以通过这两个基序预测C型凝集素结合糖类物质的特异性[1, 6]。糖识别结构域可以特异性识别和结合入侵病原微生物细胞壁中的糖类物质，从而引起机体免疫反应[7]。除糖类外C型凝集素还可以识别多种配体，如蛋白质、脂质和尿酸晶体等[8-9]。大部分C型凝集素和配体结合都需要钙离子的参与，但最近有研究表明，部分C型凝集素也可以在没有钙离子存在的情况下识别配体，这一现象在脊椎动物和无脊椎动物中均有报道[1, 10-11]。
作为一类重要的模式识别受体(Pattern-recognition receptor，PRR)，C型凝集素可以识别和结合多种配体，具有介导细胞间相互作用、调控细胞因子表达及炎症反应、诱导凋亡、激活补体系统、抗原呈递等功能，在免疫防御中发挥重要作用[12-18]。
C型凝集素在脊椎动物中的研究较为广泛深入。研究表明C型凝集素在脊椎动物免疫过程中发挥重要作用[19-23]，树突状细胞相关C型凝集素-1 (Dendritic cell-associated C-type lectin-1, Dectin-1)、树突状细胞相关C型凝集素-2(Dendritic cell-associated C-type lectin-2, Dectin-2)、巨噬细胞C型凝集素(Macrophage C-type lectin, MCL)等与病原微生物结合后通过激活Syk信号通路进行相关抗原的交叉呈递，从而引起机体免疫反应[21]；树突状细胞自然杀伤细胞凝集素群受体1(Dendritic cell NK lectin Group Receptor-1, DNGR-1)与坏死细胞暴露的F-肌动蛋白结合后，通过Syk信号途径将与坏死细胞相关的抗原交叉呈递，进而清除坏死细胞[22]；Dectin-1有助于识别癌症相关配体和增强自然杀伤细胞(Natural killer cell，NK)杀死癌细胞的活性[23]。
作为先天性免疫因子，C型凝集素在无脊椎动物免疫过程中也起着重要作用。凡纳滨对虾(Litopenaeus vannamei)的LvCTL5可以抑制细菌生长[24]；菲律宾蛤仔(Venerupis philippinarum)的MCL-4具有抑菌和增强血强胞吞噬活性[25]；黑腹果蝇(Drosophila melanogaster)的DL2、DL3能够凝集细菌[26]；家蝇(Musca domestica)的MdCTL-2具有抗病毒作用，能够抑制甲型H1N1流感病毒的复制[27]。
虽然海洋生物C型凝集素研究起步较晚，但近期取得了丰富的研究成果。本文将对海洋软体动物、海洋节肢动物、海洋棘皮动物、海洋脊索动物和海洋脊椎动物等中的C型凝集素研究进展和现状进行综述。
1 海洋软体动物C型凝集素研究现状海洋软体动物中C型凝集素的研究较多，主要集中在双壳纲一些具有经济价值的海洋贝类中。研究表明海洋软体动物中含有多种C型凝集素，如已发现栉孔扇贝(Chlamys farreri)中至少存在5种C型凝集素；海湾扇贝(Argopecten irradians)中至少含有9种[12]。之前已有关于软体动物中C型凝集素的功能以及糖识别结构域特征的相关综述[28]。本文主要从软体动物中C型凝集素的结构特征、组织分布和免疫功能等方面进行综述。
软体动物C型凝集素的结构多样化。大部分C型凝集素含有一个糖识别结构域，少部分含有3或4个，但至今尚未发现多于4个的。对于含有多个糖识别结构域的C型凝集素，每个结构域的结构和功能并不完全相同，因此含有多个糖识别结构域的C型凝集素拥有更广泛的识别图谱[12]。部分C型凝集素含有信号肽可能编码分泌蛋白，作为分泌蛋白起作用，而有的则含有跨膜结构域，可能作为膜受体发挥作用[29]。
研究表明海洋软体动物大部分C型凝集素在多个组织器官中均有表达，如在肾、肌肉、心脏、神经节、外套膜、肝胰腺和血淋巴等组织器官中表达[12, 30-33]，但是在肝胰腺或血淋巴中的表达量明显高于其他组织。菲律宾蛤仔(V. philippinarum)的VpClec-1和VpClec-2[34]、螠蛏(Sinonovacula constricta)的ScCTL-1[35]等在肝胰腺中的表达量最高，而华贵栉孔扇贝(Mimachlamys nobilis)的Cnlec-1[36]、太平洋牡蛎(Crassostrea gigas)的Cg CLec-5[37]等在血淋巴中高表达。肝胰腺和血淋巴是无脊椎动物重要的免疫组织器官[38-40]，高表达的C型凝集素可以帮助机体快速识别和清除入侵的非己成分[34-41]，这与C型凝集素是免疫系统的重要组成成分是一致的。
研究证实C型凝集素在软体动物先天性免疫中发挥多种重要功能。海湾扇贝(A. irradians)的AiCTL-7能够凝集细菌和红细胞[42]，栉孔扇贝(C. farreri)的CfLec-5可以凝集毕赤酵母(Pichia pastoris)[43]；栉孔扇贝(C. farreri)的CfLec-1、CfLec-2、CfLec-3和CfLec-4都能促进血细胞吞噬大肠杆菌(Escherichia coli)[44-47]；海湾扇贝(A. irradians)的AiCTL-9和栉孔扇贝(C. farreri)的CfLec-3可以促进血淋巴细胞对琼脂糖球的包囊作用[44, 48]。有趣的是，最近在美洲牡蛎(Crassostrea virginica)中还发现了两个在消化器官中高表达的C型凝集素基因CvML3912和CvML3914，它们可以在牡蛎摄食过程中帮助进行食物分选，而其是否具免疫功能尚不明确，需要进一步研究[49]。
2 海洋节肢动物C型凝集素研究现状C型凝集素在海洋节肢动物中的研究主要集中在对虾中。之前有综述从对虾C型凝集素的结构特征、表达模式、免疫功能等方面进行过总结[50]。在此基础上，结合近几年的研究成果我们对海洋节肢动物C型凝集素的研究进行进一步总结。
对虾中含有一个糖识别结构域的C型凝集素最为常见，仅有部分C型凝集素含有两个糖识别结构域，至今尚未发现含有两个以上糖识别结构域的C型凝集素[51]。大部分C型凝集素都含有信号肽，表明这些C型凝集素可能作为分泌性蛋白发挥作用[50]。
海洋节肢动物C型凝集素的表达模式相类似，大部分C型凝集素在免疫组织器官中的表达量明显高于其他组织器官[51-55]。日本对虾(Marsupenaeus japonicus)的Leulectin[52]和MjLTL12[53]、墨吉明对虾(Fenneropenaeus merguiensis)的FmLC3等在肝胰腺中的表达量较高[54]；中国对虾(Fenneropenaeus chinensis)的Fclectin特异性表达在血细胞中[55]；此外，日本沼虾(Macrobrachium nipponense)的MnCTL主要在鳃和胃部表达，而在其他组织中的表达量很低[56]。C型凝集素在免疫组织器官中的高表达提示其可能与对虾先天性免疫存在密切关系。
已有研究结果表明在对虾中C型凝集素参与多种免疫反应，如凝集作用：除中国对虾(F. chinensis)的FcLec6外，其余已报道的C型凝集素均具有凝集细菌的功能[50]；促吞噬作用：中国对虾(F. chinensis)的FcLec4在识别细菌后与血细胞膜中的β-整联蛋白结合，进而诱导吞噬体吞噬细菌[57]；抑菌作用：日本对虾(M. japonicus)的MjHeCL通过维持抗菌肽的表达来抑制血淋巴中菌群的增殖[58]；参与信号通路传递：日本对虾(M. japonicus)的MjCC-CL通过激活JAK/STAT信号通路调控抗菌肽的表达[59]，凡纳滨对虾(L. vannamei)中的LvCTL3、LvCTL4是NF-κB信号通路的下游基因并受其调控[60-61]。
3 海洋棘皮动物C型凝集素研究现状关于海洋棘皮动物C型凝集素的研究主要集中在海参纲动物中。近几年在仿刺参(Apostichopus japonicus)中鉴定的几个C型凝集素基因(AjCTL、AjCTL-1、AjCTL-2、SjL-1)在结构上存在一定相似性，如都含有信号肽、一个糖识别结构域以及识别甘露糖的EPN氨基酸基序[62-65]。但是在表达模式上却存在较大差异，AjCTL在纵肌和肠中的表达量较高，AjCTL-1在生殖腺中高表达，AjCTL-2在体腔中的表达量最高，而SjL-1则主要在本表和触手中高表达[62-65]。在功能方面，AjCTL-2可以结合革兰氏阴性菌、革兰氏阳性菌和真菌[64]；SjL-1既不促进对细菌的吞噬也不抑制细菌生长，而是分布在海参体表作为一道防线阻止细菌入侵[63]。
4 海洋脊索动物C型凝集素研究现状C型凝集素在海洋尾索动物(被囊动物)中的研究相对较少，到目前为止仅在玻璃海鞘(Ciona intestinalis)中克隆出1条C型凝集素基因CiCD94-1，与脊椎动物CD94是同源基因。CiCD94-1在结构上较为特殊，缺乏钙离子结合位点和EPN等经典氨基酸基序。CiCD94-1在海鞘中执行多种功能，如特异性结合LPS参与先天性免疫过程；在海鞘幼体神经系统的特定位置表达，参与海鞘神经系统的形成[66]。
文昌鱼(Branchiostoma spp.)是海洋头索动物的典型代表，基因组搜索佛罗里达文昌鱼(Branchiostoma floridae)发现有1 200多个C型凝集素候选基因，是已知物种中数量最多的[67]。然而截至目前仅在白氏文昌鱼(Branchiostoma belcheri)和日本文昌鱼(Branchiostoma japonicum)中鉴定出4个C型凝集素基因，而相关研究也主要集中在特征描述方面，剩余的大量序列是否编码真正的C型凝集素还有待进一步研究。所克隆的四个基因在结构上存在一定的相似性，如糖识别结构域都位于羧基端，在氨基端都含有信号肽，表明这4个C型凝集素可能作为分泌性蛋白发挥作用[68-69]。这4个C型凝集素和海鞘的CiCD94-1不同，它们都含有C型凝集素钙离子结合位点和保守的氨基酸基序[68-69]。这些C型凝集素在多个组织中均有表达，如AmphiCTL1和AmphiCTL2在成年文昌鱼各组织中均有表达，但在肝盲囊和肠中的表达量最高；BjCTL在多个组织中有表达，其中在脊索和卵巢中的表达量较高；AmphiCTL3在皮肤、卵巢、小肠、肌肉、鳃、脊索和肝盲囊等组织中表达[68-69]。文昌鱼C型凝集素基因的转录受病原微生物刺激调控，当受到酿酒酵母(Saccharomyces cerevisiae)、酵母聚糖或金黄色葡萄球菌(Staphylococcus aureus)特异性刺激后AmphiCTL1会上调70~400倍，而对副溶血性弧菌(Vibrio parahemolyticus)几乎没有反应；当受到细菌或细菌细胞壁成分刺激后AmphiCTL2和AmphiCTL3的表达量会上调5~20倍；当受到大肠杆菌(E. coli)和金黄色葡萄球菌(S. aureus)刺激后BjCTL的表达会被上调，这些结果提示文昌鱼C型凝集素可能参与免疫反应[68-69]。此外，AmphiCTL1和BjCTL还具有凝集细菌和抑制细菌生长的作用[68-69]。
5 海洋脊椎动物C型凝集素研究现状海洋鱼类是海洋脊椎动物的重要组成部分。虽然海洋鱼类种类繁多，但是关于C型凝集素的研究主要集中在一些具有经济价值的海洋鱼类中。之前已有综述对鱼类C型凝集素研究现状进行过总结[70]。本文将在此基础上对海洋鱼类C型凝集素研究进展进行简述。海洋鱼类C型凝集素主要在免疫组织器官中高表达，如大黄鱼(Larimichthys crocea)的LycCTLR在肝脏中的表达量较高[71]；大西洋鳕鱼(Gadus morhua)的Nlp在头肾、肝和脾中高表达[72]；牙鲆(Paralichthys olivaceus) JFCTL的仅在肝脏转录[73]。近几年鉴定的海洋鱼类C型凝集素的功能主要集中在识别病原微生物、凝集细菌、促进淋巴细胞增殖等方面。如许氏平鲉(Sebastes schlegelii)的SsCTL4具有结合细菌和病毒的特性，能够增强巨噬细胞的杀菌活性[74]；大菱鲆(Scophthalmus maximus)的SmLec1可以刺激淋巴细胞增殖和增强巨噬细胞杀菌活性[75]。
6 总结和展望我们对处于不同分类地位的海洋生物C型凝集素的研究现状进行了综述。目前鉴定的海洋生物C型凝集素主要分布在免疫组织器官中，如海洋无脊椎动物在肝胰腺、血淋巴和一些与外界直接接触的组织器官中表达量较高，在脊椎动物中C型凝集素主要分布在肝脏、脾脏等免疫器官中(见表 1)。其功能主要表现为识别和结合病原微生物、促凝集、促吞噬和包囊化、抑菌和抗病毒、参与信号通路传递等(见表 1)。
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表 1 海洋生物C型凝集素组织分布及功能 Table 1 Tissue distribution and immune function of C-type lectin in marine organisms |
C型凝集素数目种类较多，基于序列同源性的系统演化分析对于海洋生物C型凝集素的研究具有重要意义。然而C型凝集素序列并不保守，而且部分海洋生物中C型凝集素数量较多，结构多样，即使结合共线性分析等生物信息学数据也不能确定大部分海洋动物C型凝集素在高等脊椎动物中的直线同源基因。如何对海洋生物中多种不同物种的C型凝集素进行可信的系统演化分析并分类是个难题，也是今后海洋生物C型凝集素研究的一个重要研究方向。
目前海洋生物C型凝集素更多集中于体外表达蛋白的功能研究，而对它们在体内执行的功能所知甚少。在对虾中，生化和RNAi等技术的结合阐明了部分C型凝集素的体内功能和作用机制[76]。然而大部分海洋生物C型凝集素结合的特异配体、介导的免疫信号通路，执行的具体功能及作用机制等研究极度缺乏，是海洋生物C型凝集素研究亟需解决的问题。随着CRISPR/Cas9等基因编辑技术的日益发展，必将极大推动海洋生物C型凝集素的研究。
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