摘要
松江鲈(Trachidermusfasciatus Heckel)隶属于触形目(Scorpaeniformes),杜父鱼科(Cottidae),松江鲈属(Trachidermus)。历史上松江鲈分布较广,是我国渤海、黄海、东海沿岸及相邻淡水水域的习见鱼类。但自上世纪70年代以来,因为人们的过度捕捞,以及栖息地和繁殖地的严重破坏,其种群数量急剧降低。目前,松江鲈在我国许多水域已绝迹。松江鲈已列为国家二级保护动物。为恢复其自然种群,人工养殖势在必行。然而养殖过程中多种应激刺激的存在势必会引起各种疾病的出现和蔓延。只有深入开展松江鲈免疫机制的研究,才可以在人工养殖中采取有效的方法防治疾病,并且为养殖产量的提高提供长远的管理措施。凝集素通过介导蛋白质-碳水化合物的相互作用而成为动物先天免疫的重要组成部分,不仅参与病原体识别过程,同时也负责凝集细菌,固化细菌,激活补体,调理以及杀菌,甚至能够调节适应性免疫应答过程。面对水产养殖过程中日益增长的细菌、病毒、真菌以及寄生虫感染,考虑到各种凝集素不仅能够快速识别以及从体内清除病原菌,而且还能引发长期有效的适应性免疫,这激发了我们对松江鲈凝集素免疫作用的研究兴趣。本研究从松江鲈体内鉴定出三种凝集素(F型,C型,Galectin)和甘露糖结合凝集素相关的丝氨酸蛋白酶MASP,并对它们的特性和功能进行了较为全面而系统的研究,得到如下结果:
1.一种含双结构域的半乳糖结合凝集素(Tfgal-9)参与松江鲈对细菌的免疫
我们从松江鲈中克隆得到一个galectin-9,命名为TfGal-9。其cDNA全长1453bp,开放阅读框(ORF)900bp,编码299个氨基酸。TfGal-9含有两个串联的糖识别结构域(carbohydrate recognition domains, CRDs),每个结构域均包含2个保守的糖结合位点H-NPR和WG-EER.荧光实时定量PCR(qRT-PCR)分析表明,半乳糖结合凝集素广泛表达于松江鲈各组织,但在肠中表达最为丰富;其次是血、心、脑。LPS刺激后,在检测的五个组织(血液、皮肤、肝脏、胃和心)中,TfGal-9mRNA表达均明显上调。重金属刺激后脑TfGal-9表达显著上调。利用体外重组表达的TfGal-9蛋白研究其功能,发现TfGAL-9不依赖钙离子选择性凝集和结合部分细菌。管碟法检测得知TfGal-9i够抑制金黄色葡萄球菌(S. aureus)的活性。体外抗氧化实验表明TfGal-9对DPPH自由基具有清除能力。这些结果表明TfGal-9参与松江鲈对细菌的先天免疫,并具有抗氧化活性。这是迄今为止首次在鱼类对galectin-9的抗菌抗氧化活性进行研究。
2.松江鲈补体的凝集素激活途径:TfCol-11及MASP的基因克隆与功能研究
从松江鲈中鉴定的C-型凝集素collectin-11(TfCol-11)全长CDN序列开放性阅读框为795bp,编码264个氨基酸。它包含三个不同的区域:(1)含有典型的Gly-X-Y重复序列的胶原样区域;(2)颈区;(3)C-末端的CRD结构域,内含保守的可以结合甘露糖的Glu-Pro-Asn (EPN)基序。同时我们还克隆得到松江鲈MASP部分cDNA序列(包括96bp的5'非编码区共993bp),编码的氨基酸包含两个CUB结构域和一个EGF结构域(CUB-EGF-CUB)。RT-PCR研究发现TfCo1-11和MASP共表达于松江鲈肝脏,LPS刺激会引起二者在皮肤、血液、肝脏和鳃表达明显上调,值得注意的是两基因上调模式基本一致。利用原核表达系统获得TfCol-11和MASP重组蛋白。Ca2+存在条件F,TfCol-11可凝集兔红血细胞及多种细菌,且不依赖于Ca2+结合多种细菌。在体实验发现TfCol-11能够显著降低鳗弧菌(Vibrio anguillarum)引起的鲤鱼致死率。通过pull-down试验发现TfCol-11与MASP可以相互结合。根据这些结果推断TfCol-11可以激活松江鲈的补体系统,参与对细菌的免疫。
3.松江鲈岩藻糖糖结合凝集TfFBL的基因克隆与功能研究
本研究利用EST(表达序列标签)和RACE (cDNA末端快速扩增)技术从松江鲈中克隆一个F-型凝集素(TfFBL)。TfFBL的cDNA开放性阅读框为933bp,可编码310个氨基酸。TfFBL包含一个信号肽以及紧随其后的两个糖识别结构域。每个结构域含保守基序HX26RX5-6R。qRT-PCR分析显示TfFBL在卵中表达量最大,其次为皮肤、脾脏、肾脏、心脏和鳃。在受到LPS刺激后其表达量在血液、肝脏和皮肤中有明显的上调,其中在肝脏、血.液,LPS刺激后2h TfFBL表达可分别上调至正常的35.5、37.4倍。利用重组表达的TfFBL成熟肽,对其进行功能研究,发现TfFBL成熟肽可以不依赖Ca2+凝集和结合多种细菌,Ca2+存在条件下凝集的功能增强。岩藻糖抑制TfFBL对细菌的凝集,说明TfFBL可以结合岩藻糖。这些结果均表明TfFBL可作为模式识别受体参与松江鲈的先天免疫防御。
Roughskin sculpin Trachidermus fasciatus Heckel (Scorpaeniformes:Cottidae) has ever been widely distributed in Chinese coastal waters and the rivers flowing into this water body. However, wild population of roughskin sculpin has drastically declined since1970s mainly because of overfishing, as well as the broken habitats and spawning sites. Consequently, roughskin sculpin was listed as critically endangered in Category Ⅱ of the National Key Protected Wildlife List. It is crucial that alternatives such as aquaculture be pursued to recover its population in the wild. In fish aquaculture, stressful conditions facilitate the appearance and diffusion of disease. To efficiently manage disease problems and provide knowledge for long-term enhancement in roughskin sculpin aquaculture production, the roughskin sculpin immune response to pathogen exposure should be studied thoroughly. Protein-carbohydrate interactions mediated by lectins have been recognized as key components of innate immunity, not only for recognition of potential pathogens, but also for participating in effector functions, such as agglutination, immobilization, complement activation, opsonization, killing and even regulation of adaptive immune responses. Therefore, the function of various lectins in the immune response contributes not only to quickly recognize and neutralize the microbial challenge, but lead to an effective long term adaptive immunity. As such, the increasing viral, bacterial, fungal and parasitic infections in aquaculture greatly stir up our interest in the role of lectins in roughskin sculpin innate immune responses. In this study, we identified three lectins (F-type. C-type and a galectin) and a MASP (MBL-associated serine protease), and furthurly studied their biological functions in innate immune system. The results are as follows:
1. A galectin with tandem-repeat domain (TfGal-9) is involved in innate immune response of roughskin sculpin Trachidermus fasciatus
A galectin-9(TfGal-9) was cloned from roughskin sculpin Trachidermus fasciatus. The cDNA of TfGal-9is1453bp with an open reading frame (ORF) of900bp that encodes a protein of299amino acids. It has tandem repeat carbohydrate-binding domains consisting of the characteristic conserved sequence motif H-NPR and WG-E-R/K, connected by a peptide linker. qRT-PCR analysis revealed that TfGal-9was constitutively expressed in all detected tissues, with a relatively rich amount of mRNA in the intestine followed by the blood, heart and brain. Its expression was up-regulated in the five detected tissues (blood, skin, liver, stomach and heart) challenged with LPS. In the heavy metal exposure experiment. TfGal-9in the brain showed an increased expression. Recombinant TfGal-9protein agglutinated some Gram-positive and Gram-negative bacteria in a calcium-independent manner. The recombinant protein also bound to bacteria in the absence of calcium. The antimicrobial activities of recombinant expressed TfGal-9against Staphylococcus aureus could be detected with cylinder-plate method. The antioxidant experiments in vitro showed that percentage clearance of DPPH was50.38%when TfGal-9concentration reached200μg/ml. These data suggest that TfGal-9might be involved in the immune response to bacteria in roughskin sculpin and exhibited antioxidant activity. This is the first report about antibacterial and antioxidative action of galectin-9in fish.
2. Lectin pathway of roughskin sculpin complement:identification, molecular characterization and functional analysis of collectin-11(TfCol-11) and MASP
A C-type lectin collectin-11, designated TfCol-11, is reported in roughskin sculpin. TfCol-11encodes a protein of264amino acids. It is composed of three distinct domains:1) a collagenous region characterized by Gly-X-Y repeats;2) neck region; and3) a C-type lectin-like carbohydrate recognition domain (CRD) which contains a Glu-Pro-Asn (EPN) motif predicted binding to mannose specifically. Meanwhile, a993bp-length of partial MASP cDNA with96bp5'untranslated region (UTR) was also cloned from roughskin sculpin, which contained299amino acids consisted of three domains CUB-EGF-CUB. qRT-PCR indicated that TfCol-11and MASP mRNAs were predominately coexpressed in the liver. The temporal expressions of TfCol-11and MASP were both drastically up-regulated in the skin, blood, liver and gill by LPS challenge. It is noticeable that the temporal expressions of TfCol-11and MASP post LPS challenge were strikingly similar. TfCol-11and MASP recombinant proteins were constructed using an E. coli expression system. TfCol-11was able to agglutinate some Gram-positive, Gram-negative bacteria and a yeast in a Ca2+-dependent manner. Further analysis showed that TfCol-11could bind to several kinds of bacteria in a Ca2+-independent manner. In vivo, recombinant protein TfCol-11could significantly reduce mortality of carp Cyprinus carpio infected with Vibrio anguillarum. Pull-down assay showed that the recombinant TfCol-11protein could interact with MASP. It is conceivable that TfCol-11plays a role in activating complement system and in the defense against invading microorganism in roughskin sculpin。
3. Molecular characterization and functional study of TfFBL in roughskin sculpin Roughskin sculpin Trachidermus fasciatus
In our study, a F-type lectin gene (TfFBL) was cloned from roughskin sculpin by expression sequence tag (EST) and rapid amplification of cDNA ends (RACE) approach. The full-length cDNA of TfFBL contains an open reading frame (ORF) coding for310amino acids. The deduced amino acid sequence of TfFBL contained a signal peptide and two carbohydrate recognition domains (CRDs) arranged in tandem, which both had a carbohydrate-binding site (HX26RX5-6R motif). Results from qRT-PCR in adult tissues indicated that TfFBL mRNA was abundantly expressed in the spawn, moderately expressed in the skin, spleen, kidney, heart and gill, and rarely expressed in other tissues tested. The temporal expression of TfFBL was obviously up-regulated in the blood, liver and skin in time dependent manners by lipopolysaccharide (LPS) challenge. Especially in the liver and blood, expression of TfFBL mRNA was dramatically up-regulated, reaching the highest level (37.4-fold in the blood,35.5-fold in the liver compared with that of the control group) at2h post challenge. Recombinant of TfFBL mature protein was able to agglutinate some bacteria and a yeast in a Ca2+-independent manner, whereas agglutination of TfFBL against microorganism increased greatly in the presence of calcium. Fucose showed inhibition on agglutination, which indicated that TfFBL could bind to fucose. These results suggest that TfFBL might be involved in roughskin sculpin innate response as a PRR.
引文
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