动物营养学报 >

2023 , Vol. 35 >Issue 1: 23 - 30

DOI: https://doi.org/10.3969/j.issn.1006-267x.2023.01.003

综述

乳酸菌对猪免疫功能调节作用及其机制研究进展

  • 冷来福 , 1, 2 ,
  • 黄金秀 2, 3 ,
  • 刘作华 2, 3 ,
  • 王琪 , 2, 3, *
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  • 1 西南大学动物科学技术学院,重庆 402460
  • 2 重庆市畜牧科学院,重庆 402460
  • 3 国家生猪技术创新中心,重庆 402460
* 王 琪,副研究员,E-mail:

冷来福(1998—),男,贵州铜仁人,硕士研究生,从事单胃动物营养研究。E-mail:

收稿日期: 2022-05-25

  网络出版日期: 2023-01-11

基金资助

重庆市技术创新与应用发展项目(21210)

收起

Research Progress in Regulation of Lactic Acid Bacteria on Pig Immune Function and Its Mechanism

  • LENG Laifu , 1, 2 ,
  • HUANG Jinxiu 2, 3 ,
  • LIU Zuohua 2, 3 ,
  • WANG Qi , 2, 3, *
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  • 1 College of Animal Science and Technology, Southwest University, Chongqing 402460, China
  • 2 Chongqing Academy of Animal Sciences, Chongqing 402460, China
  • 3 National Pig Technology Innovation Center, Chongqing 402460, China
* associate professor, E-mail:

Received date: 2022-05-25

  Online published: 2023-01-11

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摘要

乳酸菌是人和动物胃肠道的一种优势菌群,也是动物生产中的一种重要益生菌来源,具有较强的耐酸性、耐胆盐性及黏附能力。乳酸菌在提高动物生产性能、改善肠道健康、增强免疫力等方面具有重要功能。研究证实,乳酸菌可通过影响细胞免疫、体液免疫和肠道黏膜免疫等免疫应答过程调节猪机体的免疫功能。本文综述了乳酸菌对猪机体免疫功能的影响,以期为乳酸菌在养猪业的开发应用提供参考。

关键词： 乳酸菌; 猪; 免疫功能; 机制

本文引用格式

冷来福 , 黄金秀 , 刘作华 , 王琪 . 乳酸菌对猪免疫功能调节作用及其机制研究进展[J]. 动物营养学报, 2023 , 35(1) : 23 -30 . DOI: 10.3969/j.issn.1006-267x.2023.01.003

Abstract

Lactic acid bacteria is a dominant flora in the gastrointestinal tract of humans and animals, and is also an important source of probiotics in animal production, with strong acid resistance, bile salt tolerance and adhesion ability. Lactic acid bacteria have important functions in improving animal production performance, improving intestinal health, and enhancing immunity. Studies have confirmed that lactic acid bacteria can regulate the immune function of the pig body by influencing immune response processes such as cellular immunity, humoral immunity and intestinal mucosal immunity. In this paper, the adhesion colonization of lactic acid bacteria in the gastrointestinal tract of animals and their influence on the immune function of pigs are reviewed, in order to provide a reference for the development and application of lactic acid bacteria in the pig industry.

Key words： lactic acid bacteria; pig; immune function; mechanism

近年来,抗生素的滥用使病原菌的耐药性、动物产品的药物残留等问题越来越凸显,给养殖业的发展和人类的健康造成了一定的威胁,许多国家已经禁止使用抗生素类添加剂[1]。因此,寻找一种能够有效替代抗生素的物质成为了研究重点。乳酸菌是肠道菌群的重要组成部分,同时也是一种重要的益生菌来源[2-3]。研究表明,在饲粮中添加适量乳酸菌具有提高猪只生长性能、调节肠道菌群平衡、提高免疫力及抗病力等益生作用[4⇓⇓-7]。尽管已有大量报道证实,乳酸菌对猪具有调节免疫功能的作用,但相关作用机制的报道较少。因此,本文旨在综述乳酸菌对猪的免疫功能调节作用及具体机制,以期为乳酸菌在养猪业中的应用提供理论参考。

1 乳酸菌概述

乳酸菌属于革兰氏阳性菌,单个、成双或成短链排列,主要包括乳杆菌属、链球菌属、明串珠菌属、双歧杆菌属、片球菌属和肠球菌属等[8-9]。乳酸菌按形态可分为杆状和球状两大类,厌氧或兼性厌氧,无芽孢,能够发酵碳水化合物和产生乳酸。乳酸菌对动物胃肠道环境具有较强的耐受性。研究表明,乳酸菌的生物膜具有一定的耐酸和耐胆盐性,能够促进乳酸菌在胃肠道黏膜的定植,并增强其定植的持久性[10]。Hou等[11]研究发现,罗伊氏乳杆菌基因组序列编码了大多数已知的黏附因子,包括黏液结合蛋白、纤维连接蛋白等黏附因子。还有研究表明,乳酸菌对猪小肠黏液也有较强的黏附性,其中对回肠黏液的黏附力最强[11-12]。
大量研究表明,乳酸菌具有提高动物生产性能、改善肠道健康、增强机体免疫力等益生作用,如约氏乳杆菌BS15可降低新生仔猪的腹泻率,提高其断奶后的体重[13];嗜酸乳杆菌显著提高断奶仔猪的平均日增重[14],提高仔猪的生长性能。鼠李糖乳杆菌LB1、植物乳杆菌可通过增加回肠绒毛表面积和改变肠道绒隐比来维持仔猪肠道完整性[15-16];饲喂嗜酸乳杆菌或唾液乳杆菌能增加仔猪肠道有益菌的数量并减少有害菌的数量,调节肠道的菌群结构及丰度[17-18],从而促进仔猪肠道健康。罗伊氏乳杆菌通过促进仔猪肠道发育、提高血清干扰素-γ(IFN-γ)、白细胞介素-4(IL-4)和免疫球蛋白(Ig)G的水平,进而改善仔猪的免疫功能[19]。口服发酵乳杆菌I5007可提高仔猪回肠中IFN-γ、肿瘤坏死因子-α(TNF-α)的mRNA表达水平,从而调节仔猪肠道免疫功能[20]。

2 乳酸菌对猪免疫功能的调节作用及其机制

乳酸菌是一种能够影响猪健康的重要益生菌,可显著提高猪的免疫功能。研究报道,乳酸菌可能通过促进细胞因子分泌、改变Ig含量、调节肠道菌群平衡、维持肠道结构完整性、改变免疫因子表达等途径,来调节猪的细胞免疫、体液免疫和肠道黏膜免疫功能。

2.1 乳酸菌对猪细胞免疫的调节作用

动物机体的细胞免疫应答过程主要由T细胞介导。其中,细胞毒性T细胞(CD8+细胞)对带有抗原标记的T细胞、表达抗原的靶细胞具有特异性杀伤作用,辅助性T细胞(CD4+细胞)则参与诱导细胞免疫反应发生的过程。Wang等[20]研究表明,补充发酵乳杆菌I5007可增加仔猪外周血CD4+细胞百分比,而在仔猪饲粮中添加约氏乳杆菌BS15可提高CD3+CD4+细胞百分比和降低CD3+CD8+细胞百分比,调节CD3+CD4+/CD3+CD8+的比值及外周血液中的T细胞亚群比例[13],进而提高仔猪的细胞免疫功能。鼠李糖乳杆菌GG可促进早期断奶仔猪肠道T淋巴细胞的增殖,提高仔猪肠道中CD3+和CD4+细胞的数量,且这种影响具有长期性[21]。以上结果表明,乳酸菌可通过调节T淋巴细胞亚群的比例、促进T淋巴细胞的增殖等途径改善猪的细胞免疫功能。
此外,还有研究发现,细胞免疫反应也受到树突状细胞(DC)和自然杀伤(NK)细胞的调节。DC是机体内功能最强的抗原提呈细胞,参与调节机体固有的免疫反应及适应性免疫反应,是二者相互联系的枢纽[22]。DC表面的分子标记物在抗原提呈及与T淋巴细胞的相互作用中发挥着重要的作用[23]。研究证实,约氏乳杆菌显著提高了猪单核细胞来源树突状细胞(MoDCs)中Toll样受体(TLR)2、TLR4和TLR6的mRNA表达水平及表面分子标记物CD80、组织相容复合体Ⅱ(MHC Ⅱ)和CD172a的表达;增强MoDCs诱导CD4+细胞增殖的能力;促进Th1型细胞因子和趋化因子的表达[24]。NK细胞可通过颗粒胞吐作用、Fas/Fas配体系统、抗体依赖细胞介导的细胞毒性、产生一氧化氮及TNF-α等途径自发清除肿瘤细胞或病毒感染细胞,进而调节先天免疫系统;此外,NK细胞还可通过产生细胞因子激活其他免疫细胞调节适应性免疫系统[25]。试验发现,热灭活的嗜酸乳杆菌可通过增强细胞溶解性及细胞毒性、提高粒溶素的表达、促进细胞的颗粒胞吐作用等途径激活NK细胞[26]。DC和NK细胞是动物体内不可或缺的免疫细胞,参与调节机体的多种免疫应答反应。乳酸菌在动物体内定植后,可激活DC和NK细胞,再通过促进T淋巴细胞的增殖及细胞因子的表达、清除机体内的坏死细胞及其他异物等途径参与调节机体的免疫应答反应。

2.2 乳酸菌对猪体液免疫的调节作用

来源于骨髓B淋巴细胞所产生的Ig介导了动物的体液免疫应答反应[27]。Ig主要包括IgA、IgM、IgG、IgE和IgD,其中,IgA主要分为血清型和分泌型免疫球蛋白A(SIgA),具有降低致病菌黏附率、抗炎、抗感染等作用[28];IgM和IgG具有抗菌、抗病毒、调节免疫功能等作用;IgE与变态反应有关,对嗜碱性粒细胞和肥大细胞具有高度亲和性[29]。此外,血液中总蛋白、白蛋白、尿素氮等含量也能在一定程度上反映动物的体液免疫水平。
新生仔猪的体液免疫主要由随初乳进入其血液循环的母源IgG调控[27]。NS复合乳酸菌显著提高母猪分娩时血清和初乳中的IgG、IgA和IgM的含量,并使哺乳期母猪乳汁的Ig始终维持在较高水平[27];口服发酵乳杆菌I5007可显著提高仔猪血液中IgM、IgG和IgA的含量[30]。仔猪断奶后,受断奶应激的影响,原有的肠道菌群平衡被破坏,使仔猪的免疫机能下降。有研究表明,断奶仔猪饲粮中添加植物乳杆菌和低聚果糖可显著提高血清IgG和IgA含量[31],而植物乳杆菌发酵的液体饲料可显著提高仔猪血清中IgG和IgM的含量[32]。此外,植物乳杆菌、复合乳酸菌(由乳酸片球菌ZPA017和副干酪乳杆菌ZLP018组成)发酵的液体饲料可显著提高生长育肥猪血液中总蛋白、IgG和IgM含量,降低尿素氮和总胆固醇的含量[33-34]。
体液免疫是动物免疫系统的重要组成部分,也是保障动物健康的重要屏障。研究显示,乳酸菌可能是通过提高血液中总蛋白、白蛋白、Ig和葡萄糖含量,降低尿素氮和总胆固醇含量来调节猪的体液免疫。

2.3 乳酸菌对肠道黏膜免疫的调节作用

2.3.1 乳酸菌对猪肠道黏膜免疫功能的影响

肠道屏障是肠黏膜免疫系统的重要组成部分,乳酸菌可通过影响猪的肠道屏障来调节其免疫功能。肠道屏障主要包括物理屏障、化学屏障、微生物屏障及免疫屏障4部分[35]。物理屏障主要由肠上皮细胞之间的紧密连接及其连接结构构成,是肠上皮细胞维持适宜通透性及发挥其屏障功能的基础[36]。鼠李糖乳杆菌GG等益生菌能显著降低仔猪血清内毒素和D-乳酸含量,提高紧密连接蛋白的表达,降低肠道通透性,从而提高仔猪肠道物理屏障功能[37⇓⇓⇓-41]。化学屏障是肠道的动态防御屏障,主要由肠道内的消化酶、杯状细胞分泌的黏蛋白等形成的黏液层构成[42]。研究表明,发酵乳酸杆菌I5007可提高断奶仔猪肠道黏蛋白-2(MUC-2)和黏蛋白-3(MUC-3)的表达,从而提高仔猪的化学屏障功能[43]。微生物屏障主要由动物肠道内的菌群构成。罗伊氏乳杆菌KT260178通过增加仔猪盲肠乳酸菌和双歧杆菌等有益菌的数量,减少大肠杆菌和葡萄球菌的数量,来调节仔猪肠道菌群平衡[44];德氏乳杆菌可提高双歧杆菌和乳酸杆菌的相对丰度,降低梭状芽胞杆菌的相对丰度,调节仔猪盲肠菌群结构,从而增强其微生物屏障功能[45]。肠道免疫屏障是肠道黏膜免疫系统的第1道防线,主要由肠道内的淋巴组织、弥散免疫细胞、细胞因子及SIgA等构成。乳酸菌可通过调节细胞因子的分泌来调节肠道免疫屏障功能,如植物乳杆菌ZLP001可抑制ETEC诱导的猪小肠上皮细胞(IPEC)-J2细胞中IL-6、IL-8和TNF-α分泌增加的现象[46];唾液乳杆菌B1可增强仔猪肠道TNF-α、IFN-γ、IL-6、TLR-2基因的表达[47],我们实验室前期研究结果也证实,新生仔猪灌喂植物乳杆菌299或罗伊氏乳杆菌I5007,可以显著提高肠道TLR-2、TLR-9和猪β防御素-2的基因表达,从而提高猪肠道免疫屏障功能[16,48]。SIgA是肠道免疫屏障中的重要效应因子,具有免疫清除、减少病原微生物定植、中和毒素及病毒等作用[49⇓-51]。报道证实,乳酸菌能调节影响肠道中SIgA的分泌,仔猪饲粮中添加植物乳杆菌、罗伊氏乳杆菌、鼠李糖乳杆菌GG等益生菌,均可显著提高小肠黏膜中SIgA含量[38,52-53],约氏乳杆菌BS15可显著提高仔猪粪便SIgA含量[13],从而增强猪的肠道免疫功能。
综上所述,乳酸菌可通过调节肠道菌群平衡、促进肠上皮细胞的发育、调节细胞因子的分泌、提高紧密连接蛋白和黏蛋白的表达等途径调节猪肠道屏障,进而提高其肠道免疫功能。此外,SIgA是反映动物肠道黏膜免疫水平的重要指标,乳酸菌在猪肠道定植后可引发特异性免疫反应,从而促进SIgA的分泌,提高猪的肠道黏膜免疫水平。

2.3.2 乳酸菌对肠道黏膜免疫的影响机制

乳酸菌主要通过影响p38丝裂原激活蛋白激酶(p38 mitogen-activated protein kinases,p38 MAPK)或肌球蛋白轻链激酶(myosin light chain kinase,MLCK)信号通路调节紧密连接蛋白的表达,进而改善肠道通透性,调节机体的肠道黏膜免疫力。罗伊氏乳杆菌LR1可增强IPEC-1紧密连接蛋白的表达,加入MLCK抑制剂后,罗伊氏乳杆菌LR1对紧密连接蛋白表达的增强作用受到抑制[54],说明罗伊氏乳杆菌LR1对紧密连接蛋白表达的增强作用是通过MLCK通路实现的。此外,核因子-κB(nuclear factor-kappa B,NF-κB)及MAPK通路也在肠道炎症反应和免疫反应过程中发挥着重要调节作用[55-56]。NF-κB通路对参与免疫反应启动的IL-1、TNF-α、IL-2和IL-6等促炎因子及免疫介质具有调控作用,同时,TNF-α、IL-1等又能反馈调节NF-κB通路,从而调节其他细胞因子的分泌,引起级联放大效应,进一步增强动物的免疫力[57]。Yang等[58]研究表明,植物乳杆菌对ETEC K88诱导的IL-1α、IL-6、IL-8和TNF-α的表达增强及抗炎细胞因子PPAR-γ的表达减弱的抑制作用可能是通过MAPK和NF-κB信号通路实现的。还有研究发现,干酪乳杆菌、唾液乳杆菌可提高IL-18、IL-12、IL-1β、IL-8、TNF-α、IFN-γ的mRNA表达水平以及p38 MAPK和p65 NF-κB蛋白磷酸化水平;加入通路抑制剂后,抑制了干酪乳杆菌、唾液乳杆菌对细胞因子表达水平的增强作用,说明干酪乳杆菌、唾液乳杆菌是通过影响p38 MAPK和p65 NF-κB通路来调节细胞因子水平[59-60];德氏乳杆菌能显著增加血清TNF-α以及回肠IL-4和IL-10含量,诱导NF-κB、MAPK和干扰素调节因子3(interferon regulatory factor 3,IRF3)信号激活,从而调节仔猪的免疫功能[61];植物乳杆菌ZLP001可增强断奶仔猪肠道防御肽(HDP)的mRNA表达,加入细胞外调节蛋白激酶(ERK)和c-Jun N端激酶(JNK)通路抑制剂后,抑制了植物乳杆菌ZLP001对HDP表达的增强作用,说明植物乳杆菌ZLP001是通过影响ERK和JNK通路调节HDP的表达水平[62]。此外,体外试验也表明,乳酸菌可通过抑制脂多糖(LPS)诱导的p38 MAPK及NF-κB蛋白的磷酸化来降低LPS诱导的炎症反应,调节细胞因子及趋化因子的表达[56]。
越来越多的研究表明,乳酸菌在动物肠黏膜定植后可通过促进紧密连接蛋白的表达、调节细胞因子的分泌等途径来增强肠道黏膜免疫力(图1)。乳酸菌增强动物肠道黏膜免疫力的途径主要有:1)乳酸菌激活MLCK和MAPK通路来调节紧密连接蛋白的表达并调节肠道通透性,进而调节动物的肠道黏膜免疫;2)乳酸菌激活MAPK和NF-κB通路来调节细胞因子的分泌和表达,从而调节机体免疫反应;3)乳酸菌通过调节SIgA的分泌调节肠道黏膜免疫反应。
图1 乳酸菌对肠道黏膜免疫的影响机制

MLCK:肌球蛋白轻链激酶 myosin light-chain kinase;NF-κB:核因子-κB nuclear factor-kappa B;MLC:肌球蛋白轻链 myosin light chain kinase;TJ:紧密连接蛋白 tight junction protein;MAPK:丝裂原活化蛋白激酶 mitogen-activated protein kinases;MAPKK:MAPK激酶 mitogen-activated protein kinases kinase;MAPKKK:MAPKK激酶:mitogen-activated protein kinases kinase kinase;IKK:IκB激酶 IκB kinase;TNF-α:肿瘤坏死因子-α tumor necrosis factor-alpha;IL:白细胞介素 interleukin;IFN-γ:干扰素-γ interferon-γ。

Fig.1 Effect mechanism of lactic acid bacteria on intestinal mucosal immune

3 小结

乳酸菌对猪的胃肠道环境具有较强的耐受性及黏附性,能够在其消化道内定植并形成一层稳定的生物屏障,降低致病菌在猪胃肠道的定植率,进而改善猪的肠道健康状况。给猪补充外源乳酸菌,在维持猪肠道菌群平衡、保证肠道结构完整性、改善肠黏膜免疫功能、促进免疫细胞的生长发育、调节体液免疫等方面具有重要作用。乳酸菌作为一种重要的益生菌来源,对促进养殖业的发展具有重要的作用。因此,未来需对乳酸菌在动物胃肠道的定植及其影响动物免疫功能的具体机制作更为深入的研究,为益生菌在养殖业的应用提供理论依据。

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