综述 Review

乳酸菌对猪肠道屏障功能的调节作用及其机制

展开
  • 中国农业大学动物科学技术学院, 北京 100193
谯仕彦(1963—),男,四川阆中人,教授,博士生导师,研究方向为猪的营养。E-mail:qiaoshy@mafic.ac.cn

收稿日期: 2014-08-13

  网络出版日期: 2015-01-23

Regulation and Mechanism of Lactic Acid Bacteria on Porcine Intestinal Barrier Function

Expand
  • College of Animal Science and Technology, China Agricultural University, Beijing 100193, China

Received date: 2014-08-13

  Online published: 2015-01-23

摘要

乳酸菌作为最重要和安全性最高的益生菌来源已被广泛关注,而乳酸菌调控人和动物肠道屏障功能已成为研究的热点,大量的体内外研究表明乳酸菌发挥益生作用的主要机制是通过调节肠道屏障功能实现的。相对于啮齿动物而言,乳酸菌在猪上的应用研究报道很多,对肠黏膜屏障功能的作用研究较少。这些研究尚未触及到乳酸菌作用机制的本质。猪肠道环境的复杂性,使得对乳酸菌调节肠道屏障功能机制的深入认识比较困难。近年来,基因组学、蛋白质组学和代谢组学的发展,为从体内试验的角度解析乳酸菌的确切作用机制提供了新的认识和研究手段。本文综述了乳酸菌对猪肠道屏障功能的调节作用,以期能帮助对乳酸菌的深入认识和科学应用。

本文引用格式

谯仕彦, 侯成立, 曾祥芳 . 乳酸菌对猪肠道屏障功能的调节作用及其机制[J]. 动物营养学报, 2014 , 26(10) : 3052 -3063 . DOI: 10.3969/j.issn.1006-267x.2014.10.017

Abstract

As the most important and safest source of probiotics, lactic acid bacteria (LAB) has attracted a widespread concern. Besides, the research on the regulation of LAB on the intestinal barrier function in animals and human beings has become a hot issue. Plenty of in vivo and in vitro studies indicated that the probiotic effect of LAB was primarily through the regulation of intestinal barrier function. In contrast to rodents, there are much more researches on the application and less on the intestinal barrier function for LAB in pigs. Additionally, the specific mechanisms are still unknown. Furthermore, the probiotic effect of LAB is strain specific. As the porcine intestinal environment is very complicated, it is very difficult to explore deeply the modulation of LAB on the intestinal barrier function. In recent years, the development of new technologies such as genomics, proteomics and metabonomics provides new insights and approaches to explore the mechanisms of how LAB regulates the intestinal barrier function in vivo. This article reviewed the mechanisms and regulation of LAB on porcine intestinal barrier function, with the expectation to provide further knowledge of LAB and its application.

参考文献

[1] MENNIGEN R,BRUEWER M.Effect of probiotics on intestinal barrier function[J].Annals of the New York Academy of Sciences,2009,1165(1):183-189.  

[2] OHLAND C L,MACNAUGHTON W K.Probiotic bacteria and intestinal epithelial barrier function[J].American Journal of Physiology:Gastrointestinal and Liver Physiology,2010,298(6):G807-G819.

[3] BAUMGART D C,DIGNASS A U.Intestinal barrier function[J].Current Opinion in Clinical Nutrition and Metabolic Care,2002,5(6):685-694.  

[4] MAYNARD C L,ELSON C O,HATTON R D,et al.Reciprocal interactions of the intestinal microbiota and immune system[J].Nature,2012,489(7415):231-241.  

[5] SOMMER F,BCKHED F.The gut microbiota-masters of host development and physiology[J].Nature Reviews Microbiology,2013,11(4):227-238.  

[6] WALTER J.Ecological role of lactobacilli in the gastrointestinal tract:implications for fundamental and biomedical research[J].Applied and Environmental Microbiology,2008,74(16):4985-4996.  

[7] LI X J,YUE L Y,GUAN X F,et al.The adhesion of putative probiotic lactobacilli to cultured epithelial cells and porcine intestinal mucus[J].Journal of Applied Microbiology,2008,104(4):1082-1091.  

[8] GAO Y,HAN F,HUANG X,et al.Changes in gut microbial populations,intestinal morphology,expression of tight junction proteins,and cytokine production between two pig breeds after challenge with Escherichia coli K88:a comparative study[J].Journal of Animal Science,2013,91(12):5614-5625.  

[9] HOOPER L V,MACPHERSON A J.Immune adaptations that maintain homeostasis with the intestinal microbiota[J].Nature Reviews Immunology,2010,10(3):159-169.  

[10] SHANAHAN F.Probiotics in perspective[J].Gastroenterology,2010,139(6):1808-1812.  

[11] JOHANSSON M E V,SJÖVALL H,HANSSON G C.The gastrointestinal mucus system in health and disease[J].Nature Reviews Gastroenterology and Hepatology,2013,10(6):352-361.  

[12] TURNER J R.Intestinal mucosal barrier function in health and disease[J].Nature Reviews Immunology,2009,9(11):799-809.  

[13] PODOLSKY D K.Mucosal immunity and inflammation.Ⅴ.Innate mechanisms of mucosal defense and repair:the best offense is a good defense[J].American Journal of Physiology,1999,277(3 Pt 1):G495-G499.

[14] GUTTMAN J A,FINLAY B B.Tight junctions as targets of infectious agents[J].Biochimica et Biophysica Acta (BBA):Biomembranes,2009,1788(4):832-841.  

[15] CHIBA H,OSANAI M,MURATA M,et al.Transmembrane proteins of tight junctions[J].Biochimica et Biophysica Acta (BBA):Biomembranes,2008,1778(3):588-600.  

[16] FURUSE M.Molecular basis of the core structure of tight junctions[J].Cold Spring Harbor Perspectives in Biology,2010,2(1):a002907.

[17] MIYAUCHI E,MORITA H,TANABE S.Lactobacillus rhamnosus alleviates intestinal barrier dysfunction in part by increasing expression of zonula occludens-1 and myosin light-chain kinase in vivo[J].Journal of Dairy Science,2009,92(6):2400-2408.  

[18] MACPHERSON A J,MCCOY K D,JOHANSEN F E,et al.The immune geography of IgA induction and function[J].Mucosal Immunology,2008,1(1):11-22.  

[19] HAPFELMEIER S,LAWSON M A E,SLACK E,et al.Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses[J].Science,2010,328(5986):1705-1709.  

[20] SUZUKI K,MEEK B,DOI Y,et al.Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut[J].Proceedings of the National Academy of Sciences of the United States of America,2004,101(7):1981-1986.  

[21] VAISHNAVA S,YAMAMOTO M,SEVERSON K M,et al.The antibacterial lectin regⅢ gamma promotes the spatial segregation of microbiota and host in the intestine[J].Science,2011,334(6053):255-258.  

[22] NIJNIK A,HANCOCK R E W.Host defence peptides:antimicrobial and immunomodulatory activity and potential applications for tackling antibiotic-resistant infections[J].Emerging Health Threats Journal,2009,2:e1.

[23] MUNIZ L R,KNOSP C,YERETSSIAN G.Intestinal antimicrobial peptides during homeostasis,infection,and disease[J].Frontiers in Immunology,2012,3:310.

[24] SIGGERS R H,SIGGERS J,BOYE M,et al.Early administration of probiotics alters bacterial colonization and limits diet-induced gut dysfunction and severity of necrotizing enterocolitis in preterm pigs[J].The Journal of Nutrition,2008,138(8):1437-1444.

[25] HANSEN C H F,NIELSEN D S,KVERKA M,et al.Patterns of early gut colonization shape future immune responses of the host[J].PLoS One,2012,7(3): e34043.

[26] LIU H,ZHANG J,ZHANG S H,et al.Oral administration of Lactobacillus fermentum I5007 favors intestinal development and alters the intestinal microbiota in formula-fed piglets[J].Journal of Agricultural and Food Chemistry,2014,62(4):860-866.  

[27] FUENTES S,EGERT M,JIMNEZ-VALERA M,et al.Administration of Lactobacillus casei and Lactobacillus plantarum affects the diversity of murine intestinal lactobacilli,but not the overall bacterial community structure[J].Research in Microbiology,2008,159(4):237-243.  

[28] BEZKOROVAINY A.Probiotics:determinants of survival and growth in the gut[J].The American Journal of Clinical Nutrition,2001,73(Suppl.2):399S-405S.

[29] OHASHI Y,TOKUNAGA M,TAKETOMO N,et al.Stimulation of indigenous lactobacilli by fermented milk prepared with probiotic bacterium,Lactobacillus delbrueckii subsp bulgaricus strain 2038,in the pigs[J].Journal of Nutritional Science and Vitaminology,2007,53(1):82-86.  

[30] GUILLOTEAU P,MARTIN L,EECKHAUT V,et al.From the gut to the peripheral tissues:the multiple effects of butyrate[J].Nutrition Research Reviews,2010,23(2):366-384.  

[31] YU H F,WANG A N,LI X J,et al.Effect of viable Lactobacillus fermentum on the growth performance,nutrient digestibility and immunity of weaned pigs[J].Journal of Animal and Feed Sciences,2008,17(1):61-69.

[32] SUO C,YIN Y S,WANG X N,et al.Effects of Lactobacillus plantarum ZJ316 on pig growth and pork quality[J].BMC Veterinary Research,2012,8:89.

[33] WU S P,YUAN L J,ZHANG Y G,et al.Probiotic Lactobacillus rhamnosus GG mono-association suppresses human rotavirus-induced autophagy in the gnotobiotic piglet intestine[J].Gut Pathogens,2013,5(1):22.

[34] MAO Y,YU J L,LJUNGH A,et al.Intestinal immune response to oral administration of Lactobacillus reuteri R2LC,Lactobacillus plantarum DSM 9843,pectin and oatbase on methotrexate-induced enterocolitis in rats[J].Microbial Ecology in Health and Disease,1996,9(6):261-269.  

[35] FORSYTH C B,FARHADIA A,JAKATE S M,et al.Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress,gut leakiness,and liver injury in a rat model of alcoholic steatohepatitis[J].Alcohol,2009,43(2):163-172.  

[36] JOHNSON-HENRY K C,DONATO K A,SHEN-TU G,et al.Lactobacillus rhamnosus strain GG prevents enterohemorrhagic Escherichia coli O157 ∶ H7-induced changes in epithelial barrier function[J].Infection and Immunity,2008,76(4):1340-1348.  

[37] ANDERSON R C,COOKSON A L,MCNABB W C,et al.Lactobacillus plantarum DSM 2648 is a potential probiotic that enhances intestinal barrier function[J].FEMS Microbiology Letters,2010,309(2):184-192.

[38] SETH A,YAN F,POLK D B,et al.Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism[J].American Journal of Physiology:Gastrointestinal and Liver Physiology,2008,294(4):G1060-G1069.

[39] ROSELLI M,FINAMORE A,BRITTI M S,et al.The novel porcine Lactobacillus sobrius strain protects intestinal cells from enterotoxigenic Escherichia coli K88 infection and prevents membrane barrier damage[J].The Journal of Nutrition,2007,137(12):2709-2716.

[40] QIN H,ZHANG Z,HANG X,et al.L.plantarum prevents enteroinvasive Escherichia coli-induced tight junction proteins changes in intestinal epithelial cells[J].BMC Microbiology,2009,9:63.

[41] ZYREK A A,CICHON C,HELMS S,et al.Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCζ redistribution resulting in tight junction and epithelial barrier repair[J].Cellular Microbiology,2007,9(3):804-816.  

[42] YEUNG C Y,CHIANG CHIAU J S,CHAN W T,et al.In vitro prevention of Salmonella lipopolysaccharide-induced damages in epithelial barrier function by various Lactobacillus strains[J].Gastroenterology Research and Practice,2013,doi:10.1155/2013/973209.

[43] WANG X Q,YANG F,LIU C,et al.Dietary supplementation with the probiotic Lactobacillus fermentum I5007 and the antibiotic aureomycin differentially affects the small intestinal proteomes of weanling piglets[J].The Journal of Nutrition,2012,142(1):7-13.  

[44] MIHATSCH W A,BRAEGGER C P,DECSI T,et al.Critical systematic review of the level of evidence for routine use of probiotics for reduction of mortality and prevention of necrotizing enterocolitis and sepsis in preterm infants[J].Clinical Nutrition,2012,31(1):6-15.  

[45] WALTER J,BRITTON R A,ROOS S.Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm[J].Proceedings of National Academy of Sciences of the United States of America,2011,108:4645-4652.

[46] KO J S,YANG H R,CHANG J Y,et al.Lactobacillus plantarum inhibits epithelial barrier dysfunction and interleukin-8 secretion induced by tumor necrosis factor-α[J].World Journal of Gastroenterology,2007,13(13):1962-1965.  

[47] VLASOVA A N,CHATTHA K S,KANDASAMY S,et al.Lactobacilli and bifidobacteria promote immune homeostasis by modulating innate immune responses to human rotavirus in neonatal gnotobiotic pigs[J].PLoS One,2013,8(10):e76962.

[48] WEN K,LI G H,BUI T,et al.High dose and low dose Lactobacillus acidophilus exerted differential immune modulating effects on T cell immune responses induced by an oral human rotavirus vaccine in gnotobiotic pigs[J].Vaccine,2012,30(6):1198-1207.  

[49] PARVEZ S,MALIK K A,KANG S A,et al.Probiotics and their fermented food products are beneficial for health[J].Journal of Applied Microbiology,2006,100(6):1171-1185.  

[50] DE KEERSMAECKER S C J,VERHOEVEN T L A,DESAIR J,et al.Strong antimicrobial activity of Lactobacillus rhamnosus GG against Salmonella typhimurium is due to accumulation of lactic acid[J].FEMS Microbiology Letters,2006,259(1):89-96.  

[51] PRIDMORE R D,PITTET A C,PRAPLAN F,et al.Hydrogen peroxide production by Lactobacillus johnsonii NCC 533 and its role in anti-Salmonella activity[J].FEMS Microbiology Letters,2008,283(2):210-215.  

[52] OTERO M C,NADER-MACIAS M E.Inhibition of Staphylococcus aureus by H2O2-producing Lactobacillus gasseri isolated from the vaginal tract of cattle[J].Animal Reproduction Science,2006,96(1/2):35-46.

[53] COTTER P D,HILL C,ROSS R P.Bacteriocins:developing innate immunity for food[J].Nature Reviews Microbiology,2005,3(10):777-788.  

[54] BIERBAUM G,SAHL H G.Lantibiotics:mode of action,biosynthesis and bioengineering[J].Current Pharmaceutical Biotechnology,2009,10(1):2-18.  

[55] CLEUSIX V,LACROIX C,VOLLENWEIDER S,et al.Inhibitory activity spectrum of reuterin produced by Lactobacillus reuteri against intestinal bacteria[J].BMC Microbiology,2007,7:101.

[56] CORR S C,LI Y,RIEDEL C U,et al.Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118[J].Proceedings of the National Academy of Sciences of the United States of America,2007,104(18):7617-7621.  

[57] REA M C,CLAYTON E,O’CONNOR P M,et al.Antimicrobial activity of lacticin 3,147 against clinical Clostridium difficile strains[J].Journal of Medical Microbiology,2007,56(Pt 7):940-946.

[58] BRON P A,VAN BAARLEN P,KLEEREBEZEM M.Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa[J].Nature Reviews Microbiology,2012,10(1):66-78.

[59] YAN F,CAO H W,COVER T L,et al.Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth[J].Gastroenterology,2007,132(2):562-575.  

[60] BÄUERL C,PÉREZ-MARTÍNEZ G,YAN F,et al.Functional analysis of the p40 and p75 proteins from Lactobacillus casei BL23[J].Journal of Molecular Microbiology and Biotechnology,2010,19(4):231-241.  

[61] YAN F,CAO H W,COVER T L,et al.Colon-specific delivery of a probiotic-derived soluble protein ameliorates intestinal inflammation in mice through an EGFR-dependent mechanism[J].The Journal of Clinical Investigation,2011,121(6):2242-2253.  

[62] ELLI M,ZINK R,RYTZ A,et al.Iron requirement of Lactobacillus spp.in completely chemically defined growth media[J].Journal of Applied Microbiology,2000,88(4):695-703.  

[63] DEEPIKA G,CHARALAMPOPOULOS D.Surface and adhesion properties of lactobacilli[J].Advances in Applied Microbiology,2010,70:127-152.

[64] LEBEER S,VANDER LEYDEN J,DE KEERSMAECKER S C J.Genes and molecules of lactobacilli supporting probiotic action[J].Microbiology and Molecular Biology Reviews,2008,72(4):728-764.  

[65] TRAVASSOS L H,GIRARDIN S E,PHILPOTT D J,et al.Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition[J].EMBO Reports,2004,5(10):1000-1006.  

[66] VOLZ T,NEGA M,BUSCHMANN J,et al.Natural Staphylococcus aureus-derived peptidoglycan fragments activate NOD2 and act as potent costimulators of the innate immune system exclusively in the presence of TLR signals[J].The FASEB Journal,2010,24(10):4089-4102.  

[67] FERNANDEZ E M,VALENTI V,ROCKEL C,et al.Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide[J].Gut,2011,60(8):1050-1059.  

[68] DELCOUR J,FERAIN T,DEGHORAIN M,et al.The biosynthesis and functionality of the cell-wall of lactic acid bacteria[J].Antonie Van Leeuwenhoek,1999,76(1/2/3/4):159-184.

[69] ZEUTHEN L H,FINK L N,FRKIR H.Toll-like receptor 2 and nucleotide-binding oligomerization domain-2 play divergent roles in the recognition of gut-derived lactobacilli and bifidobacteria in dendritic cells[J].Immunology,2008,124(4):489-502.  

[70] GRANGETTE C,NUTTEN S,PALUMBO E,et al.Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids[J].Proceedings of the National Academy of Sciences of the United States of America,2005,102(29):10321-10326.  

[71] CLAES I J J,LEBEER S,SHEN C,et al.Impact of lipoteichoic acid modification on the performance of the probiotic Lactobacillus rhamnosus GG in experimental colitis[J].Clinical & Experimental Immunology,2010,162(2):306-314.  

[72] KAJI R,KIYOSHIMA-SHIBATA J,NAGAOKA M,et al.Bacterial teichoic acids reverse predominant IL-12 production induced by certain Lactobacillus strains into predominant IL-10 production via TLR2-dependent ERK activation in macrophages[J].The Journal of Immunology,2010,184(7):3505-3513.  

[73] LEBEER S,VERHOEVEN T L A,FRANCIUS G,et al.Identification of a gene cluster for the biosynthesis of a long,galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase[J].Applied and Environmental Microbiology,2009,75(11):3554-3563.  

[74] LEBEER S,CLAES I J J,VERHOEVEN T L A,et al.Exopolysaccharides of Lactobacillus rhamnosus GG form a protective shield against innate immune factors in the intestine[J].Microbial Biotechnology,2011,4(3):368-374.  

[75] YASUDA E,SERATA M,SAKO T.Suppressive effect on activation of macrophages by Lactobacillus casei strain shirota genes determining the synthesis of cell wall-associated polysaccharides[J].Applied and Environmental Microbiology,2008,74(15):4746-4755.  

[76] KONSTANTINOV S R,SMIDT H,DE VOS W M,et al.S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions[J].Proceedings of the National Academy of Sciences of the United States of America,2008,105(49):19474-19479.  

[77] BOEKHORST J,DE BEEN M W,KLEEREBEZEM M,et al.Genome-wide detection and analysis of cell wall-bound proteins with LPxTG-like sorting motifs[J].Journal of Bacteriology,2005,187(14):4928-4934.  

[78] REMUS D M,BONGERS R S,MEIJERINK M,et al.Impact of Lactobacillus plantarum sortase on target protein sorting,gastrointestinal persistence,and host immune response modulation[J].Journal of Bacteriology,2013,195(3):502-509.  
文章导航

/