寄生虫与肠道菌群互作机制研究进展

doi:10.16431/j.cnki.1671-7236.2023.03.027

Abstract

Abstract: Gut microbiota is one of the important parts of animal organism,and it has coexisted with the body in the long process of evolution.Many parasites also parasitize the intestinal tract of the host,gut microbiota and parasites interact with each other.Gut microbiota can not only affect the complex processes of parasites invading,colonizing and causing disease to the host,but also regulate the intestinal health of animals,and play an important role in antagonizing the infection of foreign pathogens such as bacteria,viruses and intestinal protozoa.It plays an important role in maintaining the homeostasis of intestinal environment.Gut microbiota can affect host immunity through itself and its metabolites,so as to regulate the body’s own inflammatory response and resist intestinal parasite infection.Gut microbiota can also affect parasite invasion through space occupying effect and changes in the structure of intestinal microflora.Existing studies have found that the effects of parasite infection on gut microbiota homeostasis can not only have negative effects such as mechanical injury and inflammatory reaction,but also have beneficial regulation on the host body.After infecting the host,some parasites can activate the body-related immune response and stimulate the body to release anti-inflammatory factors,which can help the intestinal tract resist bacterial infection and reduce the inflammatory response.The excretion and secretion of some parasites can affect the structure of gut microbiota in the host body and act as an immunomodulator.In recent years,the interaction mechanism between microbiota and host pathogen antagonism has become a hot spot,which has been widely concerned by scholars at home and abroad.As a result,parasite therapy and gut microbiota transplantation have also become a research hotspot.The metabolites of parasites and intestinal flora also have certain effects on the intestinal environment and homeostasis,but the specific mechanism of their effects is not clear.There are few reports on the interaction mechanism between parasites and gut microbiota in China.The author mainly reviewed the interaction between parasites and gut microbiota in order to provide reference for researchers to carry out relevant research.

Key words: parasites; gut microbiota; interaction; infection

CLC Number:

S852.7

LI Mengrui, LI Yongxia, LIN Xiaofeng, HUANG Xiaohang, HUANG Zhijian, YIN Guangwen. Research Progress on the Interaction Mechanism Between Parasites and Gut Microbiota[J]. China Animal Husbandry and Veterinary Medicine, 2023, 50(3): 1129-1139.

References

[1] DEPOORTERE I.Taste receptors of the gut:Eemerging roles in health and disease[J].Gut,2013,63(1):179-190.
[2] DOMINGUEZ-BELLO M G,ELIZABETH K C,MONICA C,et al.Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns[J].Proceedings of the National Academy of Sciences,2010,107(26):11971-11975.
[3] SONNENBURG J L,XU J,LEIP D D,et al.Glycan foraging in vivo by an intestine-adapted bacterial symbiont[J].Science,2005,307(5717):1955-1959.
[4] LI W N,DENG Y,CHU Q,et al.Gut microbiome and cancer immunotherapy[J].Cancer Letters,2019,447:41-47.
[5] SHI N,LI N,DUAN X W,et al.Interaction between the gut microbiome and mucosal immune system[J].Military Medical Research,2017,4:14.
[6] FUKUDA S,TOH H,HASE K,et al.Bifidobacteria can protect from enteropathogenic infection through production of acetate[J].Nature,2011,469(7331):543-547.
[7] GOMAA E Z.Human gut microbiota/microbiome in health and diseases:A review[J].Antonie van Leeuwenhoek,2020,113(12):2019-2040.
[8] GOMES A C,HOFFMANN C,MOTA J F.The human gut microbiota:Metabolism and perspective in obesity[J].Gut Microbes,2018,9(4):308-325.
[9] MIYOSHI J,CHANG E B.The gut microbiota and inflammatory bowel diseases[J].Translational Research,2017(179):38-48.
[10] BAHK Y Y,SHIN E H,CHO S H,et al.Prevention and control strategies for parasitic infections in the Korea centers for disease control and prevention[J].The Korean Journal of Parasitology,2018,56(5):401-408.
[11] WORLD HEALTH ORGANIZATION.Sustaining the drive to overcome the global impact of neglected tropical diseases:Second WHO report on neglected tropical diseases[R].Geneva:World Health Organization,2011.
[12] PANELLI S,EPIS S,COCOCCIONI L,et al.Inflammatory bowel diseases,the hygiene hypothesis and the other side of the microbiota:Parasites and fungi[J].Pharmacological Research,2020,159:104962.
[13] STENSVOLD C R.Pinning down the role of common luminal intestinal parasitic protists in human health and disease-status and challenges[J].Parasitology,2019,146(6):695-701.
[14] RAMANAN D,BOWCUTT R,LEE S C,et al.Helminth infection promotes colonization resistance via type 2 immunity[J].Science,2016,352(6285):608-612.
[15] LEE S C,TANG M S,LIM Y A,et al.Helminth colonization is associated with increased diversity of the gut microbiota[J].PLoS Neglected Tropical Diseases,2014,8(5):e2880.
[16] YADAV P,DAS P,MIRDHA B R,et al.Current spectrum of malabsorption syndrome in adults in India[J].Indian Journal of Gastroenterology,2011,30(1):22-28.
[17] BOURÉE P,BISARO F.Diarrhées parasitaires[J].La Presse Médicale,2007,36(4):706-716.
[18] RAMANAN D,TANG M,BOWCUTT R,et al.Bacterial sensor NOD2 prevents inflammation of the small intestine by restricting the expansion of the commensal bacteroides vulgatus[J].Immunity,2014,41(2):311-324.
[19] STRACHAN D P.Hay fever,hygiene,and household size[J].BMJ Clinical Research,1989,299(6710):1259-1260.
[20] BACH J F.The hygiene hypothesis in autoimmunity:The role of pathogens and commensals[J].Nature Reviews Immunology,2018,18(2):105-120.
[21] CHUDNOVSKIY A,MORTHA A,KANA V,et al.Host-protozoan interactions protect from mucosal infections through activation of the inflammasome[J].Cell,2016,167(2):444-456.
[22] BROADHURST M J,LEUNG J M,KASHYAP V,et al.IL-22⁺ CD4⁺ T cells are associated with therapeutic Trichuris trichiura infection in an ulcerative colitis patient[J].Science Translational Medicine,2010,2(60):60ra88.
[23] SONNENBERG G F,MONTICELLI L A,ALENGHAT T,et al.Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria[J].Science,2012,336(6086):1321-1325.
[24] ZANDE H J P,ZAWISTOWSKA-DENIZIAK A,GUIGAS B.Immune Regulation of metabolic homeostasis by helminths and their molecules[J].Trends in Parasitology,2019,35(10):795-808.
[25] DING J,LIU X,BAI X,et al.Trichinella spiralis:Inflammation modulator[J].Journal of Helminthology,2020,94:e193.
[26] 邢鑫.旋毛虫感染小鼠肠道菌群变化与免疫应答关系初步研究[D].长春:吉林农业大学,2017. XING X.Preliminary study on the relationship between intestinal flora changes and immune response in mice infected with Trichinella spiralis[D].Changchun:Jilin Agricultural University,2017.(in Chinese)
[27] RAMASWAMY K,KUMAR P,HE Y X.A role for parasite-induced PGE₂ in IL-10-mediated host immunoregulation by skin stage schistosomula of Schistosoma mansoni[J].Journal of Immunology,2000,165(8):4567-4574.
[28] 宋秋月,张亦舒,张蓓蓓,等.日本血吸虫不同感染程度对小鼠肠道菌群的影响[J].热带医学杂志,2020,20(3):303-308. SONG Q Y,ZHANG Y S,ZHANG B B,et al.Effects of different infection degrees of Schistosoma japonicum on intestinal flora in mice[J].Journal of Tropical Medicine,2020,20(3):303-308.(in Chinese)
[29] SHIN N R,WHON T W,BAE J W.Proteobacteria:Microbial signature of dysbiosis in gut microbiota[J].Trends in Biotechnology,2015,33(9):496-503.
[30] LITVAK Y,BYNDLOSS M X,TSOLIS R M,et al.Dysbiotic proteobacteria expansion:A microbial signature of epithelial dysfunction[J].Current Opinion in Microbiology,2017,39:1-6.
[31] JENKINS T P,RATHNAYAKA Y,PERERA P K,et al.Infections by human gastrointestinal helminths are associated with changes in faecal microbiota diversity and composition[J].PLoS One,2017,12(9):e0184719.
[32] LEE S C,TANG M S,LIM Y A L,et al.Correction:Helminth colonization is associated with increased diversity of the gut microbiota[J]. PLoS Neglected Tropical Diseases,2021,15(4):e0009325.
[33] LAFOREST-LAPOINTE I,ARRIETA M C.Microbial eukaryotes:A missing link in gut microbiome studies[J].mSystems,2018,3(2):e00201-17.
[34] ANDERSEN L O,BONDE I,NIELSEN H B,et al.A retrospective metagenomics approach to studying blastocystis[J].FEMS Microbiology Ecology,2015,91(7):fiv072.
[35] RAETZ M,HWANG S H,WILHELM C L,et al.Parasite-induced TH1 cells and intestinal dysbiosis cooperate in IFN-γ-dependent elimination of Paneth cells[J]. Nature Immunology,2013,14(2):136-142.
[36] IEBBA V,SANTANGELO F,TOTINO V,et al.Gut microbiota related to giardia duodenalis,Entamoeba spp. and blastocystis hominis infections in humans from Côte d’Ivoire[J].Journal of Infection in Developing Countries,2016,10(9):1035-1041.
[37] CANTACESSI C,GIACOMIA P,CROESE J,et al.Impact of experimental hookworm infection on the human gut microbiota[J].The Journal of Infectious Diseases,2014,210(9):1431-1434.
[38] DUQUE-CORREA M A,KARP N A,CARTHY C M,et al.Exclusive dependence of IL-10Rα signalling on intestinal microbiota homeostasis and control of whipworm infection[J].PLoS Pathogens,2019,15(1):e1007265.
[39] HOULDEN A,HAYES K S,BANCROFT A J,et al.Chronic Trichuris muris infection in C57BL/6 mice causes significant changes in host microbiota and metabolome:Effects reversed by pathogen clearance[J].PLoS One,2015,10(5):e0125945.
[40] HOLM J B,SOROBETEA D,KIILERICH P,et al.Chronic Trichuris muris infection decreases diversity of the intestinal microbiota and concomitantly increases the abundance of Lactobacilli[J].PLoS One,2015,10(5):e0125495.
[41] WU J,ZHU Y,ZHOU L,et al.Parasite-derived excretory-secretory products alleviate gut microbiota dysbiosis and improve cognitive impairment induced by a high-fat diet[J]. Frontiers in Immunology,2021,12:710513.
[42] MACDONALD S E,DIEMEN P M V,MARTINEAU H,et al.Impact of Eimeria tenella coinfection on Campylobacter jejuni colonization of the chicken[J].Infection and Immunity,2019,87(2):e00772-18.
[43] HUGOT J P,CHAMAILLARD M,ZOUALI H,et al.Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn’s disease[J].Nature,2001,411(6837):599-603.
[44] ELLIOTT D E,SETIAWAN T,METWAIL A,et al.Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice[J].European Journal of Immunology,2004,34(10):2690-2698.
[45] SMITH P,MANGAN N E,WALSH C M,et al.Infection with a helminth parasite prevents experimental colitis via a macrophage-mediated mechanism[J].Journal of Immunology,2007,178(7):4557-4566.
[46] 徐慧雯,曹建平,郑葵阳,等.寄生虫感染治疗炎症性肠病的研究进展[J].中国寄生虫学与寄生虫病杂志,2017,35(2):173-179. XU H W,CAO J P,ZHENG K Y,et al.Research progress of parasitic infection in the treatment of inflammatory bowel disease[J].Chinese Journal of Parasitology and Parasitic Diseases,2017,35(2):173-179.(in Chinese)
[47] MAIZELS R M,BALIC A,GOMEZ-ESCOBAR N,et al.Helminth parasites-masters of regulation[J].Immunological Reviews,2004,201:89-116.
[48] ELLIOTT D E,WEINSTOCK J V.Where are we on worms?[J].Current Opinion in Gastroenterology,2012,28(6):551-556.
[49] MCSORLEY H J,CHAYE M A M,SMITS H H.Worms:Pernicious parasites or allies against allergies?[J].Parasite Immunology,2019,41(6):e12574.
[50] TAHAPARY D L,RUITER K D,MARTIN I,et al.Helminth infections and type 2 diabetes:A cluster-randomized placebo controlled SUGARSPIN trial in Nangapanda,Flores,Indonesia[J].BMC Infectious Diseases,2015,15:133.
[51] VARYANI F,FLEMING J O,MAIZELS R M.Helminths in the gastrointestinal tract as modulators of immunity and pathology[J].American Journal of Physiology-Gastrointestinal and Liver Physiology,2017,312(6):G537-G549.
[52] WU Z,WANG L,TANG Y,et al.Parasite-derived proteins for the treatment of allergies and autoimmune diseases[J].Frontiers in Microbiology,2017,8:2164.
[53] GAZE S,MCSORLEY H J,DAVESON J,et al.Characterising the mucosal and systemic immune res-ponses to experimental human hookworm infection[J].PLoS Pathogens,2012,8(2):e1002520.
[54] VAN LIEMP T E,VAN VLIET S J,ENGERING A,et al. Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation[J]. Cellular & Molecular Immunology,2007,44(10):2605-2615.
[55] 宋伊宁,徐静,庞建达,等.旋毛虫感染早期小鼠肠道病理变化及免疫调节相关细胞因子表达的研究[J].中国人兽共患病学报,2019,35(8):715-719. SONG Y N,XU J,PANG J D,et al.Study on intestinal pathological changes and expression of immunomodulatory related cytokines in mice infected with Trichinella spiralis[J].Chinese Journal of Zoonoses,2019,35(8):715-719.(in Chinese)
[56] MIDHA A,JANEK K,NIEWIENDA A,et al.The intestinal roundworm ascaris suum releases antimicrobial factors which interfere with bacterial growth and biofilm formation[J].Frontiers Media,2018,8:271.
[57] HARNETT W.Secretory products of helminth parasites as immunomodulators[J].Molecular and Biochemical Pparasitology,2014,195(2):130-136.
[58] CORREALE J,GAITÁN M I.Multiple sclerosis and environmental factors:The role of vitamin D,parasites,and Epstein-Barr virus infection[J].Acta Neurologica Scandinavica,2015,132(199):46-55.
[59] PIERCE D,MERONE L,LEWIS C,et al.Safety and tolerability of experimental hookworm infection in humans with metabolic disease:Study protocol for a phase 1b randomised controlled clinical trial[J].BMC Endocrine Disorders,2019,19(1):136.
[60] KRUININGEN H J V,WEST A B.Potential danger in the medical use of Trichuris suis for the treatment of inflammatory bowel disease[J].Inflammatory Bowel Diseases,2005,11(5):515.
[61] REYNOLDS L A,FINLAY B B,MAIZELS R M.Cohabitation in the intestine:Interactions among helminth parasites,bacterial microbiota,and host immunity[J].The Journal of Immunology,2015,195(9):4059-4066.
[62] ABDALLAH I N,RAGAB S H,ABD E,et al.Frequency of firmicutes and bacteroidetes in gut microbiota in obese and normal weight egyptian children and adults[J].Archives of Medical Science,2011,7(3):501-507.
[63] CABALLERO S,PAMER E G.Microbiota-mediated inflammation and antimicrobial defense in the intestine[J].Annual Review of Immunologgy,2015,33:227-256.
[64] VERSINI M,JEANDEL P Y,BASHI T,et al.Unraveling the hygiene hypothesis of helminthes and autoimmunity:Origins,pathophysiology,and clinical applications[J].BMC Medicine,2015(13):81.
[65] ZAISS M M,HARRIS N L.Interactions between the intestinal microbiome and helminth parasites[J].Parasite Immunology,2016,38(1):5-11.
[66] LI R W,LI W,SUN J,et al.The effect of helminth infection on the microbial composition and structure of the caprine abomasal microbiome[J].Scientific Reports,2016,6:20606.
[67] WILLS-KARP M,SANTELIZ J,KARP C L.The germless theory of allergic disease:Rrevisiting the hygiene hypothesis[J].Nature Reviews Immunology,2001,1(1):69-75.
[68] BENSON A,PIFER R,BEHRENDT C L,et al.Gut commensal bacteria direct a protective immune response against Toxoplasma gondii[J].Cell Host Microbe,2009,6(2):187-196.
[69] HEIMESAATEI M M,BERESWILL S,FISCHER A,et al.Gram-negative bacteria aggravate murine small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii[J].Journal of Immunology,2006,177(12):8785-8795.
[70] PERDIGON G,ALVAREZ S,RACHID M,et al.Immune system stimulation by probiotics[J].Journal of Dairy Science,1995,78(7):1597-1606.
[71] FENG Y,PENG Y,SONG X,et al.Anopheline mosquitoes are protected against parasite infection by tryptophan catabolism in gut microbiota[J].Nature Microbiology,2022,7(5):707-715.
[72] MYHILL L J,STOLLZENBACHTOL S,MEJER H,et al.Parasite-probiotic interactions in the gut:Bacillus sp.and Enterococcus faecium regulate type-2 inflammatory responses and modify the gut microbiota of pigs during helminth infection[J].Frontiers in Immunology,2021,12:793260.
[73] EICHENBERGER R M,STEPHANIE R,LINDA J,et al.Hookworm secreted extracellular vesicles interact with host cells and prevent inducible colitis in mice[J].Frontiers in Immunology,2018,9:850.
[74] ATARASHI K,TANOUE T,SHIMA T,et al.Induction of colonic regulatory T cells by indigenous Clostridium species[J].Science,2011,331(6015):337-341.
[75] 王慧芳.乳杆菌S-层蛋白的肠道免疫调节功能及作用机制研究[D].无锡:江南大学,2020. WANG H F.Intestinal immunoregulatory function and mechanism of Lactobacillus S-layer protein[D].Wuxi:Jiangnan University,2020.(in Chinese)
[76] TURRONI F,VAN SINDEREN D,VENTURA M.Genomics and ecological overview of the genus Bifidobacterium[J].International Journal of Food Microbiology,2011,149(1):37-44.
[77] SANO T,KAGEYAMA T,FANG V,et al.Redundant cytokine requirement for intestinal microbiota-induced Th17 cell differentiation in draining lymph nodes[J].Cell Reports,2021,36(8):109608.
[78] PEREIRA G Q,GOMES L A,SANTOS I S,et al.Fecal microbiota transplantation in puppies with canine Parvovirus infection[J].Journal of Veterinary Internal Medicine,2018,32(2):707-711.
[79] ZUZARTE-LUIS V,MOTA M M.Parasite sensing of host nutrients and environmental cues[J].Cell Host Microbe,2018,23(6):749-758.
[80] RAJENDRAN E,HAPUARACHCHI S V,MILLER C M,et al.Cationic amino acid transporters play key roles in the survival and transmission of apicomplexan parasites[J].Nature Communications,2017,8:14455.
[81] PARTIDA-RODRÍGUEZ O,SERRANO-VÁZQUEZ A,NIEVES-RAMíREZ M E,et al.Human intestinal microbiota:Interaction between parasites and the host immune response[J]. Archives of Medical Research,2017,48(8):690-700.
[82] REYNOLDS L A,SMITH K A,FILBEY K J,et al.Commensal-pathogen interactions in the intestinal tract[J].Gut Microbes,2014,5(4):522-532.
[83] ZHOU S,LU Y,CHEN J,et al.Parasite reliance on its host gut microbiota for nutrition and survival[J].ISME Journal,2022,16(11):2574-2586.
[84] BERRILLI F,DI CAVE D,CAVALLERO S,et al.Interactions between parasites and microbial communities in the human gut[J].Frontiers in Cellular and Infection Microbiology,2012,2:141.
[85] ATARASHI K,TANOUE T,ANDO M,et al.Th17 cell induction by adhesion of microbes to intestinal epithelial cells[J].Cell,2015,163(2):367-380.
[86] BYERS J,EICHINGER D.Entamoeba invadens:Restriction of ploidy by colonic short chain fatty acids[J].Experimental Parasitology,2005,110(3):203-206.
[87] LAWSON M A E,ROBERTS I S,GRENCIS R K.The interplay between Trichuris and the microbiota[J].Parasitology,2021,148(14):1-8.
[88] CHEN H,LI G,ZHANG J,et al.Sodium butyrate ameliorates Schistosoma japonicum-induced liver fibrosis by inhibiting HMGB1 expression[J].Experimental Parasitology,2021,231:108-171.
[89] 李云飞.短链脂肪酸对秀丽隐杆线虫寿命的影响及分子机制的初步探究[D].长春:长春理工大学,2019. LI Y F.Effects of short-chain fatty acids on the lifespan of Caenorhabditis elegans and a preliminary study on the molecular mechanism[D].Changchun:Changchun University of Technology,2019.(in Chinese)
[90] HUMEN M A,ANTONI G L D,BENYACOUB J,et al.Lactobacillus johnsonii La1 antagonizes giardia intestinalis in vivo[J].Infection and Immunity,2005,73(2):1265-1269.
[91] SHUKLA G,DEVI P,SEHGAL R.Effect of Lactobacillus casei as a probiotic on modulation of giardiasis[J].Digestive Diseases and Sciences,2008,53(10):2671-2679.
[92] DRIDER D,BENDALI F,NAGHMOUCHI K,et al.Bacteriocins:Not only antibacterial agents[J]. Probiotics Antimicrob Proteins,2016,8(4):177-182.
[93] CLWUSIX V,LACROIX C,VOLLENWEIDER S,et al.Glycerol induces reuterin production and decreases Escherichia coli population in an in vitro model of colonic fermentation with immobilized human feces[J].FEMS Microbiology Ecology,2008,63(1):56-64.
[94] MIYAUCHI E,SHIMOKAWA C,STEIMLE A,et al.The impact of the gut microbiome on extra-intestinal autoimmune diseases[J]. Nature Reviews Immunology,2022,23(1):9-23.
[95] 王志华,贾俊鹏,MATJEKE R S,等,微生态制剂调控比格幼犬生长性能和肠道菌群的研究[J].中国畜牧兽医,2022,49(2):510-520. WANG Z H,JIA J P,MATJEKE R S,et al.Regulation of growth performance and intestinal microflora in Beagle puppies by microecologics[J].China Animal Husbandry & Veterinary Medicine,2022,49(2):510-520.(in Chinese)

Research Progress on the Interaction Mechanism Between Parasites and Gut Microbiota

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