肠道线虫与肠道菌群相互作用的研究进展

doi:10.12140/j.issn.1000-7423.2024.05.012

中国寄生虫学与寄生虫病杂志 ›› 2024, Vol. 42 ›› Issue (5): 642-647.doi: 10.12140/j.issn.1000-7423.2024.05.012

肠道线虫与肠道菌群相互作用的研究进展

张芷兰¹(), 尹思萱¹, 吕芳丽¹^,²^,^*()

1 中山大学医学院寄生虫学教研室，广东深圳 518107
2 中山大学附属第七医院科研中心，广东深圳 518107

收稿日期:2024-03-18 修回日期:2024-06-26 出版日期:2024-10-30 发布日期:2024-10-25
通讯作者: * 吕芳丽，女，博士，教授，从事寄生虫相关研究工作。E-mail：lvfangli@mail.sysu.edu.cn
作者简介:张芷兰（2002—），女，本科生，从事预防医学相关研究。E-mail：zhangzhlan@mail2.sysu.edu.cn
基金资助:
国家自然科学基金面上项目(82272366);国家自然科学基金面上项目(81971955);深圳市自然科学基金面上项目(JCYJ20220530145002006);广东省自然科学基金面上项目(2021A1515012115);广东省自然科学基金面上项目(2019A1515011667);广东省研究生教育创新计划(2021SFKC003);中山大学校级本科教学质量工程项目(SYSU Undergraduate Education〔2023〕96);中山大学校级本科教学质量工程项目(〔2022〕91)

Research progress on the interaction between intestinal nematodes and intestinal flora

ZHANG Zhilan¹(), YIN Sixuan¹, LV Fangli¹^,²^,^*()

1 Department of Parasitology, School of Medicine, Sun Yat-sen University, Shenzhen 518107, Guangdong, China
2 Scientific Research Center, the Seventh Affiliated Hospital of Sun Yat-sen University, Shenzhen 518107, Guangdong, China

Received:2024-03-18 Revised:2024-06-26 Online:2024-10-30 Published:2024-10-25
Contact: * E-mail: lvfangli@mail.sysu.edu.cn
Supported by:
National Natural Science Foundation of China(82272366);National Natural Science Foundation of China(81971955);Shenzhen Municipal Natural Science Foundation(JCYJ20220530145002006);Natural Science Foundation of Guangdong Province(2021A1515012115);Natural Science Foundation of Guangdong Province(2019A1515011667);Graduate Education Innovation Plan Project of Guangdong Province(2021SFKC003);Undergraduate Teaching Quality Engineering Project of Sun Yat-sen University, China(SYSU Undergraduate Education〔2023〕96);Undergraduate Teaching Quality Engineering Project of Sun Yat-sen University, China(〔2022〕91)

摘要/Abstract

摘要：

肠道菌群是人体肠道微环境的重要组成部分，在消化吸收、营养代谢、抵御病原体感染和调节自身免疫性疾病等方面起着重要作用。寄生于宿主肠道的寄生虫与宿主肠道菌群之间存在着复杂的相互作用，影响着宿主肠道的健康和相关疾病的发生发展。本文对宿主肠道线虫与肠道菌群相互作用的研究进展进行综述，以期为深入理解相关疾病的致病机制提供科学依据。

关键词: 肠道菌群, 肠道线虫, 相互作用

Abstract:

The intestinal flora is an important component of human intestinal microenvironment, playing important roles in digestion and absorption, nutrient metabolism, defense against pathogenic infections and regulation of autoimmune diseases. There are complex interactions between parasites residing in the host’s gut and the host’s gut microbiota, influencing the health of the host’s intestine and the onset and progression of related diseases. This article reviews the research progress on the interaction between host intestinal nematodes and intestinal flora, to provide scientific basis for a deeper understanding of the pathogenic mechanisms of related diseases.

Key words: Intestinal flora, Intestinal nematodes, Interaction

中图分类号:

R383.1

张芷兰, 尹思萱, 吕芳丽. 肠道线虫与肠道菌群相互作用的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(5): 642-647.

ZHANG Zhilan, YIN Sixuan, LV Fangli. Research progress on the interaction between intestinal nematodes and intestinal flora[J]. Chinese Journal of Parasitology and Parasitic Diseases, 2024, 42(5): 642-647.

参考文献 53

[1]	Papaiakovou M, Littlewood DTJ, Doyle SR, et al. Worms and bugs of the gut: the search for diagnostic signatures using barcoding, and metagenomics-metabolomics[J]. Parasit Vectors, 2022, 15(1): 118. doi: 10.1186/s13071-022-05225-7 pmid: 35365192
[2]	Kang WH, Jee SC. Enterobius vermicularis (pinworm) infection[J]. N Engl J Med, 2019, 381(1): e1.
[3]	Lin H, Yang GY. Strongyloidiasis of human and animals[J]. Chin J Zoonoses, 2016, 32(5): 477-484, 505. (in Chinese)
	(林海, 杨光友. 人和动物的类圆线虫病[J]. 中国人兽共患病学报, 2016, 32(5): 477-484, 505.)
[4]	Brooker S, Clements AC, Bundy DA. Global epidemiology, ecology and control of soil-transmitted helminth infections[J]. Adv Parasitol, 2006, 62: 221-261.
[5]	Horrocks V, King OG, Yip AYG, et al. Role of the gut microbiota in nutrient competition and protection against intestinal pathogen colonization[J]. Microbiology (Reading), 2023, 169(8): 001377.
[6]	Cortés A, Peachey L, Scotti R, et al. Helminth-microbiota cross-talk: a journey through the vertebrate digestive system[J]. Mol Biochem Parasitol, 2019, 233: 111222.
[7]	Drew GC, Stevens EJ, King KC. Microbial evolution and transitions along the parasite-mutualist continuum[J]. Nat Rev Microbiol, 2021, 19(10): 623-638. doi: 10.1038/s41579-021-00550-7 pmid: 33875863
[8]	Hooper LV, Littman DR, MacPherson AJ. Interactions between the microbiota and the immune system[J]. Science, 2012, 336(6086): 1268-1273. doi: 10.1126/science.1223490 pmid: 22674334
[9]	Gause WC, Maizels RM. Macrobiota: helminths as active participants and partners of the microbiota in host intestinal homeostasis[J]. Curr Opin Microbiol, 2016, 32: 14-18.
[10]	Brosschot TP, Reynolds LA. The impact of a helminth-modified microbiome on host immunity[J]. Mucosal Immunol, 2018, 11(4): 1039-1046. doi: 10.1038/s41385-018-0008-5 pmid: 29453411
[11]	Kato Y, Komatsu S. ASABF, a novel cysteine-rich antibacterial peptide isolated from the nematode Ascaris suum. Purification, primary structure, and molecular cloning of cDNA[J]. J Biol Chem, 1996, 271(48): 30493-30498. doi: 10.1074/jbc.271.48.30493 pmid: 8940016
[12]	Marillier RG, Michels C, Smith EM, et al. IL-4/IL-13 independent goblet cell hyperplasia in experimental helminth infections[J]. BMC Immunol, 2008, 9: 11. doi: 10.1186/1471-2172-9-11 pmid: 18373844
[13]	Datta R, DeSchoolmeester ML, Hedeler C, et al. Identification of novel genes in intestinal tissue that are regulated after infection with an intestinal nematode parasite[J]. Infect Immun, 2005, 73(7): 4025-4033. pmid: 15972490
[14]	Sun SM, Wang XL, Wu XP, et al. Toll-like receptor activation by helminths or helminth products to alleviate inflammatory bowel disease[J]. Parasit Vectors, 2011, 4: 186. doi: 10.1186/1756-3305-4-186 pmid: 21943110
[15]	Walusimbi B, Lawson MAE, Nassuuna J, et al. The effects of helminth infections on the human gut microbiome: a systematic review and meta-analysis[J]. Front Microbiomes, 2023, 2: 1174034.
[16]	Cooper P, Walker AW, Reyes J, et al. Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota[J]. PLoS One, 2013, 8(10): e76573.
[17]	Pryshliak OY, Protsyk AL, Semaniv MV, et al. Effect of probiotics on the intestinal microbiota of patients with giardiasis and ascariasis[J]. J Med Life, 2022, 15(10): 1278-1282. doi: 10.25122/jml-2022-0191 pmid: 36420289
[18]	Guernier V, Brennan B, Yakob L, et al. Gut microbiota disturbance during helminth infection: can it affect cognition and behaviour of children?[J]. BMC Infect Dis, 2017, 17(1): 58. doi: 10.1186/s12879-016-2146-2 pmid: 28073356
[19]	Ramírez-Carrillo E, Gaona O, Nieto J, et al. Disturbance in human gut microbiota networks by parasites and its implications in the incidence of depression[J]. Sci Rep, 2020, 10(1): 3680. doi: 10.1038/s41598-020-60562-w pmid: 32111922
[20]	Klomkliew P, Sawaswong V, Chanchaem P, et al. Gut bacteriome and metabolome of Ascaris lumbricoides in patients[J]. Sci Rep, 2022, 12(1): 19524. doi: 10.1038/s41598-022-23608-9 pmid: 36376367
[21]	Jenkins TP, Pritchard DI, Tanasescu R, et al. Experimental infection with the hookworm, Necator americanus, is associated with stable gut microbial diversity in human volunteers with relapsing multiple sclerosis[J]. BMC Biol, 2021, 19(1): 74.
[22]	Cantacessi C, Giacomin P, Croese J, et al. Impact of experimental hookworm infection on the human gut microbiota[J]. J Infect Dis, 2014, 210(9): 1431-1434. doi: 10.1093/infdis/jiu256 pmid: 24795483
[23]	Giacomin P, Zakrzewski M, Croese J, et al. Experimental hookworm infection and escalating gluten challenges are associated with increased microbial richness in celiac subjects[J]. Sci Rep, 2015, 5: 13797. doi: 10.1038/srep13797 pmid: 26381211
[24]	Chen HL, Mozzicafreddo M, Pierella E, et al. Dissection of the gut microbiota in mothers and children with chronic Trichuris trichiura infection in Pemba Island, Tanzania[J]. Parasit Vectors, 2021, 14(1): 62.
[25]	Lee SC, Tang MS, Lim YA, et al. Helminth colonization is associated with increased diversity of the gut microbiota[J]. PLoS Negl Trop Dis, 2014, 8(5): e2880.
[26]	Yang CN, Liang C, Lin CL, et al. Impact of Enterobius vermicularis infection and mebendazole treatment on intestinal microbiota and host immune response[J]. PLoS Negl Trop Dis, 2017, 11(9): e0005963.
[27]	Corthésy B. Multi-faceted functions of secretory IgA at mucosal surfaces[J]. Front Immunol, 2013, 4: 185. doi: 10.3389/fimmu.2013.00185 pmid: 23874333
[28]	Nguyen HT, Hongsrichan N, Intuyod K,et al. Strongyloides stercoralis infection induces gut dysbiosis in chronic kidney disease patients[J]. PLoS Negl Trop Dis, 2022, 16(9): e0010302.
[29]	Nguyen HT, Hongsrichan N, Intuyod K, et al. Investigation of gut microbiota and short-chain fatty acids in Strongyloides stercoralis-infected patients in a rural community[J]. Biosci Microbiota Food Health, 2022, 41(3): 121-129.
[30]	Jenkins TP, Formenti F, Castro C, et al. A comprehensive analysis of the faecal microbiome and metabolome of Strongyloides stercoralis infected volunteers from a non-endemic area[J]. Sci Rep, 2018, 8(1): 15651.
[31]	Rubel MA, Abbas A, Taylor LJ, et al. Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians[J]. Genome Biol, 2020, 21(1): 122. doi: 10.1186/s13059-020-02020-4 pmid: 32450885
[32]	Springer A, Wagner L, Koehler S, et al. Modulation of the porcine intestinal microbiota in the course of Ascaris suum infection[J]. Parasit Vectors, 2022, 15(1): 433. doi: 10.1186/s13071-022-05535-w pmid: 36397169
[33]	Wang YY, Liu F, Urban JF Jr, et al. Ascaris suum infection was associated with a worm-independent reduction in microbial diversity and altered metabolic potential in the porcine gut microbiome[J]. Int J Parasitol, 2019, 49(3/4): 247-256.
[34]	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]. Front Cell Infect Microbiol, 2018, 8: 271.
[35]	Sieng S, Chen P, Wang N,et al. Toxocara canis-induced changes in host intestinal microbial communities[J]. Parasit Vectors, 2023, 16(1): 462. doi: 10.1186/s13071-023-06072-w pmid: 38115028
[36]	Walk ST, Blum AM, Ewing SAS, et al. Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus[J]. Inflamm Bowel Dis, 2010, 16(11): 1841-1849.
[37]	Ramanan D, Bowcutt R, Lee SC, et al. Helminth infection promotes colonization resistance via type 2 immunity[J]. Science, 2016, 352(6285): 608-612. doi: 10.1126/science.aaf3229 pmid: 27080105
[38]	Rausch S, Midha A, Kuhring M, et al. Parasitic nematodes exert antimicrobial activity and benefit from microbiota-driven support for host immune regulation[J]. Front Immunol, 2018, 9: 2282. doi: 10.3389/fimmu.2018.02282 pmid: 30349532
[39]	Shimokawa C, Obi S, Shibata M, et al. Suppression of obesity by an intestinal helminth through interactions with intestinal microbiota[J]. Infect Immun, 2019, 87(6): e00042-19.
[40]	Su CW, Chen CY, Jiao LF, et al. Helminth-induced and Th2-dependent alterations of the gut microbiota attenuate obesity caused by high-fat diet[J]. Cell Mol Gastroenterol Hepatol, 2020, 10(4): 763-778. doi: S2352-345X(20)30105-3 pmid: 32629118
[41]	Houlden A, Hayes KS, Bancroft AJ, 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.
[42]	Holm JB, 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.
[43]	Rosa BA, Snowden C, Martin J, et al. Whipworm-associated intestinal microbiome members consistent across both human and mouse hosts[J]. Front Cell Infect Microbiol, 2021, 11: 637570.
[44]	Schachter J, Alvarinho de Oliveira D, da Silva CM, et al. Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation[J]. Infect Immun, 2020, 88(3): e00642-19.
[45]	Afrin T, Murase K, Kounosu A, et al. Sequential changes in the host gut microbiota during infection with the intestinal parasitic nematode Strongyloides venezuelensis[J]. Front Cell Infect Microbiol, 2019, 9: 217.
[46]	Pace F, Carvalho BM, Zanotto TM, et al. Helminth infection in mice improves insulin sensitivity via modulation of gut microbiota and fatty acid metabolism[J]. Pharmacol Res, 2018, 132: 33-46. doi: S1043-6618(17)31647-X pmid: 29653264
[47]	Fricke WF, Song Y, Wang AJ, et al. Erratum to: type 2 immunity-dependent reduction of segmented filamentous bacteria in mice infected with the helminthic parasite Nippostrongylus brasiliensis[J]. Microbiome, 2015, 3: 77.
[48]	Nobre V, Serufo JC, Carvalho ODOSS, et al. Alteration in the endogenous intestinal flora of Swiss Webster mice by experimental Angiostrongylus costaricensis infection[J]. Mem Inst Oswaldo Cruz, 2004, 99(7): 717-720.
[49]	Hayes KS, Bancroft AJ, Goldrick M, et al. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris[J]. Science, 2010, 328(5984): 1391-1394. doi: 10.1126/science.1187703 pmid: 20538949
[50]	Dea-Ayuela MA, Rama-Iñiguez S, Bolás-Fernandez F. Enhanced susceptibility to Trichuris muris infection of B10Br mice treated with the probiotic Lactobacillus casei[J]. Int Immunopharmacol, 2008, 8(1): 28-35.
[51]	Oliveira-Sequeira TCG, David ÉB, Ribeiro C, et al. Effect of Bifidobacterium animalis on mice infected with Strongyloides venezuelensis[J]. Rev Inst Med Trop Sao Paulo, 2014, 56(2): 105-109.
[52]	Jang S, Lakshman S, Beshah E, et al. Flavanol-rich cocoa powder interacts with Lactobacillus rhamnossus LGG to alter the antibody response to infection with the parasitic nematode Ascaris suum[J]. Nutrients, 2017, 9(10): 1113.
[53]	Thomas DJ, Husmann RJ, Villamar M,et al. Lactobacillus rhamnosus HN001 attenuates allergy development in a pig model[J]. PLoS One, 2011, 6(2): e16577.

肠道线虫与肠道菌群相互作用的研究进展

Research progress on the interaction between intestinal nematodes and intestinal flora

RichHTML

PDF (PC)

可视化

摘要/Abstract

引用本文

使用本文

参考文献 53

相关文章 15

编辑推荐

Metrics

本文评价

[1]	汪业彬, 沈续航, 邓国强, 胡赛敏, 汪飞, 张玲玲, 沈继龙. 黄山市乡村中老年人群无症状钩虫感染对肠道菌群和代谢的作用[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(1): 17-26.
[2]	曹得萍, 毋德芳, 庞明泉, 彭小红, 李大宇, 樊海宁. 棘球蚴病患者肠道菌群差异性分析[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(1): 103-107.
[3]	潘筱雯, 吴银娟, 何晴, 殷颖璇, 李学荣. 寄生蠕虫外泌体及其功能的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2022, 40(3): 390-395.
[4]	钟秋婷, 宋健平, 吕芳丽. 疟疾和肠道菌群的相互影响[J]. 中国寄生虫学与寄生虫病杂志, 2021, 39(4): 520-525.
[5]	侯永恒, 吕芳丽. 弓形虫感染与宿主细胞自噬的相互作用[J]. 中国寄生虫学与寄生虫病杂志, 2021, 39(4): 537-542.
[6]	何兴, 潘卫庆. miRNA介导血吸虫和宿主相互作用的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2020, 38(3): 259-262.
[7]	孙成松, 胡薇, 汪天平. 胞外囊泡介导血吸虫与宿主相互作用的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2020, 38(3): 378-382.
[8]	邓积广, 余水兰, 农智, 杨益超. 2006-2016年百色市城区中小学生肠道线虫调查结果分析[J]. 中国寄生虫学与寄生虫病杂志, 2018, 36(4): 330-332.
[9]	薛峰1，2，洪彩玲1，黄敏君1，2，孙岚1，2，甘绍伯1，2，谷俊朝1，2 *. 弓形虫GRA7致密颗粒蛋白与宿主巨噬细胞蛋白的相互作用[J]. 中国寄生虫学与寄生虫病杂志, 2014, 32(5): 6-352-356.
[10]	都建1 *，安然1，程里1，陈滢2，沈继龙3. 酵母双杂交筛选与弓形虫毒力因子ROP18 相互作用的宿主蛋白[J]. 中国寄生虫学与寄生虫病杂志, 2013, 31(1): 4-18-22.
[11]	娄忠子，李宏民，闫鸿斌，倪兴维，贾万忠*. 多房棘球蚴感染与宿主相互作用的免疫学机制研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2012, 30(5): 13-401-405.
[12]	郑斌, 尹志奎, 何蔼, 李卓雅, 詹希美. GST沉降技术验证弓形虫醛缩酶与肌动蛋白的相互作用[J]. 中国寄生虫学与寄生虫病杂志, 2011, 29(5): 8-363-367.
[13]	林绍雄;王善青;胡锡敏;陈冬燕;童重锦;李善文. 海南省中部山区土源性线虫感染情况[J]. 中国寄生虫学与寄生虫病杂志, 2010, 28(2): 19-160.
[14]	李燕菁;高原;谢朝勇. 2004-2008年南京市肠道线虫感染情况分析[J]. 中国寄生虫学与寄生虫病杂志, 2010, 28(1): 18-76.
[15]	叶环;章志量;罗冬娇;张仁;杨军;何桂坤. 杭州市3～6岁儿童常见肠道线虫感染现状[J]. 中国寄生虫学与寄生虫病杂志, 2007, 25(2): 18-159.