Food and Fermentation Industries >

2024 , Vol. 50 >Issue 15: 340 - 349

DOI: https://doi.org/10.13995/j.cnki.11-1802/ts.037534

In vivo and in vitro intestinal models involved in foodborne pathogens

  • SONG Yiyang ,
  • WU Mengjie ,
  • DONG Qingli ,
  • LI Zhuosi
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  • (School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China)

Received date: 2023-10-02

  Revised date: 2023-10-27

  Online published: 2024-08-21

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Abstract

In vitro and in vivo intestinal models are an important tool for studying foodborne pathogenic bacteria.These models have been widely used to study the pathogenesis gene-to-phenotype, tolerance, immune responses, and vaccine development of foodborne pathogens.Although there have been numerous advancements in the study of intestinal models of foodborne pathogens both domestically and internationally, there is a lack of systematic summary.This review summarizes the application of in vitro and in vivo models in studies on foodborne pathogens, including rodent model, nonhuman primate model, cellular models, human intestinal organoids, and other in vitro and in vivo models.Additionally, it provides a detailed description of the strengths and weaknesses of all these models.Animal models can comprehensive review the progression of foodborne disease infections and the host immune response, but the results cannot be fully applied to humans due to species differences in physiology and pathology.Three dimensional in vitro cell culture models, especially organoids and organs-on-chips, using human cells have huge potential for studying the virulence mechanisms of foodborne pathogens at micro-level and the cell and tissue tropism of foodborne pathogens.The development of this review can serve as a scientific basis and useful reference for studying foodborne pathogens.

Key words： foodborne pathogens; in vivo model; in vitro model; human intestinal organoids; toxicity evaluation

Cite this article

SONG Yiyang , WU Mengjie , DONG Qingli , LI Zhuosi . In vivo and in vitro intestinal models involved in foodborne pathogens[J]. Food and Fermentation Industries, 2024 , 50(15) : 340 -349 . DOI: 10.13995/j.cnki.11-1802/ts.037534

References

[1] CHARLIER C, PERRODEAU É, LECLERCQ A, et al.Clinical features and prognostic factors of listeriosis:The MONALISA national prospective cohort study[J].The Lancet Infectious Diseases, 2017, 17(5):510-519.
[2] 覃兰迁, 刘霞, 刘诚志, 等.迷迭香水提物对沙门氏菌致小鼠肠道损伤的抗炎保护作用研究[J].饲料研究, 2023, 46(11):81-85.
QIN L Q, LIU X, LIU C Z, et al.Study on anti-inflammatory and protective effect of Rosmarinus officinalis extract on intestinal injury induced by Salmonella in mice[J].Feed Research, 2023, 46(11):81-85.
[3] DONG N, LI X R, XUE C Y, et al.Astragalus polysaccharides attenuated inflammation and balanced the gut microflora in mice challenged with Salmonella typhimurium[J].International Immunopharmacology, 2019, 74:105681.
[4] 王兆雨, 吴晓宇, 裴小琪, 等.生物活性肽对产肠毒素大肠杆菌诱导的小鼠肠道损伤的缓解作用[J].动物营养学报, 2023, 35(7):4659-4667.
WANG Z Y, WU X Y, PEI X Q, et al.Mitigative effects of bioactive peptide on intestinal injury of mice induced by enterotoxigenic Escherichia coli[J].Chinese Journal of Animal Nutrition, 2023, 35(7):4659-4667.
[5] HUGENHOLTZ F, DE VOS W M.Mouse models for human intestinal microbiota research:A critical evaluation[J].Cellular and Molecular Life Sciences:CMLS, 2018, 75(1):149-160.
[6] FAURE S, PERRIN-GUYOMARD A, DELMAS J M, et al.Transfer of plasmid-mediated CTX-M-9 from Salmonella enterica serotype Virchow to Enterobacteriaceae in human flora-associated rats treated with cefixime[J].Antimicrobial Agents and Chemotherapy, 2010, 54(1):164-169.
[7] LECUIT M, DRAMSI S, GOTTARDI C, et al.A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes[J].The EMBO Journal, 1999, 18(14):3956-3963.
[8] LECUIT M, VANDORMAEL-POURNIN S, LEFORT J, et al.A transgenic model for listeriosis:Role of internalin in crossing the intestinal barrier[J].Science, 2001, 292(5522):1722-1725.
[9] BARRÉ-SINOUSSI F, MONTAGUTELLI X.Animal models are essential to biological research:Issues and perspectives[J].Future Science OA, 2015, 1(4):FSO63.
[10] SEOK J, WARREN H S, CUENCA A G, et al.Genomic responses in mouse models poorly mimic human inflammatory diseases[J].Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(9):3507-3512.
[11] RASMUSSEN A L, OKUMURA A, FERRIS M T, et al.Host genetic diversity enables Ebola hemorrhagic fever pathogenesis and resistance[J].Science, 2014, 346(6212):987-991.
[12] HIGGINSON E E, PANDA A, TOAPANTA F R, et al.Immunogenicity and efficacy of live-attenuated Salmonella Typhimurium vaccine candidate CVD 1926 in a Rhesus macaque model of gastroenteritis[J].Infection and Immunity, 2021, 89(10):e0008721.
[13] ROLLENHAGEN J E, JONES F, HALL E, et al.Establishment, validation, and application of a new world primate model of enterotoxigenic Escherichia coli disease for vaccine development[J].Infection and Immunity, 2019, 87(2):e00634-e00618.
[14] TAYLOR F B Jr, TESH V L, DEBAULT L, et al.Characterization of the baboon responses to Shiga-like toxin:Descriptive study of a new primate model of toxic responses to Stx-1[J].The American Journal of Pathology, 1999, 154(4):1285-1299.
[15] SANTOS R L, ALMEIDA A P, XAVIER M N, et al.Enteric pathology and Salmonella-induced cell death in healthy and SIV-infected rhesus macaques[J].Veterinary Pathology, 2011, 48(5):933-941.
[16] MATSUHISA F, KITAJIMA S, NISHIJIMA K, et al.Transgenic rabbit models:Now and the future[J].Applied Sciences, 2020, 10(21):7416.
[17] KUEHL C J, D’GAMA J D, WARR A R, et al.An oral inoculation infant rabbit model for Shigella infection[J].mBio, 2020, 11(1):e03105-e03119.
[18] HECZKO U, ABE A, FINLAY B B.Segmented filamentous bacteria prevent colonization of enteropathogenic Escherichia coli O103 in rabbits[J].The Journal of Infectious Diseases, 2000, 181(3):1027-1033.
[19] RITCHIE J M, RUI H P, ZHOU X H, et al.Inflammation and disintegration of intestinal villi in an experimental model for Vibrio parahaemolyticus-induced diarrhea[J].PLoS Pathogens, 2012, 8(3):e1002593.
[20] RUI H P, RITCHIE J M, BRONSON R T, et al.Reactogenicity of live-attenuated Vibrio cholerae vaccines is dependent on flagellins[J].Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(9):4359-4364.
[21] MEURENS F, SUMMERFIELD A, NAUWYNCK H, et al.The pig:A model for human infectious diseases[J].Trends in Microbiology, 2012, 20(1):50-57.
[22] DAWSON H D, SMITH A D, CHEN C, et al.An in-depth comparison of the porcine, murine and human inflammasomes;lessons from the porcine genome and transcriptome[J].Veterinary Microbiology, 2017, 202:2-15.
[23] MEURENS F, BERRI M, AURAY G, et al.Early immune response following Salmonella enterica subspecies enterica serovar Typhimurium infection in porcine jejunal gut loops[J].Veterinary Research, 2009, 40(1):5.
[24] AGUIRRE GARCIA M, HILLION K, CAPPELIER J M, et al.Intestinal organoids:New tools to comprehend the virulence of bacterial foodborne pathogens[J].Foods, 2022, 11(1):108.
[25] GRASSART A, MALARDÉ V, GOBAA S, et al.Bioengineered human organ-on-chip reveals intestinal microenvironment and mechanical forces impacting Shigella infection[J].Cell Host & Microbe, 2019, 26(3):435-444.
[26] MATHIPA M G, THANTSHA M S, BHUNIA A K.Lactobacillus casei expressing internalins A and B reduces Listeria monocytogenes interaction with Caco-2 cells in vitro[J].Microbial Biotechnology, 2019, 12(4):715-729.
[27] TAKAHASHI A, SATO Y, SHIOMI Y, et al.Mechanisms of chloride secretion induced by thermostable direct haemolysin of Vibrio parahaemolyticus in human colonic tissue and a human intestinal epithelial cell line[J].Journal of Medical Microbiology, 2000, 49(9):801-810.
[28] TAKAHASHI A, IIDA T, NAIM R, et al.Chloride secretion induced by thermostable direct haemolysin of Vibrio parahaemolyticus depends on colonic cell maturation[J].Journal of Medical Microbiology, 2001, 50(10):870-878.
[29] MCNAMARA B P, KOUTSOURIS A, O’CONNELL C B, et al.Translocated EspF protein from enteropathogenic Escherichia coli disrupts host intestinal barrier function[J].The Journal of Clinical Investigation, 2001, 107(5):621-629.
[30] ZAMORA C Y, WARD E M, KESTER J C, et al.Application of a gut-immune co-culture system for the study of N-glycan-dependent host-pathogen interactions of Campylobacter jejuni[J].Glycobiology, 2020, 30(6):374-381.
[31] RODRIGUES R C, POCHERON A L, CAPPELIER J M, et al.An adapted in vitro assay to assess Campylobacter jejuni interaction with intestinal epithelial cells:Taking into stimulation with TNFα[J].Journal of Microbiological Methods, 2018, 149:67-72.
[32] GERARDI G, RIVERO-PÉREZ M D, CAVIA-SAIZ M, et al.Wine pomace product inhibit Listeria monocytogenes invasion of intestinal cell lines Caco-2 and SW-480[J].Foods, 2021, 10(7):1485.
[33] GHARBI Y, FHOULA I, RUAS-MADIEDO P, et al.In-vitro characterization of potentially probiotic Lactobacillus strains isolated from human microbiota:Interaction with pathogenic bacteria and the enteric cell line HT29[J].Annals of Microbiology, 2019, 69(1):61-72.
[34] LANGERHOLC T, MARAGKOUDAKIS P A, WOLLGAST J, et al.Novel and established intestinal cell line models-An indispensable tool in food science and nutrition[J].Trends in Food Science & Technology, 2011, 22:S11-S20.
[35] BARRILA J, YANG J, CRABBÉ A, et al.Three-dimensional organotypic co-culture model of intestinal epithelial cells and macrophages to study Salmonella enterica colonization patterns[J].NPJ Microgravity, 2017, 3:10.
[36] NICKERSON C A, GOODWIN T J, TERLONGE J, et al.Three-dimensional tissue assemblies:Novel models for the study of Salmonella enterica serovar Typhimurium pathogenesis[J].Infection and Immunity, 2001, 69(11):7106-7120.
[37] 陈晓清, 焦红, 程树军, 等.Caco-2细胞与肠道菌共培养初建体外肠道共生模型[J].中山大学学报(医学科学版), 2012, 33(1):121-126.
CHEN X Q, JIAO H, CHENG S J, et al.Co-culture of Caco-2 intestinal cell and intestinal floras to build an in vitro intestinal model[J].Journal of Sun Yat-Sen University (Medical Sciences), 2012, 33(1):121-126.
[38] SATO T, VRIES R G, SNIPPERT H J, et al.Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche[J].Nature, 2009, 459(7244):262-265.
[39] ZIETEK T, RATH E, HALLER D, et al.Intestinal organoids for assessing nutrient transport, sensing and incretin secretion[J].Scientific Reports, 2015, 5:16831.
[40] WANG X, YAMAMOTO Y, WILSON L H, et al.Cloning and variation of ground state intestinal stem cells[J].Nature, 2015, 522(7555):173-178.
[41] IN J, FOULKE-ABEL J, ZACHOS N C, et al.Enterohemorrhagic Escherichia coli reduce mucus and intermicrovillar bridges in human stem cell-derived colonoids[J].Cellular and Molecular Gastroenterology and Hepatology, 2016, 2(1):48-62.
[42] VANDUSSEN K L, MARINSHAW J M, SHAIKH N, et al.Development of an enhanced human gastrointestinal epithelial culture system to facilitate patient-based assays[J].Gut, 2015, 64(6):911-920.
[43] CROWLEY S M, HAN X, ALLAIRE J M, et al.Intestinal restriction of Salmonella Typhimurium requires caspase-1 and caspase-11 epithelial intrinsic inflammasomes[J].PLoS Pathogens, 2020, 16(4):e1008498.
[44] WILSON S S, TOCCHI A, HOLLY M K, et al.A small intestinal organoid model of non-invasive enteric pathogen-epithelial cell interactions[J].Mucosal Immunology, 2015, 8(2):352-361.
[45] GEISER P, DI MARTINO M L, SAMPERIO VENTAYOL P, et al.Salmonella enterica serovar typhimurium exploits cycling through epithelial cells to colonize human and murine enteroids[J].mBio, 2021, 12(1):e02684-e02620.
[46] PRADHAN S, WEISS A A.Probiotic properties of Escherichia coli nissle in human intestinal organoids[J].mBio, 2020, 11(4):e01470-e01420.
[47] CO J Y, MARGALEF-CATALÀ M, LI X N, et al.Controlling epithelial polarity:A human enteroid model for host-pathogen interactions[J].Cell Reports, 2019, 26(9):2509-2520.
[48] APOSTOLOU A, PANCHAKSHARI R A, BANERJEE A, et al.A micro-engineered human colon intestine-chip platform to study leaky barrier[J].Cold Spring Harbor Laboratory, 2020. DOI: https://doi.org/10.1101/2020.08.28.271759.
[49] KIM H J, HUH D, HAMILTON G, et al.Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow[J].Lab on a Chip, 2012, 12(12):2165-2174.
[50] KASENDRA M, TOVAGLIERI A, SONTHEIMER-PHELPS A, et al.Development of a primary human small intestine-on-a-chip using biopsy-derived organoids[J].Scientific Reports, 2018, 8(1):2871.
[51] YIN J Y, SUNUWAR L, KASENDRA M, et al.Fluid shear stress enhances differentiation of jejunal human enteroids in Intestine-Chip[J].American Journal of Physiology.Gastrointestinal and Liver Physiology, 2021, 320(3):G258-G271.
[52] TRIETSCH S J, NAUMOVSKA E, KUREK D, et al.Membrane-free culture and real-time barrier integrity assessment of perfused intestinal epithelium tubes[J].Nature Communications, 2017, 8(1):262.
[53] MARZORATI M, VANHOECKE B, DE RYCK T, et al.The HMITM module:A new tool to study the Host-Microbiota Interaction in the human gastrointestinal tract in vitro[J].BMC Microbiology, 2014, 14:133.
[54] SHAH P, FRITZ J V, GLAAB E, et al.A microfluidics-based in vitro model of the gastrointestinal human-microbe interface[J].Nature Communications, 2016, 7:11535.
[55] SHIN Y C, SHIN W, KOH D, et al.Three-dimensional regeneration of patient-derived intestinal organoid epithelium in a physiodynamic mucosal interface-on-a-chip[J].Micromachines, 2020, 11(7):663.
[56] ZHANG J B, HUANG Y J, YOON J Y, et al.Primary human colonic mucosal barrier crosstalk with super oxygen-sensitive Faecalibacterium prausnitzii in continuous culture[J].Med, 2021, 2(1):74-98.
[57] KIM H J, LI H, COLLINS J J, et al.Contributions of microbiome and mechanical deformation to intestinal bacterial overgrowth and inflammation in a human gut-on-a-chip[J].Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(1):E7-E15.
[58] SUNUWAR L, YIN J Y, KASENDRA M, et al.Mechanical stimuli affect Escherichia coli heat-stable enterotoxin-cyclic GMP signaling in a human enteroid intestine-chip model[J].Infection and Immunity, 2020, 88(3):e00866-e00819.
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