The Impact of Escherichia coli Probiotic Strain O83:K24:H31 on the Maturation of Dendritic Cells and Immunoregulatory Functions In Vitro and In Vivo

. 2022 May 12 ; 11 (10) : . [epub] 20220512

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35626660

Early postnatal events are important for the development of the neonatal immune system. Harboring the pioneering microorganisms forming the microbiota of the neonatal gastrointestinal tract is important for priming the immune system, as well as inducing appropriate tolerance to the relatively innocuous environmental antigens and compounds of normal healthy microbiota. Early postnatal supplementation of suitable, safe probiotics could accelerate this process. In the current study, the immunomodulatory capacity of the probiotic strain of Escherichia coli O83:K24:H31 (EcO83) was characterized in vitro and in vivo. We compared the capacity of EcO83 with and without hemolytic activity on selected immune characteristics in vitro as determined by flow cytometry and quantitative real-time PCR. Both strains with and without hemolytic activity exerted comparable capacity on the maturation of dendritic cells while preserving the induction of interleukin 10 (Il10) expression in dendritic cells and T cells cocultured with EcO83 primed dendritic cells. Early postnatal supplementation with EcO83 led to massive but transient colonization of the neonatal gastrointestinal tract, as detected by in vivo bioimaging. Early postnatal EcO83 administration promoted gut barrier function by increasing the expression of claudin and occludin and the expression of Il10. Early postnatal EcO83 application promotes maturation of the neonatal immune system and promotes immunoregulatory and gut barrier functions.

Zobrazit více v PubMed

Mishra A., Lai G.C., Yao L.J., Aung T.T., Shental N., Rotter-Maskowitz A., Shepherdson E., Singh G.S.N., Pai R., Shanti A., et al. Microbial exposure during early human development primes fetal immune cells. Cell. 2021;184:3394–3409. doi: 10.1016/j.cell.2021.04.039. PubMed DOI PMC

Pelzer E., Gomez-Arango L.F., Barrett H.L., Nitert M.D. Review: Maternal health and the placental microbiome. Placenta. 2017;54:30–37. doi: 10.1016/j.placenta.2016.12.003. PubMed DOI

Prince A.L., Ma J., Kannan P.S., Alvarez M., Gisslen T., Harris R.A., Sweeney E.L., Knox C.L., Lambers D.S., Jobe A.H., et al. The placental membrane microbiome is altered among subjects with spontaneous preterm birth with and without chorioamnionitis. Am. J. Obs. Gynecol. 2016;214:627.e1–627.e16. doi: 10.1016/j.ajog.2016.01.193. PubMed DOI PMC

Abdel-Gadir A., Massoud A.H., Chatila T.A. Antigen-specific treg cells in immunological tolerance: Implications for allergic diseases. F1000Research. 2018;7:38. doi: 10.12688/f1000research.12650.1. PubMed DOI PMC

Leiby J.S., McCormick K., Sherrill-Mix S., Clarke E.L., Kessler L.R., Taylor L.J., Hofstaedter C.E., Roche A.M., Mattei L.M., Bittinger K., et al. Lack of detection of a human placenta microbiome in samples from preterm and term deliveries. Microbiome. 2018;6:196. doi: 10.1186/s40168-018-0575-4. PubMed DOI PMC

de Goffau M.C., Lager S., Sovio U., Gaccioli F., Cook E., Peacock S.J., Parkhill J., Charnock-Jones D.S., Smith G.C.S. Human placenta has no microbiome but can contain potential pathogens. Nature. 2019;572:329–334. doi: 10.1038/s41586-019-1451-5. PubMed DOI PMC

Zhang C., Li L., Jin B., Xu X., Zuo X., Li Y., Li Z. The effects of delivery mode on the gut microbiota and health: State of art. Front. Microbiol. 2021;12:724449. doi: 10.3389/fmicb.2021.724449. PubMed DOI PMC

Kolokotroni O., Middleton N., Gavatha M., Lamnisos D., Priftis K.N., Yiallouros P.K. Asthma and atopy in children borns by caesarean section: Effect modification by family history of allergies—A population based cross-sectional study. BMC Pediatr. 2012;12:179. doi: 10.1186/1471-2431-12-179. PubMed DOI PMC

Kindinger L.M., Bennett P.R., Lee Y.S., Marchesi J.R., Smith A., Cacciatore S., Holmes E., Nicholson J.K., Teoh T.G., MacIntyre D.A. The interaction between vaginal microbiota, cervical length, and vaginal progesterone treatment for preterm birth risk. Microbiome. 2017;5:6. doi: 10.1186/s40168-016-0223-9. PubMed DOI PMC

Martin R., Makino H., Cetinyurek Yavuz A., Ben-Amor K., Roelofs M., Ishikawa E., Kubota H., Swinkels S., Sakai T., Oishi K., et al. Early-life events, including mode of delivery and type of feeding, siblings and gender, shape the developing gut microbiota. PLoS ONE. 2016;11:e0158498. doi: 10.1371/journal.pone.0158498. PubMed DOI PMC

Dominguez-Bello M.G., Costello E.K., Contreras M., Magris M., Hidalgo G., Fierer N., Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. USA. 2010;107:11971–11975. doi: 10.1073/pnas.1002601107. PubMed DOI PMC

Dogra S., Sakwinska O., Soh S.E., Ngom-Bru C., Bruck W.M., Berger B., Brussow H., Lee Y.S., Yap F., Chong Y.S., et al. Dynamics of infant gut microbiota are influenced by delivery mode and gestational duration and are associated with subsequent adiposity. mBio. 2015;6:e02419. doi: 10.1128/mBio.02419-14. PubMed DOI PMC

Sakwinska O., Foata F., Berger B., Brüssow H., Combremont S., Mercenier A., Dogra S., Soh S.-E., Yen J.C.K., Heong G.Y.S., et al. Does the maternal vaginal microbiota play a role in seeding the microbiota of neonatal gut and nose? Benef. Microbes. 2017;8:763–778. doi: 10.3920/BM2017.0064. PubMed DOI

Koren O., Goodrich J.K., Cullender T.C., Spor A., Laitinen K., Backhed H.K., Gonzalez A., Werner J.J., Angenent L.T., Knight R., et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012;150:470–480. doi: 10.1016/j.cell.2012.07.008. PubMed DOI PMC

Freitas A.C., Bocking A., Hill J.E., Money D.M., the VOGUE Research Group Increased richness and diversity of the vaginal microbiota and spontaneous preterm birth. Microbiome. 2018;6:117. doi: 10.1186/s40168-018-0502-8. PubMed DOI PMC

Romero R., Hassan S.S., Gajer P., Tarca A.L., Fadrosh D.W., Bieda J., Chaemsaithong P., Miranda J., Chaiworapongsa T., Ravel J. The vaginal microbiota of pregnant women who subsequently have spontaneous preterm labor and delivery and those with a normal delivery at term. Microbiome. 2014;2:18. doi: 10.1186/2049-2618-2-18. PubMed DOI PMC

Zommiti M., Chikindas M.L., Ferchichi M. Probiotics-live biotherapeutics: A story of success, limitations, and future prospects-not only for humans. Probiotics Antimicrob. Proteins. 2020;12:1266–1289. doi: 10.1007/s12602-019-09570-5. PubMed DOI

Markowiak P., Śliżewska K. Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients. 2017;9:1021. doi: 10.3390/nu9091021. PubMed DOI PMC

Amenyogbe N., Kollmann T.R., Ben-Othman R. Early-life host-microbiome interphase: The key frontier for immune development. Front. Pediatr. 2017;5:111. doi: 10.3389/fped.2017.00111. PubMed DOI PMC

Nash M.J., Frank D.N., Friedman J.E. Early microbes modify immune system development and metabolic homeostasis-the “restaurant” hypothesis revisited. Front. Endocrinol. 2017;8:349. doi: 10.3389/fendo.2017.00349. PubMed DOI PMC

Walker W.A. The importance of appropriate initial bacterial colonization of the intestine in newborn, child, and adult health. Pediatr. Res. 2017;82:387–395. doi: 10.1038/pr.2017.111. PubMed DOI PMC

Dzidic M., Boix-Amoros A., Selma-Royo M., Mira A., Collado M.C. Gut microbiota and mucosal immunity in the neonate. Med. Sci. 2018;6:56. doi: 10.3390/medsci6030056. PubMed DOI PMC

Kozakova H., Schwarzer M., Tuckova L., Srutkova D., Czarnowska E., Rosiak I., Hudcovic T., Schabussova I., Hermanova P., Zakostelska Z., et al. Colonization of germ-free mice with a mixture of three lactobacillus strains enhances the integrity of gut mucosa and ameliorates allergic sensitization. Cell. Mol. Immunol. 2016;13:251–262. doi: 10.1038/cmi.2015.09. PubMed DOI PMC

Ohnmacht C. Microbiota, regulatory t cell subsets, and allergic disorders. Allergo J. Int. 2016;25:114–123. doi: 10.1007/s40629-016-0118-0. PubMed DOI PMC

Zheng D., Liwinski T., Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res. 2020;30:492–506. doi: 10.1038/s41422-020-0332-7. PubMed DOI PMC

Koga M.M., Engel A., Pigni M., Lavanchy C., Stevanin M., Laversenne V., Schneider B.L., Acha-Orbea H. Il10- and il35-secreting mutudc lines act in cooperation to inhibit memory t cell activation through lag-3 expression. Front. Immunol. 2021;12 doi: 10.3389/fimmu.2021.607315. PubMed DOI PMC

Domogalla M.P., Rostan P.V., Raker V.K., Steinbrink K. Tolerance through education: How tolerogenic dendritic cells shape immunity. Front. Immunol. 2017;8:1764. doi: 10.3389/fimmu.2017.01764. PubMed DOI PMC

Olson B., Sullivan J., Burlingham W. Interleukin 35: A key mediator of suppression and the propagation of infectious tolerance. Front. Immunol. 2013;4:315. doi: 10.3389/fimmu.2013.00315. PubMed DOI PMC

Shevach E.M., Thornton A.M. Ttregs, ptregs, and itregs: Similarities and differences. Immunol. Rev. 2014;259:88–102. doi: 10.1111/imr.12160. PubMed DOI PMC

Shevach E.M. Mechanisms of foxp3+ t regulatory cell-mediated suppression. Immunity. 2009;30:636–645. doi: 10.1016/j.immuni.2009.04.010. PubMed DOI

Konieczna P., Groeger D., Ziegler M., Frei R., Ferstl R., Shanahan F., Quigley E.M., Kiely B., Akdis C.A., O’Mahony L. Bifidobacterium infantis 35624 administration induces foxp3 t regulatory cells in human peripheral blood: Potential role for myeloid and plasmacytoid dendritic cells. Gut. 2012;61:354–366. doi: 10.1136/gutjnl-2011-300936. PubMed DOI

Jeon S.G., Kayama H., Ueda Y., Takahashi T., Asahara T., Tsuji H., Tsuji N.M., Kiyono H., Ma J.S., Kusu T., et al. Probiotic bifidobacterium breve induces il-10-producing tr1 cells in the colon. PLoS Pathog. 2012;8:e1002714. doi: 10.1371/journal.ppat.1002714. PubMed DOI PMC

Macho Fernandez E., Valenti V., Rockel C., Hermann C., Pot B., Boneca I.G., Grangette C. Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by nod2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut. 2011;60:1050–1059. doi: 10.1136/gut.2010.232918. PubMed DOI

Zakostelska Z., Kverka M., Klimesova K., Rossmann P., Mrazek J., Kopecny J., Hornova M., Srutkova D., Hudcovic T., Ridl J., et al. Lysate of probiotic lactobacillus casei dn-114 001 ameliorates colitis by strengthening the gut barrier function and changing the gut microenvironment. PLoS ONE. 2011;6:e27961. doi: 10.1371/journal.pone.0027961. PubMed DOI PMC

Hrdy J., Kocourkova I., Lodinova-Zadnikova R., Kolarova L., Prokesova L. The effect of a probiotic Escherichia coli strain on regulatory t-cells in six year-old children. Benef. Microbes. 2016;7:639–648. doi: 10.3920/BM2016.0030. PubMed DOI

Hrdy J., Vlasakova K., Cerny V., Sukenikova L., Novotna O., Petraskova P., Borakova K., Lodinova-Zadnikova R., Kolarova L., Prokesova L. Decreased allergy incidence in children supplemented with E. coli o83:K24:H31 and its possible modes of action. Eur. J. Immunol. 2018;48:2015–2030. doi: 10.1002/eji.201847636. PubMed DOI

Lodinova-Zadnikova R., Cukrowska B., Tlaskalova-Hogenova H. Oral administration of probiotic Escherichia coli after birth reduces frequency of allergies and repeated infections later in life (after 10 and 20 years) Int. Arch. Allergy Immunol. 2003;131:209–211. doi: 10.1159/000071488. PubMed DOI

Lodinova-Zadnikova R., Prokesova L., Kocourkova I., Hrdy J., Zizka J. Prevention of allergy in infants of allergic mothers by probiotic Escherichia coli. Int. Arch. Allergy Immunol. 2010;153:201–206. doi: 10.1159/000312638. PubMed DOI

Wassenaar T.M. Insights from 100 years of research with probiotic E. coli. Eur. J. Microbiol. Immunol. 2016;6:147–161. doi: 10.1556/1886.2016.00029. PubMed DOI PMC

Sheshko V., Hejnova J., Rehakova Z., Sinkora J., Faldyna M., Alexa P., Felsberg J., Nemcova R., Bomba A., Sebo P. Hlya knock out yields a safer Escherichia coli a0 34/86 variant with unaffected colonization capacity in piglets. FEMS Immunol. Med. Microbiol. 2006;48:257–266. doi: 10.1111/j.1574-695X.2006.00140.x. PubMed DOI

Hrdy J., Alard J., Couturier-Maillard A., Boulard O., Boutillier D., Delacre M., Lapadatescu C., Cesaro A., Blanc P., Pot B., et al. Lactobacillus reuteri 5454 and Bifidobacterium animalis ssp. Lactis 5764 improve colitis while differentially impacting dendritic cells maturation and antimicrobial responses. Sci. Rep. 2020;10:5345. doi: 10.1038/s41598-020-62161-1. PubMed DOI PMC

Majer M., Machacek T., Sukenikova L., Hrdy J., Horak P. The peripheral immune response of mice infected with a neuropathogenic schistosome. Parasite Immunol. 2020;42:e12710. doi: 10.1111/pim.12710. PubMed DOI

Cuffaro B., Assohoun A.L.W., Boutillier D., Sukenikova L., Desramaut J., Boudebbouze S., Salome-Desnoulez S., Hrdy J., Waligora-Dupriet A.J., Maguin E., et al. In vitro characterization of gut microbiota-derived commensal strains: Selection of parabacteroides distasonis strains alleviating tnbs-induced colitis in mice. Cells. 2020;9:2104. doi: 10.3390/cells9092104. PubMed DOI PMC

Plaza-Diaz J., Gomez-Llorente C., Campana-Martin L., Matencio E., Ortuno I., Martinez-Silla R., Gomez-Gallego C., Periago M.J., Ros G., Chenoll E., et al. Safety and immunomodulatory effects of three probiotic strains isolated from the feces of breast-fed infants in healthy adults: Setoprob study. PLoS ONE. 2013;8:e78111. doi: 10.1371/journal.pone.0078111. PubMed DOI PMC

Hrdý J., Zanvit P., Novotná O., Kocourková I., Zižka J., Prokešová L. Cytokine expression in cord blood cells of children of healthy and allergic mothers. Folia Microbiol. 2010;55:515–519. doi: 10.1007/s12223-010-0085-7. PubMed DOI

Sukenikova L., Cerny V., Novotna O., Petraskova P., Borakova K., Kolarova L., Prokesova L., Hrdy J. Different capacity of in vitro generated myeloid dendritic cells of newborns of healthy and allergic mothers to respond to probiotic strain E. coli o83:K24:H31. Immunol. Lett. 2017;189:82–89. doi: 10.1016/j.imlet.2017.05.013. PubMed DOI

Meyer M.P., Chow S.S.W., Alsweiler J., Bourchier D., Broadbent R., Knight D., Lynn A.M., Patel H. Probiotics for prevention of severe necrotizing enterocolitis: Experience of new zealand neonatal intensive care units. Front. Pediatr. 2020;8:119. doi: 10.3389/fped.2020.00119. PubMed DOI PMC

Wu B.B., Yang Y., Xu X., Wang W.P. Effects of bifidobacterium supplementation on intestinal microbiota composition and the immune response in healthy infants. World J. Pediatr. WJP. 2016;12:177–182. doi: 10.1007/s12519-015-0025-3. PubMed DOI

Kim H.K., Rutten N.B., Besseling-van der Vaart I., Niers L.E., Choi Y.H., Rijkers G.T., van Hemert S. Probiotic supplementation influences faecal short chain fatty acids in infants at high risk for eczema. Benef. Microbes. 2015;6:783–790. doi: 10.3920/BM2015.0056. PubMed DOI

Simpson M.R., Dotterud C.K., Storro O., Johnsen R., Oien T. Perinatal probiotic supplementation in the prevention of allergy related disease: 6 year follow up of a randomised controlled trial. BMC Derm. 2015;15:13. doi: 10.1186/s12895-015-0030-1. PubMed DOI PMC

Harden J.L., Egilmez N.K. Indoleamine 2,3-dioxygenase and dendritic cell tolerogenicity. Immunol. Investig. 2012;41:738–764. doi: 10.3109/08820139.2012.676122. PubMed DOI PMC

Esmaeili S.A., Mahmoudi M., Rezaieyazdi Z., Sahebari M., Tabasi N., Sahebkar A., Rastin M. Generation of tolerogenic dendritic cells using Lactobacillus rhamnosus and Lactobacillus delbrueckii as tolerogenic probiotics. J. Cell. Biochem. 2018;119:7865–7872. doi: 10.1002/jcb.27203. PubMed DOI

Di Giacinto C., Marinaro M., Sanchez M., Strober W., Boirivant M. Probiotics ameliorate recurrent th1-mediated murine colitis by inducing il-10 and il-10-dependent tgf-beta-bearing regulatory cells. J. Immunol. 2005;174:3237–3246. doi: 10.4049/jimmunol.174.6.3237. PubMed DOI

Powrie F., Leach M.W., Mauze S., Menon S., Caddle L.B., Coffman R.L. Inhibition of th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells. Immunity. 1994;1:553–562. doi: 10.1016/1074-7613(94)90045-0. PubMed DOI

Asseman C., Mauze S., Leach M.W., Coffman R.L., Powrie F. An essential role for interleukin 10 in the function of regulatory t cells that inhibit intestinal inflammation. J. Exp. Med. 1999;190:995–1004. doi: 10.1084/jem.190.7.995. PubMed DOI PMC

So J.S., Lee C.G., Kwon H.K., Yi H.J., Chae C.S., Park J.A., Hwang K.C., Im S.H. Lactobacillus casei potentiates induction of oral tolerance in experimental arthritis. Mol. Immunol. 2008;46:172–180. doi: 10.1016/j.molimm.2008.07.038. PubMed DOI

Aoki-Yoshida A., Yamada K., Hachimura S., Sashihara T., Ikegami S., Shimizu M., Totsuka M. Enhancement of oral tolerance induction in do11.10 mice by Lactobacillus gasseri oll2809 via increase of effector regulatory T cells. PLoS ONE. 2016;11:e0158643. doi: 10.1371/journal.pone.0158643. PubMed DOI PMC

Lavasani S., Dzhambazov B., Nouri M., Fåk F., Buske S., Molin G., Thorlacius H., Alenfall J., Jeppsson B., Weström B. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by il-10 producing regulatory t cells. PLoS ONE. 2010;5:e9009. doi: 10.1371/journal.pone.0009009. PubMed DOI PMC

Drakes M., Blanchard T., Czinn S. Bacterial probiotic modulation of dendritic cells. Infect. Immun. 2004;72:3299–3309. doi: 10.1128/IAI.72.6.3299-3309.2004. PubMed DOI PMC

Hart A.L., Lammers K., Brigidi P., Vitali B., Rizzello F., Gionchetti P., Campieri M., Kamm M.A., Knight S.C., Stagg A.J. Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut. 2004;53:1602–1609. doi: 10.1136/gut.2003.037325. PubMed DOI PMC

Choi S.-H., Lee S.-H., Kim M.G., Lee H.J., Kim G.-B. Lactobacillus plantarum cau1055 ameliorates inflammation in lipopolysaccharide-induced raw264.7 cells and a dextran sulfate sodium–induced colitis animal model. J. Dairy Sci. 2019;102:6718–6725. doi: 10.3168/jds.2018-16197. PubMed DOI

Alard J., Peucelle V., Boutillier D., Breton J., Kuylle S., Pot B., Holowacz S., Grangette C. New probiotic strains for inflammatory bowel disease management identified by combining in vitro and in vivo approaches. Benef. Microbes. 2018;9:317–331. doi: 10.3920/BM2017.0097. PubMed DOI

Abrahamsson T.R., Sandberg Abelius M., Forsberg A., Bjorksten B., Jenmalm M.C. A th1/th2-associated chemokine imbalance during infancy in children developing eczema, wheeze and sensitization. Clin. Exp. Allergy. 2011;41:1729–1739. doi: 10.1111/j.1365-2222.2011.03827.x. PubMed DOI

West C.E., Hammarstrom M.L., Hernell O. Probiotics during weaning reduce the incidence of eczema. Pediatr. Allergy Immunol. 2009;20:430–437. doi: 10.1111/j.1399-3038.2009.00745.x. PubMed DOI

Liu Y., Wang J., Wu C. Modulation of gut microbiota and immune system by probiotics, pre-biotics, and post-biotics. Front. Nutr. 2021;8:634897. doi: 10.3389/fnut.2021.634897. PubMed DOI PMC

Kocourková I., Žádníková R., Žižka J., Rosová V. Effect of oral application of a probiotic E. coli strain on the intestinal microflora of children of allergic mothers during the first year of life. Folia Microbiol. 2007;52:189–193. doi: 10.1007/BF02932158. PubMed DOI

Sarate P.J., Heinl S., Poiret S., Drinić M., Zwicker C., Schabussova I., Daniel C., Wiedermann U.E. Coli nissle 1917 is a safe mucosal delivery vector for a birch-grass pollen chimera to prevent allergic poly-sensitization. Mucosal Immunol. 2019;12:132–144. doi: 10.1038/s41385-018-0084-6. PubMed DOI

Sanders D.S.A. Mucosal integrity and barrier function in the pathogenesis of early lesions in crohn’s disease. J. Clin. Pathol. 2005;58:568–572. doi: 10.1136/jcp.2004.021840. PubMed DOI PMC

Tlaskalová-Hogenová H., Stěpánková R., Kozáková H., Hudcovic T., Vannucci L., Tučková L., Rossmann P., Hrnčíř T., Kverka M., Zákostelská Z., et al. The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: Contribution of germ-free and gnotobiotic animal models of human diseases. Cell. Mol. Immunol. 2011;8:110–120. doi: 10.1038/cmi.2010.67. PubMed DOI PMC

Wang Y., Gu Y., Fang K., Mao K., Dou J., Fan H., Zhou C., Wang H. Lactobacillus acidophilus and clostridium butyricum ameliorate colitis in murine by strengthening the gut barrier function and decreasing inflammatory factors. Benef. Microbes. 2018;9:775–787. doi: 10.3920/BM2017.0035. PubMed DOI

Kangwan N., Kongkarnka S., Boonkerd N., Unban K., Shetty K., Khanongnuch C. Protective effect of probiotics isolated from traditional fermented tea leaves (miang) from northern thailand and role of synbiotics in ameliorating experimental ulcerative colitis in mice. Nutrients. 2022;14:227. doi: 10.3390/nu14010227. PubMed DOI PMC

Bein A., Eventov-Friedman S., Arbell D., Schwartz B. Intestinal tight junctions are severely altered in nec preterm neonates. Pediatr. Neonatol. 2018;59:464–473. doi: 10.1016/j.pedneo.2017.11.018. PubMed DOI

Halpern M.D., Denning P.W. The role of intestinal epithelial barrier function in the development of NEC. Tissue Barriers. 2015;3:e100. doi: 10.1080/21688370.2014.1000707. PubMed DOI PMC

Kokešová A., Frolová L., Kverka M., Sokol D., Rossmann P., Bártová J., Tlaskalová-Hogenová H. Oral administration of probiotic bacteria (E. coli Nissle, E. coli O83, Lactobacillus casei) influences the severity of dextran sodium sulfate-induced colitis in BALB/c mice. Folia Microbiol. 2006;51:478–484. doi: 10.1007/BF02931595. PubMed DOI

Gronbach K., Flade I., Holst O., Lindner B., Ruscheweyh H.J., Wittmann A., Menz S., Schwiertz A., Adam P., Stecher B., et al. Endotoxicity of lipopolysaccharide as a determinant of T-cell-mediated colitis induction in mice. Gastroenterology. 2014;146:765–775. doi: 10.1053/j.gastro.2013.11.033. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...