<i>Lactiplantibacillus plantarum</i> Strains Modulate Intestinal Innate Immune Response and Increase Resistance to Enterotoxigenic <i>Escherichia coli</i> Infection

Currently, probiotic bacteria with not transferable antibiotic resistance represent a sustainable strategy for the treatment and prevention of enterotoxigenic <i>Escherichia coli</i> (ETEC) in farm animals. <i>Lactiplantibacillus plantarum</i> is among the most versatile spec...

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Main Authors: Ayelen Baillo, Julio Villena, Leonardo Albarracín, Mikado Tomokiyo, Mariano Elean, Kohtaro Fukuyama, Sandra Quilodrán-Vega, Silvina Fadda, Haruki Kitazawa
Format: Article
Language:English
Published: MDPI AG 2022-12-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/11/1/63
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author Ayelen Baillo
Julio Villena
Leonardo Albarracín
Mikado Tomokiyo
Mariano Elean
Kohtaro Fukuyama
Sandra Quilodrán-Vega
Silvina Fadda
Haruki Kitazawa
author_facet Ayelen Baillo
Julio Villena
Leonardo Albarracín
Mikado Tomokiyo
Mariano Elean
Kohtaro Fukuyama
Sandra Quilodrán-Vega
Silvina Fadda
Haruki Kitazawa
author_sort Ayelen Baillo
collection DOAJ
description Currently, probiotic bacteria with not transferable antibiotic resistance represent a sustainable strategy for the treatment and prevention of enterotoxigenic <i>Escherichia coli</i> (ETEC) in farm animals. <i>Lactiplantibacillus plantarum</i> is among the most versatile species used in the food industry, either as starter cultures or probiotics. In the present work, the immunobiotic potential of <i>L. plantarum</i> CRL681 and CRL1506 was studied to evaluate their capability to improve the resistance to ETEC infection. In vitro studies using porcine intestinal epithelial (PIE) cells and in vivo experiments in mice were undertaken. Expression analysis indicated that both strains were able to trigger IL-6 and IL-8 expression in PIE cells in steady-state conditions. Furthermore, mice orally treated with these strains had significantly improved levels of IFN-γ and TNF-α in the intestine as well as enhanced activity of peritoneal macrophages. The ability of CRL681 and CRL1506 to beneficially modulate intestinal immunity was further evidenced in ETEC-challenge experiments. In vitro, the CRL1506 and CRL681 strains modulated the expression of inflammatory cytokines (IL-6) and chemokines (IL-8, CCL2, CXCL5 and CXCL9) in ETEC-stimulated PIE cells. In vivo experiments demonstrated the ability of both strains to beneficially regulate the immune response against this pathogen. Moreover, the oral treatment of mice with lactic acid bacteria (LAB) strains significantly reduced ETEC counts in jejunum and ileum and prevented the spread of the pathogen to the spleen and liver. Additionally, LAB treated-mice had improved levels of intestinal IL-10 both at steady state and after the challenge with ETEC. The protective effect against ETEC infection was not observed for the non-immunomodulatory TL2677 strain. Furthermore, the study showed that <i>L. plantarum</i> CRL1506 was more efficient than the CRL681 strain to modulate mucosal immunity highlighting the strain specific character of this probiotic activity. Our results suggest that the improved intestinal epithelial defenses and innate immunity induced by <i>L. plantarum</i> CRL1506 and CRL681 would increase the clearance of ETEC and at the same time, protect the host against detrimental inflammation. These constitute valuable features for future probiotic products able to improve the resistance to ETEC infection.
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spelling doaj.art-46f95870cb2446a6a6fc9cb7f2e7c1022023-11-30T23:35:52ZengMDPI AGMicroorganisms2076-26072022-12-011116310.3390/microorganisms11010063<i>Lactiplantibacillus plantarum</i> Strains Modulate Intestinal Innate Immune Response and Increase Resistance to Enterotoxigenic <i>Escherichia coli</i> InfectionAyelen Baillo0Julio Villena1Leonardo Albarracín2Mikado Tomokiyo3Mariano Elean4Kohtaro Fukuyama5Sandra Quilodrán-Vega6Silvina Fadda7Haruki Kitazawa8Laboratory of Technology, Reference Centre for Lactobacilli (CERELA-CONICET), Tucuman CP4000, ArgentinaLaboratory of Immunobiotechnology, Reference Centre for Lactobacilli (CERELA-CONICET), Tucuman CP4000, ArgentinaLaboratory of Immunobiotechnology, Reference Centre for Lactobacilli (CERELA-CONICET), Tucuman CP4000, ArgentinaFood and Feed Immunology Group, Laboratory of Animal Food Function, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, JapanLaboratory of Immunobiotechnology, Reference Centre for Lactobacilli (CERELA-CONICET), Tucuman CP4000, ArgentinaFood and Feed Immunology Group, Laboratory of Animal Food Function, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, JapanLaboratory of Food Microbiology, Faculty of Veterinary Sciences, University of Concepción, Chillán 3820572, ChileLaboratory of Technology, Reference Centre for Lactobacilli (CERELA-CONICET), Tucuman CP4000, ArgentinaFood and Feed Immunology Group, Laboratory of Animal Food Function, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, JapanCurrently, probiotic bacteria with not transferable antibiotic resistance represent a sustainable strategy for the treatment and prevention of enterotoxigenic <i>Escherichia coli</i> (ETEC) in farm animals. <i>Lactiplantibacillus plantarum</i> is among the most versatile species used in the food industry, either as starter cultures or probiotics. In the present work, the immunobiotic potential of <i>L. plantarum</i> CRL681 and CRL1506 was studied to evaluate their capability to improve the resistance to ETEC infection. In vitro studies using porcine intestinal epithelial (PIE) cells and in vivo experiments in mice were undertaken. Expression analysis indicated that both strains were able to trigger IL-6 and IL-8 expression in PIE cells in steady-state conditions. Furthermore, mice orally treated with these strains had significantly improved levels of IFN-γ and TNF-α in the intestine as well as enhanced activity of peritoneal macrophages. The ability of CRL681 and CRL1506 to beneficially modulate intestinal immunity was further evidenced in ETEC-challenge experiments. In vitro, the CRL1506 and CRL681 strains modulated the expression of inflammatory cytokines (IL-6) and chemokines (IL-8, CCL2, CXCL5 and CXCL9) in ETEC-stimulated PIE cells. In vivo experiments demonstrated the ability of both strains to beneficially regulate the immune response against this pathogen. Moreover, the oral treatment of mice with lactic acid bacteria (LAB) strains significantly reduced ETEC counts in jejunum and ileum and prevented the spread of the pathogen to the spleen and liver. Additionally, LAB treated-mice had improved levels of intestinal IL-10 both at steady state and after the challenge with ETEC. The protective effect against ETEC infection was not observed for the non-immunomodulatory TL2677 strain. Furthermore, the study showed that <i>L. plantarum</i> CRL1506 was more efficient than the CRL681 strain to modulate mucosal immunity highlighting the strain specific character of this probiotic activity. Our results suggest that the improved intestinal epithelial defenses and innate immunity induced by <i>L. plantarum</i> CRL1506 and CRL681 would increase the clearance of ETEC and at the same time, protect the host against detrimental inflammation. These constitute valuable features for future probiotic products able to improve the resistance to ETEC infection.https://www.mdpi.com/2076-2607/11/1/63probioticslactic acid bacteria<i>Lactiplantibacillus plantarum</i>intestinal immune responseenterotoxigenic <i>Escherichia coli</i>
spellingShingle Ayelen Baillo
Julio Villena
Leonardo Albarracín
Mikado Tomokiyo
Mariano Elean
Kohtaro Fukuyama
Sandra Quilodrán-Vega
Silvina Fadda
Haruki Kitazawa
<i>Lactiplantibacillus plantarum</i> Strains Modulate Intestinal Innate Immune Response and Increase Resistance to Enterotoxigenic <i>Escherichia coli</i> Infection
Microorganisms
probiotics
lactic acid bacteria
<i>Lactiplantibacillus plantarum</i>
intestinal immune response
enterotoxigenic <i>Escherichia coli</i>
title <i>Lactiplantibacillus plantarum</i> Strains Modulate Intestinal Innate Immune Response and Increase Resistance to Enterotoxigenic <i>Escherichia coli</i> Infection
title_full <i>Lactiplantibacillus plantarum</i> Strains Modulate Intestinal Innate Immune Response and Increase Resistance to Enterotoxigenic <i>Escherichia coli</i> Infection
title_fullStr <i>Lactiplantibacillus plantarum</i> Strains Modulate Intestinal Innate Immune Response and Increase Resistance to Enterotoxigenic <i>Escherichia coli</i> Infection
title_full_unstemmed <i>Lactiplantibacillus plantarum</i> Strains Modulate Intestinal Innate Immune Response and Increase Resistance to Enterotoxigenic <i>Escherichia coli</i> Infection
title_short <i>Lactiplantibacillus plantarum</i> Strains Modulate Intestinal Innate Immune Response and Increase Resistance to Enterotoxigenic <i>Escherichia coli</i> Infection
title_sort i lactiplantibacillus plantarum i strains modulate intestinal innate immune response and increase resistance to enterotoxigenic i escherichia coli i infection
topic probiotics
lactic acid bacteria
<i>Lactiplantibacillus plantarum</i>
intestinal immune response
enterotoxigenic <i>Escherichia coli</i>
url https://www.mdpi.com/2076-2607/11/1/63
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