Saccharomyces boulardii Strain CNCM I-745 Modifies the Mononuclear Phagocytes Response in the Small Intestine of Mice Following Salmonella Typhimurium Infection

Lidia Ibanez, Rodolphe Pontier-Bres, Frederic Larbret, Akila Rekima, Valerie Verhasselt, Claudine Blin-Wakkach, Dorota Czerucka

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Abstract

Intestinal mononuclear phagocytes (MPs) comprise dendritic cells (DCs) and macrophages (M phi s) that play different roles in response to Salmonella infection. After phagocytosis, DCs expressing CD103 transport Salmonella from the intestinal tract to the mesenteric lymph nodes (MLN) and induce adaptive immune responses whereas resident M phi s expressing CX3CR1 capture bacteria in the lumen and reside in the lamina propria (LP) where they induce a local immune response. CX3CR1(+) M phi s are generated from Ly6C(hi) monocytes that enter the colonic mucosa and differentiate locally. We previously demonstrated that the probiotic yeast Saccharomyces boulardii CNCM I-745 (S.b) prevents infection by Salmonella enterica serovar Typhimurium (ST), decreases ST translocation to the peripheral organs and modifies the pro-and anti-inflammatory cytokine profiles in the gut. In the present study, we investigated the effect of S.b on the migratory CD103(+) DCs and the resident CX3CR1(+) M phi s. MPs were isolated from the LP of streptomycin-treated mice infected by ST with or without S.b treatment before or during the infection. In S.b-pretreated mice, we observed a decrease of the CD103(+) DCs in the LP that was associated with the drop of ST recovery from MLN. Interestingly, S.b induced an infiltration of LP by classical Ly6C(hi) monocytes, and S.b modified the monocyte-M phi maturation process in ST-infected mice. Our results showed that S.b treatment induced the expansion of Ly6C(hi) monocytes in the blood as well as in the bone marrow (BM) of mice, thus contributing to the M phi replenishment in LP from blood monocytes. In vitro experiments conducted on BM cells confirmed that S.b induced the expansion of CX3CR1(+) M phi s and concomitantly ST phagocytosis. Altogether, these data demonstrate that Saccharomyces boulardii CNCM I-745 modulates the innate immune response. Although here, we cannot explicitly delineate direct effects on ST from innate immunity, S. b-amplified innate immunity correlated with partial protection from ST infection. This study shows that S. b can induce the expansion of classical monocytes that are precursors of resident M phi s in the LP.

Original languageEnglish
Article number643
Number of pages11
JournalFrontiers in Immunology
Volume10
DOIs
Publication statusPublished - 2 Apr 2019

Cite this

@article{a46be03182ff40fc853fe9492b5eb220,
title = "Saccharomyces boulardii Strain CNCM I-745 Modifies the Mononuclear Phagocytes Response in the Small Intestine of Mice Following Salmonella Typhimurium Infection",
abstract = "Intestinal mononuclear phagocytes (MPs) comprise dendritic cells (DCs) and macrophages (M phi s) that play different roles in response to Salmonella infection. After phagocytosis, DCs expressing CD103 transport Salmonella from the intestinal tract to the mesenteric lymph nodes (MLN) and induce adaptive immune responses whereas resident M phi s expressing CX3CR1 capture bacteria in the lumen and reside in the lamina propria (LP) where they induce a local immune response. CX3CR1(+) M phi s are generated from Ly6C(hi) monocytes that enter the colonic mucosa and differentiate locally. We previously demonstrated that the probiotic yeast Saccharomyces boulardii CNCM I-745 (S.b) prevents infection by Salmonella enterica serovar Typhimurium (ST), decreases ST translocation to the peripheral organs and modifies the pro-and anti-inflammatory cytokine profiles in the gut. In the present study, we investigated the effect of S.b on the migratory CD103(+) DCs and the resident CX3CR1(+) M phi s. MPs were isolated from the LP of streptomycin-treated mice infected by ST with or without S.b treatment before or during the infection. In S.b-pretreated mice, we observed a decrease of the CD103(+) DCs in the LP that was associated with the drop of ST recovery from MLN. Interestingly, S.b induced an infiltration of LP by classical Ly6C(hi) monocytes, and S.b modified the monocyte-M phi maturation process in ST-infected mice. Our results showed that S.b treatment induced the expansion of Ly6C(hi) monocytes in the blood as well as in the bone marrow (BM) of mice, thus contributing to the M phi replenishment in LP from blood monocytes. In vitro experiments conducted on BM cells confirmed that S.b induced the expansion of CX3CR1(+) M phi s and concomitantly ST phagocytosis. Altogether, these data demonstrate that Saccharomyces boulardii CNCM I-745 modulates the innate immune response. Although here, we cannot explicitly delineate direct effects on ST from innate immunity, S. b-amplified innate immunity correlated with partial protection from ST infection. This study shows that S. b can induce the expansion of classical monocytes that are precursors of resident M phi s in the LP.",
keywords = "Salmonella Typhimurium, probiotic, Saccharomyces boulardii CNCM I-745, innate immunity, monocytes, Lamina propria, bone marrow, infection, HUMAN DENDRITIC CELLS, CANDIDA-ALBICANS, LAMINA PROPRIA, MONOCYTE, RECRUITMENT, PATHOGEN, INFLAMMATION, ACTIVATION, DEFENSE, DISEASE",
author = "Lidia Ibanez and Rodolphe Pontier-Bres and Frederic Larbret and Akila Rekima and Valerie Verhasselt and Claudine Blin-Wakkach and Dorota Czerucka",
year = "2019",
month = "4",
day = "2",
doi = "10.3389/fimmu.2019.00643",
language = "English",
volume = "10",
journal = "Frontiers in Immunology",
issn = "1664-3224",
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Saccharomyces boulardii Strain CNCM I-745 Modifies the Mononuclear Phagocytes Response in the Small Intestine of Mice Following Salmonella Typhimurium Infection. / Ibanez, Lidia; Pontier-Bres, Rodolphe; Larbret, Frederic; Rekima, Akila; Verhasselt, Valerie; Blin-Wakkach, Claudine; Czerucka, Dorota.

In: Frontiers in Immunology, Vol. 10, 643, 02.04.2019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Saccharomyces boulardii Strain CNCM I-745 Modifies the Mononuclear Phagocytes Response in the Small Intestine of Mice Following Salmonella Typhimurium Infection

AU - Ibanez, Lidia

AU - Pontier-Bres, Rodolphe

AU - Larbret, Frederic

AU - Rekima, Akila

AU - Verhasselt, Valerie

AU - Blin-Wakkach, Claudine

AU - Czerucka, Dorota

PY - 2019/4/2

Y1 - 2019/4/2

N2 - Intestinal mononuclear phagocytes (MPs) comprise dendritic cells (DCs) and macrophages (M phi s) that play different roles in response to Salmonella infection. After phagocytosis, DCs expressing CD103 transport Salmonella from the intestinal tract to the mesenteric lymph nodes (MLN) and induce adaptive immune responses whereas resident M phi s expressing CX3CR1 capture bacteria in the lumen and reside in the lamina propria (LP) where they induce a local immune response. CX3CR1(+) M phi s are generated from Ly6C(hi) monocytes that enter the colonic mucosa and differentiate locally. We previously demonstrated that the probiotic yeast Saccharomyces boulardii CNCM I-745 (S.b) prevents infection by Salmonella enterica serovar Typhimurium (ST), decreases ST translocation to the peripheral organs and modifies the pro-and anti-inflammatory cytokine profiles in the gut. In the present study, we investigated the effect of S.b on the migratory CD103(+) DCs and the resident CX3CR1(+) M phi s. MPs were isolated from the LP of streptomycin-treated mice infected by ST with or without S.b treatment before or during the infection. In S.b-pretreated mice, we observed a decrease of the CD103(+) DCs in the LP that was associated with the drop of ST recovery from MLN. Interestingly, S.b induced an infiltration of LP by classical Ly6C(hi) monocytes, and S.b modified the monocyte-M phi maturation process in ST-infected mice. Our results showed that S.b treatment induced the expansion of Ly6C(hi) monocytes in the blood as well as in the bone marrow (BM) of mice, thus contributing to the M phi replenishment in LP from blood monocytes. In vitro experiments conducted on BM cells confirmed that S.b induced the expansion of CX3CR1(+) M phi s and concomitantly ST phagocytosis. Altogether, these data demonstrate that Saccharomyces boulardii CNCM I-745 modulates the innate immune response. Although here, we cannot explicitly delineate direct effects on ST from innate immunity, S. b-amplified innate immunity correlated with partial protection from ST infection. This study shows that S. b can induce the expansion of classical monocytes that are precursors of resident M phi s in the LP.

AB - Intestinal mononuclear phagocytes (MPs) comprise dendritic cells (DCs) and macrophages (M phi s) that play different roles in response to Salmonella infection. After phagocytosis, DCs expressing CD103 transport Salmonella from the intestinal tract to the mesenteric lymph nodes (MLN) and induce adaptive immune responses whereas resident M phi s expressing CX3CR1 capture bacteria in the lumen and reside in the lamina propria (LP) where they induce a local immune response. CX3CR1(+) M phi s are generated from Ly6C(hi) monocytes that enter the colonic mucosa and differentiate locally. We previously demonstrated that the probiotic yeast Saccharomyces boulardii CNCM I-745 (S.b) prevents infection by Salmonella enterica serovar Typhimurium (ST), decreases ST translocation to the peripheral organs and modifies the pro-and anti-inflammatory cytokine profiles in the gut. In the present study, we investigated the effect of S.b on the migratory CD103(+) DCs and the resident CX3CR1(+) M phi s. MPs were isolated from the LP of streptomycin-treated mice infected by ST with or without S.b treatment before or during the infection. In S.b-pretreated mice, we observed a decrease of the CD103(+) DCs in the LP that was associated with the drop of ST recovery from MLN. Interestingly, S.b induced an infiltration of LP by classical Ly6C(hi) monocytes, and S.b modified the monocyte-M phi maturation process in ST-infected mice. Our results showed that S.b treatment induced the expansion of Ly6C(hi) monocytes in the blood as well as in the bone marrow (BM) of mice, thus contributing to the M phi replenishment in LP from blood monocytes. In vitro experiments conducted on BM cells confirmed that S.b induced the expansion of CX3CR1(+) M phi s and concomitantly ST phagocytosis. Altogether, these data demonstrate that Saccharomyces boulardii CNCM I-745 modulates the innate immune response. Although here, we cannot explicitly delineate direct effects on ST from innate immunity, S. b-amplified innate immunity correlated with partial protection from ST infection. This study shows that S. b can induce the expansion of classical monocytes that are precursors of resident M phi s in the LP.

KW - Salmonella Typhimurium

KW - probiotic

KW - Saccharomyces boulardii CNCM I-745

KW - innate immunity

KW - monocytes

KW - Lamina propria

KW - bone marrow

KW - infection

KW - HUMAN DENDRITIC CELLS

KW - CANDIDA-ALBICANS

KW - LAMINA PROPRIA

KW - MONOCYTE

KW - RECRUITMENT

KW - PATHOGEN

KW - INFLAMMATION

KW - ACTIVATION

KW - DEFENSE

KW - DISEASE

U2 - 10.3389/fimmu.2019.00643

DO - 10.3389/fimmu.2019.00643

M3 - Article

VL - 10

JO - Frontiers in Immunology

JF - Frontiers in Immunology

SN - 1664-3224

M1 - 643

ER -