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Cited by 116Probiotics and Fermented FoodsGut microbiota and healthYeasts and Rust Fungi Studies

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Diversity of Saccharomyces boulardii CNCM I-745 mechanisms of action against intestinal infections

Open access
Czerucka, Dorota, Rampal, Patrick·2019·World Journal of Gastroenterology
DOI 10.3748/wjg.v25.i18.2188PMC PMC6526157
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Abstract

The yeast Saccharomyces boulardii CNCM I-745 is one of the probiotics recommended for the prevention of antibiotic-associated diarrhea.Studies conducted in vivo and in vitro demonstrated that in the case of infectious diseases there are two potential sites of action of Saccharomyces boulardii CNCM I-745: (1) An action on enteropathogenic microorganisms (adhesion of bacteria and their elimination or an effect on their virulence factors: Toxins, lipopolysaccharide, etc.); and (2) a direct action on the intestinal mucosa (trophic effects, effects on epithelial reconstitution, anti-secretory effects, anti-inflammatory, immunomodulators).Oral administration of Saccharomyces boulardii CNCM I-745 to healthy subjects does not alter their microbiota.However, in the case of diseases associated with the use of antibiotics or chronic diarrhea, Saccharomyces boulardii CNCM I-745 can restore the intestinal microbiota faster.The interaction of Saccharomyces boulardii CNCM I-745 with the innate immune system have been recently demonstrated thus opening up a new therapeutic potential of this yeast in the case of diseases associated with intestinal infections but also other pathologies associated with dysbiosis such as inflammatory diseases.

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Figure 1 Transmission microscopy image showing Saccharomyces boulardii CNCM I-745 on a culture of human epithelial cells (T84 lineages). (Source: Pontier-Bres R and Czerucka D). The arrows indicate budding yeast located either in the spaces between the cells or near the cell walls and the formation of a protective barrier.
Figure 1 Transmission microscopy image showing Saccharomyces boulardii CNCM I-745 on a culture of human epithelial cells (T84 lineages). (Source: Pontier-Bres R and Czerucka D). The arrows indicate budding yeast located either in the spaces between the cells or near the cell walls and the formation of a protective barrier.CC BY-NC · PubMed Central
Figure 2 The hypothesized targets of Saccharomyces boulardii CNCM I-745 during bacterial infections: Saccharomyces boulardii CNCM I-745 may act directly on toxins “1”, on pathogenic bacteria “2” or on host cells “3”. Sb: Saccharomyces boulardii CNCM I-745.
Figure 2 The hypothesized targets of Saccharomyces boulardii CNCM I-745 during bacterial infections: Saccharomyces boulardii CNCM I-745 may act directly on toxins “1”, on pathogenic bacteria “2” or on host cells “3”. Sb: Saccharomyces boulardii CNCM I-745.CC BY-NC · PubMed Central
Figure 3 Demonstrated mechanism of Saccharomyces boulardii CNCM I-745 action against bacterial toxins. A: Saccharomyces boulardii CNCM I-745 (S. b) produces a 120 kDa protein that inhibits adenylate cyclase and cholera toxin (CT)-induced chloride secretion. S. boulardii CNCM I-745 can also bind to CT; B: S. boulardii CNCM I-745 secretes a protease (> 54kDa) that lyses C. difficile toxins A and B and their receptors and a protein (< 10 kDa) that inhibits the signaling pathways involved in interleukin 8 synthesis. AC: Adenylate cyclase; CT: Cholera toxin; Sb: Saccharomyces boulardii CNCM I-745; IL-8: Interleukin 8.
Figure 3 Demonstrated mechanism of Saccharomyces boulardii CNCM I-745 action against bacterial toxins. A: Saccharomyces boulardii CNCM I-745 (S. b) produces a 120 kDa protein that inhibits adenylate cyclase and cholera toxin (CT)-induced chloride secretion. S. boulardii CNCM I-745 can also bind to CT; B: S. boulardii CNCM I-745 secretes a protease (> 54kDa) that lyses C. difficile toxins A and B and their receptors and a protein (< 10 kDa) that inhibits the signaling pathways involved in interleukin 8 synthesis. AC: Adenylate cyclase; CT: Cholera toxin; Sb: Saccharomyces boulardii CNCM I-745; IL-8: Interleukin 8.CC BY-NC · PubMed Central
Figure 4 The protective mechanisms against enteropathogenic Escherichia coli (enteropathogenic coli, enterohaemorrhagic coli and Citrobacter rodentium). They include an effect on the mucosa with Saccharomyces boulardii CNCM I-745 inhibiting the pathways involved in opening tight junctions (phosphorylation of myosin light chain kinase), inhibition of activation pathways of mitogen-activated protein kinases and NF-κB that are involved in the synthesis of Interleukin 8, and finally a direct effect of S. boulardii CNCM I-745 on bacteria (dephosphorylation of lipopolysaccharide of Escherichia coli and modification of the expression of pathogenicity factors of Citrobacter rodentium). EHEC: Enterohaemorrhagic coli; EPEC: Enteropathogenic coli; LPS: Lipopolysaccharide; MAPK: Mitogen-activated protein kinase; MLCK: Myosin light chain kinase; P-MLC: Phosphorylation of myosin light chain; IL-8: Interleukin 8; TNF-α: Tumor necrosis factor α Sb: Saccharomyces boulardii CNCM I-745.
Figure 4 The protective mechanisms against enteropathogenic Escherichia coli (enteropathogenic coli, enterohaemorrhagic coli and Citrobacter rodentium). They include an effect on the mucosa with Saccharomyces boulardii CNCM I-745 inhibiting the pathways involved in opening tight junctions (phosphorylation of myosin light chain kinase), inhibition of activation pathways of mitogen-activated protein kinases and NF-κB that are involved in the synthesis of Interleukin 8, and finally a direct effect of S. boulardii CNCM I-745 on bacteria (dephosphorylation of lipopolysaccharide of Escherichia coli and modification of the expression of pathogenicity factors of Citrobacter rodentium). EHEC: Enterohaemorrhagic coli; EPEC: Enteropathogenic coli; LPS: Lipopolysaccharide; MAPK: Mitogen-activated protein kinase; MLCK: Myosin light chain kinase; P-MLC: Phosphorylation of myosin light chain; IL-8: Interleukin 8; TNF-α: Tumor necrosis factor α Sb: Saccharomyces boulardii CNCM I-745.CC BY-NC · PubMed Central
Figure 5 The mechanisms of protection against enteroinvasive bacteria (Salmonella and Shigella). In the case of Salmonella, there is a decrease in the activation of the small GTPase pathway and consequently a decrease in the number of intracellular bacteria and the maintence of tight junctions. Saccharomyces boulardii CNCM I-745 also induces inhibition of mitogen-activated protein kinases and NF-κB activation pathways that are involved in interleukin 8 synthesis. And finally, a direct effect of S. boulardii CNCM I-745 on bacteria with the modification of their motility and the adhesion of Salmonella to S. boulardii CNCM I-745. IL-8: Interleukin 8; MAPK: Mitogen-activated protein kinase; Sb: Saccharomyces boulardii CNCM I-745.
Figure 5 The mechanisms of protection against enteroinvasive bacteria (Salmonella and Shigella). In the case of Salmonella, there is a decrease in the activation of the small GTPase pathway and consequently a decrease in the number of intracellular bacteria and the maintence of tight junctions. Saccharomyces boulardii CNCM I-745 also induces inhibition of mitogen-activated protein kinases and NF-κB activation pathways that are involved in interleukin 8 synthesis. And finally, a direct effect of S. boulardii CNCM I-745 on bacteria with the modification of their motility and the adhesion of Salmonella to S. boulardii CNCM I-745. IL-8: Interleukin 8; MAPK: Mitogen-activated protein kinase; Sb: Saccharomyces boulardii CNCM I-745.CC BY-NC · PubMed Central
Figure 6 Scanning electron microscopy image showing Saccharomyces boulardii CNCM I-745 and Saccharomyces typhimurium on a monolayer of T84 polarized cells. A and B: Electron microscopy image showing Saccharomyces typhimurium adhesion to Saccharomyces boulardii CNCM I-745; C and D: Confocal microscopy images showing S. typhimurium (Fluorescein IsoThioCyanate labelling), which adheres to S. boulardii CNCM I-745 (rhodamine labeling) in vitro (C) and in vivo on mouse cecum sections (D). Photos A and B: D. Czerucka1, P. Gounon2, P. Rampal1; C and D: D. Czerucka1, R. Pontier-Bres1, P. Rampal1 (1CSM, Monaco, microscopy Platform Cote d’Azur, MICA; 2University of Nice-Sophia-Antipolis). Sb: Saccharomyces boulardii CNCM I-745; St: Salmonella typhimurium.
Figure 6 Scanning electron microscopy image showing Saccharomyces boulardii CNCM I-745 and Saccharomyces typhimurium on a monolayer of T84 polarized cells. A and B: Electron microscopy image showing Saccharomyces typhimurium adhesion to Saccharomyces boulardii CNCM I-745; C and D: Confocal microscopy images showing S. typhimurium (Fluorescein IsoThioCyanate labelling), which adheres to S. boulardii CNCM I-745 (rhodamine labeling) in vitro (C) and in vivo on mouse cecum sections (D). Photos A and B: D. Czerucka1, P. Gounon2, P. Rampal1; C and D: D. Czerucka1, R. Pontier-Bres1, P. Rampal1 (1CSM, Monaco, microscopy Platform Cote d’Azur, MICA; 2University of Nice-Sophia-Antipolis). Sb: Saccharomyces boulardii CNCM I-745; St: Salmonella typhimurium.CC BY-NC · PubMed Central
Figure 7 Effect of Saccharomyces boulardii CNCM I-745 on intestinal mononuclear phagocytes: Dendritic cells expressing CD103 (CD103+DC) and macropahge expressing the fractalkine receptor (CX3CR1MΦs). A.CD103+DC which expresses the CCR7 on their surface phagocytes the Salmonella (ST) and migrate to the mesenteric lymph nodes (MLN). CX3CR1MΦs which have a high phagocytosis capacity, include bacteria, do not migrate, but remain in the LP where they stimulate T lymphocytes. These MΦs are able to form extensions that pass between the epithelial cells and capture the antigens in the intestinal lumen, among other pathogenic bacteria such as ST. Saccharomyces boulardii CNCM I-745 induces the recruitment of CX3CR1MΦs and promotes phagocytosis of ST by these cells. S. boulardii CNCM I-745 effects the expansion of Ly6C inflammatory monocytes, which are the precursors of CX3CR1 DCs in the bone marrow. In addition, S. boulardii CNCM I-745 reduces the number of ST that migrate to MLN by decreasing the number of migratory DCs. B.In vitro studies have shown that S. boulardii CNCM I-745 can modify lipopolysaccharide activation of migratory DCs. This effect would be due to a molecule of low molecular weight (< 3 kDa) present in S. boulardii CNCM I-745 conditioned medium[64]. Sb: Saccharomyces boulardiiCNCM I-745; ST: Salmonella; MLN: Mesenteric lymph nodes; DCs: Dendritic cells; LPS: Lipopolysaccharide.
Figure 7 Effect of Saccharomyces boulardii CNCM I-745 on intestinal mononuclear phagocytes: Dendritic cells expressing CD103 (CD103+DC) and macropahge expressing the fractalkine receptor (CX3CR1MΦs). A.CD103+DC which expresses the CCR7 on their surface phagocytes the Salmonella (ST) and migrate to the mesenteric lymph nodes (MLN). CX3CR1MΦs which have a high phagocytosis capacity, include bacteria, do not migrate, but remain in the LP where they stimulate T lymphocytes. These MΦs are able to form extensions that pass between the epithelial cells and capture the antigens in the intestinal lumen, among other pathogenic bacteria such as ST. Saccharomyces boulardii CNCM I-745 induces the recruitment of CX3CR1MΦs and promotes phagocytosis of ST by these cells. S. boulardii CNCM I-745 effects the expansion of Ly6C inflammatory monocytes, which are the precursors of CX3CR1 DCs in the bone marrow. In addition, S. boulardii CNCM I-745 reduces the number of ST that migrate to MLN by decreasing the number of migratory DCs. B.In vitro studies have shown that S. boulardii CNCM I-745 can modify lipopolysaccharide activation of migratory DCs. This effect would be due to a molecule of low molecular weight (< 3 kDa) present in S. boulardii CNCM I-745 conditioned medium[64]. Sb: Saccharomyces boulardiiCNCM I-745; ST: Salmonella; MLN: Mesenteric lymph nodes; DCs: Dendritic cells; LPS: Lipopolysaccharide.CC BY-NC · PubMed Central
Figure 8 Diagram illustrating the impact of Saccharomyces boulardii CNCM I-745 on dysbiosis during antibiotic therapy. A 2-wk treatment with antibiotics (red zone of the graph) induces a sudden decrease in the dominant bacterial populations of the microbiota (blue curve). Treatment with Saccharomyces boulardii CNCM I-745 during antibiotic therapy (red curve) reduces the sudden decrease in bacterial populations. When S. boulardii CNCM I-745 is administered after antibiotic therapy (green zone of the graph, green curve) the yeast accelerates the restoration of the intestinal flora to its initial level. An optimal use of yeast would be administration during and after antibiotic therapy, which is presented by the hatched curve resulting from the red and green curve (from reference[75]).
Figure 8 Diagram illustrating the impact of Saccharomyces boulardii CNCM I-745 on dysbiosis during antibiotic therapy. A 2-wk treatment with antibiotics (red zone of the graph) induces a sudden decrease in the dominant bacterial populations of the microbiota (blue curve). Treatment with Saccharomyces boulardii CNCM I-745 during antibiotic therapy (red curve) reduces the sudden decrease in bacterial populations. When S. boulardii CNCM I-745 is administered after antibiotic therapy (green zone of the graph, green curve) the yeast accelerates the restoration of the intestinal flora to its initial level. An optimal use of yeast would be administration during and after antibiotic therapy, which is presented by the hatched curve resulting from the red and green curve (from reference[75]).CC BY-NC · PubMed Central

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Research works printed but not linked: 3

  1. Adam J, Barret A, Barret-Bellet C. Essais cliniques contrôlés en double insu de l'Ultra-Levure lyophilisée. Etude multicentrique par 25 médecins de 388 cas. Méd Chirurg Dig 1976; 5: 401-405
  2. Guilbaub JF. Traitement des candidoses digestives et cutanéo-muqueuses par l'Ultra-levure à haute dose. Vie méd 1975; 8: 628-630
  3. Krammer M, Karbach U. Antidiarrheal action of the yeast Saccharomyces boulardii in the rat small and large intestine by stimulating chloride secretion. Z Gastroenterol 1993; 31:73-77

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Metadata

Authors
Czerucka, D., & Rampal, P.
Affiliations
Scientific Centre of Monaco (MC)
ORCID
Venue
World Journal of Gastroenterology
Publisher
Baishideng Publishing Group Inc.
Published
2019-05-14
Volume
25
Issue
18
Pages
2188-2203
ISSN
1007-9327 (ISSN-L)
DOI
10.3748/wjg.v25.i18.2188
PMC
PMC6526157
OpenAlex
W2946761187
Cited by
116
References
75
Citations by year
2026: 24 · 2025: 15 · 2024: 16 · 2023: 20 · 2022: 18 · 2021: 14 · 2020: 9
FWCI
0.92
Type
journal article
Language
en
Open access
Licence
cc-by-nc
Locations
  • World Journal of Gastroenterology (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Immunology and Microbiology › Microbiology › Yeasts and Rust Fungi Studies
Keywords
Saccharomyces boulardii CNCM I-745, probiotics, intestinal infection, antibiotic-associated diarrhea, bacterial adhesion, virulence factors, intestinal mucosa, anti-inflammatory activity, immunomodulation, gut microbiota, dysbiosis, innate immune system, chronic diarrhea
MeSH terms
Gastrointestinal Microbiome, Saccharomyces boulardii, Animals, Disease Models, Animal, Humans, Immunity, Innate, Intestinal Diseases, Intestinal Mucosa, Probiotics, Intraabdominal Infections

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