Effect of Mutant and Engineered High-Acetate-Producing Saccharomyces cerevisiae var. boulardii Strains in Dextran Sodium Sulphate-Induced Colitis
Abstract
:1. Introduction
2. Materials and Methods
3. Results
3.1. High-Acetate-Producing Saccharomyces cerevisiae var. boulardii Strains Attenuate Inflammation and Show Dose-Dependent Histologic Improvement
3.2. Serum Cytokines Showed Mixed Profiles across Different Treatment Groups
3.3. The Highest-Acetate-Producing Strain Exhibits Anti-Inflammatory Effects on Gene Expression
3.4. Induction of Colitis by DSS Administration Perturbs the Gut Microbiome
3.5. Gut Microbial Species Richness Remains Consistently Preserved during Inflammation upon Treatment with the Highest-Acetate-Producing Saccharomyces cerevisiae var. boulardii Strains
4. Discussion
5. Conclusions
6. Patents
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
CD | Crohn’s Disease |
DSS | Dextran sodium sulphate |
ENT | Enterol-Saccharomyces cerevisiae var. boulardii strain |
ENT3 | Extra-high-acetate-producing Saccharomyces cerevisiae var. boulardii strain |
IBD | Inflammatory bowel disease |
PBS | Phosphate buffered saline |
Sb | Saccharomyces cerevisiae var. boulardii |
Sc | Saccharomyces cerevisiae |
Sb.P | High-acetate-producing Saccharomyces cerevisiae var. boulardii strain |
SCFA | Short chain fatty acids |
SDH1 | Non-acetate-producing Saccharomyces cerevisiae var. boulardii strain |
UC | Ulcerative colitis |
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Strain | Selection Criterion | Acetate Accumulation |
---|---|---|
PBS | Negative control | 0 g/L |
S. cerevisiae [Sc] | Non-probiotic control | 0 g/L |
S. cerevisiae var. boulardii SDH1 [SDH1] | No acetate production (engineered) | 0 g/L |
S. cerevisiae var. boulardii Enterol [ENT] | Probiotic control | Transient with 1.8 g/L peak at 24 h, but 0 g/L after 48 h |
S. cerevisiae var. boulardii Sb.P [Sb.P] | High acetate accumulation (natural mutation) | 5 g/L |
S. cerevisiae var. boulardii ENT3 [ENT3] | Highest acetate accumulation (engineered) | 8.5 g/L |
Gene | DSS + PBS | DSS + Sc | DSS + SDH1 | DSS + ENT | DSS + Sb.P | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|
FC | Adj. p | FC | Adj. p | FC | Adj. p | FC | Adj. p | FC | Adj. p | ||
Inflammatory genes | Tnf | 1.31 | <0.01 | 1.55 | <0.01 | 0.88 | 0.42 * | 0.48 | 0.74 | −0.29 | NA |
Il1b | 2.49 | <0.01 | 4.6 | <0.01 | 1.77 | 0.18 * | 0.42 | 0.84 | 0.29 | NA | |
Il2 | −0.55 | 0.36 | −0.74 | 0.26 | −0.71 | 0.58 | 0.25 | 0.86 | −0.65 | NA | |
Il12a | 1.62 | <0.01 | 0.89 | 0.22 * | 0.005 | 0.99 | 0.24 | 0.89 | 0.01 | NA | |
Barrier genes | Muc2 | −0.02 | 0.97 | 0.07 | 0.88 | −0.008 | 0.99 | 0.03 | 0.98 | 0.04 | 0.94 |
Cldn1 | 1 | 0.03 | 0.75 | 0.16 * | 0.1 | 0.94 | 0.77 | 0.49 | 0.44 | NA | |
Cldn2 | −0.25 | 0.43 | −0.4 | 0.22 * | −0.54 | 0.33 | −0.5 | 0.44 | −0.76 | 0.04 | |
Cldn8 | 1.38 | <0.01 | 1.3 | <0.01 | 0.64 | 0.25 | 0.05 | 0.95 | −0.15 | 0.68 | |
Tjp1~ZO1 | 0.13 | 0.63 | 0.34 | 0.2 | 0.31 | 0.54 | −0.07 | 0.91 | 0.56 | 0.06 | |
Ocel1~OCLDN | 0.07 | 0.75 | −0.09 | 0.73 | 0.16 | 0.71 | 0.3 | 0.5 | 0.06 | 0.79 | |
CAMs | Icam1 | 1.29 | <0.01 | 1 | <0.01 | 0.55 | 0.47 | 0.28 | 0.76 | 0.14 | 0.75 |
Proliferation marker | Mki67 | 0.21 | 0.49 | 0.47 | 0.14 * | 0.09 | 0.91 | 0.2 | 0.8 | 0.07 | 0.86 |
SCFA receptors | Ffar2 | 0.26 | 0.37 | 0.26 | 0.43 | 0.37 | 0.54 | 0.1 | 0.89 | −0.13 | 0.72 |
Ffar3 | 0.32 | 0.33 | −0.08 | 0.85 | −0.06 | 0.94 | 0.21 | 0.81 | 0.13 | 0.76 | |
Ffar4 | 0.16 | 0.67 | −0.1 | 0.81 | −0.33 | 0.65 | 0.14 | 0.87 | −0.64 | 0.1 | |
Hcar2 | 0.46 | 0.3 | 1.02 | 0.02 | −0.12 | 0.92 | 0.24 | 0.84 | 0.22 | NA | |
Model related genes | S100a8 | 4 | <0.01 | 5.57 | <0.01 | 2.67 | 0.18 * | 1.36 | 0.66 * | 0.88 | NA |
S100a9 | 3.55 | <0.01 | 5.1 | <0.01 | 1.99 | 0.43 * | 0.68 | 0.83 | 0.88 | NA | |
Lcn2 | 0.77 | 0.23 | 1.71 | 0.01 | 0.46 | 0.76 | 0.03 | 0.99 | −0.65 | NA |
Mid-Experiment | End of the Experiment | |||||
---|---|---|---|---|---|---|
SCFA | Controls | DSS Colitis | p (t-Test) | Controls | DSS Colitis | p (t-Test) |
Acetate | 59.36 [24.63] | 75.28 [22.95] | <0.001 | 74.78 [20.25] | 78.25 [23.90] | 0.399 |
Propionate | 4.60 [2.10] | 6.32 [1.92] | <0.001 | 6.90 [2.46] | 9.86 [4.02] | <0.001 |
Butyrate | 6.64 [5.64] | 3.18 [1.61] | <0.001 | 9.36 [5.22] | 6.51 [5.20] | 0.004 |
Comparison | Pre (p) | Mid (p) | End (p) |
---|---|---|---|
PBS vs. DSS + PBS | 1.00 | 1.00 | 0.049 |
Sc vs. DSS + Sc | 0.47 | 0.0003 | 0.71 |
SDH1 vs. DSS + SDH1 | 0.77 | 0.037 | 0.04 |
ENT vs. DSS + ENT | 0.85 | 0.015 | 0.037 |
Sb.P vs. DSS + Sb.P | 0.08 | 0.005 | 0.0048 |
ENT3 vs. DSS + ENT3 | 0.41 | 0.93 | 0.8 |
Acetate | Propionate | Butyrate | ||||
---|---|---|---|---|---|---|
Group | Mid | End | Mid | End | Mid | End |
DSS + PBS | 77.19 [19.4] | 89.06 [38.7] | 6.78 [1.50] | 10.05 [5.24] | 3.84 [1.82] | 7.30 [6.65] |
DSS + Sc | 78.65 [23.7] | 80.44 [16.1] | 6.84 [1.33] | 9.97 [3.99] | 3.66 [1.81] | 5.41 [1.83] |
DSS + SDH1 | 76.03 [18.8] | 80.57 [22.0] | 6.37 [1.45] | 10.94 [2.89] | 2.60 [0.82] | 8.81 [8.00] |
DSS + Sb.P | 67.45 [32.0] | 76.16 [17.1] | 5.87 [2.79] | 9.54 [3.98] | 3.49 [1.93] | 5.47 [2.95] |
DSS + ENT | 73.93 [20.0] | 72.16 [23.4] | 6.12 [2.29] | 9.79 [5.46] | 2.60 [1.40] | 6.15 [5.73] |
DSS + ENT3 | 78.39 [25.3] | 70.72 [19.4] | 5.95 [2.00] | 8.88 [2.71] | 2.88 [1.56] | 5.77 [3.53] |
p | 0.9 | 0.58 | 0.81 | 0.93 | 0.33 | 0.68 |
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Deleu, S.; Jacobs, I.; Vazquez Castellanos, J.F.; Verstockt, S.; Trindade de Carvalho, B.; Subotić, A.; Verstockt, B.; Arnauts, K.; Deprez, L.; Vissers, E.; et al. Effect of Mutant and Engineered High-Acetate-Producing Saccharomyces cerevisiae var. boulardii Strains in Dextran Sodium Sulphate-Induced Colitis. Nutrients 2024, 16, 2668. https://doi.org/10.3390/nu16162668
Deleu S, Jacobs I, Vazquez Castellanos JF, Verstockt S, Trindade de Carvalho B, Subotić A, Verstockt B, Arnauts K, Deprez L, Vissers E, et al. Effect of Mutant and Engineered High-Acetate-Producing Saccharomyces cerevisiae var. boulardii Strains in Dextran Sodium Sulphate-Induced Colitis. Nutrients. 2024; 16(16):2668. https://doi.org/10.3390/nu16162668
Chicago/Turabian StyleDeleu, Sara, Inge Jacobs, Jorge F. Vazquez Castellanos, Sare Verstockt, Bruna Trindade de Carvalho, Ana Subotić, Bram Verstockt, Kaline Arnauts, Lowie Deprez, Eva Vissers, and et al. 2024. "Effect of Mutant and Engineered High-Acetate-Producing Saccharomyces cerevisiae var. boulardii Strains in Dextran Sodium Sulphate-Induced Colitis" Nutrients 16, no. 16: 2668. https://doi.org/10.3390/nu16162668
APA StyleDeleu, S., Jacobs, I., Vazquez Castellanos, J. F., Verstockt, S., Trindade de Carvalho, B., Subotić, A., Verstockt, B., Arnauts, K., Deprez, L., Vissers, E., Lenfant, M., Vandermeulen, G., De Hertogh, G., Verbeke, K., Matteoli, G., Huys, G. R. B., Thevelein, J. M., Raes, J., & Vermeire, S. (2024). Effect of Mutant and Engineered High-Acetate-Producing Saccharomyces cerevisiae var. boulardii Strains in Dextran Sodium Sulphate-Induced Colitis. Nutrients, 16(16), 2668. https://doi.org/10.3390/nu16162668