Prophylactic Effect of Bovine Colostrum on Intestinal Microbiota and Behavior in Wild-Type and Zonulin Transgenic Mice
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals
2.2. Experiment
2.3. Bovine Colostrum (BC) Administration
2.4. Behavioral Assays
2.4.1. Marble Burying (MB)
2.4.2. Light Dark Box (LDB) Test
2.5. Microbiome Analysis; Sample Collection and DNA Extraction
2.6. Bioinformatic Analysis of Microbiome Data
2.7. Statistical Processing
3. Results
3.1. Alpha Diversity Analysis in Wild-Type (WT) and Zonulin Transgenic Mice (Ztm)
3.1.1. Wild-Type (WT) Groups
3.1.2. Zonulin Transgenic Mice (Ztm) Groups
3.2. Beta Diversity Analysis
3.3. Species Composition
3.3.1. Phylum Level
3.3.2. Family Level
3.3.3. Genus Level
3.3.4. Analysis of Differential Species Abundances
3.4. Behavioral Assays
4. Discussion
4.1. Microbiota, Short Chain Fatty Acids, and Behavior in Wild-Type (WT) Mice
4.2. Dysbiosis, Intestinal Barrier, and Behavior in Zonulin Transgenic Mice (Ztm)
4.3. Dysbiosis, Behavior, Mental Disorders, and Neuroinflammation
4.4. Bovine Colostrum, Oligosaccharides, Short-Chain FattyAacids (SCFAs), and Eubiosis
4.5. Future Perspectives
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
AD | Alzheimer’s disease |
ADHD | attention deficit hyperactivity disorder |
ANS | autonomic nervous system |
ASD | autism spectrum disorder |
BC | bovine colostrum |
BP | bipolar |
CNS | central nervous system |
Ctr | control mice |
ENS | enteric nervous system |
F/B ratio | Firmicute Bacteroidetes ratio |
FDR | false discovery rate |
GABA | γ-Aminobutyric acid |
GBA | gut–brain axis |
GI | gastrointestinal |
HSD | honestly significant difference |
HPA | hypothalamic-pituitary-adrenal |
IP | intestinal permeability |
LDB | light-dark box |
LPS | lipopolysaccharide |
MB | marble burying |
MCI | mild cognitive impairment |
MDD | major depressive disorder |
MGBA | microbiota–gut–brain axis |
OTUs | operational taxonomic units |
PD | Parkinson’s Disease |
PCA | principal component analysis |
PERMANOVA | permutation multivariate analysis of variance |
SCFAs | short-chain fatty acids |
TJs | tight junctions |
TLRs | Toll-like receptors |
WT | wild-type |
Ztm | zonulin transgenic mouse |
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Pielou’s Evenness | ||||
---|---|---|---|---|
Group 1 | Group 2 | H | p-value | q-value |
WT BC (n = 14) * | WT Ctr (n = 13) | 15.549 | 0.001 | - |
WT f BC (n = 6) ** | WT f Ctr (n = 5) | 4.033 | 0.044 | 0.053 |
WT m BC (n = 8) | 6.016 | 0.014 | 0.028 | |
WT m Ctr (n = 8) | 8.816 | 0.002 | 0.017 | |
WT f Ctr (n = 5) ** | WT m BC (n = 8) | 4.200 | 0.040 | 0.053 |
WT m Ctr (n = 8) | 6.942 | 0.008 | 0.025 | |
WT m BC (n = 8) ** | WT m Ctr (n = 8) | 2.161 | 0.141 | 0.141 |
Species Richness | ||||
Group 1 | Group 2 | H | p-value | q-value |
WT BC (n = 14) * | WT Ctr (n = 13) | 3.849 | 0.278 | - |
WT f BC (n = 6) ** | WT f Ctr (n = 5) | 0.209 | 0.647 | 0.751 |
WT m BC (n = 8) | 1.845 | 0.174 | 0.374 | |
WT m Ctr (n = 8) | 1.209 | 0.271 | 0.407 | |
WT f Ctr (n = 5) ** | WT m BC (n = 8) | 2.600 | 0.106 | 0.374 |
WT m Ctr (n = 8) | 1.740 | 0.187 | 0.374 | |
WT m BC (n = 8) ** | WT m Ctr (n = 8) | 0.100 | 0.751 | 0.751 |
Shannon Diversity | ||||
Group 1 | Group 2 | H | p-value | q-value |
WT BC (n = 14) * | WT Ctr (n = 13) | 12.932 | 0.004 | - |
WT f BC (n = 6) ** | WT f Ctr (n = 5) | 4.033 | 0.044 | 0.066 |
WT m BC (n = 8) | 5.400 | 0.020 | 0.060 | |
WT m Ctr (n = 8) | 8.066 | 0.004 | 0.027 | |
WT f Ctr (n = 5) ** | WT m BC (n = 8) | 3.085 | 0.078 | 0.094 |
WT m Ctr (n = 8) | 4.200 | 0.040 | 0.066 | |
WT m BC (n = 8) ** | WT m Ctr (n = 8) | 1.863 | 0.172 | 0.172 |
Pielou’s Evenness | ||||
---|---|---|---|---|
Group 1 | Group 2 | H | p-value | q-value |
Ztm BC (n = 14) * | Ztm Ctr (n = 12) | 6.960 | 0.073 | - |
Ztm f BC (n = 6) ** | Ztm f Ctr (n = 5) | 0.000 | 1.000 | 1.000 |
Ztm m BC (n = 8) | 4.816 | 0.028 | 0.084 | |
Ztm m Ctr (n = 7) | 2.469 | 0.116 | 0.232 | |
Ztm f Ctr (n = 5) ** | Ztm m BC (n = 8) | 5.485 | 0.019 | 0.084 |
Ztm m Ctr (n = 7) | 0.323 | 0.569 | 0.683 | |
Ztm m BC (n = 8) ** | Ztm m Ctr (n = 7) | 0.482 | 0.487 | 0.683 |
Species Richness | ||||
Group 1 | Group 2 | H | p-value | q-value |
Ztm BC (n = 14) * | Ztm Ctr (n = 12) | 15.359 | 0.001 | - |
Ztm f BC (n = 6) ** | Ztm f Ctr (n = 5) | 5.659 | 0.017 | 0.026 |
Ztm m BC (n = 8) | 0.016 | 0.897 | 0.897 | |
Ztm m Ctr (n = 7) | 7.449 | 0.006 | 0.019 | |
Ztm f Ctr (n = 5) ** | Ztm m BC (n = 8) | 6.580 | 0.010 | 0.020 |
Ztm m Ctr (n = 7) | 0.797 | 0.371 | 0.446 | |
Ztm m BC (n = 8) ** | Ztm m Ctr (n = 7) | 9.053 | 0.002 | 0.015 |
Shannon Diversity | ||||
Group 1 | Group 2 | H | p-value | q-value |
Ztm BC (n = 14) * | Ztm Ctr (n = 12) | 7.609 | 0.054 | - |
Ztm f BC (n = 6) ** | Ztm f Ctr (n = 5) | 0.300 | 0.583 | 0.775 |
Ztm m BC (n = 8) | 3.750 | 0.052 | 0.158 | |
Ztm m Ctr (n = 7) | 0.081 | 0.775 | 0.775 | |
Ztm f Ctr (n = 5) ** | Ztm m BC (n = 8) | 6.942 | 0.008 | 0.050 |
Ztm m Ctr (n = 7) | 0.164 | 0.684 | 0.775 | |
Ztm m BC (n = 8) ** | Ztm m Ctr (n = 7) | 3.013 | 0.082 | 0.165 |
Beta Diverstiy Index | Permanova | Group 1 | Group 2 | n | Permutations | Pseudo-F | p-Value |
---|---|---|---|---|---|---|---|
Bray Curtis | Groups | WT BC | WT Ctr | 27 | 999 | 2.428 | 0.034 |
Ztm BC | Ztm Ctr | 26 | 999 | 4.753 | 0.001 | ||
Subgroups | WT f BC | WT f Ctr | 11 | 999 | 2.079 | 0.075 | |
WT m BC | WT m Ctr | 16 | 999 | 2.653 | 0.033 | ||
Ztm f BC | Ztm f Ctr | 11 | 999 | 4.137 | 0.012 | ||
Ztm m BC | Ztm m Ctr | 15 | 999 | 3.112 | 0.001 | ||
Jaccard | Groups | WT BC | WT Ctr | 27 | 999 | 1.561 | 0.043 |
Ztm BC | Ztm Ctr | 26 | 999 | 3.455 | 0.001 | ||
Subgroups | WT f BC | WT f Ctr | 11 | 999 | 1.967 | 0.003 | |
WT m BC | WT m Ctr | 16 | 999 | 1.501 | 0.029 | ||
Ztm f BC | Ztm f Ctr | 11 | 999 | 2.323 | 0.004 | ||
Ztm m BC | Ztm m Ctr | 15 | 999 | 2.895 | 0.001 |
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Asbjornsdottir, B.; Miranda-Ribera, A.; Fiorentino, M.; Konno, T.; Cetinbas, M.; Lan, J.; Sadreyev, R.I.; Gudmundsson, L.S.; Gottfredsson, M.; Lauth, B.; et al. Prophylactic Effect of Bovine Colostrum on Intestinal Microbiota and Behavior in Wild-Type and Zonulin Transgenic Mice. Biomedicines 2023, 11, 91. https://doi.org/10.3390/biomedicines11010091
Asbjornsdottir B, Miranda-Ribera A, Fiorentino M, Konno T, Cetinbas M, Lan J, Sadreyev RI, Gudmundsson LS, Gottfredsson M, Lauth B, et al. Prophylactic Effect of Bovine Colostrum on Intestinal Microbiota and Behavior in Wild-Type and Zonulin Transgenic Mice. Biomedicines. 2023; 11(1):91. https://doi.org/10.3390/biomedicines11010091
Chicago/Turabian StyleAsbjornsdottir, Birna, Alba Miranda-Ribera, Maria Fiorentino, Takumi Konno, Murat Cetinbas, Jinggang Lan, Ruslan I. Sadreyev, Larus S. Gudmundsson, Magnus Gottfredsson, Bertrand Lauth, and et al. 2023. "Prophylactic Effect of Bovine Colostrum on Intestinal Microbiota and Behavior in Wild-Type and Zonulin Transgenic Mice" Biomedicines 11, no. 1: 91. https://doi.org/10.3390/biomedicines11010091
APA StyleAsbjornsdottir, B., Miranda-Ribera, A., Fiorentino, M., Konno, T., Cetinbas, M., Lan, J., Sadreyev, R. I., Gudmundsson, L. S., Gottfredsson, M., Lauth, B., Birgisdottir, B. E., & Fasano, A. (2023). Prophylactic Effect of Bovine Colostrum on Intestinal Microbiota and Behavior in Wild-Type and Zonulin Transgenic Mice. Biomedicines, 11(1), 91. https://doi.org/10.3390/biomedicines11010091