Modulation of intestinal barrier by intestinal microbiota: Pathological and therapeutic implications

Natividad, Jane M.M.; Verdu, Elena F.

doi:10.1016/j.phrs.2012.10.007

Cited by 528Gut microbiota and healthGastrointestinal motility and disordersProbiotics and Fermented Foods

Modulation of intestinal barrier by intestinal microbiota: Pathological and therapeutic implications

Natividad, Jane M.M., Verdu, Elena F.·2013·Pharmacological Research

DOI 10.1016/j.phrs.2012.10.007

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Abstract

Mammals and their intestinal microbiota peacefully coexist in a mutualistic relationship. Commensal bacteria play an active role in shaping and modulating physiological processes in the host, which include, but are not restricted to, the immune system and the intestinal barrier. Both play a crucial role in containing intestinal bacteria and other potentially noxious luminal antigens within the lumen and mucosal compartment. Although mutualism defines the relationship between the host and the intestinal microbiota, disruptions in this equilibrium may promote disease. Thus, alterations in gut microbiota (dysbiosis) have been linked to the recent increased expression of obesity, allergy, autoimmunity, functional and inflammatory disorders such as irritable bowel syndrome (IBS) and inflammatory bowel disease (IBD). In this article, we review the evidence supporting a role of gut microbiota in regulating intestinal barrier function. We discuss the hypothesis that microbial factors can modulate the barrier in ways that can prevent or promote gastrointestinal disease. A better understanding of the role of the intestinal microbiota in maintaining a functional intestinal barrier may help develop targeted strategies to prevent and treat disease.

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Loss of Klf4 in mice causes altered proliferation and differentiation and precancerous changes in the adult stomach
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MyD88 signalling plays a critical role in host defence by controlling pathogen burden and promoting epithelial cell homeostasis during Citrobacter rodentium-induced colitis
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The primary defect in experimental ileitis originates from a nonhematopoietic source
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Increased Expression of HIP/PAP and Regenerating Gene III in Human Inflammatory Bowel Disease and a Murine Bacterial Reconstitution Model
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Effect of normal microbial flora on intestinal surface area
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Enteric commensal bacteria potentiate epithelial restitution via reactive oxygen species-mediated inactivation of focal adhesion kinase phosphatases
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Host Defense Peptide LL-37 Selectively Reduces Proinflammatory Macrophage Responses
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Probiotic E. coli treatment mediates antimicrobial human β-defensin synthesis and fecal excretion in humans
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Viscosity gradient within the mucus layer determines the mucosal barrier function and the spatial organization of the intestinal microbiota
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Multi-layered regulation of intestinal antimicrobial defense
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Role of M Cells in Intestinal Barrier Function
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Altered intestinal epithelial homeostasis in mice with intestine-specific deletion of the Krüppel-like factor 4 gene
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Germ-free and Colonized Mice Generate the Same Products from Enteric Prodefensins
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The MUC13 cell-surface mucin protects against intestinal inflammation by inhibiting epithelial cell apoptosis
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Enteric Salmonella Infection Inhibits Paneth Cell Antimicrobial Peptide Expression
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Commensal and Probiotic Bacteria Influence Intestinal Barrier Function and Susceptibility to Colitis in Nod1−/−;Nod2−/− Mice
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Histochemical, Lectin-Histochemical and Morphometrical Characteristics of Intestinal Goblet Cells of Germfree and Conventional Mice.
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Barrier dysfunction due to distinct defensin deficiencies in small intestinal and colonic Crohn's disease
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Campylobacter jejuni induces transcellular translocation of commensal bacteria via lipid rafts
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Epithelial dysfunction associated with the development of colitis in conventionally housed mdr1a−/− mice
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Paneth's disease
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96 Muramyl Dipeptide Activation of Nucleotide-Binding Oligomerization Domain 2 Protects Mice from Experimental Colitis
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The VSL# 3 Probiotic Mixture Modifies Microflora but Does Not Heal Chronic Dextran-Sodium Sulfate–Induced Colitis or Reinforce the Mucus Barrier in Mice
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Pre-epithelial mucus layer in the colon of conventional and germ-free rats
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Modulation of Mouse Paneth Cell α-Defensin Secretion by mIKCa1, a Ca2+-activated, Intermediate Conductance Potassium Channel
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Commensal Bacteria Exacerbate Intestinal Inflammation but Are Not Essential for the Development of Murine Ileitis
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SMALL INTESTINAL MUCOSAL CELL PROLIFERATION AND BACTERIAL FLORA IN THE CONVENTIONALIZATION OF THE GERMFREE MOUSE
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Cutting Edge: Transgenic Expression of Human MUC1 in IL-10−/− Mice Accelerates Inflammatory Bowel Disease and Progression to Colon Cancer
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Lactobacillus plantarum ameliorates colonic epithelial barrier dysfunction by modulating the apical junctional complex and PepT1 in IL-10 knockout mice
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Host Responses to Intestinal Microbial Antigens in Gluten-Sensitive Mice
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The role of indigenous microflora in the development of murine intestinal fucosyl‐ and sialyltransferases
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Innate immunity and mucosal bacterial interactions in the intestine
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A paradoxical reduction in susceptibility to colonic injury upon targeted transgenic ablation of goblet cells
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Altered Epithelial Cell Lineage Allocation and Global Expansion of the Crypt Epithelial Stem Cell Population Are Associated with Ileitis in SAMP1/YitFc Mice
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Multifaceted transcriptional regulation of the murine intestinal mucus layer by endogenous microbiota
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Changes in colonic mucins of germfree rats in response to the introduction of a "normal" rat microbial flora. Rat colonic mucin.
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Pharmabiotic Manipulation of the Microbiota in Gastrointestinal Disorders, from Rationale to Reality
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Mechanisms of Tight Junction Dysregulation in the SAMP1/YitFc Model of Crohn's Disease–like Ileitis
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Defensins keep the peace too
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Flagged first, then by citations

1 of the 146 references couldn’t be matched to a known paper.

Sorted by citations

Introduction to the human gut microbiota
Thursby, E., & Juge, N. (2017) · Biochemical Journal · doi:10.1042/bcj20160510 · Cited by 3,600 · see citing works
The gut microbiome and liver cancer: mechanisms and clinical translation
Yu, L.-X., & Schwabe, R. F. (2017) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2017.72 · Cited by 634 · see citing works
The Intestinal Microbiota and Colorectal Cancer
Cheng, Y., Ling, Z., & Li, L. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.615056 · Cited by 587 · see citing works
“A healthy human intestinal microbiota plays a crucial role in harvesting energy (20), shaping the intestinal epithelium (21), protecting against pathogens (22), and maintaining immunity (23).”
Background
Analysis of Gut Microbiota in Patients with Parkinson’s Disease
Petrov, V. A., Saltykova, I. V., Zhukova, I. A., Alifirova, V. M., Zhukova, N. G., Dorofeeva, Y. B., Tyakht, A. V., Kovarsky, B. A., Alekseev, D. G., Kostryukova, E. S., et al. (2017) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-017-3700-7 · Cited by 487 · see citing works
Functions of Gut Microbiota Metabolites, Current Status and Future Perspectives
Liu, J., Tan, Y., Cheng, H., Zhang, D., Feng, W., & Peng, C. (2022) · Aging and disease · doi:10.14336/ad.2022.0104 · Cited by 529 · see citing works
“cells and Paneth cells), and the inner lamina propria layer where innate and adaptive immune cells dwell, such as T cells, B cells, dendritic cells, macrophages, and IgA producing plasma cells [5,114,115].”
Background
The Intestinal Barrier and Current Techniques for the Assessment of Gut Permeability
Schoultz, I., & Keita, Å. V. (2020) · Cells · doi:10.3390/cells9081909 · Cited by 479 · see citing works
“paracellular permeability essential for nutrient uptake and strengthening of the mucus layer [31,32].”
Background
Intestinal Inflammation and Mucosal Barrier Function
de Medina, F. S., Romero‐Calvo, I., Mascaraque, C., & Martínez‐Augustin, O. (2014) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000204 · Cited by 435 · see citing works
“bowel syndrome, metabolic syndrome, allergy, hepatic inflammation, septic shock, etc.(2) IBD comprises ulcerative colitis (UC)”
Background
Gut microbiota in autism and mood disorders
Mangiola, F. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i1.361 · Cited by 413 · see citing works
Stress and the Microbiota–Gut–Brain Axis in Visceral Pain: Relevance to Irritable Bowel Syndrome
Moloney, R. D., Johnson, A. C., O’Mahony, S. M., Dinan, T. G., Meerveld, B. G., & Cryan, J. F. (2015) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12490 · Cited by 396 · see citing works
Microplastics and the gut microbiome: How chronically exposed species may suffer from gut dysbiosis
Fackelmann, G., & Sommer, S. (2019) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2019.04.030 · Cited by 385 · see citing works
Fundamentals of Neurogastroenterology: Basic Science
Vanner, S. J., Meerveld, B. G., Mawe, G. M., Shea‐Donohue, T., Verdu, E. F., Wood, J. D., & Grundy, D. (2016) · Gastroenterology · doi:10.1053/j.gastro.2016.02.018 · Cited by 369 · see citing works
“Adapted with permission from Natividad et al.(46) MAMP, microbeassociated molecular pattern; PRR, pattern recognition receptors.”
MethodSelf-citation
Changes in intestinal barrier function and gut microbiota in high-fat diet-fed rats are dynamic and region dependent
Hamilton, M. K., Boudry, G., Lemay, D. G., & Raybould, H. E. (2015) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00029.2015 · Cited by 325 · see citing works
A critical review on the impacts of β-glucans on gut microbiota and human health
Jayachandran, M., Chen, J., Chung, S. S. M., & Xu, B. (2018) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2018.06.010 · Cited by 333 · see citing works
“Apart from these specific health benefits, gut microbiota also offers several physiological support such as improving gut integrity [7], energy harvest [8], protect the host”
Exercise induction of gut microbiota modifications in obese, non-obese and hypertensive rats
Petriz, B. A., Castro, A. P., Almeida, J. A., Gomes, C. P., Fernandes, G. R., Kruger, R. H., Pereira, R. W., & Franco, O. L. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-511 · Cited by 293 · see citing works
Interplay Between Exercise and Gut Microbiome in the Context of Human Health and Performance
Clauss, M., Gérard, P., Mosca, A., & Leclerc, M. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.637010 · Cited by 295 · see citing works
Proteins and Carbohydrates from Red Seaweeds: Evidence for Beneficial Effects on Gut Function and Microbiota
Cian, R., Drago, S., De Medina, F., & Martínez-Augustin, O. (2015) · Marine Drugs · doi:10.3390/md13085358 · Cited by 238 · see citing works
“Interestingly, recent advances have also shown that systemic diseases, like metabolic syndrome, allergy, chronic kidney disease or hepatic inflammation, can be related to modifications in intestinal MBF [11–14].”
Antibiotics induced intestinal tight junction barrier dysfunction is associated with microbiota dysbiosis, activated NLRP3 inflammasome and autophagy
Feng, Y., Huang, Y., Wang, Y., Wang, P., Song, H., & Wang, F. (2019) · PLoS ONE · doi:10.1371/journal.pone.0218384 · Cited by 225 · see citing works
“It has been reported that intestinal microbiota and its derived SCFAs are crucial to intestinal barrier integrity [20, 21].”
Background
Lactobacillus rhamnosusCNCM I-3690 and the commensal bacteriumFaecalibacterium prausnitziiA2-165 exhibit similar protective effects to induced barrier hyper-permeability in mice
Laval, L., Martín, R., Natividad, J. M., Chain, F., Miquel, S., de Maredsous, C. D., Capronnier, S., Sokol, H., Verdu, E. F., Vlieg, J. E. T. V. H., et al. (2014) · Gut Microbes · doi:10.4161/19490976.2014.990784 · Cited by 215 · see citing works
“The TJs are composed of transmembrane proteins occludins, claudins and Junctional Adhesion Molecule (JAM/F11r) that are linked to the actin cytoskeleton through Zonula Occludens (ZO) proteins.(5) To test the hypothesis of a DNBS-induced permeability due to an alteration of TJs and AJs levels, expression of the most re…”
BackgroundSelf-citation
Crosstalk between intestinal microbiota, adipose tissue and skeletal muscle as an early event in systemic low‐grade inflammation and the development of obesity and diabetes
Bleau, C., Karelis, A. D., St‐Pierre, D. H., & Lamontagne, L. (2014) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2617 · Cited by 215 · see citing works
“tight junction assembly and epithelial cell renewal [31,32].”
Background
Efficacy of probiotic treatment with Bifidobacterium longum 536 for induction of remission in active ulcerative colitis: A randomized, double‐blinded, placebo‐controlled multicenter trial
Tamaki, H., Nakase, H., Inoue, S., Kawanami, C., Itani, T., Ohana, M., Kusaka, T., Uose, S., Hisatsune, H., Tojo, M., et al. (2016) · Digestive Endoscopy · doi:10.1111/den.12553 · Cited by 214 · see citing works
Gut Microbial Flora, Prebiotics, and Probiotics in IBD: Their Current Usage and Utility
Scaldaferri, F., Gerardi, V., Lopetuso, L. R., Zompo, F. D., Mangiola, F., Boškoski, I., Bruno, G., Petito, V., Laterza, L., Cammarota, G., et al. (2013) · BioMed Research International · doi:10.1155/2013/435268 · Cited by 207 · see citing works
“In recent years several studies investigated the correlation between dysbiosis and intestinal and extraintestinal diseases, including immune system alteration, obesity, allergies, autoimmune diseases, irritable bowel syndrome (IBS), and inflammatory bowel disease (IBD) [14, 15].”
Background
Gut Microbiota Resilience: Definition, Link to Health and Strategies for Intervention
Dogra, S. K., Dore, J. M., & Damak, S. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.572921 · Cited by 198 · see citing works
The Burden of Carbohydrates in Health and Disease
Clemente‐Suárez, V. J., Mielgo‐Ayuso, J., Martín-Rodríguez, A., Ramos‐Campo, D. J., Redondo-Flórez, L., & Tornero-Aguilera, J. F. (2022) · Nutrients · doi:10.3390/nu14183809 · Cited by 223 · see citing works
The potential probiotic Lactobacillus rhamnosus CNCM I-3690 strain protects the intestinal barrier by stimulating both mucus production and cytoprotective response
Martín, R., Chamignon, C., Mhedbi-Hajri, N., Chain, F., Derrien, M., Escribano-Vázquez, U., Garault, P., Cotillard, A., Pham, H., Chervaux, C., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-41738-5 · Cited by 188 · see citing works
Cellular and Molecular Therapeutic Targets in Inflammatory Bowel Disease—Focusing on Intestinal Barrier Function
Schoultz, I., & Keita, Å. V. (2019) · Cells · doi:10.3390/cells8020193 · Cited by 187 · see citing works
“However, a disruption of the composition of the gut microbiota will impact the host-microbial interactions and influence the intestinal physiology resulting in a diminished intestinal barrier function [10].”
Background
Chronic exposure to low concentrations of lead induces metabolic disorder and dysbiosis of the gut microbiota in mice
Xia, J., Jin, C., Pan, Z., Sun, L., Fu, Z., & Jin, Y. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.03.053 · Cited by 182 · see citing works
Dysbiosis Disrupts Gut Immune Homeostasis and Promotes Gastric Diseases
Toor, D., Wasson, M. K., Goel, C., Kaushik, N. K., Kaushik, N. K., Singh, S., Karthikeyan, G., Kumar, A., & Prakash, H. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20102432 · Cited by 182 · see citing works
Interactions between gut microbiota and polyphenols: A mechanistic and metabolomic review
Cheng, H., Zhang, D., Wu, J., Liu, J., Zhou, Y., Tan, Y., Feng, W., & Peng, C. Y. (2023) · Phytomedicine · doi:10.1016/j.phymed.2023.154979 · Cited by 188 · see citing works
Impacts of foodborne inorganic nanoparticles on the gut microbiota-immune axis: potential consequences for host health
Lamas, B., Breyner, N. M., & Houdeau, É. (2020) · Particle and Fibre Toxicology · doi:10.1186/s12989-020-00349-z · Cited by 177 · see citing works
Polystyrene microplastic-induced oxidative stress triggers intestinal barrier dysfunction via the NF-κB/NLRP3/IL-1β/MCLK pathway
Zeng, G., Li, J., Wang, Y., Su, J., Lu, Z., Zhang, F., & Ding, W. (2024) · Environmental Pollution · doi:10.1016/j.envpol.2024.123473 · Cited by 189 · see citing works
Disturbances of the Gut Microbiota and Microbiota-Derived Metabolites in Inflammatory Bowel Disease
Hu, Y., Chen, Z., Xu, C., Kan, S., & Chen, D. (2022) · Nutrients · doi:10.3390/nu14235140 · Cited by 175 · see citing works
“Gut microbiota dysbiosis can lead to a relative increase in opportunistic pathogens and the impairment of intestinal microbial barrier function, increasing intestinal permeability and opportunistic pathogen invasion and, thereby, inducing inflammatory responses in the colon [55].”
Background
Gut microbiota promote liver regeneration through hepatic membrane phospholipid biosynthesis
Yin, Y., Sichler, A., Ecker, J., Laschinger, M., Liebisch, G., Höring, M., Basic, M., Bleich, A., Zhang, X.-J., Kuebelsbeck, L. A., et al. (2023) · Journal of Hepatology · doi:10.1016/j.jhep.2022.12.028 · Cited by 174 · see citing works
Lower Neighborhood Socioeconomic Status Associated with Reduced Diversity of the Colonic Microbiota in Healthy Adults
Miller, G. E., Engen, P. A., Gillevet, P. M., Shaikh, M. W., Sikaroodi, M., Forsyth, C. B., Mutlu, E., & Keshavarzian, A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148952 · Cited by 172 · see citing works
Microbiota-Immune Interaction in the Pathogenesis of Gut-Derived Infection
Wang, C., Li, Q., & Ren, J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01873 · Cited by 167 · see citing works
“Trillions of commensal microorganisms residing in the gastrointestinal (GI) tract can compete for adhesion sites with pathogens, and comprise the first line of defense against bacterial translocation (21).”
Background
Dietary Fiber Increases Butyrate-Producing Bacteria and Improves the Growth Performance of Weaned Piglets
Zhao, J., Liu, P., Wu, Y., Guo, P., Liu, L., Ma, N., Levesque, C. L., Chen, Y., Zhao, J., Zhang, J., et al. (2018) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.8b02545 · Cited by 158 · see citing works
Oral exposure to environmental pollutant benzo[a]pyrene impacts the intestinal epithelium and induces gut microbial shifts in murine model
Ribière, C., Peyret, P., Parisot, N., Darcha, C., Déchelotte, P. J., Barnich, N., Peyretaillade, É., & Boucher, D. (2016) · Scientific Reports · doi:10.1038/srep31027 · Cited by 154 · see citing works
Quorum Sensing, Biofilm, and Intestinal Mucosal Barrier: Involvement the Role of Probiotic
Deng, Z., Luo, X., Liu, J., & Wang, H. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.538077 · Cited by 152 · see citing works
“There is constant interaction between the epithelial cells and the gut microbiota, both of which have been implicated in the regulation of intestinal barrier function (Natividad and Verdu, 2013).”
Background
Gut microbiota and Hashimoto’s thyroiditis
Virili, C., Fallahi, P., Antonelli, A., Benvenga, S., & Centanni, M. (2018) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-018-9467-y · Cited by 157 · see citing works
Mechanistic Insights Into Probiotic Properties of Lactic Acid Bacteria Associated With Ethnic Fermented Dairy Products
Ghosh, T., Beniwal, A., Semwal, A., & Navani, N. K. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00502 · Cited by 141 · see citing works
Microbial markers in colorectal cancer detection and/or prognosis
Villéger, R., Lopès, A., Véziant, J., Gagnière, J., Barnich, N., Billard, E., Boucher, D., & Bonnet, M. (2018) · World Journal of Gastroenterology · doi:10.3748/wjg.v24.i22.2327 · Cited by 139 · see citing works
Interactions between gut microbiota and berberine, a necessary procedure to understand the mechanisms of berberine
Cheng, H., Liu, J., Tan, Y., Feng, W., & Peng, C. Y. (2021) · Journal of Pharmaceutical Analysis · doi:10.1016/j.jpha.2021.10.003 · Cited by 137 · see citing works
“Studies have revealed that gut microbiota has the capacity to regulate the function of intestinal barrier by regulating intestinal epithelial cell renewal, influencing intestinal permeability, and modulating antimicrobial protein expression and the mucus layer [181].”
Background
Recent Advancements in the Development of Modern Probiotics for Restoring Human Gut Microbiome Dysbiosis
Kumar, R., Sood, U., Gupta, V., Singh, M., Scaria, J., & Lal, R. (2019) · Indian Journal of Microbiology · doi:10.1007/s12088-019-00808-y · Cited by 133 · see citing works
The Compromised Intestinal Barrier Induced by Mycotoxins
Gao, Y., Meng, L., Liu, H., Wang, J., & Zheng, N. (2020) · Toxins · doi:10.3390/toxins12100619 · Cited by 129 · see citing works
Microbiome in cancer: Role in carcinogenesis and impact in therapeutic strategies
Rahman, M. M., Islam, M. R., Shohag, S., Ahasan, M. T., Sarkar, N., Khan, H., Hasan, A. M., Cavalu, S. D., & Rauf, A. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.112898 · Cited by 129 · see citing works
The Role of the Microbiome in Cancer Initiation and Progression: How Microbes and Cancer Cells Utilize Excess Energy and Promote One Another’s Growth
Whisner, C. M., & Aktipis, A. (2019) · Current Nutrition Reports · doi:10.1007/s13668-019-0257-2 · Cited by 128 · see citing works
Metagenome and metabolism: the tissue microbiota hypothesis
Burcelin, R., Sérino, M., Chabo, C., Garidou, L., Pomié, C., Courtney, M., Amar, J., & Bouloumié, A. (2013) · Diabetes Obesity and Metabolism · doi:10.1111/dom.12157 · Cited by 124 · see citing works
“The dual relationship between the intestinal immune system and epithelium permeability results from complex interactions with the microbiota [91].”
Background
Butyrate ameliorated ferroptosis in ulcerative colitis through modulating Nrf2/GPX4 signal pathway and improving intestinal barrier
Chen, H., Qian, Y., Jiang, C., Tang, L., Yu, J., Zhang, L., Dai, Y., & Jiang, G. Z. (2023) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2023.166984 · Cited by 127 · see citing works
The Potential of Lactobacillus spp. for Modulating Oxidative Stress in the Gastrointestinal Tract
Kong, Y., Olejar, K. J., On, S. L. W., & Chelikani, V. (2020) · Antioxidants · doi:10.3390/antiox9070610 · Cited by 125 · see citing works
“They may be considered as an extension of the human body, and contribute to the gut integrity [6], nutrient metabolism [7] and metabolic homeostasis [8].”
Background
Bacteriophages as potential new mammalian pathogens
Tetz, G. V., Ruggles, K. V., Zhou, H., Heguy, A., Tsirigos, A., & Tetz, V. (2017) · Scientific Reports · doi:10.1038/s41598-017-07278-6 · Cited by 120 · see citing works
“Discussion The aims of the present study were to determine (1) whether bacteriophages could induce alterations of the gut flora, leading to gut leakiness and an impaired intestinal barrier; and (2) whether bacteriophage treatment could increase gut permeability in mammals, sufficient to facilitate endotoxemia and infl…”
Background
Effects of Anthocyanin on Intestinal Health: A Systematic Review
Verediano, T. A., Martino, H. S. D., Paes, M. C. D., & Tako, E. (2021) · Nutrients · doi:10.3390/nu13041331 · Cited by 125 · see citing works
“Therefore, impairments of the physical barrier may enhance the risk of infections, inflammatory intestinal diseases and other diseases occurring outside the intestine such as immune-related and metabolic disorders [1,3].”
Background
Short-chain fatty acids, secondary bile acids and indoles: gut microbial metabolites with effects on enteroendocrine cell function and their potential as therapies for metabolic disease
Masse, K. E., & Lu, V. B. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1169624 · Cited by 120 · see citing works
Gut-on-a-chip models for dissecting the gut microbiology and physiology
Valiei, A., Aminian-Dehkordi, J., & Mofrad, M. R. K. (2023) · APL Bioengineering · doi:10.1063/5.0126541 · Cited by 117 · see citing works
Exposure to a Healthy Gut Microbiome Protects Against Reproductive and Metabolic Dysregulation in a PCOS Mouse Model
Torres, P. J., Ho, B., Arroyo, P., Sau, L., Chen, A., Kelley, S. T., & Thackray, V. G. (2019) · Endocrinology · doi:10.1210/en.2019-00050 · Cited by 109 · see citing works
The role of gut microbiota in the effects of maternal obesity during pregnancy on offspring metabolism
Zhou, L., & Xiao, X. (2017) · Bioscience Reports · doi:10.1042/bsr20171234 · Cited by 107 · see citing works
TLR2 and TLR4 in Parkinson’s disease pathogenesis: The environment takes a toll on the gut
Gorecki, A. M., Anyaegbu, C. C., & Anderton, R. S. (2021) · Translational Neurodegeneration · doi:10.1186/s40035-021-00271-0 · Cited by 103 · see citing works
“The gut barrier is dynamically regulated by microbial metabolites and pattern recognition receptor signalling to simultaneously respond to symbiotic gut microbes and invading pathogens [80, 81].”
Background
“With a little help from my friends”—the role of microbiota in thyroid hormone metabolism and enterohepatic recycling
Virili, C., & Centanni, M. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.01.053 · Cited by 105 · see citing works
“Indeed, several changes were observed in germ-free mice: reduced intestinal surface area, mostly due to shorter villi and reduced intestinal crypts, altered permeability with impaired traffic of macromolecules and ions as well as a reduction of mucus thickness (Natividad and Verdu, 2013).”
Background
Changes in intestinal barrier functions and gut microbiota in rats exposed to zearalenone
Zhang, W., Zhang, S., Wang, J., Shan, A., & Li, X. (2020) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2020.111072 · Cited by 102 · see citing works
peu-MIR2916-p3-enriched garlic exosomes ameliorate murine colitis by reshaping gut microbiota, especially by boosting the anti-colitic Bacteroides thetaiotaomicron
Wang, X., Liu, Y., Dong, X., Duan, T., Wang, C., Wang, L., Yang, X., Tian, H., & Li, T. (2024) · Pharmacological Research · doi:10.1016/j.phrs.2024.107071 · Cited by 102 · see citing works
Impact of Protein Intake in Older Adults with Sarcopenia and Obesity: A Gut Microbiota Perspective
Prokopidis, K., Cervo, M. M., Gandham, A., & Scott, D. (2020) · Nutrients · doi:10.3390/nu12082285 · Cited by 99 · see citing works
“, bacteria, eukaryotic microbes, viruses, fungi, archaea), which are considered a contributor to a range of physiological functions, such as strengthening the gut integrity [44], regulating host immunity [45], and maintaining metabolic health [46].”
Background
Indoleacrylic acid produced by Parabacteroides distasonis alleviates type 2 diabetes via activation of AhR to repair intestinal barrier
Liu, D., Zhang, S., Li, S., Zhang, Q., Cai, Y., Li, P., Li, H., Shen, B., Liao, Q., Hong, Y., et al. (2023) · BMC Biology · doi:10.1186/s12915-023-01578-2 · Cited by 97 · see citing works
“Research confirms that a high-fat diet causes disruption of intestinal barrier functional connexin and occludin, which affects the gut microbiota [44].”
Background
Utilizing Probiotics for the Prevention and Treatment of Gastrointestinal Diseases
Milner, E., Stevens, B. D., An, M., Lam, V., Ainsworth, M., Dihle, P. J., Stearns, J., Dombrowski, A., Rego, D. T., & Segars, K. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.689958 · Cited by 97 · see citing works
Gut barrier dysfunction and microbial translocation in cancer cachexia
Klein, G. L., Petschow, B. W., Shaw, A. L., & Weaver, E. M. (2013) · Current Opinion in Supportive and Palliative Care · doi:10.1097/spc.0000000000000017 · Cited by 95 · see citing works
The connection between microbiome and schizophrenia
Golofast, B., & Vales, K. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.12.011 · Cited by 92 · see citing works
A review of saponin intervention in metabolic syndrome suggests further study on intestinal microbiota
Luo, Z., Xu, W., Zhang, Y., Di, L., & Shan, J. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2020.105088 · Cited by 93 · see citing works
Alleviation of DSS-induced colitis via Lactobacillus acidophilus treatment in mice
Kim, W.-K., Han, D. H., Jang, Y. J., Park, S., Jang, S. J., Lee, G., Han, H. S., & Ko, G. (2020) · Food & Function · doi:10.1039/d0fo01724h · Cited by 92 · see citing works
Implication of G Protein-Coupled Receptor 43 in Intestinal Inflammation: A Mini-Review
Yang, G., Chen, S., Deng, B., Tan, C., Deng, J., Zhu, G., Yin, Y., & Ren, W. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01434 · Cited by 92 · see citing works
The Microbiota and Cancer Cachexia
Herremans, K. M., Riner, A. N., Cameron, M. E., & Trevino, J. G. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20246267 · Cited by 89 · see citing works
“It serves to protect the body from intraluminal pathogens through the recognition of foreign microbes and secretion of antibodies, antimicrobial peptides and mucus [29].”
Background
Current knowledge about the connection between health status and gut microbiota from birth to elderly. A narrative review
Santacroce, L., Man, A., Charitos, I. A., Haxhirexha, K., & Topi, S. (2021) · Frontiers in Bioscience-Landmark · doi:10.52586/4930 · Cited by 87 · see citing works
“In particular, therefore, the components of microbes can promote or protect against diseases [22, 25, 26].”
Background
Probiotics’ Effects in the Treatment of Anxiety and Depression: A Comprehensive Review of 2014–2023 Clinical Trials
Merkouris, E., Mavroudi, T., Miliotas, D., Tsiptsios, D., Serdari, A., Christidi, F., Doskas, T. K., Mueller, C., & Tsamakis, K. (2024) · Microorganisms · doi:10.3390/microorganisms12020411 · Cited by 88 · see citing works
“…microorganisms, that are critical for a variety of physiological functions, including preserving gut integrity or forming the intestinal epithelium [4], obtaining energy [5], protecting against infections [6], and controlling host immunity [7]; it is thus considered an “invisible organ” of the…”
Background
Potential role of gut microbiota and tissue barriers in Parkinson's disease and amyotrophic lateral sclerosis
Fang, X. (2015) · International Journal of Neuroscience · doi:10.3109/00207454.2015.1096271 · Cited by 84 · see citing works
“Changes in the intestinal microbiota have been correlated with alterations in the intestinal barrier in gastrointestinal diseases, such as irritable bowel syndrome [31].”
Background
Does microbiota composition affect thyroid homeostasis?
Virili, C., & Centanni, M. (2014) · Endocrine · doi:10.1007/s12020-014-0509-2 · Cited by 85 · see citing works
“Mucus layer, produced by goblet cells, may vary in composition, fluidity, and electric properties [5].”
BackgroundInfluential
Pea ( Pisum sativum L.) seed albumin extracts show anti‐inflammatory effect in the DSS model of mouse colitis
Utrilla, M. P., Peinado, M. J., Ruiz, R., Rodríguez‐Nogales, A., Algieri, F., Rodríguez‐Cabezas, M. E., Clemente, A., Gálvez, J., & Rubio, L. A. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201400630 · Cited by 86 · see citing works
“This is relevant, since the inflamed mucosal epithelium in these intestinal conditions is frequently characterized by the presence of ulceration and necrosis, and the restoration of the intestinal tissue implies the renovation of these cells, a process that requires an adequate protein supply through the diet [45].”
Background
Insights Into a Possible Influence on Gut Microbiota and Intestinal Barrier Function During Chronic Exposure of Mice to Imazalil
Jin, C., Xia, J., Wu, S., Tu, W., Pan, Z., Fu, Z., Wang, Y., & Jin, Y. (2017) · Toxicological Sciences · doi:10.1093/toxsci/kfx227 · Cited by 84 · see citing works
Sulforaphane Normalizes Intestinal Flora and Enhances Gut Barrier in Mice with BBN‐Induced Bladder Cancer
He, C., Huang, L., Peng, L., Liu, X., Li, B., & Shan, Y. (2018) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201800427 · Cited by 81 · see citing works
Oral administration of green tea polyphenols (TP) improves ileal injury and intestinal flora disorder in mice with Salmonella typhimurium infection via resisting inflammation, enhancing antioxidant action and preserving tight junction
Zhang, L., Gui, S., Wang, J., Chen, Q., Zeng, J., Liu, A., Chen, Z., & Lu, X. (2019) · Journal of Functional Foods · doi:10.1016/j.jff.2019.103654 · Cited by 81 · see citing works
Factors influencing development of the infant microbiota: from prenatal period to early infancy
Jeong, S. (2021) · Korean Journal of Pediatrics · doi:10.3345/cep.2021.00955 · Cited by 81 · see citing works
“(2) Proton pump inhibitors The impact of proton pump inhibitors (PPIs) and other acidblocking medications in young infants is gaining more attention, as disturbances in the microbiome have been reported.”
Background
Age-related cognitive decline is associated with microbiota-gut-brain axis disorders and neuroinflammation in mice
Wu, M., Yang, X., Li, X., Duan, W., & Du, J. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113125 · Cited by 83 · see citing works
First evidence of altered microbiota and intestinal damage and their link to absence epilepsy in a genetic animal model, the WAG/Rij rat
Citraro, R., Lembo, F., Caro, C. D., Tallarico, M., Coretti, L., Iannone, L. F., Leo, A., Palumbo, D., Cuomo, M., Buommino, E., et al. (2021) · Epilepsia · doi:10.1111/epi.16813 · Cited by 82 · see citing works
Intestinal Microbiome‐Macrophage Crosstalk Contributes to Cholestatic Liver Disease by Promoting Intestinal Permeability in Mice
Isaacs‐Ten, A., Echeandia, M., Moreno‐Gonzalez, M., Brion, A., Goldson, A. J., Philo, M. R., Patterson, A. M., Parker, A., Galduroz, M., Baker, D., et al. (2020) · Hepatology · doi:10.1002/hep.31228 · Cited by 80 · see citing works
“aNIt-INDUCeD CHoleStaSIS pRoMoteS CHaNgeS IN tHe MICRoBIoMe CoMpoSItIoN oF gF + Wt MICe Previous studies have shown that changes in the microbiome are associated with altered TJ protein expression.(30,31) We performed 16s ribosomal RNA (rRNA) sequence analysis of fecal samples with LotuS(32) and found significant taxo…”
Background
Metallobiology of Lactobacillaceae in the gut microbiome
Huynh, U., & Zastrow, M. L. (2022) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2022.112023 · Cited by 80 · see citing works
Bifidobacterium animalis ssp. lactis CNCM-I2494 Restores Gut Barrier Permeability in Chronically Low-Grade Inflamed Mice
Martín, R., Laval, L., Chain, F., Miquel, S., Natividad, J. M., Cherbuy, C., Sokol, H., Verdu, E. F., Vlieg, J. V. H., Bermúdez‐Humarán, L. G., et al. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00608 · Cited by 78 · see citing works
“The physical barrier is formed by a mucus layer followed by a monolayer of epithelial cells (Denker and Nigam, 1998; Natividad and Verdu, 2013) performing the paracellular transport across the barrier controlled by apical junction proteins (Natividad and Verdu, 2013).”
Self-citation
Orthogonal Comparison of GC–MS and 1H NMR Spectroscopy for Short Chain Fatty Acid Quantitation
Cai, J., Zhang, J., Tian, Y., Zhang, L., Hatzakis, E., Krausz, K. W., Smith, P. B. W., Gonzalez, F. J., & Patterson, A. D. (2017) · Analytical Chemistry · doi:10.1021/acs.analchem.7b00848 · Cited by 78 · see citing works
Novel perspectives on therapeutic modulation of the gut microbiota
McCarville, J. L., Caminero, A., & Verdu, E. F. (2016) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756283x16637819 · Cited by 77 · see citing works
“This includes both functionality (permeability) and immune or structural parameters of the barrier such as secretion of antimicrobial peptides and mucins, in which the microbiota can play a central role [Vaishnava et al. 2008; Natividad and Verdu, 2013].”
Self-citation
Dietary Gluten as a Conditioning Factor of the Gut Microbiota in Celiac Disease
Bascuñán, K. A., Araya, M., Roncoroni, L., Doneda, L., & Elli, L. (2019) · Advances in Nutrition · doi:10.1093/advances/nmz080 · Cited by 76 · see citing works
Subchronic exposure of environmentally relevant concentrations of F-53B in mice resulted in gut barrier dysfunction and colonic inflammation in a sex-independent manner
Pan, Z., Yuan, X., Tu, W., Fu, Z., & Jin, Y. (2019) · Environmental Pollution · doi:10.1016/j.envpol.2019.07.021 · Cited by 74 · see citing works
A cafeteria diet triggers intestinal inflammation and oxidative stress in obese rats
Gil‐Cardoso, K., Ginés, I., Pinent, M., Ardèvol, A., Terra, X., & Blay, M. (2017) · British Journal Of Nutrition · doi:10.1017/s0007114516004608 · Cited by 75 · see citing works
“Other data suggest that certain bacterial species produce metabolites that can influence intestinal permeability and integrity((42)).”
Background
Could the beneficial effects of dietary calcium on obesity and diabetes control be mediated by changes in intestinal microbiota and integrity?
Gomes, J. M. G., Costa, J. A., & Alfenas, R. D. C. G. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114515003608 · Cited by 72 · see citing works
In Vitro Probiotic and Antioxidant Potential of Lactococcus lactis subsp. cremoris LL95 and Its Effect in Mice Behaviour
Ramalho, J. B., Soares, M. B., Spiazzi, C. C., Bicca, D. F., Soares, V. M., Pereira, J. G., da Silva, W. P., Sehn, C. P., & Cibin, F. W. S. (2019) · Nutrients · doi:10.3390/nu11040901 · Cited by 72 · see citing works
β-Sitosterol Ameliorates Endometrium Receptivity in PCOS-Like Mice: The Mediation of Gut Microbiota
Yu, Y., Cao, Y., Huang, W., Liu, Y., Lü, Y., & Zhao, J. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.667130 · Cited by 71 · see citing works
A Preliminary Study Examining the Binding Capacity of Akkermansia muciniphila and Desulfovibrio spp., to Colonic Mucin in Health and Ulcerative Colitis
Earley, H., Lennon, G., Balfe, Á., Kilcoyne, M., Clyne, M., Joshi, L., Carrington, S. D., Martin, S., Coffey, J. C., Winter, D. C., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135280 · Cited by 70 · see citing works
Impact of molecular interactions with phenolic compounds on food polysaccharides functionality
Dobson, C., Mottawea, W., Rodrigue, A. F., Pereira, B. L. B., Hammami, R., Power, K. A., & Bordenave, N. (2019) · Advances in food and nutrition research · doi:10.1016/bs.afnr.2019.02.010 · Cited by 70 · see citing works
Microbiome Metabolites and Thyroid Dysfunction
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Authors: Natividad, J. M. M., & Verdu, E. F.
Affiliations: McMaster University (CA)
Corresponding author: Verdu, Elena F.
ORCID: Verdu, Elena F.
Venue: Pharmacological Research
Publisher: Elsevier BV
Published: 2013-03
Volume: 69
Issue: 1
Pages: 42-51
ISSN: 1043-6618 (ISSN-L)
DOI: 10.1016/j.phrs.2012.10.007
OpenAlex: W2149848289
Cited by: 525
References: 146
Citations by year: 2026: 30 · 2025: 44 · 2024: 68 · 2023: 79 · 2022: 56 · 2021: 65 · 2020: 53 · 2019: 45 · 2018: 23 · 2017: 19 · 2016: 11 · 2015: 13 · 2014: 12 · 2013: 7
FWCI: 0.93
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Pharmacological Research (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Keywords: intestinal barrier, gut microbiota, dysbiosis, commensal bacteria, host-microbe mutualism, obesity, allergy, autoimmunity, irritable bowel syndrome, inflammatory bowel disease, gastrointestinal diseases, treatment options
MeSH terms: Animals, Gastrointestinal Diseases, Humans, Intestines, Bacterial Physiological Phenomena, Metagenome

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Modulation of intestinal barrier by intestinal microbiota: Pathological and therapeutic implications

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