The Role of Microbiota and Probiotics in Stress-Induced Gastrointestinal Damage

Lutgendorff, Femke; Akkermans, Louis; Soderholm, Johan

doi:10.2174/156652408784533779

Cited by 230Probiotics and Fermented FoodsGut microbiota and healthGastrointestinal motility and disorders

The Role of Microbiota and Probiotics in Stress-Induced Gastrointestinal Damage

Lutgendorff, Femke, Akkermans, Louis, Soderholm, Johan·2008·Current Molecular Medicine

DOI 10.2174/156652408784533779

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Abstract

Stress has a major impact on gut physiology and may affect the clinical course of gastro-intestinal diseases. In this review, we focus on the interaction between commensal gut microbiota and intestinal mucosa during stress and discuss the possibilities to counteract the deleterious effects of stress with probiotics. Normally, commensal microbes and their hosts benefit from a symbiotic relationship. Stress does, however, reduce the number of Lactobacilli, while on the contrary, an increased growth, epithelial adherence and mucosal uptake of gram-negative pathogens, e.g. E. coli and Pseudomonas, are seen. Moreover, intestinal bacteria have the ability to sense a stressed host and up-regulate their virulence factors when opportunity knocks. Probiotics are "live microorganisms which, when administered in adequate amounts, confer a health benefit on the host", and mainly represented by Lactic Acid Bacteria. Probiotics can counteract stress-induced changes in intestinal barrier function, visceral sensitivity and gut motility. These effects are strain specific and mediated by direct bacterial-host cell interaction and/or via soluble factors. Mechanisms of action include competition with pathogens for essential nutrients, induction of epithelial heat-shock proteins, restoring of tight junction protein structure, up-regulation of mucin genes, secretion of defensins, and regulation of the NFkappaB signalling pathway. In addition, the reduction of intestinal pain perception was shown to be mediated via cannabinoid receptors. Based on the studies reviewed here there is clearly a rationale for probiotic treatment in patients with stress-related intestinal disorders. We are however far from being able to choose the precise combination of strains or bacterial components for each clinical setting.

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Animal models of chronic stress demonstrate altered intestinal physiology and gut microbiota composition, with an increased secretory state and permeability.
“Animal models of chronic stress demonstrate altered intestinal physiology and GM composition, with an increased secretory state and permeability (352–355).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [355]
Recent studies have suggested that GC signaling derives a portion of its effects through gut microbes.
“Recent studies have suggested that GC signaling derives a portion of its effects through gut microbes.21,22”
From Using Corticosteroids to Reshape the Gut Microbiome: Implications for Inflammatory Bowel Diseases (2015) · cites this paper as [21]

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Song, Z., Yuan, D., & Zhang, S. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1010572 · Cited by 68 · see citing works
“Bacteroidetes Thetaiotaomicron expresses the small prolinerich 2A proteins, which are indispensable for maintaining epithelial villous desmosomes structure (46).”
Background
Does psychological counseling alter the natural history of inflammatory bowel disease?
Wahed, M., Corser, M., Goodhand, J., & Rampton, D. (2010) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21098 · Cited by 69 · see citing works
The Microbiome and Sustainable Healthcare
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“Psychosocial Stress Human Reduced numbers of Lactobacilli with increased gram-negative pathogens Elevated risk of intestinal disorders including loss of barrier function [140]”
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Does the microbiome and virome contribute to myalgic encephalomyelitis/chronic fatigue syndrome?
Newberry, F., Hsieh, S.-Y., Wileman, T., & Carding, S. R. (2018) · Clinical Science · doi:10.1042/cs20171330 · Cited by 61 · see citing works
c-Jun NH2-terminal kinase-2 mediates osmotic stress-induced tight junction disruption in the intestinal epithelium
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Weaning Induced Gut Dysfunction and Nutritional Interventions in Nursery Pigs: A Partial Review
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“Bacteroides thetaiotaomicron is involved in desmosome maintenance at the epithelial villus by inducing the expression of SPRR2A (small proline-rich protein 2A) [80].”
Background
Effect of probiotic yoghurt on animal-based diet-induced change in gut microbiota: an open, randomised, parallel-group study
Odamaki, T., Kato, K., Sugahara, H., Xiao, J., Abe, F., & Benno, Y. (2016) · Beneficial Microbes · doi:10.3920/bm2015.0173 · Cited by 59 · see citing works
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“Epithelial changes such as those described here in the broiler chickens of the infected groups (I and I/HS35) have been reported to trigger an imbalance in the intestinal commensal microbiota (Lutgendorff et al., 2008).”
Background
Randomized Double-Blind Crossover Study for Evaluating a Probiotic Mixture on Gastrointestinal and Behavioral Symptoms of Autistic Children
Guidetti, C., Salvini, E., Viri, M., Deidda, F., Amoruso, A., Visciglia, A., Drago, L., Calgaro, M., Vitulo, N., Pane, M., et al. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11185263 · Cited by 53 · see citing works
Impact of human aging and modern lifestyle on gut microbiota
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“It seems that we are far from being able to choose the exact combination of bacterial types or components that would properly correspond to each of the clinical environments in question (Lutgendorff et al., 2008).”
BackgroundInfluential
Crosstalk between gut microbiotas and fatty acid metabolism in colorectal cancer
Zhang, H., Tian, Y., Xu, C., Chen, M., Xiang, Z., Gu, L., Xue, H., & Xu, Q. R. (2025) · Cell Death Discovery · doi:10.1038/s41420-025-02364-5 · Cited by 52 · see citing works
“In maintaining gut barrier integrity and gastro-intestinal structure, Bacteroides thetaiotaomicron induces the expression of small proline-rich protein 2 A (SPRR2A), essential for maintaining epithelial villous desmosomes [94].”
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Lyu, Y., Su, C., Verbrugghe, A., de Wiele, T. V., Martinez-Caja, A. M., & Hesta, M. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01661 · Cited by 50 · see citing works
“Comparative studies between germ-free and specific-pathogenfree animals indicated the essential role of intestinal microbiota on the development of the GI structure and function (Cario et al., 2007; Lutgendorff et al., 2008; Al-Asmakh and Zadjali, 2015).”
Background
The cross-talk between opportunistic fungi and the mammalian host via microbiota’s metabolism
Romani, L., Zelante, T., Palmieri, M., Napolioni, V., Picciolini, M., Velardi, A., Aversa, F., & Puccetti, P. (2015) · Seminars in Immunopathology · doi:10.1007/s00281-014-0464-2 · Cited by 47 · see citing works
A systematic review of gut‐immune‐brain mechanisms in Autism Spectrum Disorder
Azhari, A., Azizan, F., & Esposito, G. (2018) · Developmental Psychobiology · doi:10.1002/dev.21803 · Cited by 47 · see citing works
The Role of the Gut Microbiota in Health, Diet, and Disease with a Focus on Obesity
Feei, Z., & Lee, Y. Y. (2025) · Foods · doi:10.3390/foods14030492 · Cited by 49 · see citing works
“The expression of the small proline-rich protein 2A induced by Bacteroides thetaiotaomicron is needed for maintaining desmosomes at the epithelial villi [38].”
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Sung, V., Hiscock, H., Tang, M. L. K., Mensah, F. K., Heine, R. G., Stock, A., York, E., Barr, R. G., & Wake, M. A. (2012) · BMC Pediatrics · doi:10.1186/1471-2431-12-135 · Cited by 43 · see citing works
“Animal studies have shown probiotics to change pain perception mediated by the gut and inhibit gut contractile activity in rats [53-59].”
Background
Metagenomic Analysis of the Dynamic Changes in the Gut Microbiome of the Participants of the MARS-500 Experiment, Simulating Long Term Space Flight
Mardanov, A. V., Babykin, M. M., Beletsky, A. V., Grigoriev, A. I., Zinchenko, V. V., Kadnikov, V. V., Kirpichnikov, M. P., Mazur, A. M., Nedoluzhko, A., Novikova, N. D., et al. (2013) · Acta Naturae · doi:10.32607/20758251-2013-5-3-116-125 · Cited by 40 · see citing works
The dichotomous role of the gut microbiome in exacerbating and ameliorating neurodegenerative disorders
Raval, U., Harary, J. M., Zeng, E., & Pasinetti, G. M. (2020) · Expert Review of Neurotherapeutics · doi:10.1080/14737175.2020.1775585 · Cited by 44 · see citing works
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Background
NUTRITION, LONGEVITY AND BEHAVIOR
CANNELLA, C., Savina, C., & Donini, L. M. (2009) · Archives of Gerontology and Geriatrics · doi:10.1016/j.archger.2009.09.008 · Cited by 40 · see citing works
Contribution of microbiota to the intestinal physicochemical barrier
Malago, J. J. (2014) · Beneficial Microbes · doi:10.3920/bm2014.0041 · Cited by 39 · see citing works
Microbiotal-Host Interactions and Hypertension
Galla, S., Chakraborty, S., Mell, B., Vijay–Kumar, M., & Joe, B. (2017) · Physiology · doi:10.1152/physiol.00003.2017 · Cited by 40 · see citing works
Complementary and Alternative Medicine Strategies for Therapeutic Gut Microbiota Modulation in Inflammatory Bowel Disease and their Next-Generation Approaches
Basson, A. R., Lam, M. C., & Cominelli, F. (2017) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2017.08.002 · Cited by 37 · see citing works
Research progress on the regulation of production traits by gastrointestinal microbiota in dairy cows
Liu, L., Wu, P., Guo, A., Yang, Y., Chen, F., & Zhang, Q. (2023) · Frontiers in Veterinary Science · doi:10.3389/fvets.2023.1206346 · Cited by 37 · see citing works
“Bacteroides thetaiotaomicron can not only promote the expression of fucose on the surface of intestinal epithelial cells (59), which facilitates the repair of damaged epithelial cells, but also induce the expression of small proline-rich protein 2A (SPRR2A), rich in proline, in intestinal epithelial cells to maintain…”
Background
Impacts of gut microbiota alteration on age-related chronic liver diseases
Adhikary, S., Esmeeta, A., Dey, A., Banerjee, A., Saha, B., Gopan, P., Duttaroy, A. K., & Pathak, S. (2023) · Digestive and Liver Disease · doi:10.1016/j.dld.2023.06.017 · Cited by 35 · see citing works
Does the Gut Microbial Metabolome Really Matter? The Connection between GUT Metabolome and Neurological Disorders
Marć, M. A., Jastrząb, R., & Mytych, J. (2022) · Nutrients · doi:10.3390/nu14193967 · Cited by 33 · see citing works
E. coli O124 K72 alters the intestinal barrier and the tight junctions proteins of guinea pig intestine
Ren, X., Zhu, Y., Gamallat, Y., Ma, S., Chiwala, G., Meyiah, A., & Xin, Y. (2017) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2017.07.123 · Cited by 31 · see citing works
Effect of ICU interventions on gastrointestinal motility
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Effect of stress on intestinal microbiota of Arctic charr, Atlantic salmon, rainbow trout and Atlantic cod: A review
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Probiotic Bacteria and Enteric Infections
Paton, A., Morona, R., & Paton, J. (2011) · Springer eBooks · doi:10.1007/978-94-007-0386-5 · Cited by 28 · see citing works
Antioxidant Capacity and Behavioral Relevance of a Polyphenolic Extract of Chrysanthellum americanum in a Rat Model of Irritable Bowel Syndrome
Cojocariu, R. O., Ciobica, A. S., Balmuș, I.-M., Guenné, S., Trifan, A. V., Stanciu, C., Hrițcu, L. D., & Lefter, R. M. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/3492767 · Cited by 27 · see citing works
“reduction and gramnegative pathogenic bacteria such as Escherichia coli and Pseudomonas overgrowth, epithelial adherence, and mucosal uptake were well documented [15, 16].”
Background
Effectiveness of Sterilized Symbiotic Drink Containing Lactobacillus helveticus Comparable to Probiotic Alone in Patients with Constipation-Predominant Irritable Bowel Syndrome
Bahrudin, M. F., Rani, R. A., Tamil, A. M., Mokhtar, N. M., & Ali, R. A. R. (2019) · Digestive Diseases and Sciences · doi:10.1007/s10620-019-05695-3 · Cited by 27 · see citing works
Protective Effects and Mechanism of a Novel Probiotic Strain Ligilactobacillus salivarius YL20 against Cronobacter sakazakii-Induced Necrotizing Enterocolitis In Vitro and In Vivo
Wang, W., Geng, M., Zhu, C., Huang, L., Zhang, Y., Zhang, T., Zhao, C., Zhang, T., Du, X., & Wang, N. (2022) · Nutrients · doi:10.3390/nu14183827 · Cited by 25 · see citing works
Clinical Management of the Microbiome in Irritable Bowel Syndrome
Andrews, C. N., Sidani, S., & Marshall, J. K. (2019) · Journal of the Canadian Association of Gastroenterology · doi:10.1093/jcag/gwz037 · Cited by 24 · see citing works
Intestinal microbiota of broilers submitted to feeding restriction and its relationship to hepatic metabolism and fat mass: Fast‐growing strain
Lunedo, R., Furlan, L. R., Alarcon, M. F. F., Squassoni, G. H., Campos, D. M. B., Perondi, D., & Macari, M. (2019) · Journal of Animal Physiology and Animal Nutrition · doi:10.1111/jpn.13093 · Cited by 23 · see citing works
Reconciling Hygiene and Cleanliness: A New Perspective from Human Microbiome
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Gut Microbiota in Heart Failure—The Role of Inflammation
Fountoulakis, P. N., Theofilis, P., Vlachakis, P. K., Karakasis, P., Pamporis, K., Sagris, Μ., Dimitroglou, Y., Tsioufis, P., Oikonomou, E. K., Tsioufis, K. P., et al. (2025) · Biomedicines · doi:10.3390/biomedicines13040911 · Cited by 23 · see citing works
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Health and Disease:Akkermansia muciniphila, the Shining Star of the Gut Flora
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Authors: Lutgendorff, F., Akkermans, L., & Soderholm, J.
Affiliations: Linköping University (SE)
University of Groningen (NL)
Venue: Current Molecular Medicine
Publisher: Bentham Science Publishers Ltd.
Published: 2008-06-01
Volume: 8
Issue: 4
Pages: 282-298
ISSN: 1566-5240 (ISSN-L)
DOI: 10.2174/156652408784533779
OpenAlex: W2099916508
Cited by: 230
References: 0
Citations by year: 2026: 8 · 2025: 16 · 2024: 16 · 2023: 22 · 2022: 22 · 2021: 11 · 2020: 7 · 2019: 12 · 2018: 10 · 2017: 11 · 2016: 11 · 2015: 13 · 2014: 16 · 2013: 13 · 2012: 5
FWCI: 19.77
Type: journal article
Language: en
Open access: closed
Locations: Current Molecular Medicine (publishedVersion)
PubMed (publishedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
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
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords: gut microbiota, probiotics, stress, gastrointestinal injury, intestinal barrier function, lactobacilli, Gram-negative pathogens, pathogen virulence factors, lactic acid bacteria, tight junctions, mucin genes, defensins, NF-κB signaling, cannabinoid receptors
MeSH terms: Animals, Enteritis, Humans, Immunologic Factors, Intestinal Mucosa, Intestines, Stress, Physiological, Stress, Psychological, Critical Illness, Probiotics

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The Role of Microbiota and Probiotics in Stress-Induced Gastrointestinal Damage

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