Cited by 1,136Gut microbiota and healthImmune Response and InflammationT-cell and B-cell Immunology

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Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut

Artis, David·2008·Nature reviews. Immunology

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Abstract

Mucosal surfaces such as the intestinal tract are continuously exposed to both potential pathogens and beneficial commensal microorganisms. This creates a requirement for a homeostatic balance between tolerance and immunity that represents a unique regulatory challenge to the mucosal immune system. Recent findings suggest that intestinal epithelial cells, although once considered a simple physical barrier, are a crucial cell lineage for maintaining intestinal immune homeostasis. This Review discusses recent findings that identify a cardinal role for epithelial cells in sampling the intestinal microenvironment, discriminating pathogenic and commensal microorganisms and influencing the function of antigen-presenting cells and lymphocytes.

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Gut microbiota-derived metabolites contribute negatively to hindgut barrier function development at the early weaning goat model
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Host‐bacteria interactions in the intestine: homeostasis to chronic inflammation
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Evolutionary and ecological forces that shape the bacterial communities of the human gut
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“In general, antibacterial factors are concentrated in the areas closest to the intestinal epithelium and are produced in response to host detection of bacteria through a number of innate and adaptive immune mechanisms.(76,77) These mechanisms have been extensively reviewed elsewhere, so this discussion will focus on s…”
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CCR6 Deficiency Impairs IgA Production and Dysregulates Antimicrobial Peptide Production, Altering the Intestinal Flora
Lin, Y.-L., Ip, P.-P., & Liao, F. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00805 · Cited by 37
“Both innate and adaptive immune cells in intestinal tissues are important for limiting tissue invasion by the resident commensal bacteria (1, 2), and maintenance of the symbiotic relationship between the bacteria and host is a critical factor in intestinal homeostasis.”
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Chitosan Oligosaccharides Regulate the Occurrence and Development of Enteritis in a Human Gut-On-a-Chip
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“This is possible due to the reduction of invading E. coli and the regulatory effect of COS on the NF-κB signaling pathway, which is the main one that regulates the occurrence and development of inflammation (Artis, 2008; Maloy and Powrie, 2011).”
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LncRNA lncLy6C induced by microbiota metabolite butyrate promotes differentiation of Ly6Chigh to Ly6Cint/neg macrophages through lncLy6C/C/EBPβ/Nr4A1 axis
Gao, Y., Zhou, J., Qi, H., Wei, J., Yang, Y., Yue, J., Liu, X., Zhang, Y., & Yang, R. (2020) · Cell Discovery · doi:10.1038/s41421-020-00211-8 · Cited by 46
S-nitrosylation of surfactant protein D as a modulator of pulmonary inflammation
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Gliadin Peptide P31-43 Induces mTOR/NFkβ Activation and Reduces Autophagy: The Role of Lactobacillus paracasei CBA L74 Postbiotc
Conte, M., Nigro, F., Porpora, M., Bellomo, C., Furone, F., Budelli, A., Nigro, R., Barone, M. V., & Nanayakkara, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073655 · Cited by 37
Protein glycosylation—an evolutionary crossroad between genes and environment
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Biofilm formation of mucosa-associated methanoarchaeal strains
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BackgroundInfluential
Human tRNA-Derived Small RNAs Modulate Host–Oral Microbial Interactions
He, X., Li, F., Bor, B., Koyano, K., Cen, L., Xiao, X. G., Shi, W., & Wong, D. T. (2018) · Journal of Dental Research · doi:10.1177/0022034518770605 · Cited by 36
“The human microbiota exists in a delicate balance with its host, and this equilibrium is maintained via multiple mechanisms of cross-domain communication and modulation (Artis 2008; Peterson and Artis 2014).”
Background
ENteric Immunity SImulator: A Tool for In Silico Study of Gastroenteric Infections
Wendelsdorf, K. V., Alam, M., Bassaganya-Riera, J., Bisset, K. R., Eubank, S., Hontecillas, R., Hoops, S., & MARATHE, M. V. (2012) · IEEE Transactions on NanoBioscience · doi:10.1109/tnb.2012.2211891 · Cited by 36
“[42] as well as cytotoxins secreted by M1 that damage epithelial cells.”
Context-Dependent Activation Kinetics Elicited by Soluble versus Outer Membrane Vesicle-Associated Heat-Labile Enterotoxin
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“The intestinal epithelium forms tight intracellular junctions and microvilli that inhibit the attachment and invasion of intestinal organisms (1).”
BackgroundInfluential
Nicotine up-regulates IL-8 expression in human gingival epithelial cells following stimulation with IL-1β or P. gingivalis lipopolysaccharide via nicotinic acetylcholine receptor signalling
Kashiwagi, Y., Yanagita, M., Kojima, Y., Shimabukuro, Y., & Murakami, S. (2011) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2011.10.007 · Cited by 36
Vibrio cholerae Cytolysin Causes an Inflammatory Response in Human Intestinal Epithelial Cells That Is Modulated by the PrtV Protease
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HIV enteropathy and aging
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The interaction between intestinal microenvironment and stroke
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Differential Responses of Colorectal Cancer Cell Lines to Enterococcus faecalis’ Strains Isolated from Healthy Donors and Colorectal Cancer Patients
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“In fact, approximately 20% of cancers are associated with microbes [10], especially CRC [12–14], where a dynamic crosstalk exists between intestinal epithelial cells, the microbes (that colonize their apical surface), and the surrounding local immune cells [15], which, in turn, have a key role in CRC progression, espe…”
Microbiota: Overview and Implication in Immunotherapy-Based Cancer Treatments
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“It is the mucus layer, together with the innate immune system that, at least in mice, actively contains microbiota, mainly in the lumen, limiting penetration into the mucosa and avoiding excessive pro-inflammatory signaling [39].”
Background
Dual oxidase Duox and Toll-like receptor 3 TLR3 in the Toll pathway suppress zoonotic pathogens through regulating the intestinal bacterial community homeostasis in Hermetia illucens L.
Huang, Y., Yu, Y., Zhan, S., Tomberlin, J. K., Huang, D., Cai, M., Zheng, L., Yu, Z., & Zhang, J. (2020) · PLoS ONE · doi:10.1371/journal.pone.0225873 · Cited by 35
A Basal Chordate Model for Studies of Gut Microbial Immune Interactions
Dishaw, L. J., Flores-Torres, J., Mueller, M. G., Karrer, C. R., Skapura, D. P., Melillo, D., Zucchetti, I., Santis, R. D., Pinto, M. R., & Litman, G. W. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00096 · Cited by 35
“Although chronic inflammation in mammals involves a variety of gut-specific lymphocytes (i.e., adaptive immunity), gut microbial recognition, and immune homeostasis largely represent an innate immune phenomenon, for which the epithelium is primarily responsible (Artis, 2008).”
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Telling apart friend from foe: discriminating between commensals and pathogens at mucosal sites
Srinivasan, N. (2010) · Innate Immunity · doi:10.1177/1753425909357577 · Cited by 35
“Besides the important contribution to mammalian metabolism, commensal-derived metabolites are thought to have an immune-modulatory role.(20) For example, butyrate, a by-product of starch digestion, has been shown to inhibit strongly the expression of pro-inflammatory cytokines such as IL-12 and TNF-a, while inducing t…”
BackgroundMethodInfluential
Development of the gut microbiota during early life in premature and term infants
Sim, K., Powell, E., Cornwell, E., Kroll, J. S., & Shaw, A. (2023) · Gut Pathogens · doi:10.1186/s13099-022-00529-6 · Cited by 35
“The community plays an important role in the digestion of food, the development of the immune system and in the maturation of the gut itself [1-3].”
Background
Factors Influencing Neonatal Gut Microbiome and Health with a Focus on Necrotizing Enterocolitis
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Background
Toll-Like Receptors: Role in Inflammation and Commensal Bacteria
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“In addition to regulating the development of the intestinal and systemic immune system, recent studies suggest that alterations in the acquisition or composition of commensal bacteria may trigger or influence the course of various metabolic and inflammatory disease states [63].”
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Rapamycin and MCC950 modified gut microbiota in experimental autoimmune encephalomyelitis mouse by brain gut axis
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Human β-Defensin 3 Peptide Is Increased and Redistributed in Crohn’s Ileitis
Meisch, J. P., Nishimura, M., Vogel, R. M., Sung, H. C., Bednarchik, B., Ghosh, S. K., Fu, P., McCormick, T. S., Weinberg, A., & Levine, A. D. (2013) · Inflammatory Bowel Diseases · doi:10.1097/mib.0b013e318280b11a · Cited by 34
“the a-defensins HD-5 and HD-6, and more recently the Reg family lectin RegIIIg, localize to granules within intestinal crypt Paneth cells.(2,10,25) mRNA of hBD-3 has also been reported in IECs residing near the base of the crypt, as well as those near the surface of the lumen.”
Background
They Must Hold Tight: Junction Proteins, Microbiota And Immunity In Intestinal Mucosa
Castoldi, Â., de Aguiar, C. F., Moraes‐Vieira, P. M., & Câmara, N. O. S. (2015) · Current Protein and Peptide Science · doi:10.2174/1389203716666150630133141 · Cited by 33
Role of the intestinal microbiota and fecal transplantation in inflammatory bowel diseases
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Developmental Immunology and Role of Host Defenses in Fetal and Neonatal Susceptibility to Infection
Lewis, D. B., & Wilson, C. B. (2010) · Elsevier eBooks · doi:10.1016/b978-1-4160-6400-8.00004-3 · Cited by 35
Bacterial protein AvrA stabilizes intestinal epithelial tight junctions via blockage of the C-Jun N-terminal kinase pathway
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“Epithelial cells are consistently exposed to bacteria, which play a key role in normal intestinal development and innate immunity.(4-11) The tight junctions (TJs) seal the space between adjacent epithelial cells.”
Background
Probiotic research priorities for the healthy adult population: A review on the health benefits of Lactobacillus rhamnosus GG and Bifidobacterium animalis subspecies lactis BB-12
Flach, J., van der Waal, M., Kardinaal, A., Schloesser, J., Ruijschop, R., & Claassen, E. (2018) · Cogent Food & Agriculture · doi:10.1080/23311932.2018.1452839 · Cited by 37
“Immune support Dysbacteriosis of the GI system is associated with several human diseases, including inflammatory bowel disease, colorectal cancer, and infections (Artis, 2008; Karin, Lawrence, & Nizet, 2006).”
Background
Effects of soy hull polysaccharide on dyslipidemia and pathoglycemia in rats induced by a high-fat-high-sucrose diet
Lin, Q., Yang, L., Han, L., Wang, Z., Luo, M., Zhu, D., Liu, H., Li, X., & Feng, Y. (2021) · Food Science and Human Wellness · doi:10.1016/j.fshw.2021.07.006 · Cited by 33
Oral Treatment with Extract of Agaricus blazei Murill Enhanced Th1 Response through Intestinal Epithelial Cells and Suppressed OVA‐Sensitized Allergy in Mice
Bouike, G., Nishitani, Y., Shiomi, H., Yoshida, M., Azuma, T., Hashimoto, T., Kanazawa, K., & Mizuno, M. (2010) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2011/532180 · Cited by 33
“As various immune cells are affected by IEC in the gut [39], we used a coculture system using splenocytes from OT-II mice, which possess CD4+ T cells that highly express the OVA-specific TCR, and Caco-2 cells for assessing the effects of ABME on the differentiation of T cells via IEC.”
Method
Altered profiles of fecal metabolites correlate with visceral hypersensitivity and may contribute to symptom severity of diarrhea-predominant irritable bowel syndrome
Zhang, W.-X., Zhang, Y., Qin, G., Li, K.-M., Wei, W., Li, S.-Y., & Yao, S.-K. (2019) · World Journal of Gastroenterology · doi:10.3748/wjg.v25.i43.6416 · Cited by 32
Glucomannan from Aloe vera Gel Promotes Intestinal Stem Cell-Mediated Epithelial Regeneration via the Wnt/β-Catenin Pathway
Zhang, D., Zhou, X., Liu, L., Guo, M., Huang, T., Zhou, W., Geng, F., Cui, S. W., & Nie, S. (2021) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c03814 · Cited by 32
Reactive Oxygen Species in Modulating Intestinal Stem Cell Dynamics and Function
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Toll-Like Receptor Stimulation Induces Nondefensin Protein Expression and Reverses Antibiotic-Induced Gut Defense Impairment
Wu, Y.-Y., Hsu, C.-M., Chen, P.-H., Fung, C.-P., & Chen, L.-W. (2014) · Infection and Immunity · doi:10.1128/iai.01578-14 · Cited by 32
“The intestinal tract acts as a major physical barrier between the microflora and internal host tissue and responds to the mucosal innate system through the commensal microflora (5).”
Background
Ecology impacts the decrease of Spirochaetes and Prevotella in the fecal gut microbiota of urban humans
Thingholm, L. B., Bang, C., Rühlemann, M. C., Starke, A., Sicks, F., Kaspari, V., Jandowsky, A., Frölich, K., Ismer, G., Bernhard, A., et al. (2021) · BMC Microbiology · doi:10.1186/s12866-021-02337-5 · Cited by 32
“Further, the gut microbiota is central for the maturation and functionality of the mammalian immune response [5–7].”
Research progress on the association between mastitis and gastrointestinal microbes in dairy cows and the effect of probiotics
Luo, S., Wang, Y., Kang, X., Liu, P., & Wang, G. (2022) · Microbial Pathogenesis · doi:10.1016/j.micpath.2022.105809 · Cited by 32

Authors: Artis, D.
Affiliations: University of Pennsylvania (US)
Corresponding author: Artis, David
ORCID: Artis, David
Venue: Nature reviews. Immunology
Publisher: Springer Science and Business Media LLC
Published: 2008-06
Volume: 8
Issue: 6
Pages: 411-420
ISSN: 1474-1733 (ISSN-L)
1474-1741
DOI: 10.1038/nri2316
OpenAlex: W2025114863
Cited by: 1,136
References: 167
Citations by year: 2026: 27 · 2025: 33 · 2024: 38 · 2023: 55 · 2022: 61 · 2021: 54 · 2020: 51 · 2019: 52 · 2018: 60 · 2017: 56 · 2016: 58 · 2015: 63 · 2014: 92 · 2013: 85 · 2012: 81
FWCI: 6.91
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: National Cancer Institute (T32CA009140, T32-CA09140-30)
National Institute of General Medical Sciences (F31-GM82187, F31GM082187)
National Institute of Allergy and Infectious Diseases (AI74878, T32AI007532, R01AI074878, F32-AI72943, F32AI072943, R01AI061570, AI 61570)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Keywords: intestinal epithelial cells, commensal bacteria, immune homeostasis, mucosal immunity, host-microbe interactions, epithelial barrier function, antigen presentation, lymphocytes, pathogen discrimination, gut microbiota
MeSH terms: Animals, Bacteria, Gastric Mucosa, Homeostasis, Humans, Intestinal Mucosa

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Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut

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