Cited by 1,598Gut microbiota and healthT-cell and B-cell ImmunologyImmune Response and Inflammation

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Reciprocal interactions of the intestinal microbiota and immune system

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Maynard, Craig L., Elson, Charles O., Hatton, Robin D., Weaver, Casey T.·2012·Nature

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Abstract

The emergence of the adaptive immune system in vertebrates set the stage for evolution of an advanced symbiotic relationship with the intestinal microbiota. The defining features of specificity and memory that characterize adaptive immunity have afforded vertebrates the mechanisms for efficiently tailoring immune responses to diverse types of microbes, whether to promote mutualism or host defence. These same attributes can put the host at risk of immune-mediated diseases that are increasingly linked to the intestinal microbiota. Understanding how the adaptive immune system copes with the remarkable number and diversity of microbes that colonize the digestive tract, and how the system integrates with more primitive innate immune mechanisms to maintain immune homeostasis, holds considerable promise for new approaches to modulate immune networks to treat and prevent disease.

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Method
Pinto beans modulate the gut microbiome, augment MHC II protein, and antimicrobial peptide gene expression in mice fed a normal or western-style diet
Ojo, B. A., Lu, P., Alake, S. E., Keirns, B. H., Anderson, K. L., Gallucci, G., Hart, M. D., El-Rassi, G. D., Ritchey, J. W., Chowanadisai, W., et al. (2020) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2020.108543 · Cited by 22
Effects of IQW and IRW on Inflammation and Gut Microbiota in ETEC‐Induced Diarrhea
Liu, N., Zhou, L., Fang, J. Q., Jiang, H., & Liu, G. (2021) · Mediators of Inflammation · doi:10.1155/2021/2752265 · Cited by 23
“The intestinal tract is a dynamic and complex system; the intestinal microenvironment is the coexistent result of host and microbiota [22, 23].”
Microbes with higher metabolic independence are enriched in human gut microbiomes under stress
Veseli, I., Chen, Y. T., Schechter, M. S., Vanni, C., Fogarty, E. C., Watson, A. R., Jabrì, B., Blekhman, R., Willis, A. D., Yu, M., et al. (2025) · eLife · doi:10.1101/2023.05.10.540289 · Cited by 29
“…after birth and plays a lifelong role in human wellbeing by contributing to immune system maturation and functioning (Belkaid and Hand 2014; Maynard et al. 2012), extracting dietary nutrients (Hijova 2019), providing protection against pathogens (Khosravi and Mazmanian 2013), metabolizing…”
Gut-Brain Axis Deregulation and Its Possible Contribution to Neurodegenerative Disorders
Villavicencio-Tejo, F., Olesen, M. A., Navarro, L., Calisto, N., Iribarren, C., GARCÍA, K. P., Corsini, G., & Quintanilla, R. A. (2023) · Neurotoxicity Research · doi:10.1007/s12640-023-00681-0 · Cited by 24
“(Maynard et al. 2012).”
Fecal microbiota transplantation for treatment of non-alcoholic fatty liver disease: Mechanism, clinical evidence, and prospect
Qiu, X., Cheng, S., Liu, Y., Li, Y. L., Zhang, R., Li, N., & Li, Z. (2024) · World Journal of Gastroenterology · doi:10.3748/wjg.v30.i8.833 · Cited by 24
“With the aid of this indirect mediation, the gut microbiota participate in nutrient digestion and absorption, host metabolism, and mucosal and systemic immunity[25].”
The Effects ofBifidobacterium breveon Immune Mediators and Proteome of HT29 Cells Monolayers
Sánchez, B., González-Rodríguez, I., Arboleya, S., López, P., Suárez, A., Ruas‐Madiedo, P., Margollés, A., & Gueimonde, M. (2015) · BioMed Research International · doi:10.1155/2015/479140 · Cited by 23
“The interest in the immunomodulatory properties of probiotic bacteria derives from the observations that intestinal microbiota plays a critical role in the development and regulation of the immune system [6].”
Can intestinal microbiota be associated with non-intestinal cancers?
Jacqueline, C. M., Brazier, L., Faugère, D., Renaud, F., Frédéric Thomas, A., & Roche, B. (2017) · Scientific Reports · doi:10.1038/s41598-017-11644-9 · Cited by 23
Development and biochemical and immunological characterization of early passage and immortalized bovine intestinal epithelial cell lines from the ileum of a young calf
Katwal, P., Thomas, M., Uprety, T., Hildreth, M. B., & Kaushik, R. S. (2019) · Cytotechnology · doi:10.1007/s10616-018-0272-y · Cited by 23
“The BIEC-c4 cells could be tested in further studies for the expression level of tight junction proteins (Anderson and Van Itallie 1995; Chaudhary et al. 2018; McNeil et al. 2006; Miyazawa et al. 2010).”
Nutritionists’ Health Study cohort: a web-based approach of life events, habits and health outcomes
Folchetti, L. G. D., da Silva, I. T., de Almeida-Pititto, B., & Ferreira, S. R. G. (2016) · BMJ Open · doi:10.1136/bmjopen-2016-012081 · Cited by 24
“gering mechanisms that favour body fat accumulation and insulin resistance in adult life.(45) Associations of events during intrauterine life or at delivery with gut”
Background
Duodenal CD8+ T resident memory cell apoptosis contributes to gut barrier dysfunction and microbial translocation in early alcohol‐associated liver disease in humans
Maccioni, L., Loriot, A., Dewulf, J., Bommer, G., Horsmans, Y., Lanthier, N., Leclercq, I., Schnabl, B., & Stärkel, P. (2022) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.17177 · Cited by 23
Gut barrier-microbiota imbalances in early life lead to higher sensitivity to inflammation in a murine model of C-section delivery
Barone, M., Ramayo‐Caldas, Y., Estellé, J., Tambosco, K., Chadi, S., Maillard, F., Gallopin, M., Planchais, J., Chain, F., Kropp, C., et al. (2023) · Microbiome · doi:10.1186/s40168-023-01584-0 · Cited by 22
“Since these children have an altered bacterial community, it has been hypothesized that these alterations lead to differences in mucosal immune tolerance and disease risk in later life [28, 29].”
Background
Dietary Influence on the Dynamics of the Human Gut Microbiome: Prospective Implications in Interventional Therapies
Adithya, K. K., Rajeev, R., Selvin, J., & Kiran, G. S. (2021) · ACS Food Science & Technology · doi:10.1021/acsfoodscitech.0c00075 · Cited by 23
The intestinal microbiota: Towards a multifactorial integrative model. Eubiosis and dysbiosis in morbid physical and psychological conditions
Giulio, P. (2021) · Archives of Clinical Gastroenterology · doi:10.17352/2455-2283.000094 · Cited by 24
The Mediating Role of the Gut Microbiota in the Physical Growth of Children
Durda, M., Ciomborowska-Basheer, J., Makałowska, I., & Szwed, A. (2022) · Life · doi:10.3390/life12020152 · Cited by 23
Epithelial Barrier: Protector and Trigger of Allergic Disorders
Izquierdo, E., Rodríguez‐Coira, J., Dolset, M. I. D., Gómez‐Casado, C., Barber, D., & Escribese, M. M. (2022) · Journal of Investigational Allergology and Clinical Immunology · doi:10.18176/jiaci.0779 · Cited by 24
“Under homeostatic conditions, interaction with microbiota induces transforming growth factor-β (TGF-β), retinoic acid, and thymic stromal lymphopoietin (TSLP), which promote tolerogenic APCs and, together with IL-10, the induction of regulatory T cells (Tregs) [39,40].”
Background
Impact of the Microbiota on Viral Infections
Campbell, D. E., Li, Y., Ingle, H., & Baldridge, M. T. (2023) · Annual Review of Virology · doi:10.1146/annurev-virology-111821-115754 · Cited by 22
Role of the mechanisms for antibody repertoire diversification in monoclonal light chain deposition disorders: when a friend becomes foe
del Pozo‐Yauner, L., Herrera, G. A., Pérez‐Carreón, J. I., Turbat‐Herrera, E. A., Rodríguez, F. J. Á., & Ruiz-Zamora, R. A. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1203425 · Cited by 23
“While both the multicellular host and its microbiota benefited from the reciprocal interaction (3, 4), the former must avoid succumbing due to the uncontrolled invasion of the later (1, 2).”
Background
Lactobacillus johnsonii N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitis
Yuan, L., Zhu, C., Gu, F., Zhu, M., Yao, J., Zhu, C., Li, S., Wang, K., Hu, P., Zhang, Y., et al. (2023) · Animal nutrition · doi:10.1016/j.aninu.2023.04.012 · Cited by 26
A Single Host-Derived Glycan Impacts Key Regulatory Nodes of Symbiont Metabolism in a Coevolved Mutualism
Pan, M., Schwartzman, J. A., Dunn, A. K., Lu, Z., & Ruby, E. G. (2015) · mBio · doi:10.1128/mbio.00811-15 · Cited by 22
“Metabolic coordination between partners is a central factor in the evolution of beneficial symbiotic associations (1–3); in particular, the provision of nutrients by the symbiont and/or host can drive coevolution, codevelopment, and ecological scaffolding in the symbiosis (2, 3).”
Background
The Gut Microbiota Reduces Colonization of the Mesenteric Lymph Nodes and IL-12-Independent IFN-γ Production During Salmonella Infection
Fernández-Santoscoy, M., Wenzel, U. A., Yrlid, U., Cardell, S., Bäckhed, F., & Wick, M. J. (2015) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2015.00093 · Cited by 22
“…functions (Tremaroli and Bäckhed, 2012; Karlsson et al., 2013; Wichmann et al., 2013), stimulating the intestinal and systemic immune compartments (Talham et al., 1999; Mazmanian et al., 2005) and maintaining mucosal homeostasis (Atarashi et al., 2008; Ivanov et al., 2009; Maynard et al., 2012).”
BackgroundInfluential
A 52-week safety study in cynomolgus macaques for genetically modified rice expressing Cry1Ab/1Ac protein
Mao, J., Sun, X., Cheng, J., Shi, Y.-J., Wang, X., Qin, J.-J., Sang, Z., He, K., & Xia, Q. (2016) · Food and Chemical Toxicology · doi:10.1016/j.fct.2016.06.015 · Cited by 22
“Disruptions in intestinal microbiota composition have been linked to various disorders, such as inflammation, obesity and aging (Ley et al., 2006; Maynard et al., 2012).”
Background
Effects of parental care on resource allocation into immune defense and buccal microbiota in mouthbrooding cichlid fishes*
Keller, I. S., Bayer, T., Salzburger, W., & Roth, O. (2018) · Evolution · doi:10.1111/evo.13452 · Cited by 22
[Correlation between gut microbiota and behavior symptoms in children with autism spectrum disorder].
Zhao, R.-H., Zheng, P., Liu, S., Tang, Y., Li, E.-Y., Sun, Z., & Jiang, M. (2019) · PubMed Central · doi:10.7499/j.issn.1008-8830.2019.07.009 · Cited by 22
“6/1 000 ([3])。该病目前尚无高效的治疗方法,因此 ASD患者及其家庭面临了沉重的精神和经济负担。 ASD 的病因尚不明确,多数研究者认为基因与环境因素的相互作用影响 ASD 的发生发展。研究报道过某些产前及新生儿危险因素可能与ASD相关, 如产前抗生素使用、生产方式和新生儿早期抗生素使用等 ([4])。近年来,大量研究发现肠道微生态在新生儿免疫系统和内分泌系统的发育成熟中发挥着重要作用 ([5])。肠道微生物稳态的打破与多种疾病的发生和发展密切相关,包括 ASD,婴儿坏死性小肠结肠炎等 ([6])。肠道微生态通过神经、免疫、内分泌和代谢途径影响肠道和中枢神经系统,这种复杂的交互作用被称作微生态 -…”
Background
The Microbiota/Microbiome and the Gut–Brain Axis: How Much Do They Matter in Psychiatry?
Marazziti, D., Buccianelli, B., Palermo, S., Parra, E., Arone, A., Beatino, M. F., Massa, L., Carpita, B., Barberi, F. M., Mucci, F., et al. (2021) · Life · doi:10.3390/life11080760 · Cited by 23
Effect of diet on the evolution of gut commensal bacteria
Đapa, T., & Xavier, K. B. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2369337 · Cited by 23
“20,27 Twelve-month-old infants who continue to be breastfed while consuming solid food have a more immature microbiota composition than infants who cease receiving breast milk, and the latter have a faster transition to an adult-like composition.”
Background
Linalool as a key component in strawberry volatile organic compounds (VOCs) modulates gut microbiota, systemic inflammation, and glucolipid metabolism
Tan, N., Zhao, M., Luo, Z., Li, Z., Zhang, X., Xu, J., Gu, X., Wang, Q., Ding, S., Ying, M., et al. (2024) · Food Chemistry · doi:10.1016/j.foodchem.2024.140361 · Cited by 21
Harnessing the human gut microbiota: an emerging frontier in combatting multidrug-resistant bacteria
Ding, W., Cheng, Y., Liu, X., Zhu, Z., Wu, L., Gao, J., Lei, W., Li, Y., Zhou, X., Wu, J., et al. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1563450 · Cited by 26
“These receptors trigger the release of antimicrobial peptides, cytokines, and chemokines, initiating in ﬂ ammatory responses to combat infections (116, 117).”
Intermittent fasting modulates IgA levels in the small intestine under intense stress: A mouse model
Lara‐Padilla, E., Godínez‐Victoria, M., Drago-Serrano, M. E., Reyna-Garfias, H., Arciniega-Martínez, I. M., Abarca‐Rojano, E., Cruz-Hernández, T. R., & Campos‐Rodríguez, R. (2015) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2015.05.013 · Cited by 21
“Differences in the parameters assessed are expected owing to the structural, neuroendocrine, immunological and physiological regionalization along the intestinal tract (Ke et al., 2011; Maynard et al., 2012; Mowat and Agace, 2014).”
Background
Protective Effect of Low Molecular Weight Seleno-Aminopolysaccharide on the Intestinal Mucosal Oxidative Damage
Wen, Z., Tang, Z., Ma, L., Zhu, T.-L., Wang, Y., Xiang, X., & Zheng, B. (2019) · Marine Drugs · doi:10.3390/md17010064 · Cited by 20
“Under normal physiological conditions, the intestine is not only an important barrier that prevents harmful substances (bacteria and toxins) from invading the body, but also an important organ that regulates the stress response of the body and produces inflammatory mediators [18,19].”
Background
The effect of maternal antibiotic use in sows on intestinal development in offspring
de Greeff, A., Schokker, D., den Hil, P. J. R.-V., Ramaekers, P., Vastenhouw, S. A., Harders, F., Bossers, A., Smits, M. A., & Rebel, J. M. J. (2020) · Journal of Animal Science · doi:10.1093/jas/skaa181 · Cited by 23
Effects of Rhodotorula mucilaginosa on the Immune Function and Gut Microbiota of Mice
Ge, Y., Huang, K., WeiTian, X., Chun-hou, X., Yao, Q., & Liu, Y. (2021) · Frontiers in Fungal Biology · doi:10.3389/ffunb.2021.705696 · Cited by 21
Infection with the enteric pathogen C. rodentium promotes islet-specific autoimmunity by activating a lymphatic route from the gut to pancreatic lymph node
Pöysti, S., Toivonen, R. K., Takeda, A., Silojärvi, S., Yatkin, E., Miyasaka, M., & Hänninen, A. L. M. (2022) · Mucosal Immunology · doi:10.1038/s41385-022-00490-2 · Cited by 21
The Neuroprotective Effects of Spray-Dried Porcine Plasma Supplementation Involve the Microbiota−Gut−Brain Axis
Rosell‐Cardona, C., Amat, C., Griñán‐Ferré, C., Polo, J., Pallàs, M., Pérez‐Bosque, A., Moretó, M., & Miró, L. (2022) · Nutrients · doi:10.3390/nu14112211 · Cited by 22
“This type of microbial alteration, which is called dysbiosis, is associated with many intestinal diseases, such as inflammatory bowel disease and irritable bowel syndrome, but is also linked to extraintestinal inflammatory diseases such as asthma and obesity [7], as well as neurodegenerative diseases such as Parkinson…”
Background
Nutritional Support in Acute Liver Failure
Abenavoli, L., Maurizi, V., Boccuto, L., Berardino, A. D., Giostra, N., Santori, P., Scarcella, M., Procopio, A. C., Rasetti, C., & Scarpellini, E. (2022) · Diseases · doi:10.3390/diseases10040108 · Cited by 23
The Impact of Microbiota–Immunity–Hormone Interactions on Autoimmune Diseases and Infection
Martinelli, S., Nannini, G., Cianchi, F., Coratti, F., & Amedei, A. (2024) · Biomedicines · doi:10.3390/biomedicines12030616 · Cited by 22
“It is now clearly recognized that GM is active and functional, exerting effects locally and over long distances with the ability to modulate metabolic and immunological messengers as well as hormone circulating levels, particularly E2 in women [208,209].”
Functional Plasticity of Th17 Cells: Implications in Gastrointestinal Tract Function
Garrido‐Mesa, N., Algieri, F., Rodríguez‐Nogales, A., & Gálvez, J. (2013) · International Reviews of Immunology · doi:10.3109/08830185.2013.834899 · Cited by 22
“However, at low doses, TGFβ cooperates with the pro-inflammatory cytokine IL-6 to overcome Foxp3-mediated repression of RORγ t and shift the promotion of iTreg in favor of Th17, thus providing a mechanism to combine immune homeostasis or pathogen clearance to extracellular bacteria at mucosal barrier locations, such a…”
Background
Gnotobiotic mouse model’s contribution to understanding host–pathogen interactions
Kubelková, K., Benuchova, M., Kozáková, H., Šinkora, M., Kročová, Z., Pejchal, J., & Macela, A. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2341-8 · Cited by 22
“crobial peptides, and contribute to neutrophil recruitment [81, 82].”
Background
A role for the microbiome in mother–infant interaction and perinatal depression
Sanders, A., Rackers, H., & Kimmel, M. (2019) · International Review of Psychiatry · doi:10.1080/09540261.2018.1548431 · Cited by 21
Gut Microbiota and Intestinal Epithelial Myd88 Signaling Are Crucial for Renal Injury in UUO Mice
Watanabe, I. K. M., Andrade-Silva, M., Foresto‐Neto, O., Felizardo, R. J. F., Matheus, M. A. C., Silva, R. C., Cenedeze, M. A., Honda, T. S. B., Perandini, L. A., Volpini, R. A., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.578623 · Cited by 19
“Several studies, especially using germ-free mice, demonstrated the importance of microbiota and host interactions in priming immunity (19, 41, 42), which could have deleterious effects in inflammatory states, such as kidney injury.”
Background
Fermented Soy and Fish Protein Dietary Sources Shape Ileal and Colonic Microbiota, Improving Nutrient Digestibility and Host Health in a Piglet Model
Li, Y., Han, Y., Zhao, Q., Tang, C., Zhang, J., & Qin, Y. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.911500 · Cited by 22
“In a previous report on children, microbial diversification was a gradual process, whereas the premature formation of an adult-type microbiota negatively affected host immune function (Maynard et al., 2012; Nylund et al., 2013).”
Background
Gut Mucosal and Fecal Microbiota Profiling Combined to Intestinal Immune System in Neonates Affected by Intestinal Ischemic Injuries
Romani, L., CHIERICO, F. D., Chiriaco, M., Foligno, S., Reddel, S., Salvatori, G., Cifaldi, C., Faraci, S., Finocchi, A., Rossi, P., et al. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00059 · Cited by 21
“In spite of these considerations, the comprehension of the mutual relationship between the intestinal IS and the microbiome in neonatal intestinal ischemic injuries is still unclear (Maynard et al., 2012; Engstrand Lilja et al., 2015).”
Background

Authors: Maynard, C. L., Elson, C. O., Hatton, R. D., & Weaver, C. T.
Affiliations: University of Alabama at Birmingham (US)
Corresponding author: Weaver, Casey T.
ORCID: Maynard, Craig L.
Elson, Charles O.
Hatton, Robin D.
Weaver, Casey T.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2012-09
Volume: 489
Issue: 7415
Pages: 231-241
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature11551
PMC: PMC4492337
OpenAlex: W2083102356
Cited by: 1,598
References: 101
Citations by year: 2026: 50 · 2025: 81 · 2024: 122 · 2023: 136 · 2022: 126 · 2021: 143 · 2020: 148 · 2019: 122 · 2018: 120 · 2017: 100 · 2016: 118 · 2015: 120 · 2014: 110 · 2013: 96 · 2012: 4
FWCI: 9.63
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Crohn's and Colitis Foundation
National Institute of Allergy and Infectious Diseases (R01AI057956, T32AI007051)
National Institute of Diabetes and Digestive and Kidney Diseases (R24DK064400, P01DK071176, R01DK093015)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords: gut microbiota, adaptive immunity, innate immunity, host-microbe symbiosis, immune homeostasis, immune-mediated diseases, immunological memory, gut microbiota modulation, host defense
MeSH terms: Blood Group Antigens, Cesarean Section, Epithelium, Female, Homeostasis, Humans, Infant, Infant, Newborn, Intestines, Pregnancy, T-Lymphocytes, Vagina, Metagenome

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Reciprocal interactions of the intestinal microbiota and immune system

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