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Reciprocal interactions of the intestinal microbiota and immune system
Open accessAbstract
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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“This is of particular importance in intestinal tissues, which are enriched in both Th17 and Treg cells and are subject to ongoing antigenic stimulation from the intestinal microbiome (70).”
From T H 17 cells require ongoing classic IL-6 receptor signaling to retain transcriptional and functional identity (2020) · cites this paper as [70]
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“Ecological conditions vary immensely along both the length of the GI tract as well as in cross-section from lumen to the mucosal brush-border[173,267,308,309].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [308]
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“fermentum I5007 decreased the mRNA expression of the inflammatory cytokine IL-1β and increased the concentrations of butyrate [15], which help strengthen the intestinal barrier and defend against pathogenic microbes [18].”
BackgroundImmune Dysfunction in Uremia 2020
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“The human immune system is crucial in preserving homeostasis with the resident microbiota, whereas in return, resident microbial populations affect the human immune defense [156].”
BackgroundGhareeb, K., Awad, W. A., Böhm, J., & Zebeli, Q. (2014) · Journal of Applied Toxicology · doi:10.1002/jat.3083 · Cited by 170
“Effects of DON on the physical mucosal defence Production and secretions of mucous, antimicrobial peptides and mucosal IgA by activated B cells are important physical mucosal barriers that decrease the contact of luminal microbes or toxins with the intestinal epithelium (Maynard et al., 2012; Fig.”
BackgroundTang, Z.-Z., Chen, G., Hong, Q., Huang, S., Smith, H., Shah, R. D., Scholz, M. B., & Ferguson, J. F. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00454 · Cited by 175
“Microbiome composition is unique to an individual, is established early in life, and plays a crucial role in lifelong health (Kau et al., 2011; Minot et al., 2011; Maynard et al., 2012; Koren et al., 2013; Mohammadkhah et al., 2018).”
BackgroundMicrobiota and Mucosal Immunity in Amphibians
Colombo, B. M., Scalvenzi, T., Benlamara, S., & Pollet, N. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00111 · Cited by 171
Gut Microbiota and Celiac Disease
Marasco, G., Biase, A. R. D., Schiumerini, R., Eusebi, L. H., Iughetti, L., Ravaioli, F., Scaioli, E., Colecchia, A., & Festi, D. (2016) · Digestive Diseases and Sciences · doi:10.1007/s10620-015-4020-2 · Cited by 176
“study was to attempt to link immunity in CD to gut microbiota; as matter of fact, intestinal epithelial homeostasis is directly dependent on TLR activation which serves to balance the response against pathogens and the excessive inflammatory response [66, 67].”
BackgroundNSCLC Immunotherapy Efficacy and Antibiotic Use: A Systematic Review and Meta-Analysis
Lurienne, L., Cervesi, J., Duhalde, L., de Gunzburg, J., Andremont, A., Zalcman, G., Buffet, R., & Bandinelli, P.-A. (2020) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2020.03.002 · Cited by 174
Role of the intestinal microbiome in liver disease
Henao‐Mejia, J., Elinav, E., Thaiss, C. A., Licona-Limón, P., & Flavell, R. A. (2013) · Journal of Autoimmunity · doi:10.1016/j.jaut.2013.07.001 · Cited by 169
“In recent years, it has been widely demonstrated that the intestinal microbiota have critical functions in multiple aspects of mammalian physiology including regulation of body weight and related metabolic homeostasis, instruction of the immune system, and regulation of epithelial cell responses that are essential to…”
BackgroundMicrobiota-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 172
“There is a dynamic and complex interaction between the gut microbiota and the mucosal immune system (102).”
BackgroundLuo, A. S., Leach, S. T., Barrès, R., Hesson, L. B., Grimm, M., & Simar, D. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00417 · Cited by 173
The Impact of Gut Microbiota on Radiation-Induced Enteritis
Jian, Y., Zhang, D., Liu, M., Wang, Y., & Xu, Z. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.586392 · Cited by 170
Arabinoxylans, gut microbiota and immunity
Mendis, M., Leclerc, E., & Şimşek, Ş. (2015) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2015.11.068 · Cited by 172
Cremonini, E., Daveri, E., Mastaloudis, A., Adamo, A. M., Mills, D. A., Kalanetra, K. M., Hester, S. N., Wood, S. M., Fraga, C. G., & Oteiza, P. I. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101269 · Cited by 170
“These three components of intestinal physiology are interrelated: i) intestinal permeabilization can lead to the paracellular transport of endotoxins present in food or those generated by the luminal microbiota, which once in the circulation, can trigger systemic inflammatory responses [5,7,8]; ii) modifications in mi…”
BackgroundNicoletti, A., Ponziani, F. R., Biolato, M., Valenza, V., Marrone, G., Sganga, G., Gasbarrini, A., Miele, L., & Grieco, A. (2019) · World Journal of Gastroenterology · doi:10.3748/wjg.v25.i33.4814 · Cited by 174
Microbial Reprogramming Inhibits Western Diet-Associated Obesity
Poutahidis, T., Kleinewietfeld, M., Smillie, C., Levkovich, T., Perrotta, A., Bhela, S., Varian, B. J., Ibrahim, Y. M., Lakritz, J. R., Kearney, S. M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068596 · Cited by 164
“Furthermore, alterations in the composition of gut microbiota may affect not only gut health but also distant tissues and overall health and longevity via immune-mediated mechanisms [15–20].”
BackgroundGut microbiota, the pharmabiotics they produce and host health
Patterson, E., Cryan, J. F., Fitzgerald, G. F., Ross, R. P., Dinan, T. G., & Stanton, C. (2014) · Proceedings of The Nutrition Society · doi:10.1017/s0029665114001426 · Cited by 174
“A symbiotic relationship exists between the gut microbiota and host such that both partners benefit; the host provides protection and nutrients for the micro-organisms to flourish within((4)), whereas the microbiota contribute to food digestion, inhibit the growth of potential invading pathogens, convert harmful compo…”
BackgroundCiaula, A. D., Baj, J., Garruti, G., Celano, G., Angelis, M. D., Wang, H. H., Palo, D. M. D., Bonfrate, L., Wang, D. Q. ‐., & Portincasa, P. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9082648 · Cited by 166
Gut Microbiota in Colorectal Cancer: Biological Role and Therapeutic Opportunities
Pandey, H., Tang, D. W. T., Wong, S. H., & Lal, D. (2023) · Cancers · doi:10.3390/cancers15030866 · Cited by 171
“The composition of the gut microbiota influences individual variations in immunity [37–39] and is necessary for the development of the immune system [40,41].”
BackgroundGonzalez-Perez, G., Hicks, A. L., Tekieli, T. M., Radens, C. M., Williams, B. L., & Lamousé-Smith, E. S. N. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1502322 · Cited by 161
“and systemic immune tissues and immune cell populations (16, 17).”
BackgroundRobinson, C. M., & Pfeiffer, J. K. (2014) · Annual Review of Virology · doi:10.1146/annurev-virology-031413-085550 · Cited by 171
Wang, X., Xu, J., Zhao, X., Vasta, G. R., & Wang, J. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.552307 · Cited by 160
Cereal-derived arabinoxylans: Structural features and structure–activity correlations
Wang, J., Bai, J., Fan, M., Li, T., Li, Y., Qian, H., Wang, L., Zhang, H., Qi, X., & Rao, Z. (2019) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2019.12.016 · Cited by 169
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“The remarkable maturation process of the gastrointestinal physiology and immunology is likely to affect the microbiota; and vice versa, microbiota is likely to be involved in these maturation events (Maynard et al., 2012).”
BackgroundKeep calm: the intestinal barrier at the interface of peace and war
Thoo, L., Noti, M., & Krebs, P. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-2086-z · Cited by 168
Immune Regulation in Obesity-Associated Adipose Inflammation
Han, J. M., & Levings, M. K. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1301035 · Cited by 162
“Moreover, a HFD causes a robust change in the composition of gut microbiota (47, 48), which could have a major influence on immune cell function (49).”
BackgroundXia, T., Liu, C., Hu, Y., Luo, Z., Chen, F., Yuan, L., & Tan, X. (2021) · Food Research International · doi:10.1016/j.foodres.2021.110717 · Cited by 162
Inflammatory bowel disease, colorectal cancer and type 2 diabetes mellitus: The links
Jurjus, A. R., Eid, A., Kattar, S. A., Zeenny, M. N., Geagea, A. G., Haydar, H., Hilal, A., Oueidat, D., Matar, M., Tawilah, J., et al. (2015) · BBA Clinical · doi:10.1016/j.bbacli.2015.11.002 · Cited by 157
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“changes in immunity also determine intestinal microbiota composition (85, 89).”
BackgroundSordillo, J. E., Zhou, Y., McGeachie, M. J., Ziniti, J. P., Lange, N. E., Laranjo, N., Savage, J. R. K., Carey, V. J., O’Connor, G. T., Sandel, M. T., et al. (2016) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2016.08.045 · Cited by 159
“Resident microbes in the human gut discourage invasion by pathogens, process vital nutrients, and harvest energy otherwise inaccessible to human cells.(1,2) In addition to producing beneficial effects locally within the human gastrointestinal tract, commensal microbiota in the human gut provide, quantitatively, the mo…”
BackgroundBifidobacterium Abundance in Early Infancy and Vaccine Response at 2 Years of Age
Huda, M. N., Ahmad, S. M., Alam, J., Khanam, A., Kalanetra, K. M., Taft, D. H., Raqib, R., Underwood, M. A., Mills, D. A., & Stephensen, C. B. (2019) · PEDIATRICS · doi:10.1542/peds.2018-1489 · Cited by 157
Gut microbiota shapes cancer immunotherapy responses
Lei, W., Zhou, K., Lei, Y., Li, Q., & Zhu, H. (2025) · npj Biofilms and Microbiomes · doi:10.1038/s41522-025-00786-8 · Cited by 182
Symbiosis as a General Principle in Eukaryotic EvolutionPreprint
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“The gut microbiota of the mouse can also be altered by diet or mutation, especially of the mouse immune system and nutrient signaling, with correlated phenotypic lesions, especially in nutrient allocation and immune function (Maslowski and Mackay 2011; Claesson et al. 2012; Maynard et al. 2012).”
BackgroundHIV-induced alteration in gut microbiota
Lozupone, C., Rhodes, M. E., Neff, C. P., Fontenot, A. P., Campbell, T., & Palmer, B. E. (2014) · Gut Microbes · doi:10.4161/gmic.32132 · Cited by 157
“However, this view ignores the concept that adaptive immunity has the means to both promote and to temper innate immune responses programmed for microbial clearance.(20) Compositional change with HIV infection may also result from the loss of mutualistic bacteria that depend on interaction with the adaptive immune sys…”
BackgroundGough, E. K., Moodie, E. E. M., Prendergast, A. J., Johnson, S. M. A., Humphrey, J. H., Stoltzfus, R. J., Walker, A. S., Trehan, I., Gibb, D. M., Goto, R., et al. (2014) · BMJ · doi:10.1136/bmj.g2267 · Cited by 153
Metadata
- 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.
- Venue
- Nature
- Published
- 2012-09
- Volume
- 489
- Issue
- 7415
- Pages
- 231-241
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- 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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