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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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“Studies on gut microbiomes of vertebrates provide compelling evidence that the adaptive immune system co-evolves with intestinal microbiota to foster maintenance of beneficial species at the expense of detrimental strains (Maynard et al. 2012).”
BackgroundMukherjee, K., Raju, R., Fischer, R., & Vilcinskas, A. (2013) · Advances in biochemical engineering, biotechnology · doi:10.1007/10_2013_203 · Cited by 44
“The complex interplay between gut microbiota and the intestinal immune system has coevolved and confers mutual benefits on both the microbiota and host; thus, its disruption can increase the risk of immune-related diseases [1, 2].”
BackgroundIntestinal innate immune cells in gut homeostasis and immunosurveillance
Tomasello, E., & Bedoui, S. (2013) · Immunology and Cell Biology · doi:10.1038/icb.2012.85 · Cited by 41
The Microbial Composition of Penaeid Shrimps’ Hepatopancreas Is Modulated by Hemocyanin
Zheng, Z., Aweya, J. J., Bao, S., Yao, D., Li, S., Tran, N. T., Ma, H., & Zhang, Y. (2021) · The Journal of Immunology · doi:10.4049/jimmunol.2100746 · Cited by 42
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Gut microbiota, microbiota‐derived metabolites, and graft‐versus‐host disease
Yue, X., Zhou, H., Wang, S., Chen, X., & Xiao, H. (2024) · Cancer Medicine · doi:10.1002/cam4.6799 · Cited by 45
“13 | GUT MICROBIOTA-RELATED”
Kaetzel, C. S. (2014) · ISRN Immunology · doi:10.1155/2014/541537 · Cited by 40
“Microbial colonization of newborn vertebrates stimulates development of mucosal B cells and class switching to mucosal Ig isotypes [1, 163].”
BackgroundInfluentialJacques, P. F., & Wang, H. (2014) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.073031 · Cited by 43
“It is believed that the bacteria in probiotic yogurt can enhance the growth of beneficial intestinal microbiota and influence gut function and distant tissues through regulation of the immune system (36); such effects may result in weight loss or in prevention of weight gain.”
BackgroundRemote control — triggering of brain autoimmune disease in the gut
Wekerle, H., Berer, K., & Krishnamoorthy, G. (2013) · Current Opinion in Immunology · doi:10.1016/j.coi.2013.09.009 · Cited by 39
The microbiota as a component of the celiac disease and non-celiac gluten sensitivity
Nylund, L., Kaukinen, K., & Lindfors, K. (2016) · Clinical Nutrition Experimental · doi:10.1016/j.yclnex.2016.01.002 · Cited by 41
“In addition, the presence of commensal microbes is needed for the induction of the endogenous production of IgA, which is slowly started while the immune system develops [24].”
BackgroundAndrés, J. D., Manzano, S., García, C. I. M., Rodríguez, J. M., Espinosa‐Martos, I., & Jiménez, E. (2018) · Beneficial Microbes · doi:10.3920/bm2017.0132 · Cited by 40
“However, at present, little is known about the direct effect of bacterial colonisation on the maturation of the immune system in infants (Hatakka et al. , 2001; Johansson et al. , 2012; Maynard et al. , 2012).”
Diversity and antimicrobial potential in sea anemone and holothurian microbiomes
León‐Palmero, E., Joglar, V., Álvarez, P. A., Martín-Platero, A. M., Llamas, I., & Reche, I. (2018) · PLoS ONE · doi:10.1371/journal.pone.0196178 · Cited by 41
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Li, K., Wu, J., Xu, S., Li, X., Zhang, Y., & Gao, X. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.01914-23 · Cited by 40
“Appropriate intestinal colonization stimulates maturation of lymphoid tissue associated with the intestinal mucosa by specific microbial communi ties during host primordial stages (19).”
BackgroundDeciphering the crosstalk among IL-1 and IL-10 family cytokines in intestinal immunity
Manzanillo, P. S., Eidenschenk, C., & Ouyang, W. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.06.003 · Cited by 44
Immunogenetic Pathogenesis of Celiac Disease and Non-celiac Gluten Sensitivity
Escudero‐Hernández, C., Peña, A. S., & Bernardo, D. (2016) · Current Gastroenterology Reports · doi:10.1007/s11894-016-0512-2 · Cited by 41
Human microbiome and prostate cancer development: current insights into the prevention and treatment
Moghadam, S. O., & Momeni, S. A. (2020) · Frontiers of Medicine · doi:10.1007/s11684-019-0731-7 · Cited by 41
Immune System Modulations by Products of the Gut Microbiota
Chénard, T., Prévost, K., Dubé, J., & Massé, É. (2020) · Vaccines · doi:10.3390/vaccines8030461 · Cited by 43
“All PRRs are able to recognize molecular patterns invading pathogens and self-components, but each family is specialized in recognition of patterns from specific groups.”
BackgroundInfluentialCao, X.-T., Pan, X.-Y., Sun, M., Liu, Y., & Lan, J.-F. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.679767 · Cited by 39
Yeast Modulation of Human Dendritic Cell Cytokine Secretion: An In Vitro Study
Smith, I. M., Christensen, J. E., Arneborg, N., & Jespersen, L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096595 · Cited by 40
“At homeostasis, DCs in the intestinal mucosa are conditioned by commensal microorganisms to promote proliferation of Foxp3 regulatory T cells (Tregs), strong producers of anti-inflammatory IL-10 contributing to intestinal tolerance [1,3,4].”
Satokari, R. M. (2014) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365521.2014.966320 · Cited by 39
“Immunological homeostasis of the mucosa is based on the coordinated actions of epithelial cells and innate and adaptive immune systems [21,82,83].”
BackgroundInfluentialBatista, S., Medina, A., Pires, M. A., Moríñigo, M. Á., Sansuwan, K., Fernandes, J. M. O., Valente, L. M. P., & Ozório, R. O. A. (2016) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-016-7592-7 · Cited by 39
“Intestinal epithelium is covered by a layer of mucus continuously produced by goblet cells and being the first line of defence against microbes (Maynard et al. 2012).”
InfluentialStudy of the Anti-Inflammatory Mechanism of β-Carotene Based on Network Pharmacology
Wu, S., Chen, R., Chen, J., Yang, N., Li, K., Zhang, Z., & Zhang, R. (2023) · Molecules · doi:10.3390/molecules28227540 · Cited by 38
“This process leads to the activation and recruitment of white blood cells to the damaged sites for further treatment [1,2].”
BackgroundGut microbiota and its therapeutic implications in tumor microenvironment interactions
Feng, P., Xue, X., Bukhari, I., Qiu, C., Li, Y., Zheng, P., & Mi, Y. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1287077 · Cited by 39
“The human gut microbiota is recognized as a fundamental component of the immune system (Hooper and Macpherson, 2010; Maynard et al., 2012).”
BackgroundSevere viral respiratory infections: are bugs bugging?
Vissers, M., de Groot, R., & Ferwerda, G. (2013) · Mucosal Immunology · doi:10.1038/mi.2013.93 · Cited by 39
Kainulainen, V., Reunanen, J., Hiippala, K., Guglielmetti, S., Vesterlund, S., Palva, A., & Satokari, R. M. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.01993-13 · Cited by 39
“Furthermore, adhering commensals and probiotics have close contact with the host epithelium and are proposed to function in immune stimulation and gut maturation and to enhance epithelial integrity (2, 4, 5).”
BackgroundInfluence of the microbiome on response to vaccination
Jamieson, A. M. (2015) · Human Vaccines & Immunotherapeutics · doi:10.1080/21645515.2015.1022699 · Cited by 37
“Even if the microbiome is disrupted transiently it will repopulate itself largely as it was initially established.(14,24) The immune response and the mcirobiome develop in concert during these first few months.”
BackgroundYacoubi, N., Saulnier, L., Bonnin, E., Devillard, E., Eeckhaut, V., Rhayat, L., Ducatelle, R., & Immerseel, F. V. (2017) · Poultry Science · doi:10.3382/ps/pex297 · Cited by 37
“It induces IgA secreting B-cells and steers the development of the T-cell repertoire (Maynard et al., 2012; Ericsson et al., 2014).”
BackgroundDaillère, R., Derosa, L., Bonvalet, M., Segata, N., Routy, B., Gariboldi, M., Budínská, E., de Vries, I. J. M., Naccarati, A., Zitvogel, V., et al. (2020) · OncoImmunology · doi:10.1080/2162402x.2020.1774298 · Cited by 41
Scarpellini, E., Fagoonee, S., Rinninella, E., Rasetti, C., Aquila, I., Larussa, T., Ricci, P., Luzza, F., & Abenavoli, L. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9082488 · Cited by 39
“, carbohydrates absorption and processing, proteins putrefaction, bile acids formation, insulin sensitivity) and last but not least, modulation of intestinal and systemic immunity, thus maintaining antigen tolerance and avoiding pathogen expansion [16].”
BackgroundHong, T., Wang, R., Wang, X., Yang, S., Wang, W., Gao, Q., & Zhang, X. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.644982 · Cited by 38
“The intestinal microbiota has been proven to be critical for maintaining healthy tissues and stimulating immunity (14), and increasing evidence has revealed that dysbiosis in intestinal microbial populations is linked to human disease and defects in immunity (15–18).”
BackgroundWestern-style diet impedes colonization and clearance of Citrobacter rodentium
An, J., Zhao, X., Wang, Y., Noriega, J., Gewirtz, A. T., & Zou, J. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009497 · Cited by 39
Gao, J., Cao, B., Zhao, R., Li, H., Xu, Q., & Wei, B. (2023) · Pharmaceuticals · doi:10.3390/ph16091216 · Cited by 40
“They promote the development and maturation of immune organs, improve specific and nonspecific immune functions, and have strong broad-spectrum antibacterial effects [57,58].”
BackgroundSkoufou, M., Tsigalou, C., Vradelis, S., & Bezirtzoglou, E. (2024) · Microorganisms · doi:10.3390/microorganisms12010194 · Cited by 41
“Several studies have highlighted the significance of probiotics that influence intestinal homeostasis such as intestinal barrier function through Tight Junction (TJ) complex regulation [43].”
BackgroundThe Gut Microbiota Composition in Dichorionic Triplet Sets Suggests a Role for Host Genetic Factors
Murphy, K., Shea, C.-A. O. ’., Ryan, C. A., Dempsey, E. M., O’Toole, P. W., Stanton, C., & Ross, R. P. (2015) · PLoS ONE · doi:10.1371/journal.pone.0122561 · Cited by 40
“The gut microbiota have been shown to play important roles in the development and maturation of the immune system, metabolic pathways and in the bi-directional communication between the GI tract and the central nervous system (CNS), the so called gut-brain axis [1–5].”
Manipulation of the glycan‐specific natural antibody repertoire for immunotherapy
New, J. S., King, R. G., & Kearney, J. F. (2016) · Immunological Reviews · doi:10.1111/imr.12397 · Cited by 37
“and Bacteroides species scavenge and incorporate host-derived carbohydrate residues into their capsular polysaccharides and glycoproteins (133).”
Background
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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