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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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“…bacterial populations in response to IL-15, as differences between the bacterial communities of the small and large bowel have been shown to parallel not only marked differences in IECs (Campbell et al., 1994) but various immune cell populations as well (Abadie et al., 2012; Maynard et al., 2012).”
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“…mucosa as well, CD8+ T cells, cd T cells, natural killer (NK) cells and innate lymphoid cells are also important producers of Th17 cytokines (Maynard et al. 2012); therefore, not only Th17 cells, but also other constellation of innate and adaptive sources of IL-17A, IL-17F and IL-22 are…”
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BackgroundThe Colon: An Overlooked Site for Therapeutics in Dialysis Patients
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“It consists of mesenteric lymph nodes, Peyer’s patches, lymphocytes located in the intestinal lamina propria and large numbers of IgA plasmablasts located in the epithelium [28-30].”
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Chitin-based barrier immunity and its loss predated mucus-colonization by indigenous gut microbiota
Nakashima, K., Kimura, S., Ogawa, Y., Watanabe, S., Soma, S., Kaneko, T., Yamada, L., Sawada, H., Tung, C., Lu, T.-M., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05884-0 · Cited by 77
Developmental responses to early‐life adversity: Evolutionary and mechanistic perspectives
Lu, A., Petrullo, L. A., Carrera, S. C., Feder, J. A., Schneider‐Crease, I. A., & Snyder‐Mackler, N. (2019) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.21791 · Cited by 78
“microbes can result in the selective seeding of certain maternal microbial strains over others.(155,156) Thus, despite the magnitude of mater-”
BackgroundWang, J., Jaramillo-Torres, A., Li, Y., Kortner, T. M., Gajardo, K., Brevik, Ø. J., Jakobsen, J. V., & Krogdahl, Å. (2021) · Animal Microbiome · doi:10.1186/s42523-021-00075-7 · Cited by 78
“intestinal barrier and immune functions, and could thereby regulate metabolic functions [78].”
BackgroundRole of cesarean section in the development of neonatal gut microbiota: A systematic review
Shaterian, N., Abdi, F., Ghavidel, N., & Alidost, F. (2021) · Open Medicine · doi:10.1515/med-2021-0270 · Cited by 85
“The neonatal immune system will rapidly mature due to the influence of microbiota, diet, exposure to new microbes, and other environmental exposures [56,69].”
BackgroundThe chemistry of negotiation: Rhythmic, glycan-driven acidification in a symbiotic conversation
Schwartzman, J. A., Koch, E. J., Heath-Heckman, E., Zhou, L. H., Kremer, N., McFall‐Ngai, M., & Ruby, E. G. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1418580112 · Cited by 76
“Squid were colonized and raised as described previously (7, 8), with the following modifications: Animals were exposed to ∼5,000 colony-forming units (cfu)/mL of the indicated V.”
MethodTang, M. S., Poles, J., Leung, J. M., Wolff, M. J., Davenport, M., Lee, S. C., Lim, Y. A. L., Chua, K. H., Loke, P., & Cho, I. (2015) · Gut Microbes · doi:10.1080/19490976.2014.1000080 · Cited by 76
“Lower microbial diversity at the intestinal mucosa is expected since this is an environment specialized to prevent their translocation across the epithelial barrier, with goblet cells secreting mucus and Paneth cells secreting antimicrobial proteins (AMPs).(25) In conclusion, the mucosal microbiota may be a reservoir…”
BackgroundFrom food to cell: nutrient exploitation strategies of enteropathogens
Staib, L., & Fuchs, T. M. (2014) · Microbiology · doi:10.1099/mic.0.078105-0 · Cited by 76
Peters, M. F., Choy, A. L., Pin, C., Leishman, D. J., Moisan, A., Ewart, L. C., Guzzie‐Peck, P., Sura, R., Keller, D. A., Scott, C. W., et al. (2020) · Lab on a Chip · doi:10.1039/c9lc01107b · Cited by 80
Rosa, V. D., Galgani, M., Santopaolo, M., Colamatteo, A., Laccetti, R., & Matarese, G. (2015) · Seminars in Immunology · doi:10.1016/j.smim.2015.10.001 · Cited by 77
Dorożyńska, I., Majewska‐Szczepanik, M., Marcińska, K., & Szczepanik, M. (2014) · Pharmacological Reports · doi:10.1016/j.pharep.2013.09.007 · Cited by 76
Cristofori, F., Indrio, F., Miniello, V. L., Angelis, M. D., & Francavilla, R. (2018) · Nutrients · doi:10.3390/nu10121824 · Cited by 82
Mucosal Immune System of Cattle
Chase, C. C. L., & Kaushik, R. S. (2019) · Veterinary Clinics of North America Food Animal Practice · doi:10.1016/j.cvfa.2019.08.006 · Cited by 75
“2).(1) Secretory IgG (sIgG) in the nasal and URT and the reproductive tract is as or more important than sIgA.”
BackgroundImmunogenetic control of the intestinal microbiota
Marietta, E. V., Rishi, A. R., & Taneja, V. (2015) · Immunology · doi:10.1111/imm.12474 · Cited by 75
The gut mucosal immune system in the neonatal period
Battersby, A., & Gibbons, D. L. (2013) · Pediatric Allergy and Immunology · doi:10.1111/pai.12079 · Cited by 75
“The importance of how intestinal cells maintain immune homoeostasis with non-pathogenic bacteria is becoming increasingly obvious (36); however, the full array of molecular and cellular mechanisms used to maintain this status quo has not been fully established (37): we discuss some emerging ideas below.”
BackgroundLi, C., Wang, W., Liu, T., Zhang, Q., Wang, G., Li, F., Li, F., Yue, X., & Li, T. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01431 · Cited by 73
Jing, B., Wang, Z. A., Zhang, C., Deng, Q., Wei, J., Luo, Y., Zhang, X., Li, J., & Du, Y. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00272 · Cited by 76
The marine mammal microbiome: current knowledge and future directions
Nelson, T. M., Apprill, A. M., Mann, J., Rogers, T. L., & Brown, M. V. (2015) · Microbiology Australia · doi:10.1071/ma15004 · Cited by 75
Development and immunity-related microRNAs of the lepidopteran model host Galleria mellonella
Mukherjee, K., & Vilcinskas, A. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-705 · Cited by 73
“The consumption of diets containing pathogenic bacteria results in the disruption of gut homeostasis, leading to dysbiosis and other gastrointestinal diseases [28].”
BackgroundVaginal microbiota transplantation for the treatment of bacterial vaginosis: a conceptual analysis
Ma, D., Chen, Y., & Chen, T. (2019) · FEMS Microbiology Letters · doi:10.1093/femsle/fnz025 · Cited by 72
Role of Inflammasomes in Intestinal Inflammation and Crohnʼs Disease
Opipari, A. W., & Franchi, L. (2014) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000230 · Cited by 75
Pop, M., Paulson, J. N., Chakraborty, S., Astrovskaya, I., Lindsay, B. R., Li, S., Bravo, H. C., Harro, C. D., Parkhill, J., Walker, A. W., et al. (2016) · BMC Genomics · doi:10.1186/s12864-016-2777-0 · Cited by 71
“The intestinal microbial community is a complex ecosystem that influences human health in numerous ways: regulating metabolism and nutrition [6–8], developing the immune system [9–11], and preventing colonization and invasion by enteropathogens [12–15].”
BackgroundMekuchi, M., Asakura, T., Sakata, K., Yamaguchi, T., Teruya, K., & Kikuchi, J. (2018) · PLoS ONE · doi:10.1371/journal.pone.0197256 · Cited by 73
Wang, Z., Zhou, J. F., Li, J., Zou, J., & Fan, L. (2020) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2020.04.053 · Cited by 71
Kant, R., de Vos, W. M., Palva, A., & Satokari, R. M. (2013) · Journal of Medical Microbiology · doi:10.1099/jmm.0.064220-0 · Cited by 74
“The immediate recognition of microbes by the innate immune system plays an important role in immune responsiveness and homeostasis in the intestine (Abreu, 2010; Maynard et al., 2012; Wells et al., 2011).”
BackgroundInfluentialTLR sorting by Rab11 endosomes maintains intestinal epithelial‐microbial homeostasis
Yu, S., Nie, Y., Knowles, B. C., Sakamori, R., Stypulkowski, E., Patel, C. A., Das, S., Douard, V., Ferraris, R. P., Bonder, E. M., et al. (2014) · The EMBO Journal · doi:10.15252/embj.201487888 · Cited by 71
“In mammals, the postnatal intestinal epithelial cells (IECs), after transitioning from a relatively germ-free fetal environment, immediately interact with enteric microbes and participate in immune surveillance against luminal pathogenic stimuli (Artis, 2008; Maynard et al , 2012).”
Osteomicrobiology: A New Cross-Disciplinary Research Field
Ohlsson, C., & Sjögren, K. (2017) · Calcified Tissue International · doi:10.1007/s00223-017-0336-6 · Cited by 75
“Perturbed microbial composition has been postulated to be involved in a range of inflammatory conditions, within and outside the gut, including rheumatoid arthritis, multiple sclerosis, inflammatory bowel diseases, diabetes, food allergies, eczema, and asthma as well as obesity and the metabolic syndrome [20, 21].”
BackgroundEffect of barrier microbes on organ-based inflammation
Garn, H., Neves, J. F., Blumberg, R. S., & Renz, H. E. (2013) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2013.04.031 · Cited by 70
“It has been recently recognized that there is a very close bidirectional interaction between these bacteria and our immune system.(33) Some microbes provide us with essential nonnutrient factors, such as vitamins.”
Innate immunity: Actuating the gears of celiac disease pathogenesis
Kim, S. M., Mayassi, T., & Jabrì, B. (2015) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2015.05.001 · Cited by 75
Feeding modes shape the acquisition and structure of the initial gut microbiota in newborn lambs
Bi, Y., Cox, M. S., Zhang, F., Suen, G., Zhang, N., Tu, Y., & Diao, Q. (2019) · Environmental Microbiology · doi:10.1111/1462-2920.14614 · Cited by 72
“…the gut microbiota of newborns is essential for health by maintaining intestinal homeostasis and barrier function, stimulating development of the immune system, contributing to nutrient digestion, and protecting against pathogens (Sekirov et al., 2010; Maynard et al., 2012; Wopereis et al., 2014).”
BackgroundThe oral microbiome in autoimmune diseases: friend or foe?
Huang, X., Huang, X., Huang, Y., Zheng, J., Ye, L., Mai, Z., Zhao, X., Cui, L., & Huang, S. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-03995-x · Cited by 76
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Impact of the mother's gut microbiota on infant microbiome and brain development
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Insights into human evolution from ancient and contemporary microbiome studies
Schnorr, S. L., Sankaranarayanan, K., Lewis, C. M., & Warinner, C. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.07.003 · Cited by 71
Milcovich, G., Lettieri, S., Antunes, F. E., Medronho, B., Fonseca, A. C., Coelho, J. F. J., Marizza, P., Perrone, F. M., Farra, R., Dapas, B., et al. (2017) · Advances in Colloid and Interface Science · doi:10.1016/j.cis.2017.05.009 · Cited by 71
“stimulation of epithelial cell proliferation or induction of mucin secretion [131,137-139].”
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“Microbiota and their metabolites in the intestinal tract can activate the AhR pathway in the form of ligand dependence, then AhR regulation of the differentiation of immune cells promotes or regulates the release of anti-inflammatory factors (Maynard et al., 2012; Bessede et al., 2014; Villa et al., 2016; Kawajiri and…”
BackgroundIn vivo and in vitro anti-inflammatory effects of water-soluble polysaccharide from Arctium lappa
Zhang, N., Wang, Y., Kan, J., Wu, X., Zhang, X., Tang, S., Sun, R., Liu, J., Qian, C., & Jin, C. (2019) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2019.05.171 · Cited by 69
Probiotic species in the modulation of the anticancer immune response
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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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