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The Impact of Gut Microbiota on Gender-Specific Differences in Immunity
Open accessAbstract
Males and females are known to have gender-specific differences in their immune system and gut microbiota composition. Whether these differences in gut microbiota composition are a cause or consequence of differences in the immune system is not known. To investigate this issue, gut microbiota from conventional males or females was transferred to germ-free animals of the same or opposing gender. We demonstrate that microbiota-independent gender differences in immunity are already present in germ-free mice. In particular type I interferon signaling was enhanced in the intestine of germ-free females. Presumably, due to these immune differences bacterial groups such as Alistipes, Rikenella, and Porphyromonadaceae known to expand in the absence of innate immune defense mechanism were overrepresented in the male microbiota. The presence of these bacterial groups was associated with induction of weight loss, inflammation, and DNA damage upon transfer of the male microbiota to female germ-free recipients. In summary, our data suggests that microbiota-independent gender differences in the immune system select a gender-specific gut microbiota composition, which in turn further contributes to gender differences in the immune system.
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“However, including both genders in the study may have hindered some of the discoveries, as gender differences in the gut microbiota are known to influence, for instance, metabolic outcomes and immunity (Fransen et al., 2017).”
From Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women (2018) · cites this paper as Fransen et al., 2017
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“as gender differences in the gut microbiota are known to influence, for instance, metabolic outcomes and immunity (Fransen et al., 2017).”
From Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women (2018) · cites this paper as Fransen et al., 2017
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Cites
QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1219 · Cited by 33,055
Bioconductor: open software development for computational biology and bioinformatics
Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. (2004) · Genome biology · doi:10.1186/gb-2004-5-10-r80 · Cited by 12,082
Statistical significance for genomewide studies
Storey, J. D., & Tibshirani, R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1530509100 · Cited by 9,692
The gut microbiota shapes intestinal immune responses during health and disease
Round, J. L., & Mazmanian, S. K. (2009) · Nature Reviews Immunology · doi:10.1038/nri2515 · Cited by 5,029
Franke, A., McGovern, D. P. B., Barrett, J. C., Wang, K., Radford-Smith, G. L., Ahmad, T., Lees, C. W., Balschun, T., Lee, J., Roberts, R., et al. (2010) · Nature Genetics · doi:10.1038/ng.717 · Cited by 2,520
STRING 8--a global view on proteins and their functional interactions in 630 organisms
Jensen, L. J., Kuhn, M., Stark, M., Chaffron, S., Creevey, C. J., Muller, J., Doerks, T., Julien, P., Roth, A. C., Simonovic, M., et al. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn760 · Cited by 2,475
Dextran Sulfate Sodium (DSS)‐Induced Colitis in Mice
Chassaing, B., Aitken, J. D., Malleshappa, M., & Vijay–Kumar, M. (2014) · Current Protocols in Immunology · doi:10.1002/0471142735.im1525s104 · Cited by 2,094
Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity
Markle, J. G. M., Frank, D. N., Mortin-Toth, S., Robertson, C. E., Feazel, L. M., Rolle-Kampczyk, U., von Bergen, M., McCoy, K. D., Macpherson, A. J., & Danska, J. S. (2013) · Science · doi:10.1126/science.1233521 · Cited by 2,025
Innate immunity and intestinal microbiota in the development of Type 1 diabetes
Wen, L., Ley, R. E., Volchkov, P. Y., Stranges, P. B., Avanesyan, L., Stonebraker, A. C., Hu, C., Wong, F. S., Szot, G. L., Bluestone, J. A., et al. (2008) · Nature · doi:10.1038/nature07336 · Cited by 1,921
Regional specialization within the intestinal immune system
Mowat, A. M., & Agace, W. W. (2014) · Nature reviews. Immunology · doi:10.1038/nri3738 · Cited by 1,882
Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron
Flo, T. H., Smith, K. D., Sato, S., Rodriguez, D. J., Holmes, M. A., Strong, R. K., Akira, S., & Aderem, A. (2004) · Nature · doi:10.1038/nature03104 · Cited by 1,877
Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data
Dai, M. (2005) · Nucleic Acids Research · doi:10.1093/nar/gni179 · Cited by 1,807
Improved extraction of PCR-quality community DNA from digesta and fecal samples
Yu, Z., & Morrison, M. (2004) · BioTechniques · doi:10.2144/04365st04 · Cited by 1,663
Sex differences in autoimmune disease
Whitacre, C. C. (2001) · Nature Immunology · doi:10.1038/ni0901-777 · Cited by 1,294
The X-files in immunity: sex-based differences predispose immune responses
Fish, E. N. (2008) · Nature reviews. Immunology · doi:10.1038/nri2394 · Cited by 1,164
Mueller, S., Saunier, K., Hanisch, C., Norin, E., Alm, L., Midtvedt, T., Cresci, A., Silvi, S., Orpianesi, C., Verdenelli, M. C., et al. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.72.2.1027-1033.2006 · Cited by 1,006
Sarma, J. V., & Ward, P. A. (2010) · Cell and Tissue Research · doi:10.1007/s00441-010-1034-0 · Cited by 988
Gender Bias in Autoimmunity Is Influenced by Microbiota
Yurkovetskiy, L., Burrows, M. P., Khan, A. A., Graham, L., Volchkov, P., Becker, L., Antonopoulos, D. A., Umesaki, Y., & Chervonsky, A. V. (2013) · Immunity · doi:10.1016/j.immuni.2013.08.013 · Cited by 943
The microbiota regulates type 2 immunity through RORγt + T cells
Ohnmacht, C., Park, J.-H., Cording, S., Wing, J. B., Atarashi, K., Obata, Y., Gaboriau-Routhiau, V., Marques, R., Dulauroy, S., Fedoseeva, M., et al. (2015) · Science · doi:10.1126/science.aac4263 · Cited by 863 · cited 2×
“The frequency of the recently described RORγt+ Foxp3+ population (26) was much lower in the PPs (Figure 2D) and MLN (Figure 2E) of GF mice.”
BackgroundT-cell development and the CD4–CD8 lineage decision
Germain, R. N. (2002) · Nature reviews. Immunology · doi:10.1038/nri798 · Cited by 813
The X chromosome in immune functions: when a chromosome makes the difference
Libert, C., Dejager, L., & Pinheiro, I. (2010) · Nature reviews. Immunology · doi:10.1038/nri2815 · Cited by 789
Intestinal Microbiota Is Influenced by Gender and Body Mass Index
Haro, C., Rangel-Zúñiga, O. A., Alcalá-Díaz, J. F., Gómez-Delgado, F., Pérez-Martínez, P., Delgado-Lista, J., Quintana-Navarro, G. M., Landa, B. B., Navas-Cortés, J. A., Tena-Sempere, M., et al. (2016) · PLOS ONE · doi:10.1371/journal.pone.0154090 · Cited by 671
NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer
Couturier-Maillard, A., Sécher, T., Rehman, A., Normand, S., Arcangelis, A. D., Häsler, R., Huot, L., Grandjean, T., Bressenot, A., Delanoye, A., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci62236 · Cited by 571
Resistin: functional roles and therapeutic considerations for cardiovascular disease
Jamaluddin, M. S., Weakley, S. M., Yao, Q. C., & Chen, C. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01369.x · Cited by 553
The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts
Ainsworth, T. D., Krause, L., Bridge, T. C. L., Torda, G., Raina, J., Zakrzewski, M., Gates, R. D., Padilla‐Gamiño, J. L., Spalding, H. L., Smith, C. M., et al. (2015) · The ISME Journal · doi:10.1038/ismej.2015.39 · Cited by 547
DNA damage induced by chronic inflammation contributes to colon carcinogenesis in mice
Meira, L. B., Bugni, J. M., Green, S. L., Lee, C., Pang, B., Borenshtein, D., Rickman, B. H., Rogers, A. B., Moroski-Erkul, C. A., McFaline‐Figueroa, J. L., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci35073 · Cited by 542
Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification
Berry, D., Mahfoudh, K. B., Wagner, M., & Loy, A. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.05220-11 · Cited by 530
TLR7 Ligands Induce Higher IFN-α Production in Females
Berghöfer, B., Frommer, T., Haley, G., Fink, L., Bein, G., & Hackstein, H. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.4.2088 · Cited by 484
Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification
Berry, D., Mahfoudh, K. B., Wagner, M., & Loy, A. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.07448-11 · Cited by 397
SeXX Matters in Infectious Disease Pathogenesis
Steeg, L. G. V., & Klein, S. L. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005374 · Cited by 383
The X chromosome and immune associated genes
Bianchi, I., Lleo, A., Gershwin, M. E., & Invernizzi, P. (2012) · Journal of Autoimmunity · doi:10.1016/j.jaut.2011.11.012 · Cited by 378
Lipocalin 2 protects from inflammation and Tumorigenesis associated with gut microbiota alterations
Moschen, A. R., Gerner, R. R., Wang, J., Klepsch, V., Adolph, T. E., Reider, S. J., Hackl, H., Pfister, A., Schilling, J., Moser, P. L., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.03.007 · Cited by 375
Variants of DENND1B Associated with Asthma in Children
Abou‐Sleiman, P. M., Flory, J. H., Imielinski, M. B., Bradfield, J. P., Annaiah, K., Willis‐Owen, S. A. G., Wang, K., Rafaels, N. M., Michel, S., Bønnelykke, K., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0901867 · Cited by 323
Sartor, M. A., Tomlinson, C. R., Wesselkamper, S. C., Sivaganesan, S., Leikauf, G. D., & Medvedovic, M. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-538 · Cited by 263
Laffont, S., Rouquié, N., Azar, P., Seillet, C., Plumas, J., Aspord, C., & Guéry, J. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1303400 · Cited by 243
Gui, J., Mustachio, L. M., Su, D., & Craig, R. W. (2012) · Europe PMC (PubMed Central) · Cited by 199
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Wagstaff, A. J., & Goa, K. L. (2002) · Drugs · doi:10.2165/00003495-200262120-00007 · Cited by 175
van den Bogert, B., de Vos, W. M., Zoetendal, E. G., & Kleerebezem, M. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.02477-10 · Cited by 174
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Lin, K., Kools, H. J., de Groot, P. J., Gavai, A., Basnet, R. K., Cheng, F., Wu, J., Wang, X., Lommen, A., Hooiveld, G. J. E. J., et al. (2011) · Berichte aus der medizinischen Informatik und Bioinformatik/Journal of integrative bioinformatics · doi:10.1515/jib-2011-160 · Cited by 170
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Bolstad, B. M., Collin, F., Simpson, K., Irizarry, R. A., & Speed, T. P. (2004) · International review of neurobiology · doi:10.1016/s0074-7742(04)60002-x · Cited by 125
Tschurtschenthaler, M., Wang, J., Fricke, C., Fritz, T. M. J., Niederreiter, L., Adolph, T. E., Sarcevic, E., Künzel, S., Offner, F. A., Kalinke, U., et al. (2014) · Gut · doi:10.1136/gutjnl-2013-305863 · Cited by 105
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Cao, S., Su, L., Zeng, B., Yan, H., Huang, Y., Wang, E., Yun, H., Zhang, Y., Liu, F., Li, W., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2015.12.070 · Cited by 93
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Kelly, C. J., & Gangur, V. (2009) · Journal of Allergy · doi:10.1155/2009/159845 · Cited by 84
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Kurashima, Y., & Kiyono, H. (2014) · Experimental & Molecular Medicine · doi:10.1038/emm.2014.7 · Cited by 42
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Metadata
- Authors
- Fransen, F., van Beek, A. A., Borghuis, T., Meijer, B., Hugenholtz, F., van der Gaast-de Jongh, C., Savelkoul, H. F., de Jonge, M. I., Faas, M. M., Boekschoten, M. V., Smidt, H., El Aidy, S., & de Vos, P.
- Affiliations
- University Medical Center Groningen (NL)
- Wageningen University & Research (NL)
- Corresponding author
- Fransen, Floris
- Venue
- Frontiers in Immunology
- Publisher
- Frontiers Media SA
- Published
- 2017-06-30
- Volume
- 8
- Pages
- 754-754
- ISSN
- 1664-3224 (ISSN-L)
- PMC
- PMC5491612
- OpenAlex
- W2649086355
- Cited by
- 266
- References
- 49
- Citations by year
- 2026: 12 · 2025: 27 · 2024: 46 · 2023: 32 · 2022: 30 · 2021: 27 · 2020: 37 · 2019: 25 · 2018: 26 · 2017: 3
- FWCI
- 10.39
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Immunology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, cc-by)
- Socio-Environmental Systems Modeling (acceptedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Radboud Repository (Radboud University) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- Data Archiving and Networked Services (DANS) (submittedVersion, cc-by)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
- Keywords
- gut microbiota, sex differences in immunity, germ-free mice, microbiota transfer, type I interferon signaling, intestinal immunity, Alistipes, Rikenella, Porphyromonadaceae, inflammation, DNA damage, weight loss
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