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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Including both genders in the Cronin et al. study may have hindered some of the discoveries.
“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
Gender differences in the gut microbiota are known to influence metabolic outcomes and immunity.
“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
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
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 · see citing works
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 · see citing works
Bioconductor: open software development for computational biology and bioinformatics
Gentleman, R., Carey, V., Bates, D., 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 13,133 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data
Dai, M. (2005) · Nucleic Acids Research · doi:10.1093/nar/gni179 · Cited by 1,797 · see citing works
Regional specialization within the intestinal immune system
Mowat, A. M., & Agace, W. W. (2014) · Nature reviews. Immunology · doi:10.1038/nri3738 · Cited by 1,769 · see citing works
Improved extraction of PCR-quality community DNA from digesta and fecal samples
Yu, Z., & Morrison, M. D. (2004) · BioTechniques · doi:10.2144/04365st04 · Cited by 1,668 · see citing works
Sex differences in autoimmune disease
Whitacre, C. C. (2001) · Nature Immunology · doi:10.1038/ni0901-777 · Cited by 1,271 · see citing works
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 · see citing works
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 · see citing works
Sarma, J. V., & Ward, P. A. (2010) · Cell and Tissue Research · doi:10.1007/s00441-010-1034-0 · Cited by 988 · see citing works
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 912 · see citing works
The microbiota regulates type 2 immunity through RORγt <sup>+</sup> 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 · see citing works
T-cell development and the CD4–CD8 lineage decision
Germain, R. N. (2002) · Nature reviews. Immunology · doi:10.1038/nri798 · Cited by 813 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 550 · see citing works
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 548 · see citing works
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 538 · see citing works
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 519 · see citing works
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 · see citing works
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 394 · see citing works
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 · see citing works
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 · see citing works
SeXX Matters in Infectious Disease Pathogenesis
Steeg, L. G. V., & Klein, S. L. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005374 · Cited by 371 · see citing works
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 321 · see citing works
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 · see citing works
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 233 · see citing works
Gui, J., Mustachio, L. M., Su, D., & Craig, R. W. (2012) · Europe PMC (PubMed Central) · Cited by 200 · see citing works
Wagstaff, A. J., & Goa, K. L. (2002) · Drugs · doi:10.2165/00003495-200262120-00007 · Cited by 175 · see citing works
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 · see citing works
Diversity of human small intestinal Streptococcus and Veillonella populations
van den Bogert, B., Erkuş, O., Boekhorst, J., de Goffau, M. C., Smid, E. J., Zoetendal, E. G., & Kleerebezem, M. (2013) · FEMS Microbiology Ecology · doi:10.1111/1574-6941.12127 · Cited by 172 · see citing works
MADMAX – Management and analysis database for multiple ~omics experiments
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 · see citing works
Experimental Design and Low-Level Analysis of Microarray Data
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 · see citing works
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 96 · see citing works
The role of type I interferons in intestinal infection, homeostasis, and inflammation
Cho, H., & Kelsall, B. L. (2014) · Immunological Reviews · doi:10.1111/imr.12195 · Cited by 91 · see citing works
The Gut Epithelial Receptor LRRC19 Promotes the Recruitment of Immune Cells and Gut Inflammation
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 91 · see citing works
α3β1 integrin–controlled Smad7 regulates reepithelialization during wound healing in mice
Reynolds, L. E., Conti, F. J. A., Silva, R., Robinson, S. D., Iyer, V., Rudling, R. J., Cross, B., Nye, E. L., Hart, I. R., DiPersio, C. M., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci33538 · Cited by 89 · see citing works
Sex Disparity in Food Allergy: Evidence from the PubMed Database
Kelly, C. J., & Gangur, V. (2009) · Journal of Allergy · doi:10.1155/2009/159845 · Cited by 84 · see citing works
MADMAX - Management and analysis database for multiple ~omics experiments
Lin, K., Kools, H. J., de Groot, P. J., et al. (2011) · PubMed · doi:10.2390/biecoll-jib-2011-160 · Cited by 77 · see citing works
Kurashima, Y., & Kiyono, H. (2014) · Experimental & Molecular Medicine · doi:10.1038/emm.2014.7 · Cited by 42 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The gut microbiome: Relationships with disease and opportunities for therapy
Durack, J., & Lynch, S. V. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20180448 · Cited by 955 · see citing works
Sex differences in gut microbiota
Kim, Y. S., Unno, T., Kim, B.-Y., & Park, M.-S. (2020) · The World Journal of Men s Health · doi:10.5534/wjmh.190009 · Cited by 610 · see citing works
The Gut Microbiota and Unhealthy Aging: Disentangling Cause from Consequence
DeJong, E. N., Surette, M. G., & Bowdish, D. M. E. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.07.013 · Cited by 370 · see citing works
Connecting the immune system, systemic chronic inflammation and the gut microbiome: the role of sex
Rizzetto, L., Fava, F., Tuohy, K. M., & Selmi, C. (2018) · Journal of Autoimmunity · doi:10.1016/j.jaut.2018.05.008 · Cited by 331 · see citing works
Takagi, T., Naito, Y., Inoüe, R., Kashiwagi, S., Uchiyama, K., Mizushima, K., Tsuchiya, S., Dohi, O., Yoshida, N., Kamada, K., et al. (2018) · Journal of Gastroenterology · doi:10.1007/s00535-018-1488-5 · Cited by 310 · see citing works
Vemuri, R., Sylvia, K. E., Klein, S. L., Forster, S. C., Plebanski, M., Eri, R., & Flanagan, K. L. (2019) · Seminars in Immunopathology · doi:10.1007/s00281-018-0716-7 · Cited by 265 · see citing works
Gut microbiome composition and diversity are related to human personality traits
Johnson, K. V. ‐. (2019) · Human Microbiome Journal · doi:10.1016/j.humic.2019.100069 · Cited by 241 · see citing works
Munukka, E., Ahtiainen, J. P., Puigbó, P., Jalkanen, S., Pahkala, K., Keskitalo, A., Kujala, U. M., Pietilä, S., Hollmén, M., Elo, L., et al. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02323 · Cited by 237 · see citing works
Exposure to polystyrene microplastics impairs hippocampus-dependent learning and memory in mice
Lee, C., Hsu, L., Wu, I.-L., Wang, Y., Chen, W.-C., Liu, Y., Yang, L.-T., Tan, C.-L., Luo, Y.-H., Wang, C.-C., et al. (2022) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2022.128431 · Cited by 235 · see citing works
The role of the gut microbiota in multiple sclerosis
Correale, J., Hohlfeld, R., & Baranzini, S. E. (2022) · Nature Reviews Neurology · doi:10.1038/s41582-022-00697-8 · Cited by 207 · see citing works
Sex, microbes, and polycystic ovary syndrome
Thackray, V. G. (2019) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2018.11.001 · Cited by 203 · see citing works
You’ve got male: Sex and the microbiota-gut-brain axis across the lifespan
Jaggar, M., Rea, K., Spichak, S., Dinan, T. G., & Cryan, J. F. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100815 · Cited by 200 · see citing works
Gadi, N., Wu, S., Spihlman, A. P., & Moulton, V. R. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.02147 · Cited by 185 · see citing works
The gut microbiome and elevated cardiovascular risk in obesity and autoimmunity
Kasselman, L. J., Vernice, N. A., DeLeon, J. R., & Reiss, A. B. (2018) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2018.02.036 · Cited by 159 · see citing works
Sex and strain dependent differences in mucosal immunology and microbiota composition in mice
Elderman, M. E., Hugenholtz, F., Belzer, C., Boekschoten, M. V., van Beek, A. A., de Haan, B., Savelkoul, H. F. J., de Vos, P., & Faas, M. M. (2018) · Biology of Sex Differences · doi:10.1186/s13293-018-0186-6 · Cited by 149 · see citing works
Self-citationGheorghe, C. E., Ritz, N. L., Martin, J. A., Wardill, H. R., Cryan, J. F., & Clarke, G. A. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1941711 · Cited by 149 · see citing works
Probiotics may have beneficial effects in parkinson’s disease: In vitro evidence
Magistrelli, L., Amoruso, A., Mogna, L., Graziano, T., Cantello, R., Pane, M., & Comi, C. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00969 · Cited by 144 · see citing works
Vemuri, R., Gundamaraju, R., Shastri, M. D., Shukla, S. D., Kalpurath, K., Ball, M. A. Z., Tristram, S. G., Shankar, E. M., Ahuja, K., & Eri, R. D. (2018) · BioMed Research International · doi:10.1155/2018/4178607 · Cited by 141 · see citing works
Billi, A. C., Kahlenberg, J. M., & Gudjonsson, J. E. (2018) · Current Opinion in Rheumatology · doi:10.1097/bor.0000000000000564 · Cited by 132 · see citing works
Sex differences in lipid metabolism are affected by presence of the gut microbiota
Baars, A., Oosting, A., Lohuis, M. A. M., Koehorst, M., Aidy, S. E., Hugenholtz, F., Smidt, H., Mischke, M., Boekschoten, M. V., Verkade, H. J., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-31695-w · Cited by 131 · see citing works
Self-citationMulti-hit early life adversity affects gut microbiota, brain and behavior in a sex-dependent manner
Rincel, M., Aubert, P., Chevalier, J., Grohard, P. ‐., Basso, L., de Oliveira, C. M., Helbling, J., Lévy, É., Chevalier, G., Leboyer, M., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.03.006 · Cited by 132 · see citing works
Profiling the Salivary microbiome of the Qatari population
Murugesan, S., Ahmad, S. F. A., Singh, P., Saadaoui, M., Kumar, M., & Khodor, S. A. (2020) · Journal of Translational Medicine · doi:10.1186/s12967-020-02291-2 · Cited by 105 · see citing works
Unraveling the Gut Microbiota: Implications for Precision Nutrition and Personalized Medicine
Abeltino, A., Hatem, D., Serantoni, C., Riente, A., Giulio, M. M. D., Spirito, M. D., Maio, F. D., & Maulucci, G. (2024) · Nutrients · doi:10.3390/nu16223806 · Cited by 108 · see citing works
Bile Acid Receptors and the Gut–Liver Axis in Nonalcoholic Fatty Liver Disease
Xue, R., Su, L., Lai, S., Wang, Y., Zhao, D., Fan, J., Chen, W., Hylemon, P. B., & Zhou, H. (2021) · Cells · doi:10.3390/cells10112806 · Cited by 95 · see citing works
Borewicz, K., Gu, F., Saccenti, E., Hechler, C., Beijers, R., de Weerth, C., van Leeuwen, S. S., Schols, H. A., & Smidt, H. (2020) · Scientific Reports · doi:10.1038/s41598-020-61024-z · Cited by 93 · see citing works
Self-citationZhang, Y., Li, Y., Lu, P., Dai, G.-C., Chen, X.-X., & Rui, Y. (2021) · Food & Function · doi:10.1039/d0fo03468a · Cited by 88 · see citing works
Sex bias in lymphocytes: Implications for autoimmune diseases
Dodd, K. C., & Menon, M. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.945762 · Cited by 87 · see citing works
Hallmarks of sex bias in immuno-oncology: mechanisms and therapeutic implications
Xiao, T., Lee, J., Gauntner, T. D., Velegraki, M., Lathia, J. D., & Li, Z. (2024) · Nature reviews. Cancer · doi:10.1038/s41568-024-00680-z · Cited by 85 · see citing works
Role of Microbiota in Sexually Dimorphic Immunity
Elderman, M. E., de Vos, P., & Faas, M. M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01018 · Cited by 87 · see citing works
Self-citationKozik, A. J., Nakatsu, C. H., Chun, H., & Jones‐Hall, Y. (2019) · PLoS ONE · doi:10.1371/journal.pone.0225079 · Cited by 85 · see citing works
Sexual dimorphism of gut microbiota at different pubertal status
Yuan, X., Chen, R., Zhang, Y., Lin, X., & Yang, X. (2020) · Microbial Cell Factories · doi:10.1186/s12934-020-01412-2 · Cited by 86 · see citing works
Li, Y., Xu, W., Zhang, F., Zhong, S. S., Sun, Y., Huo, J., Zhu, J., & Wu, C. (2020) · mSystems · doi:10.1128/msystems.00313-20 · Cited by 84 · see citing works
Vanillin Alleviates High Fat Diet-Induced Obesity and Improves the Gut Microbiota Composition
Guo, J., Han, X., Zhan, J., You, Y., & Huang, W. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02733 · Cited by 81 · see citing works
Sajdel, E. M. (2023) · Microorganisms · doi:10.3390/microorganisms11092199 · Cited by 82 · see citing works
Sawada, D., Kuwano, Y., Tanaka, H., Hara, S., Uchiyama, Y., Sugawara, T., Fujiwara, S., Rokutan, K., & Nishida, K. (2019) · Journal of Functional Foods · doi:10.1016/j.jff.2019.04.022 · Cited by 76 · see citing works
Audet, M. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100772 · Cited by 79 · see citing works
Brettle, H., Tran, V., Drummond, G. R., Franks, A. E., Petrovski, S., Vinh, A., & Jelinic, M. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.971048 · Cited by 78 · see citing works
Tesei, D., Jewczynko, A., Lynch, A., & Urbaniak, C. (2022) · Life · doi:10.3390/life12040495 · Cited by 75 · see citing works
The gut microbiome is a significant risk factor for future chronic lung disease
Liu, Y., Teo, S. M., Méric, G., Tang, H. H. F., Zhu, Q., Sanders, J. G., Vázquez‐Baeza, Y., Verspoor, K. M., Vartiainen, V. A., Jousilahti, P., et al. (2022) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2022.12.810 · Cited by 73 · see citing works
Gender aspects in food allergy
Pali‐Schöll, I., & Jensen‐Jarolim, E. (2019) · Current Opinion in Allergy and Clinical Immunology · doi:10.1097/aci.0000000000000529 · Cited by 72 · see citing works
Dong, H.-L., Zhang, S., Chen, Z.-H., Tao, H., Li, X., Qiu, J., Cui, W., Sima, Y., Cui, W.-Z., & Xu, S.-Q. (2018) · RSC Advances · doi:10.1039/c8ra04627a · Cited by 70 · see citing works
Sex differences in colorectal cancer: with a focus on sex hormone–gut microbiome axis
Wu, Z., Huang, Y., Zhang, R., Zheng, C., You, F., Wang, M., Xiao, C., & Li, X. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-024-01549-2 · Cited by 70 · see citing works
Potential biological contributers to the sex difference in multiple sclerosis progression
Álvarez‐Sánchez, N., & Dunn, S. E. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1175874 · Cited by 71 · see citing works
Schierová, D., Březina, J., Mrázek, J., Fliegerova, K. O., Kvasnová, S., Bajer, L., & Drastich, P. (2020) · Cells · doi:10.3390/cells9102283 · Cited by 67 · see citing works
Sex and Gender Differences in Alzheimer’s Disease: Genetic, Hormonal, and Inflammation Impacts
Kolahchi, Z., Henkel, N., Eladawi, M. A., Villarreal, E. C., Kandimalla, P., Lundh, A., McCullumsmith, R. E., & Cuevas, E. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25158485 · Cited by 63 · see citing works
Does the microbiome and virome contribute to myalgic encephalomyelitis/chronic fatigue syndrome?
Newberry, F., Hsieh, S.-Y., Wileman, T., & Carding, S. R. (2018) · Clinical Science · doi:10.1042/cs20171330 · Cited by 61 · see citing works
El-Hakim, Y., Mani, K. K., Eldouh, A., Pandey, S., Grimaldo, M. T., Dabney, A. R., Pilla, R., & Sohrabji, F. (2021) · Biology of Sex Differences · doi:10.1186/s13293-020-00352-1 · Cited by 58 · see citing works
Current Trends and Challenges of Fecal Microbiota Transplantation—An Easy Method That Works for All?
Almeida, C., Oliveira, R., Baylina, P., Fernandes, R., Teixeira, F. G., & Barata, P. (2022) · Biomedicines · doi:10.3390/biomedicines10112742 · Cited by 52 · see citing works
Jiang, F., Song, P., Wang, H., Zhang, J., Liu, D., Cai, Z., Gao, H., Chi, X., & Zhang, T. (2022) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-022-11775-8 · Cited by 50 · see citing works
Stoian, A. P., Toth, P. P., Kempler, P., & Rizzo, M. (2020) · International Journal of Clinical Practice · doi:10.1111/ijcp.13666 · Cited by 46 · see citing works
Cella, V., Bimonte, V. M., Sabato, C., Paoli, A., Baldari, C., Campanella, M., Lenzi, A., Ferretti, E., & Migliaccio, S. (2021) · Foods · doi:10.3390/foods10123075 · Cited by 48 · see citing works
Redondo, N., Gheorghe, A., Díaz, L. E., Villavisencio, B., Marcos, A., & Nova, E. (2019) · Nutrients · doi:10.3390/nu11030651 · Cited by 49 · see citing works
Movement ecology and sex are linked to barn owl microbial community composition
Corl, A. B., Charter, M., Rozman, G., Toledo, S., Turjeman, S. C., Kamath, P. L., Getz, W. M., Nathan, R., & Bowie, R. C. K. (2020) · Molecular Ecology · doi:10.1111/mec.15398 · Cited by 46 · see citing works
Placental Epigenome Impacts Fetal Development: Effects of Maternal Nutrients and Gut Microbiota
Basak, S., Mallick, R., Boga, N. S., & Duttaroy, A. K. (2024) · Nutrients · doi:10.3390/nu16121860 · Cited by 53 · see citing works
Yao, T., Deemer, D. G., Chen, M., Reuhs, B. L., Hamaker, B. R., & Lindemann, S. R. (2023) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2023.121039 · Cited by 46 · see citing works
Fang, S., Chen, X., Pan, J., Chen, Q., Zhou, L., Wang, C., Xiao, T., & Gan, Q. F. (2020) · BMC Microbiology · doi:10.1186/s12866-020-01797-5 · Cited by 47 · see citing works
Langgartner, D., Vaihinger, C. A., Haffner-Luntzer, M., Kunze, J. F., Weiss, A.-L. J., Foertsch, S., Bergdolt, S., Ignatius, A., & Reber, S. O. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00252 · Cited by 45 · see citing works
Ceccarelli, G., Statzu, M., Santinelli, L., Pinacchio, C., Bitossi, C., Cavallari, E. N., Vullo, V., Scagnolari, C., & d’Ettorre, G. (2019) · Expert Opinion on Biological Therapy · doi:10.1080/14712598.2019.1638907 · Cited by 44 · see citing works
The sex-specific interaction of the microbiome in neurodegenerative diseases
Cox, L. M., Abou‐El‐Hassan, H., Maghzi, A. H., Vincentini, J., & Weiner, H. L. (2019) · Brain Research · doi:10.1016/j.brainres.2019.146385 · Cited by 42 · see citing works
Qi, C., Ding, M., Li, S., Zhou, Q., Li, D., Yu, R., & Sun, J. (2021) · Journal of Dairy Science · doi:10.3168/jds.2020-19437 · Cited by 41 · see citing works
Sheng, L., Jena, P. K., Hu, Y. C., & Wan, Y. Y. (2021) · HepatoBiliary Surgery and Nutrition · doi:10.21037/hbsn-20-671 · Cited by 37 · see citing works
Dash, N. R., & Al Bataineh, M. T. (2021) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2019.0202 · Cited by 37 · see citing works
Ding, M., Li, B., Chen, H., Liang, D., Ross, R. P., Stanton, C., Zhao, J., Chen, W., & Yang, B. K. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2290344 · Cited by 36 · see citing works
Gut Microbiota and Sex Hormones: Crosstalking Players in Cardiometabolic and Cardiovascular Disease
Maffei, S., Forini, F., Canale, P., Nicolini, G., & Guiducci, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137154 · Cited by 36 · see citing works
Ba, Z., Lee, Y., Meng, H., Kris‐Etherton, P. M., Rogers, C. J., Lewis, Z. T., Mills, D. A., Furumoto, E. J., Rolon, M. L., Fleming, J. A., et al. (2021) · mSphere · doi:10.1128/msphere.00084-21 · Cited by 32 · see citing works
Approaches to discern if microbiome associations reflect causation in metabolic and immune disorders
Basic, M., Dardevet, D. P., Abuja, P. M., Bolsega, S., Bornes, S., Caesar, R., Calabrese, F. M., Collino, M., Angelis, M. D., Gérard, P., et al. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2107386 · Cited by 34 · see citing works
Babu, A., Rajeswari, V. D., Ganesh, V., Das, S., Sivaraman, D., Rani, G. U., & Ramanathan, G. (2024) · Reproductive Sciences · doi:10.1007/s43032-023-01450-2 · Cited by 31 · see citing works
Colas, L., Mongodin, E. F., Montassier, E., Chesneau, M., Guérif, P., Hittle, L. L., Giral, M., Bromberg, J. S., & Brouard, S. (2019) · American Journal of Transplantation · doi:10.1111/ajt.15549 · Cited by 31 · see citing works
Simões‐Silva, L., Araújo, R., Pestana, M., Soares‐Silva, I., & Sampaio‐Maia, B. (2020) · Microorganisms · doi:10.3390/microorganisms8020173 · Cited by 31 · see citing works
Watanabe, S., Kameoka, S., Shinozaki, N. O., Ryuichi, K. U. B. O., Nishida, A., Kuriyama, M., & Takeda, A. (2021) · Bioscience of Microbiota Food and Health · doi:10.12938/bmfh.2020-038 · Cited by 33 · see citing works
The role of the sex hormone-gut microbiome axis in tumor immunotherapy
Wang, L., Tang, L., Zhai, D., Song, M., Li, W., Xu, S., Jiang, S., Meng, H., Liang, J., Wang, Y., et al. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2185035 · Cited by 31 · see citing works
Sex—the most underappreciated variable in research: insights from helminth-infected hosts
Wesołowska, A. (2022) · Veterinary Research · doi:10.1186/s13567-022-01103-3 · Cited by 33 · see citing works
Immune Cells, Gut Microbiota, and Vaccines: A Gender Perspective
Rio, P., Caldarelli, M., Chiantore, M., Ocarino, F., Candelli, M., Gasbarrini, A., Gambassi, G., & Cianci, R. (2024) · Cells · doi:10.3390/cells13060526 · Cited by 31 · see citing works
Zuo, H., Fu, M. R., Zhao, H.-L., Du, X.-W., Hu, Z.-Y., Zhao, X.-Y., Ji, X.-Q., Feng, X.-Q., Zhumajiang, W., Zhou, T.-H., et al. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.514943 · Cited by 30 · see citing works
Sun, Q. H., Liu, Z. J., Zhang, L., Wei, H., Song, L. J., Zhu, S. W., He, M. B., & Duan, L. (2021) · Journal of Digestive Diseases · doi:10.1111/1751-2980.12988 · Cited by 30 · see citing works
Sex-Related Differences in Immunotherapy Toxicities: Insights into Dimorphic Responses
Canzian, J., Conforti, F., Jacobs, F., Benvenuti, C., Gaudio, M., Gerosa, R., Sanctis, R. D., & Zambelli, A. (2025) · Cancers · doi:10.3390/cancers17071054 · Cited by 31 · see citing works
Hu, N., Zhang, X., Yu, Z., Du, Y., He, X., Wang, H., Pu, L., Pan, D., He, S., Liu, X., et al. (2022) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2022.129605 · Cited by 28 · see citing works
Impact of Acute and Chronic Amyloid-β Peptide Exposure on Gut Microbial Commensals in the Mouse
Guilherme, M. D. S., Todorov, H., Osterhof, C., Möllerke, A., Cub, K., Hankeln, T., Gerber, S., & Endres, K. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01008 · Cited by 29 · see citing works
Singh, Y., Trautwein, C., Dhariwal, A., Salker, M. S., Alauddin, M., Zizmare, L., Pelzl, L., Feger, M., Admard, J., Casadei, N., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-72903-w · Cited by 28 · see citing works
The Urinary Microbiome: Role in Bladder Cancer and Treatment
Friedrich, V., & Choi, H. W. (2022) · Diagnostics · doi:10.3390/diagnostics12092068 · Cited by 27 · see citing works
Pioneering gut health improvements in piglets with phytogenic feed additives
Yu, S. J., Morris, A., Kayal, A., Milošević, I., Van, T. T. H., Bajagai, Y. S., & Stanley, D. (2024) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-023-12925-2 · Cited by 26 · see citing works
Ghaffar, T., Valeriani, F., & Spica, V. R. (2025) · Microbial Pathogenesis · doi:10.1016/j.micpath.2025.108094 · Cited by 28 · see citing works
Li, Y., Zhong, S. S., Yu, J., Sun, Y., Zhu, J., Ji, D.-F., & Wu, C. (2018) · Journal of Functional Foods · doi:10.1016/j.jff.2018.10.034 · Cited by 27 · see citing works
Niu, C., Tu, Y., Jin, Q., Chen, Z., Yuan, K., Wang, M., Zhang, P., Luo, J., Li, H., Yang, Y., et al. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1157368 · Cited by 26 · see citing works
JohnBritto, J. S., Ciaula, A. D., Noto, A., Cassano, V., Sciacqua, A., Khalil, M., Portincasa, P., & Bonfrate, L. (2024) · European Journal of Internal Medicine · doi:10.1016/j.ejim.2024.03.011 · Cited by 27 · see citing works
Gut microbiota and cancer immunotherapy: prognostic and therapeutic implications
Güven, D. C., Aktaş, B. Y., Şimşek, C., & Aksoy, S. (2020) · Future Oncology · doi:10.2217/fon-2019-0783 · Cited by 25 · see citing works
Comparison of inflammatory and behavioral responses to chronic stress in female and male mice
Medina-Rodriguez, E. M., Rice, K. C., Jope, R. S., & Beurel, E. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.08.017 · Cited by 24 · see citing works
Saboo, K., Shamsaddini, A., Iyer, M. V., Hu, C., Fagan, A., Gavis, E. A., White, M. B., Fuchs, M. A., Heuman, D. M., Sikaroodi, M., et al. (2020) · Journal of Hepatology · doi:10.1016/j.jhep.2020.06.046 · Cited by 24 · see citing works
Prakriti phenotypes as a stratifier of gut microbiome: A new frontier in personalized medicine?
Jnana, A., Murali, T. S., Guruprasad, K. P., & Satyamoorthy, K. (2020) · Journal of Ayurveda and Integrative Medicine · doi:10.1016/j.jaim.2020.05.013 · Cited by 27 · see citing works
Shamsi, M. M., Maryam, J., Bakhshi, B., Neda, F., Mokhtarzade, M., Mahboobeh, B., Quinn, L. S., & Kalani, B. S. (2021) · Archives of Physiology and Biochemistry · doi:10.1080/13813455.2021.1871763 · Cited by 25 · see citing works
Sex differences associate with late microbiome alterations after murine surgical sepsis
Efron, P. A., Darden, D. B., Li, E. C., Munley, J., Kelly, L., Fenner, B., Nacionales, D. C., Ungaro, R. F., Dirain, M. L., Rincon, J., et al. (2022) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/ta.0000000000003599 · Cited by 24 · see citing works
Wang, J., Choi, Y., Lee, J., Hwang, S., Gu, J., & Son, C. (2024) · European journal of medical research · doi:10.1186/s40001-024-01747-1 · Cited by 23 · see citing works
Assess the diversity of gut microbiota among healthy adults for forensic application
Wang, S., Song, F., Gu, H., Shu, Z., Wei, X., Zhang, K., Zhou, Y., Jiang, L., Wang, Z., Li, J., et al. (2022) · Microbial Cell Factories · doi:10.1186/s12934-022-01769-6 · Cited by 24 · see citing works
Magnesium: Exploring Gender Differences in Its Health Impact and Dietary Intake
Mazza, E., Maurotti, S., Ferro, Y., Castagna, A., Pujia, C., Sciacqua, A., Pujia, A., & Montalcini, T. (2025) · Nutrients · doi:10.3390/nu17132226 · Cited by 22 · see citing works
Kumar, D., Sun, Z., Cao, G., Xue, R., Hu, X., & Gong, C. (2019) · Journal of Asia-Pacific Entomology · doi:10.1016/j.aspen.2019.03.005 · Cited by 22 · see citing works
Effects of the DASH Diet and Sodium Intake on Bloating: Results From the DASH–Sodium Trial
Peng, A. W., Juraschek, S. P., Appel, L. J., Miller, E. R., & Mueller, N. T. (2019) · The American Journal of Gastroenterology · doi:10.14309/ajg.0000000000000283 · Cited by 22 · see citing works
Dendrobium officinale Polysaccharides Better Regulate the Microbiota of Women Than Men
Tao, W., Liu, W., Wang, M., Zhou, W., Xing, J., Xu, J., Pi, X., Wang, X., Lu, S., & Yang, Y. (2022) · Foods · doi:10.3390/foods11111641 · Cited by 22 · see citing works
Coordinated Induction of Antimicrobial Response Factors in Systemic Lupus Erythematosus
Ayyappan, P., Harms, R. Z., Buckner, J. H., & Sarvetnick, N. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00658 · Cited by 22 · see citing works
Ding, M., Li, B., Chen, H., Ross, R. P., Stanton, C., Zhao, J., Chen, W., & Yang, B. K. (2024) · Nutrients · doi:10.3390/nu16081148 · Cited by 20 · see citing works
Tian, J., Du, J., Han, J., Song, X., & Lü, Z. (2020) · Marine Mammal Science · doi:10.1111/mms.12728 · Cited by 20 · see citing works
- 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 · 2014: 1
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review