Antibiotic-induced socio-sexual behavioral deficits are reversed via cecal microbiota transplantation but not androgen treatment

Arnold, 2009, The organizational–activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues, Horm. Behav., 55, 570, 10.1016/j.yhbeh.2009.03.011 Agranyoni, 2021, Gut microbiota determines the social behavior of mice and induces metabolic and inflammatory changes in their adipose tissue, NPJ Biofilms Microb., 7, 28, 10.1038/s41522-021-00193-9 Bercik, 2011, The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice, Gastroenterology, 141, 599, 10.1053/j.gastro.2011.04.052 Bodo, 2008, The androgen receptor is selectively involved in organization of sexually dimorphic social behaviors in mice, Endocrinology, 149, 4142, 10.1210/en.2008-0183 Bolyen, 2019, Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2, Nat. Biotechnol., 37, 852, 10.1038/s41587-019-0209-9 Buffington, 2016, Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring, Cell, 165, 1762, 10.1016/j.cell.2016.06.001 Carabotti, 2015, The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems, Ann. Gastroenterol.: Quart. Publ. Hellenic Soc. Gastroenterol., 28, 203 Chen, 2014, New knock-out model confirms a role for androgen receptors in regulating anxiety-like behaviors and HPA response in mice, Horm. Behav., 65, 211, 10.1016/j.yhbeh.2014.01.001 Chu, 2015, Socio-sexual behaviors and reproductive success of rats (Rattus norvegicus) in a seminatural environment, Physiol. Behav., 151, 46, 10.1016/j.physbeh.2015.07.005 Clarke, 2013, The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner, Mol. Psychiatr., 18, 666, 10.1038/mp.2012.77 Colldén, 2019, The gut microbiota is a major regulator of androgen metabolism in intestinal contents, Am. J. Physiol. Endocrinol. Metab., 317, E1182, 10.1152/ajpendo.00338.2019 Cross, 2021, Puberty is a critical period for vomeronasal organ mediation of socio-sexual behavior in mice, Frontiers Behav. Neurosci., 14, 10.3389/fnbeh.2020.606788 Cryan, 2012, Mind-altering microorganisms: the impact of the gut microbiota on brain and behavior, Nat. Rev. Neurosci., 13, 701, 10.1038/nrn3346 Desbonnet, 2015, Gut microbiota depletion from early adolescence in mice: implications for brain and behavior, Brain Behav. Immun., 48, 165, 10.1016/j.bbi.2015.04.004 Desbonnet, 2014, Microbiota is essential for social development in the mouse, Mol. Psychiatr., 19, 146, 10.1038/mp.2013.65 Diaz Heijtz, 2011, Normal gut microbiota modulates brain development and behavior, Proc. Natl. Acad. Sci. U. S. A, 108, 3047, 10.1073/pnas.1010529108 Elderman, 2018, Sex and strain dependent differences in mucosal immunology and microbiota composition in mice, Biol. Sex Differ., 9, 26, 10.1186/s13293-018-0186-6 Elias-Oliveira, 2020, NLR and intestinal dysbiosis-associated inflammatory illness: drivers or dampers?, Front. Immunol., 11, 1810, 10.3389/fimmu.2020.01810 Feng, 2019, Antibiotics induced intestinal tight junction barrier dysfunction is associated with microbiota dysbiosis, activated NLRP3 inflammasome and autophagy, PLoS One, 14, 10.1371/journal.pone.0218384 François, 2016, Olfactory epithelium changes in germfree mice, Sci. Rep., 6, 10.1038/srep24687 Fransen, 2017, The impact of gut microbiota on gender-specific differences in immunity, Front. Immunol., 8, 754, 10.3389/fimmu.2017.00754 Gacias, 2016, Microbiota-driven transcriptional changes in prefrontal cortex override genetic differences in social behavior, Elife, 5, 10.7554/eLife.13442 Gunaydin, 2014, Natural neural projection dynamics underlying social behavior, Cell, 157, 1535, 10.1016/j.cell.2014.05.017 Gwak, 2021, Gut-brain connection: microbiome, gut barrier, and environmental sensors, Immune Netw., 21, e20, 10.4110/in.2021.21.e20 Hamilton, 2013, High-throughput DNA sequence analysis reveals stable engraftment of gut microbiota following transplantation of previously frozen fecal bacteria, Gut Microb., 4, 125, 10.4161/gmic.23571 Hufeldt, 2010, Variation in the gut microbiota of laboratory mice is related to both genetic and environmental factors, Comp. Med., 60, 336 Huo, 2018, Tph2-/- female mice restore socio-sexual recognition through upregulating ERα and OTR genes in the amygdala, PLoS One, 13, 10.1371/journal.pone.0193395 Im, 2012, Elevated lipopolysaccharide in the colon evokes intestinal inflammation, aggravated in immune modulator-impaired mice, Am. J. Physiol. Gastrointest. Liver Physiol., 303, G490, 10.1152/ajpgi.00120.2012 Jašarević, 2016, Sex differences in the gut microbiome–brain axis across the lifespan, Phil. Trans. Biol. Sci., 371, 10.1098/rstb.2015.0122 Kim, 2020, Sex differences in gut microbiota, World J. Men's Health, 38, 48, 10.5534/wjmh.190009 Kirchoff, 2019, The gut microbiome correlates with conspecific aggression in a small population of rescued dogs (Canis familiaris), PeerJ, 7, 10.7717/peerj.6103 Le Bastard, 2018, Fecal microbiota transplantation reverses antibiotic and chemotherapy-induced gut dysbiosis in mice, Sci. Rep., 8, 6219, 10.1038/s41598-018-24342-x Lee, 2019, Lipopolysaccharide reduces gonadotrophin-releasing hormone (GnRH) gene expression: role of RFamide-related peptide-3 and kisspeptin, Reprod. Fertil. Dev., 31, 1134, 10.1071/RD18277 Lozupone, 2011, UniFrac: an effective distance metric for microbial community comparison, ISME J., 5, 169, 10.1038/ismej.2010.133 MacFabe, 2011, Effects of the enteric bacterial metabolic product propionic acid on object-directed behavior, social behavior, cognition, and neuroinflammation in adolescent rats: relevance to autism spectrum disorder, Behav. Brain Res., 217, 47, 10.1016/j.bbr.2010.10.005 Markle, 2013, Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity, Science, 339, 1084, 10.1126/science.1233521 Martel, 2009, Adult testosterone treatment but not surgical disruption of vomeronasal function augments male-typical sexual behavior in female mice, J. Neurosci.: Off. J. Soc. Neurosci., 29, 7658, 10.1523/JNEUROSCI.1311-09.2009 Martin, 2018, The brain-gut-microbiome Axis, Cell. Mol. Gastroenterol. Hepatol., 6, 133, 10.1016/j.jcmgh.2018.04.003 Mayer, 2014, Gut microbes and the brain: paradigm shift in neuroscience, J. Neurosci.: Off. J. Soc. Neurosci., 34, 15490, 10.1523/JNEUROSCI.3299-14.2014 Menon, 2013, Diet complexity and estrogen receptor β status affect the composition of the murine intestinal microbiota, Appl. Environ. Microbiol., 79, 5763, 10.1128/AEM.01182-13 Moieni, 2018, Effects of inflammation on social processes and implications for health, Ann. N. Y. Acad. Sci., 1428, 5, 10.1111/nyas.13864 Monks, 2018, Non‐neural androgen receptors affect sexual differentiation of brain and behavior, J. Neuroendocrinol., 30, 10.1111/jne.12493 Mucignat-Caretta, 2004, Male urinary chemosignals differentially affect aggressive behavior in male mice, J. Chem. Ecol., 30, 777, 10.1023/B:JOEC.0000028431.29484.d7 Nyangahu, 2018, Disruption of maternal gut microbiota during gestation alters offspring microbiota and immunity, Microbiome, 6, 124, 10.1186/s40168-018-0511-7 O'Connor, 2021, Maternal antibiotic administration during a critical developmental window has enduring neurobehavioral effects in offspring mice, Behav. Brain Res., 404 Org, 2016, Sex differences and hormonal effects on gut microbiota composition in mice, Gut Microb., 7, 313, 10.1080/19490976.2016.1203502 Organski, 2021, Involving the life inside: the complex interplay between reproductive axis hormones and gut microbiota, Curr. Opin. Endocr. Metabol. Res., 20 Phoenix, 1959, Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female Guinea pig, Endocrinology, 65, 369, 10.1210/endo-65-3-369 Popoola, 2014, Effects of tetracycline on testis and testosterone level in adult male Wistar rats, Sch. J. Med., 4, 4 Poulsen, 2021, Standard sample storage conditions have an impact on inferred microbiome composition and antimicrobial resistance patterns, Microbiol. Spectr., 9, 10.1128/Spectrum.01387-21 Reikvam, 2011, Depletion of murine intestinal microbiota: effects on gut mucosa and epithelial gene expression, PLoS One, 6, 10.1371/journal.pone.0017996 Ridlon, 2013, Clostridium scindens: a human gut microbe with a high potential to convert glucocorticoids into androgens, JLR (J. Lipid Res.), 54, 2437, 10.1194/jlr.M038869 Rothrock, 2011, Long-term preservation of anammox bacteria, Appl. Microbiol. Biotechnol., 92, 147, 10.1007/s00253-011-3316-1 Rouyar, 2019, Type 2/Th2-driven inflammation impairs olfactory sensory neurogenesis in mouse chronic rhinosinusitis model, Allergy, 74, 549, 10.1111/all.13559 Sampson, 2016, Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson's disease, Cell, 167, 1469, 10.1016/j.cell.2016.11.018 Schellino, 2016, Opposite-sex attraction in male mice requires testosterone-dependent regulation of adult olfactory bulb neurogenesis, Sci. Rep., 6, 1, 10.1038/srep36063 Schmidt, 2020, Fecal transplant prevents gut dysbiosis and anxiety-like behavior after spinal cord injury in rats, PLoS One, 15, 10.1371/journal.pone.0226128 Scotti, 2008, The role of androgens in the mediation of seasonal territorial aggression in male Siberian hamsters (Phodopus sungorus), Physiol. Behav., 95, 633, 10.1016/j.physbeh.2008.09.009 Segal, 2020, Mechanisms underpinning the efficacy of faecal microbiota transplantation in treating gastrointestinal disease, Therapeutic Adv. Gastroenterol., 13, 10.1177/1756284820946904 Slankster, 2019, Effect of gut microbes on olfactory behavior of Drosophila melanogaster larva, Bios, 90, 227, 10.1893/0005-3155-90.4.227 Swaney, 2012, Sexual experience affects reproductive behavior and preoptic androgen receptors in male mice, Horm. Behav., 61, 472, 10.1016/j.yhbeh.2012.01.001 Swift-Gallant, 2016, Non-neural androgen receptors affect sexual differentiation of the brain and behavior, Endocrinology, 157, 788, 10.1210/en.2015-1355 Sylvia, 2017, Sex-specific modulation of the gut microbiome and behavior in Siberian hamsters, Brain Behav. Immun., 60, 51, 10.1016/j.bbi.2016.10.023 Tetel, 2018, Steroids, stress and the gut microbiome‐brain axis, J. Neuroendocrinol., 30, 10.1111/jne.12548 Thursby, 2017, Introduction to the human gut microbiota, Biochem. J., 474, 1823, 10.1042/BCJ20160510 Tillmann, 2019, Altered fecal microbiota composition in the Flinders sensitive line rat model of depression, Psychopharmacology, 236, 1445, 10.1007/s00213-018-5094-2 Tirelle, 2020, Comparison of different modes of antibiotic delivery on gut microbiota depletion efficiency and body composition in mouse, BMC Microbiol., 20, 340, 10.1186/s12866-020-02018-9 Torabi, 2020, Pro-inflammatory cytokines in the olfactory mucosa result in COVID-19 induced anosmia, ACS Chem. Neurosci., 11, 1909, 10.1021/acschemneuro.0c00249 Ubeda, 2013, Intestinal microbiota containing Barnesiella species cures vancomycin-resistant Enterococcus faecium colonization, Infect. Immun., 81, 965, 10.1128/IAI.01197-12 Wang, 2016, Sex differences in colonization of gut microbiota from a man with short-term vegetarian and inulin-supplemented diet in germ-free mice, Sci. Rep., 6 Wu, 2021, Microbiota regulate social behavior via stress response neurons in the brain, Nature, 595, 409, 10.1038/s41586-021-03669-y Yurkovetskiy, 2013, Gender bias in autoimmunity is influenced by microbiota, Immunity, 39, 400, 10.1016/j.immuni.2013.08.013 Zhu, 2017, Microbiota-gut-brain axis and the central nervous system, Oncotarget, 8, 10.18632/oncotarget.17754 Zuloaga, 2008, Mice with the testicular feminization mutation demonstrate a role for androgen receptors in the regulation of anxiety-related behaviors and the hypothalamic-pituitary-adrenal axis, Horm. Behav., 54, 758, 10.1016/j.yhbeh.2008.08.004