{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:56:37Z","timestamp":1787028997362,"version":"build-2736575974"},"reference-count":108,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2026,5,22]],"date-time":"2026-05-22T00:00:00Z","timestamp":1779408000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000071","name":"Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["1R03HD114968-01A1"],"award-info":[{"award-number":["1R03HD114968-01A1"]}],"id":[{"id":"10.13039\/100000071","id-type":"DOI","asserted-by":"publisher"}]},{"award":["1R03HD114968-01A1"],"award-info":[{"award-number":["1R03HD114968-01A1"]}],"id":[{"id":"https:\/\/ror.org\/04byxyr05","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007165","name":"University of Missouri","doi-asserted-by":"publisher","award":["Research Council Grant"],"award-info":[{"award-number":["Research Council Grant"]}],"id":[{"id":"10.13039\/100007165","id-type":"DOI","asserted-by":"publisher"}]},{"award":["Research Council Grant"],"award-info":[{"award-number":["Research Council Grant"]}],"id":[{"id":"https:\/\/ror.org\/02ymw8z06","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/100015509","name":"Missouri Department of Health and Senior Services","doi-asserted-by":"publisher","award":["#AOC23380006"],"award-info":[{"award-number":["#AOC23380006"]}],"id":[{"id":"10.13039\/100015509","id-type":"DOI","asserted-by":"publisher"}]},{"award":["#AOC23380006"],"award-info":[{"award-number":["#AOC23380006"]}],"id":[{"id":"https:\/\/ror.org\/041qkag73","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"U.S. National Science Foundation","doi-asserted-by":"crossref","award":["OAC-2232889"],"award-info":[{"award-number":["OAC-2232889"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"crossref"}]},{"award":["OAC-2232889"],"award-info":[{"award-number":["OAC-2232889"]}],"id":[{"id":"https:\/\/ror.org\/021nxhr62","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["P20GM103434"],"award-info":[{"award-number":["P20GM103434"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"award":["P20GM103434"],"award-info":[{"award-number":["P20GM103434"]}],"id":[{"id":"https:\/\/ror.org\/04q48ey07","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Probiotic supplements are increasingly being touted to have health benefits for pregnant women consuming such supplements and their unborn offspring. The placenta is in direct communication with maternal blood, and bioactive agents can thus easily be transferred to this organ where they may influence gene expression by the different trophoblast (TB) cell lineages. The underlying hypothesis assessed herein is that maternal probiotic supplementation can influence the placenta and fetal brain. The composition of bacterial short-chain fatty acids (SCFAs) was examined in fecal boli of mouse dams on a maternal probiotic supplement relative to control dams. Further, SCFA and transcriptomic profiles were examined in placenta and fetal brain from conceptuses derived from dams on the probiotic supplement and conceptuses from control dams. While this treatment did not affect bacterial SCFAs, placenta and fetal brain changes were evident in male and female conceptuses carried by dams receiving probiotics relative to controls. For the placenta, females were more sensitive to maternal probiotic supplementation, whereas the opposite was the case for the fetal brain. Slc6a4 showed increased expression in female placenta from probiotic-treated dams, which could enhance uptake of maternal 5-HT. Male placenta from probiotic-treated dams had dramatic reduction in Hsd11b2 that may render them more vulnerable to maternal stress. In the fetal brain, maternal probiotic supplementation was associated with genes linked to forebrain development, suggesting this treatment might impact life-long neurobehavioral responses. Current studies suggest that maternal probiotic supplementation might lead to adverse changes in the placenta and fetal brain of their unborn children.<\/jats:p>","DOI":"10.3390\/microorganisms14061175","type":"journal-article","created":{"date-parts":[[2026,5,22]],"date-time":"2026-05-22T16:06:08Z","timestamp":1779465968000},"page":"1175","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Susceptibility of the Placenta and Fetal Brain to Maternal Probiotic Supplementation"],"prefix":"10.3390","volume":"14","author":[{"given":"Rosalind T. B.","family":"Herrington","sequence":"first","affiliation":[{"name":"Pathobiology and Integrative Biomedical Sciences, University of Missouri, Columbia, MO 65211, USA"},{"name":"Biological Sciences, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhen","family":"Lyu","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, Joan C. Edwards School of Medicine, Marshall University, Huntington, WV 25703, USA"},{"name":"Christopher S. Bond Life Science Center, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David T.","family":"Ellenberger","sequence":"additional","affiliation":[{"name":"Pathobiology and Integrative Biomedical Sciences, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nathan J.","family":"Bivens","sequence":"additional","affiliation":[{"name":"Genomics Technology Core Facility, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhentian","family":"Lei","sequence":"additional","affiliation":[{"name":"University of Missouri Metabolomics Center, University of Missouri, Columbia, MO 65211, USA"},{"name":"Biochemistry, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tanhaul","family":"Islam","sequence":"additional","affiliation":[{"name":"University of Missouri Metabolomics Center, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4086-663X","authenticated-orcid":false,"given":"Lloyd W.","family":"Sumner","sequence":"additional","affiliation":[{"name":"University of Missouri Metabolomics Center, University of Missouri, Columbia, MO 65211, USA"},{"name":"Biochemistry, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0008-6559","authenticated-orcid":false,"given":"R. Michael","family":"Roberts","sequence":"additional","affiliation":[{"name":"Biochemistry, University of Missouri, Columbia, MO 65211, USA"},{"name":"Animal Sciences, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8944-4924","authenticated-orcid":false,"given":"Trupti","family":"Joshi","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, Joan C. Edwards School of Medicine, Marshall University, Huntington, WV 25703, USA"},{"name":"Christopher S. Bond Life Science Center, University of Missouri, Columbia, MO 65211, USA"},{"name":"Department of Electrical Engineering and Computer Science, University of Missouri, Columbia, MO 65201, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4137-3933","authenticated-orcid":false,"given":"Cheryl S.","family":"Rosenfeld","sequence":"additional","affiliation":[{"name":"Pathobiology and Integrative Biomedical Sciences, University of Missouri, Columbia, MO 65211, USA"},{"name":"MU Institute for Data Science and Informatics, University of Missouri, Columbia, MO 65211, USA"},{"name":"Department of Genetics Area Program, University of Missouri, Columbia, MO 65211, USA"},{"name":"Thompson Center for Autism and Neurobehavioral Disorders, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,5,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1007\/s00431-015-2618-1","article-title":"Maternal use of probiotics during pregnancy and effects on their offspring\u2019s health in an unselected population","volume":"175","author":"Rutten","year":"2016","journal-title":"Eur. J. Pediatr."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1017\/S0007114519003374","article-title":"Effect of probiotic supplementation in pregnant women: A meta-analysis of randomised controlled trials","volume":"123","author":"Kuang","year":"2020","journal-title":"Br. J. Nutr."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"17796","DOI":"10.1038\/s41598-020-74773-8","article-title":"Improvement of glucose metabolism in pregnant women through probiotic supplementation depends on gestational diabetes status: Meta-analysis","volume":"10","author":"Malinowska","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"3479","DOI":"10.1039\/D3FO04456D","article-title":"Comparison of the effectiveness of probiotic supplementation in glucose metabolism, lipid profile, inflammation and oxidative stress in pregnant women","volume":"15","author":"Li","year":"2024","journal-title":"Food Funct."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"8388","DOI":"10.1039\/D1FO04333A","article-title":"Effects of probiotic supplementation on glucose metabolism in pregnant women without diabetes: A systematic review and meta-analysis","volume":"13","author":"Zhang","year":"2022","journal-title":"Food Funct."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"614","DOI":"10.2174\/1389201017666160401145817","article-title":"Nutraceuticals as Lipid-Lowering Treatment in Pregnancy and Their Effects on the Metabolic Syndrome","volume":"17","author":"Nikolic","year":"2016","journal-title":"Curr. Pharm. Biotechnol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1381","DOI":"10.1007\/s00404-021-06023-9","article-title":"Dietary supplementation for gestational diabetes prevention and management: A meta-analysis of randomized controlled trials","volume":"303","author":"Chan","year":"2021","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e14033","DOI":"10.1111\/ijcp.14033","article-title":"Nutrients that modulate gestational diabetes mellitus: A systematic review of cohort studies Jan 2019\u2013Jan 2020","volume":"75","author":"Machairiotis","year":"2021","journal-title":"Int. J. Clin. Pract."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e24326","DOI":"10.1002\/jcla.24326","article-title":"The effect of probiotics on gestational diabetes and its complications in pregnant mother and newborn: A systematic review and meta-analysis during 2010\u20132020","volume":"36","author":"Teymouri","year":"2022","journal-title":"J. Clin. Lab. Anal."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Obuchowska, A., Gorczyca, K., Standy\u0142o, A., Obuchowska, K., Kimber-Trojnar, \u017b., Wierzchowska-Opoka, M., and Leszczy\u0144ska-Gorzelak, B. (2022). Effects of probiotic supplementation during pregnancy on the future maternal risk of metabolic syndrome. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23158253"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Taylor, B.L., Woodfall, G.E., Sheedy, K.E., O\u2019Riley, M.L., Rainbow, K.A., Bramwell, E.L., and Kellow, N.J. (2017). Effect of probiotics on metabolic outcomes in pregnant women with gestational diabetes: A systematic review and meta-analysis of randomized controlled trials. Nutrients, 9.","DOI":"10.3390\/nu9050461"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"772","DOI":"10.3109\/14767058.2012.755166","article-title":"Probiotics in pregnancy and maternal outcomes: A systematic review","volume":"26","author":"Lindsay","year":"2013","journal-title":"J. Matern. Fetal Neonatal Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"04038","DOI":"10.7189\/jogh.13.04038","article-title":"Impact of probiotic on anxiety and depression symptoms in pregnant and lactating women and microbiota of infants: A systematic review and meta-analysis","volume":"13","author":"Halemani","year":"2023","journal-title":"J. Glob. Health"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Movaghar, R., Abbasalizadeh, S., Vazifekhah, S., Farshbaf-Khalili, A., and Shahnazi, M. (2024). The effects of synbiotic supplementation on blood pressure and other maternal outcomes in pregnant mothers with mild preeclampsia: A triple-blinded randomized controlled trial. BMC Womens Health, 24.","DOI":"10.1186\/s12905-024-02922-6"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2623","DOI":"10.1007\/s43032-023-01206-y","article-title":"Protective effect of Akkermansia muciniphila on the preeclampsia-like mouse model","volume":"30","author":"Liu","year":"2023","journal-title":"Reprod. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e018021","DOI":"10.1136\/bmjopen-2017-018021","article-title":"Timing of probiotic milk consumption during pregnancy and effects on the incidence of preeclampsia and preterm delivery: A prospective observational cohort study in Norway","volume":"8","author":"Nordqvist","year":"2018","journal-title":"BMJ Open"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1093\/aje\/kwr168","article-title":"Intake of probiotic food and risk of preeclampsia in primiparous women: The Norwegian Mother and Child Cohort Study","volume":"174","author":"Brantsaeter","year":"2011","journal-title":"Am. J. Epidemiol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Perna, A., Venditti, N., Merolla, F., Fusco, S., Guerra, G., Zoroddu, S., De Luca, A., and Bagella, L. (2024). Nutraceuticals in pregnancy: A special focus on probiotics. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25179688"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/S0963-9969(01)00171-5","article-title":"Introduction to pre- and probiotics","volume":"35","author":"Holzapfel","year":"2002","journal-title":"Food Res. Int."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"532","DOI":"10.1093\/biolre\/ioz204","article-title":"Placental serotonin signaling, pregnancy outcomes, and regulation of fetal brain development","volume":"102","author":"Rosenfeld","year":"2020","journal-title":"Biol. Reprod."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Rosenfeld, C.S. (2021). Transcriptomics and other omics approaches to investigate effects of xenobiotics on the placenta. Front. Cell Dev. Biol., 9.","DOI":"10.3389\/fcell.2021.723656"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1002\/jnr.24603","article-title":"The placenta-brain-axis","volume":"99","author":"Rosenfeld","year":"2021","journal-title":"J. Neurosci. Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1093\/biolre\/ioad146","article-title":"Extracellular vesicles from mouse trophoblast cells: Effects on neural progenitor cells and potential participants in the placenta-brain Axis","volume":"110","author":"Kinkade","year":"2023","journal-title":"Biol. Reprod."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1909","DOI":"10.2217\/epi-2021-0339","article-title":"miRNA changes in the mouse placenta due to bisphenol A exposure","volume":"13","author":"Mao","year":"2021","journal-title":"Epigenomics"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Kinkade, J.A., Singh, P., Verma, M., Khan, T., Ezashi, T., Bivens, N.J., Roberts, R.M., Joshi, T., and Rosenfeld, C.S. (2024). Small and long non-coding RNA analysis for human trophoblast-derived extracellular vesicles and their effect on the transcriptome profile of human neural progenitor cells. Cells, 13.","DOI":"10.3390\/cells13221867"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1093\/biolre\/ioaf041","article-title":"Maternal probiotic supplementation and effects on the fetal placenta","volume":"112","author":"Herrington","year":"2025","journal-title":"Biol. Reprod."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"e2108581119","DOI":"10.1073\/pnas.2108581119","article-title":"Modifying the maternal microbiota alters the gut-brain metabolome and prevents emotional dysfunction in the adult offspring of obese dams","volume":"119","author":"Probert","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"348","DOI":"10.1111\/j.1365-2222.2007.02671.x","article-title":"Perinatal maternal application of Lactobacillus rhamnosus GG suppresses allergic airway inflammation in mouse offspring","volume":"37","author":"Sel","year":"2007","journal-title":"Clin. Exp. Allergy"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Schabussova, I., Hufnagl, K., Tang, M.L., Hoflehner, E., Wagner, A., Loupal, G., Nutten, S., Zuercher, A., Mercenier, A., and Wiedermann, U. (2012). Perinatal maternal administration of Lactobacillus paracasei NCC 2461 prevents allergic inflammation in a mouse model of birch pollen allergy. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0040271"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e1052","DOI":"10.52225\/narra.v4i3.1052","article-title":"Probiotic-rich fermented milk from Lactiplantibacillus plantarum IIA-1A5: Effects on pregnancy health in the animal model","volume":"4","author":"Sukma","year":"2024","journal-title":"Narra J."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1007\/s00018-022-04379-y","article-title":"Maternal gut microbiota Bifidobacterium promotes placental morphogenesis, nutrient transport and fetal growth in mice","volume":"79","author":"Schofield","year":"2022","journal-title":"Cell Mol. Life Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"e2426341122","DOI":"10.1073\/pnas.2426341122","article-title":"Effects of the gut microbiota on placental angiogenesis and intrauterine growth in gnotobiotic mice","volume":"122","author":"Coskun","year":"2025","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Husso, A., Pessa-Morikawa, T., Koistinen, V.M., K\u00e4rkk\u00e4inen, O., Kwon, H.N., Lahti, L., Iivanainen, A., Hanhineva, K., and Niku, M. (2023). Impacts of maternal microbiota and microbial metabolites on fetal intestine, brain, and placenta. BMC Biol., 21.","DOI":"10.1186\/s12915-023-01709-9"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1159\/000339182","article-title":"Probiotics modulate host-microbe interaction in the placenta and fetal gut: A randomized, double-blind, placebo-controlled trial","volume":"102","author":"Rautava","year":"2012","journal-title":"Neonatology"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Mantaring, J., Benyacoub, J., Destura, R., Pecquet, S., Vidal, K., Volger, S., and Guinto, V. (2018). Effect of maternal supplement beverage with and without probiotics during pregnancy and lactation on maternal and infant health: A randomized controlled trial in the Philippines. BMC Pregnancy Childbirth, 18.","DOI":"10.1186\/s12884-018-1828-8"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"109565","DOI":"10.1016\/j.neuropharm.2023.109565","article-title":"Live or heat-killed probiotic administration reduces anxiety and central cytokine expression in BALB\/c mice, but differentially alters brain neurotransmitter gene expression","volume":"235","author":"Chan","year":"2023","journal-title":"Neuropharmacology"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1016\/j.physbeh.2010.04.001","article-title":"Repetitive orogastric gavage affects the phenotype of diet-induced obese mice","volume":"100","author":"Le","year":"2010","journal-title":"Physiol. Behav."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/j.taap.2012.01.025","article-title":"A less stressful alternative to oral gavage for pharmacological and toxicological studies in mice","volume":"260","author":"Walker","year":"2012","journal-title":"Toxicol. Appl. Pharmacol."},{"key":"ref_39","first-page":"79","article-title":"Consequences of oral gavage during gestation and lactation on rat dams and the neurodevelopment and behavior of their offspring","volume":"56","author":"Kleefeld","year":"2017","journal-title":"J. Am. Assoc. Lab. Anim. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1186\/1476-069X-13-46","article-title":"Should oral gavage be abandoned in toxicity testing of endocrine disruptors?","volume":"13","author":"Vandenberg","year":"2014","journal-title":"Environ. Health"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e108","DOI":"10.1111\/epi.13392","article-title":"Effects of valproic acid on the placental barrier in the pregnant mouse: Optical imaging and transporter expression studies","volume":"57","author":"Meir","year":"2016","journal-title":"Epilepsia"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1016\/j.placenta.2020.08.006","article-title":"Maternal oxycodone treatment causes pathophysiological changes in the mouse placenta","volume":"100","author":"Green","year":"2020","journal-title":"Placenta"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"4642","DOI":"10.1073\/pnas.1919563117","article-title":"Bisphenol A and bisphenol S disruptions of the mouse placenta and potential effects on the placenta-brain axis","volume":"117","author":"Mao","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"5557","DOI":"10.1073\/pnas.1000440107","article-title":"Contrasting effects of different maternal diets on sexually dimorphic gene expression in the murine placenta","volume":"107","author":"Mao","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1016\/j.placenta.2020.06.019","article-title":"Brain and placental transcriptional responses as a readout of maternal and paternal preconception stress are fetal sex specific","volume":"100","author":"Chan","year":"2020","journal-title":"Placenta"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1093\/biolre\/ioad156","article-title":"Maternal preconception stress produces sex-specific effects at the maternal:fetal interface to impact offspring development and phenotypic outcomes","volume":"110","author":"Montgomery","year":"2024","journal-title":"Biol. Reprod."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2555","DOI":"10.1038\/s41467-018-04992-1","article-title":"Placental H3K27me3 establishes female resilience to prenatal insults","volume":"9","author":"Nugent","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"111661","DOI":"10.1016\/j.biopha.2021.111661","article-title":"Role of microbiota-derived short-chain fatty acids in nervous system disorders","volume":"139","author":"Mirzaei","year":"2021","journal-title":"Biomed. Pharmacother."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1210\/en.2011-1457","article-title":"A novel antiinflammatory role for the short-chain fatty acids in human labor","volume":"153","author":"Voltolini","year":"2012","journal-title":"Endocrinology"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Wang, S., Liu, Y., Qin, S., and Yang, H. (2022). Composition of maternal circulating short-chain fatty acids in gestational diabetes mellitus and their associations with placental metabolism. Nutrients, 14.","DOI":"10.3390\/nu14183727"},{"key":"ref_51","first-page":"123","article-title":"Propionate reduces the cytokine-induced VCAM-1 and ICAM-1 expression by inhibiting nuclear factor-kappa B (NF-kappaB) activation","volume":"60","author":"Naruszewicz","year":"2009","journal-title":"J. Physiol. Pharmacol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"5549","DOI":"10.3748\/wjg.15.5549","article-title":"Short-chain fatty acids act as antiinflammatory mediators by regulating prostaglandin E(2) and cytokines","volume":"15","author":"Cox","year":"2009","journal-title":"World J. Gastroenterol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1282","DOI":"10.1038\/nature08530","article-title":"Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43","volume":"461","author":"Maslowski","year":"2009","journal-title":"Nature"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2398","DOI":"10.2337\/db14-1213","article-title":"Short-chain fatty acids protect against high-fat diet-induced obesity via a PPAR\u03b3-dependent switch from lipogenesis to fat oxidation","volume":"64","author":"Bleeker","year":"2015","journal-title":"Diabetes"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"2611","DOI":"10.1002\/mnfr.201600305","article-title":"Importance of propionate for the repression of hepatic lipogenesis and improvement of insulin sensitivity in high-fat diet-induced obesity","volume":"60","author":"Weitkunat","year":"2016","journal-title":"Mol. Nutr. Food Res."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1045","DOI":"10.1073\/pnas.2637002100","article-title":"Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41","volume":"101","author":"Xiong","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"319","DOI":"10.4142\/jvs.2011.12.4.319","article-title":"Butyrate regulates leptin expression through different signaling pathways in adipocytes","volume":"12","author":"Soliman","year":"2011","journal-title":"J. Vet. Sci."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Nankova, B.B., Agarwal, R., MacFabe, D.F., and La Gamma, E.F. (2014). Enteric bacterial metabolites propionic and butyric acid modulate gene expression, including CREB-dependent catecholaminergic neurotransmission, in PC12 cells\u2014Possible relevance to autism spectrum disorders. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0103740"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1038\/nature09972","article-title":"A transient placental source of serotonin for the fetal forebrain","volume":"472","author":"Bonnin","year":"2011","journal-title":"Nature"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.neuroscience.2011.10.005","article-title":"Fetal, maternal, and placental sources of serotonin and new implications for developmental programming of the brain","volume":"197","author":"Bonnin","year":"2011","journal-title":"Neuroscience"},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Velasquez, J.C., Goeden, N., and Bonnin, A. (2013). Placental serotonin: Implications for the developmental effects of SSRIs and maternal depression. Front. Cell Neurosci., 7.","DOI":"10.3389\/fncel.2013.00047"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1111\/jnc.14928","article-title":"Enteric short-chain fatty acids promote proliferation of human neural progenitor cells","volume":"154","author":"Yang","year":"2020","journal-title":"J. Neurochem."},{"key":"ref_63","unstructured":"Andrews, S. (2026, March 16). FastQC: A Quality Control Tool for High Throughput Sequence Data. Available online: https:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc\/."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1038\/s41587-019-0201-4","article-title":"Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype","volume":"37","author":"Kim","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1038\/nbt.1621","article-title":"Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation","volume":"28","author":"Trapnell","year":"2010","journal-title":"Nat. Biotechnol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1093\/bioinformatics\/btt688","article-title":"RNA-seq differential expression studies: More sequence or more replication?","volume":"30","author":"Liu","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1007\/978-1-61779-839-9_16","article-title":"Computational analysis of RNA-seq","volume":"883","author":"Givan","year":"2012","journal-title":"Methods Mol. Biol."},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Ellenberger, D.T., Lyu, Z., Herrington, R.T.B., Kinkade, J.A., Leone, G.W., Sze, J.Y., Bivens, N.J., Baker, R.F., Roberts, R.M., and Joshi, T. (2025). Disruption of the placenta-brain axis in transgenic mice lacking serotonin transporter (SERT) in trophoblast cells. Int. J. Mol. Sci., 27.","DOI":"10.3390\/ijms27010436"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1109\/MCSE.2007.55","article-title":"Matplotlib: A 2D graphics environment","volume":"9","author":"Hunter","year":"2007","journal-title":"Comput. Sci. Eng."},{"key":"ref_70","first-page":"2825","article-title":"Scikit-learn: Machine Learning in Python","volume":"12","author":"Pedregosa","year":"2011","journal-title":"J. Mach. Learn. Res."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"10732","DOI":"10.1039\/D4FO01684J","article-title":"Lacticaseibacillus paracasei 207-27 alters the microbiota-gut-brain axis to improve wearable device-measured sleep duration in healthy adults: A randomized, double-blind, placebo-controlled trial","volume":"15","author":"Li","year":"2024","journal-title":"Food Funct."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"974","DOI":"10.1186\/s12967-025-06950-0","article-title":"Butyric acid and valeric acid attenuate stress-induced ferroptosis and depressive-like behaviors by suppressing hippocampal neuroinflammation","volume":"23","author":"Ma","year":"2025","journal-title":"J. Transl. Med."},{"key":"ref_73","unstructured":"Wei, T.S.V. (2026, March 16). R Package \u2018corrplot\u2019: Visualization of a Correlation Matrix. (Version 0.95). Available online: https:\/\/github.com\/taiyun\/corrplot."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Susiarjo, M., Sasson, I., Mesaros, C., and Bartolomei, M.S. (2013). Bisphenol a exposure disrupts genomic imprinting in the mouse. PLoS Genet., 9.","DOI":"10.1371\/journal.pgen.1003401"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1966","DOI":"10.1093\/bioinformatics\/bty890","article-title":"TissueEnrich: Tissue-specific gene enrichment analysis","volume":"35","author":"Jain","year":"2019","journal-title":"Bioinformatics"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"156608","DOI":"10.1016\/j.cyto.2024.156608","article-title":"Multi-species synbiotic supplementation increased fecal short chain fatty acids and anti-inflammatory cytokine interleukin-10 in adult men with dyslipidemia; A randomized, double-blind, clinical trial","volume":"179","author":"Salamat","year":"2024","journal-title":"Cytokine"},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Ting\u00f6, L., Hutchinson, A.N., Bergh, C., Stiefvatter, L., Schweinlin, A., Jensen, M.G., Kr\u00fcger, K., Bischoff, S.C., and Brummer, R.J. (2022). Potential modulation of inflammation by probiotic and omega-3 supplementation in elderly with chronic low-grade inflammation-a randomized, placebo-controlled trial. Nutrients, 14.","DOI":"10.3390\/nu14193998"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"132","DOI":"10.3109\/00365529609094568","article-title":"Short-chain fatty acids in the human colon: Relation to gastrointestinal health and disease","volume":"216","author":"Mortensen","year":"1996","journal-title":"Scand. J. Gastroenterol. Suppl."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1152\/physrev.2001.81.3.1031","article-title":"Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides","volume":"81","author":"Topping","year":"2001","journal-title":"Physiol. Rev."},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Vanderpeet, C.L., Dorey, E.S., Neal, E.S., Mullins, T., McIntyre, D.H., Callaway, L.K., Barrett, H.L., Dekker Nitert, M., and Cuffe, J.S.M. (2025). Dietary fibre modulates gut microbiota in late pregnancy without altering SCFA Levels, and propionate treatement has no effect on placental explant function. Nutrients, 17.","DOI":"10.3390\/nu17071234"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"eadk1887","DOI":"10.1126\/sciadv.adk1887","article-title":"The maternal microbiome promotes placental development in mice","volume":"9","author":"Pronovost","year":"2023","journal-title":"Sci. Adv."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1016\/j.placenta.2014.04.009","article-title":"Expression of short chain fatty acid receptors and pro-inflammatory cytokines in utero-placental tissues is altered in cows developing retention of fetal membranes","volume":"35","author":"Boro","year":"2014","journal-title":"Placenta"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1006\/dbio.2002.0773","article-title":"Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta","volume":"250","author":"Adamson","year":"2002","journal-title":"Dev. Biol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/j.ydbio.2006.03.006","article-title":"Post-implantation mouse conceptuses produce paracrine signals that regulate the uterine endometrium undergoing decidualization","volume":"294","author":"Bany","year":"2006","journal-title":"Dev. Biol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"816","DOI":"10.4161\/epi.28703","article-title":"Epigenetic regulation of the placental HSD11B2 barrier and its role as a critical regulator of fetal development","volume":"9","author":"Togher","year":"2014","journal-title":"Epigenetics"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1530\/ror.0.0020129","article-title":"Placental 11 beta-hydroxysteroid dehydrogenase: Barrier to maternal glucocorticoids","volume":"2","author":"Yang","year":"1997","journal-title":"Rev. Reprod."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1212","DOI":"10.1016\/j.placenta.2015.09.011","article-title":"Placental 11\u03b2-Hydroxysteroid dehydrogenase type 2 expression: Correlations with birth weight and placental metal concentrations","volume":"36","author":"Mikelson","year":"2015","journal-title":"Placenta"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1038\/ncpendmet0515","article-title":"Mechanisms of disease: Glucocorticoids, their placental metabolism and fetal \u2018programming\u2019 of adult pathophysiology","volume":"3","author":"Seckl","year":"2007","journal-title":"Nat. Clin. Pract. Endocrinol. Metab."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"1287","DOI":"10.1210\/en.2008-1100","article-title":"Altered placental function of 11beta-hydroxysteroid dehydrogenase 2 knockout mice","volume":"150","author":"Wyrwoll","year":"2009","journal-title":"Endocrinology"},{"key":"ref_90","doi-asserted-by":"crossref","unstructured":"Marsit, C.J., Maccani, M.A., Padbury, J.F., and Lester, B.M. (2012). Placental 11-beta hydroxysteroid dehydrogenase methylation is associated with newborn growth and a measure of neurobehavioral outcome. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0033794"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1609","DOI":"10.1210\/en.2017-03025","article-title":"Pathway of maternal serotonin to the human embryo and fetus","volume":"159","author":"Kliman","year":"2018","journal-title":"Endocrinology"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"730","DOI":"10.1093\/biolre\/ioaf141","article-title":"Effects of selective serotonin reuptake inhibitors on the placenta","volume":"113","author":"Ellenberger","year":"2025","journal-title":"Biol. Reprod."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.placenta.2021.09.021","article-title":"Placental Changes in the serotonin transporter (Slc6a4) knockout mouse suggest a role for serotonin in controlling nutrient acquisition","volume":"115","author":"Mao","year":"2021","journal-title":"Placenta"},{"key":"ref_94","doi-asserted-by":"crossref","unstructured":"Andonotopo, W., Bachnas, M.A., Dewantiningrum, J., Pramono, M.B.A., Sanjaya, I.N.H., Darmawan, E., Akbar, M.I.A., Aldiansyah, D., Yeni, C.M., and Bernolian, N. (2025). The intrauterine microbiome-neurodevelopment axis: Decoding the prenatal microbial imprint on lifelong mental health. J. Perinat. Med.","DOI":"10.1515\/jpm-2025-0242"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.1038\/nbt.3353","article-title":"A catalog of the mouse gut metagenome","volume":"33","author":"Xiao","year":"2015","journal-title":"Nat. Biotechnol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/j.chom.2021.12.003","article-title":"The mouse gastrointestinal bacteria catalogue enables translation between the mouse and human gut microbiotas via functional mapping","volume":"30","author":"Forster","year":"2022","journal-title":"Cell Host Microbe"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1111\/j.1439-0531.2012.02051.x","article-title":"Effects of maternal diet and exposure to bisphenol A on sexually dimorphic responses in conceptuses and offspring","volume":"47","author":"Rosenfeld","year":"2012","journal-title":"Reprod. Domest. Anim."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"3422","DOI":"10.1210\/en.2015-1227","article-title":"Sex-specific placental responses in fetal development","volume":"156","author":"Rosenfeld","year":"2015","journal-title":"Endocrinology"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1093\/ilar.53.3-4.253","article-title":"Sexually selected traits: A fundamental framework for studies on behavioral epigenetics","volume":"53","author":"Geary","year":"2012","journal-title":"ILAR J."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/j.yhbeh.2012.09.009","article-title":"Sex and dose-dependent effects of developmental exposure to bisphenol A on anxiety and spatial learning in deer mice (Peromyscus maniculatus bairdii) offspring","volume":"63","author":"Williams","year":"2013","journal-title":"Horm. Behav."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"104890","DOI":"10.1016\/j.yhbeh.2020.104890","article-title":"Disruption of global hypothalamic microRNA (miR) profiles and associated behavioral changes in California mice (Peromyscus californicus) developmentally exposed to endocrine disrupting chemicals","volume":"128","author":"Kaur","year":"2021","journal-title":"Horm. Behav."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1523\/ENEURO.0150-21.2021","article-title":"Maternal oxycodone treatment results in neurobehavioral disruptions in mice offspring","volume":"8","author":"Martin","year":"2021","journal-title":"eNeuro"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1002\/jnr.23896","article-title":"Sex-dependent differences in voluntary physical activity","volume":"95","author":"Rosenfeld","year":"2017","journal-title":"J. Neurosci. Res."},{"key":"ref_104","doi-asserted-by":"crossref","unstructured":"Shay, D.A., Vieira-Potter, V.J., and Rosenfeld, C.S. (2018). Sexually dimorphic effects of aromatase on neurobehavioral responses. Front. Mol. Neurosci., 11.","DOI":"10.3389\/fnmol.2018.00374"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"104719","DOI":"10.1016\/j.yhbeh.2020.104719","article-title":"Changes in nucleus accumbens gene expression accompany sex-specific suppression of spontaneous physical activity in aromatase knockout mice","volume":"121","author":"Shay","year":"2020","journal-title":"Horm. Behav."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"e01714","DOI":"10.1002\/brb3.1714","article-title":"Pre-Gestational intake of Lactobacillus helveticus NS8 has anxiolytic effects in adolescent Sprague Dawley offspring","volume":"10","author":"Niu","year":"2020","journal-title":"Brain Behav."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"48","DOI":"10.14715\/cmb\/2024.70.6.8","article-title":"Maternal and filial consumption of probiotics protects from acute stress-induced anxiety and loss of benevolent gut microbes","volume":"70","author":"Wali","year":"2024","journal-title":"Cell. Mol. Biol."},{"key":"ref_108","doi-asserted-by":"crossref","unstructured":"Rosenfeld, C.S. (2024). Placenta extracellular vesicles: Messengers connecting maternal and fetal systems. Biomolecules, 14.","DOI":"10.3390\/biom14080995"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/14\/6\/1175\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,24]],"date-time":"2026-05-24T04:12:19Z","timestamp":1779595939000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/14\/6\/1175"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,5,22]]},"references-count":108,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2026,6]]}},"alternative-id":["microorganisms14061175"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms14061175","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,5,22]]}}}