The DOI matches its Crossref record; 60 of the 60 references it cites were found in a registry or an index.
The maternal vaginal microbiome partially mediates the effects of prenatal stress on offspring gut and hypothalamus
Abstract
Early prenatal stress disrupts maternal-to-offspring microbiota transmission and has lasting effects on metabolism, physiology, cognition, and behavior in male mice. Here we show that transplantation of maternal vaginal microbiota from stressed dams into naive pups delivered by cesarean section had effects that partly resembled those seen in prenatally stressed males. However, transplantation of control maternal vaginal microbiota into prenatally stressed pups delivered by cesarean section did not rescue the prenatal-stress phenotype. Prenatal stress was associated with alterations in the fetal intestinal transcriptome and niche, as well as with changes in the adult gut that were altered by additional stress exposure in adulthood. Further, maternal vaginal transfer also partially mediated the effects of prenatal stress on hypothalamic gene expression, as observed after chronic stress in adulthood. These findings suggest that the maternal vaginal microbiota contribute to the lasting effects of prenatal stress on gut and hypothalamus in male mice.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“Furthermore, the transfer of the maternal vaginal microbiota from stressed dams to non-stressed pups is sufficient to alter their response to stress in adulthood (Jasarevic et al., 2018).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Jasarevic et al., 2018
In the citing paper
“In a subsequent study, it was shown that FMT from stressed dams into stress-naïve germ-free mice was sufficient to instill the phenotype observed in stress-exposed offspring (344).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [344]
Citations
Cites
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,893
limma powers differential expression analyses for RNA-sequencing and microarray studies
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., & Smyth, G. K. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv007 · Cited by 40,458
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
Analyzing real-time PCR data by the comparative CT method
Schmittgen, T. D., & Livak, K. J. (2008) · Nature Protocols · doi:10.1038/nprot.2008.73 · Cited by 26,190
Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., et al. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.01541-09 · Cited by 19,549
Near-optimal probabilistic RNA-seq quantification
Bray, N. L., Pimentel, H., Melsted, P., & Pachter, L. (2016) · Nature Biotechnology · doi:10.1038/nbt.3519 · Cited by 9,723
Akira, S., & Takeda, K. (2004) · Nature reviews. Immunology · doi:10.1038/nri1391 · Cited by 8,312
Human gut microbiome viewed across age and geography
Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R. N., Anokhin, A. P., et al. (2012) · Nature · doi:10.1038/nature11053 · Cited by 7,815
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., & Schloss, P. D. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.01043-13 · Cited by 7,246
voom: precision weights unlock linear model analysis tools for RNA-seq read counts
Law, C. W., Chen, Y., Shi, W., & Smyth, G. K. (2014) · Genome Biology · doi:10.1186/gb-2014-15-2-r29 · Cited by 6,155
Cani, P. D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A. M., Delzenne, N. M., & Burcelin, R. (2008) · Diabetes · doi:10.2337/db07-1403 · Cited by 4,819
Dominguez-Bello, M. G., Costello, E. K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., & Knight, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002601107 · Cited by 4,774
Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour
Cryan, J. F., & Dinan, T. G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3346 · Cited by 4,572
Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences
Soneson, C., Love, M. I., & Robinson, M. D. (2015) · F1000Research · doi:10.12688/f1000research.7563.1 · Cited by 3,929
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102999108 · Cited by 3,888
Differential abundance analysis for microbial marker-gene surveys
Paulson, J. N., Stine, O. C., Bravo, H. C., & Pop, M. (2013) · Nature Methods · doi:10.1038/nmeth.2658 · Cited by 2,471
Gut feelings: the emerging biology of gut-brain communication
Mayer, E. A. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3071 · Cited by 1,726
Comparative genomics of the lactic acid bacteria.
Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., Pavlov, A., Pavlova, N., Karamychev, V., Polouchine, N., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607117103 · Cited by 1,391
The maternal microbiota drives early postnatal innate immune development
Gomez de Agüero, M., Ganal-Vonarburg, S. C., Fuhrer, T., Rupp, S., Uchimura, Y., Li, H., Steinert, A., Heikenwalder, M., Hapfelmeier, S., Sauer, U., et al. (2016) · Science · doi:10.1126/science.aad2571 · Cited by 1,231
Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring
Buffington, S. A., Di Prisco, G. V., Auchtung, T. A., Ajami, N. J., Petrosino, J. F., & Costa-Mattioli, M. (2016) · Cell · doi:10.1016/j.cell.2016.06.001 · Cited by 1,163
Control of brain development, function, and behavior by the microbiome
Sampson, T. R., & Mazmanian, S. K. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.04.011 · Cited by 1,093
Microbiota and neurodevelopmental windows: implications for brain disorders
Borre, Y. E., O’Keeffe, G. W., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2014) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.05.002 · Cited by 1,089
Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer
Dominguez-Bello, M. G., De Jesus-Laboy, K. M., Shen, N., Cox, L. M., Amir, A., Gonzalez, A., Bokulich, N. A., Song, S. J., Hoashi, M., Rivera-Vinas, J. I., et al. (2016) · Nature Medicine · doi:10.1038/nm.4039 · Cited by 1,014
Sex-Specific Programming of Offspring Emotionality after Stress Early in Pregnancy
Mueller, B. R., & Bale, T. L. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1424-08.2008 · Cited by 988
Rawls, J. F., Mahowald, M. A., Ley, R. E., & Gordon, J. I. (2006) · Cell · doi:10.1016/j.cell.2006.08.043 · Cited by 978
Early Life Programming and Neurodevelopmental Disorders
Bale, T. L., Baram, T. Z., Brown, A. S., Goldstein, J. M., Insel, T. R., McCarthy, M. M., Nemeroff, C. B., Reyes, T. M., Simerly, R. B., Susser, E. S., et al. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.05.028 · Cited by 961
Bale, T. L., Contarino, A., Smith, G. W., Chan, R. K. W., Gold, L. H., Sawchenko, P. E., Koob, G. F., Vale, W. W., & Lee, K. (2000) · Nature Genetics · doi:10.1038/74263 · Cited by 850
Rodgers, A. B., Morgan, C. P., Bronson, S. L., Revello, S., & Bale, T. L. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.0914-13.2013 · Cited by 814
The neurobiology of stress and gastrointestinal disease
MAYER, E. A. (2000) · Gut · doi:10.1136/gut.47.6.861 · Cited by 666
Ait-Belgnaoui, A., Durand, H., Cartier, C., Chaumaz, G., Eutamene, H., Ferrier, L., Houdeau, E., Fioramonti, J., Bueno, L., & Theodorou, V. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.03.024 · Cited by 612
Deshmukh, H. S., Liu, Y., Menkiti, O. R., Mei, J., Dai, N., O'Leary, C. E., Oliver, P. M., Kolls, J. K., Weiser, J. N., & Worthen, G. S. (2014) · Nature Medicine · doi:10.1038/nm.3542 · Cited by 579
Plaisier, S. B., Taschereau, R., Wong, J. A., & Graeber, T. G. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq636 · Cited by 468
Immunomodulatory mechanisms of lactobacilli
Wells, J. M. (2011) · Microbial Cell Factories · doi:10.1186/1475-2859-10-s1-s17 · Cited by 449
Maternal prenatal stress is associated with the infant intestinal microbiota
Zijlmans, M. A. C., Korpela, K., Riksen-Walraven, J. M., de Vos, W. M., & de Weerth, C. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.01.006 · Cited by 438
Ait‐Belgnaoui, A., Colom, A., Braniste, V., Ramalho, L., Marrot, A., Cartier, C., Houdeau, E., Theodorou, V., & Tompkins, T. (2014) · Neurogastroenterology & Motility · doi:10.1111/nmo.12295 · Cited by 434
Why Is Initial Bacterial Colonization of the Intestine Important to Infants' and Children's Health?
Houghteling, P. D., & Walker, W. A. (2014) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000000597 · Cited by 353
Prenatal Stress Alters Bacterial Colonization of the Gut in Infant Monkeys
Bailey, M. T., Lubach, G. R., & Coe, C. L. (2004) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-200404000-00009 · Cited by 339
Jašarević, E., Howerton, C. L., Howard, C. D., & Bale, T. L. (2015) · Endocrinology · doi:10.1210/en.2015-1177 · Cited by 329
Self-citationSeo, S.-U., Kamada, N., Muñoz-Planillo, R., Kim, Y.-G., Kim, D., Koizumi, Y., Hasegawa, M., Himpsl, S. D., Browne, H. P., Lawley, T. D., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.03.004 · Cited by 318
Sex differences in the gut microbiome–brain axis across the lifespan
Jašarević, E., Morrison, K. E., & Bale, T. L. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0122 · Cited by 307
Bronson, S. L., & Bale, T. L. (2014) · Endocrinology · doi:10.1210/en.2014-1040 · Cited by 299
Golubeva, A. V., Crampton, S., Desbonnet, L., Edge, D., O'Sullivan, O., Lomasney, K. W., Zhdanov, A. V., Crispie, F., Moloney, R. D., Borre, Y. E., et al. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.06.002 · Cited by 283
Kerschensteiner, M., Stadelmann, C., Dechant, G., Wekerle, H., & Hohlfeld, R. (2003) · Annals of Neurology · doi:10.1002/ana.10446 · Cited by 275
Jašarević, E., Howard, C. D., Misic, A. M., Beiting, D. P., & Bale, T. L. (2017) · Scientific Reports · doi:10.1038/srep44182 · Cited by 262
Self-citationEarly prenatal stress impact on coping strategies and learning performance is sex dependent
Mueller, B. R., & Bale, T. L. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.01.017 · Cited by 222
Gur, T. L., Shay, L., Palkar, A. V., Fisher, S., Varaljay, V. A., Dowd, S., & Bailey, M. T. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.12.021 · Cited by 213
Impact of prenatal stress on long term body weight is dependent on timing and maternal sensitivity
MUELLER, B., & Bale, T. L. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.05.019 · Cited by 162
Howerton, C. L., & Bale, T. L. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1401203111 · Cited by 159
Effect of Lactobacilli on Paracellular Permeability in the Gut
Ahrné, S., & Hagslätt, M.-L. J. (2011) · Nutrients · doi:10.3390/nu3010104 · Cited by 157
Intraluminal Containment of Commensal Outgrowth in the Gut during Infection-Induced Dysbiosis
Molloy, M. J., Grainger, J. R., Bouladoux, N. J., Hand, T. W., Koo, L. Y., Naik, S., Quiñones, M., Dzutsev, A., Gao, J., Trinchieri, G., et al. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.08.003 · Cited by 156
Nemeghaire, S., Argudín, M. Á., Feßler, A. T., Hauschild, T., Schwarz, Š., & Butaye, P. (2014) · Veterinary Microbiology · doi:10.1016/j.vetmic.2014.02.005 · Cited by 153
Manipulating the Gut Microbiota: Methods and Challenges: Figure 1
Ericsson, A. C., & Franklin, C. L. (2015) · ILAR Journal · doi:10.1093/ilar/ilv021 · Cited by 140
Analysis of gene–environment interactions in postnatal development of the mammalian intestine
Rakoff-Nahoum, S., Kong, Y., Kleinstein, S. H., Subramanian, S., Ahern, P. P., Gordon, J. I., & Medzhitov, R. M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1424886112 · Cited by 108
Winter, S., & Bäumler, A. J. (2013) · Cellular Microbiology · doi:10.1111/cmi.12245 · Cited by 107
Pankevich, D. E., Mueller, B. R., Brockel, B. J., & Bale, T. L. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.04.015 · Cited by 84
McEuen, J. G., Semsar, K., Lim, M. A., & Bale, T. L. (2009) · Endocrinology · doi:10.1210/en.2008-1721 · Cited by 35
Almirón, M. A., Traglia, G. M., Rubio, A., & Sanjuan, N. A. (2013) · Current Microbiology · doi:10.1007/s00284-013-0367-9 · Cited by 16
Caesarean Section and FosteringPreprint
Nagy, A., Gertsenstein, M., Vintersten, K., & Behringer, R. R. (2006) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot4381 · Cited by 8
Caesarean Section and Fostering
Murphy, D. (2003) · Humana Press eBooks · doi:10.1385/0-89603-245-0:177 · Cited by 8
Bailey (1999) · doi:10.1002/(sici)1098-2302(199909)35:2
Cited by
Sorted by citations
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286
The gut microbiota–brain axis in behaviour and brain disorders
Morais, L. H., Schreiber, H. L., & Mazmanian, S. K. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-020-00460-0 · Cited by 2,149
Maternal immune activation and neuroinflammation in human neurodevelopmental disorders
Han, V. X., Patel, S., Jones, H. F., & Dale, R. C. (2021) · Nature Reviews Neurology · doi:10.1038/s41582-021-00530-8 · Cited by 683
The maternal microbiome modulates fetal neurodevelopment in mice
Vuong, H. E., Pronovost, G. N., Williams, D. W., Coley, E. J. L., Siegler, E. L., Qiu, A., Kazantsev, M., Wilson, C. J., Rendon, T., & Hsiao, E. Y. (2020) · Nature · doi:10.1038/s41586-020-2745-3 · Cited by 564
The impact of the gut microbiota on the reproductive and metabolic endocrine system
Qi, X., Yun, C., Pang, Y., & Qiao, J. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1894070 · Cited by 587
Metadata
- Authors
- Jašarević, E., Howard, C. D., Morrison, K., Misic, A., Weinkopff, T., Scott, P., Hunter, C., Beiting, D., & Bale, T. L.
- Affiliations
- University of Maryland, Baltimore (US)
- University of Pennsylvania (US)
- Corresponding author
- Bale, Tracy L.
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2018-07-09
- Volume
- 21
- Issue
- 8
- Pages
- 1061-1071
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2840355095
- Cited by
- 189
- References
- 60
- Citations by year
- 2026: 12 · 2025: 24 · 2024: 20 · 2023: 26 · 2022: 30 · 2021: 38 · 2020: 18 · 2019: 17 · 2018: 4
- FWCI
- 6.85
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (F32AI114080)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- prenatal stress, microbiota transfer, gut microbiota, hypothalamus, chronic stress, neurodevelopmental disorders, cesarean section, male offspring
- MeSH terms
- Animals, Body Weight, Cesarean Section, Female, Hypothalamo-Hypophyseal System, Hypothalamus, Intestinal Absorption, Male, Mice, Inbred C57BL, Paraventricular Hypothalamic Nucleus, Phenotype, Pregnancy, Prenatal Exposure Delayed Effects, Stress, Psychological, Vagina, Gene Expression, Gastrointestinal Tract, Mice, Transcriptome, Microbiota
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