Cited by 250Genetics and Neurodevelopmental DisordersBirth, Development, and HealthMaternal Mental Health During Pregnancy and Postpartum

The DOI matches its Crossref record; 86 of the 86 references it cites were found in a registry or an index.

The placenta and neurodevelopment: sex differences in prenatal vulnerability

Open access

Bale, Tracy L.·2016·Dialogues in Clinical Neuroscience

DOI 10.31887/dcns.2016.18.4/tbalePMC PMC5286731

Open this paper in CoChat — free account

Abstract

Prenatal insults, such as maternal stress, are associated with an increased neurodevelopmental disease risk and impact males significantly more than females, including increased rates of autism, mental retardation, stuttering, dyslexia, and attention deficit/hyperactivity disorder (ADHD). Sex differences in the placenta, which begin with sex chromosomes, are likely to produce sex-specific transplacental signals to the developing brain. Our studies and others have identified X-linked genes that are expressed at higher levels in the female placenta. Through a genome-wide screen after maternal stress in mice, we identified the X-linked gene O-linked N-acetylglucosamine transferase (OGT) and demonstrated its causality in neurodevelopmental programming producing a male-specific stress phenotype. Elucidating the sex-specific molecular mechanisms involved in transplacental signals that impact brain development is key to understanding the sex bias in neurodevelopmental disorders and is expected to yield novel insight into disease risk and resilience.

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

Crossref · 10.31887/dcns.2016.18.4/tbale

Cites

86 of 86 references verified0 citation errors · 0 not checkable

Statistics

Figure 1 Schematic illustrating the chromatin regulation and transcriptional control by O-linked N-acetylgluosamine transferase (OGT). For transcriptional silencing, OGT controls protein stability of EZH2, the H3K27me3 methyltransferase. Utx is a H3K27me3 demethylase. Increased OGT positively correlates with levels of H3K27me3 and transcriptional repression. EZH2, enhancer of zeste homolog 2; H3, histone H3; K27, lysine 27; Me, methyl; OGT, O-linked N-acetylgluosamine transferase; Utx, a histone H3-lysine 27 demethylaseCC BY-NC-ND · PubMed Central

Figure 2 Summary illustration of the hypothesis regarding sex differences in chromatin regulation via O-linked N-acetylgluosamine transferase (OGT) and its regulation of the repressive histone mark H3K27me3 that may underlie the male bias for neurodevelopmental disorders. The increased expression of the X-linked gene OGT, in the female placenta provides them with a starting point from which a reduction due to a prenatal insult, such as maternal stress (orange lightning bolt), still affords significantly higher female OGT levels than found in males. Maternal insults can promote widespread transcriptional changes in male placentas (blue) but relatively little in female tissue due to differences in transcriptional repression (pink). The increased H3K27me3 levels in female placentas may then promote sex differences in transcriptional responses and, ultimately, placental function in response to early prenatal stress, placing males at an increased risk for neurodevelopmental disorders stemming from prenatal insults. EPS, early prenatal stress; H3K27me3, histone H3 trimethylated at lysine 27; Neurodev, neurodevopmental disorder; OGT, O-linked N-acetylgluosamine transferase; XX, female; XY, male.CC BY-NC-ND · PubMed Central

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cerebral Lateralization
Geschwind, N. (1985) · Archives of Neurology · doi:10.1001/archneur.1985.04060060019009 · Cited by 1,773
Cerebral Lateralization
Geschwind, N. (1985) · Archives of Neurology · doi:10.1001/archneur.1985.04060050026008 · Cited by 1,452
Placental development: Lessons from mouse mutants
Rossant, J., & Cross, J. C. (2001) · Nature Reviews Genetics · doi:10.1038/35080570 · Cited by 1,299
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
Self-citation
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
Self-citation
Postnatal disappearance of the pregnancy-associated reduced sensitivity of plasma cortisol to feedback inhibition
Owens, P. C., Smith, R., Brinsmead, M. W., Hall, C., Foureur, M. J., Hurt, D., Lovelock, M., Chan, E.-C., Cubis, J., & Lewin, T. J. (1987) · Life Sciences · doi:10.1016/0024-3205(87)90603-5 · Cited by 958
Review: Sex and the human placenta: Mediating differential strategies of fetal growth and survival
Clifton, V. L. (2010) · Placenta · doi:10.1016/j.placenta.2009.11.010 · Cited by 868
The association between prenatal stress and infant birth weight and gestational age at birth: a prospective investigation
Wadhwa, P. D., Sandman, C. A., Porto, M., Dunkel-Schetter, C., & Garite, T. J. (1993) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(93)90016-c · Cited by 794
Why are autism spectrum conditions more prevalent in males?
Baron-Cohen, S., Lombardo, M. V., Auyeung, B., Ashwin, E., Chakrabarti, B., & Knickmeyer, R. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001081 · Cited by 754
Mechanisms of Disease: glucocorticoids, their placental metabolism and fetal 'programming' of adult pathophysiology
Seckl, J. R., & Holmes, M. C. (2007) · Nature Clinical Practice Endocrinology & Metabolism · doi:10.1038/ncpendmet0515 · Cited by 754

Show all 86 references

Research works printed but not linked: 8

Sandman CA., 2013, J Psychosom Res., 75, 327, 10.1016/j.jpsychores.2013.07.009 · DOI · Paper page
Gabory A., 2013, Biol Sex Differ., 4, 5, 10.1186/2042-6410-4-5 · DOI · Paper page
Howerton CL., 2014, Proc Natl Acad Sci U S A., 111, 9639, 10.1073/pnas.1401203111 · DOI
Howerton CL., 2013, Proc Natl Acad Sci USA., 110, 5169, 10.1073/pnas.1300065110 · DOI
Mao J., 2010, Proc Natl Acad Sci U S A., 107, 5557, 10.1073/pnas.1000440107 · DOI · Paper page
Nugent BM., 2015, Front Neuroendocrinol., 39, 28, 10.1016/j.yfrne.2015.09.001 · DOI · Paper page
Bronson SL., 2016, Neuropsychopharmacology., 41, 207, 10.1038/npp.2015.231 · DOI
Nyirenda MJ., 1998, Int J Mol Med., 2, 607

Sorted by citations

Prenatal developmental origins of future psychopathology: mechanisms and pathways
Monk, C., Lugo-Candelas, C., & Trumpff, C. (2019) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050718-095539 · Cited by 388
“…there is an extended critical period of prenatal vulnerability—as an explanatory model; another lead considers hormone exposure, especially to testosterone, given its role of organizing sexual variation in the developing brain and association with risk of neurodevelopmental disease (Bale 2016).”
BackgroundInfluential
Sex and gender differences in developmental programming of metabolism
Dearden, L., Bouret, S. G., & Ozanne, S. E. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.04.007 · Cited by 353
Maternal prenatal stress phenotypes associate with fetal neurodevelopment and birth outcomes
Walsh, K., McCormack, C. A., Webster, R., Pinto, A., Lee, S., Feng, T., Krakovsky, H. S., O’Grady, S. M., Tycko, B., Champagne, F. A., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1905890116 · Cited by 273
Parental Advisory: Maternal and Paternal Stress Can Impact Offspring Neurodevelopment
Chan, J. C., Nugent, B. M., & Bale, T. L. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.005 · Cited by 241
“During pregnancy, maternal stress alters the maternal milieu, which can directly or indirectly impact fetal development (3,4).”
BackgroundSelf-citation
IL-6 and IL-8: An Overview of Their Roles in Healthy and Pathological Pregnancies
Vilotić, A., Nacka-Aleksić, M., Pirković, A., Bojić‐Trbojević, Ž., Dekanski, D., & Krivokuća, M. J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232314574 · Cited by 271
Sex Differences in Immunity to Viral Infections
Jacobsen, H., & Klein, S. L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.720952 · Cited by 246
Maternal Cortisol Concentrations During Pregnancy and Sex-Specific Associations With Neonatal Amygdala Connectivity and Emerging Internalizing Behaviors
Graham, A. M., Rasmussen, J. M., Entringer, S., Ben Ward, E., Rudolph, M. D., Gilmore, J. H., Styner, M., Wadhwa, P. D., Fair, D. A., & Buss, C. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.023 · Cited by 203
Sex Differences in Vulnerability to Prenatal Stress: a Review of the Recent Literature
Sutherland, S. L., & Brunwasser, S. M. (2018) · Current Psychiatry Reports · doi:10.1007/s11920-018-0961-4 · Cited by 194
Male sex bias in early and late onset neurodevelopmental disorders: Shared aspects and differences in Autism Spectrum Disorder, Attention Deficit/hyperactivity Disorder, and Schizophrenia
Santos, S., Ferreira, H., Martins, J., Gonçalves, J., & Castelo-Branco, M. S. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104577 · Cited by 148
“Interestingly, it has been shown that sex chromosome genes mediate transcription regulation, affecting transplacental signalling, resulting in differential responses to maternal insults that can culminate in neurodevelopmental disorders (Bale, 2016).”
Background
The cortisol switch between vulnerability and resilience
de Kloet, E. R., & Joëls, M. (2023) · Molecular Psychiatry · doi:10.1038/s41380-022-01934-8 · Cited by 161
“Coping of females, by contrast, seems to involve a more pro-social strategy, analogous to the human ‘ tend to befriend ’ [178 – 181].”
Gender Specific Differences in Disease Susceptibility: The Role of Epigenetics
Migliore, L., Nicolì, V., & Stoccoro, A. (2021) · Biomedicines · doi:10.3390/biomedicines9060652 · Cited by 120
“Placenta function is also influenced by fetal sex, and placental sex seems to be a major determinant in the magnitude and functional responses of the placenta to perturbations during pregnancy [101].”
Background
Maternal obesity and the impact of associated early-life inflammation on long-term health of offspring
Denizli, M., Capitano, M. L., & Kua, K. L. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.940937 · Cited by 125
“Significantly decreased levels ofOGTand its controloverH3K27me3 in themale placenta predisposes male chromatin to be in a reactive state and more vulnerable to maternal stress (Bale, 2016).”
Background
Bridging autism spectrum disorders and schizophrenia through inflammation and biomarkers – pre-clinical and clinical investigations
Prata, J., Santos, S. G., Almeida, M. I., Coelho, R., & Barbosa, M. A. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0938-y · Cited by 115
Placental programming of neuropsychiatric disease
Kratimenos, P., & Penn, A. A. (2019) · Pediatric Research · doi:10.1038/s41390-019-0405-9 · Cited by 115
Prenatal environmental risk factors for autism spectrum disorder and their potential mechanisms
Love, C., Sominsky, L., O’Hely, M., Berk, M., Vuillermin, P., & Dawson, S. L. (2024) · BMC Medicine · doi:10.1186/s12916-024-03617-3 · Cited by 110
“Mouse and human studies indicate that placental immune responses may occur in a sex-specific manner in response to maternal stressors, potentially mediated by hormonal disruptions and consequently influencing neurodevelopmental outcomes [104, 105].”
Background
A Review on the Vagus Nerve and Autonomic Nervous System During Fetal Development: Searching for Critical Windows
Cerritelli, F., Frasch, M. G., Antonelli, M. C., Viglione, C., Vecchi, S., Chiera, M., & Manzotti, A. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.721605 · Cited by 108
“A dysregulation in CRH production, secondary to various maternal conditions, such as hypoxia, increased inflammatory cytokines and glucocorticoids, stress, preeclampsia, and eclampsia, may lead to altered neurodevelopmental patterns of these fetal structures (Allen, 2001; Bale, 2016; Sheng et al., 2020).”
BackgroundInfluential
Maternal-fetal cross-talk via the placenta: influence on offspring development and metabolism
Kramer, A. C., Jansson, T., Bale, T. L., & Powell, T. L. (2023) · Development · doi:10.1242/dev.202088 · Cited by 119
Self-citation
Treating the placenta to prevent adverse effects of gestational hypoxia on fetal brain development
Phillips, T. J., Scott, H., Menassa, D. A., Bignell, A. L., Sood, A., Morton, J. S., Akagi, T., Azuma, K., Rogers, M. F., Gilmore, C. E., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-06300-1 · Cited by 97
Sex differences in major depression and comorbidity of cardiometabolic disorders: impact of prenatal stress and immune exposures
Goldstein, J. M., Hale, T. M., Foster, S. L., Tobet, S. A., & Handa, R. J. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0146-1 · Cited by 98
Prenatal lead exposure impacts cross-hemispheric and long-range connectivity in the human fetal brain
Thomason, M. E., Hect, J. L., Rauh, V. A., Trentacosta, C., Wheelock, M. D., Eggebrecht, A. T., Espinoza-Heredia, C., & Burt, S. A. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.02.017 · Cited by 94
“Indeed, it is well recognized that males and females demonstrate variation in sensitivity and vulnerability to insults in early development (Bale, 2016; Barnett and Scaramella, 2013; G oes et al., 2015; Whitfield et al., 1997).”
Maternal immune activation-induced PPARγ-dependent dysfunction of microglia associated with neurogenic impairment and aberrant postnatal behaviors in offspring
Zhao, Q., Wang, Q., Wang, J., Tang, M.-M., Huang, S., Peng, K., Han, Y., Zhang, J., Liu, G., Fang, Q., et al. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.01.005 · Cited by 87
Placental Macrophages: A Window Into Fetal Microglial Function in Maternal Obesity
Edlow, A. G., Glass, R. M., Smith, C. J. W., Tran, P. K., James, K. E., & Bilbo, S. D. (2018) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2018.11.004 · Cited by 82
“As the interface between the maternal and fetal environments and the source of fetal nutrition, the placenta has been implicated in developmental programming (Jansson and Powell 2007), including of the developing fetal brain (Hsiao and Patterson 2012; Bale 2016; Bronson and Bale 2016).”
BackgroundInfluential
Canada’s Colonial Genocide of Indigenous Peoples: A Review of the Psychosocial and Neurobiological Processes Linking Trauma and Intergenerational Outcomes
Matheson, K., Seymour, A. M., Landry, J., Ventura, K., Arsenault, E., & Anisman, H. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19116455 · Cited by 111
“These epigenetic effects could involve actions related to diverse biological processes, and particular attention has been devoted to those that influence or reflect stress reactivity (HPA functioning) and emotionality in offspring [125].”
Background
Nutrient‐driven O‐Glc NA c in proteostasis and neurodegeneration
Akan, I., Stichelen, S. O.-V., Bond, M. R., & Hanover, J. A. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14242 · Cited by 84
“Several studies suggest that maternal stress increases the risk of neurodevelopmental diseases including autism, stuttering, dyslexia, and attention deficit/hyperactivity disorder and that males are more significantly affected than females (reviewed in Bale 2016).”
Background
Epigenome-wide DNA methylation in placentas from preterm infants: association with maternal socioeconomic status
Junior, H. P. D. O. S., Bhattacharya, A., Martin, E. M., Addo, K., Psioda, M., Smeester, L., Joseph, R. M., Hooper, S. R., Frazier, J. A., Kuban, K., et al. (2019) · Epigenetics · doi:10.1080/15592294.2019.1614743 · Cited by 82
“Elucidating the sex-specific mechanisms involved in transplacental signals could lead to novel insights into disease risk and resilience related to early life adversity [47,48].”
Background
Fetal brain and placental programming in maternal obesity: A review of human and animal model studies
Shook, L. L., Kışlal, S., & Edlow, A. G. (2020) · Prenatal Diagnosis · doi:10.1002/pd.5724 · Cited by 88
“ways to maternal stressors, which differentially impact the developing male and female fetal brains.(132) Decreased expression of X-linked genes in male placentas, placental production of sex hormones, and”
Background
Microglia along sex lines: From brain colonization, maturation and function, to implication in neurodevelopmental disorders
Bordeleau, M., Carrier, M., Luheshi, G. N., & Tremblay, M.-È. (2019) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2019.06.001 · Cited by 75
Effects of prenatal exposure to a mixture of organophosphate flame retardants on placental gene expression and serotonergic innervation in the fetal rat brain
Rock, K. D., St Armour, G., Horman, B., Phillips, A., Ruis, M., Stewart, A. K., Jima, D., Muddiman, D. C., Stapleton, H. M., & Patisaul, H. B. (2020) · Toxicological Sciences · doi:10.1093/toxsci/kfaa046 · Cited by 69
“Placental function is environmentally responsive and sex-specific, with placental sex (XX vs XY) determining many aspects of placental development and function (Bale, 2016; Konkel, 2016; Nugent and Bale, 2015).”
Background
Sex Differences Are Here to Stay: Relevance to Prenatal Care
Inkster, A. M., Fernández-Boyano, I., & Robinson, W. P. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10133000 · Cited by 67
Sex modifies placental gene expression in response to metabolic and inflammatory stress
Barke, T. L., Money, K. M., Du, L., Serezani, A. P. M., GANNON, M. A., Mirnics, K., & Aronoff, D. M. (2019) · Placenta · doi:10.1016/j.placenta.2019.02.008 · Cited by 62
Maternal Prenatal Mood, Pregnancy-Specific Worries, and Early Child Psychopathology: Findings From the DREAM BIG Consortium
Székely, E., Neumann, A., Sallis, H., Jolicoeur‐Martineau, A., Verhulst, F. C., Meaney, M. J., Pearson, R. M., Levitan, R. D., Kennedy, J. L., Lydon, J. E., et al. (2020) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2020.02.017 · Cited by 63
Perinatal exposure to maternal obesity: Lasting cardiometabolic impact on offspring
Kışlal, S., Shook, L. L., & Edlow, A. G. (2020) · Prenatal Diagnosis · doi:10.1002/pd.5784 · Cited by 62
Mineralocorticoid receptor and glucocorticoid receptor work alone and together in cell-type-specific manner: Implications for resilience prediction and targeted therapy
Daskalakis, N. P., Meijer, O. C., & de Kloet, E. R. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100455 · Cited by 64
“ticoid secretion pattern and signaling in response to an acute stressor, taking also into account the sex difference (Bale, 2016; Kokras et al., 2021; Kroon et al., 2020; Quinn et al., 2014).”
Influential
EDC IMPACT: Molecular effects of developmental FM 550 exposure in Wistar rat placenta and fetal forebrain
Rock, K. D., Horman, B. M., Phillips, A. L., McRitchie, S., Watson, S. L., Deese-Spruill, J., Jima, D. D., Sumner, S., Stapleton, H. M., & Patisaul, H. B. (2018) · Endocrine Connections · doi:10.1530/ec-17-0373 · Cited by 55
“For example, the fetal side of the placenta is the sole source of 5-HT for the developing forebrain from GD 10–15 (5, 6).”
BackgroundInfluential
Maternal stressors and the developmental origins of neuropsychiatric risk
Khambadkone, S. G., Cordner, Z. A., & Tamashiro, K. L. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2020.100834 · Cited by 61
“Studies across a variety of maternal insults have revealed sexually dimorphic placental responses to stressors (Bronson and Bale, 2016; Davis and Pfaff, 2014; Sandman et al., 2013; Mao et al., 2010; Howerton et al., 2013; Bronson and Bale, 2014; Dunn et al., 2011; Gabory et al., 2013; Clifton,…”
BackgroundInfluential
Maternal overnutrition induces long-term cognitive deficits across several generations
Sarker, G., & Peleg-Raibstein, D. (2018) · Nutrients · doi:10.3390/nu11010007 · Cited by 52
Cortisol levels versus self-report stress measures during pregnancy as predictors of adverse infant outcomes: a systematic review
Caparrós-González, R. A., Lynn, F. A., Alderdice, F. A., & Peralta‐Ramírez, M. I. (2022) · Stress · doi:10.1080/10253890.2022.2059348 · Cited by 53
“This finding is in line with a previous study reporting a higher impact of prenatal stress on male infants, including higher rates of dyslexia and autism (Bale, 2016).”
Result
Gender-based research underscores sex differences in biological processes, clinical disorders and pharmacological interventions
Bernstein, S. R., Kelleher, C., & Khalil, R. A. (2023) · Biochemical Pharmacology · doi:10.1016/j.bcp.2023.115737 · Cited by 55
Sex difference of pre- and post-natal exposure to six developmental neurotoxicants on intellectual abilities: a systematic review and meta-analysis of human studies
Goodman, C. V., Green, R. R., DaCosta, A., Flora, D. B., Lanphear, B. P., & Till, C. (2023) · Environmental Health · doi:10.1186/s12940-023-01029-z · Cited by 56
“This pattern is consistently seen in response to exposure to prenatal stress [107].”
Background
Sexual Dimorphism in the Age of Genomics: How, When, Where
Deegan, D. F., & Engel, N. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00186 · Cited by 54
“Moreover, male and female embryos exhibit different susceptibilities to environmental factors during early gestation (Jenkins et al., 2007; Gabory et al., 2012; Bale, 2016; Bansal et al., 2017).”
Background
Cohort profile: the ECHO prenatal and early childhood pathways to health consortium (ECHO-PATHWAYS)
LeWinn, K. Z., Karr, C. J., Hazlehurst, M. F., Carroll, K. N., Loftus, C. T., Nguyen, R. H. N., Barrett, E. S., Swan, S. H., Szpiro, A. A., Paquette, A. G., et al. (2022) · BMJ Open · doi:10.1136/bmjopen-2022-064288 · Cited by 54
Cellular stress mechanisms of prenatal maternal stress: Heat shock factors and oxidative stress
Dowell, J., Elser, B. A., Schroeder, R. E., & Stevens, H. E. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2019.134368 · Cited by 51
“Furthermore, given that the placenta consists of cells of both embryonic and maternal origin, sex differences in placental function are present throughout gestation, mediating sex-specific responses to maternal stress [13, 161].”
Background
Prenatal pregnancy-related anxiety predicts boys’ ADHD symptoms via placental C-reactive protein
Shao, S., Wang, J., Huang, K., Wang, S., Liu, H., Wan, S., Yan, S., Hao, J., Zhu, P., & Tao, F. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104797 · Cited by 50
Examining Sex Differences in the Human Placental Transcriptome During the First Fetal Androgen Peak
Braun, A. E., Muench, K. L., Robinson, B. G., Wang, A., Palmer, T. D., & Winn, V. D. (2020) · Reproductive Sciences · doi:10.1007/s43032-020-00355-8 · Cited by 55
Chronic maternal interleukin-17 and autism-related cortical gene expression, neurobiology, and behavior
Gumusoglu, S. B., Hing, B. W. Q., Chilukuri, A. S. S., Dewitt, J. J., Scroggins, S. M., & Stevens, H. E. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0640-0 · Cited by 49
“In early development, placental sex differences influence the brain [50].”
Background
The public reception of putative epigenetic mechanisms in the transgenerational effects of trauma
Yehuda, R., Lehrner, A. L., & Bierer, L. M. (2018) · Current Zoology · doi:10.1093/eep/dvy018 · Cited by 51
The Contribution of Inflammation to Autism Spectrum Disorders: Recent Clinical Evidence
Prata, J., Machado, A. S., von Doellinger, O., Almeida, M. I., Barbosa, M. A., Coelho, R. C., & Santos, S. G. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9554-7_29 · Cited by 47
Placental genomic risk scores and early neurodevelopmental outcomes
Ursini, G., Punzi, G., Langworthy, B., Chen, Q., Xia, K., Cornea, E. A., Goldman, B. D., Styner, M. A., Knickmeyer, R. C., Gilmore, J. H., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2019789118 · Cited by 46
A cross-cohort analysis of autosomal DNA methylation sex differences in the term placenta
Inkster, A. M., Yuan, V., Konwar, C., Matthews, A., Brown, C. J., & Robinson, W. P. (2021) · Biology of Sex Differences · doi:10.1186/s13293-021-00381-4 · Cited by 46
Maternal prenatal cortisol programs the infant hypothalamic–pituitary–adrenal axis
Irwin, J. L., Meyering, A. L., Peterson, G., Glynn, L. M., Sandman, C. A., Hicks, L. M., & Davis, E. P. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.105106 · Cited by 48
Exposure to Prenatal Stress Is Associated With an Excitatory/Inhibitory Imbalance in Rat Prefrontal Cortex and Amygdala and an Increased Risk for Emotional Dysregulation
Marchisella, F., Creutzberg, K. C., Begni, V., Sanson, A., Wearick‐Silva, L. E., Tractenberg, S. G., Orso, R., Kestering-Ferreira, É., Grassi‐Oliveira, R., & Riva, M. A. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.653384 · Cited by 50
“However, sex-specific neurobehavioral outcomes have been reported for rodents and humans (for reviews, see Weinstock, 2007; Bale, 2016).”
Background
Pathogenic Infections during Pregnancy and the Consequences for Fetal Brain Development
Jash, S., & Sharma, S. (2022) · Pathogens · doi:10.3390/pathogens11020193 · Cited by 48
Transmission of the adverse consequences of childhood maltreatment across generations: Focus on gestational biology
Moog, N. K., Heim, C. C., Entringer, S., Simhan, H. N., Wadhwa, P. D., & Buß, C. (2022) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2022.173372 · Cited by 49
“The placenta shows variation in magnitude and functional response to maternal perturbations depending on fetal (and placental) sex (Bale, 2016).”
Background
Extracellular vesicles are dynamic regulators of maternal glucose homeostasis during pregnancy
Zierden, H. C., Marx-Rattner, R., Rock, K. D., Montgomery, K. R., Anastasiadis, P., Folts, L. M., & Bale, T. L. (2023) · Scientific Reports · doi:10.1038/s41598-023-31425-x · Cited by 42
Self-citation
Sex Differences in Early Embryogenesis: Inter‐Chromosomal Regulation Sets the Stage for Sex‐Biased Gene Networks
Engel, N. (2018) · BioEssays · doi:10.1002/bies.201800073 · Cited by 41
Methods for Evaluating the Combined Effects of Chemical and Nonchemical Exposures for Cumulative Environmental Health Risk Assessment
Payne-Sturges, D., Scammell, M. K., Levy, J. I., Cory‐Slechta, D. A., Symanski, E., Shmool, J. L. C., Laumbach, R. J., Linder, S. H., & Clougherty, J. E. (2018) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph15122797 · Cited by 43
Altered offspring neurodevelopment in an arginine vasopressin preeclampsia model
Gumusoglu, S. B., Chilukuri, A. S. S., Hing, B. W. Q., Scroggins, S. M., Kundu, S., Sandgren, J. A., Santillan, M. K. O., Santillan, D. A., Grobe, J. L., & Stevens, H. E. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01205-0 · Cited by 39
Sex Differences in Pancreatic β-Cell Physiology and Glucose Homeostasis in C57BL/6J Mice
Jo, S., Beetch, M., Gustafson, E. C., Wong, A., Oribamise, E. I., Chung, G., Vadrevu, S., Satin, L. S., Bernal‐Mizrachi, E., & Alejandro, E. U. (2023) · Journal of the Endocrine Society · doi:10.1210/jendso/bvad099 · Cited by 38
“…mechanisms bestowed to the developing fetus to differential responses of the placenta and gonadal hormones during and following puberty, which may all impose lasting epigenetic changes and hormone-driven cellular signaling responses in different organs and physiology between sexes [9, 56].”
Background
Post-translational histone modifications and their interaction with sex influence normal brain development and elaboration of neuropsychiatric disorders
Singh, G., Singh, V., & Schneider, J. S. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.10.016 · Cited by 38
Chromosomal and environmental contributions to sex differences in the vulnerability to neurological and neuropsychiatric disorders: Implications for therapeutic interventions
Pallier, P. N., Ferrara, M., Romagnolo, F., Ferretti, M. T., Soreq, H., & Cerase, A. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102353 · Cited by 37
“…in-utero developmental perturbations than females (Clifton, 2010; Eriksson et al., 2010) could be because their brain develops more slowly than that of females, placing them at increased vulnerability to adverse challenges over a relatively longer period than females during gestation (Bale, 2016).”
Background
Maternal oxycodone treatment causes pathophysiological changes in the mouse placenta
Green, M. T., Martin, R. E., Kinkade, J. A., Schmidt, R., Bivens, N. J., Tuteja, G., Mao, J., & Rosenfeld, C. S. (2020) · Placenta · doi:10.1016/j.placenta.2020.08.006 · Cited by 34
“We, and others, have shown that by mounting robust placental gene expression changes in response to maternal challenges, including high fat diet or stress, females demonstrate later resistance to behavioral changes relative to male counterparts [12, 26, 64-66].”
Background
Sexual Dimorphism of the Heart: Genetics, Epigenetics, and Development
Deegan, D. F., Nigam, P., & Engel, N. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.668252 · Cited by 37
Maternal Stress and Coping Strategies in Developmental Dyslexia: An Italian Multicenter Study
Carotenuto, M., Messina, A., Monda, V., Precenzano, F., Iacono, D., Verrotti, A., Piccorossi, A., Gallai, B., Roccella, M., Parisi, L., et al. (2017) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2017.00295 · Cited by 33
Impact of early term and late preterm birth on infants’ neurodevelopment: evidence from a cohort study in Wuhan, China
Chen, Z., Xiong, C., Liu, H., Duan, J., Kang, C., Yao, C., Chen, K., Chen, Y., Liu, Y., Liu, M., et al. (2022) · BMC Pediatrics · doi:10.1186/s12887-022-03312-3 · Cited by 33
“Prior studies have shown that fetal gender may play an essential role in regulating the influence of prenatal exposure on neurodevelopment [41, 42].”
Background
The Prenatal Hormone Milieu in Autism Spectrum Disorder
Worsham, W., Dalton, S., & Bilder, D. A. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.655438 · Cited by 29
“, hyperglycemia, insulin insensitivity) could influence the sex-differential observed in ASD (20).”
Background
Associations of Maternal Prenatal Stress and Depressive Symptoms With Childhood Neurobehavioral Outcomes in the ECHO Cohort of the NICHD Fetal Growth Studies: Fetal Growth Velocity as a Potential Mediator
Babineau, V., Fonge, Y. N., Miller, E. S., Grobman, W. A., Ferguson, P. L., Hunt, K. J., Vena, J. E., Newman, R., Guille, C., Tita, A., et al. (2022) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2022.03.021 · Cited by 31
“In addition to finding associations between prenatal stress and depressive symptoms with multiple interrelated domains of child neurobehavior, we also corroborate prior evidence of biological male vulnerability to prenatal adversity.(31,50) Prenatal depressive symptoms, but not prenatal stress, were associated with ob…”
Result
O-GlcNAc: Regulator of Signaling and Epigenetics Linked to X-linked Intellectual Disability
Konzman, D., Abramowitz, L. K., Steenackers, A., Mukherjee, M., Na, H., & Hanover, J. A. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.605263 · Cited by 31
“Interestingly, a recent hypothesis to explain the malebiased presentation of neurodevelopmental diseases focuses on sex differences in the placenta in relaying signals to the developing brain regarding maternal perturbations (Charil et al., 2010; Howerton and Bale, 2012, 2014; Gabory et al., 2013; Howerton et al., 201…”
Background
Human Placental Adaptive Changes in Response to Maternal Obesity: Sex Specificities
Santos, E. D., Hernández, M. H., Serazin-Leroy, V., Vialard, F., & Dieudonné, M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24119770 · Cited by 29
“More specifically, reduced OGT expression could result in male placentas having less of the histone repressive mark H3K2me3 and, thus, being more vulnerable to modifications of the maternal environmental [92,93].”
Background
Fish Oil Supplementation in Pregnancy and Neurodevelopment in Childhood—A Randomized Clinical Trial
Sass, L., Bjarnadóttir, E., Stokholm, J., Chawes, B., Vinding, R., Mora‐Jensen, A. C., Thorsen, J., Nørgaard, S. K., Ebdrup, B. H., Jepsen, J. R. M., et al. (2021) · Child Development · doi:10.1111/cdev.13541 · Cited by 29
Sex differences in the effects of prematurity and/or low birthweight on neurodevelopmental outcomes: systematic review and meta-analyses
Christians, J. K., Ahmadzadeh-Seddeighi, S., Bilal, A., Bogdanovic, A., Ho, R., Leung, E. V., MacGregor, M. A., Nadasdy, N. M., & Principe, G. M. (2023) · Biology of Sex Differences · doi:10.1186/s13293-023-00532-9 · Cited by 34
“Some studies have suggested increased male vulnerability in long-term behavioral and cognitive outcomes [15, 19, 20, 22, 23], and so we focused on such outcomes measured at 1 year of age or older, including assessments of abilities relating to language (including reading and speech), behaviour, memory, learning, think…”
Background
What risk factors for Developmental Language Disorder can tell us about the neurobiological mechanisms of language development
Boerma, T., ter Haar, S. M., Ganga, R., Wijnen, F. N. K., Blom, E., & Wierenga, C. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105398 · Cited by 36
“…at greater risk for neurodevelopmental cognitive deficits, including (persisting) language delays and being diagnosed with DLD, compared to females (Bale, 2016; Cheuk and Wong, 2005; Dale et al., 2003; Harrison and McLeod, 2010; Law et al., 2009; Mossabeb et al., 2012; Prathanee et al., 2007;…”
Maternal Lifetime Trauma and Birthweight: Effect Modification by In Utero Cortisol and Child Sex
Flom, J. D., Chiu, Y.-H. M., Hsu, H. L., Devick, K. L., Brunst, K. J., Campbell, R. K., Enlow, M. B., Coull, B. A., & Wright, R. J. (2018) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2018.07.069 · Cited by 31
“Our results are consistent with literature showing that males are more susceptible to effects of in utero stress and stress correlates on fetal growth.(31,57) For example, Thayer et al found that elevated maternal cortisol levels assessed before conception disproportionately impacted fetal growth in boys.”
The Placenta’s Role in Sexually Dimorphic Fetal Growth Strategies
Christians, J. K. (2021) · Reproductive Sciences · doi:10.1007/s43032-021-00780-3 · Cited by 31
Sex-based differences in placental DNA methylation profiles related to gestational age: an NIH ECHO meta-analysis
Bulka, C. M., Everson, T. M., Burt, A., Marsit, C. J., Karagas, M. R., Boyle, K. E., Niemiec, S., Kechris, K. J., Davidson, E., Yang, I. V., et al. (2023) · Epigenetics · doi:10.1080/15592294.2023.2179726 · Cited by 29
“After birth, male infants are also more likely than females to exhibit morbidities, including respiratory distress and neurological impairments [32–35]; it has been posited that the pathogenesis of these conditions originates in utero and is influenced by the placenta [36, 37].”
Background
Associations between maternal prenatal cortisol and fetal growth are specific to infant sex: findings from the Wirral Child Health and Development Study
Braithwaite, E., Hill, J., Pickles, A. R., Glover, V. A. S., O’Donnell, K. J., & Sharp, H. M. (2018) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174418000181 · Cited by 28
“Fetal sex is a key determinant in the functional responses of the placenta to maternal perturbations during pregnancy.(51) Sex differences in placental mechanisms are evident throughout gestation, and therefore could provide a plausible mechanism by which the maternal milieu could have sexdependent effects on fetal gr…”
Background
Sex differences in early and term placenta are conserved in adult tissues
Olney, K. C., Plaisier, S. B., Phung, T. N., Silasi, M., Perley, L. E., O’Bryan, J., Ramirez, L., Kliman, H. J., & Wilson, M. A. (2022) · Biology of Sex Differences · doi:10.1186/s13293-022-00470-y · Cited by 27
“…genes such as O-linked N-acetylglucosamine transferase (OGT), which is expressed at a higher level in XX females because it escapes X chromosome inactivation, leading to increased histone methylation and decreased gene expression thought to provide a neuroprotective state in females (Bale, 2016).”
Background
Prenatal Risk for Autism Spectrum Disorder (ASD): Fetal Cortisol Exposure Predicts Child ASD Symptoms
Ram, S., Howland, M. A., Sandman, C. A., Davis, E. P., & Glynn, L. M. (2018) · Clinical Psychological Science · doi:10.1177/2167702618811079 · Cited by 28
Associations of urinary non-persistent endocrine disrupting chemical biomarkers with early-to-mid pregnancy plasma sex-steroid and thyroid hormones
Ryva, B. A., Pacyga, D. C., Anderson, K. Y., Calafat, A. M., Whalen, J., Aung, M. T., Gardiner, J. C., Braun, J. M., Schantz, S. L., & Strakovsky, R. S. (2024) · Environment International · doi:10.1016/j.envint.2024.108433 · Cited by 27
“Additionally, other studies have shown that male placentas are more responsive to stressors than female placentas (Bale, 2016; Bronson and Bale, 2016; Eriksson et al., 2010).”
Result
Pregnant women with bipolar disorder who have a history of childhood maltreatment: Intergenerational effects of trauma on fetal neurodevelopment and birth outcomes
Babineau, V., McCormack, C. A., Feng, T., Lee, S., Berry, O. O., Knight, B. T., Newport, D. J., Stowe, Z. N., & Monk, C. E. (2022) · Bipolar Disorders · doi:10.1111/bdi.13207 · Cited by 26
“54 Evidence for intergenerational transmission of maternal CM via prenatal programming was specific to birth outcomes only.”
Sex-dependence and comorbidities of the early-life adversity induced mental and metabolic disease risks: Where are we at?
Reemst, K., Ruigrok, S. R., Bleker, L. S., Naninck, E. F. G., Ernst, T. R., Kotah, J. M., Lucassen, P. J., Roseboom, T. J., Pollux, B. J. A., de Rooij, S. R., et al. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104627 · Cited by 26
Association between prenatal antibiotic exposure and autism spectrum disorder among term births: A population‐based cohort study
Nitschke, A. S., do Valle, H. A., Vallance, B. A., Bickford, C., Ip, A., Lanphear, N. E., Lanphear, B. P., Weikum, W., Oberlander, T. F., & Hanley, G. E. (2023) · Paediatric and Perinatal Epidemiology · doi:10.1111/ppe.12972 · Cited by 28
A novel murine model to study the impact of maternal depression and antidepressant treatment on biobehavioral functions in the offspring
Scarborough, J., Mueller, F. S., Weber‐Stadlbauer, U., Mattei, D., Opitz, L., Cattaneo, A., & Richetto, J. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01145-7 · Cited by 25
“The sex-specific programming of behavioral abnormalities observed here is in line with the findings from other rodent models of gestational stress exposure [86] and may be explained by a differential susceptibility of male and female placental functions to prenatal perturbations, with male placentas being more vulnera…”
Result
Association between placental toxic metal exposure and NICU Network Neurobehavioral Scales (NNNS) profiles in the Rhode Island Child Health Study (RICHS)
Tung, P. W., Burt, A., Karagas, M. R., Jackson, B. P., Punshon, T., Lester, B. M., & Marsit, C. J. (2021) · Environmental Research · doi:10.1016/j.envres.2021.111939 · Cited by 26
Elevated prenatal maternal sex hormones, but not placental aromatase, are associated with child neurodevelopment
Firestein, M. R., Romeo, R. D., Winstead, H., Goldman, D. A., Grobman, W. A., Haas, D., Mercer, B., Parker, C., Parry, S., Reddy, U., et al. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105125 · Cited by 22
“…Robinson et al., 1977; Rodeck et al., 1985), and the observed sex bias in the prevalence of neurodevelopmental disorders (Al-Zaid, 2017; Constantino and Charman, 2012; Werling and Geschwind, 2013), we hypothesized that male vulnerability (Bale, 2016) would be reflected in sex-specific associations.”
Background
Ozone-induced fetal growth restriction in rats is associated with sexually dimorphic placental and fetal metabolic adaptation
Miller, C. N., Dye, J. A., Henriquez, A. R., Stewart, E. J., Lavrich, K. S., Carswell, G. K., Ren, H., Freeborn, D. L., Snow, S. J., Schladweiler, M. C. J., et al. (2020) · Molecular Metabolism · doi:10.1016/j.molmet.2020.101094 · Cited by 24
Maternal immune activation in rats induces dysfunction of placental leucine transport and alters fetal brain growth
Kowash, H. M., Potter, H. G., Woods, R. M., Ashton, N., Hager, R., Neill, J. C., & Glazier, J. D. (2022) · Clinical Science · doi:10.1042/cs20220245 · Cited by 23
Profiling placental DNA methylation associated with maternal SSRI treatment during pregnancy
Inkster, A. M., Konwar, C., Peñaherrera, M. S., Brain, U. M., Khan, A., Price, E. M., Schuetz, J. M., Portales-Casamar, É., Burt, A., Marsit, C. J., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-26071-8 · Cited by 24
Gender differences in the prevalence, comorbidities and antipsychotic prescription of early-onset schizophrenia: a nationwide population-based study in Taiwan
Hsu, C., Lee, S.-Y., & Wang, L. (2018) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-018-1242-9 · Cited by 23
Fetal Hippocampal Connectivity Shows Dissociable Associations with Maternal Cortisol and Self-Reported Distress during Pregnancy
Hendrix, C. L., Srinivasan, H., Feliciano, I., Carré, J. M., & Thomason, M. E. (2022) · Life · doi:10.3390/life12070943 · Cited by 21
“Well-replicated preclinical studies in mouse models have isolated sexual dimorphisms in the placenta that lead to this strengthened effect on male neurodevelopment [16,16].”
Background
Neurodevelopmental Disruptions in Children of Preeclamptic Mothers: Pathophysiological Mechanisms and Consequences
González, A., & Valencia, M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25073632 · Cited by 22
“Moreover, their findings identified the brain as being structurally sexually dimorphic and vascularly dimorphic, as other authors have described [91,189,190].”
Result
Shaping the risk for late-life neurodegenerative disease: A systematic review on prenatal risk factors for Alzheimer’s disease-related volumetric brain biomarkers
Boots, A., Wiegersma, A. M., Vali, Y., den Hof, M. V., Langendam, M. W., Limpens, J., Backhouse, E. V., Shenkin, S. D., Wardlaw, J. M., Roseboom, T. J., et al. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.105019 · Cited by 22
“For instance, prenatal exposure to alcohol or tobacco restricts fetal brain growth, mostly observed as reduced whole brain and regional brain volumes (e.g. Banderali et al., 2015; Caputo et al., 2016; Ekblad et al., 2015; Popova et al., 2021).”
Background
Individual longitudinal changes in DNA-methylome identify signatures of early-life adversity and correlate with later outcome
Short, A. K., Weber, R., Kamei, N., Thai, C. W., Arora, H., Mortazavi, A., Stern, H. S., Glynn, L. M., & Baram, T. Z. (2024) · Neurobiology of Stress · doi:10.1016/j.ynstr.2024.100652 · Cited by 21
“Initially detected in experimental animal models of early-life adversity (Molet et al., 2014, 2016; Rice et al., 2008), unpredictable sequences of parental care behaviors have emerged as an important potential predictor of susceptibility to later cognitive and emotional deficits (Groh et al., 2012).”
Background
Utility of DNA methylation to assess placental health
Wilson, S. L., & Robinson, W. P. (2017) · Placenta · doi:10.1016/j.placenta.2017.12.013 · Cited by 24
The genetics of autism and steroid-related traits in prenatal and postnatal life
Tsompanidis, A., Warrier, V., & Baron‐Cohen, S. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1126036 · Cited by 21
Preeclampsia promotes autism in offspring via maternal inflammation and fetal NFκB signaling
Liu, X., Liu, H., Gu, N.-H., Pei, J., Lin, X.-H., & Zhao, W. (2023) · Life Science Alliance · doi:10.26508/lsa.202301957 · Cited by 19
“Prior works have suggested that female hormones or placental sex differences might in ﬂ uence the development and (68).”
Background
Daily Early-Life Exposures to Diet Soda and Aspartame Are Associated with Autism in Males: A Case-Control Study
Fowler, S. P., Gimeno, D., Swartz, M. D., Granados, P. S., Heilbrun, L. P., & Palmer, R. F. (2023) · Nutrients · doi:10.3390/nu15173772 · Cited by 19
Maternal preconception stress produces sex-specific effects at the maternal:fetal interface to impact offspring development and phenotypic outcomes
Cissé, Y. M., Montgomery, K. R., Zierden, H. C., Hill, E. M., Kane, P. J., Huang, W., Kane, M. A., & Bale, T. L. (2023) · Biology of Reproduction · doi:10.1093/biolre/ioad156 · Cited by 19
“Consistent with other models examining effects of prenatal insults, preconception stress was associated with sex-specific effects on gene expression in the placenta [26, 56–58].”
Self-citation
Exploring sex differences in fetal programming for childhood emotional disorders
Galbally, M., Watson, S., Lappas, M., de Kloet, E. R., Wyrwoll, C. S., Mark, P. J., & Lewis, A. J. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105764 · Cited by 19
“Prenatal stress may produce sex-dependent signals via the placenta to the developing brain, underpinning sex differences in child mental health outcomes (Bale, 2016; Clifton, 2010; Mueller and Bale, 2007, 2008).”
Background
Transgenerational impacts of early life adversity: from health determinants, implications to epigenetic consequences
Holuka, C., Grova, N., Charalambous, E. G., Cléac`H, J. L., Turner, J. D., & Mposhi, A. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105785 · Cited by 18
“Subsequent reprogramming events then establish new methylation marks that direct the cells to follow specific developmental pathways. influence foetal development through placenta (Bale, 2016).”
Human Umbilical Cord: Information Mine in Sex-Specific Medicine
Campesi, I., Franconi, F., Montella, A., Dessole, S., & Capobianco, G. (2021) · Life · doi:10.3390/life11010052 · Cited by 18

Authors: Bale, T. L.
Affiliations: University of Pennsylvania (US)
Corresponding author: Bale, Tracy L.
ORCID: Bale, Tracy L.
Venue: Dialogues in Clinical Neuroscience
Publisher: Informa UK Limited
Published: 2016-12-31
Volume: 18
Issue: 4
Pages: 459-464
ISSN: 1294-8322 (ISSN-L)
1958-5969
DOI: 10.31887/dcns.2016.18.4/tbale
PMC: PMC5286731
OpenAlex: W2988356887
Cited by: 236
References: 86
Citations by year: 2026: 23 · 2025: 29 · 2024: 23 · 2023: 35 · 2022: 30 · 2021: 32 · 2020: 20 · 2019: 17 · 2018: 20 · 2017: 7
FWCI: 11.85
Type: journal article
Language: en
Open access: diamond
doi.org
Licence: cc-by-nc-nd
creativecommons.org/licenses/by-nc-nd/3.0/ (vor)
Locations: Dialogues in Clinical Neuroscience (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01mh091258-05)
National Institute of Mental Health (P50MH099910, R37MH108286, R33MH104184, R01 MH-091258, R01MH087597)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
Keywords: placenta, sex differences, brain development, prenatal stress, maternal stress, neurodevelopmental disorders, autism spectrum disorder, attention deficit hyperactivity disorder, X-linked genes, O-GlcNAc transferase, sex bias
MeSH terms: Animals, Female, Humans, Male, Placenta, Pregnancy, Prenatal Exposure Delayed Effects, Sex Characteristics, Stress, Physiological, Stress, Psychological, Neurodevelopmental Disorders

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

The placenta and neurodevelopment: sex differences in prenatal vulnerability

Abstract

Overview

Integrity signals

Figures

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks