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BDNF and glucocorticoids regulate corticotrophin-releasing hormone (CRH) homeostasis in the hypothalamus
Open accessAbstract
Regulation of the hypothalamic–pituitary–adrenal (HPA) axis is critical for adaptation to environmental changes. The principle regulator of the HPA axis is corticotrophin-releasing hormone (CRH), which is made in the parventricular nucleus and is an important target of negative feedback by glucocorticoids. However, the molecular mechanisms that regulate CRH are not fully understood. Disruption of normal HPA axis activity is a major risk factor of neuropsychiatric disorders in which decreased expression of the glucocorticoid receptor (GR) has been documented. To investigate the role of the GR in CRH neurons, we have targeted the deletion of the GR, specifically in the parventricular nucleus. Impairment of GR function in the parventricular nucleus resulted in an enhancement of CRH expression and an up-regulation of hypothalamic levels of BDNF and disinhibition of the HPA axis. BDNF is a stress and activity-dependent factor involved in many activities modulated by the HPA axis. Significantly, ectopic expression of BDNF in vivo increased CRH, whereas reduced expression of BDNF, or its receptor TrkB, decreased CRH expression and normal HPA functions. We find the differential regulation of CRH relies upon the cAMP response-element binding protein coactivator CRTC2, which serves as a switch for BDNF and glucocorticoids to direct the expression of CRH.
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“Additional evidence for CORT acting directly on PVN neurons comes from studies where targeted deletion of GR in the PVN increased CRH expression and CORT and ACTH levels in male mice (Jeanneteau et al., 2012).”
From Hypothalamic–pituitary–adrenal and hypothalamic–pituitary–gonadal axes: sex differences in regulation of stress responsivity (2017) · cites this paper as Jeanneteau et al., 2012
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“This cross-talk between BDNF and CRH may be at least partly mediated by the CREB and MAPK pathway and is involved in the enhancement of fear memory under stress (187).”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [187]
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“The administration of BDNF in vivo induces increased CRH level and reduction of BDNF or its receptor normalizes the CRH level and thus, the HPA axis.”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [187]
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“Moreover, there is a feedback loop whereby directly regulates CRH, and thus, the HPA axis (187).”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [187]
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“For BDNF, its expression level responds to stress-related HPA axis activation.”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [187]
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“BDNF directly regulates the HPA axis.”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [187]
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“Finally, the broad disruption of the GR allele in the CNS [GRNesCre (5)] and its targeted deletion in the forebrain [forebrain-specific GR knock-out; FBGRKO mice] (119), or the PVN all resulted in the disinhibition of the HPA axis (120).”
From The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [120]
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InfluentialGray, J. D., Milner, T. A., & McEwen, B. S. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.034 · Cited by 250
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InfluentialSelf-citationThe interplay between oxytocin and the CRF system: regulation of the stress response
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“Recent studies have demonstrated that expression of CRH, the principle regulator of the hypothalamic–pituitary– adrenal (HPA) axis, is regulated in the PVN positively by BDNF–TrkB–cAMP response element-binding protein (CREB) signaling and negatively by glucocorticoid–glucocorticoid receptor–CREB coactivator CRTC2 sign…”
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“This transcriptional regulator serves as a bidirectional switch for BDNF and glucocorticoids to control expression of CRH (42).”
BackgroundHeat Stress Responses in Birds: A Review of the Neural Components
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“Neurons in the POA synapse on brain-derived neurotropic factor (BDNF)-releasing neurons in the PVN [72], which may then release BDNF onto CRF-releasing neurons in rats [73,74], mice [74], and chickens [75] and TRH-releasing neurons in rats [76] and thus stimulate the”
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“A different PVN GR knockout mouse generated by Jeanneatteau and colleagues showed a more drastic phenotype in that the homozygous mutants (GRflox/flox; Sim1Cre+) are embryonic lethal due to possible residual Cre-recombinase expression in the lung (Jeanneteau et al., 2012).”
InfluentialBDNF Methylation and Maternal Brain Activity in a Violence-Related Sample
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“Both BDNF and glucocorticoids regulate the release of Corticotrophin releasing factor in the hypothalamus [7].”
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“For instance, BDNF is involved in several homeostatic control mechanisms in the hypothalamus including activation of the hypothalamic-pituitary-adrenal (HPA) axis (18, 22) and regulation of food intake and body weight (26, 40, 42, 51).”
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“The slower, longer-lasting response is activation of the HPA axis that begins with the release of CRF into the circulation from the paraventricular nucleus of the hypothalamus, which then stimulates the pituitary to release ACTH into the bloodstream.”
InfluentialRegulatory role of NGFs in neurocognitive functions
Kumar, A., Pareek, V., Faiq, M. A., Kumar, P., Raza, K., Prasoon, P., Dantham, S., & Mochan, S. (2017) · Reviews in the Neurosciences · doi:10.1515/revneuro-2016-0031 · Cited by 44
Understanding stress-effects in the brain via transcriptional signal transduction pathways
Zalachoras, I., Houtman, R., & Meijer, O. C. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.03.038 · Cited by 41
“CRTC2 has been shown to be involved in the regulation of CRH. Recently Jeanneteau et al. (2012) studied how BDNF, GR, and CREB regulate CRH expression.”
Haematopoietic cells produce BDNF and regulate appetite upon migration to the hypothalamus
Urabe, H., Kojima, H., Chan, L., Terashima, T., Ogawa, N., Katagi, M., Fujino, K., Kumagai, A., Kawai, H., Asakawa, A., et al. (2013) · Nature Communications · doi:10.1038/ncomms2536 · Cited by 41
Jiang, R., Babyak, M. A., Brummett, B. H., Siegler, I. C., Kuhn, C. M., & Williams, R. B. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.02.005 · Cited by 39
“Although the precise mechanism linking BDNF to HPA axis activity remains unclear, animal studies have shown that HPA axis activity was maintained by both BDNF/TrkB and glucocorticoid signaling in the hypothalamic corticotropin releasing hormone (CRH) neurons (Jeanneteau et al., 2012).”
BackgroundAlgamal, M., Pearson, A., Hahn-Townsend, C., Burca, I., MULLAN, M. J., Crawford, F., & Ojo, J. O. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110035 · Cited by 37
Meakin, C. J., Martin, E. M., Junior, H. P. D. O. S., Mokrova, I. L., Kuban, K., O’Shea, T. M., Joseph, R. M., Smeester, L., & Fry, R. C. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.02.007 · Cited by 37
“BDNF promotes synaptic plasticity and regulation of Corticotropin-Releasing Hormone (CRH) in the hypothalamus, and is involved in regulating and maintaining homeostasis in the HPA axis during times of stress (Cowansage et al., 2010; Jeanneteau et al., 2012; Naert et al., 2015).”
Malta, M. B., Martins, J., Novaes, L. S., dos Santos, N. B., Sita, L. V., Camarini, R., Scavone, C., Bittencourt, J. C., & Munhoz, C. D. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02470-2 · Cited by 37
Osterlund, C., Rodriguez-Santiago, M., Woodruff, E. R., Newsom, R. J., Chadayammuri, A. P., & Spencer, R. L. (2016) · Endocrinology · doi:10.1210/en.2016-1123 · Cited by 38
Epigenetic Programming Effects of Early Life Stress: A Dual-Activation Hypothesis
Lux, V. (2018) · Current Genomics · doi:10.2174/1389202919666180307151358 · Cited by 39
“The authors also demonstrated that differential regulation of Crf in the PVN depends on the cAMP response-element binding protein coactivator Crtc2, which interacts with Bdnf and glucocorticoids to regulate Crf [133].”
BackgroundNeuroinflammatory Markers in the Serum of Prepubertal Children with Down Syndrome
Tarani, L., Carito, V., Ferraguti, G., Petrella, C., Greco, A., Ralli, M., Messina, M. P., Rasio, D., Luca, E. D., Putotto, C., et al. (2020) · Journal of Immunology Research · doi:10.1155/2020/6937154 · Cited by 36
“However, some animal model and human studies have shown that the activity of the superoxide dismutase enzyme (SOD) is elevated in Down Syndrome [41, 42].”
Cramer, T., Kisliouk, T., Yeshurun, S., & Meiri, N. (2014) · Developmental Neurobiology · doi:10.1002/dneu.22252 · Cited by 35
“We previously showed that neurotrophic signal transduction of brain-derived neurotrophic factor (BDNF) is critically involved in thermotolerance acquisition, and that long-term thermal resilience involves epigenetic alterations in the regulation of BDNF expression (Katz and Meiri, 2006; Yossifoff et al., 2008; Kisliou…”
BackgroundArango-Lievano, M., & Jeanneteau, F. D. (2016) · Pharmacological Research · doi:10.1016/j.phrs.2016.08.005 · Cited by 38
Self-citationIkeno, T., Deats, S., Soler, J. E., Lonstein, J. S., & Yan, L. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.12.004 · Cited by 34
“[63] Jeanneteau FD, Lambert WM, Ismaili N, Bath KG, Lee FS, Garabedian MJ, et al.”
Modulatory Activity of Soluble Beta Amyloid on HPA Axis Function in Rats
Morgese, M. G., Tucci, P., Colaianna, M., Zotti, M., Cuomo, V., Schiavone, S., & Trabace, L. (2014) · Current Pharmaceutical Design · doi:10.2174/13816128113199990500 · Cited by 35
Kadhim, H. J., Kang, S. W., & Kuenzel, W. J. (2019) · Brain Research · doi:10.1016/j.brainres.2019.02.018 · Cited by 37
Arango-Lievano, M., Peguet, C., Catteau, M., Parmentier, M., Wu, S. H., Chao, M. V., Ginsberg, S. D., & Jeanneteau, F. D. (2016) · Scientific Reports · doi:10.1038/srep37231 · Cited by 37
Self-citationNaert, G., Zussy, C., Ba, C. T. V., Chevallier, N., Tang, Y., Maurice, T., & Givalois, L. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12324 · Cited by 33
Neuroimaging genetic approaches to Posttraumatic Stress Disorder
Lebois, L. A. M., Wolff, J. D., & Ressler, K. J. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.04.019 · Cited by 31
“Higher levels of BDNF are associated with enhanced glucocorticoid receptor signaling, and glucocorticoids are important for neuronal plasticity (Arango-Lievano et al., 2015; Jeanneteau et al., 2012).”
BackgroundAnorexic action of deoxynivalenol in hypothalamus and intestine
Tominaga, M., Momonaka, Y., Yokose, C., Tadaishi, M., Shimizu, M., Yamane, T., Oishi, Y., & Kobayashi, K. (2016) · Toxicon · doi:10.1016/j.toxicon.2016.04.036 · Cited by 31
Munoz, M. J., Kumar, R. G., Oh, B., Conley, Y. P., Wang, Z., Failla, M. D., & Wagner, A. K. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00044 · Cited by 30
“, 2004), may also regulate HPA-axis reactivity and cortisol releasing hormone (Jeanneteau et al., 2012).”
BackgroundEffect of Maternal Stress Prior to Conception on Hippocampal BDNF Signaling in Rat Offspring
Niknazar, S., Nahavandi, A., Peyvandi, A. A., Peyvandi, H., Mehrjerdi, F. Z., & Karimi, M. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0143-5 · Cited by 31
Effects of environmental manipulations in genetically targeted animal models of affective disorders
Renoir, T., Pang, T. Y., & Hannan, A. J. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.04.003 · Cited by 32
Dong, W., Xu, D., Hu, Z., He, X., Guo, Z., Jiao, Z., Yu, Y., & Wang, H. (2018) · Toxicology Letters · doi:10.1016/j.toxlet.2017.10.020 · Cited by 27
Transactivation of TrkB Receptors by Oxytocin and Its G Protein-Coupled Receptor
Mitre, M., Saadipour, K., Williams, K., Khatri, L., Froemke, R. C., & Chao, M. V. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.891537 · Cited by 31
Self-citationMolecular Biology of Glucocorticoid Signaling
Arango-Lievano, M., Lambert, W. M., & Jeanneteau, F. D. (2015) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-2895-8_2 · Cited by 28
“The typical inverted U-shape responses to increasing dose of glucocorticoids could be in part explained by “squelching” or titration of a limiting co-factor required for full response by the activated GR [ 110 – 112 ].”
BackgroundSelf-citationGriesbach, G. S., Vincelli, J., Tio, D. L., & Hovda, D. A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.03.005 · Cited by 28
Rein, T., Ambrée, O., Fries, G. R., Rappeneau, V., Schmidt, U., & Touma, C. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813333-0.00009-3 · Cited by 29
Sapio, M. R., Iadarola, M. J., LaPaglia, D. M., Lehky, T., Thurm, A. E., Danley, K. M., Fuhr, S. R., Lee, M. D., Huey, A. E., Sharp, S. J., et al. (2019) · Pain · doi:10.1097/j.pain.0000000000001485 · Cited by 30
“consistent with other reports where decreased Bdnf expression, or that of its receptor, was associated with decreased Crh expression.(31) However, this gene is not highly expressed, and it is unclear to what extent Crh signaling contributes to the Bdnf1/2 phenotype.”
Tobet, S. A., Handa, R. J., & Goldstein, J. M. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-013-1248-6 · Cited by 28
“This amino acid substitution has been linked to CRH homeostatis [46] and to multiple psychiatric disorders [47].”
Backgroundde la Tremblaye, P. B., & Plamondon, H. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.07.001 · Cited by 28
“mediated CRH induction by neutralizing the function of the CREB coactivator CRTC2 (Jeanneteau et al., 2012).”
BackgroundThe capacity for acute exercise to modulate emotional memories: A review of findings and mechanisms
Keyan, D., & Bryant, R. A. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.033 · Cited by 27
Environmental stimulation in Huntington disease patients and animal models
Novati, A., Nguyen, H. P., & Schulze-Hentrich, J. M. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105725 · Cited by 29
“It is noteworthy that BDNF/TrkB signaling is involved in the regulation of the HPA axis, is beneficial for cell survival and plays a major role in regulating neuroplasticity related genes (Azogu-Sepe and Plamondon, 2021; Jeanneteau et al., 2012; Zuccato and Cattaneo, 2007).”
BackgroundOsterlund, C., Thompson, V., Hinds, L. R., & Spencer, R. L. (2013) · Journal of Endocrinology · doi:10.1530/joe-13-0365 · Cited by 26
“…of Mkp1 gene expression in mammalian brain, there is evidence for it being regulated in an activity-dependent manner, contributing to neuronal axonal plasticity, and being associated with major depressive disorder (Sgambato et al. 1998, Kodama et al. 2005, Doi et al. 2007, Jeanneteau et al. 2012).”
BackgroundInfluentialHerhaus, B., Heni, M., Bloch, W., & Petrowski, K. (2024) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2024.107192 · Cited by 34
“Thus, BDNF is a stress-dependent factor (Jeanneteau et al., 2012).”
BackgroundRole of BDNF val66met polymorphism in modulating exercised-induced emotional memories
Keyan, D., & Bryant, R. A. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.12.013 · Cited by 25
Wagner, A. K., & Kumar, R. G. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.09.011 · Cited by 24
“, 2004), may also regulate HPA-axis reactivity (Jeanneteau et al., 2012).”
BackgroundPandya, C. D., & Pillai, A. (2014) · Cell Communication and Signaling · doi:10.1186/preaccept-8374202491198307 · Cited by 27
Penney, J., Taylor, T., MacLusky, N. J., & Lu, R. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00352 · Cited by 25
“Regulation of CRH secretion is complex and occurs through numerous mechanisms, including immune regulation through interleukin-1β, in addition to neuropeptides such as norepinephrine (NE), serotonin (Wei et al., 2002) and brain derived neurotrophic factor (BDNF) (Jeanneteau et al., 2012).”
BackgroundInfluential
Metadata
- Authors
- Jeanneteau, F. D., Lambert, W. M., Ismaili, N., Bath, K. G., Lee, F. S., Garabedian, M. J., & Chao, M. V.
- Affiliations
- New York University (US)
- Department of Microbiology, New York University School of Medicine, New York, NY 10016;
- Brown University (US)
- Weill Cornell Medicine (US)
- Department of Cell Biology, Department of Physiology, Department of Neuroscience, and Department of Psychiatry, Skirball Institute of Biomolecular Medicine, and
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-01-09
- Volume
- 109
- Issue
- 4
- Pages
- 1305-1310
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3268297
- OpenAlex
- W2021067562
- Cited by
- 252
- References
- 38
- Citations by year
- 2026: 11 · 2025: 11 · 2024: 18 · 2023: 12 · 2022: 12 · 2021: 17 · 2020: 18 · 2019: 18 · 2018: 18 · 2017: 27 · 2016: 19 · 2015: 17 · 2014: 15 · 2013: 24 · 2012: 15
- FWCI
- 9.42
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Alliance for Research on Schizophrenia and Depression
- National Institute of Biomedical Innovation
- National Institutes of Health (NS-21072)
- National Institute of Mental Health (R01MH086651, MH086651)
- National Institute of Allergy and Infectious Diseases (5T32 AI07180-29, T32AI007180)
- National Institute of Neurological Disorders and Stroke (R01NS021072, NS-21072, R56NS021072)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Keywords
- brain-derived neurotrophic factor, glucocorticoids, corticotropin-releasing factor, hypothalamic-pituitary-adrenal axis, hypothalamus, glucocorticoid receptor, CRTC2, TrkB receptor, CREB, stress response, negative feedback
- MeSH terms
- Analysis of Variance, Animals, Corticotropin-Releasing Hormone, Glucocorticoids, Homeostasis, Hypothalamo-Hypophyseal System, Hypothalamus, Immunohistochemistry, Mice, Inbred C57BL, Neurons, Pituitary-Adrenal System, Receptors, Glucocorticoid, Transcription Factors, Trans-Activators, Mutagenesis, Site-Directed, Rats, Sprague-Dawley, Mice, Knockout, Microscopy, Confocal, Brain-Derived Neurotrophic Factor, Chromatin Immunoprecipitation, Mice, Rats, Real-Time Polymerase Chain Reaction
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