Cited by 557Stress Responses and CortisolAdrenal Hormones and DisordersNeuropeptides and Animal Physiology

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Regulation of Pituitary ACTH Secretion during Chronic Stress

Aguilera, Greti·1994·Frontiers in Neuroendocrinology

DOI 10.1006/frne.1994.1013

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Abstract

Maintenance of adequate levels of response of the hypothalamic-pituitary-adrenal axis during chronic stress is important for survival. Three basic patterns of response can be identified depending on the type of stress: (a) desensitization of ACTH responses to the sustained stimulus, but hyperresponsiveness to a novel stress despite elevated plasma glucocorticoid levels, as occurs in physical-psychological paradigms; (b) no desensitization of ACTH response to the repeated stimulus and hyperresponsiveness to a novel stress, as occurs during repeated painful stress and insulin hypoglycemia; and (c) small and transient increases in ACTH, but sustained elevations of plasma corticosterone and diminished ACTH responses. The level of response of the pituitary corticotroph is determined by differential regulation of the hypothalamic regulators, corticotropin-releasing hormone (CRH) and vasopressin (VP), and the sensitivity of the negative glucocorticoid feedback. While osmotic stimulation increases VP expression in magnocellular neurons of the paraventricular (PVN) and supraoptic nuclei of the hypothalamus, chronic stress paradigms with high pituitary responsiveness are associated with activation of CRH and CRH/VP parvicellular neurons of the PVN, predominantly of the VP-containing population. While moderate increase of CRH output is important for stimulation of POMC transcription, the increase of the VP:CRH secretion ratio appears to be important in maintaining the secretory capacity of the pituitary corticotroph during chronic stimulation. Decreased sensitivity of the glucocorticoid feedback, probably due to interaction of glucocorticoid receptors with transcription factors induced by CRH and VP, is critical for the maintenance of ACTH responses in the presence of elevated plasma glucocorticoid levels during chronic stress. Although both CRH and VP receptors are activated and undergo regulatory variations during chronic stress, only the changes in VP receptor levels are parallel to the changes in pituitary ACTH responsiveness. The inhibitory effect of chronic osmotic stimulation on ACTH secretion in spite of high circulating levels of VP is probably the result of diminished activity of parvicellular PVN neurons and downregulation of pituitary VP receptors. Although the exact interaction between regulatory factors and the molecular mechanisms controlling the sensitivity of the corticotroph during adaptation to chronic stress remain to be determined, it is clear that regulation of the proportional secretion of CRH and VP in the PVN, modulation of pituitary VP receptors, and the sensitivity to feedback inhibition play a critical role.

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Self-citation
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Background
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Background
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Background
Glucocorticoids are active players and therapeutic targets in atherosclerotic cardiovascular disease
van der Sluis, R. J., & Hoekstra, M. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.110728 · Cited by 27
“Since the majority of clinical Cushing's cases are resulting from ACTH-mediated adrenal overstimulation, i.e. ACTH-producing pituitary tumors, it can be suggested that targeting SR-BI functionality may be of use in the treatment of Cushing's syndrome patients.”
Influential
Maternal Genotype Influences Stress Reactivity of Vasopressin‐Deficient Brattleboro Rats
Zelena, D., Mergl, Z., & Makara, G. B. (2003) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2003.01101.x · Cited by 26
Long-term effects of maternal separation on chronic stress response suppressed by amitriptyline treatment
Cotella, E. M., Lascano, I. M., Franchioni, L., Levin, G. M., & Suárez, M. M. (2013) · Stress · doi:10.3109/10253890.2013.775241 · Cited by 25
“…response of ACTH to chronic stress accompanied by a slight rise of corticosterone could be explained by transient rise in CRH during the paradigm (Aguilera, 1994), which means that a response of ACTH could be detected after individual stressors but not as a rise of basal secretion at the end of…”
Background
Cortisol in Correlation to Other Indicators of Fish Welfare
Kalamarz‐Kubiak, H. (2018) · InTech eBooks · doi:10.5772/intechopen.72392 · Cited by 28
“It is also shown that stress upregulates the number of AVP receptors in rat anterior pituitary [96].”
Background
Preclinical Profile of Bacopasides From Bacopa monnieri (BM) As An Emerging Class of Therapeutics for Management of Chronic Pains
Rauf, K., Subhan, F., Al-Othman, A. M., Khan, I., Zarrelli, A., & Shah, M. R. (2013) · Current Medicinal Chemistry · doi:10.2174/0929867311320080006 · Cited by 31
“(6) [42-54].”
Background
Sex-dependent effects of chronic variable stress on discrete corticotropin-releasing factor receptor 1 cell populations
Rosinger, Z. J., Guzman, R. M. D., Jacobskind, J. S., Saglimbeni, B., Malone, M., Fico, D., Justice, N. J., Forni, P. E., & Zuloaga, D. G. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.112847 · Cited by 24
“Furthermore, the number of c-Fos/CRFR1-GFP+ cells was elevated in females compared to males (F(1,20) = 12.”
BackgroundMethodInfluential
Transcriptional and post-transcriptional mechanisms regulating the rat pituitary vasopressin V1b receptor gene
Aguilera, G., Volpi, S., & Rabadan‐Diehl, C. (2003) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0300099 · Cited by 24
Self-citation
Immediate and longterm effects of immune stimulation: hypothesis linking the immune response to subsequent physical and psychological wellbeing
Hurwitz, E. L., & Morgenstern, H. (2001) · Medical Hypotheses · doi:10.1054/mehy.2000.1217 · Cited by 25
The influence of salt loading on vasopressin gene expression in magno- and parvocellular hypothalamic neurons: An immunocytochemical andin situ hybridization analysis
Amaya, F., Tanaka, M., Tamada, Y., Tanaka, Y., Nilaver, G., & Ibata, Y. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00343-1 · Cited by 25
Hypothalamo-Pituitary-Adrenal Axis Sensitization after Chronic Salt Loading
Amaya, F., Tanaka, M., Hayashi, S., Tanaka, Y., & Ibata, Y. (2001) · Neuroendocrinology · doi:10.1159/000054635 · Cited by 22
“Repeated stress affects responsiveness of pituitary corticotropes, an effect depending upon the type of stress and determined by corticotropin-releasing hormone (CRH) and vasopressin (VP) release from the paraventricular nucleus (PVN) in the hypothalamus [”
Background
Transcriptional Regulation of the Pituitary Vasopressin V1b Receptor Involves a GAGA-binding Protein
Volpi, S., Rabadan‐Diehl, C., Cawley, N. X., & Aguilera, G. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m201508200 · Cited by 23
Self-citation
Salt-loading increases vasopressin and vasopressin 1b receptor mRNA in the hypothalamus and choroid plexus
Zemo, D. A., & McCabe, J. T. (2001) · Neuropeptides · doi:10.1054/npep.2001.0864 · Cited by 24
Melatonin effects on animal behavior: circadian rhythm, stress response, and modulation of behavioral patterns
Song, Y., & Yoon, M. (2024) · Journal of Animal Science and Technology · doi:10.5187/jast.2024.e105 · Cited by 25
Regulatory mechanism of hypothalamo-pituitary–adrenal (HPA) axis and neuronal changes after adrenalectomy in type 2 diabetes
Yi, S. S., Hwang, I. K., Shin, J. H., Choi, J. H., Lee, C. H., Kim, I. Y., Kim, Y. N., Won, M., Park, I.-S., Seong, J. K., et al. (2010) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2010.05.003 · Cited by 22
“Previous studies have shown a correlation between the numbers of binding sites for AVP in the pituitary with corticotroph responsiveness (Jard et al., 1986; Aguilera, 1994; Aguilera et al., 1994).”
Vasopressin signaling at brain level controls stress hormone release: the vasopressin-deficient Brattleboro rat as a model
Zelena, D., Pintér, O., Balázsfi, D., Langnaese, K., Richter, K., Landgraf, R., Makara, G. B., & Engelmann, M. (2015) · Amino Acids · doi:10.1007/s00726-015-2026-x · Cited by 24
“Although the theory of a predominant AVP regulation of the HPA axis predominantly during chronic stress (Aguilera 1994; Dallman 1993) is widely accepted, the data collected in recent studies do not support this hypothesis (Zelena et al.”
BackgroundMethodResultInfluential
Stress-Induced Stimulation of Pituitary POMC Gene Expression Is Associated with Activation of Transcription Factor AP-1 in Hypothalamus and Pituitary
Autelitano, D. J. (1998) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00303-1 · Cited by 23
Hormonal Disturbances in Visceral Leishmaniasis (Kala-Azar)
Verde, F. A. L., Verde, F. A. A. L., Neto, A. S., et al. (2011) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2011.09-0171 · Cited by 23
The Effect of Cold Stress on Lymphocyte Proliferation in Fetal Ethanol‐Exposed Rats
Giberson, P. K., Kim, C. K., Hutchinson, S., et al. (1997) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1997.tb04474.x · Cited by 23
Development and therapeutic indications of orally-active non-peptide vasopressin receptor antagonists
Thibonnier, M. (1998) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.7.5.729 · Cited by 23
Allopregnanolone reduces neuroendocrine response to acute stressful stimuli in sheep
Misztal, T., Młotkowska, P., Marciniak, E., & Misztal, A. (2020) · Journal of Endocrinology · doi:10.1530/joe-19-0376 · Cited by 22
“The number of active CRH receptors in the cell membrane, however, does not depend on the levels of mRNA and full ACTH responses can be achieved with partial receptor occupancy (Aguilera 1994, Nikodemova et al.”
Background
Psychological and physiological stressors
(2005) · Techniques in the behavioral and neural sciences · doi:10.1016/s0921-0709(05)80041-0 · Cited by 24
Identification of Stimulatory and Inhibitory Inputs to the Hypothalamic‐Pituitary‐Adrenal Axis During Hypoglycaemia or Transport In Ewes
Smith, R. F., French, N. P., Saphier, P. W., Lowry, P. J., Veldhuis, J. D., & Dobson, H. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01038.x · Cited by 22
Protective Effect of Prior Acute Immune Challenge, but Not Footshock, on Inflammation in the Rat
Harbuz, M. S., Chover-Gonzalez, A., Gibert‐Rahola, J., & Jessop, D. S. (2002) · Brain Behavior and Immunity · doi:10.1006/brbi.2001.0658 · Cited by 22
Untitled work
McEwen (2004) · doi:10.1016/s1054-3589(04)50016-9 · Cited by 22
Inhibition of Vasopressin V1b Receptor Translation By Upstream Open Reading Frames in the 5′‐Untranslated Region
Rabadan‐Diehl, C., Martı́nez, A., Volpi, S., Subburaju, S., & Aguilera, G. (2007) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2007.01533.x · Cited by 21
Self-citation
Expression of stress hormones AVP and CRH in the hypothalamus of Mus musculus following water and food deprivation
Yadawa, A. K., & Chaturvedi, C. M. (2016) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2016.03.005 · Cited by 22
“(2016), http://dx.d during chronic stimulation (Aguilera, 1994).”
Vasopressinergic control of stress-related behavior: studies in Brattleboro rats
Csikota, P., Fodor, A., Balázsfi, D., Pintér, O., Mizukami, H., Weger, S., Heilbronn, R., Engelmann, M., & Zelena, D. (2016) · Stress · doi:10.1080/10253890.2016.1183117 · Cited by 21
“Chronic stress is a widely used model of experimental depression and the switch from primarily CRH- to AVP-controlled ACTH secretion under chronic stress conditions found in rodents (Aguilera, 1994; Dallman, 1993) turned attention to AVP as a possible drug target.”
Background
Hyponatremia and the Use of Vasopressin Receptor Antagonists In Critically Ill Patients
Lehrich, R. W., & Greenberg, A. (2011) · Journal of Intensive Care Medicine · doi:10.1177/0885066610397016 · Cited by 21
“Lastly, AVP binds to Vasopressin-1b receptor (V1bR) which facilitates the release of adrenocorticotropin.(43) Similar to AVP interaction with V1aR, V1bR is coupled to a signal transduction pathway mediated through intracellular calcium release.”
Background
Immunohistochemical characterization of chicken pituitary cells containing the vasotocin VT2 receptor
Jurkevich, A., Berghman, L. R., Cornett, L. E., & Kuenzel, W. J. (2008) · Cell and Tissue Research · doi:10.1007/s00441-008-0636-2 · Cited by 21
“One of the most documented hypophysiotropic functions of AVP/AVT is the stimulation of adrenocorticotropic hormone (ACTH) release from corticotropes during stress responses (Rivier and Vale 1983; Castro et al. 1986; Familari et al. 1989; Aguilera 1994; Baker et al. 1996).”
Background
Nicotine self‐administration diminishes stress‐induced norepinephrine secretion but augments adrenergic‐responsiveness in the hypothalamic paraventricular nucleus and enhances adrenocorticotropic hormone and corticosterone release
Yu, G., & Sharp, B. M. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06551.x · Cited by 21
“2008) and other stressors (Aguilera 1994) augment ACTH and corticosterone responses to novel stressors, e.”
Background
Adaptation to Mild, Intermittent Stress Delays Development of Hyperglycemia in the Zucker Diabetic Fatty Rat Independent of Food Intake: Role of Habituation of the Hypothalamic-Pituitary-Adrenal Axis
Bates, H. E., Sirek, A. S., Kiràly, M. A., Yue, J. T. Y., Montes, D. G., Matthews, S. G., & Vranić, M. (2008) · Endocrinology · doi:10.1210/en.2007-1473 · Cited by 21
“Stress induces CRH secretion from the hypothalamic paraventricular nucleus (PVN), stimulating proopiomelanocortin (POMC) synthesis and processing in the anterior pituitary into ACTH (2, 3).”
Background
Neuroendocrinology of Neurodegenerative Diseases
de Aguilar, J. G., René, F., Dupuis, L., & Loeffler, J. (2003) · Neuroendocrinology · doi:10.1159/000074445 · Cited by 22
“genes. Though these transgenic models do not reproduce the complete pathology of AD, they have provided important insights into its molecular mechanisms.Regarding the endocrine system, numerous studies have reported hormonal modifications associated with AD. Whether such modifications are causative or secondary to AD…”
Background
Vasopressin Mediates Mitogenic Responses to Adrenalectomy in the Rat Anterior Pituitary
Subburaju, S., & Aguilera, G. (2007) · Endocrinology · doi:10.1210/en.2007-0103 · Cited by 21
“V1b receptor content in the pituitary and ACTH responses by the pituitary corticotroph (3, 13).”
BackgroundSelf-citation
Hypothalamic Pituitary Adrenal Axis and Immune Responses to Endotoxin in Rats with Chronic Adjuvant-Induced Arthritis
Grinevich, V., Harbuz, M. S., Ma, X., Jessop, D. S., Tilders, F. J. H., Lightman, S. L., & Aguilera, G. (2002) · Experimental Neurology · doi:10.1006/exnr.2002.8022 · Cited by 20
Self-citation
Role of Endogenous Nociceptin in the Regulation of Arginine Vasopressin Release in Conscious Rats
Kakiya, S., Murase, T., Arima, H., et al. (2000) · Endocrinology · doi:10.1210/endo.141.12.7809 · Cited by 21
“AVP is also a major stimulator of ACTH release from the anterior pituitary via V1b receptors (32, 33).”
Background
Hypothalamic-pituitary corticotroph function after shunting of magnocellular vasopressin and oxytocin to the hypophyseal portal circulation.
Makara, G. B., KISS, A. J., Lolait, S. J., et al. (1996) · Endocrinology · doi:10.1210/endo.137.2.8593805 · Cited by 21
Self-citation
The Vasopressin-Deficient Brattleboro Rat: Lessons for the Hypothalamo–Pituitary–Adrenal Axis Regulation
Makara, G. B., Varga, J. M., Barna, I., Pintér, O., Klausz, B., & Zelena, D. (2012) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-012-9842-2 · Cited by 20
“A turning point was the theories of Dallman (1993) and Aguilera (1994) suggesting a predominant AVP regulation of the HPA axis during chronic stress.”
Background
Lack of vasopressin does not prevent the behavioural and endocrine changes induced by chronic unpredictable stress
Varga, J. M., Domokos, Á., Barna, I., Jankord, R., Bagdy, G., & Zelena, D. (2010) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2010.09.014 · Cited by 20

Authors: Aguilera, G.
Affiliations: National Institutes of Health (US)
Corresponding author: Aguilera, Greti
Venue: Frontiers in Neuroendocrinology
Publisher: Elsevier BV
Published: 1994-12
Volume: 15
Issue: 4
Pages: 321-350
ISSN: 0091-3022 (ISSN-L)
DOI: 10.1006/frne.1994.1013
OpenAlex: W2031934304
Cited by: 557
References: 0
Citations by year: 2026: 10 · 2025: 11 · 2024: 14 · 2023: 16 · 2022: 11 · 2021: 12 · 2020: 11 · 2019: 14 · 2018: 11 · 2017: 17 · 2016: 21 · 2015: 19 · 2014: 14 · 2013: 18 · 2012: 18
FWCI: 5.50
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Frontiers in Neuroendocrinology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords: ACTH secretion, chronic stress, hypothalamic-pituitary-adrenal axis, corticotropin-releasing factor, vasopressin, corticotrophs, glucocorticoid negative feedback, paraventricular nucleus, supraoptic nucleus, osmotic stimulation, glucocorticoid receptor, stress adaptation, corticosterone, insulin-induced hypoglycemia
MeSH terms: Adrenocorticotropic Hormone, Animals, Corticosterone, Corticotropin-Releasing Hormone, Glucocorticoids, Homeostasis, Humans, Hypothalamus, Pituitary Gland, Stress, Physiological, Vasopressins

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Regulation of Pituitary ACTH Secretion during Chronic Stress

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