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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BackgroundResultInfluentialSelf-citation
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Miyata, S., Tsujioka, H., Itoh, M., Matsunaga, W., Kuramoto, H., & Kiyohara, T. (2001) · Molecular Brain Research · doi:10.1016/s0169-328x(01)00072-9 · Cited by 53
Hyperreninemic hypoaldosteronism after chronic stress in the rat.
Aguilera, G., Kiss, A., & Akbaşak, B. S. (1995) · Journal of Clinical Investigation · doi:10.1172/jci118189 · Cited by 52
Self-citation
Study of Active Substances Involved in Skin Dysfunction Induced by Crowding Stress. I. Effect of Crowding and Isolation on Some Physiological Variables, Skin Function and Skin Blood Perfusion in Hairless Mice.
Ishida, H., Mitsui, K., Nukaya, H., et al. (2003) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.26.170 · Cited by 52
Responses of the HPA axis after chronic variable stress: effects of novel and familiar stressors.
Simpkiss, J. L., & Devine, D. P. (2003) · PubMed · Cited by 52
Regulation of the Stress Response by Corticotropin-Releasing Factor Receptors
Hauger, R. L., & Dautzenberg, F. M. (2000) · Humana Press eBooks · doi:10.1007/978-1-59259-707-9_15 · Cited by 52
A single administration of interleukin‐1 or amphetamine induces long‐lasting increases in evoked noradrenaline release in the hypothalamus and sensitization of ACTH and corticosterone responses in rats
Schmidt, E. D., Schoffelmeer, A. N. M., Vries, T. J. D., Wardeh, G., Dogterom, G. E., Bol, J. G. J. M., Binnekade, R., & Tilders, F. J. H. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01569.x · Cited by 52
“…seen following adrenalectomy, chronic stress (Plotsky & Sawchenko, 1987; Aguilera et al., 1992; De Goeij et al., 1992; Harbuz & Lightman, 1992; Bartanusz et al., 1993; Dallman, 1993; Whitnall, 1993; Aguilera, 1994; Shanks et al., 1998) and depression (Nemeroff et al., 1984; Tilders et al., 1999).”
The Role of Vasopressin in Hypothalamo‐Pituitary‐Adrenal Axis Activation during Stress: An Assessment of the Evidence
Makara, G. B., Mergl, Z., & Zelena, D. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1296.018 · Cited by 52
Pattern of c-fos mRNA induction in rat brain by acute morphine
Gutstein, H. B., Thome, J. L., Fine, J. L., Watson, S. J., & Akil, H. (1998) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-76-3-294 · Cited by 51
“It has been shown that habituation to a specific stressor can alter responses to a novel stressor in an unpredictable fashion (Armario et al. 1988; Konarska et al. 1989; Aguilera 1994).”
Background
CRH in chronic inflammatory stress
Jessop, D. S., Harbuz, M. S., & Lightman, S. L. (2001) · Peptides · doi:10.1016/s0196-9781(01)00394-1 · Cited by 49
Neural Regulation of Corticotropin Releasing Hormone (CRH) and CRH Receptor mRNA in the Hypothalamic Paraventricular Nucleus in the Rat
Kiss, A., Palkovits, M., & Aguilera, G. (1996) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1996.tb00830.x · Cited by 49
“A major factor to consider is glucocorticoids since their levels are markedly elevated during stress (4).”
BackgroundSelf-citation
Coping with Stress During Aging: The Importance of a Resilient Brain
Sampedro-Piquero, P., Alvarez-Suarez, P., & Begega, A. (2018) · Current Neuropharmacology · doi:10.2174/1570159x15666170915141610 · Cited by 41
“This leads to stimulation of glucocorticoid secretion by the adrenal cortex, which is essential for stress adaptation [28, 29].”
Background
Prenatal Ethanol Exposure Alters the Effects of Gonadectomy on Hypothalamic‐Pituitary‐Adrenal Activity in Male Rats
Lan, N., Yamashita, F. S., Halpert, A. G., Ellis, L. A., Yu, W., Viau, V., & Weinberg, J. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01462.x · Cited by 51
Heat stress during late gestation disrupts maternal microbial transmission with altered offspring’s gut microbial colonization and serum metabolites in a pig model
He, J., Zheng, W., Tao, C., Guo, H., Xue, Y., Zhao, R., & Yao, W. (2020) · Environmental Pollution · doi:10.1016/j.envpol.2020.115111 · Cited by 50
Differential actions of acute and chronic citalopram on the rodent hypothalamic–pituitary–adrenal axis response to acute restraint stress
Hesketh, S. A., Jessop, D. S., Hogg, S. L., & Harbuz, M. S. (2005) · Journal of Endocrinology · doi:10.1677/joe.1.06074 · Cited by 50
“CRF is the main hypothalamic peptide involved in the release of ACTH from the anterior pituitary (Aguilera 1994).”
Background
Consequences of pandemic-associated social restrictions: Role of social support and the oxytocin system
Gryksa, K., & Neumann, I. D. (2021) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2021.105601 · Cited by 53
“AVP seems to become prominent during chronic or prolonged psychosocial stress (Keeney et al., 2006; Füchsl et al., 2013; Aguilera, 1994).”
Relationship between obsessive compulsive disorder and cortisol: Systematic review and meta-analysis
Sousa-Lima, J., Moreira, P. S., Raposo-Lima, C., Sousa, N., & Morgado, P. F. (2019) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2019.09.001 · Cited by 49
“…proposed to contribute to the development of various disease states, including major depression, schizophrenia, anxiety disorders and addictive disorders ( Aguilera, 1994; Bremner et al., 1996; Jarcho et al., 2013; Herman et al., 2012; Nasca et al., 2015; Sinha, 2008; Walker and Diforio, 1997 ).”
Background
Vasopressin and oxytocin
Douglas, A. J. (2005) · Techniques in the behavioral and neural sciences · doi:10.1016/s0921-0709(05)80014-8 · Cited by 48
Smoking as a complex but critical covariate in neurobiological studies of posttraumatic stress disorders: a review
Rasmusson, A. M., Picciotto, M. R., & Krishnan‐Sarin, S. (2006) · Journal of Psychopharmacology · doi:10.1177/0269881106060193 · Cited by 49
“AVP potentiates the activation of ACTH by CRF and mediates novelty-induced increases in ACTH after chronic stress (Aguilera, 1994; Marti et al., 1994).”
Background
Plasma corticosterone levels is elevated in rats submitted to chronic intermittent hypoxia
Zoccal, D. B., Bonagamba, L. G. H., Antunes‐Rodrigues, J., & Machado, B. H. (2007) · Autonomic Neuroscience · doi:10.1016/j.autneu.2007.01.004 · Cited by 47
Genomic Copy Number Variations of the Complement Component C4B Gene Are Associated With Chronic Central Serous Chorioretinopathy
Breukink, M. B., Schellevis, R. L., Boon, C. J. F., Fauser, S., Hoyng, C. B., den Hollander, A. I., & de Jong, E. K. (2015) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.15-17343 · Cited by 45
“These results are of interest in the context of cCSC because of the described clinical associations with stress and the use of corticosteroids that both exert physiological effects at the level of the HPA axis.(17) Various relatively small studies have studied cortisol levels in cCSC patients.”
Background
Maternal neglect with reduced depressive-like behavior and blunted c-fos activation in Brattleboro mothers, the role of central vasopressin
Fodor, A., Klausz, B., Pintér, O., Daviu, N., Rabasa, C., Rotllant, D., Balázsfi, D., Kovács, K., Nadal, R. A., & Zelena, D. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.09.003 · Cited by 47
Involvement of Transducer of Regulated cAMP Response Element-Binding Protein Activity on Corticotropin Releasing Hormone Transcription
Liu, Y., Escoto, A. C., Grinevich, V., & Aguilera, G. (2010) · Endocrinology · doi:10.1210/en.2009-0963 · Cited by 46
Self-citation
Should I Lay or Should I Grow: Photoperiodic Versus Metabolic Cues in Chickens
Hanlon, C., Ramachandran, R., Zuidhof, M. J., & Bédécarrats, G. Y. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00707 · Cited by 48
“, 1994), ACTH is a key link between regulation of appetite and stress response via the hypothalamicpituitary adrenal (HPA) axis (Aguilera, 1994), further decreasing feed intake when injected (Kawakami et al.”
Background
Pattern of c-fos mRNA induction in rat brain by acute morphine
Gutstein, H. B., Thome, J. L., Fine, J. L., Watson, S. J., & Akil, H. (1998) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y98-027 · Cited by 46
Depression and type 2 diabetes: Cortisol pathway implication and investigational needs
Gragnoli, C. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.23012 · Cited by 47
“The stressor activates the HPA axis by stimulating the hypothalamus to release CRH (Aguilera, 1994).”
Background
Modelling occupational stress and health: the impact of the demand–control model on academic research and on workplace practice
Jones, F. A., Bright, J. E. H., Searle, B. J., & Cooper, L. (1998) · Stress Medicine · doi:10.1002/(sici)1099-1700(1998100)14:4 · Cited by 32
Differential Effects of Repeated Restraint Stress on Pulsatile Lutenizing Hormone Secretion in Female Fischer, Lewis and Wistar Rats
Li, X. F., Edward, J., Mitchell, J. C., Shao, B., Bowes, J., Coen, C. W., Lightman, S. L., & O'Byrne, K. T. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2004.01209.x · Cited by 45
Inhibition of Corticotropin Releasing Hormone Type-1 Receptor Translation by an Upstream AUG Triplet in the 5′ Untranslated Region
Xu, G., Rabadan‐Diehl, C., Nikodémová, M., WYNN, P. C., Spiess, J., & Aguilera, G. (2001) · Molecular Pharmacology · doi:10.1124/mol.59.3.485 · Cited by 47
“As other plasma membrane receptors, CRHR1 are low-abundance proteins, and receptor number undergoes rapid regulatory changes during functional alterations of the pituitary corticotroph (Aguilera, 1994).”
InfluentialSelf-citation
Involvement of central angiotensin receptors in stress adaptation
Dumont, É. C., Rafrafi, S., Laforest, S., & Drolet, G. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00206-7 · Cited by 44
The Adrenal Cortex
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Coupling corticotropin-releasing-hormone and angiotensin converting enzyme 2 dampens stress responsiveness in male mice
Wang, L. A., de Kloet, A. D., Smeltzer, M. D., Cahill, K. M., Hiller, H., Bruce, E. B., Pioquinto, D. J., Ludin, J. A., Katovich, M. J., Raizada, M. K., et al. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.01.025 · Cited by 45
“POMC is the precursor for the glucocortoid secretagogue, ACTH, and previous in vitro and in vivo studies determined that levels of CRH in the PVN regulate POMC synthesis and the release of ACTH from the pituitary (for review see (Aguilera, 1994; Antoni, 1993)).”
Stress Adaptation and the Brainstem with Focus on Corticotropin-Releasing Hormone
Chaves, T., Fazekas, C. L., Horváth, K., Correia, P., Szabó, A., Török, B., Bánrévi, K., & Zelena, D. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22169090 · Cited by 49
“Nevertheless, in 1994, Greti Aguilera suggested that during chronic stress the activity of the HPA axis is maintained by vasopressin rather than CRH as it is less sensitive to the glucocorticoid feedback [18].”
Background
Prolonged alcohol intake leads to reversible depression of corticotropin-releasing hormone and vasopressin immunoreactivity and mRNA levels in the parvocellular neurons of the paraventricular nucleus
Silva, S. M., Paula-Barbosa, M. M., & Madeira, M. D. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03346-2 · Cited by 42
Persistent Increase in Hypothalamic Arginine Vasopressin Gene Expression During Protracted Withdrawal from Chronic Escalating-Dose Cocaine in Rodents
Zhou, Y., Litvin, Y., Piras, A. P., Pfaff, D. W., & Kreek, M. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.97 · Cited by 42
“In cocaine addicts with depressive symptoms, basal plasma cortisol levels are increased during early cocaine abstinence (”
Background
Amygdalar vasopressin mRNA increases in acute cocaine withdrawal: Evidence for opioid receptor modulation
Zhou, Y., Bendor, J., Yuferov, V. P., Schlussman, S. D., Ho, A., & Kreek, M. J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.032 · Cited by 41

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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