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Feast and Famine: Critical Role of Glucocorticoids with Insulin in Daily Energy Flow
Abstract
The hypothesis proposed in this review is that normal diurnal rhythms in the hypothalamic-pituitary-adrenal (HPA) axis are highly regulated by activity in medial hypothalamic nuclei to effect an interaction between corticosteroids and insulin such that optimal metabolism results in response to changes in the fed or fasted state of the animal. There are marked diurnal rhythms in function of the HPA axis under both basal and stress conditions. The HPA axis controls corticosteroid output from the adrenal and, in turn, forward elements of this axis are inhibited by feedback from circulating plasma corticosteroid levels. Basal activity in the HPA axis of mammals fed ad lib peaks about 2 h before the peak of the diurnal feeding rhythm, and is controlled by input from the suprachiasmatic nuclei. The rhythm in stress responsiveness is lowest at the time of the basal peak and highest at the time of the basal trough in the HPA axis activity. There are also diurnal rhythms in corticosteroid feedback sensitivity of basal and stress-induced ACTH secretion which peak at the time of the basal trough. These rhythms are all overridden when feeding, and thus insulin secretion, is disrupted. Corticosteroids interact with insulin on food intake and body composition, and corticosteroids also increase insulin secretion. Corticosteroids stimulate feeding at low doses but inhibit it at high doses; however, it is the high levels of insulin, induced by high levels of corticosteroids, that may inhibit feeding. The effects of corticosteroids on liver, fat, and muscle cell metabolism, with emphasis on their interactions with insulin, are briefly reviewed. Corticosteroids both synergize with and antagonize the effects of insulin. The effects of stress hormones, and their interactions with insulin on lipid and protein metabolism, followed by some of the metabolic effects of injury stress, with or without nutritional support, are evaluated. In the presence of elevated insulin stimulated by glucocorticoids and nutrition, stress causes less severe catabolic effects. In the central nervous system, regulation of function in the HPA axis is clearly affected by the activity of medial hypothalamic nuclei that also alter feeding, metabolism, and obesity in rats. Lesions of the arcuate (ARC) and ventromedial (VMN) paraventricular (PVN) nuclei result in obesity and hyperactivity in the HPA axis. Moreover, adrenalectomy inhibits or prevents development of the lesion-induced obesity. There are interactions among these nuclei; one mode of communication is via inputs of neuropeptide Y (NPY) cells in the ARC to the VMN, dorsomedial nuclei, and PVN.(ABSTRACT TRUNCATED AT 400 WORDS)
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“Similarly, stress has been shown to be associated with increased appetite (Dallman et al., 1993)”
From The impact of stress on students in secondary school and higher education (2020) · cites this paper as Dallman et al., 1993
In the citing paper
“In fact, experimentally increasing late-afternoon and early-evening cortisol through hydrocortisone administration induces insulin resistance the following day [69, 73, 74].”
From Sleep, testosterone and cortisol balance, and ageing men (2022) · cites this paper as [69]
In the citing paper
“These findings are highly relevant because hypercortisolemia during the late-afternoon and early-evening is harmful, and is believed to cause the insulin resistance observed with advanced age [60, 69, 70], impair physical performance [71] and trigger neurocognitive deficits [72].”
From Sleep, testosterone and cortisol balance, and ageing men (2022) · cites this paper as [69]
In the citing paper
“Administration of glucocorticoids to bolster cortisol levels in the late afternoon and early evening also induces insulin resistance [69, 73, 74] through post-receptor mechanisms [90–92].”
From Sleep, testosterone and cortisol balance, and ageing men (2022) · cites this paper as [69]
In the citing paper
“Raised cortisol concentrations in the evening are thought to contribute to age-related insulin resistance [55], [56].”
From Impact of Five Nights of Sleep Restriction on Glucose Metabolism, Leptin and Testosterone in Young Adult Men (2012) · cites this paper as [55]
In the citing paper
“Circadian misalignment may lead to central and peripheral deleterious consequences, such as memory deficit and insulin resistance [69–71].”
From Impact of Sleep and Its Disturbances on Hypothalamo-Pituitary-Adrenal Axis Activity (2010) · cites this paper as [70]
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“Elevated serum corticosterone and low insulin are, therefore, hallmarks of the food-deprived state [reviewed in (26)].”
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Therapeutic manipulation of glucocorticoid metabolism in cardiovascular disease
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“Most of the indirect systemic effects of glucocorticoids lead to an increase in cardiovascular risk factors and, therefore, are linked to the prognosis of increased cardiovascular events (Dallman et al., 1993; Andrews and Walker, 1999; Walker, 2007b).”
BackgroundGlucocorticoids and their receptors: Insights into specific roles in mitochondria
Lee, S., Kim, H. K., Song, I.-S., Youm, J., Dizon, L. A., Jeong, S.-H., Ko, T.-H., Heo, H.-J., Ko, K. S., Rhee, B. D., et al. (2013) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2013.04.001 · Cited by 99
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BackgroundDeterminants of within- and among-clutch variation in yolk corticosterone in the European starling
Love, O. P., Wynne‐Edwards, K. E., Bond, L., & Williams, T. D. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.09.007 · Cited by 102
“Since plasma glucocorticoids are tightly tied to homeostatic energy balance (Harvey et al., 1984; Dallman et al., 1993; Remage-Healey and Romero, 2001), an increase in maternal energetic deficits across laying may hormonally manifest itself in both increasing maternal plasma and yolk corticosterone levels across the l…”
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“These nuclei are important for regulation of energy balance (Dallman et al., 1993).”
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Glucocorticoids and insulin both modulate caloric intake through actions on the brain
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“GC and insulin are intimately entwined in regulating both the amount and choice of food intake and caloric disposition (Dallman et al. 1993).”
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“It has previously been reported that plasma ACTH and corticosterone concentrations tend to rise just before feeding bouts (17, 18).”
BackgroundBehavior and pituitary-adrenal function in large white and Meishan pigs
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Cortisol Is Negatively Associated with Insulin Sensitivity in Overweight Latino Youth
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“Persistent increases in glucocorticoids have, in particular, been linked to metabolic and behavioral abnormalities including obesity, compromised immunity and depression (Dallman et al., 1993, 2006, 2007; Black, 2006; Bartolomucci et al., 2009).”
BackgroundRole of glucocorticoids in mediating effects of fasting and diabetes on hypothalamic gene expression
Makimura, H., Mizuno, T. M., Isoda, F., Beasley, J., Silverstein, J. H., & Mobbs, C. V. (2003) · BMC Physiology · doi:10.1186/1472-6793-3-5 · Cited by 94
Blas, J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-407160-5.00033-6 · Cited by 98
Lattin, C. R., Bauer, C. M., de Bruijn, R., & Romero, L. M. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.07.013 · Cited by 92
Landys, M. M., Wingfield, J. C., & Ramenofsky, M. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.06.006 · Cited by 92
“Thus, much in the same way as diel corticosterone elevations in most vertebrates anticipate ensuing demands of the active period (Dallman et al., 1993), preflight elevations in corticosterone may help migrants to prepare for the impending energetic demands of migratory activity.”
BackgroundLeptin and the Neuroendocrinology of Fasting
Ahima, R. S. (1999) · KARGER eBooks · doi:10.1159/000061014 · Cited by 93
Burnweit, C. A., Zerpa, J., Nahmad, M., Lankau, C. A., Weinberger, M., Malvezzi, L., Smith, L., Shapiro, T., & Thayer, K. (2004) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2003.11.037 · Cited by 92
Baran, K., Preston, E., Wilks, D. L., Cooney, G. J., Kraegen, E. W., & Sainsbury, A. (2002) · Diabetes · doi:10.2337/diabetes.51.1.152 · Cited by 89
“This effect was probably mediated by SHU9119induced hyperphagia because feeding is known to increase corticosteronemia (36), and because in the present study MC4 receptor antagonist infusion with concomitant pairfeeding caused no such hypercorticosteronemia.”
BRADBURY, M. J., McBurnie, M. I., Denton, D. A., et al. (2000) · Endocrinology · doi:10.1210/endo.141.8.7606 · Cited by 90
“For example, CRFR1 is expressed in the dorsomedial nuclei and medial preoptic areas of the hypothalamus (16) and the central nucleus of the amygdala (16), all areas documented to modulate energy expenditure (17, 18).”
InfluentialSelf-citationThe Contribution of Psychosocial Stress to the Obesity Epidemic: An Evolutionary Approach
Siervo, M., Wells, J. C. K., & Cizza, G. (2009) · Hormone and Metabolic Research · doi:10.1055/s-0028-1119377 · Cited by 96
Sullivan, E. C., Hinde, K., Mendoza, S. P., & Capitanio, J. P. (2010) · Developmental Psychobiology · doi:10.1002/dev.20483 · Cited by 89
Stress hormones, carcass composition and meat quality in Large White×Duroc pigs
Foury, A., Devillers, N., Sanchez, M.-P., et al. (2004) · Meat Science · doi:10.1016/j.meatsci.2004.11.002 · Cited by 89
“The hypothalamic–pituitary–adrenocortical (HPA) axis influences feeding behavior, pancreatic hormone secretion, energy expenditure and the protein/lipid balance (Dallman et al., 1993).”
BackgroundMormède, P., Courvoisier, H., Ramos, A., Marissal‐Arvy, N., Ousova, O., Désautés, C., Duclos, M., Chaouloff, F., & Moisan, M. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00093-2 · Cited by 92
“Glucocorticoid hormones can influence a wide range of bodily as well as brain functions and in the stress response potentate the activity of catecholamines to increase metabolic fuels availability (Dallman et al., 1993).”
BackgroundAltered expression of type 2 CRH receptor mRNA in the VMH by glucocorticoids and starvation
Makino, S., Nishiyama, M., Asaba, K., Gold, P. W., & Hashimoto, K. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.275.4.r1138 · Cited by 87
Role of biological rhythms in gastrointestinal health and disease
Hoogerwerf, W. A. (2009) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-009-9119-3 · Cited by 87
“The suprachiasmatic nucleus controls the rhythm of glucocorticoid secretion via periodic release of corticotropin-releasing factor (CRF), which subsequently stimulates the synthesis and release of adrenocortiocotropin (ATCH) from the anterior pituitary [10–12].”
BackgroundPrendergast, B. J., Nelson, R. J., & Zucker, I. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50021-4 · Cited by 87
Makino, S., Asaba, K., Nishiyama, M., & Hashimoto, K. (1999) · Neuroendocrinology · doi:10.1159/000054472 · Cited by 84
Castéra, L., Nègre, I., Samii, K., & Buffet, C. (2001) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2001.03776.x · Cited by 84
Walker, B., Wingfield, J. C., & Boersma, P. D. (2005) · Physiological and Biochemical Zoology · doi:10.1086/422769 · Cited by 86
Molecular regulation of eating behavior: new insights and prospects for therapeutic strategies
Ahima, R. S., & Osei, S. Y. (2001) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(01)01989-x · Cited by 85
APPLE, J. K., Kegley, E. B., Galloway, D. L., Wistuba, T. J., & Rakes, L. K. (2005) · Journal of Animal Science · doi:10.2527/2005.8351202x · Cited by 85
Metadata
- Authors
- Dallman, M. F., Strack, A. M., Akana, S. F., Bradbury, M. J., Hanson, E. S., Scribner, K. A., & Smith, M.
- Affiliations
- University of California, San Francisco (US)
- Venue
- Frontiers in Neuroendocrinology
- Publisher
- Elsevier BV
- Published
- 1993-10
- Volume
- 14
- Issue
- 4
- Pages
- 303-347
- ISSN
- 0091-3022 (ISSN-L)
- OpenAlex
- W1971922927
- Cited by
- 796
- References
- 0
- Citations by year
- 2026: 6 · 2025: 11 · 2024: 12 · 2023: 21 · 2022: 15 · 2021: 20 · 2020: 22 · 2019: 22 · 2018: 13 · 2017: 13 · 2016: 30 · 2015: 26 · 2014: 27 · 2013: 20 · 2012: 33
- FWCI
- 6.82
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Frontiers in Neuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (DK28172)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Keywords
- glucocorticoids, insulin, hypothalamic-pituitary-adrenal axis, diurnal cycle, feeding behavior, stress hormones, corticosteroid feedback, ACTH secretion, arcuate nucleus, neuropeptide Y, obesity, energy metabolism, lipid metabolism, protein metabolism, catabolism, adrenalectomy, body composition
- MeSH terms
- Animals, Circadian Rhythm, Eating, Energy Metabolism, Fasting, Feeding Behavior, Glucocorticoids, Humans, Hypothalamo-Hypophyseal System, Insulin, Pituitary-Adrenal System, Stress, Physiological, Rats
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