Maternal corticosterone during lactation permanently affects brain corticosteroid receptors, stress response and behaviour in rat progeny

Catalani, A.; Casolini, Paola; Scaccianoce, Sergio; Patacchioli, Francesca Romana; Spinozzi, P; Angelucci, L.

doi:10.1016/s0306-4522(00)00277-3

Cited by 130 publications

(104 citation statements)

References 80 publications

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“…Our findings confirm and substantially extend previously published data that show that corticosterone secretion in response to a neurogenic stress was elevated in perinatally overfed rats (18) and that maturation of the adrenocortical rhythm was delayed in underfed animals (19). The model of postnatal overfeeding differs from previously published postnatal manipulations in rats (11)(12)(13)(14) in that 1) it uses a mild exclusively environmental stimulus and does not involve any pharmacological treatment, 2) the changes of corticosterone status found in adults parallel those of developing animals, 3) it associates systemic and AT changes in glucocorticoid metabolism, and 4) it induces the metabolic syndrome in adulthood. As a consequence, the experimental paradigm of neonatal overfeeding in rats is an interesting model that could shed light on some of the pathophysiological mechanisms underlying obesity and its associated complications in humans.…”

Section: Discussionmentioning

confidence: 99%

“…Corticotropinreleasing hormone (CRH), GR, PEPCK, and 11␤-HSD-1 antisense probes were generated by in vitro transcription in the presence of 35 S-uridine triphosphate (Perkin Elmer, Paris, France) from cDNA inserted into pPCR script and corresponding to bases 261-1020, 1617-2150, 174-531, and 18-271 of their respective mRNA. Slides were exposed to X-ray films (BIOMAX MR; Kodak, Le Pontet, France) together with 14 C standards. Hybridization with the sense probes showed no signal, demonstrating the specificity of the probes (not shown).…”

Section: Methodsmentioning

confidence: 99%

“…It is established that, in rats, during the immediate postnatal period, environmental or pharmacological manipulations permanently program the HPA axis. Indeed, adult basal and/or stress-induced corticosterone secretion is increased after postnatal maternal separation (11), modified maternal behavior (11), or endotoxin injection (12) and is decreased after handling (11) and parenteral (13) or maternal (14) glucocorticoid treatment. Interestingly, it is known that postnatal overfeeding leads to overweight, metabolic disturbances, and hypertension in adulthood (15).…”

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Postnatal Diet-Induced Obesity in Rats Upregulates Systemic and Adipose Tissue Glucocorticoid Metabolism During Development and in Adulthood

et al. 2005

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In humans, a hyperactivity of glucocorticoid metabolism was postulated to be involved in the intrauterine programming of the metabolic syndrome in adulthood. We studied in rats the effects of overfeeding, obtained by reducing the size of the litter in the immediate postnatal period, a time crucial for neuroendocrine maturation such as late gestation in humans. Overfeeding induced early-onset obesity and accelerated the maturation of the hypothalamo-pituitary-adrenal (HPA) axis together with an upregulation of adipose tissue glucocorticoid receptor (GR) mRNA. In adulthood, neonatally overfed rats presented with moderate increases in basal and stress-induced corticosterone secretion and striking changes in visceral adipose tissue glucocorticoid signaling, that is, enhanced GR and 11␤-hydroxysteroid dehydrogenase type 1 mRNA levels. The above-mentioned alterations in the endocrine status of overfed rats were accompanied by a moderate overweight status and significant metabolic disturbances comparable to those described in the metabolic syndrome. Our data demonstrate for the first time that postnatal overfeeding accelerates the maturation of the HPA axis and leads to permanent upregulation of the HPA axis and increased adipose tissue glucocorticoid sensitivity. Thus, the experimental paradigm of postnatal overfeeding is a powerful tool to understand the pathophysiology of glucocorticoid-induced programming of metabolic axes. Diabetes 54: [197][198][199][200][201][202][203] 2005 N umerous clinical and biological findings indicate that glucocorticoids are involved in the pathophysiology of abdominal obesity and its accompanying complications. Indeed, an excess of glucocorticoids, when associated with hyperinsulinism, favors an increase of lipogenesis and a decrease of lipolysis, together with a stimulation of hepatic neoglucogenesis and an inhibition of peripheral glucose utilization (1). Alterations in the hypothalamo-pituitary-adrenal (HPA) axis have been described in human obesity and in rodent models of obesity. They could involve a hyperactivity of the central command of ACTH secretion, secondary to an increased exposure or sensitization to stress (2) or decreased negative glucocorticoid feedback (3). In addition, changes in peripheral glucocorticoid signaling with increased visceral adipose tissue glucocorticoid receptor (GR) concentrations and local reactivation of circulating inert cortisone (11-dehydrocorticosterone in rodents) to cortisol (corticosterone) driven by 11␤-hydroxysteroid dehydrogenase type 1 (11␤-HSD-1) could play a pivotal role (4). However, the origins of the abovementioned dysregulations have not been established.Clinical and experimental evidence shows that the environment during the perinatal period plays an important role in the regulation of both metabolic and hormonal axes in adulthood. In humans, hyperglycemia and hyperinsulinemia in macrosomic fetuses of diabetic mothers were shown to favor later development of overweight (5). Conversely, it has been demonstrated that intrauterine g...

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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Postnatal Diet-Induced Obesity in Rats Upregulates Systemic and Adipose Tissue Glucocorticoid Metabolism During Development and in Adulthood

et al. 2005

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“…Elevated CORT during development has immediate effects, such as inhibition of growth and immune function (Butler et al, 2010;Yorty and Bonneau, 2004). However, brief elevations of stress during development can also have life-long consequences for physiology, morphology and behavior (Catalani et al, 2000;Gluckman and Hanson, 2004;Seckl and Meaney, 2004). For example, developmental stress can sensitize the hypothalamic-pituitary-adrenal (HPA) axis (the neuroendocrine pathway that releases glucocorticoids) such that stressed neonates are hypersensitive to stress as adults (Francis et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

The effects of experimentally elevated traffic noise on nestling white-crowned sparrow stress physiology, immune function, and life-history

Crino

Johnson

Blickley

et al. 2013

Journal of Experimental Biology

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SUMMARYRoads have been associated with behavioral and physiological changes in wildlife. In birds, roads decrease reproductive success and biodiversity and increase physiological stress. Although the consequences of roads on individuals and communities have been well described, the mechanisms through which roads affect birds remain largely unexplored. Here, we examine one mechanism through which roads could affect birds: traffic noise. We exposed nestling mountain white-crowned sparrows (Zonotrichia leucophrys oriantha) to experimentally elevated traffic noise for 5days during the nestling period. Following exposure to traffic noise we measured nestling stress physiology, immune function, body size, condition and survival. Based on prior studies, we expected the traffic noise treatment to result in elevated stress hormones (glucocorticoids), and declines in immune function, body size, condition and survival. Surprisingly, nestlings exposed to traffic noise had lower glucocorticoid levels and improved condition relative to control nests. These results indicate that traffic noise does affect physiology and development in white-crowned sparrows, but not at all as predicted. Therefore, when evaluating the mechanisms through which roads affect avian populations, other factors (e.g. edge effects, pollution and mechanical vibration) may be more important than traffic noise in explaining elevated nestling stress responses in this species.

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“…In rodents, offspring have been shown to be responsive to several factors that interact to affect the development of the postnatal brain. [32,34] and mice [33]. Interestingly, while low doses of neonatal corticosterone result in individual with an advantageous phenotype, high doses seem to lead to negative outcomes.…”

Section: Multiple Factors Interact To Mediate Environmental Effects Omentioning

confidence: 99%

Rodent models of early environment effects on offspring development and susceptibility to neurological diseases in adulthood

Coutellier

2012

Translational Neuroscience

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Rodent Models of eaRly envIRonMent effects on offspRIng developMent and susceptIbIlIty to neuRologIcal dIseases In adulthood abstractEvents early in life can program brain for a pattern of neuroendocrine and behavioral responses in later life. This mechanism is named "developmental phenotypic plasticity". Experimental evidences from rodents show that early experiences influence long-term development of behavioral, neuroendocrine and cognitive functions. While some neonatal conditions lead to positive outcomes, offspring might also display neurological dysfunctions in adulthood in case of adverse conditions during the early development. Different factors have been suggested to mediate the effects of neonatal conditions on offspring development but their exact contribution as well as their interaction still needs to be clarified. Studies based on rodents have been developed to model the longterm effects of early environmental conditions on the developing brain. These studies highlight importance of maternal behavior in mediating the effects of early environmental conditions on the offspring. However, other studies suggest that aside from the level of maternal care, other factors (gender, neonatal glucocorticoid levels) contribute to the adjustment of offspring phenotype to early environmental cues. Altogether, rodentsbased evidence suggests that developmental plasticity is a very complex phenomenon mediated by multiple factors that interact one to each other. Ultimately, the goal is to understand how early life events can lead to advantageous phenotype in adult life, or, on the contrary, can predispose individuals to psychopathologies such as depression or anxiety.

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Maternal corticosterone during lactation permanently affects brain corticosteroid receptors, stress response and behaviour in rat progeny

Cited by 130 publications

References 80 publications

Postnatal Diet-Induced Obesity in Rats Upregulates Systemic and Adipose Tissue Glucocorticoid Metabolism During Development and in Adulthood

Postnatal Diet-Induced Obesity in Rats Upregulates Systemic and Adipose Tissue Glucocorticoid Metabolism During Development and in Adulthood

The effects of experimentally elevated traffic noise on nestling white-crowned sparrow stress physiology, immune function, and life-history

Rodent models of early environment effects on offspring development and susceptibility to neurological diseases in adulthood

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