Maternal stress alters endocrine function of the feto-placental unit in rats

Mairesse, Jérôme; Lésage, Jean; Breton, Christophe; Bréant, Bernadette; Hahn, Tom; Darnaudéry, Muriel; Dickson, Suzanne L.; Seckl, Jonathan R.; Blondeau, Bertrand; Vieau, Didier; Maccari, Stefania; Viltart, Odile

doi:10.1152/ajpendo.00574.2006

Cited by 342 publications

(265 citation statements)

References 71 publications

Supporting

Mentioning

234

Contrasting

Unclassified

Order By: Relevance

“…Research into the interplay between the HPA axis and metabolism suggests that the relationship between these systems is established during the prenatal and early postnatal period (3,10,39,53), and maternal stress experienced by the fetus during gestation has proven developmental and metabolic effects (26,34,37,38). Persistent stress also influences bone function, with chronic elevations of cortisol leading to low bone mineral in humans (12).…”

Section: Discussionmentioning

confidence: 99%

Short-term voluntary exercise in the rat causes bone modeling without initiating a physiological stress response

Rosa¹,

Firth²,

Blair³

et al. 2010

American Journal of Physiology-Regulatory, Integrative and Comp

View full text Add to dashboard Cite

research has revealed a neuroendocrine connection between the skeleton and metabolism. Exercise alters both bone modeling and energy balance and may be useful in further developing our understanding of this complex interplay. However, research in this field requires an animal model of exercise that does not cause a physiological stress response in the exercised subjects. In this study, we develop a model of short-term voluntary exercise in the female rat that causes bone modeling without causing stress. Rats were randomly assigned to one of three age-matched groups: control, tower climbing, and squat exercise (rising to an erect bipedal stance). Exercise for 21 days resulted in bone modeling as assessed by peripheral quantitative computed tomography. Fecal corticosterone output was used to assess physiological stress at three time points during the study (preexercise, early exercise, and late in the exercise period). There were no differences in fecal corticosterone levels between groups or time points. This model of voluntary exercise in the rat will be useful for future studies of the influence of exercise on the relationship between skeletal and metabolic health and may be appropriate for investigation of the developmental origins of those effects. computed tomography; corticosterone; exercise; metabolism; stress RECENT ADVANCES IN OUR UNDERSTANDING of the dynamic relationship between body structure and metabolism have revealed a neuroendocrine connection between bone remodeling and energy balance, with both bone and fat acting as endocrine organs (14). The osteoblast-specific protein osteocalcin regulates glucose handling through effects on insulin secretion and sensitivity (33). This action is in turn mediated by the adipokine leptin, which inhibits insulin secretion through direct effects on pancreatic ␤-cells (18) and through inhibition of osteocalcin activity (25). The interplay between bone and metabolism has recently been further elucidated by the discovery that the Forkhead family transcription factor FoxO1, a key regulator of insulin handling in multiple tissues, also acts within the osteoblast to control osteocalcin expression and bioactivity (46).Exercise stimulates modeling of the musculoskeletal system (19, 55, 65), alters metabolism (40), and enhances brain function (17), and thus exercise provides an excellent means of exploring the neuroendocrine connection between bone, fat, and energy balance. The rat model of exercise has been used extensively to study the physiological effects of physical activity using such exercise modalities as swimming (24, 32), running (20,29,41,49,52), jumping (57), tower climbing (43), rising to an erect bipedal stance (11, 64), and weight lifting (62). The effects of exercise on bone have been widely characterized in the rat. Ovariectomized rats undergo changes in bone structure that are nearly identical to those seen in human osteoporosis (28,42), and these animals have proven useful for the study of exercise interventions in osteoporosis treatment (36).In examini...

show abstract

Section: Discussionmentioning

confidence: 99%

Short-term voluntary exercise in the rat causes bone modeling without initiating a physiological stress response

Rosa¹,

Firth²,

Blair³

et al. 2010

American Journal of Physiology-Regulatory, Integrative and Comp

View full text Add to dashboard Cite

show abstract

“…In addition to the structural separation within the labyrinth zone that prevents direct contact between maternal and fetal blood supplies (depicted in Figure 1, inset), metabolizing enzymes localized within trophoblasts facilitate fetal protection from excess glucocorticoids and amines (Brown et al, 1996;Nguyen et al, 1999). These barrier enzymes can be sensitive to maternal stress, where, eg, reduced placental expression of the glucocorticoid-inactivating enzyme, 11β-hydroxysteroid dehydrogenase type-2 (11βHSD2), has been associated with maternal anxiety and depressed mood in humans, as well as with chronic maternal stress in rodents (Blakeley et al, 2013;Jensen Peña et al, 2012;Mairesse et al, 2007;O'Donnell et al, 2012;Pankevich et al, 2009;Ponder et al, 2011). The result is for a potential fetal glucocorticoid overexposure to impact ongoing developmental events including a restriction of fetal growth, premature maturation of proliferative neural precursors, and altered HPA axis development (Seckl and Holmes, 2007).…”

Section: Transplacental Barrier Permeabilitymentioning

confidence: 99%

The Placenta as a Mediator of Stress Effects on Neurodevelopmental Reprogramming

Bronson

Bale

2015

Neuropsychopharmacol

205

180

View full text Add to dashboard Cite

Adversity experienced during gestation is a predictor of lifetime neuropsychiatric disease susceptibility. Specifically, maternal stress during pregnancy predisposes offspring to sex-biased neurodevelopmental disorders, including schizophrenia, attention deficit/hyperactivity disorder, and autism spectrum disorders. Animal models have demonstrated disease-relevant endophenotypes in prenatally stressed offspring and have provided unique insight into potential programmatic mechanisms. The placenta has a critical role in the deleterious and sex-specific effects of maternal stress and other fetal exposures on the developing brain. Stress-induced perturbations of the maternal milieu are conveyed to the embryo via the placenta, the maternal-fetal intermediary responsible for maintaining intrauterine homeostasis. Disruption of vital placental functions can have a significant impact on fetal development, including the brain, outcomes that are largely sex-specific. Here we review the novel involvement of the placenta in the transmission of the maternal adverse environment and effects on the developing brain.

show abstract

“…In humans and in animal models, placental 11β-HSD2 expression is reduced in adverse situations, including poor maternal nutrition or maternal stress (13)(14)(15). Bypass of this protective enzyme, be it through synthetic glucocorticoids that are poor substrates (9,16), inhibition (by liquorice), or genetic ablation of Hsd11b2 that encodes 11β-HSD2 (10), reduces placental weight.…”

mentioning

confidence: 99%

Pravastatin ameliorates placental vascular defects, fetal growth, and cardiac function in a model of glucocorticoid excess

Wyrwoll

Noble

Thomson

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Fetoplacental glucocorticoid overexposure is a significant mechanism underlying fetal growth restriction and the programming of adverse health outcomes in the adult. Placental glucocorticoid inactivation by 11β-hydroxysteroid dehydrogenase type 2 (11β-HSD2) plays a key role. We previously discovered that Hsd11b2 −/− mice, lacking 11β-HSD2, show marked underdevelopment of the placental vasculature. We now explore the consequences for fetal cardiovascular development and whether this is reversible. We studied Hsd11b2 +/+ , Hsd11b2 +/− , and Hsd11b2 −/− littermates from heterozygous (Hsd11b +/− ) matings at embryonic day (E)14.5 and E17.5, where all three genotypes were present to control for maternal effects. Using high-resolution ultrasound, we found that umbilical vein blood velocity in Hsd11b2 −/− fetuses did not undergo the normal gestational increase seen in Hsd11b2 +/+ littermates. Similarly, the resistance index in the umbilical artery did not show the normal gestational decline. Surprisingly, given that 11β-HSD2 absence is predicted to initiate early maturation, the E/A wave ratio was reduced at E17.5 in Hsd11b2 −/− fetuses, suggesting impaired cardiac function. Pravastatin administration from E6.5, which increases placental vascular endothelial growth factor A and, thus, vascularization, increased placental fetal capillary volume, ameliorated the aberrant umbilical cord velocity, normalized fetal weight, and improved the cardiac function of Hsd11b2 −/− fetuses. This improved cardiac function occurred despite persisting indications of increased glucocorticoid exposure in the Hsd11b2 −/− fetal heart. Thus, the pravastatin-induced enhancement of fetal capillaries within the placenta and the resultant hemodynamic changes correspond with restored fetal cardiac function. Statins may represent a useful therapeutic approach to intrauterine growth retardation due to placental vascular hypofunction.placenta | 11β-HSD2 | glucocorticoids | fetal heart | developmental programming

show abstract

Maternal stress alters endocrine function of the feto-placental unit in rats

Cited by 342 publications

References 71 publications

Short-term voluntary exercise in the rat causes bone modeling without initiating a physiological stress response

Short-term voluntary exercise in the rat causes bone modeling without initiating a physiological stress response

The Placenta as a Mediator of Stress Effects on Neurodevelopmental Reprogramming

Pravastatin ameliorates placental vascular defects, fetal growth, and cardiac function in a model of glucocorticoid excess

Contact Info

Product

Resources

About