Early post-natal life stress induces permanent adrenocorticotropin-dependent hypercortisolism in male mice.
Cushing’s syndrome
Early-life stress
Metabolic syndrome
Mouse
Pituitary ACTH hypersecretion
Journal
Endocrine
ISSN: 1559-0100
Titre abrégé: Endocrine
Pays: United States
ID NLM: 9434444
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
09
11
2020
accepted:
10
02
2021
pubmed:
26
2
2021
medline:
9
7
2021
entrez:
25
2
2021
Statut:
ppublish
Résumé
It has been hypothesized that specific early-life stress (ES) procedures on CD-1 male mice produce diabetes-like alterations due to the failure of negative feedback of glucocorticoid hormone in the pituitary. The aim of this study is to investigate the possible mechanism that leads to this pathological model, framing it in a more specific clinical condition. Metabolic and hypothalamic-pituitary-adrenal-related hormones of stressed mice (SM) have been analyzed immediately after stress procedures (21 postnatal days, PND) and after 70 days of a peaceful (unstressed) period (90 PND). These data have been compared to parameters from age-matched controls (CTR), and mice treated during ES procedures with oligonucleotide antisense for pro-opiomelanocortin (AS-POMC). At 21 PND, SM presented an increased secretion of hypothalamic CRH and pituitary POMC-derived peptides, as well as higher plasmatic levels of ACTH and corticosterone vs. CTR. At 90 PND, SM showed hyperglycemia, with suppression of hypothalamic CRH, while pituitary and plasmatic ACTH levels, as well as plasma corticosterone, were constantly higher than in CTR. These values are accompanied by a progressive acceleration in gaining total body weight, which became significant vs. CTR at 90 PND together with a higher pituitary weight. Treatment with AS-POMC prevented all hormonal and metabolic alterations observed in SM, both at 21 and 90 PND. These findings show that these specific ES procedures affect the negative glucocorticoid feedback in the pituitary, but not in the hypothalamus, suggesting a novel model of ACTH-dependent hypercortisolism that can be prevented by silencing the POMC gene.
Identifiants
pubmed: 33630246
doi: 10.1007/s12020-021-02659-4
pii: 10.1007/s12020-021-02659-4
doi:
Substances chimiques
Adrenocorticotropic Hormone
9002-60-2
Corticosterone
W980KJ009P
Corticotropin-Releasing Hormone
9015-71-8
Pro-Opiomelanocortin
66796-54-1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
186-195Références
J.K. Gjerstad, S.L. Lightman, F. Spiga, Role of glucocorticoid negative feedback in the regulation of HPA axis pulsatility. Stress 21, 403 (2018)
pubmed: 29764284
pmcid: 6220752
E.T. Uchoa, G. Aguilera, J.P. Herman et al. Novel aspects of glucocorticoid actions. J. Neuroendocrinol. 26, 557 (2014)
pubmed: 24724595
pmcid: 4161987
N.C. Vamvakopoulos, G.P. Chrousos, Hormonal regulation of human corticotropin-releasing hormone gene expression: implications for the stress response and immune/inflammatory reaction. Endocr. Rev. 15, 409 (1994)
pubmed: 7988479
A.M. Bao, D.F. Swaab, The human hypothalamus in mood disorders: the HPA axis in the center. IBRO Rep. 6, 45 (2019)
pubmed: 31211281
A. Chatzittofis, S. Arver, K. Öberg et al. HPA axis dysregulation in men with hypersexual disorder. Psychoneuroendocrinology 63, 247 (2016)
pubmed: 26519779
F. Xiong, L. Zhang, Role of the hypothalamic-pituitary-adrenal axis in developmental programming of health and disease. Front. Neuroendocrinol. 34, 27 (2013)
pubmed: 23200813
A. Agorastos, P. Pervanidou, G.P. Chrousos et al. Developmental trajectories of early life stress and trauma: a narrative review on neurobiological aspects beyond stress system dysregulation. Front. Psychiatry 10, 118 (2019)
pubmed: 30914979
O. Cooper, V. Bonert, F. Moser et al. Altered pituitary gland structure and function in posttraumatic stress disorder. J. Endocr. Soc. 1, 577 (2017)
pubmed: 29264511
N. Sonino, G.A. Fava, S. Grandi et al. Stressful life events in the pathogenesis of Cushing’s syndrome. Clin. Endocrinol. 29, 617 (1988)
N. Sonino, G.A. Fava, M. Boscaro, A role for life events in the pathogenesis of Cushing’s disease. Clin. Endocrinol. 38, 261 (1993)
B. Catargi, V. Rigalleau, A. Poussin et al. Occult Cushing’s syndrome in type-2 diabetes. J. Clin. Endocrinol. Metab. 88, 5808 (2003)
pubmed: 14671173
I. Chiodini, M. Torlontano, A. Scillitani et al. Association of subclinical hypercortisolism with type 2 diabetes mellitus: a case-control study in hospitalized patients. Eur. J. Endocrinol. 153, 837 (2005)
pubmed: 16322389
J.W. Findling, H. Raff, Diagnosis of endocrine disease: differentiation of pathologic/neoplastic hypercortisolism (Cushing’s syndrome) from physiologic/non-neoplastic hypercortisolism (formerly known as pseudo-Cushing’s syndrome). Eur. J. Endocrinol. 176, R205 (2017)
pubmed: 28179447
E.B. Geer, J. Islam, C. Buettner, Mechanisms of glucocorticoid-induced insulin resistance: focus on adipose tissue function and lipid metabolism. Endocrinol. Metab. Clin. North Am. 43, 75 (2014)
pubmed: 24582093
pmcid: 3942672
H. Raff, T. Carroll, Cushing’s syndrome: from physiological principles to diagnosis and clinical care. J. Physiol. 593, 493 (2015)
pubmed: 25480800
pmcid: 4324701
C. Steffensen, O.M. Dekkers, J. Lyhne et al. Hypercortisolism in newly diagnosed type 2 diabetes: a prospective study of 384 newly diagnosed patients. Horm. Metab. Res. 51, 62 (2019)
pubmed: 30522146
A. Loizzo, S. Loizzo, G. Galietta et al. Overweight and metabolic and hormonal parameter disruption are induced in adult male mice by manipulations during lactation period. Pediatr. Res. 59, 111 (2006)
pubmed: 16326992
S. Loizzo, G. Campana, S. Vella et al. Post-natal stress-induced endocrine and metabolic alterations in mice at adulthood involve different pro-opiomelanocortin-derived peptides. Peptides 31, 2123 (2010)
pubmed: 20727932
A. Loizzo, S.M. Spampinato, G. Campana et al. Etiopathogenesis and pharmacological prevention of a type-2 diabetes model in male mice. J. Pharmacol. Exp. Ther. 364, 347 (2018)
pubmed: 29162628
N.C. Victoria, A.Z. Murphy, The long-term impact of early life pain on adult responses to anxiety and stress: Historical perspectives and empirical evidence. Exp. Neurol. 275, 261 (2016)
pubmed: 26210872
S.M. Mooney-Leber, S. Brummelte, Neonatal pain and reduced maternal care alter adult behavior and hypothalamic-pituitary-adrenal axis reactivity in a sex-specific manner. Dev. Psychobiol. 62, 631 (2019)
pubmed: 31788799
G. Galietta, A. Loizzo, S. Loizzo et al. Administration of antisense oligonucleotide against pro-opiomelanocortin prevents enduring hormonal alterations induced by neonatal handling in male mice. Eur. J. Pharmacol. 550, 180 (2006)
pubmed: 17045988
A. Loizzo, S.M. Spampinato, A. Fortuna et al. Antisense versus proopiomelanocortin mRNA reduces vascular risk in a murine model of type-2 diabetes following stress exposure in early post-natal life. Peptides 64, 34 (2015)
pubmed: 25554217
S. Spampinato, M. Canossa, L. Carboni et al. Inhibition of proopiomelanocortin expression by an oligodeoxynucleotide complementary to beta-endorphin mRNA. Proc. Natl Acad. Sci. USA 91, 8072 (1994)
pubmed: 8058759
R.M. Philpot, M.E. Engberg, L. Wecker, Effects of nicotine exposure on locomotor activity and pCREB levels in the ventral striatum of adolescent rats. Behav. Brain Res. 230, 62 (2012)
pubmed: 22301350
M. John, A.R. Lila, T. Bandgar et al. Diagnostic efficacy of midnight cortisol and midnight ACTH in the diagnosis and localisation of Cushing’s syndrome. Pituitary 13, 48 (2010)
pubmed: 19714471
S.C. Tzou, M.A. Landek-Salgado, H. Kimura et al. Preparation of mouse pituitary immunogen for the induction of experimental autoimmune hypophysitis. J. Vis. Exp. 46, 2182 (2010)
M.K. Gill, S. Karanth, A. Dutt et al. Effect of castration and steroid treatment on the release of gonadotropins by the rat pituitary-hypothalamus complex in vitro. Horm. Metab. Res. 17, 141 (1985)
pubmed: 3922864
S. Spampinato, A. Goldstein, Immunoreactive dynorphin in rat tissues and plasma. Neuropeptides 3, 193 (1983)
pubmed: 16229162
W.E. Nicholson, D.R. Davis, B.J. Sherrell et al. Rapid radioimmunoassay for corticotropin in unextracted human plasma. Clin. Chem. 30, 259 (1984)
pubmed: 6319046
F. Fontana, P. Bernardi, E.M. Pich et al. Opioid peptide modulation of circulatory and endocrine response to mental stress in humans. Peptides 18, 169 (1997)
pubmed: 9149287
M.M. Bradford, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248 (1976).
pubmed: 942051
S. Loizzo, S. Vella, A. Loizzo et al. Sexual dimorphic evolution of metabolic programming in non-genetic non-alimentary mild metabolic syndrome model in mice depends on feed-back mechanisms integrity for pro-opiomelanocortin-derived endogenous substances. Peptides 31, 1598 (2010)
pubmed: 20493223
V. Mela, F. Díaz, M.J. Vázquez et al. Interaction between neonatal maternal deprivation and serum leptin levels on metabolism, pubertal development, and sexual behavior in male and female rats. Biol. Sex. Differ. 7, 2 (2016)
pubmed: 26759712
pmcid: 4710050
R. M. Dores, Adrenocorticotropic hormone, melanocyte-stimulating hormone, and the melanocortin receptors: Revisiting the work of Robert Schwyzer: a thirty-year retrospective. Ann. N. Y. Acad. Sci. 1163, 93 (2009)
pubmed: 19456331
R.D. Cone, Studies on the physiological functions of the melanocortin system. Endocr. Rev. 27, 736 (2006)
pubmed: 17077189
J.P. Herman, J.G. Tasker, Paraventricular hypothalamic mechanisms of chronic stress adaptation. Front. Endocrinol. 7, 137 (2016)
C.J. Rice, C.A. Sandman, M.R. Lenjavi et al. A novel mouse model for acute and long-lasting consequences of early life stress. Endocrinology 149, 4892 (2008)
pubmed: 18566122
pmcid: 2582918
L. Groenink, A. Dirks, P.M. Verdouw et al. HPA axis dysregulation in mice overexpressing corticotropin releasing hormone. Biol. Psychiatry 51, 875 (2002)
pubmed: 12022960
M.J. Lee, P. Pramyothin, K. Karastergiou et al. Deconstructing the roles of glucocorticoids in adipose tissue biology and the development of central obesity. Biochim. Biophys. Acta 1842, 473 (2014)
pubmed: 23735216
C. Scaroni, M. Zilio, M. Foti et al. Glucose metabolism abnormalities in cushing syndrome: from molecular basis to clinical management. Endocr. Rev. 38, 189 (2017)
pubmed: 28368467
L.C. Martins, F.L. Conceição, E.S. Muxfeldt et al. Prevalence and associated factors of subclinical hypercortisolism in patients with resistant hypertension. J. Hypertens. 30, 967 (2012)
pubmed: 22406465
M. Terzolo, G. Reimondo, I. Chiodini et al. Screening of Cushing’s syndrome in outpatients with type 2 diabetes: results of a prospective multicentric study in Italy. Clin. Endocrinol. Metab. 97, 3467 (2012)
R. Pivonello, A.M. Isidori, M.C. De Martino, Complications of Cushing’s syndrome: state of the art. Lancet Diabetes Endocrinol. 4, 611 (2016)
pubmed: 27177728
V. Morelli, C. Aresta, A. Gaudio et al. Prediction of hypertension, diabetes and fractures in eucortisolemic women by measuring parameters of cortisol milieu. Endocrine 68, 411 (2020)
pubmed: 31989409
V. Morelli, A. Ghielmetti, A. Caldiroli, Mental health in patients with adrenal incidentalomas: is there a relation with different degrees of cortisol secretion? J. Clin. Endocrinol. Metab. 106, e130 (2020)
V. Morelli, C. Aresta, A. Gaudio et al. Prediction of hypertension, diabetes and fractures in eucortisolemic women by measuring parameters of cortisol milieu. Endocrine 68, 411 (2020)
pubmed: 31989409
G. Tirabassi, M. Boscaro, G. Arnaldi, Harmful effects of functional hypercortisolism: a working hypothesis. Endocrine 46, 370 (2014)
pubmed: 24282037
V. Morelli, F. Donadio, C. Eller-Vainicher et al. Role of glucocorticoid receptor polymorphism in adrenal incidentalomas. Eur. J. Clin. Investig. 40, 803 (2010)
R.N. Clayton, W.E. Farrell, Pituitary tumour clonality revisited. Front. Horm. Res. 32, 186 (2004)
pubmed: 15281347