Glucocorticoid-sensitive period of corticotroph development-Implications for mechanisms of early life stress.
POMC cell clusters
behaviour
cortisol
pituitary
temporal dynamics
Journal
Journal of neuroendocrinology
ISSN: 1365-2826
Titre abrégé: J Neuroendocrinol
Pays: United States
ID NLM: 8913461
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
19
12
2022
received:
13
06
2022
accepted:
20
12
2022
medline:
23
11
2023
pubmed:
21
1
2023
entrez:
20
1
2023
Statut:
ppublish
Résumé
Corticotrophs are intermediaries in the hypothalamic-pituitary-adrenal (HPA) axis, which plays a crucial role in stress response in vertebrates. The HPA axis displays an intricate mode of negative feedback regulation, whereby the peripheral effector, cortisol inhibits the secretion of its upstream regulator, adrenocorticotropic hormone (ACTH) from proopiomelanocortin (POMC)-expressing cells in the pituitary. While the feedback regulation of the HPA axis is well characterized in the adult organism, the effect of feedback regulation on the development of corticotrophs is poorly understood. Here, we studied the effect of glucocorticoids on the development of POMC-expressing cells in the zebrafish pituitary. The development of POMC cells showed a steady increase in numbers between 2-6 days post fertilization. Inhibition of endogenous glucocorticoid synthesis resulted in an increase in POMC cell number due to reduced developmental feedback inhibition of cortisol on POMC cells. Conversely, addition of exogenous dexamethasone at a critical developmental window led to a decrease in corticotroph cell number, mimicking greater feedback control due to increased cortisol levels. Finally, developmental dysregulation of ACTH levels resulted in impaired anxiety-like and stress-coping behaviours. Hence, we identified a sensitive developmental window for the effect of glucocorticoids on corticotrophs and demonstrate the downstream effect on stress-responsive behaviour.
Substances chimiques
Adrenocorticotropic Hormone
9002-60-2
Glucocorticoids
0
Hydrocortisone
WI4X0X7BPJ
Pro-Opiomelanocortin
66796-54-1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13229Subventions
Organisme : Israel Science Foundation
ID : 349/21
Organisme : US-Israel Bi-national Science Foundation
ID : 2017325
Organisme : Israel Ministry of Science and Technology
ID : 3-16548
Informations de copyright
© 2022 The Authors. Journal of Neuroendocrinology published by John Wiley & Sons Ltd on behalf of British Society for Neuroendocrinology.
Références
Smith SM, Vale WW. The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin Neurosci. 2006;8(4):383-395.
Jones MT, Hillhouse EW, Burden JL. Dynamics and mechanics of corticosteroid feedback at the hypothalamus and anterior pituitary gland. J Endocrinol. 1977;73(3):405-417.
Gjerstad JK, Lightman SL, Spiga F. Role of glucocorticoid negative feedback in the regulation of HPA axis pulsatility. Stress. 2018;21(5):403-416.
Karin O, Raz M, Tendler A, et al. A new model for the HPA axis explains dysregulation of stress hormones on the timescale of weeks. Mol Syst Biol. 2020;16(7):e9510.
Sheng JA, Bales NJ, Myers SA, et al. The hypothalamic-pituitary-adrenal axis: development, programming actions of hormones, and maternal-fetal interactions. Front Behav Neurosci. 2020;14:601939.
Alsop D, Vijayan MM. Development of the corticosteroid stress axis and receptor expression in zebrafish. Am J Physiol Regul Integr Comp Physiol. 2008;294(3):R711-R719.
Biran J, Wircer E, Blechman J, Levkowitz G. Development and function of the zebrafish neuroendocrine system. In: Ludwig M, Levkowitz G, eds. Model Animals in Neuroendocrinology: From Mouse to Man. Wiley-Blackwell; 2018:101-131.
Amir-Zilberstein L, Blechman J, Sztainberg Y, et al. Homeodomain protein otp and activity-dependent splicing modulate neuronal adaptation to stress. Neuron. 2012;73(2):279-291.
Yeh CM, Glöck M, Ryu S. An optimized whole-body cortisol quantification method for assessing stress levels in larval zebrafish. PLoS One. 2013;8(11):e79406.
Aleström P, D'Angelo L, Midtlyng PJ, et al. Zebrafish: housing and husbandry recommendations. Lab Anim. 2020;54(3):213-224.
Liu NA, Huang H, Yang Z, et al. Pituitary corticotroph ontogeny and regulation in transgenic zebrafish. Mol Endocrinol. 2003;17(5):959-966.
Anbalagan S, Gordon L, Blechman J, et al. Pituicyte cues regulate the development of permeable neuro-vascular interfaces. Developmental Cell. 2018;47(6):711-726.e5. https://doi.org/10.1016/j.devcel.2018.10.017
Sternberg JR, Severi KE, Fidelin K, et al. Optimization of a neurotoxin to investigate the contribution of excitatory interneurons to speed modulation in vivo. Curr Biol. 2016;26(17):2319-2328.
Anbalagan S, Blechman J, Gliksberg M, et al. Robo2 regulates synaptic oxytocin content by affecting actin dynamics. ELife, 2019:8. https://doi.org/10.7554/elife.45650
Swaminathan A, Gliksberg M, Anbalagan S, Wigoda N, Levkowitz G. Stress resilience is established during development and is regulated by complement factors. Cell Reports. 2022;42(1):111973. https://doi.org/10.1016/j.celrep.2022.111973
Sun L, Xu W, He J, Yin Z. In vivo alternative assessment of the chemicals that interfere with anterior pituitary POMC expression and interrenal steroidogenesis in POMC: EGFP transgenic zebrafish. Toxicol Appl Pharmacol. 2010;248(3):217-225.
To TT, Hahner S, Nica G, et al. Pituitary-interrenal interaction in zebrafish interrenal organ development. Mol Endocrinol. 2007;21(2):472-485.
Kalueff AV, Gebhardt M, Stewart AM, et al. Towards a comprehensive catalog of zebrafish behavior 1.0 and beyond. Zebrafish. 2013;10(1):70-86.
Steenbergen PJ, Richardson MK, Champagne DL. Patterns of avoidance behaviours in the light/dark preference test in young juvenile zebrafish: a pharmacological study. Behav Brain Res. 2011;222(1):15-25.
Biran J, Gliksberg M, Shirat I, et al. Splice-specific deficiency of the PTSD-associated gene PAC1 leads to a paradoxical age-dependent stress behavior. Sci Rep. 2020;10(1):9559.
Herzog W, Zeng X, Lele Z, et al. Adenohypophysis formation in the zebrafish and its dependence on sonic hedgehog. Dev Biol. 2003;254(1):36-49.
Alsop D, Vijayan MM. Molecular programming of the corticosteroid stress axis during zebrafish development. Comp Biochem Physiol A Mol Integr Physiol. 2009;153(1):49-54.
Alderman SL, Bernier NJ. Ontogeny of the corticotropin-releasing factor system in zebrafish. Gen Comp Endocrinol. 2009;164(1):61-69.
Katie M. Early life stress and psychopathology. In: Harkness KL, Hayden EP, eds. The Oxford Handbook of Stress and Mental Health. Oxford library of psychology; 2018.
Smith KE, Pollak SD. Early life stress and development: potential mechanisms for adverse outcomes. J Neurodev Disord. 2020;12(1):34.
Carr CP, Martins CM, Stingel AM, Lemgruber VB, Juruena MF. The role of early life stress in adult psychiatric disorders: a systematic review according to childhood trauma subtypes. J Nerv Ment Dis. 2013;201(12):1007-1020.