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Volume 2018, Article ID 5689165, 12 pages
https://doi.org/10.1155/2018/5689165
Review Article

Perinatal Programming of Circadian Clock-Stress Crosstalk

Institute of Neurobiology, Center of Brain, Behavior & Metabolism, University of Lübeck, Marie-Curie Street, 23562 Lübeck, Germany

Correspondence should be addressed to Henrik Oster; ed.hsku@retso.kirneh

Received 10 September 2017; Accepted 26 December 2017; Published 8 February 2018

Academic Editor: Oliver Stork

Copyright © 2018 Mariana Astiz and Henrik Oster. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. Dibner, U. Schibler, and U. Albrecht, “The mammalian circadian timing system: organization and coordination of central and peripheral clocks,” Annual Review of Physiology, vol. 72, no. 1, pp. 517–549, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Ralph, R. Foster, F. Davis, and M. Menaker, “Transplanted suprachiasmatic nucleus determines circadian period,” Science, vol. 247, no. 4945, pp. 975–978, 1990. View at Publisher · View at Google Scholar
  3. H. Oster, S. Damerow, S. Kiessling et al., “The circadian rhythm of glucocorticoids is regulated by a gating mechanism residing in the adrenal cortical clock,” Cell Metabolism, vol. 4, no. 2, pp. 163–173, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. U. Schibler, J. Ripperger, and S. A. Brown, “Peripheral circadian oscillators in mammals: time and food,” Journal of Biological Rhythms, vol. 18, no. 3, pp. 250–260, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. S.-H. Yoo, S. Yamazaki, P. L. Lowrey et al., “PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 15, pp. 5339–5346, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Guo, J. M. Brewer, A. Champhekar, R. B. S. Harris, and E. L. Bittman, “Differential control of peripheral circadian rhythms by suprachiasmatic-dependent neural signals,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 8, pp. 3111–3116, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Husse, A. Leliavski, A. H. Tsang, H. Oster, and G. Eichele, “The light-dark cycle controls peripheral rhythmicity in mice with a genetically ablated suprachiasmatic nucleus clock,” The FASEB Journal, vol. 28, no. 11, pp. 4950–4960, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Husse, G. Eichele, and H. Oster, “Synchronization of the mammalian circadian timing system: light can control peripheral clocks independently of the SCN clock: alternate routes of entrainment optimize the alignment of the body’s circadian clock network with external time,” BioEssays, vol. 37, no. 10, pp. 1119–1128, 2015. View at Publisher · View at Google Scholar · View at Scopus
  9. J. L. Barclay, A. H. Tsang, and H. Oster, “Chapter 10 - interaction of central and peripheral clocks in physiological regulation,” Progress in Brain Research, vol. 199, pp. 163–181, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Balsalobre, S. A. Brown, L. Marcacci et al., “Resetting of circadian time in peripheral tissues by glucocorticoid signaling,” Science, vol. 289, no. 5488, pp. 2344–2347, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Dumbell, O. Matveeva, and H. Oster, “Circadian clocks, stress, and immunity,” Frontiers in Endocrinology, vol. 7, p. 37, 2016. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Ehrhart-Bornstein, J. P. Hinson, S. R. Bornstein, W. A. Scherbaum, and G. P. Vinson, “Intraadrenal interactions in the regulation of adrenocortical steroidogenesis,” Endocrine Reviews, vol. 19, no. 2, pp. 101–143, 1998. View at Publisher · View at Google Scholar
  13. A. Ishida, T. Mutoh, T. Ueyama et al., “Light activates the adrenal gland: timing of gene expression and glucocorticoid release,” Cell Metabolism, vol. 2, no. 5, pp. 297–307, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. G. H. Son, S. Chung, H. K. Choe et al., “Adrenal peripheral clock controls the autonomous circadian rhythm of glucocorticoid by causing rhythmic steroid production,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 52, pp. 20970–20975, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. R. M. Sapolsky, L. M. Romero, and A. U. Munck, “How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions,” Endocrine Reviews, vol. 21, no. 1, pp. 55–89, 2000. View at Publisher · View at Google Scholar
  16. E. R. de Kloet, M. Joëls, and F. Holsboer, “Stress and the brain: from adaptation to disease,” Nature Reviews Neuroscience, vol. 6, no. 6, pp. 463–475, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. M. F. Dallman, S. F. Akana, C. S. Cascio, D. N. Darlington, L. Jacobson, and N. Levin, “Regulation of ACTH secretion: variations on a theme of B,” Recent Progress in Hormone Research, vol. 43, pp. 113–173, 1987. View at Google Scholar
  18. A. H. Tsang, M. Astiz, B. Leinweber, and H. Oster, “Rodent models for the analysis of tissue clock function in metabolic rhythms research,” Frontiers in Endocrinology, vol. 8, p. 27, 2017. View at Publisher · View at Google Scholar · View at Scopus
  19. K. A. Lamia, K.-F. Storch, and C. J. Weitz, “Physiological significance of a peripheral tissue circadian clock,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 39, pp. 15172–15177, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Oishi, N. Amagai, H. Shirai, K. Kadota, N. Ohkura, and N. Ishida, “Genome-wide expression analysis reveals 100 adrenal gland-dependent circadian genes in the mouse liver,” DNA Research, vol. 12, no. 3, pp. 191–202, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. A. B. Reddy, E. S. Maywood, N. A. Karp et al., “Glucocorticoid signaling synchronizes the liver circadian transcriptome,” Hepatology, vol. 45, no. 6, pp. 1478–1488, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. M. C. Holmes, K. L. French, and J. R. Seckl, “Modulation of serotonin and corticosteroid receptor gene expression in the rat hippocampus with circadian rhythm and stress,” Molecular Brain Research, vol. 28, no. 2, pp. 186–192, 1995. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Joëls and E. L. S. Van Riel, “Mineralocorticoid and glucocorticoid receptor-mediated effects on serotonergic transmission in health and disease,” Annals of the New York Academy of Sciences, vol. 1032, no. 1, pp. 301–303, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. F. Levi and U. Schibler, “Circadian rhythms: mechanisms and therapeutic implications,” Annual Review of Pharmacology and Toxicology, vol. 47, no. 1, pp. 593–628, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. B. Karlsson, A. Knutsson, and B. Lindahl, “Is there an association between shift work and having a metabolic syndrome? Results from a population based study of 27,485 people,” Occupational & Environmental Medicine, vol. 58, no. 11, pp. 747–752, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Cho, A. Ennaceur, J. C. Cole, and C. K. Suh, “Chronic jet lag produces cognitive deficits,” Journal of Neuroscience, vol. 20, no. 6, article RC66, 2000. View at Google Scholar
  27. T. A. LeGates, C. M. Altimus, H. Wang et al., “Aberrant light directly impairs mood and learning through melanopsin-expressing neurons,” Nature, vol. 491, no. 7425, pp. 594–598, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Dickmeis, B. D. Weger, and M. Weger, “The circadian clock and glucocorticoids – interactions across many time scales,” Molecular and Cellular Endocrinology, vol. 380, no. 1-2, pp. 2–15, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. B. J. Kolber, L. Wieczorek, and L. J. Muglia, “Hypothalamic-pituitary-adrenal axis dysregulation and behavioral analysis of mouse mutants with altered glucocorticoid or mineralocorticoid receptor function,” Stress, vol. 11, no. 5, pp. 321–338, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. N. Nader, G. P. Chrousos, and T. Kino, “Interactions of the circadian CLOCK system and the HPA axis,” Trends in Endocrinology & Metabolism, vol. 21, no. 5, pp. 277–286, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. N. C. Nicolaides, E. Charmandari, G. P. Chrousos, and T. Kino, “Circadian endocrine rhythms: the hypothalamic-pituitary-adrenal axis and its actions,” Annals of the New York Academy of Sciences, vol. 1318, no. 1, pp. 71–80, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Y.-L. So, T. U. Bernal, M. L. Pillsbury, K. R. Yamamoto, and B. J. Feldman, “Glucocorticoid regulation of the circadian clock modulates glucose homeostasis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 41, pp. 17582–17587, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. A. J. Galliher-Beckley, J. G. Williams, J. B. Collins, and J. A. Cidlowski, “Glycogen synthase kinase 3β-mediated serine phosphorylation of the human glucocorticoid receptor redirects gene expression profiles,” Molecular and Cellular Biology, vol. 28, no. 24, pp. 7309–7322, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Takabe, K. Mochizuki, and T. Goda, “De-phosphorylation of GR at Ser203 in nuclei associates with GR nuclear translocation and GLUT5 gene expression in Caco-2 cells,” Archives of Biochemistry and Biophysics, vol. 475, no. 1, pp. 1–6, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Surjit, K. P. Ganti, A. Mukherji et al., “Widespread negative response elements mediate direct repression by agonist-liganded glucocorticoid receptor,” Cell, vol. 145, no. 2, pp. 224–241, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. B. L. Conway-Campbell, R. A. Sarabdjitsingh, M. A. McKenna et al., “Glucocorticoid ultradian rhythmicity directs cyclical gene pulsing of the clock gene period 1 in rat hippocampus,” Journal of Neuroendocrinology, vol. 22, no. 10, pp. 1093–1100, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. N. Nader, G. P. Chrousos, and T. Kino, “Circadian rhythm transcription factor CLOCK regulates the transcriptional activity of the glucocorticoid receptor by acetylating its hinge region lysine cluster: potential physiological implications,” The FASEB Journal, vol. 23, no. 5, pp. 1572–1583, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. K. A. Lamia, S. J. Papp, R. T. Yu et al., “Cryptochromes mediate rhythmic repression of the glucocorticoid receptor,” Nature, vol. 480, no. 7378, pp. 552–556, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Okabe, R. Chavan, S. S. Fonseca Costa, A. Brenna, J. A. Ripperger, and U. Albrecht, “REV-ERBα influences the stability and nuclear localization of the glucocorticoid receptor,” Journal of Cell Science, vol. 129, no. 21, pp. 4143–4154, 2016. View at Publisher · View at Google Scholar · View at Scopus
  40. U. Albrecht, “Molecular mechanisms in mood regulation involving the circadian clock,” Frontiers in Neurology, vol. 8, p. 30, 2017. View at Publisher · View at Google Scholar · View at Scopus
  41. G. Hampp, J. A. Ripperger, T. Houben et al., “Regulation of monoamine oxidase a by circadian-clock components implies clock influence on mood,” Current Biology, vol. 18, no. 9, pp. 678–683, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Chung, E. J. Lee, S. Yun et al., “Impact of circadian nuclear receptor REV-ERBα on midbrain dopamine production and mood regulation,” Cell, vol. 157, no. 4, pp. 858–868, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Carpentier, P. Sacchetti, P. Ségard, B. Staels, and P. Lefebvre, “The glucocorticoid receptor is a co-regulator of the orphan nuclear receptor Nurr1,” Journal of Neurochemistry, vol. 104, no. 3, pp. 777–789, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Zhang, N. F. Lahens, H. I. Ballance, M. E. Hughes, and J. B. Hogenesch, “A circadian gene expression atlas in mammals: implications for biology and medicine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 45, pp. 16219–16224, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. P. Pezük, J. A. Mohawk, L. A. Wang, and M. Menaker, “Glucocorticoids as entraining signals for peripheral circadian oscillators,” Endocrinology, vol. 153, no. 10, pp. 4775–4783, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Kiessling, G. Eichele, and H. Oster, “Adrenal glucocorticoids have a key role in circadian resynchronization in a mouse model of jet lag,” The Journal of Clinical Investigation, vol. 120, no. 7, pp. 2600–2609, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Tahara, S. Aoyama, and S. Shibata, “The mammalian circadian clock and its entrainment by stress and exercise,” The Journal of Physiological Sciences, vol. 67, no. 1, pp. 1–10, 2017. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Tahara, T. Shiraishi, Y. Kikuchi et al., “Entrainment of the mouse circadian clock by sub-acute physical and psychological stress,” Scientific Reports, vol. 5, no. 1, p. 11417, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Dunn, L. Scheving, and P. Millet, “Circadian variation in stress-evoked increases in plasma corticosterone,” American Journal of Physiology, vol. 223, no. 2, pp. 402–406, 1972. View at Publisher · View at Google Scholar
  50. F. P. Gibbs, “Circadian variation of ether-induced corticosterone secretion in the rat,” American Journal of Physiology, vol. 219, no. 2, pp. 288–292, 1970. View at Publisher · View at Google Scholar
  51. A. Kalsbeek, M. Ruiter, S. E. La Fleur, C. Van Heijningen, and R. M. Buijs, “The diurnal modulation of hormonal responses in the rat varies with different stimuli,” Journal of Neuroendocrinology, vol. 15, no. 12, pp. 1144–1155, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. C. E. Koch, B. Leinweber, B. C. Drengberg, C. Blaum, and H. Oster, “Interaction between circadian rhythms and stress,” Neurobiology of Stress, vol. 6, pp. 57–67, 2017. View at Publisher · View at Google Scholar · View at Scopus
  53. M. J. Bradbury, C. S. Cascio, K. A. Scribner, and M. F. Dallman, “Stress-induced adrenocorticotropin secretion: diurnal responses and decreases during stress in the evening are not dependent on corticosterone,” Endocrinology, vol. 128, no. 2, pp. 680–688, 1991. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Torrellas, C. Guaza, J. Borrell, and S. Borrell, “Adrenal hormones and brain catecholamines responses to morning and afternoon immobilization stress in rats,” Physiology & Behavior, vol. 26, no. 1, pp. 129–133, 1981. View at Publisher · View at Google Scholar · View at Scopus
  55. C. E. Koch, M. S. Bartlang, J. T. Kiehn et al., “Time-of-day-dependent adaptation of the HPA axis to predictable social defeat stress,” Journal of Endocrinology, vol. 231, no. 3, pp. 209–221, 2016. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Leliavski, A. Shostak, J. Husse, and H. Oster, “Impaired glucocorticoid production and response to stress in Arntl-deficient male mice,” Endocrinology, vol. 155, no. 1, pp. 133–142, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. F. W. Turek, C. Joshu, A. Kohsaka et al., “Obesity and metabolic syndrome in circadian clock mutant mice,” Science, vol. 308, no. 5724, pp. 1043–1045, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Yang, A. Liu, A. Weidenhammer et al., “The role of mPer2 clock gene in glucocorticoid and feeding rhythms,” Endocrinology, vol. 150, no. 5, pp. 2153–2160, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Di Segni, D. Andolina, and R. Ventura, “Long-term effects of early environment on the brain: lesson from rodent models,” Seminars in Cell & Developmental Biology, 2017, In press. View at Publisher · View at Google Scholar
  60. J. R. Seckl, “Prenatal glucocorticoids and long-term programming,” European Journal of Endocrinology, vol. 151, Supplement 3, pp. U49–U62, 2004. View at Publisher · View at Google Scholar
  61. P. J. Brunton, “Programming the brain and behaviour by early-life stress: a focus on neuroactive steroids,” Journal of Neuroendocrinology, vol. 27, no. 6, pp. 468–480, 2015. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Lesage, F. del-Favero, M. Leonhardt et al., “Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat,” Journal of Endocrinology, vol. 181, no. 2, pp. 291–296, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. J. Mairesse, V. Silletti, C. Laloux et al., “Chronic agomelatine treatment corrects the abnormalities in the circadian rhythm of motor activity and sleep/wake cycle induced by prenatal restraint stress in adult rats,” International Journal of Neuropsychopharmacology, vol. 16, no. 2, pp. 323–338, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. T. J. Varcoe, M. J. Boden, A. Voultsios, M. D. Salkeld, L. Rattanatray, and D. J. Kennaway, “Characterisation of the maternal response to chronic phase shifts during gestation in the rat: implications for fetal metabolic programming,” PLoS One, vol. 8, no. 1, article e53800, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. J. C. Borniger, Z. D. McHenry, B. A. Abi Salloum, and R. J. Nelson, “Exposure to dim light at night during early development increases adult anxiety-like responses,” Physiology & Behavior, vol. 133, pp. 99–106, 2014. View at Publisher · View at Google Scholar · View at Scopus
  66. G. Coleman and M. M. Canal, “Postnatal light effects on pup stress axis development are independent of maternal behavior,” Frontiers in Neuroscience, vol. 11, p. 46, 2017. View at Publisher · View at Google Scholar · View at Scopus
  67. G. Coleman, J. Gigg, and M. M. Canal, “Postnatal light alters hypothalamic-pituitary-adrenal axis function and induces a depressive-like phenotype in adult mice,” European Journal of Neuroscience, vol. 44, no. 10, pp. 2807–2817, 2016. View at Publisher · View at Google Scholar · View at Scopus
  68. S. E. Voiculescu, D. le Duc, A. E. Roșca et al., “Behavioral and molecular effects of prenatal continuous light exposure in the adult rat,” Brain Research, vol. 1650, pp. 51–59, 2016. View at Publisher · View at Google Scholar · View at Scopus
  69. N. Mendez, D. Halabi, C. Spichiger et al., “Gestational chronodisruption impairs circadian physiology in rat male offspring, increasing the risk of chronic disease,” Endocrinology, vol. 157, no. 12, pp. 4654–4668, 2016. View at Publisher · View at Google Scholar · View at Scopus
  70. B. L. Smarr, A. D. Grant, L. Perez, I. Zucker, and L. J. Kriegsfeld, “Maternal and early-life circadian disruption have long-lasting negative consequences on offspring development and adult behavior in mice,” Scientific Reports, vol. 7, no. 1, p. 3326, 2017. View at Publisher · View at Google Scholar
  71. B. Claustrat, J.-L. Valatx, C. Harthé, and J. Brun, “Effect of constant light on prolactin and corticosterone rhythms evaluated using a noninvasive urine sampling protocol in the rat,” Hormone and Metabolic Research, vol. 40, no. 6, pp. 398–403, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. A. S. Ivy, K. L. Brunson, C. Sandman, and T. Z. Baram, “Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress,” Neuroscience, vol. 154, no. 3, pp. 1132–1142, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. K. Hoshino, Y. Wakatsuki, M. Iigo, and S. Shibata, “Circadian Clock mutation in dams disrupts nursing behavior and growth of pups,” Endocrinology, vol. 147, no. 4, pp. 1916–1923, 2006. View at Publisher · View at Google Scholar · View at Scopus
  74. Q. Wan, K. Gao, H. Rong et al., “Histone modifications of the Crhr1 gene in a rat model of depression following chronic stress,” Behavioural Brain Research, vol. 271, pp. 1–6, 2014. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Maccari and S. Morley-Fletcher, “Effects of prenatal restraint stress on the hypothalamus–pituitary–adrenal axis and related behavioural and neurobiological alterations,” Psychoneuroendocrinology, vol. 32, Supplement 1, pp. S10–S15, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. V. Van Waes, M. Enache, I. Dutriez et al., “Hypo-response of the hypothalamic-pituitary-adrenocortical axis after an ethanol challenge in prenatally stressed adolescent male rats,” European Journal of Neuroscience, vol. 24, no. 4, pp. 1193–1200, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Koehl, Y. Bjijou, M. Le Moal, and M. Cador, “Nicotine-induced locomotor activity is increased by preexposure of rats to prenatal stress,” Brain Research, vol. 882, no. 1-2, pp. 196–200, 2000. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Darnaudéry, M. Perez-Martin, G. Bélizaire, S. Maccari, and L. M. Garcia-Segura, “Insulin-like growth factor 1 reduces age-related disorders induced by prenatal stress in female rats,” Neurobiology of Aging, vol. 27, no. 1, pp. 119–127, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Morley-Fletcher, M. Darnaudery, M. Koehl, P. Casolini, O. Van Reeth, and S. Maccari, “Prenatal stress in rats predicts immobility behavior in the forced swim test: effects of a chronic treatment with tianeptine,” Brain Research, vol. 989, no. 2, pp. 246–251, 2003. View at Publisher · View at Google Scholar · View at Scopus
  80. H. M. Sickmann, C. Skoven, J. F. Bastlund et al., “Sleep patterning changes in a prenatal stress model of depression,” Journal of Developmental Origins of Health and Disease, vol. 29, pp. 1–10, 2017. View at Publisher · View at Google Scholar
  81. J. Mairesse, G. van Camp, E. Gatta et al., “Sleep in prenatally restraint stressed rats, a model of mixed anxiety-depressive disorder,” Advances in Neurobiology, vol. 10, pp. 27–44, 2015. View at Publisher · View at Google Scholar · View at Scopus
  82. V. Joseph, J. Mamet, F. Lee, Y. Dalmaz, and O. Van Reeth, “Prenatal hypoxia impairs circadian synchronisation and response of the biological clock to light in adult rats,” The Journal of Physiology, vol. 543, no. 1, pp. 387–395, 2002. View at Publisher · View at Google Scholar · View at Scopus
  83. L. Burd and H. Wilson, “Fetal, infant, and child mortality in a context of alcohol use,” American Journal of Medical Genetics Part C: Seminars in Medical Genetics, vol. 127C, no. 1, pp. 51–58, 2004. View at Publisher · View at Google Scholar
  84. S. G. Tractenberg, M. L. Levandowski, L. A. de Azeredo et al., “An overview of maternal separation effects on behavioural outcomes in mice: evidence from a four-stage methodological systematic review,” Neuroscience & Biobehavioral Reviews, vol. 68, pp. 489–503, 2016. View at Publisher · View at Google Scholar · View at Scopus
  85. J.-H. Lee, H. J. Kim, J. G. Kim et al., “Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation,” Neuroscience Research, vol. 58, no. 1, pp. 32–39, 2007. View at Publisher · View at Google Scholar · View at Scopus
  86. S. Santarelli, C. Zimmermann, G. Kalideris et al., “An adverse early life environment can enhance stress resilience in adulthood,” Psychoneuroendocrinology, vol. 78, pp. 213–221, 2017. View at Publisher · View at Google Scholar · View at Scopus
  87. C. E. Wood and C.-D. Walker, “Fetal and neonatal HPA axis,” Comprehensive Physiology, vol. 6, no. 1, pp. 33–62, 2015. View at Publisher · View at Google Scholar · View at Scopus
  88. M. V. Ugrumov, “Developing hypothalamus in differentiation of neurosecretory neurons and in establishment of pathways for neurohormone transport,” International Review of Cytology, vol. 129, pp. 207–267, 1991. View at Publisher · View at Google Scholar
  89. M. Grino, W. Scott Young III, and J. M. Burgunder, “Ontogeny of expression of the corticotropin-releasing factor gene in the hypothalamic paraventricular nucleus and of the proopiomelanocortin gene in rat pituitary,” Endocrinology, vol. 124, no. 1, pp. 60–68, 1989. View at Publisher · View at Google Scholar · View at Scopus
  90. J. J. Lee and E. P. Widmaier, “Gene array analysis of the effects of chronic adrenocorticotropic hormone in vivo on immature rat adrenal glands,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 96, no. 1, pp. 31–44, 2005. View at Publisher · View at Google Scholar · View at Scopus
  91. C.-C. J. Huang, M.-C. M. Shih, N.-C. Hsu, Y. Chien, and B. Chung, “Fetal glucocorticoid synthesis is required for development of fetal adrenal medulla and hypothalamus feedback suppression,” Endocrinology, vol. 153, no. 10, pp. 4749–4756, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. S. Levine, “The ontogeny of the hypothalamic-pituitary-adrenal axis. The influence of maternal factors,” Annals of the New York Academy of Sciences, vol. 746, no. 1, pp. 275–288, 1994. View at Publisher · View at Google Scholar
  93. M. Schmidt, L. Enthoven, M. van der Mark, S. Levine, E. R. de Kloet, and M. S. Oitzl, “The postnatal development of the hypothalamic-pituitary-adrenal axis in the mouse,” International Journal of Developmental Neuroscience, vol. 21, no. 3, pp. 125–132, 2003. View at Publisher · View at Google Scholar · View at Scopus
  94. C. D. Walker, R. M. Sapolsky, M. J. Meaney, W. W. Vale, and C. L. Rivier, “Increased pituitary sensitivity to glucocorticoid feedback during the stress nonresponsive period in the neonatal rat,” Endocrinology, vol. 119, no. 4, pp. 1816–1821, 1986. View at Publisher · View at Google Scholar · View at Scopus
  95. M. E. Stanton and S. Levine, “Inhibition of infant glucocorticoid stress response: specific role of maternal cues,” Developmental Psychobiology, vol. 23, no. 5, pp. 411–426, 1990. View at Publisher · View at Google Scholar · View at Scopus
  96. Y. Chen, C. M. Dubé, C. J. Rice, and T. Z. Baram, “Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone,” The Journal of Neuroscience, vol. 28, no. 11, pp. 2903–2911, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. H. J. Hulshof, A. Novati, A. Sgoifo, P. G. M. Luiten, J. A. den Boer, and P. Meerlo, “Maternal separation decreases adult hippocampal cell proliferation and impairs cognitive performance but has little effect on stress sensitivity and anxiety in adult Wistar rats,” Behavioural Brain Research, vol. 216, no. 2, pp. 552–560, 2011. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Tzanoulinou and C. Sandi, “The programming of the social brain by stress during childhood and adolescence: from rodents to humans,” Current Topics in Behavioral Neurosciences, vol. 30, pp. 411–429, 2017. View at Publisher · View at Google Scholar · View at Scopus
  99. L. Goldman, C. Winget, G. W. Hollingshead, and S. Levine, “Postweaning development of negative feedback in the pituitary-adrenal system of the rat,” Neuroendocrinology, vol. 12, no. 3, pp. 199–211, 1973. View at Publisher · View at Google Scholar
  100. C. E. Wood, “Development and programming of the hypothalamus-pituitary-adrenal axis,” Clinical Obstetrics and Gynecology, vol. 56, no. 3, pp. 610–621, 2013. View at Publisher · View at Google Scholar · View at Scopus
  101. C. S. Kabrita and F. C. Davis, “Development of the mouse suprachiasmatic nucleus: determination of time of cell origin and spatial arrangements within the nucleus,” Brain Research, vol. 1195, pp. 20–27, 2008. View at Publisher · View at Google Scholar · View at Scopus
  102. S. Sekaran, D. Lupi, S. L. Jones et al., “Melanopsin-dependent photoreception provides earliest light detection in the mammalian retina,” Current Biology, vol. 15, no. 12, pp. 1099–1107, 2005. View at Publisher · View at Google Scholar · View at Scopus
  103. M. Seron-Ferre, G. J. Valenzuela, and C. Torres-Farfan, “Circadian clocks during embryonic and fetal development,” Birth Defects Research Part C: Embryo Today: Reviews, vol. 81, no. 3, pp. 204–214, 2007. View at Publisher · View at Google Scholar · View at Scopus
  104. D. Landgraf, C. Achten, F. Dallmann, and H. Oster, “Embryonic development and maternal regulation of murine circadian clock function,” Chronobiology International, vol. 32, no. 3, pp. 416–427, 2015. View at Publisher · View at Google Scholar · View at Scopus
  105. D. Landgraf, C. E. Koch, and H. Oster, “Embryonic development of circadian clocks in the mammalian suprachiasmatic nuclei,” Frontiers in Neuroanatomy, vol. 8, p. 143, 2014. View at Publisher · View at Google Scholar · View at Scopus
  106. E. Christ, H.-W. Korf, and C. von Gall, “Chapter 6 - when does it start ticking? Ontogenetic development of the mammalian circadian system,” Progress in Brain Research, vol. 199, pp. 105–118, 2012. View at Publisher · View at Google Scholar · View at Scopus
  107. A. Sumová, Z. Bendová, M. Sládek et al., “The rat circadian clockwork and its photoperiodic entrainment during development,” Chronobiology International, vol. 23, no. 1-2, pp. 237–243, 2006. View at Publisher · View at Google Scholar · View at Scopus
  108. H. Ohta, S. Xu, T. Moriya et al., “Maternal feeding controls fetal biological clock,” PLoS One, vol. 3, no. 7, article e2601, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. V. G. Moisiadis and S. G. Matthews, “Glucocorticoids and fetal programming part 1: outcomes,” Nature Reviews Endocrinology, vol. 10, no. 7, pp. 391–402, 2014. View at Publisher · View at Google Scholar · View at Scopus
  110. J. S. Meyer, “Early adrenalectomy stimulates subsequent growth and development of the rat brain,” Experimental Neurology, vol. 82, no. 2, pp. 432–446, 1983. View at Publisher · View at Google Scholar · View at Scopus
  111. T. J. Cole, J. A. Blendy, A. P. Monaghan et al., “Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation,” Genes & Development, vol. 9, no. 13, pp. 1608–1621, 1995. View at Publisher · View at Google Scholar
  112. J. R. Seckl, “Glucocorticoids, developmental ‘programming’ and the risk of affective dysfunction,” Progress in Brain Research, vol. 167, pp. 17–34, 2008. View at Publisher · View at Google Scholar · View at Scopus
  113. M. D. Wharfe, P. J. Mark, and B. J. Waddell, “Circadian variation in placental and hepatic clock genes in rat pregnancy,” Endocrinology, vol. 152, no. 9, pp. 3552–3560, 2011. View at Publisher · View at Google Scholar · View at Scopus
  114. C. S. Wyrwoll, J. R. Seckl, and M. C. Holmes, “Altered placental function of 11β-hydroxysteroid dehydrogenase 2 knockout mice,” Endocrinology, vol. 150, no. 3, pp. 1287–1293, 2009. View at Publisher · View at Google Scholar · View at Scopus
  115. E. C. Cottrell, J. R. Seckl, M. C. Holmes, and C. S. Wyrwoll, “Foetal and placental 11β-HSD2: a hub for developmental programming,” Acta Physiologica, vol. 210, no. 2, pp. 288–295, 2014. View at Publisher · View at Google Scholar · View at Scopus
  116. S. Navailles, R. Zimnisky, and C. Schmauss, “Expression of glucocorticoid receptor and early growth response gene 1 during postnatal development of two inbred strains of mice exposed to early life stress,” Developmental Neuroscience, vol. 32, no. 2, pp. 139–148, 2010. View at Publisher · View at Google Scholar · View at Scopus
  117. J. D. Gray, J. F. Kogan, J. Marrocco, and B. S. McEwen, “Genomic and epigenomic mechanisms of glucocorticoids in the brain,” Nature Reviews Endocrinology, vol. 13, no. 11, pp. 661–673, 2017. View at Publisher · View at Google Scholar
  118. I. C. G. Weaver, N. Cervoni, F. A. Champagne et al., “Epigenetic programming by maternal behavior,” Nature Neuroscience, vol. 7, no. 8, pp. 847–854, 2004. View at Publisher · View at Google Scholar · View at Scopus
  119. M. J. Meaney, J. Diorio, D. Francis et al., “Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: the effects of thyroid hormones and serotonin,” The Journal of Neuroscience, vol. 20, no. 10, pp. 3926–3935, 2000. View at Google Scholar
  120. R. Alikhani-Koopaei, F. Fouladkou, F. J. Frey, and B. M. Frey, “Epigenetic regulation of 11β-hydroxysteroid dehydrogenase type 2 expression,” The Journal of Clinical Investigation, vol. 114, no. 8, pp. 1146–1157, 2004. View at Publisher · View at Google Scholar
  121. J. Chen, A. N. Evans, Y. Liu, M. Honda, J. M. Saavedra, and G. Aguilera, “Maternal deprivation in rats is associated with corticotrophin-releasing hormone (CRH) promoter hypomethylation and enhances CRH transcriptional responses to stress in adulthood,” Journal of Neuroendocrinology, vol. 24, no. 7, pp. 1055–1064, 2012. View at Publisher · View at Google Scholar · View at Scopus
  122. Y. Wu, A. V. Patchev, G. Daniel, O. F. X. Almeida, and D. Spengler, “Early-life stress reduces DNA methylation of the Pomc gene in male mice,” Endocrinology, vol. 155, no. 5, pp. 1751–1762, 2014. View at Publisher · View at Google Scholar · View at Scopus
  123. F. Rakers, S. Rupprecht, M. Dreiling, C. Bergmeier, O. W. Witte, and M. Schwab, “Transfer of maternal psychosocial stress to the fetus,” Neuroscience & Biobehavioral Reviews, 2017, In press. View at Publisher · View at Google Scholar · View at Scopus
  124. Y. Dong, G. Liu, Z. Wang, J. Li, J. Cao, and Y. Chen, “Effects of catecholaminergic nerve lesion on endometrial development during early pregnancy in mice,” Histology and Histopathology, vol. 31, no. 4, pp. 415–424, 2016. View at Publisher · View at Google Scholar · View at Scopus
  125. Y. Okatani, K. Okamoto, K. Hayashi, A. Wakatsuki, S. Tamura, and Y. Sagara, “Maternal-fetal transfer of melatonin in pregnant women near term,” Journal of Pineal Research, vol. 25, no. 3, pp. 129–134, 1998. View at Publisher · View at Google Scholar · View at Scopus
  126. L. Thomas, C. C. Purvis, J. E. Drew, D. R. Abramovich, and L. M. Williams, “Melatonin receptors in human fetal brain: 2-[125I]iodomelatonin binding and MT1 gene expression,” Journal of Pineal Research, vol. 33, no. 4, pp. 218–224, 2002. View at Publisher · View at Google Scholar · View at Scopus
  127. C. Torres-Farfan, V. Rocco, C. Monsó et al., “Maternal melatonin effects on clock gene expression in a nonhuman primate fetus,” Endocrinology, vol. 147, no. 10, pp. 4618–4626, 2006. View at Publisher · View at Google Scholar · View at Scopus
  128. L. P. Shearman and D. R. Weaver, “Distinct pharmacological mechanisms leading to c-fos gene expression in the fetal suprachiasmatic nucleus,” Journal of Biological Rhythms, vol. 16, no. 6, pp. 531–540, 2001. View at Publisher · View at Google Scholar · View at Scopus
  129. C. Jud and U. Albrecht, “Circadian rhythms in murine pups develop in absence of a functional maternal circadian clock,” Journal of Biological Rhythms, vol. 21, no. 2, pp. 149–154, 2006. View at Publisher · View at Google Scholar · View at Scopus
  130. S. Reppert and W. Schwartz, “Maternal coordination of the fetal biological clock in utero,” Science, vol. 220, no. 4600, pp. 969–971, 1983. View at Publisher · View at Google Scholar
  131. T. J. Varcoe, A. Voultsios, K. L. Gatford, and D. J. Kennaway, “The impact of prenatal circadian rhythm disruption on pregnancy outcomes and long-term metabolic health of mice progeny,” Chronobiology International, vol. 33, no. 9, pp. 1171–1181, 2016. View at Publisher · View at Google Scholar · View at Scopus
  132. A.-L. Opperhuizen, L. W. M. van Kerkhof, K. I. Proper, W. Rodenburg, and A. Kalsbeek, “Rodent models to study the metabolic effects of shiftwork in humans,” Frontiers in Pharmacology, vol. 6, p. 50, 2015. View at Publisher · View at Google Scholar · View at Scopus
  133. J. Ryan, T. Mansell, P. Fransquet, and R. Saffery, “Does maternal mental well-being in pregnancy impact the early human epigenome?” Epigenomics, vol. 9, no. 3, pp. 313–332, 2017. View at Publisher · View at Google Scholar · View at Scopus
  134. A. S. Khashan, K. M. Abel, R. McNamee et al., “Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events,” Archives of General Psychiatry, vol. 65, no. 2, pp. 146–152, 2008. View at Publisher · View at Google Scholar · View at Scopus
  135. T. G. O’Connor, Y. Ben-Shlomo, J. Heron, J. Golding, D. Adams, and V. Glover, “Prenatal anxiety predicts individual differences in cortisol in pre-adolescent children,” Biological Psychiatry, vol. 58, no. 3, pp. 211–217, 2005. View at Publisher · View at Google Scholar · View at Scopus
  136. S. S. H. Simons, R. Beijers, A. H. N. Cillessen, and C. de Weerth, “Development of the cortisol circadian rhythm in the light of stress early in life,” Psychoneuroendocrinology, vol. 62, pp. 292–300, 2015. View at Publisher · View at Google Scholar · View at Scopus
  137. C. de Weerth, R. H. Zijl, and J. K. Buitelaar, “Development of cortisol circadian rhythm in infancy,” Early Human Development, vol. 73, no. 1-2, pp. 39–52, 2003. View at Publisher · View at Google Scholar · View at Scopus
  138. J. L. Zhu, N. H. Hjollund, A.-M. N. Andersen, and J. Olsen, “Shift work, job stress, and late fetal loss: the National Birth Cohort in Denmark,” Journal of Occupational and Environmental Medicine, vol. 46, no. 11, pp. 1144–1149, 2004. View at Publisher · View at Google Scholar · View at Scopus
  139. A. Lewy, R. Sack, L. Miller, and T. Hoban, “Antidepressant and circadian phase-shifting effects of light,” Science, vol. 235, no. 4786, pp. 352–354, 1987. View at Publisher · View at Google Scholar
  140. C. Vetter and F. A. J. L. Scheer, “Circadian biology: uncoupling human body clocks by food timing,” Current Biology, vol. 27, no. 13, pp. R656–R658, 2017. View at Publisher · View at Google Scholar
  141. N. Alexander, F. Rosenlöcher, L. Dettenborn et al., “Impact of antenatal glucocorticoid therapy and risk of preterm delivery on intelligence in term-born children,” The Journal of Clinical Endocrinology & Metabolism, vol. 101, no. 2, pp. 581–589, 2016. View at Publisher · View at Google Scholar · View at Scopus
  142. E. Asztalos, “Antenatal corticosteroids: a risk factor for the development of chronic disease,” Journal of Nutrition and Metabolism, vol. 2012, Article ID 930591, 9 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  143. T. F. Yeh, Y. J. Lin, H. C. Lin et al., “Outcomes at school age after postnatal dexamethasone therapy for lung disease of prematurity,” The New England Journal of Medicine, vol. 350, no. 13, pp. 1304–1313, 2004. View at Publisher · View at Google Scholar · View at Scopus
  144. D. Roberts, J. Brown, N. Medley, and S. R. Dalziel, “Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth,” Cochrane Database of Systematic Reviews, vol. 3, article CD004454, 2017. View at Publisher · View at Google Scholar · View at Scopus
  145. R. Beijers, J. K. Buitelaar, and C. de Weerth, “Mechanisms underlying the effects of prenatal psychosocial stress on child outcomes: beyond the HPA axis,” European Child & Adolescent Psychiatry, vol. 23, no. 10, pp. 943–956, 2014. View at Publisher · View at Google Scholar · View at Scopus
  146. D. H. Brandon, D. Holditch-Davis, and M. Belyea, “Preterm infants born at less than 31 weeks’ gestation have improved growth in cycled light compared with continuous near darkness,” The Journal of Pediatrics, vol. 140, no. 2, pp. 192–199, 2002. View at Publisher · View at Google Scholar · View at Scopus
  147. Y. Kaneshi, H. Ohta, K. Morioka et al., “Influence of light exposure at nighttime on sleep development and body growth of preterm infants,” Scientific Reports, vol. 6, no. 1, article 21680, 2016. View at Publisher · View at Google Scholar · View at Scopus