Publication Cover
Stress
The International Journal on the Biology of Stress
Volume 21, 2018 - Issue 1
767
Views
7
CrossRef citations to date
0
Altmetric
Original Article

Adrenal-dependent and -independent stress-induced Per1 mRNA in hypothalamic paraventricular nucleus and prefrontal cortex of male and female rats

, , , , &
Pages 69-83 | Received 13 Jun 2017, Accepted 09 Nov 2017, Published online: 22 Nov 2017

References

  • Al-Safadi, S., Al-Safadi, A., Branchaud, M., Rutherford, S., Dayanandan, A., Robinson, B., … Yamazaki, S. (2014). Stress-induced changes in the expression of the clock protein PERIOD1 in the rat limbic forebrain and hypothalamus: Role of stress type, time of day, and predictability. PLoS One, 9, e111166. doi: 10.1371/journal.pone.0111166
  • Arnsten, A.F.T., & Rubia, K. (2012). Neurobiological circuits regulating attention, cognitive control, motivation, and emotion: Disruptions in neurodevelopmental psychiatric disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 51, 356–367. doi: 10.1016/j.jaac.2012.01.008
  • Babb, J.A., Masini, C.V., Day, H.E.W., & Campeau, S. (2014). Habituation of hypothalamic-pituitary-adrenocortical axis hormones to repeated homotypic stress and subsequent heterotypic stressor exposure in male and female rats. Stress, 17, 224–234. doi: 10.3109/10253890.2014.905534
  • Bae, K., Jin, X., Maywood, E.S., Hastings, M.H., Reppert, S.M., & Weaver, D.R. (2001). Differential functions of mPer1, mPer2, and mPer3 in the SCN circadian clock. Neuron, 30, 525–536. doi: 10.1016/S0896-6273(01)00302-6
  • Balsalobre, A., Brown, S.A., Marcacci, L., Tronche, F., Kellendonk, C., Reichardt, H.M., … Schibler, U. (2000). Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science (New York, N.Y.), 289, 2344–2347. doi: 10.1126/science.289.5488.2344
  • Bland, S.T., Schmid, M.J., Der-Avakian, A., Watkins, L.R., Spencer, R.L., & Maier, S.F. (2005). Expression of c-Fos and BDNF mRNA in subregions of the prefrontal cortex of male and female rats after acute uncontrollable stress. Brain Research, 1051, 90–99. doi: 10.1016/j.brainres.2005.05.065
  • Bohacek, J., Manuella, F., Roszkowski, M., & Mansuy, I.M. (2015). Hippocampal gene expression induced by cold swim stress depends on sex and handling. Psychoneuroendocrinology, 52, 1–12. doi: 10.1016/j.psyneuen.2014.10.026
  • Buijs, R.M., Markman, M., Nunes-Cardoso, B., Hou, Y.X., & Shinn, S. (1993). Projections of the suprachiasmatic nucleus to stress-related areas in the rat hypothalamus: A light and electron microscopic study. The Journal of Comparative Neurology, 335, 42–54. doi: 10.1002/cne.903350104
  • Buijs, R.M., La Fleur, S.E., Wortel, J., Van Heyningen, C., Zuiddam, L., Mettenleiter, T.C., … Niijima, A. (2003). The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons. The Journal of Comparative Neurology, 464, 36–48. doi: 10.1002/cne.10765
  • Bunger, M.K., Wilsbacher, L.D., Moran, S.M., Clendenin, C., Radcliffe, L.A., Hogenesch, J.B., … Bradfield, C.A. (2000). Mop3 is an essential component of the master circadian pacemaker in mammals. Cell, 103, 1009–1017. doi: 10.1016/S0092-8674(00)00205-1
  • Bunney, B.G., Li, J.Z., Walsh, D.M., Stein, R., Vawter, M.P., Cartagena, P., … Bunney, W.E. (2015). Circadian dysregulation of clock genes: Clues to rapid treatments in major depressive disorder. Molecular Psychiatry, 20, 48–55. doi: 10.1038/mp.2014.138
  • Burioka, N., Takata, M., Okano, Y., Ohdo, S., Fukuoka, Y., Miyata, M., … Shimizu, E. (2005). Dexamethasone influences human clock gene expression in bronchial epithelium and peripheral blood mononuclear cells in vitro. Chronobiology International, 22, 585–590. doi: 10.1081/CBI-200062416
  • Cheon, S., Park, N., Cho, S., & Kim, K. (2013). Glucocorticoid-mediated period 2 induction delays the phase of circadian rhythm. Nucleic Acids Research, 41, 6161–6174. doi: 10.1093/nar/gkt307
  • Chun, L.E., Woodruff, E.R., Morton, S., Hinds, L.R., & Spencer, R.L. (2015). Variations in phase and amplitude of rhythmic clock gene expression across prefrontal cortex, hippocampus, amygdala, and hypothalamic paraventricular and suprachiasmatic nuclei of male and female rats. Journal of Biological Rhythms, 30, 417–436. doi: 10.1177/0748730415598608
  • Conway-Campbell, B.L., Sarabdjitsingh, R.A., McKenna, M.A., Pooley, J.R., Kershaw, Y.M., Meijer, O.C., … Lightman, S.L. (2010). Glucocorticoid ultradian rhythmicity directs cyclical gene pulsing of the clock gene period 1 in rat hippocampus. Journal of Neuroendocrinology, 22, 1093–1100. doi: 10.1111/j.1365-2826.2010.02051.x
  • Dibner, C., Schibler, U., & Albrecht, U. (2010). The mammalian circadian timing system: Organization and coordination of central and peripheral clocks. Annual Review of Physiology, 72, 517–549. doi: 10.1146/annurev-physiol-021909-135821
  • Dickmeis, T. (2009). Glucocorticoids and the circadian clock. The Journal of Endocrinology, 200, 3–22. doi: 10.1677/JOE-08-0415
  • Droste, S.K., de Groote, L., Lightman, S.L., Reul, J.M.H.M., & Linthorst, A.C.E. (2009). The ultradian and circadian rhythms of free corticosterone in the brain are not affected by gender: An in vivo microdialysis study in Wistar rats. Journal of Neuroendocrinology, 21, 132–140. doi: 10.1111/j.1365-2826.2008.01811.x
  • Dunn, A.J. (1988). Stress-related changes in cerebral catecholamine and indoleamine metabolism: Lack of effect of adrenalectomy and corticosterone. Journal of Neurochemistry, 51, 406–412. doi: 10.1111/j.1471-4159.1988.tb01053.x
  • Edelstein, K., & Amir, S. (1995). Non-photic manipulations induce expression of Fos protein in the suprachiasmatic nucleus and intergeniculate leaflet in the rat. Brain Research, 690, 254–258. doi: 10.1016/0006-8993(95)00736-A
  • Figueiredo, H.F., Dolgas, C.M., & Herman, J.P. (2002). Stress activation of cortex and hippocampus is modulated by sex and stage of estrus. Endocrinology, 143, 2534–2540. doi: 10.1210/endo.143.7.8888
  • Ginsberg, A.B., Campeau, S., Day, H.E., & Spencer, R.L. (2003). Acute glucocorticoid pretreatment suppresses stress-induced hypothalamic-pituitary-adrenal axis hormone secretion and expression of corticotropin-releasing hormone hnRNA but does not affect c-Fos mRNA or Fos protein expression in the paraventricular nucleus of the hypothalamus. Journal of Neuroendocrinology, 15, 1075–1083. doi: 10.1046/j.1365-2826.2003.01100.x
  • Harbour, V.L., Weigl, Y., Robinson, B., Amir, S., & Bartell, P.A. (2014). Phase differences in expression of circadian clock genes in the central nucleus of the amygdala, dentate gyrus, and suprachiasmatic nucleus in the rat. PLoS One, 9, e103309. doi: 10.1371/journal.pone.0103309
  • Hastings, M., O’Neill, J.S., & Maywood, E.S. (2007). Circadian clocks: Regulators of endocrine and metabolic rhythms. The Journal of Endocrinology, 195, 187–198. doi: 10.1677/JOE-07-0378
  • Heidbreder, C.A., & Groenewegen, H.J. (2003). The medial prefrontal cortex in the rat: Evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neuroscience and Biobehavioral Reviews, 27, 555–579. doi: 10.1016/j.neubiorev.2003.09.003
  • Hughes, P., & Dragunow, M. (1995). Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmacological Reviews, 47, 133–178.
  • Kalsbeek, A., Liu, J., Lei, J., Timmermans, L., Foppen, E., Cailotto, C., & Fliers, E. (2012a). Differential involvement of the suprachiasmatic nucleus in lipopolysaccharide-induced plasma glucose and corticosterone responses. Chronobiology International, 29, 835–849. doi: 10.3109/07420528.2012.699123
  • Kalsbeek, A., van der Spek, R., Lei, J., Endert, E., Buijs, R.M., & Fliers, E. (2012b). Circadian rhythms in the hypothalamo-pituitary-adrenal (HPA) axis. Molecular and Cellular Endocrinology, 349, 20–29. doi: 10.1016/j.mce.2011.06.042
  • Kessler, R. (2003). Epidemiology of women and depression. Journal of Affective Disorders, 74, 5–13. https://doi.org/10.1016/S0165-0327(02)00426-3
  • Kovács, K.J. (1998). Invited review c-Fos as a transcription factor: A stressful (re)view from a functional map. Neurochemistry International, 33, 287–297. https://doi.org/10.1016/S0197-0186(98)00023-0
  • Li, J.Z., Bunney, B.G., Meng, F., Hagenauer, M.H., Walsh, D.M., Vawter, M.P., … Bunney, W.E. (2013). Circadian patterns of gene expression in the human brain and disruption in major depressive disorder. Proceedings of the National Academy of Sciences of the United States of America, 110, 9950–9955. doi: 10.1073/pnas.1305814110
  • Logan, R.W., Edgar, N., Gillman, A.G., Hoffman, D., Zhu, X., & McClung, C.A. (2015). Chronic stress induces brain region-specific alterations of molecular rhythms that correlate with depression-like behavior in mice. Biological Psychiatry, 78, 249–258. doi: 10.1016/j.biopsych.2015.01.011
  • Mayberg, H.S., Liotti, M., Brannan, S.K., McGinnis, S., Mahurin, R.K., Jerabek, P.A., … Fox, P.T. (1999). Reciprocal limbic-cortical function and negative mood: Converging PET findings in depression and normal sadness. The American Journal of Psychiatry, 156, 675–682.
  • McCarthy, M.J., & Welsh, D.K. (2012). Cellular circadian clocks in mood disorders. Journal of Biological Rhythms, 27, 339–352. doi: 10.1177/0748730412456367
  • Mifsud, K.R., & Reul, J.M.H.M. (2016). Acute stress enhances heterodimerization and binding of corticosteroid receptors at glucocorticoid target genes in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 113, 11336–11341. doi: 10.1073/pnas.1605246113
  • Moghaddam, B. (2002). Stress activation of glutamate neurotransmission in the prefrontal cortex: Implications for dopamine-associated psychiatric disorders. Biological Psychiatry, 51, 775–787. doi: 10.1016/S0006-3223(01)01362-2
  • Mukherjee, S., Coque, L., Cao, J.L., Kumar, J., Chakravarty, S., Asaithamby, A., … McClung, C.A. (2010). Knockdown of clock in the ventral tegmental area through RNA interference results in a mixed state of mania and depression-like behavior. Biological Psychiatry, 68, 503–511. doi: 10.1016/j.biopsych.2010.04.031
  • Oishi, K., Sakamoto, K., Okada, T., Nagase, T., & Ishida, N. (1998). Antiphase circadian expression between BMAL1 and period homologue mRNA in the suprachiasmatic nucleus and peripheral tissues of rats. Biochemical and Biophysical Research Communications, 253, 199–203.
  • Oster, H., Werner, C., Magnone, M.C., Mayser, H., Feil, R., Seeliger, M.W., … Albrecht, U. (2003). cGMP-dependent protein kinase II modulates mPer1 and mPer2 gene induction and influences phase shifts of the circadian clock. Current Biology, 13, 725–733. doi: 10.1016/S0960-9822(03)00252-5
  • Paxinos, G., & Watson, C. (1998). The rat brain in stereotaxic coordinates (4th ed.). San Diego (CA): Academic Press.
  • Rath, M.F., Rohde, K., Fahrenkrug, J., & Møller, M. (2013). Circadian clock components in the rat neocortex: Daily dynamics, localization and regulation. Brain Structure and Function, 218, 551–562. doi: 10.1007/s00429-012-0415-4
  • Razzoli, M., Karsten, C., Yoder, J.M., Bartolomucci, A., & Engeland, W.C. (2014). Chronic subordination stress phase advances adrenal and anterior pituitary clock gene rhythms. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 307, R198–R205. doi: 10.1152/ajpregu.00101.2014
  • Reddy, A.B., Maywood, E.S., Karp, N.A., King, V.M., Inoue, Y., Gonzalez, F.J., … Hastings, M.H. (2007). Glucocorticoid signaling synchronizes the liver circadian transcriptome. Hepatology (Baltimore, Md.), 45, 1478–1488. doi: 10.1002/hep.21571
  • Reddy, T.E., Gertz, J., Crawford, G.E., Garabedian, M.J., & Myers, R.M. (2012). The hypersensitive glucocorticoid response specifically regulates period 1 and expression of circadian genes. Molecular and Cellular Biology, 32, 3756–3767. doi: 10.1128/MCB.00062-12
  • Reppert, S.M., & Weaver, D.R. (2002). Coordination of circadian timing in mammals. Nature, 418, 935–941. doi: 10.1038/nature00965
  • Savontaus, E., Conwell, I.M., & Wardlaw, S.L. (2002). Effects of adrenalectomy on AGRP, POMC, NPY and CART gene expression in the basal hypothalamus of fed and fasted rats. Brain Research, 958, 130–138. https://doi.org/10.1016/S0006-8993(02)03674-0
  • Shearman, L.P., Zylka, M.J., Weaver, D.R., Kolakowski, L.F., & Reppert, S.M. (1997). Two period homologs: Circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron, 19, 1261–1269. doi: 10.1016/S0896-6273(00)80417-1
  • Shigeyoshi, Y., Taguchi, K., Yamamoto, S., Takekida, S., Yan, L., Tei, H., … Okamura, H. (1997). Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell, 91, 1043–1053. doi: 10.1016/S0092-8674(00)80494-8
  • So, A.Y.L., Bernal, T.U., Pillsbury, M.L., Yamamoto, K.R., & Feldman, B.J. (2009). Glucocorticoid regulation of the circadian clock modulates glucose homeostasis. Proceedings of the National Academy of Sciences of the United States of America, 106, 17582–17587. doi: 10.1073/pnas.0909733106
  • Spencer, R.L., & Deak, T. (2017). A users guide to HPA axis research. Physiology & Behavior, 178, 43–65. doi: 10.1016/j.physbeh.2016.11.014
  • Spencer, S., Falcon, E., Kumar, J., Krishnan, V., Mukherjee, S., Birnbaum, S.G., & McClung, C.A. (2013). Circadian genes period 1 and period 2 in the nucleus accumbens regulate anxiety-related behavior. European Journal of Neuroscience, 37, 242–250. doi: 10.1111/ejn.12010
  • Spiga, F., Walker, J.J., Terry, J.R., & Lightman, S.L. (2014). HPA axis – rhythms (Vol. 4, pp. 1273–1298). Hoboken (NJ): John Wiley & Sons, Inc.
  • Tahara, Y., Shiraishi, T., Kikuchi, Y., Haraguchi, A., Kuriki, D., Sasaki, H., … Shibata, S. (2015). Entrainment of the mouse circadian clock by sub-acute physical and psychological stress. Scientific Reports, 5, 11417. doi: 10.1038/srep11417
  • Takahashi, K., Yamada, T., Tsukita, S., Kaneko, K., Shirai, Y., Munakata, Y., … Katagiri, H. (2013). Chronic mild stress alters circadian expressions of molecular clock genes in the liver. American Journal of Physiology. Endocrinology and Metabolism, 304, E301–E309. doi: 10.1152/ajpendo.00388.2012
  • Takahashi, S., Yokota, S.-I., Hara, R., Kobayashi, T., Akiyama, M., Moriya, T., & Shibata, S. (2001). Physical and inflammatory stressors elevate circadian clock gene mPer1 mRNA levels in the paraventricular nucleus of the mouse. Endocrinology, 142, 4910–4917. doi: 10.1210/endo.142.11.8487
  • Tischkau, S.A., Mitchell, J.W., Tyan, S.-H., Buchanan, G.F., & Gillette, M.U. (2003). Ca2+/cAMP response element-binding Protein (CREB)-dependent activation of Per1 is required for light-induced signaling in the suprachiasmatic nucleus circadian clock. Journal of Biological Chemistry, 278, 718–723. doi: 10.1074/jbc.M209241200
  • Ulrich-Lai, Y.M., Arnhold, M.M., & Engeland, W.C. (2006). Adrenal splanchnic innervation contributes to the diurnal rhythm of plasma corticosterone in rats by modulating adrenal sensitivity to ACTH. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 290, R1128–R1135. doi: 10.1152/ajpregu.00042.2003
  • Ulrich-Lai, Y.M., & Herman, J.P. (2009). Neural regulation of endocrine and autonomic stress responses. Nature Reviews. Neuroscience, 10, 397–409. doi: 10.1038/nrn2647
  • Viau, V., & Meaney, M.J. (1991). Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology, 129, 2503–2511. doi: 10.1210/endo-129-5-2503
  • Watts, A.G., Swanson, L.W., & Sanchez-Watts, G. (1987). Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. The Journal of Comparative Neurology, 258, 204–229. doi: 10.1002/cne.902580204
  • Welsh, D.K., Takahashi, J.S., & Kay, S.A. (2010). Suprachiasmatic nucleus: Cell autonomy and network properties. Annual Review of Physiology, 72, 551–577. doi: 10.1146/annurev-physiol-021909-135919
  • Woodruff, E.R., Chun, L.E., Hinds, L.R., & Spencer, R.L. (2016). Diurnal corticosterone presence and phase modulate clock gene expression in the male rat prefrontal cortex. Endocrinology, 157, 1522–1534. doi: 10.1210/en.2015-1884
  • Yamamoto, T., Nakahata, Y., Soma, H., Akashi, M., Mamine, T., & Takumi, T. (2004). Transcriptional oscillation of canonical clock genes in mouse peripheral tissues. BMC Molecular Biology, 5, 18. doi: 10.1186/1471-2199-5-18
  • Yamamoto, T., Nakahata, Y., Tanaka, M., Yoshida, M., Soma, H., Shinohara, K., … Takumi, T. (2005). Acute physical stress elevates mouse period1 mRNA expression in mouse peripheral tissues via a glucocorticoid-responsive element. Journal of Biological Chemistry, 280, 42036–42043. doi: 10.1074/jbc.M509600200

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.