Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
권호 표지
DOI QR코드

DOI QR Code

Enhancement of Anxiety and Modulation of TH and pERK Expressions in Amygdala by Repeated Injections of Corticosterone

  • Lim, Hee-Na (Department of Neuroscience and TIDRC, School of Medicine, Ewha Womans University) ;
  • Jang, So-Yong (Department of Neuroscience and TIDRC, School of Medicine, Ewha Womans University) ;
  • Lee, Yeon-Ju (Department of Neuroscience and TIDRC, School of Medicine, Ewha Womans University) ;
  • Moon, So-Hyeon (Department of Neuroscience and TIDRC, School of Medicine, Ewha Womans University) ;
  • Kim, Ji-Eun (Department of Neuroscience and TIDRC, School of Medicine, Ewha Womans University) ;
  • Oh, Sei-Kwan (Department of Neuroscience and TIDRC, School of Medicine, Ewha Womans University)
  • Received : 2012.05.14
  • Accepted : 2012.07.10
  • Published : 2012.07.31
Download PDF
⟨ Previous Next ⟩

Abstract

Repeated stress induces corticosterone release. However, it is not clear that stress results in further elevation of corticosterone levels, and the roles of released corticosterone to aggravate stress-related symptoms are also not clear. This study investigated whether neuronal modulation was induced in the amygdala after two kinds of stress, that is, such as electric shock and corticosterone injection. It was found that stress by electric shock decreased the expression of tyrosine hydoroxylase (TH) in the amygdala while the expression of pERK was increased. However, there is no difference in the expressions of TH and pERK in the frontal cortex compared with those of the control group. The level of corticosterone was significantly increased in the serum after stress. To determine the effect of corticosterone on the induction of anxiety and the expression of TH, the rats received corticosterone (20 mg or 40 mg/kg i.p.) for 1 day, 1 week, 2 weeks and 3 weeks, respectively. The spent time in open arms of the EPM (elevated plus maze) test was significantly decreased after 1 week, 2 weeks and 3 weeks. The time spent in open arms of the EPM test after repeated injections of corticosterone was significantly decreased in a dose-dependent manner. The expression of TH in the amygdala was reduced after following repeated corticosterone treatment for 2 weeks and 3 weeks. Collectively, this study suggests that corticosterone has a major role in the induction of anxiety and the modulation of TH expression, at least, in the amygdala.

Keywords

References

  1. Andreis, P. G., Neri, G. and Nussdorfer, G. G. (1991) Corticotropin-releasing hormone (CRH) directly stimulates corticosterone secretion by the rat adrenal gland. Endocrinology 128, 1198-1200. https://doi.org/10.1210/endo-128-2-1198
  2. Carrasco, G. A. and Van de Kar, L. D. (2003) Neuroendocrine pharmacology of stress. Eur. J. Pharmacol. 463, 235-272. https://doi.org/10.1016/S0014-2999(03)01285-8
  3. Chida, Y., Sudo, N., Motomura, Y. and Kubo, C. (2004) Electric footshock stress drives TNF-alpha production in the liver of IL-6-defi - cient mice. Neuroimmunomodulation 11, 419-424. https://doi.org/10.1159/000080153
  4. Duncko, R., Kiss, A., Skultetyova, I., Rusnak, M. and Jezova, D. (2001) Corticotropin-releasing hormone mRNA levels in response to chronic mild stress rise in male but not in female rats while tyrosine hydroxylase mRNA levels decrease in both sexes. Psychoneuroendocrinology 26, 77-89. https://doi.org/10.1016/S0306-4530(00)00040-8
  5. Dwivedi, Y., Rizavi, H. S., Conley, R. R. and Pandey, G. N. (2004) ERK MAP kinase signaling in post-mortem brain of suicide subjects: differential regulation of upstream Raf kinases Raf-1 and B-Raf. Mol. Psychiatry 11, 86-98.
  6. Feng, Q., Cheng, B., Yang, R., Sun, F. Y. and Zhu, C. Q. (2005) Dynamic changes of phosphorylated tau in mouse hippocampus after cold water stress. Neurosci. Lett. 388, 13-16. https://doi.org/10.1016/j.neulet.2005.06.022
  7. Fumagalli, F., Molteni, R., Calabrese, F., Frasca, A., Racagni, G. and Riva, M. A. (2005) Chronic fluoxetine administration inhibits extracellular signal-regulated kinase 1/2 phosphorylation in rat brain. J. Neurochem. 93, 1551-1560. https://doi.org/10.1111/j.1471-4159.2005.03149.x
  8. Galea, L. A., McEwen, B. S., Tanapat, P., Deak, T., Spencer, R. L. and Dhabhar. F. S. (1997) Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 81, 689-697. https://doi.org/10.1016/S0306-4522(97)00233-9
  9. Gilad, G. M. and McCarty, R. (1981) Difference in choline acetyltransferase but similarities in catecholamine biosynthetic enzymes in brains of two rat strains differing in their response to stress. Brain Res. 206, 239-243. https://doi.org/10.1016/0006-8993(81)90124-4
  10. Glavin, G. B. (1985) Stress and brain noradrenaline: a review. Neurosci. Biobehav. Rev. 9, 233-243. https://doi.org/10.1016/0149-7634(85)90048-X
  11. Gourley, S. L., Wu, F. J., Kiraly, D. D., Ploski, J. E., Kedves, A. T., Duman, R. S. and Taylor, J. R. (2008) Regionally specifi c regulation of ERK MAP kinase in a model of antidepressant-sensitive chronic depression. Biol. Psychiatry 63, 353-359. https://doi.org/10.1016/j.biopsych.2007.07.016
  12. Gregus, A., Wintink, A. J., Davis, A. C. and Kalynchuk. L. E. (2005) Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behav. Brain Res. 156, 105-114. https://doi.org/10.1016/j.bbr.2004.05.013
  13. Hisaoka, K., Nishida, A., Koda, T., Miyata, M., Zensho, H., Morinobu, S., Ohta, M. and Yamawaki, S. (2001) Antidepressant drug treatments induce glial cell line-derived neurotrophic factor (GDNF) synthesis and release in rat C6 glioblastoma cells. J. Neurochem. 79, 25-34.
  14. Hogg, S. (1996) A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol. Biochem. Behav. 54, 21-30. https://doi.org/10.1016/0091-3057(95)02126-4
  15. Jang, S., Kim, D., Lee, Y., Moon, S. and Oh, S. (2011) Modulation of sphingosine 1-phosphate and tyrosine hydroxylase in the stressinduced anxiety. Neurochem. Res. 36, 258-267. https://doi.org/10.1007/s11064-010-0313-1
  16. Iwasaki-Sekino, A., Mano-Otagiri, A., Ohata, H., Yamauchi, N. and Shibasaki, T. (2009) Gender differences in corticotropin and corticosterone secretion and corticotropin-releasing factor mRNA expression in the paraventricular nucleus of the hypothalamus and the central nucleus of the amygdala in response to footshock stress or psychological stress in rats. Psychoneuroendocrinology 34, 226-237. https://doi.org/10.1016/j.psyneuen.2008.09.003
  17. Kodama, M., Russell, D. S. and Duman, R. S. (2005) Electroconvulsive seizures increase the expression of MAP kinase phosphatases in limbic regions of rat brain. Neuropsychopharmacology 30, 360-371. https://doi.org/10.1038/sj.npp.1300588
  18. Kopin, I. J. (1995) Definitions of stress and sympathetic neuronal responses. Ann. N. Y. Acad. Sci. 771, 19-30. https://doi.org/10.1111/j.1749-6632.1995.tb44667.x
  19. Kvetnansky, R., Gewirtz, G. P., Weise, V. K. and Kopin. I. J. (1970) Effect of hypophysectomy on immobilization-induced elevation of tyrosine hydroxylase and phenylethanolamine-N-methyl transferase in the rat adrenal. Endocrinology 87, 1323-1329. https://doi.org/10.1210/endo-87-6-1323
  20. Lechin, F., van der Dijs, B., Lechin, A., Orozco, B., Lechin, M., Baez,S., Rada, I., León, G. and Acosta, E. (1994) Plasma neurotransmitters and cortisol in chronic illness: role of stress. J. Med. 25, 181-192.
  21. Makino, S., Smith, M. A. and Gold, P. W. (2002) Regulatory role of glucocorticoids and glucocorticoid receptor mRNA levels on tyrosine hydroxylase gene expression in the locus coeruleus during repeated immobilization stress. Brain Res. 943, 216-223. https://doi.org/10.1016/S0006-8993(02)02647-1
  22. Masserano, J. M., Takimoto, G. S. and Weiner, N. (1981) Electroconvulsive shock increases tyrosine hydroxylase activity in the brain and adrenal gland of the rat. Science 214, 662-665. https://doi.org/10.1126/science.6117127
  23. McEwen, B. S. (2000) The neurobiology of stress: from serendipity to clinical relevance. Brain Res. 886, 172-189. https://doi.org/10.1016/S0006-8993(00)02950-4
  24. Meller, E., Shen, C., Nikolao, T. A., Jensen, C., Tsimberg, Y., Chen, J. and Gruen, R. J. (2003) Region-specifi c effects of acute and repeated restraint stress on the phosphorylation of mitogen-activated protein kinases. Brain Res. 979, 57-64. https://doi.org/10.1016/S0006-8993(03)02866-X
  25. Mitra, R. and Sapolsky. R. M. (2008) Acute corticosterone treatment is suffi cient to induce anxiety and amygdaloid dendritic hypertrophy. Proc. Natl. Acad. Sci. USA 105, 5573-5578. https://doi.org/10.1073/pnas.0705615105
  26. Mo, B., Feng, N., Renner, K. and Forster, G. (2008) Restraint stress increases serotonin release in the central nucleus of the amygdala via activation of corticotropin-releasing factor receptors. Brain Res. Bull. 76, 493-498. https://doi.org/10.1016/j.brainresbull.2008.02.011
  27. Musacchio, J. M., Julou, L., Kety, S. S. and Glowinski, J. (1969) Increase in rat brain tyrosine hydroxylase activity produced by electroconvulsive shock. Proc. Natl. Acad. Sci. USA 63, 1117-1119. https://doi.org/10.1073/pnas.63.4.1117
  28. Nankova, B., Kvetnansky, R., Hiremagalur, B., Sabban, B., Rusnak, M. and Sabban, E. L. (1996) Immobilization stress elevates gene expression for catecholamine biosynthetic enzymes and some neuropeptides in rat sympathetic ganglia: effects of adrenocorticotropin and glucocorticoids. Endocrinology 137, 5597-5604. https://doi.org/10.1210/en.137.12.5597
  29. Ortiz, J., DeCaprio, J. L., Kosten, T. A. and Nestler, E. J. (1995) Strainselective effects of corticosterone on locomotor sensitization to cocaine and on levels of tyrosine hydroxylase and glucocorticoid receptor in the ventral tegmental area. Neuroscience 67, 383-397. https://doi.org/10.1016/0306-4522(95)00018-E
  30. Oztas, B., Akgül, S. and Arslan, F. B. (2004) Influence of surgical pain stress on the blood-brain barrier permeability in rats. Life Sci. 74, 1973-1979. https://doi.org/10.1016/j.lfs.2003.07.054
  31. Qi, X., Lin, W., Li, J., Pan, Y. and Wang, W. (2006) The depressive-like behaviors are correlated with decreased phosphorylation of mitogen- activated protein kinases in rat brain following chronic forced swim stress. Behav. Brain Res. 175, 233-240. https://doi.org/10.1016/j.bbr.2006.08.035
  32. Qian, Y. R. and Kim, Y. S. (2007) Effect of immobilization stress on the expression of TH, BDH and CRH gene in rat brain. J. Genet. Med. 4, 179-185.
  33. Rastogi, R. B. and Singhal, R. L. (1978) Evidence for the role of adrenocortical hormones in the regulation of noradrenaline and dopamine metabolism in certain brain areas. Br. J. Pharmacol. 62, 131-136. https://doi.org/10.1111/j.1476-5381.1978.tb07015.x
  34. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Belzung, C. and Hen, R. (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809. https://doi.org/10.1126/science.1083328
  35. Shen, C. P., Tsimberg, Y., Salvadore, C. and Meller, E. (2004) Activation of Erk and JNK MAPK pathways by acute swim stress in rat brain regions. BMC. Neurosci. 5, 36. https://doi.org/10.1186/1471-2202-5-36
  36. Stutzmann, G. E. and LeDoux, J. E. (1999) GABAergic antagonists block the inhibitory effects of serotonin in the lateral amygdala: a mechanism for modulation of sensory inputs related to fear conditioning. J. Neurosci. 19, RC8.
  37. Sweatt, J. D. (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem. 76, 1-10.
  38. Tiraboschi, E., Tardito, D., Kasahara, J., Moraschi, S., Pruneri, P., Gennarelli, M., Racagni, G. and Popoli, M. (2004) Selective phosphorylation of nuclear CREB by fl uoxetine is linked to activation of CaM kinase IV and MAP kinase cascades. Neuropsychopharmacology 29, 1831-1840. https://doi.org/10.1038/sj.npp.1300488
  39. Van de Kar, L. D., Piechowski, R. A., Rittenhouse, P. A. and Gray, T. S. (1991) Amygdaloid lesions: differential effect on conditioned stress and immobilization-induced increases in corticosterone and renin secretion. Neuroendocrinology 54, 89-95. https://doi.org/10.1159/000125856
  40. Wong, D. L. (2006) Epinephrine biosynthesis: hormonal and neural control during stress. Cell Mol. Neurobiol. 26, 891-900.
  41. Wu, S. L., Hsu, L. S., Tu, W. T., Wang, W. F., Huang, Y. T., Pawlak, C. R. and Ho, Y. J. (2008) Effects of D-cycloserine on the behavior and ERK activity in the amygdala: role of individual anxiety levels. Behav. Brain Res. 187, 246-253. https://doi.org/10.1016/j.bbr.2007.09.013
  42. Yamano, Y., Yoshioka, M., Toda, Y., Oshida, Y., Chaki, S., Hamamoto, K. and Morishima, I. (2004) Regulation of CRF, POMC and MC4R gene expression after electrical foot shock stress in the rat amygdala and hypothalamus. J. Vet. Med. Sci. 66, 1323-1327. https://doi.org/10.1292/jvms.66.1323
  43. Yoshihara, T. and Yawaka, Y. (2008) Repeated immobilization stress in the early postnatal period increases stress response in adult rats. Physiol. Behav. 93, 322-326. https://doi.org/10.1016/j.physbeh.2007.09.004
  44. Zhao, Y., Ma, R., Shen, J., Su, H., Xing, D. and Du, L. (2008) A mouse model of depression induced by repeated corticosterone injections. Eur. J. Pharmacol. 581, 113-120. https://doi.org/10.1016/j.ejphar.2007.12.005

Cited by

  1. SCOP/PHLPP1β in the basolateral amygdala regulates circadian expression of mouse anxiety-like behavior vol.6, pp.1, 2016, https://doi.org/10.1038/srep33500
  2. Quinpirole Increases Melatonin-Augmented Pentobarbital Sleep via Cortical ERK, p38 MAPK, and PKC in Mice vol.24, pp.2, 2016, https://doi.org/10.4062/biomolther.2015.097
  3. Alterations in the corticotropin-releasing hormone (CRH) neurocircuitry: Insights into post stroke functional impairments vol.42, 2016, https://doi.org/10.1016/j.yfrne.2016.07.001
  4. Repeated corticosterone injections in adult mice alter stress hormonal receptor expression in the cerebellum and motor coordination without affecting spatial learning vol.326, 2017, https://doi.org/10.1016/j.bbr.2017.02.035
  5. Alpha-Asarone, a Major Component ofAcorus gramineus, Attenuates Corticosterone-Induced Anxiety-Like Behaviours via Modulating TrkB Signaling Process vol.18, pp.3, 2014, https://doi.org/10.4196/kjpp.2014.18.3.191
  6. Formyl Peptide Receptor as a Novel Therapeutic Target for Anxiety-Related Disorders vol.9, pp.12, 2014, https://doi.org/10.1371/journal.pone.0114626
  7. The effects of a standardized Acanthopanax koreanum extract on stress-induced behavioral alterations in mice vol.148, pp.3, 2013, https://doi.org/10.1016/j.jep.2013.05.019
  8. Polygala tenuifoliaprevents anxiety-like behaviors in mice exposed to repeated restraint stress vol.19, pp.1, 2015, https://doi.org/10.1080/19768354.2014.982176
  9. Neuroanatomical pathways underlying the effects of hypothalamo-hypophysial-adrenal hormones on exploratory activity vol.28, pp.6, 2012, https://doi.org/10.1515/revneuro-2016-0075
  10. Neuroanatomical pathways underlying the effects of hypothalamo-hypophysial-adrenal hormones on exploratory activity vol.28, pp.6, 2012, https://doi.org/10.1515/revneuro-2016-0075
  11. The effects of glucocorticoids on depressive and anxiety-like behaviors, mineralocorticoid receptor-dependent cell proliferation regulates anxiety-like behaviors vol.362, pp.None, 2012, https://doi.org/10.1016/j.bbr.2019.01.026
  12. Increased vulnerability of nigral dopamine neurons after expansion of their axonal arborization size through D2 dopamine receptor conditional knockout vol.15, pp.8, 2012, https://doi.org/10.1371/journal.pgen.1008352