DOI QR코드

DOI QR Code

L-Tetrahydropalmatine Ameliorates Development of Anxiety and Depression-Related Symptoms Induced by Single Prolonged Stress in Rats

  • Lee, Bombi (Acupuncture and Meridian Science Research Center) ;
  • Sur, Bongjun (Graduate School of Basic Science of Korean Medicine, College of Korean Medicine, Kyung Hee University) ;
  • Yeom, Mijung (Acupuncture and Meridian Science Research Center) ;
  • Shim, Insop (Acupuncture and Meridian Science Research Center) ;
  • Lee, Hyejung (Acupuncture and Meridian Science Research Center) ;
  • Hahm, Dae-Hyun (Acupuncture and Meridian Science Research Center)
  • Received : 2014.03.12
  • Accepted : 2014.05.07
  • Published : 2014.05.31

Abstract

Abnormal adaptation of the stress-response system following traumatic stress can lead to alterations in the hypothalamic-pituitaryadrenal (HPA) axis that may contribute to the development of post-traumatic stress disorder (PTSD). The present study used several behavioral tests to investigate the anxiolytic-like and antidepressant activity of L-tetrahydropalmatine (L-THP) in an experimental rat model of anxiety and depression induced by single prolonged stress (SPS), an animal model of PTSD. Male rats were treated intraperitoneally (i.p.) with vehicle or varied doses of THP 30 min prior to SPS for 8 consecutive days. Daily THP (50 mg/kg) administration significantly increased the number and duration of open arm visits in the elevated plus maze (EPM) test, reduced the anxiety index, increased the risk assessment, and increased the number of head dips over the borders of the open arms after SPS. THP was also associated with increased time spent at the center of the open field, reduced grooming behaviors in the EPM test, and reduced time spent immobile in the forced swimming test (FST). It also blocked the decrease in neuropeptide Y (NPY) and the increase in corticotrophin-releasing factor (CRF) expression in the hypothalamus. This is the first study to determine that THP exerts pronounced anxiolytic-like and antidepressant effects on the development of the behavioral and biochemical symptoms associated with PTSD, indicating its prophylactic potential. Thus, THP reversed several behavioral impairments triggered by the traumatic stress of SPS and is a potential non-invasive therapeutic intervention for PTSD.

Keywords

References

  1. Castro, J. E., Diessler, S., Varea, E., Marquez, C., Larsen, M. H., Cordero, M. I. and Sandi, C. (2012) Personality traits in rats predict vulnerability and resilience to developing stress-induced depression- like behaviors, HPA axis hyper-reactivity and brain changes in pERK1/2 activity. Psychoneuroendocrinology 37, 1209-1223. https://doi.org/10.1016/j.psyneuen.2011.12.014
  2. Ceremuga, T. E., Shellabarger, P., Persson, T., Fanning, M., Galey, P., Robinson, D., Bertsch, S., Ceremuga, G. A. and Bentley, M. (2013) Effects of tetrahydropalmatine on post-traumatic stress disorderinduced changes in rat brain gene expression. J. Integr. Neurosci. 12, 513-528. https://doi.org/10.1142/S0219635213500313
  3. Cohen, H., Liu, T., Kozlovsky, N., Kaplan, Z., Zohar, J. and Mathe, A. A. (2012) The neuropeptide Y (NPY)-ergic system is associated with behavioral resilience to stress exposure in an animal model of post-traumatic stress disorder. Neuropsychopharmacology 37, 350-363. https://doi.org/10.1038/npp.2011.230
  4. Colman, I. and Ataullahjan, A. (2010) Life course perspectives on the epidemiology of depression. Can. J. Psychiatry 55, 622-632.
  5. Cryan, J. F. and Holmes, A. (2005) The ascent of mouse: advances in modelling human depression and anxiety. Nat. Rev. Drug Discov. 4, 775-790. https://doi.org/10.1038/nrd1825
  6. Cui, H., Sakamoto, H., Higashi, S. and Kawata, M. (2008) Effects of single- prolonged stress on neurons and their afferent inputs in the amygdala. Neuroscience 152, 703-712. https://doi.org/10.1016/j.neuroscience.2007.12.028
  7. Dabrowska, J., Hazra, R., Guo, J. D., Li, C., Dewitt, S., Xu, J., Lombroso, P. J. and Rainnie, D. G. (2013) Striatal-enriched protein tyrosine phosphatase-STEPs toward understanding chronic stressinduced activation of corticotrophin releasing factor neurons in the rat bed nucleus of the stria terminalis. Biol. Psychiatry 74, 817-826. https://doi.org/10.1016/j.biopsych.2013.07.032
  8. Deligiannidis, K. M. and Freeman, M. P. (2010) Complementary and alternative medicine for the treatment of depressive disorders in women. Psychiatr. Clin. North Am. 33, 441-463. https://doi.org/10.1016/j.psc.2010.01.002
  9. Fox, J. H. and Lowry, C. A. (2013) Corticotropin-releasing factor-related peptides, serotonergic systems, and emotional behavior. Front. Neurosci. 7, 169-173.
  10. George, S. A., Knox, D., Curtis, A. L., Aldridge, J. W., Valentino, R. J. and Liberzon, I. (2013a) Altered locus coeruleus-norepinephrine function following single prolonged stress. Eur. J. Neurosci. 37, 901-909. https://doi.org/10.1111/ejn.12095
  11. George, S. A., Stout, S. A., Tan, M., Knox, D. and Liberzon, I. (2013b) Early handling attenuates enhancement of glucocorticoid receptors in the prefrontal cortex in an animal model of post-traumatic stress disorder. Biol. Mood Anxiety Disord. 3, 22-23. https://doi.org/10.1186/2045-5380-3-22
  12. Han, Y., Zhang, W., Tang, Y., Bai, W., Yang, F., Xie, L., Li, X., Zhou, S., Pan, S., Chen, Q., Ferro, A. and Ji, Y. (2012) l-Tetrahydropalmatine, an active component of Corydalis yanhusuo W.T. Wang, protects against myocardial ischaemia-reperfusion injury in rats. PLoS One 7, e38627. https://doi.org/10.1371/journal.pone.0038627
  13. Hsiao, Y. T., Yi, P. L., Li, C. L. and Chang, F. C. (2012) Effect of cannabidiol on sleep disruption induced by the repeated combination tests consisting of open field and elevated plus-maze in rats. Neuropharmacology 62, 373-384. https://doi.org/10.1016/j.neuropharm.2011.08.013
  14. Jindal, A., Mahesh, R. and Kumar, B. (2013) Anxiolytic-like effect of linezolid in experimental mouse models of anxiety. Prog. Neuropsychopharmacol. Biol. Psychiatry 40, 47-53.
  15. Kohda, K., Harada, K., Kato, K., Hoshino, A., Motohashi, J., Yamaji, T., Morinobu, S., Matsuoka, N., Kato, N. (2007) Glucocorticoid receptor activation is involved in producing abnormal phenotypes of single-prolonged stress rats: a putative post-traumatic stress disorder model. Neuroscience 148, 22-33. https://doi.org/10.1016/j.neuroscience.2007.05.041
  16. Kokras, N., Dalla, C., Sideris, A. C., Dendi, A., Mikail, H. G., Antoniou, K., and Papadopoulou-Daifoti, Z. (2012) Behavioral sexual dimorphism in models of anxiety and depression due to changes in HPA axis activity. Neuropharmacology 62, 436-445. https://doi.org/10.1016/j.neuropharm.2011.08.025
  17. Kozlovsky, N., Matar, M.A., Kaplan, Z., Zohar, J. and Cohen, H. (2009) The role of the galaninergic system in modulating stress-related responses in an animal model of posttraumatic stress disorder. Biol. Psychiatry 65, 383-391. https://doi.org/10.1016/j.biopsych.2008.10.034
  18. Kupferschmidt, D. A., Newman, A. E., Boonstra, R. and Erb, S. (2012) Antagonism of cannabinoid 1 receptors reverses the anxiety-like behavior induced by central injections of corticotropin-releasing factor and cocaine withdrawal. Neuroscience 204, 125-133. https://doi.org/10.1016/j.neuroscience.2011.07.022
  19. Lee, B., Sur, B., Kwon, S., Yeom, M., Shim, I., Lee, H. and Hahm, D. H. (2013) Chronic administration of catechin decreases depression and anxiety-like behaviors in a rat model using chronic corticosterone injections. Biomol. Ther. 21, 313-322. https://doi.org/10.4062/biomolther.2013.004
  20. Liu, Y. L., Liang, J. H., Yan, L. D., Su, R. B., Wu, C. F. and Gong, Z. H. (2005) Effects of l-tetrahydropalmatine on locomotor sensitization to oxycodone in mice. Acta Pharmacol. Sin. 26, 533-538. https://doi.org/10.1111/j.1745-7254.2005.00101.x
  21. Mao, Q. Q., Ip, S. P., Ko, K. M., Tsai, S. H. and Che, C. T. (2009) Peony glycosides produce antidepressant-like action in mice exposed to chronic unpredictable mild stress: effects on hypothalamic-pituitary- adrenal function and brain-derived neurotrophic factor. Prog. Neuropsychopharmacol. Biol. Psychiatry 33, 1211-1216. https://doi.org/10.1016/j.pnpbp.2009.07.002
  22. Marquez, C., Nadal, R. and Armario, A. (2006) Influence of reactivity to novelty and anxiety on hypothalamic-pituitary-adrenal and prolactin responses to two different novel environments in adult male rats. Behav. Brain Res. 168, 13-22. https://doi.org/10.1016/j.bbr.2005.10.004
  23. Meyer, E. M., Long, V., Fanselow, M. S. and Spigelman, I. (2013) Stress increases voluntary alcohol intake, but does not alter established drinking habits in a rat model of posttraumatic stress disorder. Alcohol Clin. Exp. Res. 37, 566-574. https://doi.org/10.1111/acer.12012
  24. Paxinos, G. and Watson, C. (1986) The rat brain in stereotaxic coordinates. 3th ed., 54-85, Academic Press, New York.
  25. Roth, M. K., Bingham, B., Shah, A., Joshi, A., Frazer, A., Strong, R. and Morilak, D. A. (2012) Effects of chronic plus acute prolonged stress on measures of coping style, anxiety, and evoked HPA-axis reactivity. Neuropharmacology 63, 1118-1126. https://doi.org/10.1016/j.neuropharm.2012.07.034
  26. Serova, L. I., Laukova, M., Alaluf, L. G., Pucillo, L. and Sabban, E. L. (2014) Intranasal neuropeptide Y reverses anxiety and depressivelike behavior impaired by single prolonged stress PTSD model. Eur. Neuropsychopharmacol 24, 142-147. https://doi.org/10.1016/j.euroneuro.2013.11.007
  27. Serova, L. I., Laukova, M., Alaluf, L. G. and Sabban, E. L. (2013a) Intranasal infusion of melanocortin receptor four (MC4R) antagonist to rats ameliorates development of depression and anxiety related symptoms induced by single prolonged stress. Behav. Brain Res. 250, 139-147. https://doi.org/10.1016/j.bbr.2013.05.006
  28. Serova, L. I., Tillinger, A., Alaluf, L. G., Laukova, M., Keegan, K. and Sabban, E. L. (2013b) Single intranasal neuropeptide Y infusion attenuates development of PTSD-like symptoms to traumatic stress in rats. Neuroscience 236, 298-312. https://doi.org/10.1016/j.neuroscience.2013.01.040
  29. Shea, A., Walsh, C., Macmillan, H. and Steiner, M. (2005) Child maltreatment and HPA axis dysregulation: relationship to major depressive disorder and post traumatic stress disorder in females. Psychoneuroendocrinology 30, 162-178. https://doi.org/10.1016/j.psyneuen.2004.07.001
  30. Takahashi, T., Morinobu, S., Iwamoto, Y. and Yamawaki, S. (2006) Effect of paroxetine on enhanced contextual fear induced by single prolonged stress in rats. Psychopharmacology (Berl) 189, 165-173. https://doi.org/10.1007/s00213-006-0545-6
  31. Uliaszek, A. A., Zinbarg, R. E., Mineka, S., Craske, M. G., Sutton, J. M., Griffith, J. W., Rose, R., Waters, A. and Hammen, C. (2010) The role of neuroticism and extraversion in the stress-anxiety and stress-depression relationships. Anxiety Stress Coping 23, 363-381. https://doi.org/10.1080/10615800903377264
  32. Xi, Z. X., Yang, Z., Li, S. J., Li, X., Dillon, C., Peng, X. Q., Spiller, K. and Gardner, E. L. (2007) Levo-tetrahydropalmatine inhibits cocaine's rewarding effects: experiments with self-administration and brainstimulation reward in rats. Neuropharmacology 53, 771-782. https://doi.org/10.1016/j.neuropharm.2007.08.004
  33. Zhao, N., Chen, Y., Zhu, J., Wang, L., Cao, G., Dang, Y., Yan, C., Wang, J. and Chen, T. (2014) Levo-tetrahydropalmatine attenuates the development and expression of methamphetamine-induced locomotor sensitization and the accompanying activation of ERK in the nucleus accumbens and caudate putamen in mice. Neuroscience 258, 101-110. https://doi.org/10.1016/j.neuroscience.2013.11.025
  34. Zhu, K. Y., Mao, Q. Q., Ip, S. P., Choi, R. C., Dong, T. T., Lau, D. T. and Tsim, K. W. (2012) A standardized chinese herbal decoction, kai-xin-san, restores decreased levels of neurotransmitters and neurotrophic factors in the brain of chronic stress-induced depressive rats. Evid. Based Complement. Alternat. Med. 2012, 149256.

Cited by

  1. Tetrahydropalmatine attenuates irradiation induced lung injuries in rats vol.153, 2016, https://doi.org/10.1016/j.lfs.2016.03.056
  2. Neuropeptide Y (NPY) and posttraumatic stress disorder (PTSD): A translational update vol.284, 2016, https://doi.org/10.1016/j.expneurol.2016.06.020
  3. Effect of oleuropein on cognitive deficits and changes in hippocampal brain-derived neurotrophic factor and cytokine expression in a rat model of post-traumatic stress disorder 2017, https://doi.org/10.1007/s11418-017-1103-8
  4. Effects of systemic administration of ibuprofen on stress response in a rat model of post-traumatic stress disorder vol.20, pp.4, 2016, https://doi.org/10.4196/kjpp.2016.20.4.357
  5. Alterations in splenic function and gene expression in mice with depressive-like behavior induced by exposure to corticosterone vol.39, pp.2, 2017, https://doi.org/10.3892/ijmm.2017.2850
  6. Ginsenoside Rb1 rescues anxiety-like responses in a rat model of post-traumatic stress disorder vol.70, pp.2, 2016, https://doi.org/10.1007/s11418-015-0943-3
  7. Tetrahydropalmatine inhibits lipid accumulation through AMPK signaling pathway in 3T3-L1 adipocytes vol.15, pp.6, 2017, https://doi.org/10.3892/mmr.2017.6473
  8. L-tetrahydropalamatine inhibits tumor necrosis factor-α-induced monocyte-endothelial cell adhesion through downregulation of intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 involving suppression of nuclear factor-κ B signaling pathway vol.21, pp.5, 2015, https://doi.org/10.1007/s11655-015-2165-7
  9. Antiaging and Anxiolytic Effects of Combinatory Formulas Based on Four Medicinal Herbs vol.2017, 2017, https://doi.org/10.1155/2017/4624069
  10. l-tetrahydropalmatine reduces nicotine self-administration and reinstatement in rats vol.17, pp.1, 2016, https://doi.org/10.1186/s40360-016-0093-6
  11. The polymethoxylated flavone, Tangeretin improves cognitive memory in rats experiencing a single episode of prolonged post-traumatic stress vol.22, pp.1, 2018, https://doi.org/10.1080/19768354.2018.1426627
  12. Gypenosides attenuate lipopolysaccharide-induced neuroinflammation and anxiety-like behaviors in rats vol.22, pp.5, 2018, https://doi.org/10.1080/19768354.2018.1517825
  13. Effects of Epigallocatechin Gallate on Behavioral and Cognitive Impairments, Hypothalamic–Pituitary–Adrenal Axis Dysfunction, and Alternations in Hippocampal BDNF Expression Under Single Prolonged Stress vol.21, pp.10, 2018, https://doi.org/10.1089/jmf.2017.4161
  14. Tetramethylpyrazine reverses anxiety-like behaviors in a rat model of post-traumatic stress disorder vol.22, pp.5, 2018, https://doi.org/10.4196/kjpp.2018.22.5.525
  15. Gypenosides Attenuate Lipopolysaccharide-Induced Neuroinflammation and Memory Impairment in Rats vol.2018, pp.1741-4288, 2018, https://doi.org/10.1155/2018/4183670
  16. Berberine alleviates symptoms of anxiety by enhancing dopamine expression in rats with post-traumatic stress disorder vol.22, pp.2, 2018, https://doi.org/10.4196/kjpp.2018.22.2.183
  17. The ethanolic extract of Aralia continentalis ameliorates cognitive deficits via modifications of BDNF expression and anti-inflammatory effects in a rat model of post-traumatic stress disorder vol.19, pp.1, 2019, https://doi.org/10.1186/s12906-018-2417-0
  18. Influence of Tacrolimus on Depressive-Like Behavior in Diabetic Rats Through Brain-Derived Neurotrophic Factor Regulation in the Hippocampus vol.36, pp.2, 2014, https://doi.org/10.1007/s12640-019-00062-6
  19. Glycyrrhizin treatment ameliorates post‐traumatic stress disorder‐like behaviours and restores circadian oscillation of intracranial serotonin vol.47, pp.1, 2014, https://doi.org/10.1111/1440-1681.13173
  20. Umbelliferone modulates depression-like symptoms by altering monoamines in a rat post-traumatic stress disorder model vol.74, pp.2, 2014, https://doi.org/10.1007/s11418-019-01373-w
  21. Tacrolimus Decreases Cognitive Function by Impairing Hippocampal Synaptic Balance: a Possible Role of Klotho vol.58, pp.11, 2014, https://doi.org/10.1007/s12035-021-02499-3