DOI QR코드

DOI QR Code

Chronic Administration of Baicalein Decreases Depression-Like Behavior Induced by Repeated Restraint Stress in Rats

  • Lee, Bombi (Acupuncture and Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Sur, Bongjun (The Graduate School of Basic Science of Oriental Medicine, College of Oriental Medicine, Kyung Hee University) ;
  • Park, Jinhee (Acupuncture and Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Kim, Sung-Hun (Acupuncture and Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Kwon, Sunoh (Acupuncture and Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Yeom, Mijung (Acupuncture and Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Shim, Insop (Acupuncture and Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Lee, Hyejung (Acupuncture and Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Hahm, Dae-Hyun (Acupuncture and Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University)
  • 투고 : 2013.04.23
  • 심사 : 2013.08.06
  • 발행 : 2013.10.30

초록

Baicalein (BA), a plant-derived active flavonoid present in the root of Scutellaria baicalensis, has been widely used for the treatment of stress-related neuropsychiatric disorders including depression. Previous studies have demonstrated that repeated restraint stress disrupts the activity of the hypothalamic-pituitary-adrenal (HPA) axis, resulting in depression. The behavioral and neurochemical basis of the BA effect on depression remain unclear. The present study used the forced swimming test (FST) and changes in brain neurotransmitter levels to confirm the impact of BA on repeated restraint stress-induced behavioral and neurochemical changes in rats. Male rats received 10, 20, or 40 mg/kg BA (i.p.) 30 min prior to daily exposure to repeated restraint stress (2 h/day) for 14 days. Activation of the HPA axis in response to repeated restraint stress was confirmed by measuring serum corticosterone levels and the expression of corticotrophin-releasing factor in the hypothalamus. Daily BA administration significantly decreased the duration of immobility in the FST, increased sucrose consumption, and restored the stress-related decreases in dopamine concentrations in the hippocampus to near normal levels. BA significantly inhibited the stress-induced decrease in neuronal tyrosine hydroxylase immunoreactivity in the ventral tegmental area and the expression of brain-derived neurotrophic factor (BDNF) mRNA in the hippocampus. Taken together, these findings indicate that administration of BA prior to the repeated restraint stress significantly improves helpless behaviors and depressive symptoms, possibly by preventing the decrease in dopamine and BDNF expression. Thus, BA may be a useful agent for the treatment or alleviation of the complex symptoms associated with depression.

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참고문헌

  1. Xiong Z, Jiang B, Wu PF, Tian J, Shi LL, Gu J, Hu ZL, Fu H, Wang F, Chen JG. Antidepressant effects of a plant-derived flavonoid baicalein involving extracellular signal-regulated kinases cascade. Biol Pharm Bull. 2011;34:253-259. https://doi.org/10.1248/bpb.34.253
  2. Chandrashekar N, Selvamani A, Subramanian R, Pandi A, Thiruvengadam D. Baicalein inhibits pulmonary carcinogenesis-associated inflammation and interferes with COX-2, MMP-2 and MMP-9 expressions in-vivo. Toxicol Appl Pharmacol. 2012;261:10-21. https://doi.org/10.1016/j.taap.2012.02.004
  3. Park SJ, Kim DH, Kim JM, Shin CY, Cheong JH, Ko KH, Ryu JH. Mismatch between changes in baicalein-induced memoryrelated biochemical parameters and behavioral consequences in mouse. Brain Res. 2010;1355:141-150. https://doi.org/10.1016/j.brainres.2010.07.098
  4. Wang W, Wang F, Yang YJ, Hu ZL, Long LH, Fu H, Xie N, Chen JG. The flavonoid baicalein promotes NMDA receptordependent long-term potentiation and enhances memory. Br J Pharmacol. 2011;162:1364-1379. https://doi.org/10.1111/j.1476-5381.2010.01143.x
  5. Tsai TH, Liu SC, Tsai PL, Ho LK, Shum AY, Chen CF. The effects of the cyclosporin A, a P-glycoprotein inhibitor, on the pharmacokinetics of baicalein in the rat: a microdialysis study. Br J Pharmacol. 2002;137:1314-1320. https://doi.org/10.1038/sj.bjp.0704959
  6. Oh SB, Park HR, Jang YJ, Choi SY, Son TG, Lee J. Baicalein attenuates impaired hippocampal neurogenesis and the neurocognitive deficits induced by ${\gamma}$-ray radiation. Br J Pharmacol. 2013;168:421-431. https://doi.org/10.1111/j.1476-5381.2012.02142.x
  7. Wang SY, Wang HH, Chi CW, Chen CF, Liao JF. Effects of baicalein on beta-amyloid peptide-(25-35)-induced amnesia in mice. Eur J Pharmacol. 2004;506:55-61. https://doi.org/10.1016/j.ejphar.2004.10.029
  8. Liu C, Wu J, Gu J, Xiong Z, Wang F, Wang J, Wang W, Chen J. Baicalein improves cognitive deficits induced by chronic cerebral hypoperfusion in rats. Pharmacol Biochem Behav. 2007;86:423-430. https://doi.org/10.1016/j.pbb.2006.11.005
  9. Liu C, Wu J, Xu K, Cai F, Gu J, Ma L, Chen J. Neuroprotection by baicalein in ischemic brain injury involves PTEN/AKT pathway. J Neurochem. 2010;112:1500-1512. https://doi.org/10.1111/j.1471-4159.2009.06561.x
  10. Guo QL, Ding QL, Wu ZQ. Effect of baicalein on experimental prostatic hyperplasia in rats and mice. Biol Pharm Bull. 2004;27:333-337. https://doi.org/10.1248/bpb.27.333
  11. Colman I, Ataullahjan A. Life course perspectives on the epidemiology of depression. Can J Psychiatry. 2010;55:622-632. https://doi.org/10.1177/070674371005501002
  12. Uliaszek AA, Zinbarg RE, Mineka S, Craske MG, Sutton JM, Griffith JW, Rose R, Waters A, Hammen C. The role of neuroticism and extraversion in the stress-anxiety and stressdepression relationships. Anxiety Stress Coping. 2010;23:363-381. https://doi.org/10.1080/10615800903377264
  13. Skorzewska A, Bidzinski A, Lehner M, Turzynska D, Wislowska-Stanek A, Sobolewska A, Szyndler J, Maciejak P, Taracha E, Plaznik A. The effects of acute and chronic administration of corticosterone on rat behavior in two models of fear responses, plasma corticosterone concentration, and c-Fos expression in the brain structures. Pharmacol Biochem Behav. 2006;85:522-534. https://doi.org/10.1016/j.pbb.2006.10.001
  14. Steiner MA, Marsicano G, Nestler EJ, Holsboer F, Lutz B, Wotjak CT. Antidepressant-like behavioral effects of impaired cannabinoid receptor type 1 signaling coincide with exaggerated corticosterone secretion in mice. Psychoneuroendocrinology. 2008;33:54-67. https://doi.org/10.1016/j.psyneuen.2007.09.008
  15. Huang Z, Zhong XM, Li ZY, Feng CR, Pan AJ, Mao QQ. Curcumin reverses corticosterone-induced depressive-like behavior and decrease in brain BDNF levels in rats. Neurosci Lett. 2011;493:145-148. https://doi.org/10.1016/j.neulet.2011.02.030
  16. Lee B, Shim I, Lee HJ, Yang Y, Hahm DH. Effects of acupuncture on chronic corticosterone-induced depression-like behavior and expression of neuropeptide Y in the rats. Neurosci Lett. 2009;453:151-156. https://doi.org/10.1016/j.neulet.2009.01.076
  17. Mokler DJ, Torres OI, Galler JR, Morgane PJ. Stress-induced changes in extracellular dopamine and serotonin in the medial prefrontal cortex and dorsal hippocampus of prenatally malnourished rats. Brain Res. 2007;1148:226-233. https://doi.org/10.1016/j.brainres.2007.02.031
  18. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci. 2002;22:6810-6818.
  19. Mizoguchi K, Yuzurihara M, Ishige A, Aburada M, Tabira T. Saiko-ka-ryukotsu-borei-to, a herbal medicine, ameliorates chronic stress-induced depressive state in rotarod performance. Pharmacol Biochem Behav. 2003;75:419-425. https://doi.org/10.1016/S0091-3057(03)00131-X
  20. Torres IL, Gamaro GD, Vasconcellos AP, Silveira R, Dalmaz C. Effects of chronic restraint stress on feeding behavior and on monoamine levels in different brain structures in rats. Neurochem Res. 2002;27:519-525. https://doi.org/10.1023/A:1019856821430
  21. Anisman H, Matheson K. Stress, depression, and anhedonia: caveats concerning animal models. Neurosci Biobehav Rev. 2005;29:525-546. https://doi.org/10.1016/j.neubiorev.2005.03.007
  22. Bravo JA, Diaz-Veliz G, Mora S, Ulloa JL, Berthoud VM, Morales P, Arancibia S, Fiedler JL. Desipramine prevents stress-induced changes in depressive-like behavior and hippocampal markers of neuroprotection. Behav Pharmacol. 2009;20:273-285. https://doi.org/10.1097/FBP.0b013e32832c70d9
  23. O'Mahony CM, Clarke G, Gibney S, Dinan TG, Cryan JF. Strain differences in the neurochemical response to chronic restraint stress in the rat: relevance to depression. Pharmacol Biochem Behav. 2011;97:690-699. https://doi.org/10.1016/j.pbb.2010.11.012
  24. Zhu KY, Mao QQ, Ip SP, Choi RC, Dong TT, Lau DT, Tsim KW. 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;2012:149256.
  25. Xu Y, Ku BS, Yao HY, Lin YH, Ma X, Zhang YH, Li XJ. Antidepressant effects of curcumin in the forced swim test and olfactory bulbectomy models of depression in rats. Pharmacol Biochem Behav. 2005;82:200-206. https://doi.org/10.1016/j.pbb.2005.08.009
  26. Molina-Hernandez M, Tellez-Alcantara NP, Olivera-Lopez JI, Jaramillo MT. Intra-lateral septal infusions of folic acid alone or combined with various antidepressant drugs produce antidepressant-like actions in male Wistar rats forced to swim. Prog Neuropsychopharmacol Biol Psychiatry. 2012;36:78-84. https://doi.org/10.1016/j.pnpbp.2011.08.020
  27. Lee B, Shim I, Lee H, Hahm DH. Effect of ginsenoside Re on depression- and anxiety-like behaviors and cognition memory deficit induced by repeated immobilization in rats. J Microbiol Biotechnol. 2012;22:708-720. https://doi.org/10.4014/jmb.1112.12046
  28. Mao QQ, Ip SP, Ko KM, Tsai SH, Che CT. Peony glycosides produce antidepressant-like action in mice exposed to chronic unpredictable mild stress: effects on hypothalamic-pituitaryadrenal function and brain-derived neurotrophic factor. Prog Neuropsychopharmacol Biol Psychiatry. 2009;33:1211-1216. https://doi.org/10.1016/j.pnpbp.2009.07.002
  29. Gmeiner BM, Seelos CC. Measurement of phosphotyrosine phosphatase activity using the Folin-Ciocalteu phenol reaction. Biochem Mol Biol Int. 1995;36:943-948.
  30. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 3th ed. New York, USA: Academic Press; 1986. 54-85 p.
  31. Ling S, Jamali F. Effect of cannulation surgery and restraint stress on the plasma corticosterone concentration in the rat: application of an improved corticosterone HPLC assay. J Pharm Pharm Sci. 2003;6:246-251.
  32. Sun H, Che QM, Zhao X, Pu XP. Antifibrotic effects of chronic baicalein administration in a CCl4 liver fibrosis model in rats. Eur J Pharmacol. 2010;631:53-60. https://doi.org/10.1016/j.ejphar.2010.01.002
  33. Chiba S, Numakawa T, Ninomiya M, Richards MC, Wakabayashi C, Kunugi H. Chronic restraint stress causes anxietyand depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry. 2012;39:112-119. https://doi.org/10.1016/j.pnpbp.2012.05.018
  34. Nacher J, Pham K, Gil-Fernandez V, McEwen BS. Chronic restraint stress and chronic corticosterone treatment modulate differentially the expression of molecules related to structural plasticity in the adult rat piriform cortex. Neuroscience. 2004;126:503-509 https://doi.org/10.1016/j.neuroscience.2004.03.038
  35. Sigwalt AR, Budde H, Helmich I, Glaser V, Ghisoni K, Lanza S, Cadore EL, Lhullier FL, de Bem AF, Hohl A, de Matos FJ, de Oliveira PA, Prediger RD, Guglielmo LG, Latini A. Molecular aspects involved in swimming exercise training reducing anhedonia in a rat model of depression. Neuroscience. 2011;192:661-674. https://doi.org/10.1016/j.neuroscience.2011.05.075
  36. Strekalova T, Gorenkova N, Schunk E, Dolgov O, Bartsch D. Selective effects of citalopram in a mouse model of stressinduced anhedonia with a control for chronic stress. Behav Pharmacol. 2006;17:271-287. https://doi.org/10.1097/00008877-200605000-00008
  37. Ulloa JL, Castaneda P, Berrios C, Diaz-Veliz G, Mora S, Bravo JA, Araneda K, Menares C, Morales P, Fiedler JL. Comparison of the antidepressant sertraline on differential depression-like behaviors elicited by restraint stress and repeated corticosterone administration. Pharmacol Biochem Behav. 2010;97:213-221. https://doi.org/10.1016/j.pbb.2010.08.001
  38. Zhang W, Rosenkranz JA. Repeated restraint stress increases basolateral amygdala neuronal activity in an age-dependent manner. Neuroscience. 2012;226:459-474. https://doi.org/10.1016/j.neuroscience.2012.08.051
  39. Zheng J, Babygirija R, Bulbul M, Cerjak D, Ludwig K, Takahashi T. Hypothalamic oxytocin mediates adaptation mechanism against chronic stress in rats. Am J Physiol Gastrointest Liver Physiol. 2010;299:G946-953. https://doi.org/10.1152/ajpgi.00483.2009
  40. Cook CJ. Stress induces CRF release in the paraventricular nucleus, and both CRF and GABA release in the amygdala. Physiol Behav. 2004;82:751-762. https://doi.org/10.1016/j.physbeh.2004.06.013
  41. Raone A, Cassanelli A, Scheggi S, Rauggi R, Danielli B, De Montis MG. Hypothalamus-pituitary-adrenal modifications consequent to chronic stress exposure in an experimental model of depression in rats. Neuroscience. 2007;146:1734-1742. https://doi.org/10.1016/j.neuroscience.2007.03.027
  42. Park HJ, Shim HS, Kim H, Kim KS, Lee H, Hahm DH, Shim I. Effects of glycyrrhizae radix on repeated restraint stressinduced neurochemical and behavioral responses. Korean J Physiol Pharmacol. 2010;14:371-376. https://doi.org/10.4196/kjpp.2010.14.6.371
  43. Wang YC, Ho UC, Ko MC, Liao CC, Lee LJ. Differential neuronal changes in medial prefrontal cortex, basolateral amygdala and nucleus accumbens after postweaning social isolation. Brain Struct Funct. 2012;217:337-351. https://doi.org/10.1007/s00429-011-0355-4
  44. Sevgi S, Ozek M, Eroglu L. L-NAME prevents anxiety-like and depression-like behavior in rats exposed to restraint stress. Methods Find Exp Clin Pharmacol. 2006;28:95-99. https://doi.org/10.1358/mf.2006.28.2.977840
  45. Spasojevic N, Gavrilovic L, Dronjak S. Effects of repeated maprotiline and fluoxetine treatment on gene expression of catecholamine synthesizing enzymes in adrenal medulla of unstressed and stressed rats. Auton Autacoid Pharmacol. 2010;30:213-217. https://doi.org/10.1111/j.1474-8673.2010.00458.x
  46. Shishkina GT, Kalinina TS, Dygalo NN. Effects of swim stress and fluoxetine on 5-HT1A receptor gene expression and monoamine metabolism in the rat brain regions. Cell Mol Neurobiol. 2012;32:787-794. https://doi.org/10.1007/s10571-012-9828-0
  47. Cui J, Jiang L, Xiang H. Ginsenoside Rb3 exerts antidepressant-like effects in several animal models. J Psychopharmacol. 2012;26:697-713. https://doi.org/10.1177/0269881111415735
  48. Dallman MF, Akana SF, Strack AM, Scribner KS, Pecoraro N, La Fleur SE, Houshyar H, Gomez F. Chronic stress-induced effects of corticosterone on brain: direct and indirect. Ann N Y Acad Sci. 2004;1018:141-150. https://doi.org/10.1196/annals.1296.017
  49. Bergstrom A, Jayatissa MN, Mork A, Wiborg O. Stress sensitivity and resilience in the chronic mild stress rat model of depression; an in situ hybridization study. Brain Res. 2008; 1196:41-52. https://doi.org/10.1016/j.brainres.2007.12.025
  50. Cirulli F, Berry A, Bonsignore LT, Capone F, D'Andrea I, Aloe L, Branchi I, Alleva E. Early life influences on emotional reactivity: evidence that social enrichment has greater effects than handling on anxiety-like behaviors, neuroendocrine responses to stress and central BDNF levels. Neurosci Biobehav Rev. 2010;34:808-820. https://doi.org/10.1016/j.neubiorev.2010.02.008
  51. Dagnino-Subiabre A, Zepeda-Carreno R, Diaz-Veliz G, Mora S, Aboitiz F. Chronic stress induces upregulation of brain-derived neurotrophic factor (BDNF) mRNA and integrin alpha5 expression in the rat pineal gland. Brain Res. 2006;1086:27-34. https://doi.org/10.1016/j.brainres.2006.02.118
  52. Gatt JM, Nemeroff CB, Dobson-Stone C, Paul RH, Bryant RA, Schofield PR, Gordon E, Kemp AH, Williams LM. Interactions between BDNF Val66Met polymorphism and early life stress predict brain and arousal pathways to syndromal depression and anxiety. Mol Psychiatry. 2009;14:681-695. https://doi.org/10.1038/mp.2008.143
  53. Franklin TB, Perrot-Sinal TS. Sex and ovarian steroids modulate brain-derived neurotrophic factor (BDNF) protein levels in rat hippocampus under stressful and non-stressful conditions. Psychoneuroendocrinology. 2006;31:38-48. https://doi.org/10.1016/j.psyneuen.2005.05.008
  54. Murakami S, Imbe H, Morikawa Y, Kubo C, Senba E. Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci Res. 2005;53:129-139. https://doi.org/10.1016/j.neures.2005.06.008
  55. Zhang W, Li J, Zhu J, Shi Z, Wang Y, Kong L. Chinese medicine Banxia-houpu decoction regulates c-fos expression in the brain regions in chronic mild stress model in rats. Phytother Res. 2004;18:200-203. https://doi.org/10.1002/ptr.1391

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