Animal cells and systems

  • 제16권3호
  • /
  • Pages.190-197
  • /
  • 2012
  • /
  • 1976-8354(pISSN)
  • /
  • 2151-2485(eISSN)
한국통합생물학회 (The Korean Society for Integrative Biology)
권호 표지
DOI QR코드

DOI QR Code

Alcohol exposure induces depression-like behavior by decreasing hippocampal neuronal proliferation through inhibition of the BDNF-ERK pathway in gerbils

  • Kim, Ji-Eun (Department of Physiology, Kyung Hee University) ;
  • Ji, Eun-Sang (Department of Physiology, Kyung Hee University) ;
  • Seo, Jin-Hee (Department of Physiology, Kyung Hee University) ;
  • Lee, Moon-Hyoung (Department of Physiology, Kyung Hee University) ;
  • Cho, Se-Hyung (Department of Physiology, Kyung Hee University) ;
  • KimPak, Young-Mi (Department of Physiology, Kyung Hee University) ;
  • Seo, Tae-Beom (Department of Biochemistry, Division of Sports Science & Engineering, Korea Institute of Sports Science) ;
  • Kim, Chang-Ju (Department of Physiology, Kyung Hee University)
  • 투고 : 2011.08.21
  • 심사 : 2011.11.08
  • 발행 : 2012.06.30
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Depression is one of the most prevalent diseases of alcohol abuse. Brain-derived neurotrophic factor (BDNF) plays a critical role in cell survival in the hippocampus. Phosphorylation of extracellular signal-regulated kinase 1/2 (p-ERK1/2) is induced by BDNF, and it regulates cell proliferation and differentiation in the brain. We investigated the effects of alcohol intake on depression-like behavior, cell proliferation, expressions of BDNF and its downstream molecules in the hippocampus using Mongolian gerbils. The gerbils were divided into four groups: control group, 0.5 g/kg alcohol-treated group, 1 g/kg alcohol-treated group, 2 g/kg alcohol-treated group. Each dose of alcohol was orally administered for 3 weeks. The present results demonstrated that alcohol intake induced depression-like behavior. Both 5-hydroxytryptamine synthesis and its synthesizing enzyme tryptophan hydroxylase expression in the dorsal raphe and cell proliferation in the hippocampal dentate gyrus were decreased by alcohol intake. Alcohol intake suppressed BDNF expression, and resulted in the decrease of its downstream molecules, pERK1/2 and Bcl-2, in the hippocampus. We showed that alcohol intake may lead to a depressed-like state with reduced hippocampal cell proliferation through inhibition of the BDNF-ERK signaling pathway.

키워드

참고문헌

  1. Adams JM, Cory S. 1998. The Bcl-2 protein family: arbiters of cell survival. Science. 281:1322-1326. https://doi.org/10.1126/science.281.5381.1322
  2. Altar CA. 1999. Neurotrophins and depression. Trends Pharmacol Sci. 20:59-61. https://doi.org/10.1016/S0165-6147(99)01309-7
  3. Angelucci F, BreneS, Mathe AA. 2005. BDNF in schizophrenia, depression and corresponding animal models. Mol Psychiatry. 10:345-352. https://doi.org/10.1038/sj.mp.4001637
  4. Arvidsson U, Cullheim S, Ulfhake B, Luppi PH, Kitahama K, Jouvet M, Ho kfelt T. 1994. Quantitative and qualitative aspects on the distribution of 5-HT and its coexistence with substance P and TRH in cat ventral medullary neurons. J Chem Neuroanat. 7:3-12. https://doi.org/10.1016/0891-0618(94)90003-5
  5. Boldrini M, UnderwoodMD, Mann JJ, Arango V. 2005. More tryptophan hydroxylase in the brainstem dorsal raphe nucleus in depressed suicides. Brain Res. 1041:19-28. https://doi.org/10.1016/j.brainres.2005.01.083
  6. Chamas F, Serova L, Sabban EL. 1999. Tryptophan hydroxylase mRNA levels are elevated by repeated immobilization stress in rat raphe nuclei but not in pineal gland. Neurosci Lett. 267:157-160. https://doi.org/10.1016/S0304-3940(99)00340-7
  7. Coyle JT, Duman RS. 2003. Finding the intracellular signaling pathways affected by mood disorder treatments. Neuron. 38:157-160. https://doi.org/10.1016/S0896-6273(03)00195-8
  8. Cryan JF, Markou A, Lucki I. 2002. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci. 23:238-245. https://doi.org/10.1016/S0165-6147(02)02017-5
  9. de la Monte SM, Longato L, Tong M, DeNucci S,Wands JR. 2009. The liver-brain axis of alcohol-mediated neurodegeneration: role of toxic lipids. Int J Environ Res Public Health. 6:2055-2075. https://doi.org/10.3390/ijerph6072055
  10. Detke MJ, Rickels M, Lucki I. 1995. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology (Berl) 121:66-72. https://doi.org/10.1007/BF02245592
  11. Duman RS. 2004. Depression: a case of neuronal life and death? Biol Psychiatry. 56:140-145. https://doi.org/10.1016/j.biopsych.2004.02.033
  12. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med. 4:1313-1317. https://doi.org/10.1038/3305
  13. Givalois L, Marmigere F, Rage F, Ixart G, Arancibia S, Tapia-Arancibia L. 2001. Immobilization stress rapidly and differentially modulates BDNF and TrkB mRNA expression in the pituitary gland of adult male rats. Neuroendocrinology. 74:148-159. https://doi.org/10.1159/000054681
  14. Herrera DG, Yague AG, Johnsen-Soriano S, Bosch-Morell F, Collado-Morente L, Muriach M, Romero FJ, Garcia- Verdugo JM. 2003. Selective impairment of hippocampal neurogenesis by chronic alcoholism: protective effects of an antioxidant. Proc Natl Acad Sci US A. 100:7919-7924. https://doi.org/10.1073/pnas.1230907100
  15. Huang EJ, Reichardt LF. 2001. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci. 24:677-736. https://doi.org/10.1146/annurev.neuro.24.1.677
  16. Kim SW, Park SY, Hwang O. 2002. Up-regulation of tryptophan hydroxylase expression and serotonin synthesis by sertraline. Mol Pharmacol. 61:778-785. https://doi.org/10.1124/mol.61.4.778
  17. Kim SE, Ko IG, Kim BK, Shin MS, Cho S, Kim CJ, Kim SH, Baek SS, Lee EK, Jee YS. 2010a. Treadmill exercise prevents aging-induced failure of memory through an increase in neurogenesis and suppression of apoptosis in rat hippocampus. Exp Gerontol. 45:357-365. https://doi.org/10.1016/j.exger.2010.02.005
  18. Kim SE, Ko IG, Kim BK, Sung YH, Shin MS, Cho S, Kim CJ, Kim KH, Lee KW, Kim DH. 2010b. Transplantation of human adipose-derived stem cells into the urethra ameliorates stress urinary incontinence and blunts the induction of c-Fos immunoreactivities in brain areas related to micturition in female rats. Anim Cells Syst. 14:237-244. https://doi.org/10.1080/19768354.2010.525839
  19. Koponen E, Voikar V, Riekki R, Saarelainen T, Rauramaa T, Rauvala H, Taira T, Castren E. 2004. Transgenic mice overexpressing the full-length neurotrophin receptor trkB exhibit increased activation of the trkB-PLCg pathway, reduced anxiety, and facilitated learning. Mol Cell Neurosci. 26:166-181. https://doi.org/10.1016/j.mcn.2004.01.006
  20. Lee E, Son H. 2009. Adult hippocampal neurogenesis and related neurotrophic factors. BMB Rep. 42:239-244. https://doi.org/10.5483/BMBRep.2009.42.5.239
  21. Malberg JE, Duman RS. 2003. Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology. 28:1562-1571. https://doi.org/10.1038/sj.npp.1300234
  22. Malberg JE, Eisch AJ, Nestler EJ, Duman RS. 2000. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci. 20:9104-9110.
  23. Manji HK, Duman RS. 2001. Impairments of neuroplasticity and cellular resilience in severe mood disorders: implications for the development of novel therapeutics. Psychopharmacol Bull. 35:5-49.
  24. Moonat S, Starkman BG, Sakharkar A, Pandey SC. 2010. Neuroscience of alcoholism: molecular and cellular mechanisms. Cell Mol Life Sci. 67:73-88. https://doi.org/10.1007/s00018-009-0135-y
  25. Morris SA, Eaves DW, Smith AR, Nixon K. 2010. Alcohol inhibition of neurogenesis: a mechanism of hippocampal neurodegeneration in an adolescent alcohol abuse model. Hippocampus. 20:596-607.
  26. Nixon K. 2006. Alcohol and adult neurogenesis: roles in neurodegeneration and recovery in chronic alcoholism. Hippocampus. 16:287-295. https://doi.org/10.1002/hipo.20162
  27. Nixon K, Crews FT. 2004. Temporally specific burst in cell proliferation increases hippocampal neurogenesis in protracted abstinence from alcohol. J Neurosci. 24:9714-9722. https://doi.org/10.1523/JNEUROSCI.3063-04.2004
  28. Pietropaolo S, Paterna JC, Bu eler H, Feldon J, Yee BK. 2007. Bidirectional changes in water-maze learning following recombinant adenovirus-associated viral vector (rAAV)- mediated brain-derived neurotrophic factor expression in the rat hippocampus. Behav Pharmacol. 18:533-547. https://doi.org/10.1097/FBP.0b013e3282da0bf6
  29. Powrozek TA, Miller MW. 2009. Ethanol affects transforming growth factor beta1-initiated signals: cross-talking pathways in the developing rat cerebral wall. J Neurosci. 29:9521-9533. https://doi.org/10.1523/JNEUROSCI.2371-09.2009
  30. Reus GZ, Stringari RB, Ribeiro KF, Ferraro AK, Vitto MF, Cesconetto P, Souza CT, Quevedo J. 2011. Ketamine plus imipramine treatment induces antidepressant-like behavior and increases CREB and BDNF protein levels and PKA and PKC phosphorylation in rat brain. Behav Brain Res. 221:166-171. https://doi.org/10.1016/j.bbr.2011.02.024
  31. Rubio JM, Markowitz JC, Alegria A, Perez-Fuentes G, Liu SM, Lin KH, Blanco C. 2011. Epidemiology of chronic and nonchronic major depressive disorder: results from the national epidemiologic survey on alcohol and related conditions. Depress Anxiety. 28:622-631. https://doi.org/10.1002/da.20864
  32. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R. 2003. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science. 301:805-809. https://doi.org/10.1126/science.1083328
  33. Sellers EM, Higgins GA, Sobell MB. 1992. 5-HT and alcohol abuse. Trends Pharmacol Sci. 13:69-75. https://doi.org/10.1016/0165-6147(92)90026-3
  34. Seo JH, Sung YH, Kim KJ, Shin MS, Lee EK, Kim CJ. 2011. Effects of Phellinus linteus administration on serotonin synthesis in the brain and expression of monocarboxylate transporters in the muscle during exhaustive exercise in rats. J Nutr Sci Vitaminol (Tokyo) 57:95-103. https://doi.org/10.3177/jnsv.57.95
  35. Stevenson JR, Schroeder JP, Nixon K, Besheer J, Crews FT, Hodge CW. 2009. Abstinence following alcohol drinking produces depression-like behavior and reduced hippocampal neurogenesis in mice. Neuropsychopharmacology. 34:1209-1222. https://doi.org/10.1038/npp.2008.90
  36. Sung YH, ShinMS, Cho C, Baik HH, Jin BK, Chang HK, Lee EK, Kim CJ. 2010. Depression-like state in maternal rats induced by repeated separation of pups is accompanied by a decrease of cell proliferation and an increase of apoptosis in the hippocampus. Neurosci Lett. 470:86-90. https://doi.org/10.1016/j.neulet.2009.12.063
  37. Vasudeva RK, Lin RC, Simpson KL, Waterhouse BD. 2011. Functional organization of the dorsal raphe efferent system with special consideration of nitrergic cell groups. J Chem Neuroanat. 41:281-293. https://doi.org/10.1016/j.jchemneu.2011.05.008
  38. Warner-Schmidt JL, Duman RS. 2006. Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus. 16:239-249. https://doi.org/10.1002/hipo.20156
  39. Yang LM, Hu B, Xia YH, Zhang BL, Zhao H. 2008. Lateral habenula lesions improve the behavioral response in depressed rats via increasing the serotonin level in dorsal raphe nucleus. Behav Brain Res. 188:84-90. https://doi.org/10.1016/j.bbr.2007.10.022

피인용 문헌

  1. Treadmill exercise ameliorates symptoms of methimazole-induced hypothyroidism through enhancing neurogenesis and suppressing apoptosis in the hippocampus of rat pups vol.31, pp.3, 2012, https://doi.org/10.1016/j.ijdevneu.2013.01.003
  2. Treadmill exercise alleviates short-term memory impairment in 6-hydroxydopamine-induced Parkinson’s rats vol.9, pp.3, 2013, https://doi.org/10.12965/jer.130048
  3. Adenosine A2A-receptor agonist polydeoxyribonucleotide promotes gastric ulcer healing in Mongolian gerbils vol.18, pp.6, 2012, https://doi.org/10.1080/19768354.2014.983968
  4. Dexmedetomidine, α2-adrenoceptor agonist, does not induce apoptosis in the brachial plexus of rats vol.18, pp.6, 2012, https://doi.org/10.1080/19768354.2014.983969
  5. Voluntary wheel running ameliorates symptoms of MK-801-induced schizophrenia in mice vol.10, pp.6, 2014, https://doi.org/10.3892/mmr.2014.2644
  6. Inhibitory effects of Angelica gigas extract on memory deficits induced by chronic stress in the rat vol.18, pp.1, 2014, https://doi.org/10.1080/19768354.2013.879922
  7. Stress-Induced Depression Is Alleviated by Aerobic Exercise Through Up-Regulation of 5-Hydroxytryptamine 1A Receptors in Rats vol.19, pp.1, 2015, https://doi.org/10.5213/inj.2015.19.1.27
  8. Treadmill exercise alleviates stress-induced impairment of social interaction through 5-hydroxytryptamine 1A receptor activation in rats vol.11, pp.4, 2012, https://doi.org/10.12965/jer.150225
  9. Treadmill exercise ameliorates depressive symptoms through increasing serotonin expression in postpartum depression rats vol.13, pp.2, 2017, https://doi.org/10.12965/jer.1734968.484
  10. Long-term chemical castration induces depressive symptoms by suppressing serotonin expression in rats vol.22, pp.1, 2012, https://doi.org/10.1080/19768354.2018.1427626
  11. Post-stroke BDNF concentration changes following proprioceptive neuromuscular facilitation (PNF) exercises vol.9, pp.7, 2020, https://doi.org/10.4103/jfmpc.jfmpc_1051_19
  12. Brain-derived neurotrophic factor levels in acute stroke and its clinical implications vol.6, pp.3, 2012, https://doi.org/10.4103/bc.bc_23_20