Title

Aging Effects on the BDNF mRNA and TrkB mRNA Expression of the Hippocampus in Different Durations of Stress

Authors

Shu-Hong Shao;Shou-Sen Shi;Zun-Ling Li;Ming-Shan Zhao;Shu-Yang Xie;Fang Pan

Key Words

BNDF ; hippocampus ; behavior ; senescence

PublicationName

The Chinese Journal of Physiology

Volume or Term/Year and Month of Publication

53卷5期(2010 / 10 / 31)

Page #

285 - 293

Content Language

英文

English Abstract

Brain-derived neurotrophins factor (BDNF) belongs to the neurotrophins family which acts on neuronal survival and growth and has been associated with cognition process. TrkB is the primary signal transduction receptor for BDNF. In the present study, hippocampal BDNF and TrkB mRNA were detected by RT-PCR in 2-and 22-month rats, respectively, which were exposed to different durations of mild stress protocol of 8-day, 21-day and 28-day chronic unpredictable mild stress (CUMS). Observation of exploratory behavior in an open field (OF) test indicated stress levels and changes of spontaneous activity. We demonstrated that CUMS induced decrease of BDNF mRNA in two aged groups, but the increase change of TrkB mRNA compared with those of the control groups. Moreover, the changes of BDNF mRNA and TrkB mRNA measured in both the 21-day and 28-day stress groups represent obvious decrease than those of the 8-day stress groups, and the expression examined in young groups appeared to be higher than those of the aged group, especially in the 28-day stress groups. Results of OF test showed that explicit behaviors in two age groups decreased gradually with the process of stress revealing a depressive state under the stress condition. Meanwhile, the behaviors of young rats seemed to be more active than those of the aged rats, exhibiting weak adaptation to the stress. The study suggested that stress paradigm and aging certainly had effect on the regulation of BDNF mRNA and TrkB mRNA which might be related to damage and protection function of the hippocampus.

Topic Category 醫藥衛生 > 基礎醫學
Reference
  1. Adlard, P. A.,Cotman, C. W.(2004).Voluntary exercise protects against stress-induced decreases in brain- derived neurotrophic factor protein expression.Neuroscience,124,985-992.
  2. Aggleton, J. P.,Vann, S. D.,Oswald, C. J.,Good, M.(2000).Identifying cortical inputs to the rat hippocampus that subserve allocentric spatial processes: a simple problem with a complex answer.Hippocampus,10,466-474.
  3. Alberts, S. C.,Sapolsky, R. M.,Altmann, J.(1992).Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group.Horm. Behav.,26,167-178.
  4. Altar, C. A.(1999).Neurotrophins and depression.Trends Pharmacol. Sci.,20,59-61.
  5. Baker, S. L.,Kentner, A. C.,Konkle, A. T.,Santa-Maria Barbagallo, L.,Bielajew, C.(2006).Behavioral and physiological effects of chronic mild stress in female rats.Physiol. Behav.,87,314-322.
  6. Barde, Y. A.(1994).Neurotrophins: a family of proteins supporting the survival of neurons.Prog. Clin. Biol. Res.,390,45-56.
  7. Beck, K. D.,Luine, V. N.(1999).Food deprivation modulates chronic stress effects on object recognition in male rats: role of monoamines and amino acids.Brain Res.,830,56-71.
  8. Benelli, A.,Filaferro, M.,Bertolini, A.,Genedani, S.(1999).Influence of S-adenosyl-L-methionine on chronic mild stress-induced anhedonia in castrated rats.Br. J. Pharmacol.,127,645-654.
  9. Berg-von der Emde, K.,Dees, W. L.,Hiney, J. K.,Hill, D. F.,Dissen, G. A.,Costa, M. E.,Moholt-Siebert, M.,Ojeda, S. R.(1995).Neurotrophins and the neuroendocrine brain: different neurotrophins sustain anatomically and functionally segregated subsets of hypothalamic dopaminergic neurons.J. Neurosci.,15,4223-4237.
  10. Bremner, J. D.(2006).Stress and brain atrophy.CNS Neurol. Disord. Drug Targets,5,503-512.
  11. Chourbaji, S.,Hellweg, R.,Brandis, D.,Zorner, B.,Zacher, C.,Lang, U. E.,Henn, F. A.,Hortnagl, H.,Gass, P.(2004).Mice with reduced brain-derived neurotrophic factor expression show decreased choline acetyltransferase activity, but regular brain monoamine levels and unaltered emotional behavior.Mol. Brain Res.,121,28-36.
  12. Cosi, C.,Spoerri, P. E.,Comelli, M. C.,Guidolin, D.,Skaper, S. D.(1993).Glucocorticoids depress activity-dependent expression of BDNF mRNA in hippocampal neurons.Neuroreport,4,527-530.
  13. Croll, S. D.,IP, N. Y.,Lindsay R. M.,Wieqand, S. J.(1998).Expression of BDNF and TrkB as a function of age and cognitive performance.Brain Res.,812,200-208.
  14. De Kloet, E. R.,Vreugdenhil, E.,Oitzl, M. S.,Joels, M.(1998).Brain corticosteroid receptor balance in health and disease.Endocr. Rev.,19,269-301.
  15. Duman, R. S.,Heninger, G. R.,Nestler, E. J.(1997).A molecular and cellular theory of depression.Arch. Gen. Psychiatry,54,597-606.
  16. Fuchikami, M.,Morinobu, S.,Kurata, A.,Yamarmoto, S.,Yamawaki, S.(2009).Single immobilization stress differentially alters the expression profile of transcripts of the brain-derived neurotrophic factor (BDNF) gene and histone acetylation at its promoters in the rat hippocampus.Int. J. Neuropsychopharmacol,12,73-82.
  17. Fukumoto, T.,Morinobu, S.,Okamoto, Y.,Kagaya, A.,Yamawaki, S.(2001).Chronic lithium treatment increases the expression of brain-derived neurotrophic factor in the rat brain.Psychopharmacology,158,100-106.
  18. Givolois, 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.
  19. Gregus, A.,Wintink, A. J.,Davis, A. C.,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.
  20. Gronli, J.,Bramham, C.,Murison, R.,Kanhema, T.,Fiske, E.,Bjorvatn, B.,Ursin, R.,Portas, C. M.(2006).Chronic mild stress inhibits BDNF protein expression and CREB activation in the dentate gyrus but not in the hippocampus proper.Pharmacol. Biochem. Behav.,85,842-849.
  21. Gronli, J.,Murison, R.,Bjorvatn, B.,Sorensen, E.,Portas, C. M.,Ursin, R.(2004).Chronic mild stress affects sucrose intake and sleep in rats.Behav. Brain Res.,150,139-147.
  22. Gronli, J.,Murison, R.,Fiske, E.,Bjorvatn, B.,Sorensen, E.,Portas, C. M.,Ursin, R.(2005).Effects of chronic mild stress on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions.Physiol. Behav.,84,571-577.
  23. Hashimoto, K.,Shimizu, E.,Iyo, M.(2004).Critical role of brainderived neurotrophic factor in mood disorders.Brain Res. Rev.,45,104-114.
  24. Hibberd, C.,Yau, J. L. W.,Seckl, J. R.(2000).Glucocorticoids and the aging hippocampus.J. Anat.,197,553-562.
  25. Hock, C.,Heese, K.,Hulette, C.,Rosenberg, C.,Otten, U.(2000).Region specific neurotrophin imbalances in Alzheimer's disease: decreased levels of nerve growth factor on hippocampus and cortical areas.Arch. Neurol.,57,846-851.
  26. Horch, H. W.,Kruttgen, A.,Portbury, S. D.,Katz, L. C.(1999).Destabilization of cortical dendrites and spines by BDNF.Neuron,23,353-364.
  27. Hosinger, R. M. D.,Schnarr, J.,Henry, P.,Castelo, V. T.,Fahnestock, M.(2000).Quantitation of BDNF mRNA in human parietal cortex by competitive reverse transcription-polymerase chain reaction: decreased levels in Alzheimer's disease.Mol. Brain Res.,76,347-354.
  28. Jayatissa, M. N.,Bisgaard, C.,Tingstrom, A.,Papp, M.,Wiborg, O.(2006).Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression.Neuropsychopharmacology,31,2395-2404.
  29. Korte, S. M.(2001).Corticosteroids in relation to fear, anxiety and psychopathology.Neurosci. Biobehav. Rev.,25,117-142.
  30. Laifenfeld, D.,Kerry, R.,Grauer, E.,Klein, E.,Ben-Shacher, D.(2005).Antidepressant and prolonged stress in rats modulate CAM-L1, laminin, and pCREB, implicated in neuronal plasticity.Neurobiol. Dis.,20,432-441.
  31. Lauterborn, J. C.,Poulsen, F. R.,Stinis, C. T.,Isackson, P. J.,Gall, C. M.(1998).Transcript-specific effects of adrenalectomy on seizureinduced BDNF expression in rat hippocampus.Brain Res. Mol. Brain Res.,55,81-91.
  32. Lee, T.,Saruta, J.,Sasaquri, K.,Sato, S.,Tsukinoki, K.(2008).Allowing animals to bite reverses the effects of immobilization stress on hippocampal neurotrophin expression.Brain Res.,1195,43-49.
  33. Lupien, S. J.,de Leon, M.,de Santi, S.,Convit, A.,Tarchish, C.,Nair, N. P. V.,Thakur, M.,McEwen, B. S.,Hauger, R. L.,Meaney, M. J.(1998).Cortisol levels during human aging predict hippocampal atrophy and memory deficits.Nat. Neurosci.,1,69-73.
  34. Makino, S.,Kaneda, T.,Nishiyama, M.,Asaba, K.,Hashimoto, K.(2001).Lack of decrease in hypothalamic and hippocampal glucocorticoid receptor mRNA during starvation.Neuroendocrinology,74,120-128.
  35. Mazure, C. M.,Maciejewski, P. K.,Jacobs, S. C.,Bruce, M. L.(2002).Stressful life events interacting with cognitive/personality styles to predict lateonset major depression.Am. J. Geriatr. Psychiatry,10,297-304.
  36. McEwen, B. S.(2006).Protective and damaging effects of stress mediators: central role of the brain.Dialogues Clin. Neurosci.,8,367-381.
  37. McEwen, B. S.(1999).Stress and hippocampal plasticity.Annu. Rev. Neurosci.,22,105-122.
  38. McEwen, B. S.,Magarinos, A. M.(1997).Stress effects on morphology and function of the hippocampus.Ann. N. Y. Acad. Sci.,821,271-284.
  39. Murakami, S.,Imbe, H.,Morikawa, Y.,Kubo, C.,Senba, E.(2005).Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly.Neurosci. Res.,53,129-139.
  40. Murer, M. G.,Boissiere, F.,Yan, Q.,Hunot, S.,Villares, J.,Fauchex, B.,Agid, Y.,Hirsch, E.,Raisman-Vozari, R.(1999).An immunohistochemical study of the distribution of brain-derived neurotrophic factor in the adult human brain, with particular reference to Alzheimer's disease.Neuroscience,88,1015-1032.
  41. Murua, V. S.,Gomez, R. A.,Andrea, M. E.,Molina, V. A.(1991).Shuttlebox deficits induced by chronic variable stress: reversal by imipramine administration.Pharmacol. Biochem. Behav.,38,125-130.
  42. Nibuya, M.,Takahashi, M.,Russell, D. S.,Duman, R. S.(1999).Repeated stress increases catalytic TrkB mRNA in rat hippocampus.Neurosci. Lett.,267,81-84.
  43. Rage, F.,Givalois, L.,Marmigere, F.,Tapia-Arancibia, L.,Arancibia, S.(2002).Immobilization stress rapidly modulates BDNF mRNA expression in the hypothalamus of adult male rats.Neuroscience,112,309-318.
  44. Sarkisova, K. Yu.,Kulikov, M. A.(2001).Prophylactic actions of the antioxidant agent AEKOL on behavioral (psychoemotional) disturbances induced by chronic stress in rats.Neurosci. Behav. Physiol.,31,503-508.
  45. Scaccianoce, S.,Del Bianco, P.,Caricasole, A.,Nicoletti, F.,Catalani, A.(2003).Relationship between learning, stress and hippocampal brain-derived neurotrophic factor.Neuroscience,121,825-828.
  46. Silhol, M.,Bonnichon, V.,Rage, F.,Tapia-Arancibia L.(2005).Agerelated changes in brain-derived neurotrophic factor and tyrosine kinase receptor isoforms in the hippocampus and hypothalamus in male rats.Neuroscience,132,613-624.
  47. Siuciak, J. A.,Lewis, D. R.,Wiegand, S. J.,Lindsay, R. M.(1997).Antidepressant-like effect of brain-derived neurotrophic factor (BDNF).Pharmacol. Biochem. Behav.,56,131-137.
  48. Smith, J. A.,Boyd, K. M.(1991).The Ethics of Using Animals in Biomedical Research.Oxford:Oxford University Press.
  49. Smith, M. A.,Makino, S.,Kvetnansky, R.,Post, R. M.(1995).Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus.J. Neurosci.,15,1768-1777.
  50. Sun, C. Y.,Qi, S. S.,Lou, X. F.,Sun, S. H.,Wang, X.,Dai, K. Y.,Hu, S. W.,Liu, N. B.(2006).Changes of learning, memory and levels of CaMKII, CaM mRNA, CREB mRNA in the hippocampus of chronic multiple-stressed rats.Chinese Med. J.,119,140-147.
  51. Thoenen, H.(2000).Neurotrophins and activity-dependent plasticity.Prog. Brain Res.,128,183-191.
  52. Toth, E.,Gersner, R.,Wilf-Yarkoni, A.,Raizel, H.,Dar, D. E.,Richter-Levin, G.,Levit, O.,Zangen, A.(2008).Age-dependent effects of chronic stress on brain plasticity and depressive behavior.J. Neurochem.,107,522-532.
  53. Ueyama, T.,Kawai, Y.,Nemoto, K.,Sekimoto, M.,Tone, S.,Senba, E.(1997).Immobilization stress reduced the expression of neurotrophins and their receptors in the rat brain.Neurosci. Res.,28,103-110.
  54. Willner, P.,Sampson, D.,Phillips, G.,Fichera, R.,Foxlow, P.,Muscat, R.(1989).Effects of isolated housing and chronic antidepressant treatment on cooperative social behaviour in rats.Behav. Pharmacol.,1,85-90.
  55. Willner, P.,Sanger, D.,Oglesby, M.(1997).The behavioural pharmacology of anxiety and depression.Behav. Pharmacol.,8,475-476.
  56. Willner, P.,Towell, A.,Sampson, D.,Sophokleous, S.,Muscat, R.(1987).Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant.Psychopharmacology,93,358-364.
  57. Yamada, K.,Mizuno, M.,Nabeshima, T.(2002).Role for brain-derived neurotrophic factor in learning and memory.Life Sci.,70,735-744.
  58. Yamasaki, Y.,Shigeno, T.,Furukawa, Y.,Furukawa, S.(1998).Reduction in brain-derived neurotrophic factor protein level in the hippocampal CA1 dendritic field precedes the delayed neuronal damage in the rat brain.J. Neurosci. Res.,53,318-329.
  59. Yun, S. J.,Park, H. J.,Yeom, M. J.,Hahm, D. H.,Lee, H. J.,Lee, E. H.(2002).Effect of electroacupuncture on the stress induced changes in brain derived neurotrophic factor expression in rat hippocampus.Neurosci. Lett.,318,85-88.
  60. Zhou, J.,Zhang, F.,Zhang, Y.(2000).Corticosterone inhibits generation of long-term potentiation in rat hippocampal slice: involvement of brain derived neurotrophic factor.Brain Res.,885,182-191.
Times Cited
  1. Wu, Shu-Ting,Lee, Yi-Hsuan,Hung, Chia-Hsiu,Hu, Chaur-Jong,Hsieh, Chia-Yu(2015).Effects of Light-Dark Cycle on Hippocampal iNOS Expression and CREB Activation in Rats.中國生理學雜誌,58(1),19-26.