Comparison of the influence of two models of mild stress on hippocampal brain - derived neurotrophin factor (BDNF) immunoreactivity in old age rats

• Autorzy: Badowska-Szalewska E. , Ludkiewicz B. , Krawczyk R. , Melka N. , Morys J.
• Języki publikacji: EN

Abstrakty

EN

The way hippocampal neurons function during stress in old age (critical times of life) is dependent on brain derived neurotrophin factor (BDNF). This study examined the influence of acute and chronic forced swim (FS) or high‑light open field (HL‑OF) stimulation on the density of BDNF immunoreactive (ir) neurons in the hippocampal pyramidal layers of CA1, CA2, CA3 regions and the granular layer of dentate gyrus (DG) in old (postnatal day 720; P720) Wistar Han rats. Our data showed that in comparison with non‑stressed rats, acute FS caused a significant increase in the density of BDNF‑ir neurons in CA2 and CA3, while acute HL‑OF led to an increase in this factor in all hippocampal subfields with the exception of DG. However, the density of BDNF‑ir cells remained unchanged after exposure to chronic FS or HL‑OF in the hippocampal regions in relation to the control rats. These results indicate that acute FS or HL‑OF proved to be a stressor that induces an increase in the density of BDNF‑ir pyramidal neurons, which was probably connected with up‑regulation of HPA axis activity and short‑time memory processing of the stressful situation. Moreover, as far as the influence on BDNF‑ir cells in hippocampus is concerned, chronic FS or HL‑OF was not an aggravating factor for rats in the ontogenetic periods studied.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2017
• Tom: 77
• Numer: 1
• Opis fizyczny: p.68-76,fig.,ref.

Twórcy

autor

Badowska-Szalewska E.

• Department of Anatomy and Neurobiology, Medical University of Gdansk, Gdansk, Poland

autor

Ludkiewicz B.

• Department of Anatomy and Neurobiology, Medical University of Gdansk, Gdansk, Poland

autor

Krawczyk R.

• Department of Anatomy and Neurobiology, Medical University of Gdansk, Gdansk, Poland

autor

Melka N.

• Department of Anatomy and Neurobiology, Medical University of Gdansk, Gdansk, Poland

autor

Morys J.

• Department of Anatomy and Neurobiology, Medical University of Gdansk, Gdansk, Poland

Bibliografia

• Adlard PA, Engesser‑Cesar C, Cotman CW (2011) Mild stress facilitates learning and exercise improves retention in aged mice. Exp Gerontol 46: 53–59. doi: 10.1016/j.exger.2010.10.001.
• Alleva E, Santucci D (2001) Psychosocial vs. “physical” stress situations in rodents and humans: role of neurotrophins. Physiol Behav 73: 313–320.
• Amaral DG, Witter MP (1995) Hippocampal formation. In: The Rats Nervous System (2nd ed.) (Paxinos G, Ed.). Academic Press Inc., San Diego, CA, USA. p. 443–493.
• Badowska‑Szalewska E, Ludkiewicz B, Klejbor I, Świetlik D, Moryś J (2012) Brain derived neurotrophic factor (BDNF) containing neurons in the hypothalamic paraventricular and supraoptic nuclei of juvenile and middle‑aged rats after chronic stress. Int J Dev Neurosci 30: 139–146. doi: 10.1016/j.ijdevneu.2011.12.001.
• Badowska‑Szalewska E, Ludkiewicz B, Krawczyk R, Moryś J (2016a) Exposure to mild stress and brain derived neurotrophin factor (BDNF) immunoreactivity in the hypothalamic paraventricular (PVN) and supraoptic (SON) nuclei: Comparison between aged and adult rats. J Chem Neuroanat 78: 57–64. doi: 10.1016/j.jchemneu.2016.08.007.
• Badowska‑Szalewska E, Ludkiewicz B, Krawczyk R, Moryś J (2016b) The impact of two mild stressors on the nerve growth factor (NGF) immunoreactivity in the amygdala in aged rats compared to adult ones. Int J Dev Neurosci 49: 6–13. doi: 10.1016/j.ijdevneu.2015.12.005.
• Badowska‑Szalewska E, Spodnik E, Klejbor I, Morys J (2010) Effects of chronic forced swim stress on hippocampal brain‑derived neutrophic factor (BDNF) and its receptor (TrkB) immunoreactive cells in juvenile and aged rats. Acta Neurobiol Exp (Wars) 70(4): 370–381.
• Bartolomucci A, De Biurrun G, Czéh, B, Van Kampen  M, Fuchs E (2002) Selective enhancement of spatial learning under chronic psychosocial stress. Eur J Neurosci 15: 1863–1866.
• Bouwknecht JA, Spiga F, Staub DR, Hale MW, Shekhar A, Lowry CA (2007) Differential effects of exposure to low‑light or high‑light open‑field on anxiety‑related behaviors: relationship to c‑Fos expression in serotonergic and non‑serotonergic neurons in the dorsal raphe nucleus. Brain Res Bull 72: 32–43.
• Cirulli F, Alleva E (2009) The NGF saga: from animal models of psychosocial stress to stress‑related psychopathology. Front Neuroendocrinol 30: 379–395.
• Dal‑Zotto S, Martí O, Armario A (2000) Influence of single or repeated experience of rats with forced swimming on behavioural and physiological responses to the stressor. Behav Brain Res 114: 175–181.
• Dhabhar FS, McEwen BS, Spencer RL (1997) Adaptation to prolonged or repeated stress – comparison between rat strains showing intrinsic differences in reactivity to acute stress. Neuroendocrinology 65: 360–368.
• Frolkis VV (1993) Stress‑age syndrome. Mech Ageing Dev 69: 93–107.
• Fuchs E, Flügge G (2003) Chronic social stress: effects on limbic brain structures. Physiol Behav 79: 417–427.
• Givalois  L, Naert G, Rage F, Ixart G, Arancibia S, Tapia‑Arancibia  L (2004) A single brain‑derived neurotrophic factor injection modifies hypothalamo‑pituitary‑adrenocortical axis activity in adult male rats. Mol Cell Neurosci 27: 280–295.
• Gray JD, Milner TA, McEwen BS (2013) Dynamic plasticity: the role of glucocorticoids, brain‑derived neurotrophic factor and other trophic factors. Neuroscience 239: 214–227. doi: 10.1016/j. neuroscience.2012.08.034.
• Greenberg ME, Xu B, Lu B, Hempstead BL (2009) New insights in the biology of BDNF synthesis and release: implications in CNS function. J Neurosci 29: 12764–12767. doi: 10.1523/JNEUROSCI.3566‑09.2009.
• Herman JP (1993) Regulation of adrenocorticosteroid receptor mRNA expression in the central nervous system. Cell Mol Neurobiol 13: 349–372.
• Herman JP, Figueiredo H, Mueller NK, Ulrich‑Lai Y, Ostrander MM, Choi DC, Cullinan WE (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo‑pituitary‑adrenocortical responsiveness. Front Neuroendocrinol 24: 151–180.
• Herman JP, Ostrander MM, Mueller NK, Figueiredo H (2005) Limbic system mechanisms of stress regulation: hypothalamo‑pituitary‑adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29: 1201–1213.
• Jacobson L, Sapolsky R (1991) The role of the hippocampus in feedback regulation of the hypothalamic‑pituitary‑adrenocortical axis. Endocr Rev 12: 118–134.
• Jankord R, Herman JP (2008) Limbic regulation of hypothalamo‑pituitary‑adrenocortical function during acute and chronic stress. Ann N Y Acad Sci 1148: 64–73. doi: 10.1196/annals.1410.012.
• Katoh‑Semba R, Semba R, Takeuchi IK, Kato K (1998) Age‑related changes in levels of brain‑derived neurotrophic factor in selected brain regions of rats, normal mice and senescence‑accelerated mice: a comparison to those of nerve growth factorand neurotrophin‑3. Neurosci Res 31: 227–234.
• Kim JJ, Diamond DM (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci. 3: 453–462.
• Kovács KJ (1998) c‑Fos as a transcription factor: a stressful (re)view from a functional map. Neurochem Int 33: 287–297.
• Lessmann V, Gottmann K, Heumann R (1994) BDNF and NT‑4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones. Neuroreport 6: 21–25.
• Li Y, Ji YJ, Jiang H, Liu DX, Zhang Q, Fan SJ, Pan F (2009) Effects of unpredictable chronic stress on behavior and brain‑derived neurotrophic factor expression in CA3 subfield and dentate gyrus of the hippocampus in different aged rats. Chin Med J (Engl) 122: 1564–1569.
• Marmigère F, Givalois  L, Rage F, Arancibia S, Tapia‑Arancibia  L (2003) Rapid induction of BDNF expression in the hippocampus during immobilization stress challenge in adult rats. Hippocampus 13: 646–655.
• Mattson MP, Maudsley S, Martin B (2004) A neural signaling triumvirate that influences ageing and age‑related disease: insulin/IGF‑1, BDNF and serotonin. Ageing Res Rev 3: 445–464.
• McAllister AK, Katz LC, Lo DC (1999) Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22: 295–318.
• McEwen BS (2006) Protective and damaging effects of stress mediators: central role of the brain. Dialogues Clin Neurosci 8: 367–381.
• McEwen BS, Magarinos AM (2001) Stress and hippocampal plasticity: Implications for the pathophysiology of affective disorders. Hum Psychopharmacol 16: S7–S19.
• Meyza KZ, Boguszewski PM, Nikolaev E, Zagrodzka J (2007) The effect of age on the dynamics and the level of c‑Fos activation in response to acute restraint in Lewis rats. Behav Brain Res 180: 183–189.
• 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.
• Pardon MC (2007) Stress and ageing interactions: A paradox in the context of shared etiological and physiopathological processes. Brain Res Rev 54: 251–273.
• Paxinos G, Watson C (2007) The Rat Brain in Stereotaxic Coordinates (6th ed.). New York: Academic Press Inc, New York, NY, USA. Pedersen WA, Wan R, Mattson MP (2001) Impact of aging on stress‑responsive neuroendocrine systems. Mech Ageing Dev 122: 963–983.
• Poo M (2001) Neurotrophins as synaptic modulators. Nat Rev Neurosci 2: 24–32.
• Rex CS, Kramár EA, Colgin LL, Lin B, Gall CM, Lynch G (2005) Long‑term potentiation is impaired in middle‑aged rats: regional specificity and reversal by adenosine receptor antagonists. J Neurosci 25: 5956–5966.
• Richter‑Levin G (2004) The amygdala, the hippocampus, and emotional modulation of memory. Neuroscientist 10: 31–39.
• Russo‑Neustadt A (2003) Brain‑derived neurotrophic factor, behavior, and new directions for the treatment of mental disorders. Semin Clin Neuropsychiatry 8: 109–118.
• Schulte‑Herbrüggen O, Chourbaji S, Ridder S, Brandwein C, Gass P, Hörtnagl H, Hellweg R (2006) Stress‑resistant mice overexpressing glucocorticoid receptors display enhanced BDNF in the amygdala and hippocampus with unchanged NGF and serotonergic function. Psychoneuroendocrinology 31: 1266–1277.
• Shao SH, Shi SS, Li ZL, Zhao MS, Xie SY, Pan F (2010) Aging effects on the BDNF mRNA and TrkB mRNA expression of the hippocampus in different durations of stress. Chin J  Physiol 53: 285–293.
• Erratum in: Chin J Physiol 53: 472. Shi SS, Shao SH, Yuan BP, Pan F, Li ZL (2010) Acute stress and chronic stress change brain‑derived neurotrophic factor (BDNF) and tyrosine kinase‑coupled receptor (TrkB) expression in both young and aged rat hippocampus. Yonsei Med J 51: 661–671. doi: 10.3349/ymj.2010.51.5.661.
• Silhol  M, Bonnichon  V, Rage F, Tapia‑Arancibia  L (2005) Age‑related changes in brain‑derived neurotrophic factor and tyrosine kinase receptor isoforms in the hippocampus and hypothalamus in male rats. Neuroscience 132: 613–624.
• Smith MA (1996) Hippocampal vulnerability to stress and aging: possible role of neurotrophic factors. Behav Brain Res 78: 25–36.
• Smith MA, Cizza G (1996) Stress‑induced changes in brain‑derived neurotrophic factor expression are attenuated in aged Fischer 344/N rats. Neurobiol Aging 17: 859–864.
• Smith MA, Makino S, Kvetnansky R, Post RM (1995) Stress and glucocorticoids affect the expression of brain‑derived neurotrophic factor and neurotrophin‑3 mRNAs in the hippocampus. J Neurosci 15: 1768–1777.
• Tapia‑Arancibia L, Aliaga E, Silhol M, Arancibia S (2008) New insights into brain BDNF function in normal aging and Alzheimer disease. Brain Res Rev 59: 201–220.
• Tapia‑Arancibia L, Rage F, Givalois L, Arancibia S (2004) Physiology of BDNF: focus on hypothalamic function. Front Neuroendocrinol 25: 77–107.
• Thoenen H (1995) Neurotrophins and neuronal plasticity. Science 270: 593–598.
• Thrivikraman KV, Nemeroff CB, Plotsky PM (2000) Sensitivity to glucocorticoid‑mediated fast‑feedback regulation of the hypothalamic‑pituitary‑adrenal axis is dependent upon stressor specific neurocircuitry. Brain Res 870: 87–101.
• Ulrich‑Lai YM, Herman JP (2009) Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10: 397–409.
• Venero C, Borrell J (1999) Rapid glucocorticoid effects on excitatory amino acid levels in the hippocampus: a microdialysis study in freely moving rats. Eur J Neurosci 11: 2465–2473.
• West AE (2008) Biological functions of activity‑dependent transcription revealed. Neuron 60: 523–525.