The differential effects of neuroleptic drugs and PACAP on the expression of BDNF mRNA and protein in a human glioblastoma cell line

• Autorzy: Jozwiak-Bebenista M. , Jasinska-Straschein M. , Kowalczyk E.
• Języki publikacji: EN

Abstrakty

EN

It has been suggested that, in addition to modulation of monoaminergic neurotransmission, antipsychotic drugs can also affect expression of neurotrophic factors in the brain. The present study was aimed to examine the effects of the first generation neuroleptic drug (FGA; haloperidol) and second generation neuroleptic drugs (SGAs; olanzapine and amisulpride) on expression and level of brain-derived neurotrophic factor (BDNF) in astrocyte-like T98G glioblastoma cell line. Effects of these drugs were compared to the action of PACAP38, a neuropeptide with well known BDNF-mediated neuroprotective effects. The tested neuroleptics differentially regulated the mRNA expression and protein level of BDNF depending on the concentration and incubation time. Using rtPCR technique, we demonstrate that, from the three tested neuroleptics, both haloperidol as well as olanzapine at 5 μM concentration (but not at 20 μM) increased BDNF mRNA expression with a similar efficacy after a 72 h incubation. In order to confirm the observed changes in the mRNA expression of BDNF, a protein expression assay was performed. The exposure of cells only to 5 μM olanzapine for 72 h increased BDNF concentration in the culture medium by 29%. Additionally, PACAP significantly up-regulated BDNF mRNA expression in T98G cells and the obtained results correlated positively with the increased production of BDNF protein, by 22% above control. The results of the paper show that olanzapine, similarly to exogenous PACAP38, increased BDNF mRNA expression and protein release, which can contribute to its neuroprotective mechanism of action in the cells of nonneuronal origin. The results of the present paper confirm the findings that BDNF may represent the key target for olanzapine and PACAP.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2017
• Tom: 77
• Numer: 3
• Opis fizyczny: p.205-213,fig.,ref.

Twórcy

autor

Jozwiak-Bebenista M.

• Department of Pharmacology and Toxicology, Interfaculty Chair of Basic and Clinical Pharmacology and Toxicology, Medical University of Lodz, Poland

autor

Jasinska-Straschein M.

• Department of Biopharmacy, Medical University of Lodz, Lodz, Poland

autor

Kowalczyk E.

• Department of Pharmacology and Toxicology, Interfaculty Chair of Basic and Clinical Pharmacology and Toxicology, Medical University of Lodz, Poland

Bibliografia

• Angelucci F, Aloe  L, Iannitelli A, Gruber SH, Mathe AA (2005) Effect of chronic olanzapine treatment on nerve growth factor and brain-derived neurotrophic factor in the rat brain. Eur Neuropsychopharmacol 15: 311–317.
• Angelucci F, Mathe AA, Aloe L (2000) Brain-derived neurotrophic factor and tyrosine kinase receptor TrkB in rat brain are significantly altered after haloperidol and risperidone administration. J Neurosci Res 60: 783–794.
• Avila Rodriguez  M, Garcia-Segura LM, Cabezas R, Torrente D, Capani F, Gonzalez J, Barreto GE (2014) Tibolone protects T98G cells from glucose deprivation. J Steroid Biochem Mol Biol 144: 294–303.
• Bai O, Chlan-Fourney J, Bowen R, Keegan D, Li XM (2003) Expression of brain-derived neurotrophic factor mRNA in rat hippocampus after treatment with antipsychotic drugs. J Neurosci Res 71: 127–131.
• Beck T, Lindholm D, Castrén E, Wree A (1994) Brain-derived neurotrophic factor protects against ischemic cell damage in rat hippocampus. J Cereb Blood Flow Metab 14: 689–692.
• Bernstein HG, Steiner J, Guest PC, Dobrowolny H, Bogerts B (2015) Glial cells as key players in schizophrenia pathology: recent insights and concepts of therapy. Schizophr Res 161: 4–18.
• Bramham CR, Messaoudi E (2005) BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog Neurobiol 76: 99–125.
• Cabezas R, Avila MF, González J, El-Bachá RS, Barreto GE (2015) PDGF-BB protects mitochondria from rotenone in T98G cells. Neurotox Res 27: 355–367.
• Chen Y, Samal B, Hamelink CR, Xiang CC, Chen Y, Chen  M, Vaudry D, Brownstein MJ, Hallenbeck JM, Eiden LE (2006) Neuroprotection by endogenous and exogenous PACAP following stroke. Regul Pept 137: 4–19.
• Chlan-Fourney J, Ashe P, Nylen K, Juorio AV, Li XM (2002) Differential regulation of hippocampal BDNF mRNA by typical and atypical antipsychotic administration. Brain Res 954: 11–20.
• Cohen CI, Meesters PD, Zhao J (2015) New perspectives on schizophrenia in later life: implications for treatment, policy, and research. Lancet Psychiatry 4: 340–350.
• Coppell  AL,  Pei  Q,  Zetterström TS (2003) Bi-phasic change in BDNF gene expression following antidepressant drug treatment. Neuropharmacology 44: 903–10.
• de Bartolomeis A, Tomasetti C, Iasevoli F (2015) Update on the Mechanism of Action of Aripiprazole: Translational Insights into Antipsychotic Strategies Beyond Dopamine Receptor Antagonism. CNS Drugs 9: 773–799.
• de Joannon AC, Mancini F, Landolfi C, Soldo  L, Leta A, Ruggieri A, Mangano  G, Polenzani  L, Pinza  M, Milanese C. (2000) Adenosine triphosphate affects interleukin-1beta release by T98G glioblastoma cells through a  purinoceptorindependent mechanism. Neurosci Lett 285: 218–222.
• Dold  M, Samara MT, Li C, Tardy  M, Leucht S (2015) Haloperidol versus first-generation antipsychotics for the treatment of schizophrenia and other psychotic disorders. Cochrane Database Syst Rev. Durany N, Thome J (2004) Neurotrophic factors and the pathophysiology of schizophrenic psychoses. Eur Psychiatry 19: 326–337.
• Frechilla D, Garcia-Osta A, Palacios S, Cenarruzabeitia E, Del Rio J (2001) BDNF mediates the neuroprotective effect of PACAP-38 on rat cortical neurons. Neuroreport 12: 919–923.
• Georg B, Fahrenkrug J. (2000) Pituitary adelylate cyclase-activating peptide is an activator of vasoactive intestinal polypeptide gene transcription in human neuroblastoma cells. Brain Res Mol Brain Res 79: 67–76.
• Hashimoto R, Hashimoto H, Shintani N, Ohi K, Hori H, Saitoh O, Kosuga A, Tatsumi M, Iwata N, Ozaki N, Kamijima K, Baba A, Takeda M, Kunugi H (2010) Possible association between the pituitary adenylate cyclase-activating polypeptide (PACAP) gene and major depressive disorder. Neurosci Lett 468: 300–302.
• Hutchinson AJ, Chou CL, Israel DD, Xu W, Regan JW (2009) Activation of EP2 prostanoid receptors in human glial cell lines stimulates the secretion of BDNF. Neurochem Int 54: 439–446.
• Jóźwiak-Bębenista  M,  Kowalczyk  E. (2017) Neuroleptic Drugs and PACAP Differentially Affect the mRNA Expression of Genes Encoding PAC1/ VPAC Type Receptors. Neurochem Res 42: 943–952. 
• Jóźwiak-Bębenista M, Kowalczyk E, Nowak JZ (2015) The cyclic AMP effects and neuroprotective activities of PACAP and VIP in cultured astrocytes and neurons exposed to oxygen-glucose deprivation. Pharmacol Rep 67: 332–338.
• Kotani  S,  Yamauchi T,  Teramoto  T,  Ogura H (2006) Pharmacological evidence of cholinergic involvement in adult hippocampal neurogenesis in rats. Neuroscience. 142: 505–14.
• Kusumi I, Boku S, Takahashi Y (2015) Psychopharmacology of atypical antipsychotic drugs: From the receptor binding profile to neuroprotection and neurogenesis. Psychiatry Clin Neurosci 69: 243–258.
• Lu XH, Dwyer DS (2005) Second-generation antipsychotic drugs, olanzapine, quetiapine, and clozapine enhance neurite outgrowth in PC12 cells via PI3K/AKT, ERK, and pertussis toxin-sensitive pathways. J Mol Neurosci 27: 43–64.
• Matsuzaki S, Tohyama  M (2008) Regulation of pituitary adenylyl cyclase-activating polypeptide (PACAP, ADCYAP1: adenylyl cyclase-activating polypeptide 1) in the treatment of schizophrenia. Expert Opin Ther Targets 12: 1097–1108.
• Mattson MP, Lovell MA, Furukawa K, Markesbery WR (1995) Neurotrophic factors attenuate glutamate-induced accumulation of peroxides, elevation of intracellular Ca2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J Neurochem 65: 1740–1751.
• Mattson MP, Zhang Y, Bose S (1993) Growth factors prevent mitochondrial dysfunction, loss of calcium homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose. Exp Neurol 121: 1–13.
• Ogata K, Shintani N, Hayata-Takano A, Kamo T, Higashi S, Seiriki K, Momosaki H, Vaudry D, Vaudry H, Galas  L, Kasai A, Nagayasu K, Nakazawa T, Hashimoto R, Ago Y, Matsuda T, Baba A, Hashimoto H (2015) PACAP enhances axon outgrowth in cultured hippocampal neurons to a comparable extent as BDNF. PLoS One 10:e0120526.
• Paczkowska E, Łuczkowska K, Piecyk K, Rogińska D, Pius-Sadowska E, Ustianowski P, Cecerska E, Dołęgowska B, Celewicz Z, Machaliński  B (2015) The influence of BDNF on human umbilical cord blood stem/progenitor cells: implications for stem cell-based therapy of neurodegenerative disorders. Acta Neurobiol Exp 75: 172–191.
• Pandya CD, Kutiyanawalla A, Pillai A (2013) BDNF-TrkB signaling and neuroprotection in schizophrenia. Asian J Psychiatr 6: 22–28.
• Parikh V, Khan MM, Mahadik SP (2004) Olanzapine counteracts reduction of brain-derived neurotrophic factor and TrkB receptors in rat hippocampus produced by haloperidol. Neurosci Lett 356: 135–139.
• Park SW, Lee SK, Kim JM, Yoon JS, Kim YH (2006) Effects of quetiapine on the brain-derived neurotrophic factor expression in the hippocampus and neocortex of rats. Neurosci Lett 402: 25–29.
• Park SW, Lee CH, Lee JG, Lee SJ, Kim NR, Choi SM, Kim YH (2009) Differential effects of ziprasidone and haloperidol on immobilization stress-induced mRNA BDNF expression in the hippocampus and neocortex of rats. J Psychiatr Res 43: 274–281.
• Park SW, Seo MK, Cho HY, Lee JG, Lee BJ, Seol  W, Kim YH (2011) Differential effects of amisulpride and haloperidol on dopamine D2 receptor-mediated signaling in SH-SY5Y cells. Neuropharmacology 61: 761–769.
• Pillai A, Kale A, Joshi S, Naphade N, Raju MS, Nasrallah H, Mahadik SP (2010) Decreased BDNF levels in CSF of drug-naive first-episode psychotic subjects: correlation with plasma BDNF and psychopathology. Int J Neuropsychopharmacol 13: 535–539.
• Ratajczak P, Kus K, Murawiecka P, Słodzińska I, Giermaziak  W, Nowakowska E (2015) Biochemical and cognitive impairments observed in animal models of schizophrenia induced by prenatal stress paradigm or methylazoxymethanol acetate administration. Acta Neurobiol Exp 75: 314–325.
• Reichenstein  M, Rehavi  M, Pinhasov A (2008) Involvement of pituitary adenylate cyclase activating polypeptide (PACAP) and its receptors in the mechanism of antidepressant action. J Mol Neurosci 36: 330–338.
• Rizos EN, Papadopoulou A, Laskos E, Michalopoulou PG, Kastania A, Vasilopoulos D, Katsafouros K, Lykouras  L (2010) Reduced serum BDNF levels in patients with chronic schizophrenic disorder in relapse, who were treated with typical or atypical antipsychotics. World J Biol Psychiatry 11: 251–255.
• Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101–1108.
• Seeman P (2002) Atypical antipsychotics: mechanism of action. Can J Psychiatry 47: 27–38
• Shao Z, Dyck LE, Wang H, Li XM (2006) Antipsychotic drugs cause glial cell line-derived neurotrophic factor secretion from C6 glioma cells. J Psychiatry Neurosci 31: 32–37.
• Shin H, Song JH (2014) Antipsychotics, chlorpromazine and haloperidol inhibit voltage-gated proton currents in BV2 microglial cells. Eur J Pharmacol 738: 256–262.
• Steffek AE, McCullumsmith RE, Haroutunian  V, Meador-Woodruff JH (2008) Cortical expression of glial fibrillary acidic protein and glutamine synthetase is decreased in schizophrenia. Schizophr Res 103: 71–82.
• Tan YL, Zhou DF, Zhang XY (2005) Decreased plasma brain-derived neurotrophic factor levels in schizophrenic patients with tardive dyskinesia: association with dyskinetic movements. Schizophr Res 74, 260–270.
• Tsapakis EM, Dimopoulou T, Tarazi FI (2015) Clinical management of negative symptoms of schizophrenia: An update. Pharmacol Ther 153: 135–147.
• Vaidya  VA,  Marek  GJ,  Aghajanian GK,  Duman  RS (1997) 5-HT2A receptor-mediated regulation of brain-derived neurotrophic factor mRNA in the hippocampus and the neocortex. J Neurosci 17: 2785–95.
• Xie Q, Thompson R, Hardy K, DeCamp L, Berghuis B, Sigler R, Knudsen B, Cottingham S, Zhao P, Dykema K, Cao B, Resau J, Hay R, Vande Woude GF (2008) A highly invasive human glioblastoma pre-clinical model for testing therapeutics. J Transl Med. 6: 77.
• Zabłocka A, Mitkiewicz M, Macała J, Janusz M (2015) Neurotrophic Activity of Cultured Cell Line U87 is Up-Regulated by Proline-Rich Polypeptide Complex and Its Constituent Nonapeptide. Cell Mol Neurobiol 35: 977–986.