PL EN


Preferencje help
Widoczny [Schowaj] Abstrakt
Liczba wyników
2014 | 74 | 3 |
Tytuł artykułu

BDNF modifies hippocampal KCC2 and NKCC1 expression in a temporal lobe epilepsy model

Treść / Zawartość
Warianty tytułu
Języki publikacji
EN
Abstrakty
EN
Excitatory GABA actions, induced by altered expression of chloride transporters (KCC2/NKCC1), can contribute to seizure generation in temporal lobe epilepsy. In the present study, we evaluated whether BDNF administration can affect KCC2/ NKCC1 expression, ictogenesis and behavioral alterations in this paradigm. Status epilepticus was induced in male rats with pilocarpine, followed by a treatment of either a single high dose or multiple injections of BDNF during the latent phase of temporal lobe epilepsy. Chloride transporters expression, spontaneous recurrent seizures, and hyperexcitability post-seizural behaviors were evaluated after treatment. NKCC1 protein expression was markedly upregulated, whereas that of KCC2 was significantly downregulated in epileptic hippocampi compared to intact controls. Application of BDNF (both single high dose and multiple injections) increased KCC2 expression in epileptic hippocampi, while NKCC1 expression was downregulated exclusively by the single high dose injection of BDNF. Development of spontaneous recurrent seizures was delayed but not prevented by the treatment, and hyperexcitability behaviors were ameliorated for a short period of time. To prevent GABA-A mediated depolarization and design appropriate treatment strategies for temporal lobe epilepsy, chloride transporters can be considered as a target. Future studies are warranted to investigate any possible therapeutic effects of BDNF via altering chloride transporters expression.
Słowa kluczowe
Wydawca
-
Rocznik
Tom
74
Numer
3
Opis fizyczny
p.176-187,fig.,ref.
Twórcy
autor
  • Department of Neuroscience, School of Advanced Technologies in Medicine
  • Division of Neuroscience, Cellular and Molecular Research Center
autor
  • Division of Neuroscience, Cellular and Molecular Research Center
  • Department of Neuroscience, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran
autor
  • Division of Neuroscience, Cellular and Molecular Research Center
  • Department of Anatomy, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
  • Department of Anatomy, School of Medicine
  • Department of Neuroscience, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran
autor
  • Department of Neuroscience, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran
autor
  • Department of Physiology and Pharmacology, Zanjan University of Medical Sciences, Zanjan, Iran
autor
  • Division of Neuroscience, Cellular and Molecular Research Center
autor
  • Department of Pharmaceutical Biotechnology, School of Pharmacy, Shahid Beheshti University of Medical Sciences, Tehran, Iran
  • Department of Neuroscience, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran
  • Division of Neuroscience, Cellular and Molecular Research Center
autor
  • Department of Physiology and Pharmacology, Zanjan University of Medical Sciences, Zanjan, Iran
autor
  • Department of Pharmaceutical Biotechnology, School of Pharmacy, Shahid Beheshti University of Medical Sciences, Tehran, Iran
  • Department of Neuroscience, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran
  • Division of Neuroscience, Cellular and Molecular Research Center
  • Department of Neuroscience, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran
  • Brain and Spinal Cord Injury Research Centre, Imam Khomeini Hospital, Tehran University of Medical sciences, Tehran, Iran
  • Department of Neuroscience, School of Advanced Technologies in Medicine
  • Division of Neuroscience, Cellular and Molecular Research Center
  • Department of Anatomy, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
Bibliografia
  • Aguado F, Carmona MA, Pozas E, Aguiló A, Martínez- Guijarro FJ, Alcantara S, Borrell V, Yuste R, Ibañez CF, Soriano E (2003) BDNF regulates spontaneous correlated activity at early developmental stages by increasing syn- aptogenesis and expression of the K+/Cl- co-transporter KCC2. Development 130: 1267-1280.
  • Ben-Ari Y (2002) Excitatory actions of gaba during devel¬opment: the nature of the nurture. Nat Rev Neurosci 3: 728-739.
  • Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R (2007) GABA: a pioneer transmitter that excites immature neurons and gen-erates primitive oscillations. Physiol Rev 87: 1215-1284.
  • Blaesse P, Guillemin I, Schindler J, Schweizer M, Delpire E, Khiroug L, Friauf E, Nothwang HG (2006) Oligomerization of KCC2 correlates with development of inhibitory neu¬rotransmission. J Neurosci 26: 10407-10419.
  • Boulenguez P, Liabeuf S, Bos R, Bras H, Jean-Xavier C, Brocard C, Stil A, Darbon P, Cattaert D, Delpire E, Marsala M, Vinay L (2010) Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury. Nat Med 16: 302-307.
  • Brandt C, ozadze M, Heuchert N, Rattka M, Loscher W (2010) Disease-modifying effects of phenobarbital and the NKCC1 inhibitor bumetanide in the pilocarpine model of temporal lobe epilepsy. J Neurosci 30: 8602-8612.
  • Carmona MA, Pozas E, Martinez A, Espinosa-Parrilla JF, Soriano E, Aguado F (2006) Age-dependent spontaneous hyperexcitability and impairment of GABAergic function in the hippocampus of mice lacking trkB. Cereb Cortex 16: 47-63.
  • Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R (2002) On the origin of interictal activity in human tem¬poral lobe epilepsy in vitro. Science 298: 1418-1421.
  • Cohen I, Navarro V, Le Duigou C, Miles R (2003) Mesial temporal lobe epilepsy: a pathological replay of develop¬mental mechanisms? Biol Cell 95: 329-333.
  • Dzhala VI, Talos DM, Sdrulla DA, Brumback AC, Mathews GC, Benke TA, Delpire E, Jensen FE, Staley KJ (2005) NKCC1 transporter facilitates seizures in the developing brain. Nat Med 11: 1205-1213.
  • Eftekhari S, Mehvari Habibabadi J, Najafi Ziarani M, Hashemi Fesharaki SS, Gharakhani M, Mostafavi H, Joghataei MT, Beladimoghadam N, Rahimian E, Hadjighassem MR (2013) Bumetanide reduces seizure frequency in patients with temporal lobe epilepsy. Epilepsia 54: e9-12.
  • Engel J Jr (2001) Mesial temporal lobe epilepsy: what have we learned? Neuroscientist 7: 340-352.
  • Ferhat L, Esclapez M, Represa A, Fattoum A, Shirao T, Ben- Ari Y (2003) Increased levels of acidic calponin during dendritic spine plasticity after pilocarpine-induced sei¬zures. Hippocampus 13: 845-858.
  • Fukuchi M, Nii T, Ishimaru N, Minamino A, Hara D, Takasaki I, Tabuchi A, Tsuda M (2009) Valproic acid induces up- or down-regulation of gene expression responsible for the neuronal excitation and inhibition in rat cortical neurons through its epigenetic actions. Neurosci Res 65: 35-43.
  • Gagnon M, Bergeron MJ, Lavertu G, Castonguay A, Tripathy S, Bonin RP, Perez-Sanchez J, Boudreau D, Wang B, Dumas L, Valade I, Bachand K, Jacob-Wagner M, Tardif C, Kianicka I, Isenring P, Attardo G, Coull JA, De Koninck Y (2013) Chloride extrusion enhancers as novel therapeutics for neurological diseases. Nat Med 19: 1524-1528.
  • Han X,Yang N, Xu Y, Zhu J, Chen Z, Liu Z, Dang G, Song C (2011) Simvastatin treatment improves functional recovery after experimental spinal cord injury by upregu- lating the expression of BDNF and GDNF. Neurosci Lett 487: 255-259.
  • Huberfeld G, Wittner L, Clemenceau S, Baulac M, Kaila K, Miles R, Rivera C (2007) Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epi¬lepsy. J Neurosci 27: 9866-9873.
  • Koyama R, Ikegaya Y (2005) To BDNF or not to BDNF: that is the epileptic hippocampus. Neuroscientist 11: 282-287.
  • Leibrock J, Lottspeich F, Hohn A, Hofer M, Hengerer B, Masiakowski P, Thoenen H, Barde YA (1989) Molecular cloning and expression of brain-derived neurotrophic fac¬tor. Nature 341: 149-152.
  • Ludwig A, varov P, Soni S, Thomas-Crusells J, Airaksinen MS, Rivera C (2011) Early growth response 4 mediates BDNF induction of potassium chloride cotransporter 2 transcription. J Neurosci 31: 644-649.
  • Mao X, Ma P, Cao D, Sun C, Ji Z, Min D, Sun H, Xie N, Cai J, Cao Y (2011) Altered expression of GABAA receptors (a4, y2 subunit), potassium chloride cotransporter 2 and astrogliosis in tremor rat hippocampus. Brain Res Bull 86: 373-379.
  • Munoz A, Méndez P, DeFelipe J, Alvarez-Leefmans FJ (2007) Cation-chloride cotransporters and GABA-ergic innervation in the human epileptic hippocampus. Epilepsia 48: 663-673.
  • Nabekura J, Ueno T, Okabe A, Furuta A, Iwaki T, Shimizu- Okabe C, Fukuda A, Akaike N (2002) Reduction of KCC2 expression and GABAA receptor-mediated excita¬tion after in vivo axonal injury. J Neurosci 22: 4412¬4417.
  • Okabe A, Ohno K, Toyoda H, Yokokura M, Sato K, Fukuda A (2002) Amygdala kindling induces upregulation of mRNA for NKCC1, a Na(+), K(+)-2Cl(-) cotransporter, in the rat piriform cortex. Neurosci Res 44: 225-229.
  • Palma E, Amici M, Sobrero F, Spinelli G, Di Angelantonio S, Ragozzino D, Mascia A, Scoppetta C, Esposito V, Miledi R, Eusebi F (2006) Anomalous levels of Cl- trans¬porters in the hippocampal subiculum from temporal lobe epilepsy patients make GABA excitatory. Proc Natl Acad Sci U S A 103: 8465-8468.
  • Paradiso B, Marconi P, Zucchini S, Berto E, Binaschi A, Bozac A, Buzzi A, Mazzuferi M, Magri E, Navarro Mora G, Rodi D, Su T, Volpi I, Zanetti L, Marzola A, Manservigi R, Fabene PF, Simonato M (2009) Localized delivery of fibroblast growth factor-2 and brain-derived neurotrophic factor reduces spontaneous seizures in an epilepsy model. Proc Natl Acad Sci U S A 106: 7191-7196.
  • Pathak HR , Weissinger F, Terunuma M, Carlson GC, Hsu FC, Moss SJ, Coulter DA (2007) "Disrupted dentate granule cell chloride regulation enhances synaptic excit¬ability during development of temporal lobe epilepsy. J Neurosci 27: 14012-14022.
  • Payne JA, ivera C, Voipio J, Kaila K (2003) Cation-chloride co-transporters in neuronal communication, development and trauma.Trends Neurosci 26: 199-206.
  • Pellegrino LJ, Cushman AJ (1979) A Stereotaxic Atlas of the Rat Brain. Plenum Press, New York, NY.
  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expres¬sion software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36.
  • Racine RJ (1972) Modification of seizure activity by electri¬cal stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32: 281-294.
  • Rice AC , Floyd CL, Lyeth BG, Hamm RJ, DeLorenzo RJ (1998) Status epilepticus causes long-term NMDA recep-tor-dependent behavioral changes and cognitive deficits. Epilepsia 39: 1148-1157.
  • Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K (1999) The K+/ Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397: 251-255.
  • Rivera C, Voipio J, Thomas-Crusells J, Li H, Emri Z, Sipila S, Payne JA, Minichiello L, Saarma M, Kaila K (2004) Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J Neurosci 24: 4683-4691.
  • Shulga A, Blaesse A, Kysenius K, Huttunen HJ, Tanhuanpää K, Saarma M, Rivera C (2009) Thyroxin regulates BDNF expression to promote survival of injured neurons. Mol Cell Neurosci 42: 408-418.
  • Shulga A, Thomas-Crusells J, Sigl T, Blaesse A, Mestres P, Meyer M, Yan Q, Kaila K, Saarma M, Rivera C, Giehl KM (2008) Posttraumatic GABA(A)-mediated [Ca2+]i increase is essential for the induction of brain-derived neurotrophic factor-dependent survival of mature central neurons. J Neurosci 28: 6996-7005.
  • Tanaka T, Saito H, Matsuki N (1997) Inhibition of GABAA synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J Neurosci 17: 2959-2966.
  • Woo NS, Lu J, England R, McClellan R, Dufour S, Mount DB, Deutch AY, Lovinger DM, Delpire E (2002) Hyperexcitability and epilepsy associated with disruption of the mouse neuronal-specific K-Cl cotransporter gene. Hippocampus 12: 258-268.
  • Ziemlińska E, Kügler S, Schachner M, Wewiór I, Czarkowska-Bauch J, Skup M (2014) Overexpression of BDNF increases excitability of the lumbar spinal network and leads to robust early locomotor recovery in com¬pletely spinalized rats. PLoS One 9: e88833.
Typ dokumentu
Bibliografia
Identyfikatory
Identyfikator YADDA
bwmeta1.element.agro-0b1b2fba-d412-4109-9edc-c99db825de9a
JavaScript jest wyłączony w Twojej przeglądarce internetowej. Włącz go, a następnie odśwież stronę, aby móc w pełni z niej korzystać.