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

Acta Neurobiologiae Experimentalis

Volumn 74, Issue 3, 2014, Pages 276-287

  Eftekhari, Sanaz ^a,b   Mehrabi, Soraya ^b,e   Soleimani, Mansooreh ^b,c   Hassanzadeh, Gholamreza ^d,e   Shahrokhi, Amene ^e   Mostafavi, Hossein ^f   Hayat, Parisa ^b   Barati, Mahmood ^g   Mehdizadeh, Hajar ^e   Rahmanzadeh, Reza ^b   Hadjighassem, Mahmoud Reza ^e,h   Joghataei, Mohammad Taghi ^a,b,c  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d BIRJAND UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^e TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^f ZANJAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^g SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^h TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

BDNF; GABA; KCC2; NKCC1; Temporal lobe epilepsy

Indexed keywords

4 AMINOBUTYRIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; COTRANSPORTER; PILOCARPINE; POTASSIUM-CHLORIDE SYMPORTERS; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1;

ANIMAL; DISEASE MODEL; DRUG EFFECT; HIPPOCAMPUS; MALE; METABOLISM; NERVE CELL; TEMPORAL LOBE EPILEPSY; WISTAR RAT;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DISEASE MODELS, ANIMAL; EPILEPSY, TEMPORAL LOBE; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; MALE; NEURONS; PILOCARPINE; RATS, WISTAR; SOLUTE CARRIER FAMILY 12, MEMBER 2; SYMPORTERS;

EID: 84907188595     PISSN: 00651400     EISSN: 16890035     Source Type: Journal    
DOI: None     Document Type: Article

References (39)

1. 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 synaptogenesis and expression of the K+/Cl-co-transporter KCC2. Development 130: 1267-1280.
2. Ben-Ari Y (2002) Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3: 728-739.
3. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R (2007) GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87: 1215-1284.
4. 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 neurotransmission. J Neurosci 26: 10407-10419.
5. 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.
6. Brandt C, ozadze M, Heuchert N, Rattka M, Löscher 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.
7. Carmona MA, Pozas E, Martínez 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.
8. Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R (2002) On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298: 1418-1421.
9. Cohen I, Navarro V, Le Duigou C, Miles R (2003) Mesial temporal lobe epilepsy: a pathological replay of developmental mechanisms? Biol Cell 95: 329-333.
10. 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.
11. 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.
12. Engel J Jr (2001) Mesial temporal lobe epilepsy: what have we learned? Neuroscientist 7: 340-352.
13. 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 seizures. Hippocampus 13: 845-858.
14. 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.
15. 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.
16. 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 upregulating the expression of BDNF and GDNF. Neurosci Lett 487: 255-259.
17. 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 epilepsy. J Neurosci 27: 9866-9873.
18. Koyama R, Ikegaya Y (2005) To BDNF or not to BDNF: that is the epileptic hippocampus. Neuroscientist 11: 282-287.
19. 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 factor. Nature 341: 149-152.
20. 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.
21. 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 (α4, γ2 subunit), potassium chloride cotransporter 2 and astrogliosis in tremor rat hippocampus. Brain Res Bull 86: 373-379.
22. 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.
23. 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 excitation after in vivo axonal injury. J Neurosci 22: 4412-4417.
24. 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.
25. 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-transporters in the hippocampal subiculum from temporal lobe epilepsy patients make GABA excitatory. Proc Natl Acad Sci U S A 103: 8465-8468.
26. 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.
27. 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.
28. Payne JA, ivera C, Voipio J, Kaila K (2003) Cation-chloride co-transporters in neuronal communication, development and trauma.Trends Neurosci 26: 199-206.
29. Pellegrino LJ, Cushman AJ (1979) A Stereotaxic Atlas of the Rat Brain. Plenum Press, New York, NY.
30. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36.
31. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32: 281-294.
32. Rice AC, Floyd CL, Lyeth BG, Hamm RJ, DeLorenzo RJ (1998) Status epilepticus causes long-term NMDA receptor-dependent behavioral changes and cognitive deficits. Epilepsia 39: 1148-1157.
33. 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.
34. Rivera C, Voipio J, Thomas-Crusells J, Li H, Emri Z, Sipilä 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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 completely spinalized rats. PLoS One 9: e88833.