Dysregulation of GABAergic System in the Inferior Colliculi of Rats during the Development of Audiogenic Epilepsy

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Resumo

Epilepsy is tightly associated with dysfunction of inhibitory GABA neurotransmission. In this study, Krushinsky–Molodkina (KM) rats genetically prone to audiogenic seizures (AGS) were used. KM rats are characterized by the development of audiogenic epilepsy during postnatal ontogenesis, with AGS onset at the age of 1.5–2 months and fully developed AGS expression by 3rd month. We analyzed GABAergic system of the inferior colliculi (IC) of KM rats at different stages of postnatal development. Wistar rats were used as a control. In the IC of young KM rats, Na+/K+/Cl– cotransporter 1 (NKCC1) expression was increased, while K+/Cl– cotransporter 2 (KCC2) was unchanged indicating impairment of postsynaptic GABA action at early stages of postnatal development. Moreover, we revealed also an increase in the expression of vesicular GABA transporter (VGAT) in the IC which additionally pointed on the higher activity of GABA release. In adult rats, in opposite, we revealed a decrease in the expression of KCC2 transporter indicating downregulation of GABA inhibition on the target cells. Thus, GABA dysregulation in the IC can mediate the seizure susceptibility in adult KM rats.

Sobre autores

S. Nikolaeva

Sechenov Institute of Evolutionary Physiology and Biochemistry, the Russian Academy of Sciences

Email: mglazova@iephb.ru
Russia, St. Petersburg

A. Ivlev

Sechenov Institute of Evolutionary Physiology and Biochemistry, the Russian Academy of Sciences

Email: mglazova@iephb.ru
Russia, St. Petersburg

A. Naumova

Sechenov Institute of Evolutionary Physiology and Biochemistry, the Russian Academy of Sciences

Email: mglazova@iephb.ru
Russia, St. Petersburg

A. Kulikov

Sechenov Institute of Evolutionary Physiology and Biochemistry, the Russian Academy of Sciences

Email: mglazova@iephb.ru
Russia, St. Petersburg

M. Glazova

Sechenov Institute of Evolutionary Physiology and Biochemistry, the Russian Academy of Sciences

Autor responsável pela correspondência
Email: mglazova@iephb.ru
Russia, St. Petersburg

E. Chernigovskaya

Sechenov Institute of Evolutionary Physiology and Biochemistry, the Russian Academy of Sciences

Email: mglazova@iephb.ru
Russia, St. Petersburg

Bibliografia

  1. Blauwblomme T, Dossi E, Pellegrino C, Goubert E, Iglesias BG, Sainte-Rose C, Rouach N, Nabbout R, Huberfeld G (2019) Gamma-aminobutyric acidergic transmission underlies interictal epileptogenicity in pediatric focal cortical dysplasia. Ann Neurol 85: 204–217. https://doi.org/10.1002/ana.25403
  2. Wang Y, Wang Y, Chen Z (2018) Double-edged GABAergic synaptic transmission in seizures: The importance of chloride plasticity. Brain Res 1701: 126–136. https://doi.org/10.1016/j.brainres.2018.09.008
  3. Houser CR (2014) Do structural changes in GABA neurons give rise to the epileptic state? Adv Exp Med Biol 813: 151–160. https://doi.org/10.1007/978-94-017-8914-1_12
  4. Goodkin HP, Yeh JL, Kapur J (2005) Status epilepticus increases the intracellular accumulation of GABAA receptors. J Neurosci 25: 5511–5520. https://doi.org/10.1523/JNEUROSCI.0900-05.2005
  5. Scharfman HE, Brooks-Kayal AR (2014) Is plasticity of GABAergic mechanisms relevant to epileptogenesis? Adv Exp Med Biol 813: 133–150. https://doi.org/10.1007/978-94-017-8914-1_11
  6. Liu R, Wang J, Liang S, Zhang G, Yang X (2019) Role of NKCC1 and KCC2 in Epilepsy: From Expression to Function. Front Neurol 10: 1407. https://doi.org/10.3389/fneur.2019.01407
  7. 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. https://doi.org/10.1073/pnas.0602979103
  8. Vinogradova LV (2017) Audiogenic kindling and secondary subcortico-cortical epileptogenesis: Behavioral correlates and electrographic features. Epilepsy Behav 71: 142–153. https://doi.org/10.1016/j.yebeh.2015.06.014
  9. Faingold CL (1999) Neuronal networks in the genetically epilepsy-prone rat. Adv Neurol 79: 311–321.
  10. Ribak CE (2017) An abnormal GABAergic system in the inferior colliculus provides a basis for audiogenic seizures in genetically epilepsy-prone rats. Epilepsy Behav 71: 160–164. https://doi.org/10.1016/j.yebeh.2015.02.024
  11. Ribak CE, Morin CL (1995) The role of the inferior colliculus in a genetic model of audiogenic seizures. Anat Embryol (Berl) 191: 279–295. https://doi.org/10.1007/BF00534681
  12. Lasley SM (1991) Roles of neurotransmitter amino acids in seizure severity and experience in the genetically epilepsy-prone rat. Brain Res 560: 63–70.
  13. Simler S, Ciesielski L, Clement J, Rastegar A, Mandel P (1992) Involvement of synaptosomal neurotransmitter amino acids in audiogenic seizure-susceptibility and -severity of Rb mice. Neurochem Res 17: 953–959. https://doi.org/10.1007/BF00993272
  14. Fuentes-Santamaria V, Alvarado JC, Herranz AS, Garcia-Atares N, Lopez DE (2008) Decreased levels of GABA in the inferior colliculus of the epilepsy-prone hamster (GPG/Vall). Epilepsy Res 79: 224–227. https://doi.org/10.1016/j.eplepsyres.2008.02.003
  15. Prieto-Martin AI, Aroca-Aguilar JD, Sanchez-Sanchez F, Munoz LJ, Lopez DE, Escribano J, de Cabo C (2017) Molecular and neurochemical substrates of the audiogenic seizure strains: The GASH:Sal model. Epilepsy Behav 71: 218–225. https://doi.org/10.1016/j.yebeh.2015.05.025
  16. Lohmann C, Friauf E (1996) Distribution of the calcium-binding proteins parvalbumin and calretinin in the auditory brainstem of adult and developing rats. J Comp Neurol 367: 90–109. https://doi.org/10.1002/(SICI)1096-9861(19960325)367:1<90::AID-CNE7>3.0.CO;2-E
  17. Achilles K, Okabe A, Ikeda M, Shimizu-Okabe C, Yamada J, Fukuda A, Luhmann HJ, Kilb W (2007) Kinetic properties of Cl uptake mediated by Na+-dependent K+-2Cl cotransport in immature rat neocortical neurons. J Neurosci 27: 8616–8627. https://doi.org/10.1523/JNEUROSCI.5041-06.2007
  18. Valeeva G, Valiullina F, Khazipov R (2013) Excitatory actions of GABA in the intact neonatal rodent hippocampus in vitro. Front Cell Neurosci 7: 20. https://doi.org/10.3389/fncel.2013.00020
  19. Федотова ИБ, Семиохина АФ (2002) Аудиогенная эпилепсия и миоклонус в онтогенезе крыс КМ. Журн высш нерв деят 52(2): 261–265. [Fedotova IB, Semiokhina AF (2002) Developmental changes in audiogenic epilepsy and myoclonus in KM rats. Zh Vyssh Nerv Deiat Im I P Pavlova 52(2): 261–265. (In Russ)].
  20. Chernigovskaya EV, Dorofeeva NA, Nasluzova EV, Kulikov AA, Ovsyannikova VV, Glazova MV (2018) Apoptosis and proliferation in the inferior colliculus during postnatal development and epileptogenesis in audiogenic Krushinsky-Molodkina rats. Epilepsy Behav 88: 227–234. https://doi.org/10.1016/j.yebeh.2018.09.023
  21. Chernigovskaya EV, Dorofeeva NA, Lebedenko OO, Nikolaeva SD, Naumova AA, Lavrova EA, Glazova MV (2019) Neurochemical Organization of the Inferior Colliculus in Audiogenic Krushinsky-Molodkina Rats During Development of Seizure Susceptibility. Russ J Physiol 105: 724–741. https://doi.org/10.1134/S0869813919060013
  22. Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH, Storm-Mathisen J (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18: 9733–9750. https://doi.org/10.1523/JNEUROSCI.18-23-09733.1998
  23. Olsen RW, Sieghart W (2009) GABA A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology 56: 141–148. https://doi.org/10.1016/j.neuropharm.2008.07.045
  24. Geal-Dor M, Freeman S, Li G, Sohmer H (1993) Development of hearing in neonatal rats: air and bone conducted ABR thresholds. Hear Res 69: 236–242. https://doi.org/10.1016/0378-5955(93)90113-f
  25. Chernigovskaya EV, Korotkov AA, Dorofeeva NA, Gorbacheva EL, Kulikov AA, Glazova MV (2019) Delayed audiogenic seizure development in a genetic rat model is associated with overactivation of ERK1/2 and disturbances in glutamatergic signaling. Epilepsy Behav 99: 106494. https://doi.org/10.1016/j.yebeh.2019.106494
  26. Leidenheimer NJ (2008) Regulation of excitation by GABA(A) receptor internalization. Results Probl Cell Differ 44: 1–28. https://doi.org/10.1007/400_2007_039
  27. Barnes EM Jr (1996) Use-dependent regulation of GABAA receptors. Int Rev Neurobiol 39: 53–76. https://doi.org/10.1016/s0074-7742(08)60663-7
  28. 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. https://doi.org/10.1523/JNEUROSCI.3257-06.2006
  29. Lu J, Karadsheh M, Delpire E (1999) Developmental regulation of the neuronal-specific isoform of K-Cl cotransporter KCC2 in postnatal rat brains. J Neurobiol 39: 558–568.
  30. Kanaka C, Ohno K, Okabe A, Kuriyama K, Itoh T, Fukuda A, Sato K (2001) The differential expression patterns of messenger RNAs encoding K-Cl cotransporters (KCC1,2) and Na-K-2Cl cotransporter (NKCC1) in the rat nervous system. Neuroscience 104: 933–946. https://doi.org/10.1016/s0306-4522(01)00149-x
  31. Wang C, Shimizu-Okabe C, Watanabe K, Okabe A, Matsuzaki H, Ogawa T, Mori N, Fukuda A, Sato K (2002) Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Brain Res Dev Brain Res 139: 59–66. https://doi.org/10.1016/s0165-3806(02)00536-9
  32. Solius GM, Revishchin AV, Pavlova GV, Poletaeva II (2016) Audiogenic epilepsy and GABAergic system of the colliculus inferior in Krushinsry-Molodkina rats Dokl Biochem Biophys 466: 32–34.https://doi.org/10.1134/S1607672916010099

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Declaração de direitos autorais © С.Д. Николаева, А.П. Ивлев, А.А. Наумова, А.А. Куликов, М.В. Глазова, Е.В. Черниговская, 2023

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