2018, Number 4
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Arch Neurocien 2018; 23 (4)
Microglia and neurodegeneration in the infant rat dorso-medial thalamic nucleus after status epilepticus
García-Martínez A, Quiroz-Vergara F, Véliz-Castillo I, Álvarez- Croda M, López-Meraz María-Leonor
Language: Spanish
References: 64
Page: 6-15
PDF size: 817.13 Kb.
ABSTRACT
Introduction: Status epilepticus (SE) produces extensive neuronal death in the developing brain.
Among the affected brain structures, neuronal degeneration is most prominent in the central and
lateral segments of the mediodorsal nucleus of the thalamus. On the other hand, microglia is a
specialized system of cellular immunity that is activated or over-expressed when there is damage
to brain tissue.
Aim: The goal of this study was to determine the extent and the time course of microglia activation
and neuronal injury in the mediodorsal thalamic nucleus after SE induced in fourteen-days-old
rat pups.
Method: SE was induced with the lithium-pilocarpine model. Presence of microglia with nonactivated
and activated morphology was determined in the mediodorsal thalamic nucleus by
immunohistochemical methods, in control conditions and 2, 6, 24 and 48 h following SE and
correlated to the appearance of neuronal injury detected by Fluoro-Jade C (F-JC) staining.
Results: Activated microglial and neuronal injury was detected in the mediodorsal thalamus 6-48
h following SE, while no changes in total microglia were observed.
Conclusion: These data demonstrate that in the mediodorsal thalamic nucleus, microglia is
activated in response to seizures and that this activation may contribute to SE-induced neuronal
injury in the immature brain.
REFERENCES
Fisher RS, van Emde Boas W, Blume W, Elger C, Genton P, Lee P, et al. Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia 2005; 46(4):470-2.
Trinka E, Cock H, Hesdorffer D, Rossetti AO, Scheffer IE, Shinnar S, et al. A definition and classification of status epilepticus-Report of the ILAE Task Force on Classification of Status Epilepticus. Epilepsia 2015; 56(10):1515-23.
DeLorenzo RJ, Pellock JM, Towne AR, Boggs JG. Epidemiology of status epilepticus. J Clin Neurophysiol 1995; 12(4):316-25.
DeLorenzo, Hauser WA, Towne AR, Boggs JG, Pellock JM, Penberthy L, Garnett L, et al. A prospective, population-based epidemiologic study of status epilepticus in Richmond, Virginia. Neurol 1996; 46:1029-35.
Hauser, W. The prevalence and incidence of convulsive disorders in children. Epilepsia 1994; 35 Suppl2: S1–6.
Sankar R, Shin DH, Liu H, Mazarati A, Pereira de Vasconcelos A, Wasterlain CG. Patterns of status epilepticus-induced neuronal injury during development and long-term consequences. J Neurosci 1998; 18(20):8382-93.
Kubová H, Druga R, Lukasiuk K, Suchomelova L, Haugvicova R, Jirmanova I, et al. Status epilepticus causes necrotic damage in the mediodorsal nucleus of the thalamus in immature rats. J Neurosci 2001; 21(10):3593–9.
Nairismägi J, Pitkänen A, Kettunen MI, Kauppinen RA, Kubova H. Status epilepticus in 12-day-old rats leads to temporal lobe neurodegeneration and volume reduction: a histologic and MRI study. Epilepsia 2006; 47(3): 479-88.
López-Meraz ML, Wasterlain CG, Rocha LL, Allen S, Niquet J. Vulnerability of postnatal hippocampal neurons to seizures varies regionally with their maturational stage. Neurobiol Dis 2010; 37(2): 394-402.
Nakajima M, Halassa MM. Thalamic control of functional cortical connectivity. Curr Opin Neurobiol 2017; 44:127-31.
Hanisch UK, KettenmannH. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007; 10(11):1387–94.
Vezzani A, Ravizza T, Balosso S, Aronica E. Glia as a source of cytokines: Implications for neuronal excitability and survival. Epilepsia 2008; 49 Suppl 2:24–32.
Vezzani A , C onti M , D e L uigi A , R avizza T, M oneta D , M archesi F, e t a l. I nterleukin- 1beta i mmunoreactivity a nd microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures. J Neurosci 1999; 19(12): 5054-65.
Wang N, Mi X, Gao B, Gu J, Wang W, Zhang Y, et al. Minocycline inhibits brain inflammation and attenuates spontaneous recurrent seizures following pilocarpine-induced status epilepticus. Neuroscience 2015; 287:144–56.
Haas KZ, Sperber EF, Moshe SL. Kindling in developing animals: expression of severe seizures and enhanced development of bilateral foci. Brain Res Dev Brain Res 1990; 56(2): 275-80.
Sherwood NM, Timiras PS. A stereotaxic atlas of the developing rat brain. Berkeley-Los Angeles-London, University of California Press, 1970.
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biologicalimage analysis. Nat Methods 2012; 9 (7):676-82.
Jonas RA, Yuan TF, Liang YX, Jonas JB, Tay DK, Ellis-Behnke RG. The spider effect: morphological and orienting classification of microglia in response to stimuli in vivo. PLoS One 2012; 7(2) p.e30763.
Avignone E, Ulmann L, Levavasseur F, Rassendren F, Audinat E. Status epilepticus induces a particular microglial activation state characterized by enhanced purinergic signaling. J Neurosci 2008; 28 (37): 9133-44.
De Simoni MG, Perego C, Ravizza T, Moneta D, Conti M, Marchesi F, et al. Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus. Eur J Neurosci 2000; 12(7): 2623–33.
Ravizza T, Rizzi M, Perego C. Inflammatory response and glia activation in developing rat hippocampus after status epilepticus. Epilepsia 2005; 46 Suppl 5:113-7.
Eyo U, Peng J, Swiatkowski P, Mukherjee A, Bispo A, Wu LJ. Neuronal hyperactivity recruits microglial processes via neuronal NMDA receptors and microglial P2Y12 receptors after status epilepticus. J Neurosci 2014; 34(32):10528-40.
Ouhaz Z, Ba-M'hamed S, Bennis M. Morphological, structural, and functional alterations of the prefrontal cortex and the basolateral amygdala after early lesion of the rat mediodorsal thalamus. Brain Struct Fun 2017; 222(6): 2527-45.
Rizzi M, Perego C, Aliprandi M, Richichi C, Ravizza T, Colella D, et al. Glia activation and cytokine increase in rat hippocampus by kainic acid-induced status epilepticus during postnatal development. Neurobiol Dis 2003; 14(3): 494-503.
Järvelä JT, Lopez-Picon FR, Plysjuk A, Ruohonen S, Holopainen IE. Temporal profiles of age-dependent changes in cytokine mRNA expression and glial cell activation after status epilepticus in postnatal rat hippocampus. J Neuroinflammation 2011; 8:29.
Kaur C, Rathnasamy G, Ling EA. Biology of microglia in the developing brain. J Neuropathol Exp Neurol. 2017; 76(9):736-43.
Álvarez-Croda DM, Santiago-García J, Medel-Matus JS, Martínez-Quiroz J, Puig-Lagunes AA, Beltrán-Parrazal L, et al. Hippocampal distribution of IL-1β and IL-1RI following lithium-pilocarpine-induced status epilepticus in the developing rat. An Acad Bras Cienc 2016; 88 Suppl 1:653-63.
Medel-Matus JS, Álvarez-Croda DM, Martínez-Quiroz J, Beltrán-Parrazal L, Morgado-Valle C, López-Meraz MC. IL-1β increases necrotic neuronal cell death in the developing rat hippocampus after status epilepticus by activating type 1 IL-1 receptor (IL-1RI). Int J Dev Neurosci 2014; 238: 232-40.
Merrill JE, Benveniste EN. Cytokines in inflammatory brain lesions: helpful and harmful. Trends Neurosci 1996; 19(8):331–8.
Denker SP, Ji S, Dingman A, Lee SY, Derugin N, Wendland MF, et al. Macrophages are comprised of resident brain microglia not infiltrating peripheral monocytes acutely after neonatal stroke. J Neurochem 2007; 100(4): 893-904.
Ravizza T, Gagliardi B, Noé F, Boer K, Aronica E, Vezzani A. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis 2008; 29(1):142-60.
Fabene PF, Navarro MG, Martinello M, Rossi B, Merigo F, Ottoboni L, et al. A role for leukocyte-endothelial adhesion mechanisms in epilepsy. Nat Med. 2008; 14(12):1377-83.
Fisher RS, van Emde Boas W, Blume W, Elger C, Genton P, Lee P, et al. Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia 2005; 46(4):470-2.
Trinka E, Cock H, Hesdorffer D, Rossetti AO, Scheffer IE, Shinnar S, et al. A definition and classification of status epilepticus-Report of the ILAE Task Force on Classification of Status Epilepticus. Epilepsia 2015; 56(10):1515-23.
DeLorenzo RJ, Pellock JM, Towne AR, Boggs JG. Epidemiology of status epilepticus. J Clin Neurophysiol 1995; 12(4):316-25.
DeLorenzo, Hauser WA, Towne AR, Boggs JG, Pellock JM, Penberthy L, Garnett L, et al. A prospective, population-based epidemiologic study of status epilepticus in Richmond, Virginia. Neurol 1996; 46:1029-35.
Hauser, W. The prevalence and incidence of convulsive disorders in children. Epilepsia 1994; 35 Suppl2: S1–6.
Sankar R, Shin DH, Liu H, Mazarati A, Pereira de Vasconcelos A, Wasterlain CG. Patterns of status epilepticus-induced neuronal injury during development and long-term consequences. J Neurosci 1998; 18(20):8382-93.
Kubová H, Druga R, Lukasiuk K, Suchomelova L, Haugvicova R, Jirmanova I, et al. Status epilepticus causes necrotic damage in the mediodorsal nucleus of the thalamus in immature rats. J Neurosci 2001; 21(10):3593–9.
Nairismägi J, Pitkänen A, Kettunen MI, Kauppinen RA, Kubova H. Status epilepticus in 12-day-old rats leads to temporal lobe neurodegeneration and volume reduction: a histologic and MRI study. Epilepsia 2006; 47(3): 479-88.
López-Meraz ML, Wasterlain CG, Rocha LL, Allen S, Niquet J. Vulnerability of postnatal hippocampal neurons to seizures varies regionally with their maturational stage. Neurobiol Dis 2010; 37(2): 394-402.
Nakajima M, Halassa MM. Thalamic control of functional cortical connectivity. Curr Opin Neurobiol 2017; 44:127-31.
Hanisch UK, KettenmannH. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007; 10(11):1387–94.
Vezzani A, Ravizza T, Balosso S, Aronica E. Glia as a source of cytokines: Implications for neuronal excitability and survival. Epilepsia 2008; 49 Suppl 2:24–32.
Vezzani A , C onti M , D e L uigi A , R avizza T, M oneta D , M archesi F, e t a l. I nterleukin- 1beta i mmunoreactivity a nd microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures. J Neurosci 1999; 19(12): 5054-65.
Wang N, Mi X, Gao B, Gu J, Wang W, Zhang Y, et al. Minocycline inhibits brain inflammation and attenuates spontaneous recurrent seizures following pilocarpine-induced status epilepticus. Neuroscience 2015; 287:144–56.
Haas KZ, Sperber EF, Moshe SL. Kindling in developing animals: expression of severe seizures and enhanced development of bilateral foci. Brain Res Dev Brain Res 1990; 56(2): 275-80.
Sherwood NM, Timiras PS. A stereotaxic atlas of the developing rat brain. Berkeley-Los Angeles-London, University of California Press, 1970.
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biologicalimage analysis. Nat Methods 2012; 9 (7):676-82.
Jonas RA, Yuan TF, Liang YX, Jonas JB, Tay DK, Ellis-Behnke RG. The spider effect: morphological and orienting classification of microglia in response to stimuli in vivo. PLoS One 2012; 7(2) p.e30763.
Avignone E, Ulmann L, Levavasseur F, Rassendren F, Audinat E. Status epilepticus induces a particular microglial activation state characterized by enhanced purinergic signaling. J Neurosci 2008; 28 (37): 9133-44.
De Simoni MG, Perego C, Ravizza T, Moneta D, Conti M, Marchesi F, et al. Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus. Eur J Neurosci 2000; 12(7): 2623–33.
Ravizza T, Rizzi M, Perego C. Inflammatory response and glia activation in developing rat hippocampus after status epilepticus. Epilepsia 2005; 46 Suppl 5:113-7.
Eyo U, Peng J, Swiatkowski P, Mukherjee A, Bispo A, Wu LJ. Neuronal hyperactivity recruits microglial processes via neuronal NMDA receptors and microglial P2Y12 receptors after status epilepticus. J Neurosci 2014; 34(32):10528-40.
Ouhaz Z, Ba-M'hamed S, Bennis M. Morphological, structural, and functional alterations of the prefrontal cortex and the basolateral amygdala after early lesion of the rat mediodorsal thalamus. Brain Struct Fun 2017; 222(6): 2527-45.
Rizzi M, Perego C, Aliprandi M, Richichi C, Ravizza T, Colella D, et al. Glia activation and cytokine increase in rat hippocampus by kainic acid-induced status epilepticus during postnatal development. Neurobiol Dis 2003; 14(3): 494-503.
Järvelä JT, Lopez-Picon FR, Plysjuk A, Ruohonen S, Holopainen IE. Temporal profiles of age-dependent changes in cytokine mRNA expression and glial cell activation after status epilepticus in postnatal rat hippocampus. J Neuroinflammation 2011; 8:29.
Kaur C, Rathnasamy G, Ling EA. Biology of microglia in the developing brain. J Neuropathol Exp Neurol. 2017; 76(9):736-43.
Álvarez-Croda DM, Santiago-García J, Medel-Matus JS, Martínez-Quiroz J, Puig-Lagunes AA, Beltrán-Parrazal L, et al. Hippocampal distribution of IL-1β and IL-1RI following lithium-pilocarpine-induced status epilepticus in the developing rat. An Acad Bras Cienc 2016; 88 Suppl 1:653-63.
Medel-Matus JS, Álvarez-Croda DM, Martínez-Quiroz J, Beltrán-Parrazal L, Morgado-Valle C, López-Meraz MC. IL-1β increases necrotic neuronal cell death in the developing rat hippocampus after status epilepticus by activating type 1 IL-1 receptor (IL-1RI). Int J Dev Neurosci 2014; 238: 232-40.
Merrill JE, Benveniste EN. Cytokines in inflammatory brain lesions: helpful and harmful. Trends Neurosci 1996; 19(8):331–8.
Denker SP, Ji S, Dingman A, Lee SY, Derugin N, Wendland MF, et al. Macrophages are comprised of resident brain microglia not infiltrating peripheral monocytes acutely after neonatal stroke. J Neurochem 2007; 100(4): 893-904.
Ravizza T, Gagliardi B, Noé F, Boer K, Aronica E, Vezzani A. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis 2008; 29(1):142-60.
Fabene PF, Navarro MG, Martinello M, Rossi B, Merigo F, Ottoboni L, et al. A role for leukocyte-endothelial adhesion mechanisms in epilepsy. Nat Med. 2008; 14(12):1377-83.