Status epilepticus alters neurogenesis and decreases the number of GABAergic neurons in the septal dentate gyrus of 9-day-old rats at the early phase of epileptogenesis

Brain Research

Volumn 1516, Issue , 2013, Pages 33-44

  Lauren H B ^a,b   Ruohonen, S ^a   Kukko Lukjanov, T K ^a,c   Virta, J E ^a   Gronman M ^a   Lopez Picon, F R ^a,d   Jarvela J T ^a   Holopainen, I E ^a,b,e  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d TURKU PET CENTRE   (Finland)

^e TURKU UNIVERSITY HOSPITAL   (Finland)

Author keywords

Dentate gyrus; Developing brain; GABAA receptor; Hippocampus; Neurogenesis; Status epilepticus

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID RECEPTOR; ANTIBODY; BROXURIDINE; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE DECARBOXYLASE 67; KAINIC ACID; MESSENGER RNA; NESTIN; PARVALBUMIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; EPILEPTIC STATE; EPILEPTOGENESIS; GLIA CELL; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE DOUBLE LABELING; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; ANIMALS, NEWBORN; BROMODEOXYURIDINE; CELL COUNT; DENTATE GYRUS; DISEASE MODELS, ANIMAL; EPILEPSY; EXCITATORY AMINO ACID AGONISTS; GABAERGIC NEURONS; GENE EXPRESSION REGULATION; GLUTAMATE DECARBOXYLASE; KAINIC ACID; NERVE TISSUE PROTEINS; NEUROGENESIS; PARVALBUMINS; RATS; RECEPTORS, GABA-A;

RATTUS;

EID: 84878611341     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.04.028     Document Type: Article

References (70)

1. J. Altman, and S.A. Bayer Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods J. Comp. Neurol. 301 1990 365 381
2. Y. Ben-Ari Excitatory actions of gaba during development: the nature of the nurture Nat. Rev. Neurosci. 3 2002 728 739
3. Y. Ben-Ari, and G.L. Holmes Effects of seizures on developmental processes in the immature brain Lancet Neurol. 5 2006 1055 1063
4. R.A. Bender, C. Dube, R. Gonzalez-Vega, E.W. Mina, and T.Z. Baram Mossy fiber plasticity and enhanced hippocampal excitability, without hippocampal cell loss or altered neurogenesis, in an animal model of prolonged febrile seizures Hippocampus 13 2003 399 412
5. J. Bengzon, Z. Kokaia, E. Elmer, A. Nanobashvili, M. Kokaia, and O. Lindvall Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures Proc. Natl. Acad. Sci. U. S. A. 94 1997 10432 10437
6. I. Blümcke, J.C. Schewe, S. Normann, O. Brustle, J. Schramm, C.E. Elger, and O.D. Wiestler Increase of nestin-immunoreactive neural precursor cells in the dentate gyrus of pediatric patients with early onset temporal lobe epilepsy Hippocampus 11 2001 311 321
7. A receptor expression in a mouse model of mesial temporal lobe epilepsy Hippocampus 10 2000 305 324
8. M.D. Brandt, S. Jessberger, B. Steiner, G. Kronenberg, K. Reuter, A. Bick-Sander, W. von der Behrens, and G. Kempermann Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice Mol. Cell. Neurosci. 24 2003 603 613
9. P.S. Buckmaster, and F.E. Dudek Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats J. Comp. Neurol. 385 1997 385 404
10. J.E. Cheyne, L. Grant, C. Butler-Munro, J.W. Foote, B. Connor, and J.M. Montgomery Synaptic integration of newly generated neurons in rat dissociated hippocampal cultures Mol. Cell. Neurosci. 47 2011 203 214
11. S. Couillard-Despres, B. Winner, S. Schaubeck, R. Aigner, M. Vroemen, N. Weidner, U. Bogdahn, J. Winkler, H.G. Kuhn, and L. Aigner Doublecortin expression levels in adult brain reflect neurogenesis Eur. J. Neurosci. 21 2005 1 14
12. S.C. Danzer, X. He, A.W. Loepke, and J.O. McNamara Structural plasticity of dentate granule cell mossy fibers during the development of limbic epilepsy Hippocampus 20 2010 113 124
13. A.G. Dayer, A.A. Ford, K.M. Cleaver, M. Yassaee, and H.A. Cameron Short-term and long-term survival of new neurons in the rat dentate gyrus J. Comp. Neurol. 460 2003 563 572
14. J.A. del Rio, and E. Soriano Immunocytochemical detection of 5′-bromodeoxyuridine incorporation in the central nervous system of the mouse Brain Res. Dev. Brain Res 49 1989 311 317
15. H. Dong, C.A. Csernansky, B. Goico, and J.G. Csernansky Hippocampal neurogenesis follows kainic acid-induced apoptosis in neonatal rats J. Neurosci. 23 2003 1742 1749
16. A receptor-mediated regulation of adult hippocampal neurogenesis Eur. J. Neurosci. 34 2011 362 373
17. V. Filippov, G. Kronenberg, T. Pivneva, K. Reuter, B. Steiner, L.P. Wang, M. Yamaguchi, H. Kettenmann, and G. Kempermann Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes Mol. Cell. Neurosci. 23 2003 373 382
18. T.F. Freund, and G. Buzsaki Interneurons of the hippocampus Hippocampus 6 1996 347 470
19. A receptor subtypes during postnatal development: an immunohistochemical study J. Neurosci. 14 1994 5302 5324
20. A receptors containing the alpha 1 subunit to neurochemically distinct subpopulations of rat hippocampal interneurons Eur. J. Neurosci 6 1994 837 853
21. S. Ge, E.L. Goh, K.A. Sailor, Y. Kitabatake, G.L. Ming, and H. Song GABA regulates synaptic integration of newly generated neurons in the adult brain Nature 439 2006 589 593
22. J.G. Gleeson, P.T. Lin, L.A. Flanagan, and C.A. Walsh Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons Neuron 23 1999 257 271
23. W.P. Gray, and L.E. Sundström Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat Brain Res. 790 1998 52 59
24. K.Z. Haas, E.F. Sperber, L.A. Opanashuk, P.K. Stanton, and S.L. Moshe Resistance of immature hippocampus to morphologic and physiologic alterations following status epilepticus or kindling Hippocampus 11 2001 615 625
25. H. Hagihara, K. Toyama, N. Yamasaki, and T. Miyakawa Dissection of hippocampal dentate gyrus from adult mouse J. Vis. Exp. 33 2009 153
26. J. Hellsten, M.J. West, A. Arvidsson, J. Ekstrand, L. Jansson, M. Wennström, and A. Tingström Electroconvulsive seizures induce angiogenesis in adult rat hippocampus Biol. Psychiatr. 58 2005 871 878
27. G.L. Holmes, J.L. Gairsa, N. Chevassus-Au-Louis, and Y. Ben-Ari Consequences of neonatal seizures in the rat: morphological and behavioral effects Ann. Neurol. 44 1998 845 857
28. I.E. Holopainen Seizures in the developing brain: cellular and molecular mechanisms of neuronal damage, neurogenesis and cellular reorganization Neurochem. Int. 52 2008 935 947
29. C.L. Indulekha, R. Sanalkumar, A. Thekkuveettil, and J. James Seizure induces activation of multiple subtypes of neural progenitors and growth factors in hippocampus with neuronal maturation confined to dentate gyrus Biochem. Biophys. Res. Commun. 393 2010 864 871
30. S. Jessberger, C. Zhao, N. Toni, G.D. Clemenson Jr.; Y. Li, and F.H. Gage Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling J. Neurosci. 27 2007 9400 9407
31. J.T. Järvelä, F.R. Lopez-Picon, A. Plysjuk, S. Ruohonen, and I.E. Holopainen Temporal profiles of age-dependent changes in cytokine mRNA expression and glial cell activation after status epilepticus in postnatal rat hippocampus J. Neuroinflamm. 8 2011 29
32. G. Kempermann, S. Jessberger, B. Steiner, and G. Kronenberg Milestones of neuronal development in the adult hippocampus Trends Neurosci. 27 2004 447 452
33. J.E. Kim, S.E. Kwak, D.S. Kim, M.H. Won, O.S. Kwon, S.Y. Choi, and T.C. Kang Reduced calcium binding protein immunoreactivity induced by electroconvulsive shock indicates neuronal hyperactivity, not neuronal death or deactivation Neuroscience 137 2006 317 326
34. M. Kobayashi, and P.S. Buckmaster Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy J. Neurosci. 23 2003 2440 2452
35. J.E. Kralic, D.A. Ledergerber, and J.M. Fritschy Disruption of the neurogenic potential of the dentate gyrus in a mouse model of temporal lobe epilepsy with focal seizures Eur. J. Neurosci. 22 2005 1916 1927
36. H.B. Laurén, F.R. Lopez-Picon, A.M. Brandt, C.J. Rios-Rojas, and I.E. Holopainen Transcriptome analysis of the hippocampal CA1 pyramidal cell region after kainic acid-induced status epilepticus in juvenile rats PLoS One 5 2010 e10733
37. A receptor subunit mRNA and protein expression in the developing rat hippocampus J. Neurochem. 94 2005 1384 1394
38. 3H]flunitrazepam binding in the developing rat brain Neuroscience 146 2007 802 811
39. A receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development J. Neurosci. 12 1992 4151 4172
40. U. Lendahl, L.B. Zimmerman, and R.D. McKay CNS stem cells express a new class of intermediate filament protein Cell 60 1990 585 595
41. H. Liu, J. Kaur, K. Dashtipour, R. Kinyamu, C.E. Ribak, and L.K. Friedman Suppression of hippocampal neurogenesis is associated with developmental stage, number of perinatal seizure episodes, and glucocorticosteroid level Exp. Neurol. 184 2003 196 213
42. F. Lopez-Picon, N. Puustinen, T.K. Kukko-Lukjanov, and I.E. Holopainen Resistance of neurofilaments to degradation, and lack of neuronal death and mossy fiber sprouting after kainic acid-induced status epilepticus in the developing rat hippocampus Neurobiol. Dis. 17 2004 415 426
43. J.J. LoTurco, D.F. Owens, M.J. Heath, M.B. Davis, and A.R. Kriegstein GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis Neuron 15 1995 1287 1298
44. J. Marcon, B. Gagliardi, S. Balosso, M. Maroso, F. Noe, M. Morin, M. Lerner-Natoli, A. Vezzani, and T. Ravizza Age-dependent vascular changes induced by status epilepticus in rat forebrain: implications for epileptogenesis Neurobiol. Dis. 34 2009 121 132
45. S. Marty, R. Wehrle, and C. Sotelo Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus J. Neurosci. 20 2000 8087 8095
46. G.W. Mathern, P.D. Adelson, L.D. Cahan, and J.P. Leite Hippocampal neuron damage in human epilepsy: Meyer's hypothesis revisited Prog. Brain Res. 135 2002 237 251
47. E.A. Mathews, N.A. Morgenstern, V.C. Piatti, C. Zhao, S. Jessberger, A.F. Schinder, and F.H. Gage A distinctive layering pattern of mouse dentate granule cells is generated by developmental and adult neurogenesis J. Comp. Neurol. 518 2010 4479 4490
48. B.K. McCabe, D.C. Silveira, M.R. Cilio, B.H. Cha, X. Liu, Y. Sogawa, and G.L. Holmes Reduced neurogenesis after neonatal seizures J. Neurosci. 21 2001 2094 2103
49. T. Namba, H. Mochizuki, M. Onodera, Y. Mizuno, H. Namiki, and T. Seki The fate of neural progenitor cells expressing astrocytic and radial glial markers in the postnatal rat dentate gyrus Eur. J. Neurosci. 22 2005 1928 1941
50. R.S. Nowakowski, S.B. Lewin, and M.W. Miller Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population J. Neurocytol. 18 1989 311 318
51. D.S. Packard Jr.; R.A. Menzies, and R.G. Skalko Incorporation of thymidine and its analogue, bromodeoxyuridine, into embryos and maternal tissues of the mouse Differentiation 1 1973 397 404
52. T.D. Palmer, A.R. Willhoite, and F.H. Gage Vascular niche for adult hippocampal neurogenesis J. Comp. Neurol. 425 2000 479 494
53. J.M. Parent, R.C. Elliott, S.J. Pleasure, N.M. Barbaro, and D.H. Lowenstein Aberrant seizure-induced neurogenesis in experimental temporal lobe epilepsy Ann. Neurol. 59 2006 81 91
54. J.M. Parent, T.W. Yu, R.T. Leibowitz, D.H. Geschwind, R.S. Sloviter, and D.H. Lowenstein Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus J. Neurosci. 17 1997 3727 3738
55. J.P. Pierce, J. Melton, M. Punsoni, D.P. McCloskey, and H.E. Scharfman Mossy fibers are the primary source of afferent input to ectopic granule cells that are born after pilocarpine-induced seizures Exp. Neurol. 196 2005 316 331
56. B.E. Porter, M. Maronski, and A.R. Brooks-Kayal Fate of newborn dentate granule cells after early life status epilepticus Epilepsia 45 2004 13 19
57. C.E. Ribak, P.H. Tran, I. Spigelman, M.M. Okazaki, and J.V. Nadler Status epilepticus-induced hilar basal dendrites on rodent granule cells contribute to recurrent excitatory circuitry J. Comp. Neurol. 428 2000 240 253
58. M. Rizzi, C. Perego, M. Aliprandi, C. Richichi, T. Ravizza, D. Colella, J. Veliskova, S.L. Moshe, M.G. De Simoni, and A. Vezzani Glia activation and cytokine increase in rat hippocampus by kainic acid-induced status epilepticus during postnatal development Neurobiol. Dis. 14 2003 494 503
59. A. Saghyan, G.N. LaTorre, R. Keesey, A. Sharma, V. Mehta, V. Rudenko, B.H. Hallas, A. Rafiuddin, B. Goldstein, and L.K. Friedman Glutamatergic and morphological alterations associated with early life seizure-induced preconditioning in young rats Eur. J. Neurosci. 32 2010 1897 1911
60. R. Sankar, D. Shin, H. Liu, H. Katsumori, and C.G. Wasterlain Granule cell neurogenesis after status epilepticus in the immature rat brain Epilepsia 41 Suppl. 6 2000 S53 56
61. H.E. Scharfman, J.H. Goodman, and A.L. Sollas Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis J. Neurosci. 20 2000 6144 6158
62. H.E. Scharfman, and W.P. Gray Relevance of seizure-induced neurogenesis in animal models of epilepsy to the etiology of temporal lobe epilepsy Epilepsia 48 Suppl. 2 2007 33 41
63. H.E. Scharfman, A.L. Sollas, R.E. Berger, and J.H. Goodman Electrophysiological evidence of monosynaptic excitatory transmission between granule cells after seizure-induced mossy fiber sprouting J. Neurophysiol. 90 2003 2536 2547
64. B. Seri, J.M. Garcia-Verdugo, B.S. McEwen, and A. Alvarez-Buylla Astrocytes give rise to new neurons in the adult mammalian hippocampus J. Neurosci. 21 2001 7153 7160
65. B. Steiner, F. Klempin, L. Wang, M. Kott, H. Kettenmann, and G. Kempermann Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis Glia 54 2006 805 814
66. A receptor expression in newborn dentate granule cells after early life febrile seizures Dev. Neurobiol. 2012 10.1002/dneu.22016
67. Y. Tozuka, S. Fukuda, T. Namba, T. Seki, and T. Hisatsune GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells Neuron 47 2005 803 815
68. C. Walter, B.L. Murphy, R.Y. Pun, A.L. Spieles-Engemann, and S.C. Danzer Pilocarpine-induced seizures cause selective time-dependent changes to adult-generated hippocampal dentate granule cells J. Neurosci. 27 2007 7541 7552
69. A receptor alpha1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons J. Neurosci. 21 2001 3009 3016
70. A receptors are age-dependent Neuroscience 125 2004 299 303