Reduced Adult Hippocampal Neurogenesis and Cognitive Impairments following Prenatal Treatment of the Antiepileptic Drug Valproic Acid

Stem Cell Reports

Volumn 5, Issue 6, 2015, Pages 996-1009

  Juliandi, Berry ^a,b   Tanemura, Kentaro ^c   Igarashi, Katsuhide ^d   Tominaga, Takashi ^e   Furukawa, Yusuke ^f   Otsuka, Maky ^d   Moriyama, Noriko ^f   Ikegami, Daigo ^d   Abematsu, Masahiko ^g   Sanosaka, Tsukasa ^a   Tsujimura, Keita ^a   Narita, Minoru ^d   Kanno, Jun ^f   Nakashima, Kinichi ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b BOGOR AGRICULTURAL UNIVERSITY   (Indonesia)

^c TOHOKU UNIVERSITY   (Japan)

^d HOSHI UNIVERSITY   (Japan)

^e TOKUSHIMA BUNRI UNIVERSITY   (Japan)

^f NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^g KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; HISTONE DEACETYLASE; VALPROIC ACID; ANTICONVULSIVE AGENT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTICONVULSANT THERAPY; ARTICLE; CELL STRUCTURE; COGNITIVE DEFECT; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HISTONE ACETYLATION; LEARNING; LEARNING AND MEMORY TEST; MEMORY; MICROGLIA; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; POSTNATAL DEVELOPMENT; PRENATAL EXPOSURE; PRENATAL PERIOD; PRIORITY JOURNAL; RUNNING; ABNORMALITIES; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; GENE EXPRESSION REGULATION; MALE; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PREGNANCY;

ANIMALS; ANTICONVULSANTS; COGNITION DISORDERS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; LEARNING; MALE; MEMORY; MICE; MICE, INBRED C57BL; NEUROGENESIS; NEURONS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; VALPROIC ACID;

EID: 84949530914     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2015.10.012     Document Type: Article

References (63)

1. M. Abematsu, K. Tsujimura, M. Yamano, M. Saito, K. Kohno, J. Kohyama, M. Namihira, S. Komiya, and K. Nakashima Neurons derived from transplanted neural stem cells restore disrupted neuronal circuitry in a mouse model of spinal cord injury J. Clin. Invest. 120 2010 3255 3266
2. A. Alvarez-Buylla, and D.A. Lim For the long run: maintaining germinal niches in the adult brain Neuron 41 2004 683 686
3. V. Balasubramaniyan, E. Boddeke, R. Bakels, B. Küst, S. Kooistra, A. Veneman, and S. Copray Effects of histone deacetylation inhibition on neuronal differentiation of embryonic mouse neural stem cells Neuroscience 143 2006 939 951
4. D. Battino, and T. Tomson Management of epilepsy during pregnancy Drugs 67 2007 2727 2746
5. P. Bekinschtein, C.A. Oomen, L.M. Saksida, and T.J. Bussey Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable? Semin. Cell Dev. Biol. 22 2011 536 542
6. R.A. Blaheta, and J. Cinatl Jr. Anti-tumor mechanisms of valproate: a novel role for an old drug Med. Res. Rev. 22 2002 492 511
7. B.S. Chang, and D.H. Lowenstein Epilepsy N. Engl. J. Med. 349 2003 1257 1266
8. W. Deng, J.B. Aimone, and F.H. Gage New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci. 11 2010 339 350
9. J.H. DiLiberti, P.A. Farndon, N.R. Dennis, and C.J. Curry The fetal valproate syndrome Am. J. Med. Genet. 19 1984 473 481
10. J. Farmer, X. Zhao, H. van Praag, K. Wodtke, F.H. Gage, and B.R. Christie Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo Neuroscience 124 2004 71 79
11. E. Gebara, S. Sultan, J. Kocher-Braissant, and N. Toni Adult hippocampal neurogenesis inversely correlates with microglia in conditions of voluntary running and aging Front. Neurosci. 7 2013 145
12. H.S. Go, K.C. Kim, C.S. Choi, S.J. Jeon, K.J. Kwon, S.H. Han, J. Lee, J.H. Cheong, J.H. Ryu, C.H. Kim, and et al. Prenatal exposure to valproic acid increases the neural progenitor cell pool and induces macrocephaly in rat brain via a mechanism involving the GSK-3β/β-catenin pathway Neuropharmacology 63 2012 1028 1041
13. M. Göttlicher, S. Minucci, P. Zhu, O.H. Krämer, A. Schimpf, S. Giavara, J.P. Sleeman, F. Lo Coco, C. Nervi, P.G. Pelicci, and T. Heinzel Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells EMBO J. 20 2001 6969 6978
14. J. Hall, K.L. Thomas, and B.J. Everitt Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories J. Neurosci. 21 2001 2186 2193
15. Y. Hao, T. Creson, L. Zhang, P. Li, F. Du, P. Yuan, T.D. Gould, H.K. Manji, and G. Chen Mood stabilizer valproate promotes ERK pathway-dependent cortical neuronal growth and neurogenesis J. Neurosci. 24 2004 6590 6599
16. J. Hsieh, K. Nakashima, T. Kuwabara, E. Mejia, and F.H. Gage Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells Proc. Natl. Acad. Sci. USA 101 2004 16659 16664
17. G.W. Humphrey, Y.H. Wang, T. Hirai, R. Padmanabhan, D.M. Panchision, L.F. Newell, R.D. McKay, and B.H. Howard Complementary roles for histone deacetylases 1, 2, and 3 in differentiation of pluripotent stem cells Differentiation 76 2008 348 356
18. S. Jessberger, K. Nakashima, G.D. Clemenson Jr.; E. Mejia, E. Mathews, K. Ure, S. Ogawa, C.M. Sinton, F.H. Gage, and J. Hsieh Epigenetic modulation of seizure-induced neurogenesis and cognitive decline J. Neurosci. 27 2007 5967 5975
19. Joint Epilepsy Council Epilepsy Prevalence, Incidence, and Other Statistic 2011 Joint Epilepsy Council Publication
20. B. Juliandi, M. Abematsu, T. Sanosaka, K. Tsujimura, A. Smith, and K. Nakashima Induction of superficial cortical layer neurons from mouse embryonic stem cells by valproic acid Neurosci. Res. 72 2012 23 31
21. G.A. Jung, J.Y. Yoon, B.S. Moon, D.H. Yang, H.Y. Kim, S.H. Lee, V. Bryja, E. Arenas, and K.Y. Choi Valproic acid induces differentiation and inhibition of proliferation in neural progenitor cells via the beta-catenin-Ras-ERK-p21Cip/WAF1 pathway BMC Cell Biol. 9 2008 66
22. A.G. Kazantsev, and L.M. Thompson Therapeutic application of histone deacetylase inhibitors for central nervous system disorders Nat. Rev. Drug Discov. 7 2008 854 868
23. R.A. Kohman, T.K. Bhattacharya, E. Wojcik, and J.S. Rhodes Exercise reduces activation of microglia isolated from hippocampus and brain of aged mice J. Neuroinflammation 10 2013 114
24. M. Kostrouchová, Z. Kostrouch, and M. Kostrouchová Valproic acid, a molecular lead to multiple regulatory pathways Folia Biol. (Praha) 53 2007 37 49
25. J. LeDoux The emotional brain, fear, and the amygdala Cell. Mol. Neurobiol. 23 2003 727 738
26. J.L. MacDonald, and A.J. Roskams Histone deacetylases 1 and 2 are expressed at distinct stages of neuro-glial development Dev. Dyn. 237 2008 2256 2267
27. J.L. MacDonald, C.S. Gin, and A.J. Roskams Stage-specific induction of DNA methyltransferases in olfactory receptor neuron development Dev. Biol. 288 2005 461 473
28. T. Matsuda, N. Murao, Y. Katano, B. Juliandi, J. Kohyama, S. Akira, T. Kawai, and K. Nakashima TLR9 signalling in microglia attenuates seizure-induced aberrant neurogenesis in the adult hippocampus Nat. Commun. 6 2015 6514
29. K.J. Meador, G.A. Baker, N. Browning, J. Clayton-Smith, D.T. Combs-Cantrell, M. Cohen, L.A. Kalayjian, A. Kanner, J.D. Liporace, P.B. Pennell, et al. NEAD Study Group Cognitive function at 3 years of age after fetal exposure to antiepileptic drugs N. Engl. J. Med. 360 2009 1597 1605
30. K.J. Meador, G.A. Baker, N. Browning, M.J. Cohen, J. Clayton-Smith, L.A. Kalayjian, A. Kanner, J.D. Liporace, P.B. Pennell, M. Privitera, D.W. Loring NEAD Study Group Foetal antiepileptic drug exposure and verbal versus non-verbal abilities at three years of age Brain 134 2011 396 404
31. K.J. Meador, G.A. Baker, N. Browning, M.J. Cohen, R.L. Bromley, J. Clayton-Smith, L.A. Kalayjian, A. Kanner, J.D. Liporace, P.B. Pennell, et al. NEAD Study Group Effects of fetal antiepileptic drug exposure: outcomes at age 4.5 years Neurology 78 2012 1207 1214
32. K.J. Meador, G.A. Baker, N. Browning, M.J. Cohen, R.L. Bromley, J. Clayton-Smith, L.A. Kalayjian, A. Kanner, J.D. Liporace, P.B. Pennell, et al. NEAD Study Group Fetal antiepileptic drug exposure and cognitive outcomes at age 6 years (NEAD study): a prospective observational study Lancet Neurol. 12 2013 244 252
33. H. Meinardi, R.A. Scott, R. Reis, J.W. Sander ILAE Commission on the Developing World The treatment gap in epilepsy: the current situation and ways forward Epilepsia 42 2001 136 149
34. B.J. Molyneaux, P. Arlotta, J.R. Menezes, and J.D. Macklis Neuronal subtype specification in the cerebral cortex Nat. Rev. Neurosci. 8 2007 427 437
35. M. Murabe, J. Yamauchi, Y. Fujiwara, M. Hiroyama, A. Sanbe, and A. Tanoue A novel embryotoxic estimation method of VPA using ES cells differentiation system Biochem. Biophys. Res. Commun. 352 2007 164 169
36. H. Nau, R.S. Hauck, and K. Ehlers Valproic acid-induced neural tube defects in mouse and human: aspects of chirality, alternative drug development, pharmacokinetics and possible mechanisms Pharmacol. Toxicol. 69 1991 310 321
37. A.K. Ngugi, C. Bottomley, I. Kleinschmidt, J.W. Sander, and C.R. Newton Estimation of the burden of active and life-time epilepsy: a meta-analytic approach Epilepsia 51 2010 883 890
38. C.J. Phiel, F. Zhang, E.Y. Huang, M.G. Guenther, M.A. Lazar, and P.S. Klein Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen J. Biol. Chem. 276 2001 36734 36741
39. G. Rosenberg The mechanisms of action of valproate in neuropsychiatric disorders: can we see the forest for the trees? Cell. Mol. Life Sci. 64 2007 2090 2103
40. J.W. Sander The epidemiology of epilepsy revisited Curr. Opin. Neurol. 16 2003 165 170
41. Z. Sarnyai, E.L. Sibille, C. Pavlides, R.J. Fenster, B.S. McEwen, and M. Tóth Impaired hippocampal-dependent learning and functional abnormalities in the hippocampus in mice lacking serotonin(1A) receptors Proc. Natl. Acad. Sci. USA 97 2000 14731 14736
42. M.D. Saxe, F. Battaglia, J.W. Wang, G. Malleret, D.J. David, J.E. Monckton, A.D. Garcia, M.V. Sofroniew, E.R. Kandel, L. Santarelli, and et al. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus Proc. Natl. Acad. Sci. USA 103 2006 17501 17506
43. S. Shen, J. Li, and P. Casaccia-Bonnefil Histone modifications affect timing of oligodendrocyte progenitor differentiation in the developing rat brain J. Cell Biol. 169 2005 577 589
44. T.J. Shors, D.A. Townsend, M. Zhao, Y. Kozorovitskiy, and E. Gould Neurogenesis may relate to some but not all types of hippocampal-dependent learning Hippocampus 12 2002 578 584
45. A. Sierra, J.M. Encinas, J.J. Deudero, J.H. Chancey, G. Enikolopov, L.S. Overstreet-Wadiche, S.E. Tsirka, and M. Maletic-Savatic Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis Cell Stem Cell 7 2010 483 495
46. A.M. Stranahan Physiological variability in brain-derived neurotrophic factor expression predicts dendritic spine density in the mouse dentate gyrus Neurosci. Lett. 495 2011 60 62
47. H. Suh, W. Deng, and F.H. Gage Signaling in adult neurogenesis Annu. Rev. Cell Dev. Biol. 25 2009 253 275
48. G. Sun, C. Fu, C. Shen, and Y. Shi Histone deacetylases in neural stem cells and induced pluripotent stem cells J. Biomed. Biotechnol. 2011 2011 835968
49. R.J. Tolwani, P.S. Buckmaster, S. Varma, J.M. Cosgaya, Y. Wu, C. Suri, and E.M. Shooter BDNF overexpression increases dendrite complexity in hippocampal dentate gyrus Neuroscience 114 2002 795 805
50. G. Turrigiano Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement Annu. Rev. Neurosci. 34 2011 89 103
51. G.G. Turrigiano, and S.B. Nelson Homeostatic plasticity in the developing nervous system Nat. Rev. Neurosci. 5 2004 97 107
52. K. Van der Borght, R. Havekes, T. Bos, B.J. Eggen, and E.A. Van der Zee Exercise improves memory acquisition and retrieval in the Y-maze task: relationship with hippocampal neurogenesis Behav. Neurosci. 121 2007 324 334
53. H. van Praag Exercise and the brain: something to chew on Trends Neurosci. 32 2009 283 290
54. H. van Praag, B.R. Christie, T.J. Sejnowski, and F.H. Gage Running enhances neurogenesis, learning, and long-term potentiation in mice Proc. Natl. Acad. Sci. USA 96 1999 13427 13431
55. H. van Praag, G. Kempermann, and F.H. Gage Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus Nat. Neurosci. 2 1999 266 270
56. H. van Praag, T. Shubert, C. Zhao, and F.H. Gage Exercise enhances learning and hippocampal neurogenesis in aged mice J. Neurosci. 25 2005 8680 8685
57. N.M. van Strien, N.L. Cappaert, and M.P. Witter The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network Nat. Rev. Neurosci. 10 2009 272 282
58. J. Vukovic, M.J. Colditz, D.G. Blackmore, M.J. Ruitenberg, and P.F. Bartlett Microglia modulate hippocampal neural precursor activity in response to exercise and aging J. Neurosci. 32 2012 6435 6443
59. J.M. Wojtowicz, M.L. Askew, and G. Winocur The effects of running and of inhibiting adult neurogenesis on learning and memory in rats Eur. J. Neurosci. 27 2008 1494 1502
60. R.J. Yang, K. Mozhui, R.M. Karlsson, H.A. Cameron, R.W. Williams, and A. Holmes Variation in mouse basolateral amygdala volume is associated with differences in stress reactivity and fear learning Neuropsychopharmacology 33 2008 2595 2604
61. I.T. Yu, J.Y. Park, S.H. Kim, J.S. Lee, Y.S. Kim, and H. Son Valproic acid promotes neuronal differentiation by induction of proneural factors in association with H4 acetylation Neuropharmacology 56 2009 473 480
62. P.X. Yuan, L.D. Huang, Y.M. Jiang, J.S. Gutkind, H.K. Manji, and G. Chen The mood stabilizer valproic acid activates mitogen-activated protein kinases and promotes neurite growth J. Biol. Chem. 276 2001 31674 31683
63. C. Zhao, W. Deng, and F.H. Gage Mechanisms and functional implications of adult neurogenesis Cell 132 2008 645 660