Valproic acid reduces spatial working memory and cell proliferation in the hippocampus

Neuroscience

Volumn 166, Issue 1, 2010, Pages 15-22

  Umka, J ^a   Mustafa, S ^a   ElBeltagy, M ^b   Thorpe, A ^a   Latif, L ^a   Bennett, G ^a   Wigmore, P M ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b MENOUFIA UNIVERSITY   (Egypt)

Author keywords

cognition; hippocampus; neural progenitor proliferation

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DOUBLECORTIN; NOTCH1 RECEPTOR; VALPROIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; MALE; MEMORY DISORDER; MENTAL PERFORMANCE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; WORKING MEMORY;

ANIMALS; ANTICONVULSANTS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL PROLIFERATION; COGNITION; COGNITION DISORDERS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; MALE; MEMORY; MEMORY DISORDERS; NEUROGENESIS; NEURONAL PLASTICITY; NEUROPSYCHOLOGICAL TESTS; RATS; RECEPTOR, NOTCH1; SPACE PERCEPTION; VALPROIC ACID;

EID: 74449087273     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.11.073     Document Type: Article

References (78)

1. Abrous D.N., Koehl M., and Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85 (2005) 523-569
2. Bannerman D.M., Rawlins J.N., Mchugh S.B., Deacon R.M., Yee B.K., Bast T., Zhang W.N., Pothuizen H.H., and Feldon J. Regional dissociations within the hippocampus-memory and anxiety. Neurosci Biobehav Rev 28 (2004) 273-283
3. Bekinschtein P., Cammarota M., Katche C., Slipczuk L., Rossato J.I., Goldin A., Izquierdo I., and Medina J.H. BDNF is essential to promote persistence of long-term memory storage. Proc Natl Acad Sci U S A 105 (2008) 2711-2716
4. Bolanos A.R., Sarkisian M., Yang Y., Hori A., Helmers S.L., Mikati M., Tandon P., Stafstrom C.E., and Holmes G.L. Comparison of valproate and phenobarbital treatment after status epilepticus in rats. Neurology 51 (1998) 41-48
5. Breunig J.J., Silbereis J., Vaccarino F.M., Sestan N., and Rakic P. Notch regulates cell fate and dendrite morphology of newborn neurons in the postnatal dentate gyrus. Proc Natl Acad Sci U S A 104 (2007) 20558-20563
6. Bruel-Jungerman E., Laroche S., and Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 21 (2005) 513-521
7. Buckley P.F. Update on the treatment and management of schizophrenia and bipolar disorder. CNS Spectr 13 (2008) 1-10 quiz 11-12
8. Carpay J.A., Aldenkamp A.P., and Van Donselaar C.A. Complaints associated with the use of antiepileptic drugs: results from a community-based study. Seizure 14 (2005) 198-206
9. Chan J.P., Cordeira J., Calderon G.A., Iyer L.K., and Rios M. Depletion of central BDNF in mice impedes terminal differentiation of new granule neurons in the adult hippocampus. Mol Cell Neurosci 39 (2008) 372-383
10. Costa R.M., Drew C., and Silva A.J. Notch to remember. Trends Neurosci 28 (2005) 429-435
11. Costa R.M., Honjo T., and Silva A.J. Learning and memory deficits in Notch mutant mice. Curr Biol 13 (2003) 1348-1354
12. Couillard-Despres S., Winner B., Schaubeck S., Aigner R., Vroemen M., Weidner N., Bogdahn U., Winkler J., Kuhn H.G., and Aigner L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21 (2005) 1-14
13. Cysique L.A., Maruff P., and Brew B.J. Valproic acid is associated with cognitive decline in HIV-infected individuals: a clinical observational study. BMC Neurol 6 (2006) 42
14. Das C.M., Aguilera D., Vasquez H., Prasad P., Zhang M., Wolff J.E., and Gopalakrishnan V. Valproic acid induces p21 and topoisomerase-II (alpha/beta) expression and synergistically enhances etoposide cytotoxicity in human glioblastoma cell lines. J Neuro Oncol 85 (2007) 159-170
15. Des Portes V., Pinard J.M., Billuart P., Vinet M.C., Koulakoff A., Carrie A., Gelot A., Dupuis E., Motte J., Berwald-Netter Y., Catala M., Kahn A., Beldjord C., and Chelly J. A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92 (1998) 51-61
16. Dix S.L., and Aggleton J.P. Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition. Behav Brain Res 99 (1999) 191-200
17. Drapeau E., Mayo W., Aurousseau C., LeMoal M., Piazza P.V., and Abrous D.N. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci U S A 100 (2003) 14385-14390
18. Duman R.S., Malberg J., and Nakagawa S. Regulation of adult neurogenesis by psychotropic drugs and stress. J Pharmacol Exp Ther 299 (2001) 401-407
19. Dupret D., Revest J.M., Koehl M., Ichas F., De Giorgi F., Costet P., Abrous D.N., and Piazza P.V. Spatial relational memory requires hippocampal adult neurogenesis. PLoS ONE 3 (2008) e1959
20. Ehninger D., and Kempermann G. Neurogenesis in the adult hippocampus. Cell Tissue Res 331 (2008) 243-250
21. Ennaceur A., and Delacour J. A new one-trial test for neurobiological studies of memory in rats1: Behavioral data. Behav Brain Res 31 (1988) 47-59
22. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., and Gage F.H. Neurogenesis in the adult human hippocampus. Nat Med 4 (1998) 1313-1317
23. Gleeson J.G., Lin P.T., Flanagan L.A., and Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23 (1999) 257-271
24. Gottlicher M., Minucci S., Zhu P., Kramer O.H., Schimpf A., Giavara S., Sleeman J.P., Lo Coco F., Nervi C., Pelicci P.G., and Heinzel T. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 20 (2001) 6969-6978
25. Green W., Patil P., Marsden C.A., Bennett G.W., and Wigmore P.M. Treatment with olanzapine increases cell proliferation in the subventricular zone and prefrontal cortex. Brain Res 1070 (2006) 242-245
26. Gualtieri C.T., and Johnson L.G. Comparative neurocognitive effects of 5 psychotropic anticonvulsants and lithium. MedGenMed 8 (2006) 46
27. Gurvich N., Berman M.G., Wittner B.S., Gentleman R.C., Klein P.S., and Green J.B. Association of valproate-induced teratogenesis with histone deacetylase inhibition in vivo. FASEB J 19 (2005) 1166-1168
28. Henry T.R. The history of valproate in clinical neuroscience. Psychopharmacol Bull 37 Suppl 2 (2003) 5-16
29. Holick K.A., Lee D.C., Hen R., and Dulawa S.C. Behavioral effects of chronic fluoxetine in BALB/cJ mice do not require adult hippocampal neurogenesis or the serotonin 1A receptor. Neuropsychopharmacology 33 (2008) 406-417
30. Hommet C., Mondon K., DeToffol B., and Constans T. Reversible cognitive and neurological symptoms during valproic acid therapy. J Am Geriatr Soc 55 (2007) 628
31. Hsieh J., Nakashima K., Kuwabara T., Mejia E., and Gage F.H. Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci U S A 101 (2004) 16659-16664
32. Huang G.J., and Herbert J. Stimulation of neurogenesis in the hippocampus of the adult rat by fluoxetine requires rhythmic change in corticosterone. Biol Psychiatry 59 (2006) 619-624
33. Imayoshi I., Sakamoto M., Ohtsuka T., Takao K., Miyakawa T., Yamaguchi M., Mori K., Ikeda T., Itohara S., and Kageyama R. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11 (2008) 1153-1161
34. Jessberger S., Clark R.E., Broadbent N.J., Clemenson Jr. G.D., Consiglio A., Lie D.C., Squire L.R., and Gage F.H. Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16 (2009) 147-154
35. Jessberger S., Nakashima K., Clemenson Jr. G.D., Mejia E., Mathews E., Ure K., Ogawa S., Sinton C.M., Gage F.H., and Hsieh J. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci 27 (2007) 5967-5975
36. Jung G.A., Yoon J.Y., Moon B.S., Yang D.H., Kim H.Y., Lee S.H., Bryja V., Arenas E., and Choi K.Y. 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
37. Kee N., Sivalingam S., Boonstra R., and Wojtowicz J.M. The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115 (2002) 97-105
38. Kee N., Teixeira C.M., Wang A.H., and Frankland P.W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10 (2007) 355-362
39. Kempermaan G. Adult neurogenesis (2006), Oxford University Press, New York
40. Kempermann G., and Gage F.H. Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur J Neurosci 16 (2002) 129-136
41. Kitabatake Y., Sailor K.A., Ming G.L., and Song H. Adult neurogenesis and hippocampal memory function: new cells, more plasticity, new memories?. Neurosurg Clin North Am 18 (2007) 105-113 x
42. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., and Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci U S A 92 (1995) 8856-8860
43. Kostrouchova M., Kostrouch Z., and Kostrouchova M. Valproic acid, a molecular lead to multiple regulatory pathways. Folia Biol (Praha) 53 (2007) 37-49
44. Kwan P., Sills G.J., and Brodie M.J. The mechanisms of action of commonly used antiepileptic drugs. Pharmacol Ther 90 (2001) 21-34
45. Lee I., Hunsaker M.R., and Kesner R.P. The role of hippocampal subregions in detecting spatial novelty. Behav Neurosci 119 (2005) 145-153
46. Li X.N., Shu Q., Su J.M., Perlaky L., Blaney S.M., and Lau C.C. Valproic acid induces growth arrest, apoptosis, and senescence in medulloblastomas by increasing histone hyperacetylation and regulating expression of p21Cip1, CDK4, and CMYC. Mol Cancer Ther 4 (2005) 1912-1922
47. Lossius M.I., Hessen E., Mowinckel P., Stavem K., Erikssen J., Gulbrandsen P., and Gjerstad L. Consequences of antiepileptic drug withdrawal: a randomized, double-blind study (Akershus Study). Epilepsia 49 (2008) 455-463
48. Lu Y., Christian K., and Lu B. BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory?. Neurobiol Learn Mem 89 (2008) 312-323
49. Madsen T.M., Kristjansen P.E., Bolwig T.G., and Wortwein G. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119 (2003) 635-642
50. Masmoudi K., Gras-Champel V., Masson H., and Andrejak M. Parkinsonism and/or cognitive impairment with valproic acid therapy: a report of ten cases. Pharmacopsychiatry 39 (2006) 9-12
51. Mayhew T.M., and Burton G.J. Methodological problems in placental morphometry: apologia for the use of stereology based on sound sampling practice. Placenta 9 (1988) 565-581
52. Meador K., Reynolds M.W., Crean S., Fahrbach K., and Probst C. Pregnancy outcomes in women with epilepsy: a systematic review and meta-analysis of published pregnancy registries and cohorts. Epilepsy Res 81 (2008) 1-13
53. Meshi D., Drew M.R., Saxe M., Ansorge M.S., David D., Santarelli L., Malapani C., Moore H., and Hen R. Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat Neurosci 9 (2006) 729-731
54. Minichiello L., Korte M., Wolfer D., Kuhn R., Unsicker K., Cestari V., Rossi-Arnaud C., Lipp H.P., Bonhoeffer T., and Klein R. Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24 (1999) 401-414
55. Mizuno M., Yamada K., Takei N., Tran M.H., He J., Nakajima A., Nawa H., and Nabeshima T. Phosphatidylinositol 3-kinase: a molecule mediating BDNF-dependent spatial memory formation. Mol Psychiatry 8 (2003) 217-224
56. Mumby D.G., Gaskin S., Glenn M.J., Schramek T.E., and Lehmann H. Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. Learn Mem 9 (2002) 49-57
57. Mustafa S., Walker A., Bennett G., and Wigmore P.M. 5-Fluorouracil chemotherapy affects spatial working memory and newborn neurons in the adult rat hippocampus. Eur J Neurosci 28 (2008) 323-330
58. Nicolai J., Vles J.S., and Aldenkamp A.P. Neurodevelopmental delay in children exposed to antiepileptic drugs in utero: a critical review directed at structural study-bias. J Neurol Sci 271 (2008) 1-14
59. Nissinen J., and Pitkanen A. Effect of antiepileptic drugs on spontaneous seizures in epileptic rats. Epilepsy Res 73 (2007) 181-191
60. Phiel C.J., Zhang F., Huang E.Y., Guenther M.G., Lazar M.A., and Klein P.S. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276 (2001) 36734-36741
61. Raber J., Rola R., Lefevour A., Morhardt D., Curley J., Mizumatsu S., Vandenberg S.R., and Fike J.R. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 162 (2004) 39-47
62. Rao M.S., and Shetty A.K. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 19 (2004) 234-246
63. Redmond L., Oh S.R., Hicks C., Weinmaster G., and Ghosh A. Nuclear Notch1 signaling and the regulation of dendritic development. Nat Neurosci 3 (2000) 30-40
64. Ristic A.J., Vojvodic N., Jankovic S., Sindelic A., and Sokic D. The frequency of reversible parkinsonism and cognitive decline associated with valproate treatment: a study of 364 patients with different types of epilepsy. Epilepsia 47 (2006) 2183-2185
65. Sairanen M., O'Leary O.F., Knuuttila J.E., and Castren E. Chronic antidepressant treatment selectively increases expression of plasticity-related proteins in the hippocampus and medial prefrontal cortex of the rat. Neuroscience 144 (2007) 368-374
66. Saxe M.D., Battaglia F., Wang J.W., Malleret G., David D.J., Monckton J.E., Garcia A.D., Sofroniew M.V., Kandel E.R., Santarelli L., Hen R., and Drew M.R. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci U S A 103 (2006) 17501-17506
67. Schmitz C., and Hof P.R. Design-based stereology in neuroscience. Neuroscience 130 (2005) 813-831
68. Seigers R., Schagen S.B., Beerling W., Boogerd W., Van Tellingen O., Van Dam F.S., Koolhaas J.M., and Buwalda B. Long-lasting suppression of hippocampal cell proliferation and impaired cognitive performance by methotrexate in the rat. Behav Brain Res 186 (2008) 168-175
69. Senturk V., Goker C., Bilgic A., Olmez S., Tugcu H., Oncu B., and Atbasoglu E.C. Impaired verbal memory and otherwise spared cognition in remitted bipolar patients on monotherapy with lithium or valproate. Bipolar Disord 9 Suppl 1 (2007) 136-144
70. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., and Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410 (2001) 372-376
71. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., and Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12 (2002) 578-584
72. Snyder J.S., Hong N.S., Mcdonald R.J., and Wojtowicz J.M. A role for adult neurogenesis in spatial long-term memory. Neuroscience 130 (2005) 843-852
73. Stump G., Durrer A., Klein A.L., Lutolf S., Suter U., and Taylor V. Notch1 and its ligands Delta-like and Jagged are expressed and active in distinct cell populations in the postnatal mouse brain. Mech Dev 114 (2002) 153-159
74. Tashiro A., Makino H., and Gage F.H. Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J Neurosci 27 (2007) 3252-3259
75. Thuret S., Toni N., Aigner S., Yeo G.W., and Gage F.H. Hippocampus-dependent learning is associated with adult neurogenesis in MRL/MpJ mice. Hippocampus 19 (2009) 658-669
76. Wang Y., Chan S.L., Miele L., Yao P.J., Mackes J., Ingram D.K., Mattson M.P., and Furukawa K. Involvement of Notch signaling in hippocampal synaptic plasticity. Proc Natl Acad Sci U S A 101 (2004) 9458-9462
77. Zhao C., Deng W., and Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 132 (2008) 645-660
78. Zhao C., Teng E.M., Summers Jr. R.G., Ming G.L., and Gage F.H. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26 (2006) 3-11