Acute prenatal exposure to a moderate dose of valproic acid increases social behavior and alters gene expression in rats

International Journal of Developmental Neuroscience

Volumn 31, Issue 8, 2013, Pages 740-750

  Cohen, Ori S ^a   Varlinskaya, Elena I ^b,c,d,e,f   Wilson, Carey A ^a   Glatt, Stephen J ^a,h   Mooney, Sandra M ^c,d,e,f,g  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

^b BINGHAMTON UNIVERSITY   (United States)

^c Developmental Exposure Alcohol Research Center   (United States)

^d Developmental Exposure Alcohol Research Center   (United States)

^e Developmental Exposure Alcohol Research Center   (United States)

^f Developmental Exposure Alcohol Research Center   (United States)

^g UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^h SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

Adolescence; Autism; Gene expression; Sex differences; Social interaction; Teratogen

Indexed keywords

ISOPROTEIN; SODIUM CHLORIDE; VALPROIC ACID;

ACETYLATION; ADOLESCENCE; ADULTHOOD; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN REGION; CEREBELLUM VERMIS; CONTROLLED STUDY; DRUG EFFECT; EPIGENETICS; EXON; FEMALE; FIGHTING; GENE EXPRESSION; LOCOMOTION; LONG EVANS RAT; MALE; NONHUMAN; ORBITAL CORTEX; PILOT STUDY; PLAY; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROTEIN PROCESSING; RAT; SOCIAL AVOIDANCE BEHAVIOR; SOCIAL BEHAVIOR; SOCIAL INTERACTION; TRANSCRIPTOMICS;

AA; ADOLESCENCE; AMINO ACID; ANALYSIS OF COVARIANCE; ANALYSIS OF VARIANCE; ANCOVA; ANOVA; ANTERIOR AMYGDALA; AUTISM; CAMP RESPONSE ELEMENT BINDING PROTEIN; CEREBELLAR VERMIS; CREB; CREB BINDING PROTEIN; CREBBP; CV; DEOXYRIBOSE NUCLEIC ACID; DNA; G; GABA; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; GESTATIONAL DAY; HDAC; HDACI; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; I.P.; ID; IDENTITY; INTERSECTION/UNION TESTS; INTRAPERITONEAL; IUTS; MESSENGER RNA; MG/KG; MILLIGRAMS PER KILOGRAM BODY WEIGHT; MRNA; OFC; ORBITOFRONTAL CORTEX; P; P. C.; POSTNATAL DAY; PRINCIPAL COMPONENT; RIBONUCLEIC ACID; RNA; RTS; RUBINSTEIN-TAYBI SYNDROME; SEX DIFFERENCES; SOCIAL INTERACTION; TERATOGEN; VALPROIC ACID; VPA;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANTICONVULSANTS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICROARRAY ANALYSIS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRINCIPAL COMPONENT ANALYSIS; RATS; RATS, LONG-EVANS; RNA, MESSENGER; SOCIAL BEHAVIOR; VALPROIC ACID;

EID: 84885761570     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2013.09.002     Document Type: Article

References (75)

1. Altman J., Bayer S.A. Development of the brain stem in the rat I. Thymidine-radiographic study of the time of origin of neurons of the lower medulla. J. Comp. Neurol. 1980, 194:1-35.
2. Altman J., Bayer S.A. Development of the brain stem in the rat II. Thymidine-radiographic study of the time of origin of neurons of the upper medulla, excluding the vestibular and auditory nuclei. J. Comp. Neurol. 1980, 194:37-56.
3. Altman J., Bayer S.A. Development of the brain stem in the rat IV. Thymidine-radiographic study of the time of origin of neurons in the pontine region. J. Comp. Neurol. 1980, 194:905-929.
4. Ammer A.G., Weed S.A. Cortactin branches out: roles in regulating protrusive actin dynamics. Cell Motil. Cytoskeleton 2008, 65:687-707.
5. Brownell J.E., Allis C.D. Special HATs for special occasions: linking histone acetylation to chromatin assembly and gene activation. Curr. Opin. Genet. Dev. 1996, 6:176-184.
6. Chen H., Lin R.J., Xie W., Wilpitz D., Evans R.M. Regulation of hormone-induced histone hyperacetylation and gene activation via acetylation of an acetylase. Cell 1999, 98:675-686.
7. Chen Z., Kastaniotis A.J., Miinalainen I.J., Rajaram V., Wierenga R.K., Hiltunen J.K. 17beta-hydroxysteroid dehydrogenase type 8 and carbonyl reductase type 4 assemble as a ketoacyl reductase of human mitochondrial FAS. Faseb J. 2009, 23:3682-3691.
8. Cheng L., Lumb M., Polgar L., Mudge A.W. How can the mood stabilizer VPA limit both mania and depression?. Mol. Cell. Neurosci. 2005, 29:155-161.
9. Daenen E.W., Wolterink G., Gerrits M.A., Van Ree J.M. The effects of neonatal lesions in the amygdala or ventral hippocampus on social behaviour later in life. Behav. Brain Res. 2002, 136:571-582.
10. DelBello M.P., Strakowski S.M., Zimmerman M.E., Hawkins J.M., Sax K.W. MRI analysis of the cerebellum in bipolar disorder: a pilot study. Neuropsychopharmacology 1999, 21:63-68.
11. Demeer B., Andrieux J., Receveur A., Morin G., Petit F., Julia S., Plessis G., Martin-Coignard D., Delobel B., Firth H.V., Thuresson A.C., Lanco Dosen S., Sjors K., Le Caignec C., Devriendt K., Mathieu-Dramard M. Duplication 16p13.3 and the CREBBP gene: confirmation of the phenotype. Eur. J. Med. Genet. 2013, 56:26-31.
12. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., Lempicki R.A. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 2003, 4:P3.
13. Detich N., Bovenzi V., Szyf M. Valproate induces replication-independent active DNA demethylation. J. Biol. Chem. 2003, 278:27586-27592.
14. Diergaarde L., Gerrits M.A., Stuy A., Spruijt B.M., van Ree J.M. Neonatal amygdala lesions and juvenile isolation in the rat: differential effects on locomotor and social behavior later in life. Behav. Neurosci. 2004, 118:298-305.
15. Dong L.Q., Landa L.R., Wick M.J., Zhu L., Mukai H., Ono Y., Liu F. Phosphorylation of protein kinase N by phosphoinositide-dependent protein kinase-1 mediates insulin signals to the actin cytoskeleton. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:5089-5094.
16. Dufour-Rainfray D., Vourc'h P., Le Guisquet A.M., Garreau L., Ternant D., Bodard S., Jaumain E., Gulhan Z., Belzung C., Andres C.R., Chalon S., Guilloteau D. Behavior and serotonergic disorders in rats exposed prenatally to valproate: a model for autism. Neurosci. Lett. 2010, 470:55-59.
17. File S.E., Hyde J.R. Can social interaction be used to measure anxiety?. Br. J. Pharmacol. 1978, 62:19-24.
18. File S.E., Seth P. A review of 25 years of the social interaction test. Eur. J. Pharmacol. 2003, 463:35-53.
19. Fulop V., Bocskei Z., Polgar L. Prolyl oligopeptidase: an unusual beta-propeller domain regulates proteolysis. Cell 1998, 94:161-170.
20. Glatt S.J., Chandler S.D., Bousman C.A., Chana G., Lucero G.R., Tatro E., May T., Lohr J.B., Kremen W.S., Everall I.P., Tsuang M.T. Alternatively spliced genes as biomarkers for schizophrenia, bipolar disorder and psychosis: a blood-based spliceome-profiling exploratory study. Curr. Pharmacogenomics Person Med. 2009, 7:164-188.
21. Grassart A., Meas-Yedid V., Dufour A., Olivo-Marin J.C., Dautry-Varsat A., Sauvonnet N. Pak1 phosphorylation enhances cortactin-N-WASP interaction in clathrin-caveolin-independent endocytosis. Traffic 2010, 11:1079-1091.
22. Harrison B.C., Huynh K., Lundgaard G.L., Helmke S.M., Perryman M.B., McKinsey T.A. Protein kinase C-related kinase targets nuclear localization signals in a subset of class IIa histone deacetylases. FEBS Lett. 2010, 584:1103-1110.
23. Hayashi M.L., Rao B.S., Seo J.S., Choi H.S., Dolan B.M., Choi S.Y., Chattarji S., Tonegawa S. Inhibition of p21-activated kinase rescues symptoms of fragile X syndrome in mice. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:11489-11494.
24. Hennekam R.C., Tilanus M., Hamel B.C., Voshart-van Heeren H., Mariman E.C., van Beersum S.E., van den Boogaard M.J., Breuning M.H. Deletion at chromosome 16p13.3 as a cause of Rubinstein-Taybi syndrome: clinical aspects. Am. J. Hum. Genet. 1993, 52:255-262.
25. Ichimiya T., Okubo Y., Suhara T., Sudo Y. Reduced volume of the cerebellar vermis in neuroleptic-naive schizophrenia. Biol. Psychiatry 2001, 49:20-27.
26. Ingram J.L., Peckham S.M., Tisdale B., Rodier P.M. Prenatal exposure of rats to valproic acid reproduces the cerebellar anomalies associated with autism. Neurotoxicol. Teratol. 2000, 22:319-324.
27. Kaufmann W.E., Cooper K.L., Mostofsky S.H., Capone G.T., Kates W.R., Newschaffer C.J., Bukelis I., Stump M.H., Jann A.E., Lanham D.C. Specificity of cerebellar vermian abnormalities in autism: a quantitative magnetic resonance imaging study. J. Child Neurol. 2003, 18:463-470.
28. Kuwagata M., Ogawa T., Shioda S., Nagata T. Observation of fetal brain in a rat valproate-induced autism model: a developmental neurotoxicity study. Int. J. Dev. Neurosci. 2009, 27:399-405.
29. Loeber R.T., Cintron C.M., Yurgelun-Todd D.A. Morphometry of individual cerebellar lobules in schizophrenia. Am. J. Psychiatry 2001, 158:952-954.
30. Mackie S., Shaw P., Lenroot R., Pierson R., Greenstein D.K., Nugent T.F., Sharp W.S., Giedd J.N., Rapoport J.L. Cerebellar development and clinical outcome in attention deficit hyperactivity disorder. Am. J. Psychiatry 2007, 164:647-655.
31. Maes M., Goossens F., Scharpe S., Calabrese J., Desnyder R., Meltzer H.Y. Alterations in plasma prolyl endopeptidase activity in depression, mania, and schizophrenia: effects of antidepressants, mood stabilizers, and antipsychotic drugs. Psychiatry Res. 1995, 58:217-225.
32. Mah L., Arnold M.C., Grafman J. Impairment of social perception associated with lesions of the prefrontal cortex. Am. J. Psychiatry 2004, 161:1247-1255.
33. Mannaerts I., Nuytten N.R., Rogiers V., Vanderkerken K., van Grunsven L.A., Geerts A. Chronic administration of valproic acid inhibits activation of mouse hepatic stellate cells in vitro and in vivo. Hepatology 2010, 51:603-614.
34. Markram K., Rinaldi T., La Mendola D., Sandi C., Markram H. Abnormal fear conditioning and amygdala processing in an animal model of autism. Neuropsychopharmacology 2008, 33:901-912.
35. McIntosh A.L., Senthivinayagam S., Moon K.C., Gupta S., Lwande J.S., Murphy C.C., Storey S.M., Atshaves B.P. Direct interaction of Plin2 with lipids on the surface of lipid droplets: a live cell FRET analysis. Am. J. Physiol. Cell Physiol. 2012, 303:C728-C742.
36. Meaney M.J., Stewart J. Neonatal-androgens influence the social play of prepubescent rats. Horm. Behav. 1981, 15:197-213.
37. Meera P., Wallner M., Jiang Z., Toro L. A calcium switch for the functional coupling between alpha (hslo) and beta subunits (Kv,cabeta) of maxi K channels. FEBS Lett. 1996, 385:127-128.
38. Metzger E., Muller J.M., Ferrari S., Buettner R., Schule R. A novel inducible transactivation domain in the androgen receptor: implications for PRK in prostate cancer. EMBO J. 2003, 22:270-280.
39. Middei S., Spalloni A., Longone P., Pittenger C., O'Mara S.M., Marie H., Ammassari-Teule M. CREB selectively controls learning-induced structural remodeling of neurons. Learn. Mem. 2012, 19:330-336.
40. Middleton F.A., Varlinskaya E.I., Mooney S.M. Molecular substrates of social avoidance seen following prenatal ethanol exposure and its reversal by social enrichment. Dev. Neurosci. 2012, 34:115-128.
41. Mooney S.M., Miller M.W. Time-specific effects of ethanol exposure on cranial nerve nuclei: gastrulation and neuronogenesis. Exp. Neurol. 2007, 205:56-63.
42. Mooney S.M., Varlinskaya E.I. Acute prenatal exposure to ethanol and social behavior: effects of age, sex, and timing of exposure. Behav. Brain Res. 2011, 216:358-364.
43. Mychasiuk R., Richards S., Nakahashi A., Kolb B., Gibb R. Effects of rat prenatal exposure to valproic acid on behavior and neuro-anatomy. Dev. Neurosci. 2012, 34:268-276.
44. Ohno S., Nishikawa K., Honda Y., Nakajin S. Expression in E. coli and tissue distribution of the human homologue of the mouse Ke 6 gene, 17beta-hydroxysteroid dehydrogenase type 8. Mol. Cell Biochem. 2008, 309:209-215.
45. Partek Incorporated Partek Documentation 2008, Partek Incorporated.
46. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates, Burlington, MA 2009.
47. Peltonen I., Mannisto P.T. Effects of diverse psychopharmacological substances on the activity of brain prolyl oligopeptidase. Basic Clin. Pharmacol. Toxicol. 2011, 108:46-54.
48. Phiel C.J., Zhang F., Huang E.Y., Guenther M.G., Lazar M.A., Klein P.S. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J. Biol. Chem. 2001, 276:36734-36741.
49. Picard H., Amado I., Mouchet-Mages S., Olie J.P., Krebs M.O. The role of the cerebellum in schizophrenia: an update of clinical, cognitive, and functional evidences. Schizophr. Bull. 2008, 34:155-172.
50. Raymond G.V., Bauman M.L., Kemper T.L. Hippocampus in autism: a Golgi analysis. Acta Neuropathol. 1996, 91:117-119.
51. Rinaldi T., Silberberg G., Markram H. Hyperconnectivity of local neocortical microcircuitry induced by prenatal exposure to valproic acid. Cereb. Cortex 2008, 18:763-770.
52. Rodier P.M., Ingram J.L., Tisdale B., Nelson S., Romano J. Embryological origin for autism: developmental anomalies of the cranial nerve motor nuclei. J. Comp. Neurol. 1996, 370:247-261.
53. Rosenberg G. The mechanisms of action of valproate in neuropsychiatric disorders: can we see the forest for the trees?. Cell Mol. Life Sci. 2007, 64:2090-2103.
54. Rosenberg G. The mechanisms of action of valproate in neuropsychiatric disorders: can we see the forest for the trees?. Cell. Mol. Life Sci. 2007, 64:2090-2103.
55. Rudebeck P.H., Walton M.E., Millette B.H., Shirley E., Rushworth M.F., Bannerman D.M. Distinct contributions of frontal areas to emotion and social behaviour in the rat. Eur. J. Neurosci. 2007, 26:2315-2326.
56. Schneider T., Labuz D., Przewlocki R. Nociceptive changes in rats after prenatal exposure to valproic acid. Pol. J. Pharmacol. 2001, 53:531-534.
57. Schneider T., Przewlocki R. Behavioral alterations in rats prenatally exposed to valproic acid: animal model of autism. Neuropsychopharmacology 2005, 30:80-89.
58. Schneider T., Roman A., Basta-Kaim A., Kubera M., Budziszewska B., Schneider K., Przewlocki R. Gender-specific behavioral and immunological alterations in an animal model of autism induced by prenatal exposure to valproic acid. Psychoneuroendocrinology 2008, 33:728-740.
59. Seese R.R., Babayan A.H., Katz A.M., Cox C.D., Lauterborn J.C., Lynch G., Gall C.M. LTP induction translocates cortactin at distant synapses in wild-type but not Fmr1 knock-out mice. J. Neurosci. 2012, 32:7403-7413.
60. Snow W.M., Hartle K., Ivanco T.L. Altered morphology of motor cortex neurons in the VPA rat model of autism. Dev. Psychobiol. 2008, 50:633-639.
61. Stanton M.E., Peloso E., Brown K.L., Rodier P. Discrimination learning and reversal of the conditioned eyeblink reflex in a rodent model of autism. Behav. Brain Res. 2007, 176:133-140.
62. Strick P.L., Dum R.P., Fiez J.A. Cerebellum and nonmotor function. Annu. Rev. Neurosci. 2009, 32:413-434.
63. Thor D.H., Holloway W.R. Social play in juvenile rats: a decade of methodological and experimental research. Neurosci. Biobehav. Rev. 1984, 8:455-464.
64. van der Horst A., Tertoolen L.G., de Vries-Smits L.M., Frye R.A., Medema R.H., Burgering B.M. FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1). J. Biol. Chem. 2004, 279:28873-28879.
65. Vanderschuren L.J., Niesink R.J., Van Ree J.M. The neurobiology of social play behavior in rats. Neurosci. Biobehav. Rev. 1997, 21:309-326.
66. Varlinskaya E.I., Spear L.P. Acute effects of ethanol on social behavior of adolescent and adult rats: role of familiarity of the test situation. Alcohol Clin. Exp. Res. 2002, 26:1502-1511.
67. Varlinskaya E.I., Spear L.P. Social interactions in adolescent and adult Sprague-Dawley rats: impact of social deprivation and test context familiarity. Behav. Brain Res. 2008, 188:398-405.
68. Varlinskaya E.I., Spear L.P. Sensitization to social anxiolytic effects of ethanol in adolescent and adult Sprague-Dawley rats after repeated ethanol exposure. Alcohol 2010, 44:99-110.
69. Varlinskaya E.I., Spear L.P., Spear N.E. Social behavior and social motivation in adolescent rats: role of housing conditions and partner's activity. Physiol. Behav. 1999, 67:475-482.
70. Varlinskaya E.I., Spear L.P., Spear N.E. Acute effects of ethanol on behavior of adolescent rats: role of social context. Alcohol Clin. Exp. Res. 2001, 25:377-385.
71. von Holleben M., Gohla A., Janssen K.P., Iritani B.M., Beer-Hammer S. Immunoinhibitory adapter protein Src homology domain 3 lymphocyte protein 2 (SLy2) regulates actin dynamics and B cell spreading. J. Biol. Chem. 2011, 286:13489-13501.
72. Vorhees C.V. Teratogenicity and developmental toxicity of valproic acid in rats. Teratology 1987, 135:195-202.
73. Webb B.A., Zhou S., Eves R., Shen L., Jia L., Mak A.S. Phosphorylation of cortactin by p21-activated kinase. Arch. Biochem. Biophys. 2006, 456:183-193.
74. Welches W.R., Brosnihan K.B., Ferrario C.M. A comparison of the properties and enzymatic activities of three angiotensin processing enzymes: angiotensin converting enzyme, prolyl endopeptidase and neutral endopeptidase 24.11. Life Sci. 1993, 52:1461-1480.
75. Zhang M.M., Yu K., Xiao C., Ruan D.Y. The influence of developmental periods of sodium valproate exposure on synaptic plasticity in the CA1 region of rat hippocampus. Neurosci. Lett. 2003, 351:165-168.