Inhibition of histone deacetylase in utero causes sociability deficits in postnatal mice

Behavioural Brain Research

Volumn 257, Issue , 2013, Pages 253-264

  Moldrich, Randal X ^a   Leanage, Gayeshika ^a   She, David ^a   Dolan Evans, Elliot ^a   Nelson, Michael ^a   Reza, Nargis ^a   Reutens, David C ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Autism; Histone acetylation; Histone deacetylase; Sociability; Sodium valproate; Trichostatin A

Indexed keywords

HISTONE DEACETYLASE; HISTONE H3; HISTONE H4; LYSINE; TRICHOSTATIN A; VALPROIC ACID;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; EMBRYO; ENZYME INHIBITION; GROOMING; HABITUATION; HISTONE ACETYLATION; HISTONE METHYLATION; MOUSE; MOUSE EMBRYO; NONHUMAN; PERINATAL PERIOD; PREGNANCY OUTCOME; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PUP (RODENT); SMELLING; SOCIABILITY DEFICIT; SOCIAL BEHAVIOR; VOCALIZATION;

AUTISM; HISTONE ACETYLATION; HISTONE DEACETYLASE; SOCIABILITY; SODIUM VALPROATE; TRICHOSTATIN A;

ANIMALS; ANIMALS, NEWBORN; EMBRYO, MAMMALIAN; FEMALE; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HYDROXAMIC ACIDS; INTERPERSONAL RELATIONS; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; ROTAROD PERFORMANCE TEST; SMELL; SOCIAL BEHAVIOR DISORDERS; VALPROIC ACID; VOCALIZATION, ANIMAL;

EID: 84886404961     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.09.049     Document Type: Article

References (58)

1. Hallmayer J., Glasson E.J., Bower C., Petterson B., Croen L., Grether J., et al. On the twin risk in autism. Am J Hum Genet 2002, 71:941-946.
2. Kinney D.K., Barch D.H., Chayka B., Napoleon S., Munir K.M. Environmental risk factors for autism: do they help cause de novo genetic mutations that contribute to the disorder. Med Hypotheses 2010, 74:102-106.
3. Dufour-Rainfray D., Vourc'h P., Tourlet S., Guilloteau D., Chalon S., Andres C.R. Fetal exposure to teratogens: evidence of genes involved in autism. Neurosci Biobehav Rev 2011, 35:1254-1265.
4. Moore S.J., Turnpenny P., Quinn A., Glover S., Lloyd D.J., Montgomery T., et al. A clinical study of 57 children with fetal anticonvulsant syndromes. J Med Genet 2000, 37:489-497.
5. Dean J.C., Hailey H., Moore S.J., Lloyd D.J., Turnpenny P.D., Little J. Long term health and neurodevelopment in children exposed to antiepileptic drugs before birth. J Med Genet 2002, 39:251-259.
6. Rasalam A.D., Hailey H., Williams J.H., Moore S.J., Turnpenny P.D., Lloyd D.J., et al. Characteristics of fetal anticonvulsant syndrome associated autistic disorder. Dev Med Child Neurol 2005, 47:551-555.
7. Bromley R.L., Mawer G., Clayton-Smith J., Baker G.A. Autism spectrum disorders following in utero exposure to antiepileptic drugs. Neurology 2008, 71:1923-1924.
8. Vinten J., Bromley R.L., Taylor J., Adab N., Kini U., Baker G.A. The behavioral consequences of exposure to antiepileptic drugs in utero. Epilepsy Behav 2009, 14:197-201.
9. Nadebaum C., Anderson V.A., Vajda F., Reutens D.C., Barton S., Wood A.G. Language skills of school-aged children prenatally exposed to antiepileptic drugs. Neurology 2011, 76:719-726.
10. Baker G.A., Bromley R.L. School-aged children who were exposed to sodium valproate in utero have impaired language scores when compared with a population mean score. Evid Based Med 2011, 16:178-179.
11. Nadebaum C., Anderson V., Vajda F., Reutens D., Barton S., Wood A. The Australian brain and cognition and antiepileptic drugs study: IQ in school-aged children exposed to sodium valproate and polytherapy. J Int Neuropsychol Soc 2011, 17:133-142.
12. Nadebaum C., Anderson V., Vajda F., Reutens D., Wood A. Neurobehavioral consequences of prenatal antiepileptic drug exposure. Dev Neuropsychol 2012, 37:1-29.
13. Bromley R.L., Mawer G.E., Briggs M., Cheyne C., Clayton-Smith J., Garcia-Finana M., et al. The prevalence of neurodevelopmental disorders in children prenatally exposed to antiepileptic drugs. J Neurol Neurosurg Psychiatry 2013, 84:637-643.
14. Chapman A., Keane P.E., Meldrum B.S., Simiand J., Vernieres J.C. Mechanism of anticonvulsant action of valproate. Prog Neurobiol 1982, 19:315-359.
15. VanDongen A.M., VanErp M.G., Voskuyl R.A. Valproate reduces excitability by blockage of sodium and potassium conductance. Epilepsia 1986, 27:177-182.
16. Zhang Y., Sun Y., Wang F., Wang Z., Peng Y., Li R. Downregulating the canonical Wnt/beta-catenin signaling pathway attenuates the susceptibility to autism-like phenotypes by decreasing oxidative stress. Neurochem Res 2012, 37:1409-1419.
17. Blaheta R.A., Cinatl J. Anti-tumor mechanisms of valproate: a novel role for an old drug. Med Res Rev 2002, 22:492-511.
18. Gottlicher M., Minucci S., Zhu P., Kramer O.H., Schimpf A., Giavara S., et al. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 2001, 20:6969-6978.
19. 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.
20. 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.
21. 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.
22. Schneider T., Przewlocki R. Behavioral alterations in rats prenatally exposed to valproic acid: animal model of autism. Neuropsychopharmacology 2005, 30:80-89.
23. Wagner G.C., Reuhl K.R., Cheh M., McRae P., Halladay A.K. A new neurobehavioral model of autism in mice: pre- and postnatal exposure to sodium valproate. J Autism Dev Disord 2006, 36:779-793.
24. 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.
25. Roullet F.I., Wollaston L., Decatanzaro D., Foster J.A. Behavioral and molecular changes in the mouse in response to prenatal exposure to the anti-epileptic drug valproic acid. Neuroscience 2010, 170:514-522.
26. Kim K.C., Kim P., Go H.S., Choi C.S., Yang S.I., Cheong J.H., et al. The critical period of valproate exposure to induce autistic symptoms in Sprague-Dawley rats. Toxicol Lett 2011, 201:137-142.
27. Kataoka S., Takuma K., Hara Y., Maeda Y., Ago Y., Matsuda T. Autism-like behaviours with transient histone hyperacetylation in mice treated prenatally with valproic acid. Int J Neuropsychopharmacol 2011, 1-13.
28. Kini U. Fetal valproate syndrome: a review. Paediatr Perinatal Drug Ther 2006, 7:123-130.
29. DiLiberti J.H., Farndon P.A., Dennis N.R., Curry C.J. The fetal valproate syndrome. Am J Med Genet 1984, 19:473-481.
30. Naruse I., Collins M.D., Scott W.J. Strain differences in the teratogenicity induced by sodium valproate in cultured mouse embryos. Teratology 1988, 38:87-96.
31. Fox W.M. Reflex-ontogeny and behavioural development of the mouse. Anim Behav 1965, 13:234-241.
32. Russell G., Steer C., Golding J. Social and demographic factors that influence the diagnosis of autistic spectrum disorders. Soc Psychiatry Psychiatr Epidemiol 2011, 46:1283-1293.
33. Fombonne E. Epidemiological trends in rates of autism. Mol Psychiatry 2002, 7:S4-S6.
34. Schneider T., Roman A., Basta-Kaim A., Kubera M., Budziszewska B., Schneider K., et al. Gender-specific behavioral and immunological alterations in an animal model of autism induced by prenatal exposure to valproic acid. Psychoneuroendocrinology 2008, 33:728-740.
35. Scattoni M.L., Gandhy S.U., Ricceri L., Crawley J.N. Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PLoS One 2008, 3:e3067.
36. Yang M., Silverman J.L., Crawley J.N. Automated three-chambered social approach task for mice. Curr Protoc Neurosci 2011, 56:8.26.1-8.26.16.
37. Silverman J.L., Yang M., Lord C., Crawley J.N. Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 2010, 11:490-502.
38. Marinova Z., Leng Y., Leeds P., Chuang D.M. Histone deacetylase inhibition alters histone methylation associated with heat shock protein 70 promoter modifications in astrocytes and neurons. Neuropharmacology 2011, 60:1109-1115.
39. Arriaga G., Zhou E.P., Jarvis E.D. Of mice, birds, and men: the mouse ultrasonic song system has some features similar to humans and song-learning birds. PLoS ONE 2012, 7:e46610.
40. Hofer M.A., Shair H.N. Ultrasonic vocalization, laryngeal braking, and thermogenesis in rat pups: a reappraisal. Behav Neurosci 1993, 107:354-362.
41. Shaked M., Weissmuller K., Svoboda H., Hortschansky P., Nishino N., Wolfl S., et al. Histone deacetylases control neurogenesis in embryonic brain by inhibition of BMP2/4 signaling. PLoS One 2008, 3:e2668.
42. Sanderson L., Taylor G.W., Aboagye E.O., Alao J.P., Latigo J.R., Coombes R.C., et al. Plasma pharmacokinetics and metabolism of the histone deacetylase inhibitor trichostatin a after intraperitoneal administration to mice. Drug Metab Dispos 2004, 32:1132-1138.
43. Nau H., Loscher W. Valproic acid: brain and plasma levels of the drug and its metabolites, anticonvulsant effects and gamma-aminobutyric acid (GABA) metabolism in the mouse. J Pharmacol Exp Ther 1982, 220:654-659.
44. Dendrinos G., Hemelt M., Keller A. Prenatal VPA exposure and changes in sensory processing by the superior colliculus. Front Integr Neurosci 2011, 5:68.
45. Luo A.H., Cannon E.H., Wekesa K.S., Lyman R.F., Vandenbergh J.G., Anholt R.R. Impaired olfactory behavior in mice deficient in the alpha subunit of G(o). Brain Res 2002, 941:62-71.
46. Crawley J.N., Chen T., Puri A., Washburn R., Sullivan T.L., Hill J.M., et al. Social approach behaviors in oxytocin knockout mice: comparison of two independent lines tested in different laboratory environments. Neuropeptides 2007, 41:145-163.
47. Stack C.M., Lim M.A., Cuasay K., Stone M.M., Seibert K.M., Spivak-Pohis I., et al. Deficits in social behavior and reversal learning are more prevalent in male offspring of VIP deficient female mice. Exp Neurol 2008, 211:67-84.
48. Llaneza D.C., DeLuke S.V., Batista M., Crawley J.N., Christodulu K.V., Frye C.A. Communication, interventions, and scientific advances in autism: a commentary. Physiol Behav 2010, 100:268-276.
49. Felix-Ortiz A.C., Febo M. Gestational valproate alters BOLD activation in response to complex social and primary sensory stimuli. PLoS ONE 2012, 7:e37313.
50. Wohr M., Dahlhoff M., Wolf E., Holsboer F., Schwarting R.K., Wotjak C.T. Effects of genetic background, gender, and early environmental factors on isolation-induced ultrasonic calling in mouse pups: an embryo-transfer study. Behav Genet 2008, 38:579-595.
51. Chabout J., Serreau P., Ey E., Bellier L., Aubin T., Bourgeron T., et al. Adult male mice emit context-specific ultrasonic vocalizations that are modulated by prior isolation or group rearing environment. PLoS One 2012, 7:e29401.
52. Marks P.A., Breslow R. Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nature biotechnology 2007, 25:84-90.
53. Naito H., Tonoue T. Sex difference in ultrasound distress call by rat pups. Behav Brain Res 1987, 25:13-21.
54. Jung G.A., Yoon J.Y., Moon B.S., Yang D.H., Kim H.Y., Lee S.H., et al. Valproic acid induces differentiation and inhibition of proliferation in neural progenitor cells via the beta-catenin-Ras-ERK-p21Cip/WAF1 pathway. BMC Cell Biol 2008, 9:66.
55. Yamauchi J., Miyamoto Y., Murabe M., Fujiwara Y., Sanbe A., Fujita Y., et al. Gadd45a, the gene induced by the mood stabilizer valproic acid, regulates neurite outgrowth through JNK and the substrate paxillin in N1E-115 neuroblastoma cells. Exp Cell Res 2007, 313:1886-1896.
56. Chen G., Manji H.K., Hawver D.B., Wright C.B., Potter W.Z. Chronic sodium valproate selectively decreases protein kinase C alpha and epsilon in vitro. J Neurochem 1994, 63:2361-2364.
57. Hall A.C., Brennan A., Goold R.G., Cleverley K., Lucas F.R., Gordon-Weeks P.R., et al. Valproate regulates GSK-3-mediated axonal remodeling and synapsin I clustering in developing neurons. Mol Cell Neurosci 2002, 20:257-270.
58. Detich N., Bovenzi V., Szyf M. Valproate induces replication-independent active DNA demethylation. J Biol Chem 2003, 278:27586-27592.