Prenatal exposure to phencyclidine produces abnormal behaviour and NMDA receptor expression in postpubertal mice

International Journal of Neuropsychopharmacology

Volumn 13, Issue 7, 2010, Pages 877-889

  Lu, Lingling ^a,b   Mamiya, Takayoshi ^a   Lu, Ping ^a,b   Toriumi, Kazuya ^a   Mouri, Akihiro ^a,d   Hiramatsu, Masayuki ^a   Kim, Hyoung Chun ^e   Zou, Li Bo ^b   Nagai, Taku ^c   Nabeshima, Toshitaka ^a,f  

^a MEIJO UNIVERSITY   (Japan)

^b SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d Japanese Society of Pharmacopoeia   (Japan)

^e Kangwon National University   (South Korea)

^f Japanese Drug Organization of Appropriate Use and Research   (Japan)

Author keywords

Antipsychotic; behaviour; neurodevelopment; NMDA receptor; PCP; prenatal

Indexed keywords

CLOZAPINE; HALOPERIDOL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; PHENCYCLIDINE;

ABNORMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; DRUG EFFECT; EMBRYO; FEMALE; GESTATIONAL AGE; HYPERSENSITIVITY; LOCOMOTION; MALE; MEMORY; MOUSE; NERVE CELL DIFFERENTIATION; NEURULATION; NONHUMAN; PRENATAL EXPOSURE; PRENATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECOGNITION;

ANIMALS; BRAIN; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; HALLUCINOGENS; HUMANS; LATERAL VENTRICLES; MALE; MENTAL DISORDERS; MICE; MICE, INBRED ICR; MOTOR ACTIVITY; PHENCYCLIDINE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; RECOGNITION (PSYCHOLOGY); RETENTION (PSYCHOLOGY);

EID: 77957235287     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145709990757     Document Type: Article

References (56)

1. Abekawa T, Ito K, Nakagawa S, Koyama T (2007). Prenatal exposure to an NMDA receptor antagonist, MK-801 reduces density of parvalbumin-immunoreactive GABAergic neurons in the medial prefrontal cortex and enhances phencyclidine-induced hyperlocomotion but not behavioral sensitization to methamphetamine in postpubertal rats. Psychopharmacology (Berlin) 192, 303-316. (Pubitemid 46701582)
2. Akbarian S, Sucher NJ, Bradley D, Tafazzoli A, et al. (1996). Selective alterations in gene expression for NMDA receptor subunits in prefrontal cortex of schizophrenics. Journal of Neuroscience 16, 19-30. (Pubitemid 26010694)
3. Amitai N, Semenova S, Markou A (2007). Cognitivedisruptive effects of the psychotomimetic phencyclidine and attenuation by atypical antipsychotic medications in rats. Psychopharmacology (Berlin) 193, 521-537. (Pubitemid 47094377)
4. Anastasio NC, Johnson KM (2008). Differential regulation of the NMDA receptor by acute and sub-chronic phencyclidine administration in the developing rat. Journal of Neurochemistry 104, 1210-1218.
5. Andersen JD, Pouzet B (2004). Spatial memory deficits induced by perinatal treatment of rats with PCP and reversal effect of D-serine. Neuropsychopharmacology 29, 1080-1090. (Pubitemid 38670046)
6. Angelucci F, Brenè S, Mathé AA (2005). BDNF in schizophrenia, depression and corresponding animal models. Molecular Psychiatry 10, 345-352. (Pubitemid 40490802)
7. Ashdown H, Dumont Y, Ng M, Poole S, et al. (2006). The role of cytokines in mediating effects of prenatal infection on the fetus: implications for schizophrenia. Molecular Psychiatry 11, 47-55. (Pubitemid 43251087)
8. Behar TN, Scott CA, Greene CL, Wen X, et al. (1999). Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. Journal of Neuroscience 19, 4449-4461. (Pubitemid 29241096)
9. Bellinger FP, Wilce PA, Bedi KS, Wilson P (2002). Long-lasting synaptic modification in the rat hippocampus resulting from NMDA receptor blockade during development. Synapse 43, 95-101. (Pubitemid 34028492)
10. Bogerts B (1993). Recent advances in the neuropathology of schizophrenia. Schizophrenia Bulletin 19, 431-445. (Pubitemid 23183155)
11. Brown AS, Susser ES (2002). In utero infection and adult schizophrenia. Mental Retardation and Developmental Disabilities Research Reviews 8, 51-57.
12. Chen L, Yang CR (2002). Interaction of dopamine D1 and NMDA receptors mediates acute clozapine potentiation of glutamate EPSPs in rat prefrontal cortex. Journal of Neurophysiology 87, 2324-2336. (Pubitemid 34670705)
13. Crow TJ, Ball J, Bloom SR, Brown R, et al. (1989). Schizophrenia as an anomaly of development of cerebral asymmetry. A postmortem study and a proposal concerning the genetic basis of the disease. Archives of General Psychiatry 46, 1145-1150. (Pubitemid 20016453)
14. Deutsch SI, Mastropaolo J, Rosse RB (1998). Neurodevelopmental consequences of early exposure to phencyclidine and related drugs. Clinical Neuropharmacology 21, 320-332. (Pubitemid 28543946)
15. Dracheva S, Marras SA, Elhakem SL, Kramer FR, et al. (2001). N-methyl-D-aspartic acid receptor expression in the dorsolateral prefrontal cortex of elderly patients with schizophrenia. American Journal of Psychiatry 158, 1400-1410. (Pubitemid 32847238)
16. Emamian ES, Karayiorgou M, Gogos JA (2004). Decreased phosphorylation of NMDA receptor type 1 at serine 897 in brains of patients with schizophrenia. Journal of Neuroscience 24, 1561-1564. (Pubitemid 38240950)
17. Enomoto T, Noda Y, Mouri A, Shin EJ, et al. (2005). Longlasting impairment of associative learning is correlated with a dysfunction of N-methyl-D-aspartate-extracellular signaling-regulated kinase signaling in mice after withdrawal from repeated administration of phencyclidine. Molecular Pharmacology 68, 1765-7174. (Pubitemid 41654359)
18. Fico TA, Vanderwende C (1988). Phencyclidine during pregnancy: fetal brain levels and neurobehavioral effects. Neurotoxicology and Teratology 10, 349-354. (Pubitemid 19267574)
19. Gemperle AY, Enz A, Pozza MF, Luthi A, Olpe HR (2003). Effects of clozapine, haloperidol and iloperidone on neurotransmission and synaptic plasticity in prefrontal cortex and their accumulation in brain tissue: an in vitro study. Neuroscience 117, 681-695. (Pubitemid 36263161)
20. Green MF, Bracha HS, Satz P, Christenson CD (1994). Preliminary evidence for an association between minor physical anomalies and second trimester neurodevelopment in schizophrenia. Psychiatry Research 53, 119-127.
21. Haberny KA, Paule MG, Scallet AC, Sistare FD, et al. (2002). Ontogeny of the N-methyl-D-aspartate (NMDA) receptor system and susceptibility to neurotoxicity. Toxicological Sciences 68, 9-17.
22. Husi H, Grant SG (2001). Proteomics of the nervous system. Trends Neuroscience 24, 259-266. (Pubitemid 32304467)
23. Ikonomidou C, Bosch F, Miksa M, Bittigau P, et al. (1999). Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283, 70-74. (Pubitemid 29044848)
24. Impagnatiello F, Guidotti AR, Pesold C, Dwivedi Y, et al. (1998). A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proceedings of the National Academy of Sciences USA 95, 15718-15723. (Pubitemid 29018766)
25. Javitt DC, Zukin SR (1991). Recent advances in the phencyclidine model of schizophrenia. American Journal of Psychiatry 148, 1301-1308.
26. Jones P, Rodgers B, Murray R, Marmot M (1994). Child development risk factors for adult schizophrenia in the British 1946 birth cohort. Lancet 344, 1398-1402. (Pubitemid 24365314)
27. Kaufman KR, Petrucha RA, Pitts Jr. FN, Weekes ME (1983). PCP in amniotic fluid and breast milk: case report. Journal of Clinical Psychiatry 44, 269-270.
28. Komuro H, Rakic P (1993). Modulation of neuronal migration by NMDA receptors. Science 260, 95-97. (Pubitemid 23122752)
29. Leveque JC, Mac?́as W, Rajadhyaksha A, Carlson RR, et al. (2000). Intracellular modulation of NMDA receptor function by antipsychotic drugs. Journal of Neuroscience 20, 4011-4020. (Pubitemid 30365671)
30. Lu P, Mamiya T, Lu LL, Mouri A, et al. (2009). Silibinin prevents amyloid b peptide-induced memory impairment and oxidative stress in mice. British Journal of Pharmacology 157, 1270-1277.
31. Maddox VH, Godefroi EF, Parcell RF (1965). The synthesis of phencyclidine and other 1-arylcyclohexylamines. Journal of Medicinal Chemistry 8, 230-235.
32. Millan MJ (2005). N-methyl-D-aspartate receptors as a target for improved antipsychotic agents: novel insight and clinical perspectives. Psychopharmacology 179, 30-53.
33. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994). Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529-540. (Pubitemid 24100885)
34. Mouri A, Noda Y, Enomoto T, Nabeshima T (2007a). Phencyclidine animal models of schizophrenia: approaches from abnormality of glutamatergic neurotransmission and neurodevelopment. Neurochemistry International 51, 173-184. (Pubitemid 47176714)
35. Mouri A, Noda Y, Hara H, Mizoguchi H, et al. (2007b). Oral vaccination with a viral vector containing Ab cDNA attenuates age-related Ab accumulation and memory deficits without causing inflammation in a mouse Alzheimer model. Journal of the Federation of American Societies for Experimental Biology 21, 2135-2148. (Pubitemid 47026449)
36. Mouri A, Noda Y, Noda A, Nakamura T, et al. (2007c). Involvement of a dysfunctional dopamine-D1/ N-methyl-d-aspartate-NR1 and Ca2+/calmodulindependent protein kinase II pathway in the impairment of latent learning in a model of schizophrenia induced by phencyclidine. Molecular Pharmacology 71, 1598-1609. (Pubitemid 47010913)
37. Murai R, Noda Y, Matsui K, Kamei H, et al. (2007). Hypofunctional glutamatergic neurotransmission in the prefrontal cortex is involved in the emotional deficit induced by repeated treatment with phencyclidine in mice: implications for abnormalities of glutamate release and NMDA-CaMKII signaling. Behavioral Brain Research 180, 152-160. (Pubitemid 46719421)
38. Murray RM, OCallaghan E, Castle DJ, Lewis SW (1992). A neurodevelopmental approach to the classification of schizophrenia. Schizophrenia Bulletin 18, 319-332.
39. Nabeshima T, Fukaya H, Yamaguchi K, Ishikawa K, et al. (1987). Development of tolerance and supersensitivity to phencyclidine in rats after repeated administration of phencyclidine. European Journal of Pharmacology 135, 23-33. (Pubitemid 17051006)
40. Nabeshima T, Hiramatsu M, Yamaguchi K, Kasugai M, et al. (1988). Effects of prenatal administration of phencyclidine on the learning and memory processes of rat offspring. Journal of Pharmacobiodynamics 11, 816-823. (Pubitemid 19036198)
41. Nagai T, Murai R, Matsui K, Kamei H, et al. (2009). Aripiprazole ameliorates phencyclidine-induced impairment of recognition memory through dopamine D1 and serotonin 5-HT1A receptors. Psychopharmacology 202, 315-328.
42. Nagai T, Noda Y, Une T, Furukawa K, et al. (2003). Effect of AD-5423 on animal models of schizophrenia: phencyclidine-induced behavioral changes in mice. Neuroreport 14, 269-272. (Pubitemid 36308425)
43. Nicholas JM, Lipshitz J, Schreiber EC (1982). Phencyclidine: its transfer across the placenta as well as into breast milk. American Journal of Obstetrics and Gynecology 143, 143-146. (Pubitemid 12104982)
44. Noda Y, Yamada K, Furukawa H, Nabeshima T (1995). Enhancement of immobility in a forced swimming test by subacute or repeated treatment with phencyclidine: a new model of schizophrenia. British Journal of Pharmacology 116, 2531-2537.
45. Pilowski LS, Kerwin RW, Murray RM (1993). Schizophrenia: a neuro-developmental perspective. Neuropsychopharmacology 9, 83-91.
46. Qiao H, Noda Y, Kamei H, Nagai T, et al. (2001). Clozapine, but not haloperidol, reverses social behavior deficit in mice during withdrawal from chronic phencyclidine treatment. Neuroreport 12, 11-15. (Pubitemid 32099018)
47. Raman IM, Tong G, Jahr CE (1996). Beta-adrenergic regulation of synaptic NMDA receptors by cAMPdependent protein kinase. Neuron 16, 415-421. (Pubitemid 2625345)
48. Rao VR, Finkbeiner S (2007). NMDA and AMPA receptors: old channels, new tricks. Trends in Neurosciences 30, 284-291. (Pubitemid 46802833)
49. Scheetz AJ, Constantine-Paton M (1994). Modulation of NMDA receptor function: implications for vertebrate neural development. Journal of the Federation of American Societies for Experimental Biology 8, 745-752. (Pubitemid 24229769)
50. Scott DB, Blanpied TA, EhlersMD(2003). Coordinated PKA and PKC phosphorylation suppresses RXR-mediated ER retention and regulates the surface delivery of NMDA receptors. Neuropharmacology 45, 755-767.
51. Shen S, Lang B, Nakamoto C, Zhang F, et al. (2008). Schizophrenia-related neural and behavioral phenotypes in transgenic mice expressing truncated Disc1. Journal of Neuroscience 28, 10893-10904.
52. Slikker Jr. W, Paule MG, Wright LK, Patterson TA, Wang C (2007). System biology approaches for toxicology. Journal of Applied Toxicology 27, 201-217.
53. Theiler K (1989). The House Mouse - Atlas of Embryonic Development. New York, USA: Springer-Verlag.
54. Wang C, McInnis J, Ross-SanchezM, Shinnick-Gallagher P, et al. (2001). Long-term behavioral and neurodegenerative effects of perinatal phencyclidine administration: implications for schizophrenia. Neuroscience 107, 535-550. (Pubitemid 33097492)
55. Watanabe M, Inoue Y, Sakimura K, Mishina M (1992). Developmental changes in distribution of NMDA receptor channel subunit mRNAs. Neuroreport 3, 1138-1140. (Pubitemid 23034721)
56. Yanai J, Avraham Y, Levy S, Maslaton J, et al. (1992). Alterations in septohippocampal cholinergic innervations and related behaviors after early exposure to heroin and phencyclidine. Brain Research Developmental Brain Research 69, 207-214.