Sustained brain-derived neurotrophic factor up-regulation and sensorimotor gating abnormality induced by postnatal exposure to phencyclidine: Comparison with adult treatment

Journal of Neurochemistry

Volumn 99, Issue 3, 2006, Pages 770-780

  Takahashi, Makoto ^a   Kakita, Akiyoshi ^b   Futamura, Takashi ^b   Watanabe, Yuichiro ^a,b   Mizuno, Makoto ^b   Sakimura, Kenji ^b   Castren, Eero ^c   Nabeshima, Toshitaka ^d   Someya, Toshiyuki ^a   Nawa, Hiroyuki ^b  

^a NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^b NIIGATA UNIVERSITY   (Japan)

^c UNIVERSITY OF HELSINKI   (Finland)

^d NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Limbic system; N methyl D aspartate; Neurotrophin; Phencyclidine; Prepulse inhibition; Schizophrenia

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; PHENCYCLIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG DEPENDENCE; EMBRYO; ENTORHINAL CORTEX; HIPPOCAMPUS; LIMBIC SYSTEM; MALE; NERVE CELL PLASTICITY; NEUROTOXICITY; NONHUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RAT STRAIN; SENSORIMOTOR INTEGRATION; SIGNAL TRANSDUCTION; SYNAPTOGENESIS; UPREGULATION;

AGING; ANIMALS; ANIMALS, NEWBORN; BLOTTING, NORTHERN; BLOTTING, WESTERN; BRAIN; BRAIN CHEMISTRY; BRAIN-DERIVED NEUROTROPHIC FACTOR; HALLUCINOGENS; HIPPOCAMPUS; IMMUNOENZYME TECHNIQUES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROINJECTIONS; PHENCYCLIDINE; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; STARTLE REACTION; UP-REGULATION;

EID: 33750072589     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04106.x     Document Type: Article

References (60)

1. Angelucci F., Mathe A. A. and Aloe L. (2000) Brain-derived neurotrophic factor and tyrosine kinase receptor TrkB in rat brain are significantly altered after haloperidol and risperidone administration. J. Neurosci. Res. 60, 783-794.
2. Angelucci F., Aloe L., Iannitelli A., Gruber S. H. and Mathe A. A. (2005) Effect of chronic olanzapine treatment on nerve growth factor and brain-derived neurotrophic factor in the rat brain. Eur. Neuropsychopharmacol. 15, 311-317.
3. Bakshi V. P. and Geyer M. A. (1998) Multiple limbic regions mediate the disruption of prepulse inhibition produced in rats by the noncompetitive NMDA antagonist dizocilpine. J. Neurosci. 18, 8394-8401.
4. Braff D. L., Geyer M. A. and Swerdlow N. R. (2001) Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology 156, 234-258.
5. Brooks W. J., Petit T. L. and LeBoutillier J. C. (1997a) Effect of chronic administration of NMDA antagonists on synaptic development. Synapse 26, 104-113.
6. Brooks W. J., Weeks A. C., Leboutillier J. C. and Petit T. L. (1997b) Altered NMDA sensitivity and learning following chronic developmental NMDA antagonism. Physiol. Behav. 62, 955-962.
7. Castren E., Pitkanen M., Sirvio J., Parsadanian A., Lindholm D., Thoenen H. and Riekkinen P. J. (1993) The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus. Neuroreport 4, 895-898.
8. Croll S. D., Wiegand S. J., Anderson K. D., Lindsay R. M. and Nawa H. (1994) Regulation of neuropeptides in adult rat forebrain by the neurotrophins BDNF and NGF. Eur. J. Neurosci. 6, 1343-1353.
9. Ehrhardt J., Sabel B. A. and Schroeder U. (1999) Subchronically applied phencyclidine fails to disrupt prepulse inhibition in rats. Eur. Neuropsychopharmacol. 10, 69-74.
10. Feinberg A. P. and Vogelstein B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6-13.
11. Fumagalli F., Bedogni F., Perez J., Racagni G. and Riva M. A. (2004) Corticostriatal brain-derived neurotrophic factor dysregulation in adult rats following prenatal stress. Eur. J. Neurosci. 20, 1348-1354.
12. Genoud C., Knott G. W., Sakata K., Lu B. and Welker E. (2004) Altered synapse formation in the adult somatosensory cortex of brain-derived neurotrophic factor heterozygote mice. J. Neurosci. 24, 2394-2400.
13. Geyer M. A., Krebs-Thomson K., Braff D. L. and Swerdlow N. R. (2001) Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in press. Psychopharmacology 156, 117-154.
14. Gianfranceschi L., Siciliano R., Walls J., Morales B., Kirkwood A., Huang Z. J., Tonegawa S. and Maffei L. (2003) Visual cortex is rescued from the effects of dark rearing by overexpression of BDNF. Proc. Natl Acad. Sci. USA 100, 12 486-12 491.
15. Greisen M. H., Altar C. A., Bolwig T. G., Whitehead R. and Wortwein G. (2005) Increased adult hippocampal brain-derived neurotrophic factor and normal levels of neurogenesis in maternal separation rats. J. Neurosci. Res. 79, 772-778.
16. Grimm J. W., Lu L., Hayashi T., Hope B. T., Su T. P. and Shaham Y. (2003) Time-dependent increases in brain-derived neurotrophic factor protein levels within the mesolimbic dopamine system after withdrawal from cocaine: implications for incubation of cocaine craving. J. Neurosci. 23, 742-747.
17. Guillin O., Diaz J., Carroll P., Griffon N., Schwartz J. C. and Sokoloff P. (2001) BDNF controls dopamine D3 receptor expression and triggers behavioural sensitization. Nature 411, 86-89.
18. Harris L. W., Sharp T., Gartlon J., Jones D. N. and Harrison P. J. (2003) Long-term behavioural, molecular and morphological effects of neonatal NMDA receptor antagonism. Eur. J. Neurosci. 18, 1706-1710.
19. Harrison P. J. and Weinberger D. R. (2005) Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol. Psychiatry 10, 40-68.
20. Holcomb H. H., Lahti A. C., Medoff D. R., Cullen T. and Tamminga C. A. (2005) Effects of noncompetitive NMDA receptor blockade on anterior cingulate cerebral blood flow in volunteers with schizophrenia. Neuropsychopharmacology 30, 2275-2282.
21. Hyman C., Hofer M., Barde Y. A., Juhasz M., Yancopoulos G. D., Squinto S. P. and Lindsay R. M. (1991) BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350, 230-232.
22. Ibaraki K., Otsu Y. and Nawa H. (1999) A novel two-site enzyme immunoassay reveals the regional distributions of and developmental changes in GluR1 and NMDAR1 protein contents in the rat brain. J. Neurochem. 73, 408-417.
23. Javitt D. C. and Zukin S. R. (1991) Recent advances in the phencyclidine model of schizophrenia. Am. J. Psychiatry 148, 1301-1308.
24. Jentsch J. D. and Roth R. H. (1999) The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 20, 201-225.
25. Kelley A. E. (2004) Memory and addiction: shared neural circuitry and molecular mechanisms. Neuron 44, 161-179.
26. Koch M. and Ebert U. (1998) Deficient sensorimotor gating following seizures in amygdala-kindled rats. Biol. Psychiatry 44, 290-297.
27. Kuma H., Miki T., Matsumoto Y., et al. (2004) Early maternal deprivation induces alterations in brain-derived neurotrophic factor expression in the developing rat hippocampus. Neurosci. Lett. 372, 68-73.
28. Kutsuwada T., Sakimura K., Manabe T., et al. (1996) Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor epsilon 2 subunit mutant mice. Neuron 16, 333-344.
29. Lauri S. E., Lamsa K., Pavlov I., Riekki R., Johnson B. E., Molnar E., Rauvala H. and Taira T. (2003) Activity blockade increases the number of functional synapses in the hippocampus of newborn rats. Mol. Cell. Neurosci. 22, 107-117.
30. Li Q., Clark S., Lewis D. V. and Wilson W. A. (2002) NMDA receptor antagonists disinhibit rat posterior cingulate and retrosplenial cortices: a potential mechanism of neurotoxicity. J. Neurosci. 22, 3070-3080.
31. Linden A. M., Vaisanen J., Lakso M., Nawa H., Wong G. and Castren E. (2000) Expression of neurotrophins BDNF and NT-3, and their receptors, in rat brain after administration of antipsychotic and psychotrophic agents. J. Mol. Neurosci. 14, 27-37.
32. Luthi A., Schwyzer L., Mateos J. M., Gahwiler B. H. and McKinney R. A. (2001) NMDA receptor activation limits the number of synaptic connections during hippocampal development. Nat. Neurosci. 4, 1102-1107.
33. Maisonpierre P. C., Le Beau M. M., Espinosa R. 3rd, Ip N. Y., Belluscio L., de la Monte S. M., Squinto S., Furth M. E. and Yancopoulos G. D. (1991) Human and rat brain-derived neurotrophic factor and neurotrophin-3: gene structures, distributions, and chromosomal localizations. Genomics 10, 558-568.
34. Martinez Z. A., Ellison G. D., Geyer M. A. and Swerdlow N. R. (1999) Effects of sustained phencyclidine exposure on sensorimotor gating of startle in rats. Neuropsychopharmacology 21, 28-39.
35. Meredith G. E., Callen S. and Scheuer D. A. (2002) Brain-derived neurotrophic factor expression is increased in the rat amygdala, piriform cortex and hypothalamus following repeated amphetamine administration. Brain Res. 949, 218-227.
36. Moghaddam B. and Adams B. W. (1998) Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats. Science 281, 1349-1352.
37. Narisawa-Saito M., Carnahan J., Araki K., Yamaguchi T. and Nawa H. (1999) Brain-derived neurotrophic factor regulates the expression of AMPA receptor proteins in neocortical neurons. Neuroscience 88, 1009-1014.
38. Nawa H., Carnahan J. and Gall C. (1995) BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: partial disagreement with mRNA levels. Eur. J. Neurosci. 7, 1527-1535.
39. Ninan I., Jardemark K. E. and Wang R. Y. (2003) Olanzapine and clozapine but not haloperidol reverse subchronic phencyclidine-induced functional hyperactivity of N-methyl-D-aspartate receptors in pyramidal cells of the rat medial prefrontal cortex. Neuropharmacology 44, 462-472.
40. Olney J. W. and Farber N. B. (1995) Glutamate receptor dysfunction and schizophrenia. Arch. Gen. Psychiatry 52, 998-1007.
41. Patterson S. L., Grover L. M., Schwartzkroin P. A. and Bothwell M. (1992) Neurotrophin expression in rat hippocampal slices: a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron 9, 1081-1088.
42. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego, CA.
43. Roceri M., Cirulli F., Pessina C., Peretto P., Racagni G. and Riva M. A. (2004) Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol. Psychiatry 55, 708-714.
44. Rostas J. A., Brent V. A., Voss K., Errington M. L., Bliss T. V. and Gurd J. W. (1996) Enhanced tyrosine phosphorylation of the 2B subunit of the N-methyl-D-aspartate receptor in long-term potentiation. Proc. Natl Acad. Sci. USA 93, 10 452-10 456.
45. Sakimura K., Kutsuwada T., Ito I., et al. (1995) Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor epsilon 1 subunit. Nature 373, 151-155.
46. Sams-Dodd F. (1998) Effects of continuous D-amphetamine and phencyclidine administration on social behaviour, stereotyped behaviour, and locomotor activity in rats. Neuropsychopharmacology 19, 18-25.
47. Scharfman H. E., Goodman J. H., Sollas A. L. and Croll S. D. (2002) Spontaneous limbic seizures after intrahippocampal infusion of brain-derived neurotrophic factor. Exp. Neurol. 174, 201-214.
48. Sircar R. (2003) Postnatal phencyclidine-induced deficit in adult water maze performance is associated with N-methyl-D-aspartate receptor upregulation. Int. J. Dev. Neurosci. 21, 159-167.
49. Son G. H., Geum D., Chung S., et al. (2006) Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. J. Neurosci. 26, 3309-3318.
50. Super H., Martinez A., Del Rio J. A. and Soriano E. (1998) Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus. J. Neurosci. 18, 4616-4626.
51. Takahashi M., Hayashi S., Kakita A., Wakabayashi K., Fukuda M., Kameyama S., Tanaka R., Takahashi H. and Nawa H. (1999) Patients with temporal lobe epilepsy show an increase in brain-derived neurotrophic factor protein and its correlation with neuropeptide Y. Brain Res. 818, 579-582.
52. Takahashi M., Shirakawa O., Toyooka K., et al. (2000) Abnormal expression of brain-derived neurotrophic factor and its receptor in the corticolimbic system of schizophrenic patients. Mol. Psychiatry 5, 293-300.
53. Takeuchi T., Kiyama Y., Nakamura K., et al. (2001) Roles of the glutamate receptor epsilon2 and delta2 subunits in the potentiation and prepulse inhibition of the acoustic startle reflex. Eur. J. Neurosci. 14, 153-160.
54. Trentani A., Kuipers S. D., Ter Horst G. J. and Den Boer J. A. (2002) Selective chronic stress-induced in vivo ERK1/2 hyperphosphorylation in medial prefrontocortical dendrites: implications for stress-related cortical pathology? Eur. J. Neurosci. 15, 1681-1691.
55. Wang C. Z. and Johnson K. M. (2005) Differential effects of acute and subchronic administration on phencyclidine-induced neurodegeneration in the perinatal rat. J. Neurosci. Res. 81, 284-292.
56. Wang C., McInnis J., Ross-Sanchez M., Shinnick-Gallagher P., Wiley J. L. and Johnson K. M. (2001) Long-term behavioral and neurodegenerative effects of perinatal phencyclidine administration: implications for schizophrenia. Neuroscience 107, 535-550.
57. Weickert C. S., Hyde T. M., Lipska B. K., Herman M. M., Weinberger D. R. and Kleinman J. E. (2003) Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol. Psychiatry 8, 592-610.
58. Yamakura T., Mori H., Masaki H., Shimoji K. and Mishina M. (1993) Different sensitivities of NMDA receptor channel subtypes to non-competitive antagonists. Neuroreport 4, 687-690.
59. Zafra F., Hengerer B., Leibrock J., Thoenen H. and Lindholm D. (1990) Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J. 9, 3545-3550.
60. Zhou J., Bradford H. F. and Stern G. M. (1996) Induction of dopaminergic neurotransmitter phenotype in rat embryonic cerebrocortex by the synergistic action of neurotrophins and dopamine. Eur. J. Neurosci. 8, 2328-2339.