Changes in gene expression after phencyclidine administration in developing rats: A potential animal model for schizophrenia

International Journal of Developmental Neuroscience

Volumn 29, Issue 3, 2011, Pages 351-358

  Liu, F ^a   Zou, X ^a   Sadovova, N ^a   Zhang, X ^a   Shi, L ^a   Guo, L ^a   Qian, F ^b   Wen, Z ^a   Patterson, T A ^a   Hanig, J P ^c   Paule, M G ^a   Slikker, W ^a   Wang, C ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b ICF INTERNATIONAL   (United States)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

Apoptosis; DNA microarray; Gene expression; Neuronal development; Phencyclidine (PCP); Schizophrenia

Indexed keywords

BASIC HELIX LOOP HELIX DOMAIN CONTAINING CLASS B 2 PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; PHENCYCLIDINE; RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; DNA MICROARRAY; FEMALE; FRONTAL CORTEX; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HISTOPATHOLOGY; MALE; MOLECULAR PROBE; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROTOXICITY; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SCHIZOPHRENIA;

ANIMALS; BRAIN; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID ANTAGONISTS; FLUORESCEINS; GENE EXPRESSION; GENE EXPRESSION PROFILING; MICROARRAY ANALYSIS; MOLECULAR SEQUENCE DATA; NERVE DEGENERATION; PHENCYCLIDINE; PRINCIPAL COMPONENT ANALYSIS; RATS; RATS, SPRAGUE-DAWLEY; SCHIZOPHRENIA;

ANIMALIA; RATTUS;

EID: 79953293815     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2010.07.234     Document Type: Article

References (59)

1. Ashe P.C., Chlan-Fourney J., Juorio A.V., Li X.M. Brain-derived neurotrophic factor (BDNF) mRNA in rats with neonatal ibotenic acid lesions of the ventral hippocampus. Brain Res. 2002, 956(1):126-135.
2. Baldridge E.B., Bessen H.A. Phencyclidine. Emerg. Med. Clin. North Am. 1990, 8(3):541-550.
3. Barbera J.P., Rodriguez T.A., Greene N.D., Weninger W.J., Simeone A., Copp A.J., Beddington R.S., Dunwoodie S. Folic acid prevents exencephaly in Cited2 deficient mice. Hum. Mol. Genet. 2002, 11(3):283-293.
4. Benes F.M., McSparren J., Bird E.D., SanGiovanni J.P., Vincent S.L. Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch. Gen. Psychiatry 1991, 48(11):996-1001.
5. Braff D.L., Grillon C., Geyer M.A. Gating and habituation of the startle reflex in schizophrenic patients. Arch. Gen. Psychiatry 1992, 49(3):206-215.
6. Brazil D.P., Hemmings B.A. Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem. Sci. 2001, 26(11):657-664.
7. Bromet E.J., Fennig S. Epidemiology and natural history of schizophrenia. Biol. Psychiatry 1999, 46(7):871-881.
8. Chao M.V. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci. 2003, 4(4):299-309.
9. Clancy B., Darlington R.B., Finlay B.L. Translating developmental time across mammalian species. Neuroscience 2001, 105(1):7-17.
10. Coyle J.T. Glutamate and schizophrenia: beyond the dopamine hypothesis. Cell. Mol. Neurobiol. 2006, 26(4-6):365-384.
11. Durany N., Michel T., Zochling R., Boissl K.W., Cruz-Sanchez F.F., Riederer P., Thome J. Brain-derived neurotrophic factor and neurotrophin 3 in schizophrenic psychoses. Schizophr. Res. 2001, 52(1-2):79-86.
12. Ghosh A., Carnahan J., Greenberg M.E. Requirement for BDNF in activity-dependent survival of cortical neurons. Science 1994, 263(5153):1618-1623.
13. Guo L., Lobenhofer E.K., Wang C., Shippy R., Harris S.C., Zhang L., Mei N., Chen T., Herman D., Goodsaid F.M., Hurban P., Phillips K.L., Xu J., Deng X., Sun Y.A., Tong W., Dragan Y.P., Shi L. Rat toxicogenomic study reveals analytical consistency across microarray platforms. Nat. Biotechnol. 2006, 24(9):1162-1169.
14. Iritani S., Niizato K., Nawa H., Ikeda K., Emson P.C. Immunohistochemical study of brain-derived neurotrophic factor and its receptor, TrkB, in the hippocampal formation of schizophrenic brains. Prog. Neuropsychopharmacol. Biol. Psychiatry 2003, 27(5):801-807.
15. James S.H., Schnoll S.H. Phencyclidine: tissue distribution in the rat. Clin. Toxicol. 1976, 9(4):573-582.
16. Javitt D.C., Zukin S.R. Recent advances in the phencyclidine model of schizophrenia. Am. J. Psychiatry 1991, 148(10):1301-1308.
17. Jentsch J.D., Redmond D.E., Elsworth J.D., Taylor J.R., Youngren K.D., Roth R.H. Enduring cognitive deficits and cortical dopamine dysfunction in monkeys after long-term administration of phencyclidine. Science 1997, 277(5328):953-955.
18. Jiang X., Tian F., Du Y., Copeland N.G., Jenkins N.A., Tessarollo L., Wu X., Pan H., Hu X.Z., Xu K., Kenney H., Egan S.E., Turley H., Harris A.L., Marini A.M., Lipsky R.H. BHLHB2 controls Bdnf promoter 4 activity and neuronal excitability. J. Neurosci. 2008, 28(5):1118-1130.
19. Johnson K.M., Phillips M., Wang C., Kevetter G.A. Chronic phencyclidine induces behavioral sensitization and apoptotic cell death in the olfactory and piriform cortex. J. Neurosci. Res. 1998, 52(6):709-722.
20. Kafitz K.W., Rose C.R., Thoenen H., Konnerth A. Neurotrophin-evoked rapid excitation through TrkB receptors. Nature 1999, 401(6756):918-921.
21. Kalkman H.O. The role of the phosphatidylinositide 3-kinase-protein kinase B pathway in schizophrenia. Pharmacol. Ther. 2006, 110(1):117-134.
22. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 1996, 274(5290):1133-1138.
23. Kim J.S., Kornhuber H.H., Schmid-Burgk W., Holzmuller B. Low cerebrospinal fluid glutamate in schizophrenic patients and a new hypothesis on schizophrenia. Neurosci. Lett. 1980, 20(3):379-382.
24. Lahti A.C., Koffel B., LaPorte D., Tamminga C.A. Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology 1995, 13(1):9-19.
25. Lindholm D., Carroll P., Tzimagiogis G., Thoenen H. Autocrine-paracrine regulation of hippocampal neuron survival by IGF-1 and the neurotrophins BDNF, NT-3 and NT-4. Eur. J. Neurosci. 1996, 8(7):1452-1460.
26. Lipska B.K., Khaing Z.Z., Weickert C.S., Weinberger D.R. BDNF mRNA expression in rat hippocampus and prefrontal cortex: effects of neonatal ventral hippocampal damage and antipsychotic drugs. Eur. J. Neurosci. 2001, 14(1):135-144.
27. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) method. Methods 2001, 25(4):402-408.
28. Lu B., Figurov A. Role of neurotrophins in synapse development and plasticity. Rev. Neurosci. 1997, 8(1):1-12.
29. Malhotra A.K., Pinals D.A., Adler C.M., Elman I., Clifton A., Pickar D., Breier A. Ketamine-induced exacerbation of psychotic symptoms and cognitive impairment in neuroleptic-free schizophrenics. Neuropsychopharmacology 1997, 17(3):141-150.
30. Marcotte E.R., Pearson D.M., Srivastava L.K. Animal models of schizophrenia: a critical review. J. Psychiatry Neurosci. 2001, 26(5):395-410.
31. Marini A.M., Rabin S.J., Lipsky R.H., Mocchetti I. Activity-dependent release of brain-derived neurotrophic factor underlies the neuroprotective effect of N-methyl-d-aspartate. J. Biol. Chem. 1998, 273(45):29394-29399.
32. Murray R.M., O'Callaghan E., Castle D.J., Lewis S.W. A neurodevelopmental approach to the classification of schizophrenia. Schizophr. Bull. 1992, 18(2):319-332.
33. Olney J.W., Farber N.B. Glutamate receptor dysfunction and schizophrenia. Arch. Gen. Psychiatry 1995, 52(12):998-1007.
34. Papadia S., Soriano F.X., Leveille F., Martel M.A., Dakin K.A., Hansen H.H., Kaindl A., Sifringer M., Fowler J., Stefovska V., McKenzie G., Craigon M., Corriveau R., Ghazal P., Horsburgh K., Yankner B.A., Wyllie D.J., Ikonomidou C., Hardingham G.E. Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat. Neurosci. 2008, 11(4):476-487.
35. Petersen A.A., Larsen K.E., Behr G.G., Romero N., Przedborski S., Brundin P., Sulzer D. Brain-derived neurotrophic factor inhibits apoptosis and dopamine-induced free radical production in striatal neurons but does not prevent cell death. Brain Res. Bull. 2001, 56(3-4):331-335.
36. Pilowsky L.S., Kerwin R.W., Murray R.M. Schizophrenia: a neurodevelopmental perspective. Neuropsychopharmacology 1993, 9(1):83-91.
37. Reich D.L., Silvay G. Ketamine: an update on the first twenty-five years of clinical experience. Can. J. Anaesth. 1989, 36(2):186-197.
38. Reynolds G.P., Harte M.K. The neuronal pathology of schizophrenia: molecules and mechanisms. Biochem. Soc. Trans. 2007, 35(Pt 2):433-436.
39. Rossner M.J., Dorr J., Gass P., Schwab M.H., Nave K.A. SHARPs: mammalian enhancer-of-split- and hairy-related proteins coupled to neuronal stimulation. Mol. Cell. Neurosci. 1997, 10(3-4):460-475.
40. Sawa A., Snyder S.H. Schizophrenia: diverse approaches to a complex disease. Science 2002, 296(5568):692-695.
41. Schmued L.C., Hopkins K.J. Fluoro-Jade: novel fluorochromes for detecting toxicant-induced neuronal degeneration. Toxicol. Pathol. 2000, 28(1):91-99.
42. Schulze P.C., Yoshioka J., Takahashi T., He Z., King G.L., Lee R.T. Hyperglycemia promotes oxidative stress through inhibition of thioredoxin function by thioredoxin-interacting protein. J. Biol. Chem. 2004, 279(29):30369-30374.
43. Schwartz P.M., Borghesani P.R., Levy R.L., Pomeroy S.L., Segal R.A. Abnormal cerebellar development and foliation in BDNF-/- mice reveals a role for neurotrophins in CNS patterning. Neuron 1997, 19(2):269-281.
44. Shi L., Reid L.H., Jones W.D., Shippy R., Warrington J.A., Baker S.C., Collins P.J., de Longueville F., Kawasaki E.S., Lee K.Y., Luo Y., Sun Y.A., Willey J.C., Setterquist R.A., Fischer G.M., Tong W., Dragan Y.P., Dix D.J., Frueh F.W., Goodsaid F.M., Herman D., Jensen R.V., Johnson C.D., Lobenhofer E.K., Puri R.K., Schrf U., Thierry-Mieg J., Wang C., Wilson M., Wolber P.K., Zhang L., Amur S., Bao W., Barbacioru C.C., Lucas A.B., Bertholet V., Boysen C., Bromley B., Brown D., Brunner A., Canales R., Cao X.M., Cebula T.A., Chen J.J., Cheng J., Chu T.M., Chudin E., Corson J., Corton J.C., Croner L.J., Davies C., Davison T.S., Delenstarr G., Deng X., Dorris D., Eklund A.C., Fan X.H., Fang H., Fulmer-Smentek S., Fuscoe J.C., Gallagher K., Ge W., Guo L., Guo X., Hager J., Haje P.K., Han J., Han T., Harbottle H.C., Harris S.C., Hatchwell E., Hauser C.A., Hester S., Hong H., Hurban P., Jackson S.A., Ji H., Knight C.R., Kuo W.P., LeClerc J.E., Levy S., Li Q.Z., Liu C., Liu Y., Lombardi M.J., Ma Y., Magnuson S.R., Maqsodi B., McDaniel T., Mei N., Myklebost O., Ning B., Novoradovskaya N., Orr M.S., Osborn T.W., Papallo A., Patterson T.A., Perkins R.G., Peters E.H., Peterson R., Philips K.L., Pine P.S., Pusztai L., Qian F., Ren H., Rosen M., Rosenzweig B.A., Samaha R.R., Schena M., Schroth G.P., Shchegrova S., Smith D.D., Staedtler F., Su Z., Sun H., Szallasi Z., Tezak Z., Thierry-Mieg D., Thompson K.L., Tikhonova I., Turpaz Y., Vallanat B., Van C., Walker S.J., Wang S.J., Wang Y., Wolfinger R., Wong A., Wu J., Xiao C., Xie Q., Xu J., Yang W., Zhang L., Zhong S., Zong Y., Slikker W. The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements. Nat. Biotechnol. 2006, 24(9):1151-1161.
45. Shi L., Jones W.D., Jensen R.V., Harris S.C., Perkins R.G., Goodsaid F.M., Guo L., Croner L.J., Boysen C., Fang H., Qian F., Amur S., Bao W., Barbacioru C.C., Bertholet V., Cao X.M., Chu T.M., Collins P.J., Fan X.H., Frueh F.W., Fuscoe J.C., Guo X., Han J., Herman D., Hong H., Kawasaki E.S., Li Q.Z., Luo Y., Ma Y., Mei N., Peterson R.L., Puri R.K., Shippy R., Su Z., Sun Y.A., Sun H., Thorn B., Turpaz Y., Wang C., Wang S.J., Warrington J.A., Willey J.C., Wu J., Xie Q., Zhang L., Zhong S., Wolfinger R.D., Tong W. The balance of reproducibility, sensitivity, and specificity of lists of differentially expressed genes in microarray studies. BMC Bioinform. 2008, 9(Suppl. 9):S10.
46. Shi Q., Guo L., Patterson T.A., Dial S., Li Q., Sadovova N., Zhang X., Hanig J.P., Paule M.G., Slikker W., Wang C. Gene expression profiling in the developing rat brain exposed to ketamine. Neuroscience 2010, 166(3):852-863.
47. Snyder S.H. Phencyclidine. Nature 1980, 285(5764):355-356.
48. Spee B., Mandigers P.J., Arends B., Bode P., van den Ingh T.S., Hoffmann G., Rothuizen J., Penning L.C. Differential expression of copper-associated and oxidative stress related proteins in a new variant of copper toxicosis in Doberman pinschers. Comp. Hepatol. 2005, 4(1):3.
49. Tamminga C.A. Schizophrenia and glutamatergic transmission. Crit. Rev. Neurobiol. 1998, 12(1-2):21-36.
50. Tenkova T., Young C., Dikranian K., Labruyere J., Olney J.W. Ethonal-induced apoptosis in the developing visual system during synaptogesis. Invest. ophthalmol. Vis. Sci. 2003, 44:2809-2817.
51. Thoenen H. Neurotrophins and neuronal plasticity. Science 1995, 270(5236):593-598.
52. Thome J., Foley P., Riederer P. Neurotrophic factors and the maldevelopmental hypothesis of schizophrenic psychoses. Review article. J. Neural Transm. 1998, 105(1):85-100.
53. Toyooka K., Asama K., Watanabe Y., Muratake T., Takahashi M., Someya T., Nawa H. Decreased levels of brain-derived neurotrophic factor in serum of chronic schizophrenic patients. Psychiatry Res. 2002, 110(3):249-257.
54. Wang C., Kaufmann J.A., Sanchez-Ross M.G., Johnson K.M. Mechanisms of N-methyl-d-aspartate-induced apoptosis in phencyclidine-treated cultured forebrain neurons. J. Pharmacol. Exp. Ther. 2000, 294(1):287-295.
55. Wang C., McInnis J., Ross-Sanchez M., Shinnick-Gallagher P., Wiley J.L., Johnson K.M. Long-term behavioral and neurodegenerative effects of perinatal phencyclidine administration: implications for schizophrenia. Neuroscience 2001, 107(4):535-550.
56. Wang C., McInnis J., West J.B., Bao J., Anastasio N., Guidry J.A., Ye Y., Salvemini D., Johnson K.M. Blockade of phencyclidine-induced cortical apoptosis and deficits in prepulse inhibition by M40403, a superoxide dismutase mimetic. J. Pharmacol. Exp. Ther. 2003, 304(1):266-271.
57. Weinberger D.R. Implications of normal brain development for the pathogenesis of schizophrenia. Arch. Gen. Psychiatry 1987, 44(7):660-669.
58. Welch M.J., Correa G.A. PCP intoxication in young children and infants. Clin. Pediatr. (Phila) 1980, 19(8):510-514.
59. Yoshida T., Nakamura H., Masutani H., Yodoi J. The involvement of thioredoxin and thioredoxin binding protein-2 on cellular proliferation and aging process. Ann. N.Y. Acad. Sci. 2005, 1055:1-12.