Downregulation of oligodendrocyte transcripts is associated with impaired prefrontal cortex function in rats

Schizophrenia Research

Volumn 113, Issue 2-3, 2009, Pages 277-287

  Gregg, Justin R ^a   Herring, Nicole R ^a   Naydenov, Alipi V ^a   Hanlin, Ryan P ^a   Konradi, Christine ^a,b  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Adolescence; Attentional set shifting task; Hippocampus; Oligodendrocytes; Prefrontal cortex; Schizophrenia

Indexed keywords

CUPRIZONE; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE MODEL; DOWN REGULATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HIPPOCAMPUS; MALE; NONHUMAN; OLIGODENDROGLIA; PATHOGENESIS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SCHIZOPHRENIA; WISCONSIN CARD SORTING TEST;

AGE FACTORS; ANIMALS; ATTENTION; BODY WEIGHT; CORPUS STRIATUM; CUPRIZONE; DOWN-REGULATION; EATING; GENE EXPRESSION PROFILING; HIPPOCAMPUS; LOCOMOTION; MALE; MONOAMINE OXIDASE INHIBITORS; NEUROPSYCHOLOGICAL TESTS; OLIGODENDROGLIA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; STARTLE REACTION;

EID: 68049116921     PISSN: 09209964     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.schres.2009.05.023     Document Type: Article

References (74)

1. Adamo A.M., Paez P.M., Escobar Cabrera O.E., Wolfson M., Franco P.G., Pasquini J.M., and Soto E.F. Remyelination after cuprizone-induced demyelination in the rat is stimulated by apotransferrin. Exp. Neurol. 198 (2006) 519-529
2. Bagary M.S., Symms M.R., Barker G.J., Mutsatsa S.H., Joyce E.M., and Ron M.A. Gray and white matter brain abnormalities in first-episode schizophrenia inferred from magnetization transfer imaging. Arch. Gen. Psychiatry 60 (2003) 779-788
3. Barch D.M. The cognitive neuroscience of schizophrenia. Annu. Rev. Clin. Psychol. 1 (2005) 321-353
4. Benjamini Y., and Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc., Ser. B Stat. Methodol. 57 (1995) 289-300
5. Berman K.F., Zec R.F., and Weinberger D.R. Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia. II. Role of neuroleptic treatment, attention, and mental effort. Arch. Gen. Psychiatry 43 (1986) 126-135
6. Birrell J.M., and Brown V.J. Medial frontal cortex mediates perceptual attentional set shifting in the rat. J. Neurosci. 20 (2000) 4320-4324
7. Black Y.D., Maclaren F.R., Naydenov A.V., Carlezon Jr. W.A., Baxter M.G., and Konradi C. Altered attention and prefrontal cortex gene expression in rats after binge-like exposure to cocaine during adolescence. J. Neurosci. 26 (2006) 9656-9665
8. Blakemore W.F. Observations on oligodendrocyte degeneration, the resolution of status spongiosus and remyelination in cuprizone intoxication in mice. J. Neurocytol. 1 (1972) 413-426
9. Blakemore W.F. Remyelination of the superior cerebellar peduncle in the mouse following demyelination induced by feeding cuprizone. J. Neurol. Sci. 20 (1973) 73-83
10. Boeker H., Kleiser M., Lehman D., Jaenke L., Bogerts B., and Northoff G. Executive dysfunction, self, and ego pathology in schizophrenia: an exploratory study of neuropsychology and personality. Compr. Psychiatry 47 (2006) 7-19
11. Bolstad B.M., Irizarry R.A., Astrand M., and Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19 (2003) 185-193
12. Breier A., Buchanan R.W., Elkashef A., Munson R.C., Kirkpatrick B., and Gellad F. Brain morphology and schizophrenia. A magnetic resonance imaging study of limbic, prefrontal cortex, and caudate structures. Arch. Gen. Psychiatry 49 (1992) 921-926
13. Buchanan R.W., Vladar K., Barta P.E., and Pearlson G.D. Structural evaluation of the prefrontal cortex in schizophrenia. Am. J. Psychiatry 155 (1998) 1049-1055
14. Carpenter W.T., and Koenig J.I. The evolution of drug development in schizophrenia: past issues and future opportunities. Neuropsychopharmacology 33 (2008) 2061-2079
15. Davis K.L., Stewart D.G., Friedman J.I., Buchsbaum M., Harvey P.D., Hof P.R., Buxbaum J., and Haroutunian V. White matter changes in schizophrenia: evidence for myelin-related dysfunction. Arch. Gen. Psychiatry 60 (2003) 443-456
16. de Bie P., Muller P., Wijmenga C., and Klomp L.W. Molecular pathogenesis of Wilson and Menkes disease: correlation of mutations with molecular defects and disease phenotypes. J. Med. Genet. 44 (2007) 673-688
17. Dennis Jr. G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., and Lempicki R.A. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4 (2003) P3
18. Dias R., Robbins T.W., and Roberts A.C. Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380 (1996) 69-72
19. Dias R., Robbins T.W., and Roberts A.C. Primate analogue of the Wisconsin Card Sorting Test: effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behav. Neurosci. 110 (1996) 872-886
20. Dias R., Robbins T.W., and Roberts A.C. Dissociable forms of inhibitory control within prefrontal cortex with an analog of the Wisconsin Card Sort Test: restriction to novel situations and independence from "on-line" processing. J. Neurosci. 17 (1997) 9285-9297
21. Dwork A.J., Mancevski B., and Rosoklija G. White matter and cognitive function in schizophrenia. Int. J. Neuropsychopharmacol. 10 (2007) 513-536
22. Eisen M.B., Spellman P.T., Brown P.O., and Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 14863-14868
23. Feinstein A. Neuropsychiatric syndromes associated with multiple sclerosis. J. Neurol. 254 Suppl 2 (2007) II73-II76
24. Fields R.D. White matter in learning, cognition and psychiatric disorders. Trends Neurosci. 31 (2008) 361-370
25. Flatmark T., Kryvi H., and Tangeras A. Induction of megamitochondria by cuprizone(biscyclohexanone oxaldihydrazone). Evidence for an inhibition of the mitochondrial division process. Eur. J. Cell Biol. 23 (1980) 141-148
26. Franke P., Maier W., Hain C., and Klingler T. Wisconsin Card Sorting Test: an indicator of vulnerability to schizophrenia?. Schizophr. Res. 6 (1992) 243-249
27. Green M.F., Kern R.S., Braff D.L., and Mintz J. Neurocognitive deficits and functional outcome in schizophrenia: are we measuring the "right stuff"?. Schizophr. Bull. 26 (2000) 119-136
28. Hakak Y., Walker J.R., Li C., Wong W.H., Davis K.L., Buxbaum J.D., Haroutunian V., and Fienberg A.A. Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 4746-4751
29. Haroutunian V., Katsel P., Dracheva S., Stewart D.G., and Davis K.L. Variations in oligodendrocyte-related gene expression across multiple cortical regions: implications for the pathophysiology of schizophrenia. Int. J. Neuropsychopharmacol. 10 (2007) 565-573
30. Harrison M.D., Jones C.E., Solioz M., and Dameron C.T. Intracellular copper routing: the role of copper chaperones. Trends Biochem. Sci. 25 (2000) 29-32
31. Haut M.W., Cahill J., Cutlip W.D., Stevenson J.M., Makela E.H., and Bloomfield S.M. On the nature of Wisconsin Card Sorting Test performance in schizophrenia. Psychiatry Res. 65 (1996) 15-22
32. Hiremath M.M., Saito Y., Knapp G.W., Ting J.P., Suzuki K., and Matsushima G.K. Microglial/macrophage accumulation during cuprizone-induced demyelination in C57BL/6 mice. J. Neuroimmunol. 92 (1998) 38-49
33. Hosack D., Dennis G., Sherman B., Lane H., and Lempicki R. Identifying biological themes within lists of genes with EASE. Genome Biol. 4 (2003) P4
34. Hyde T.M., Ziegler J.C., and Weinberger D.R. Psychiatric disturbances in metachromatic leukodystrophy. Insights into the neurobiology of psychosis. Arch. Neurol. 49 (1992) 401-406
35. Irizarry R.A., Hobbs B., Collin F., Beazer-Barclay Y.D., Antonellis K.J., Scherf U., and Speed T.P. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4 (2003) 249-264
36. Karoutzou G., Emrich H.M., and Dietrich D.E. The myelin-pathogenesis puzzle in schizophrenia: a literature review. Mol. Psychiatry 13 (2008) 245-260
37. Kim B.E., Nevitt T., and Thiele D.J. Mechanisms for copper acquisition, distribution and regulation. Nat. Chem. Biol. 4 (2008) 176-185
38. Komoly S., Hudson L.D., Webster H.D., and Bondy C.A. Insulin-like growth factor I gene expression is induced in astrocytes during experimental demyelination. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 1894-1898
39. Konradi C. Gene expression microarray studies in polygenic psychiatric disorders: applications and data analysis. Brain Res. Brain Res. Rev. 50 (2005) 142-155
40. Li C., and Wong W.H. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 31-36
41. Love S. Cuprizone neurotoxicity in the rat: morphologic observations. J. Neurol. Sci. 84 (1988) 223-237
42. Ludwin S.K. Central nervous system demyelination and remyelination in the mouse: an ultrastructural study of cuprizone toxicity. Lab. Invest. 39 (1978) 597-612
43. Mason J.L., Ye P., Suzuki K., D'Ercole A.J., and Matsushima G.K. Insulin-like growth factor-1 inhibits mature oligodendrocyte apoptosis during primary demyelination. J. Neurosci. 20 (2000) 5703-5708
44. Mason J.L., Xuan S., Dragatsis I., Efstratiadis A., and Goldman J.E. Insulin-like growth factor (IGF) signaling through type 1 IGF receptor plays an important role in remyelination. J. Neurosci. 23 (2003) 7710-7718
45. Matsushima G.K., and Morell P. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol. 11 (2001) 107-116
46. McAlonan K., and Brown V.J. Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behav. Brain Res. 146 (2003) 97-103
47. Menkes J.H., Alter M., Steigleder G.K., Weakley D.R., and Sung J.H. A sex-linked recessive disorder with retardation of growth, peculiar hair, and focal cerebral and cerebellar degeneration. Pediatrics 29 (1962) 764-779
48. Messori L., Casini A., Gabbiani C., Sorace L., Muniz-Miranda M., and Zatta P. Unravelling the chemical nature of copper cuprizone. Dalton Trans. (2007) 2112-2114
49. Miller E.K., and Cohen J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24 (2001) 167-202
50. Mimmack M.L., Ryan M., Baba H., Navarro-Ruiz J., Iritani S., Faull R.L., McKenna P.J., Jones P.B., Arai H., Starkey M., Emson P.C., and Bahn S. Gene expression analysis in schizophrenia: reproducible up-regulation of several members of the apolipoprotein L family located in a high-susceptibility locus for schizophrenia on chromosome 22. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 4680-4685
51. Morell P., Barrett C.V., Mason J.L., Toews A.D., Hostettler J.D., Knapp G.W., and Matsushima G.K. Gene expression in brain during cuprizone-induced demyelination and remyelination. Mol. Cell. Neurosci. 12 (1998) 220-227
52. Mueser K.T., and McGurk S.R. Schizophrenia. Lancet 363 (2004) 2063-2072
53. Pasquini L.A., Calatayud C.A., Bertone Una A.L., Millet V., Pasquini J.M., and Soto E.F. The neurotoxic effect of cuprizone on oligodendrocytes depends on the presence of pro-inflammatory cytokines secreted by microglia. Neurochem. Res. 32 (2007) 279-292
54. Paxinos G., and Watson C. In: The Rat Brain in Stereotaxic Coordinates (1986), Academic, San Diego
55. Petronilli V., and Zoratti M. A characterization of cuprizone-induced giant mouse liver mitochondria. J. Bioenerg. Biomembranes 22 (1990) 663-677
56. Prohaska J.R., and Smith T.L. Effect of dietary or genetic copper deficiency on brain catecholamines, trace metals and enzymes in mice and rats. J. Nutr. 112 (1982) 1706-1717
57. Puig S., and Thiele D.J. Molecular mechanisms of copper uptake and distribution. Curr Opin Chem Biol 6 (2002) 171-180
58. Purves D.C., Garrod I.J., and Dayan A.D. A comparison of spongiosis induced in the brain by hexachlorophene, cuprizone and triethyl tin in the Sprague-Dawley rat. Human Exp. Toxicol. 10 (1991) 439-444
59. Remington L.T., Babcock A.A., Zehntner S.P., and Owens T. Microglial recruitment, activation, and proliferation in response to primary demyelination. Am. J. Pathol. 170 (2007) 1713-1724
60. Ridderinkhof K.R., van den Wildenberg W.P., Segalowitz S.J., and Carter C.S. Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain Cogn. 56 (2004) 129-140
61. Salomonis N., Hanspers K., Zambon A.C., Vranizan K., Lawlor S.C., Dahlquist K.D., Doniger S.W., Stuart J., Conklin B.R., and Pico A.R. GenMAPP 2: new features and resources for pathway analysis. BMC Bioinformatics 8 (2007) 217
62. Sanfilipo M., Lafargue T., Rusinek H., Arena L., Loneragan C., Lautin A., Feiner D., Rotrosen J., and Wolkin A. Volumetric measure of the frontal and temporal lobe regions in schizophrenia: relationship to negative symptoms. Arch. Gen. Psychiatry 57 (2000) 471-480
63. Seiwa C., Yamamoto M., Tanaka K., Fukutake M., Ueki T., Takeda S., Sakai R., Ishige A., Watanabe K., Akita M., Yagi T., Tanaka K., and Asou H. Restoration of FcRgamma/Fyn signaling repairs central nervous system demyelination. J. Neurosci. Res. 85 (2007) 954-966
64. Sigmundsson T., Suckling J., Maier M., Williams S., Bullmore E., Greenwood K., Fukuda R., Ron M., and Toone B. Structural abnormalities in frontal, temporal, and limbic regions and interconnecting white matter tracts in schizophrenic patients with prominent negative symptoms. Am. J. Psychiatry 158 (2001) 234-243
65. Skripuletz T., Lindner M., Kotsiari A., Garde N., Fokuhl J., Linsmeier F., Trebst C., and Stangel M. Cortical demyelination is prominent in the murine cuprizone model and is strain-dependent. Am. J. Pathol. 172 (2008) 1053-1061
66. Sokolov B.P. Oligodendroglial abnormalities in schizophrenia, mood disorders and substance abuse. Comorbidity, shared traits, or molecular phenocopies?. Int. J. Neuropsychopharmacol. 10 (2007) 547-555
67. Stewart D.G., and Davis K.L. Possible contributions of myelin and oligodendrocyte dysfunction to schizophrenia. Int. Rev. Neurobiol. 59 (2004) 381-424
68. Stidworthy M.F., Genoud S., Suter U., Mantei N., and Franklin R.J. Quantifying the early stages of remyelination following cuprizone-induced demyelination. Brain Pathol. 13 (2003) 329-339
69. Uranova N., Orlovskaya D., Vikhreva O., Zimina I., Kolomeets N., Vostrikov V., and Rachmanova V. Electron microscopy of oligodendroglia in severe mental illness. Brain Res. Bull. 55 (2001) 597-610
70. Uranova N.A., Vostrikov V.M., Vikhreva O.V., Zimina I.S., Kolomeets N.S., and Orlovskaya D.D. The role of oligodendrocyte pathology in schizophrenia. Int. J. Neuropsychopharmacol. 10 (2007) 537-545
71. Vertes R.P. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142 (2006) 1-20
72. Vostrikov V.M., Uranova N.A., and Orlovskaya D.D. Deficit of perineuronal oligodendrocytes in the prefrontal cortex in schizophrenia and mood disorders. Schizophr. Res. 94 (2007) 273-280
73. Xiao L., Xu H., Zhang Y., Wei Z., He J., Jiang W., Li X., Dyck L.E., Devon R.M., Deng Y., and Li X.M. Quetiapine facilitates oligodendrocyte development and prevents mice from myelin breakdown and behavioral changes. Mol. Psychiatry 13 (2008) 697-708
74. Zatta P., Raso M., Zambenedetti P., Wittkowski W., Messori L., Piccioli F., Mauri P.L., and Beltramini M. Copper and zinc dismetabolism in the mouse brain upon chronic cuprizone treatment. Cell. Mol. Life Sci. 62 (2005) 1502-1513