Schizophrenia Research
Volume 120, Issue 1 , Pages 150-158 , July 2010

Gene expression abnormalities and oligodendrocyte deficits in the internal capsule in schizophrenia

  • David Kerns

      Affiliations

    • J.J. Peters VA Medical Center, 130 West Kingsbridge Ave., Bronx, New York, NY 10468, United States
  • ,
  • Ghe S. Vong

      Affiliations

    • J.J. Peters VA Medical Center, 130 West Kingsbridge Ave., Bronx, New York, NY 10468, United States
  • ,
  • Kevin Barley

      Affiliations

    • J.J. Peters VA Medical Center, 130 West Kingsbridge Ave., Bronx, New York, NY 10468, United States
  • ,
  • Stella Dracheva

      Affiliations

    • J.J. Peters VA Medical Center, 130 West Kingsbridge Ave., Bronx, New York, NY 10468, United States
    • Department of Psychiatry Mount Sinai School of Medicine, One Gustave Levy Place, New York, NY 10029, United States
  • ,
  • Pavel Katsel

      Affiliations

    • J.J. Peters VA Medical Center, 130 West Kingsbridge Ave., Bronx, New York, NY 10468, United States
    • Department of Psychiatry Mount Sinai School of Medicine, One Gustave Levy Place, New York, NY 10029, United States
  • ,
  • Patrizia Casaccia

      Affiliations

    • Department of Psychiatry Mount Sinai School of Medicine, One Gustave Levy Place, New York, NY 10029, United States
  • ,
  • Vahram Haroutunian

      Affiliations

    • J.J. Peters VA Medical Center, 130 West Kingsbridge Ave., Bronx, New York, NY 10468, United States
    • Department of Psychiatry Mount Sinai School of Medicine, One Gustave Levy Place, New York, NY 10029, United States
  • ,
  • William Byne

      Affiliations

    • J.J. Peters VA Medical Center, 130 West Kingsbridge Ave., Bronx, New York, NY 10468, United States
    • Department of Psychiatry Mount Sinai School of Medicine, One Gustave Levy Place, New York, NY 10029, United States
    • Corresponding Author InformationCorresponding author. Fax: +1 718 741 4207.

Received 5 February 2010 ,Accepted 22 April 2010.

References 

  1. Ardekani BA, Nierenberg J, Hoptman MJ, Javitt DC, Lim KO. MRI study of white matter diffusion anisotropy in schizophrenia. NeuroReport. 2003;14:2025–2029
  2. Aston C, Jiang L, Sokolov BP. Microarray analysis of postmortem temporal cortex from patients with schizophrenia. J. Neurosci. Res. 2004;77:858–866
  3. Bansal R, Marin-Husstege M, Bryant M, Casaccia-Bonnefil P. S-phase entry of oligodendrocyte lineage cells is associated with increased levels of p21Cip1. J. Neurosci. Res. 2005;80:360–368
  4. Barley K, Dracheva S, Byne W. Subcortical oligodendrocyte- and astrocyte-associated gene expression in subjects with schizophrenia, major depression and bipolar disorder. Schizophr. Res. 2009;112:54–64
  5. Beaulieu C. The basis of anisotropic water diffusion in the nervous system — a technical review. NMR Biomed. 2002;15:435–455
  6. Brosnan CF, John GR. Revisiting Notch in remyelination of multiple sclerosis lesions. J. Clin. Invest. 2009;119:10–13
  7. Buchsbaum MS, Tang CY, Peled S, Gudbjartsson H, Lu D, Hazlett EA, et al. MRI white matter diffusion anisotropy and PET metabolic rate in schizophrenia. NeuroReport. 1998;9:425–430
  8. Butts BD, Houde C, Mehmet H. Maturation-dependent sensitivity of oligodendrocyte lineage cells to apoptosis: implications for normal development and disease. Cell Death Differ. 2008;15:1178–1186
  9. Byne W, Kidkardnee S, Tatusov A, Yiannoulos G, Buchsbaum MS, Haroutunian V. Schizophrenia-associated reduction of neuronal and oligodendrocyte numbers in the anterior principal thalamic nucleus. Schizophr. Res. 2006;85:245–253
  10. Byne W, Tatusov A, Yiannoulos G, Vong GS, Marcus S. Effects of mental illness and aging in two thalamic nuclei. Schizophr. Res. 2008;106:172–181
  11. Carmen J, Magnus T, Cassiani-Ingoni R, Sherman L, Rao MS, Mattson MP. Revisiting the astrocyte–oligodendrocyte relationship in the adult CNS. Prog. Neurobiol. 2007;82:151–162
  12. Cheung V, Cheung C, McAlonan GM, Deng Y, Wong JG, Yip L, et al. A diffusion tensor imaging study of structural dysconnectivity in never-medicated, first-episode schizophrenia. Psychol. Med. 2008;38:877–885
  13. Cui XY, Hu QD, Tekaya M, Shimoda Y, Ang BT, Nie DY, et al. NB-3/Notch1 pathway via Deltex1 promotes neural progenitor cell differentiation into oligodendrocytes. J. Biol. Chem. 2004;279:25858–25865
  14. Dawson MR, Levine JM, Reynolds R. NG2-expressing cells in the central nervous system: are they oligodendroglial progenitors?. J. Neurosci. Res. 2000;61:471–479
  15. Di X, Chan RC, Gong QY. White matter reduction in patients with schizophrenia as revealed by voxel-based morphometry: an activation likelihood estimation meta-analysis. Prog. Neuropsychopharmacol. Biol. Psychiatry. 2009;33:1390–1394
  16. Dracheva S, Davis KL, Chin B, Woo DA, Schmeidler J, Haroutunian V. Myelin-associated mRNA and protein expression deficits in the anterior cingulate cortex and hippocampus in elderly schizophrenia patients. Neurobiol. Dis. 2006;21:531–540
  17. Geha S, Pallud J, Junier MP, Devaux B, Leonard N, Chassoux F, et al. NG2+/Olig2+ cells are the major cycle-related cell population of the adult human normal brain. Brain Pathol. 2010;20:399–411
  18. Hakak Y, Walker JR, Li C, Wong WH, Davis KL, Buxbaum JD, et al. Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 2001;98:4746–4751
  19. Haroutunian V, Katsel P, Dracheva S, Stewart DG, Davis KL. Variations in oligodendrocyte-related gene expression across multiple cortical regions: implications for the pathophysiology of schizophrenia. Int. J. Neuropsychopharmacol. 2007;10:565–573
  20. Hashimoto K, Shimizu E, Komatsu N, Nakazato M, Okamura N, Watanabe H, et al. Increased levels of serum basic fibroblast growth factor in schizophrenia. Psychiatry Res. 2003;120:211–218
  21. Hu QD, Ang BT, Karsak M, Hu WP, Cui XY, Duka T, et al. F3/contactin acts as a functional ligand for Notch during oligodendrocyte maturation. Cell. 2003;115:163–175
  22. Hu QD, Ma QH, Gennarini G, Xiao ZC. Cross-talk between F3/contactin and Notch at axoglial interface: a role in oligodendrocyte development. Dev. Neurosci. 2006;28:25–33
  23. John GR, Shankar SL, Shafit-Zagardo B, Massimi A, Lee SC, Raine CS, et al. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat. Med. 2002;8:1115–1121
  24. Kanaan RA, Kim JS, Kaufmann WE, Pearlson GD, Barker GJ, McGuire PK. Diffusion tensor imaging in schizophrenia. Biol. Psychiatry. 2005;58:921–929
  25. Katsel P, Davis KL, Haroutunian V. Variations in myelin and oligodendrocyte-related gene expression across multiple brain regions in schizophrenia: a gene ontology study. Schizophr. Res. 2005;79:157–173
  26. Katsel P, Davis KL, Li C, Tan W, Greenstein E, Kleiner Hoffman LB, et al. Abnormal indices of cell cycle activity in schizophrenia and their potential association with oligodendrocytes. Neuropsychopharmacology. 2008;33:2993–3009
  27. Konopaske GT, Dorph-Petersen KA, Sweet RA, Pierri JN, Zhang W, Sampson AR, et al. Effect of chronic antipsychotic exposure on astrocyte and oligodendrocyte numbers in macaque monkeys. Biol. Psychiatry. 2008;63:759–765
  28. Kubicki M, McCarley RW, Shenton ME. Evidence for white matter abnormalities in schizophrenia. Curr. Opin. Psychiatry. 2005;18:121–134
  29. Li H, He Y, Richardson WD, Casaccia P. Two-tier transcriptional control of oligodendrocyte differentiation. Curr. Opin. Neurobiol. 2009;19:479–485
  30. Liu Z, Hu X, Cai J, Liu B, Peng X, Wegner M, et al. Induction of oligodendrocyte differentiation by Olig2 and Sox10: evidence for reciprocal interactions and dosage-dependent mechanisms. Dev. Biol. 2007;302:683–693
  31. McCullumsmith RE, Gupta D, Beneyto M, Kreger E, Haroutunian V, Davis KL, et al. Expression of transcripts for myelination-related genes in the anterior cingulate cortex in schizophrenia. Schizophr. Res. 2007;90:15–27
  32. McTigue DM, Tripathi RB. The life, death, and replacement of oligodendrocytes in the adult CNS. J. Neurochem. 2008;107:1–19
  33. Narayan S, Kass KE, Thomas EA. Chronic haloperidol treatment results in a decrease in the expression of myelin/oligodendrocyte-related genes in the mouse brain. J. Neurosci. Res. 2007;85:757–765
  34. Oh JS, Kubicki M, Rosenberger G, Bouix S, Levitt JJ, McCarley RW, et al. Thalamo-frontal white matter alterations in chronic schizophrenia: a quantitative diffusion tractography study. Hum. Brain Mapp. 2009;30:3812–3825
  35. Peters A, Verderosa A, Sethares C. The neuroglial population in the primary visual cortex of the aging rhesus monkey. Glia. 2008;56:1151–1161
  36. Roberts JM. Evolving ideas about cyclins. Cell. 1999;98:129–132
  37. Sherr CJ, Roberts . Mammalian G1 cyclins and cell cycle progression. Proc. Assoc. Am. Physicians. 1995;181–186
  38. Stephan KE, Friston KJ, Frith CD. Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophr. Bull. 2009;35:509–527
  39. Stolt CC, Rehberg S, Ader M, Lommes P, Riethmacher D, Schachner M, et al. Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev. 2002;16:165–170
  40. Tkachev D, Mimmack ML, Ryan MM, Wayland M, Freeman T, Jones PB, et al. Oligodendrocyte dysfunction in schizophrenia and bipolar disorder. Lancet. 2003;362:798–805
  41. Torrey EF, Webster M, Knable M, Johnston N, Yolken RH. The stanley foundation brain collection and neuropathology consortium. Schizophr. Res. 2000;44:151–155
  42. Uranova N, Orlovskaya D, Vikhreva O, Zimina I, Kolomeets N, Vostrikov V, et al. Electron microscopy of oligodendroglia in severe mental illness. Brain Res. Bull. 2001;55:597–610
  43. Uranova NA, Vostrikov VM, Orlovskaya DD, Rachmanova VI. Oligodendroglial density in the prefrontal cortex in schizophrenia and mood disorders: a study from the Stanley Neuropathology Consortium. Schizophr. Res. 2004;67:269–275
  44. Vostrikov VM, Uranova NA, Orlovskaya DD. Deficit of perineuronal oligodendrocytes in the prefrontal cortex in schizophrenia and mood disorders. Schizophr. Res. 2007;94:273–280
  45. Wang S, Sdrulla AD, diSibio G, Bush G, Nofziger D, Hicks C, et al. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron. 1998;21:63–75
  46. West MJ, Slomianka L, Gundersen HJG. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 1991;231:482–497
  47. Wu Y, Liu Y, Levine EM, Rao MS. Hes1 but not Hes5 regulates an astrocyte versus oligodendrocyte fate choice in glial restricted precursors. Dev. Dyn. 2003;226:675–689
  48. Yamamoto N, Yamamoto S, Inagaki F, Kawaichi M, Fukamizu A, Kishi N, et al. Role of Deltex-1 as a transcriptional regulator downstream of the Notch receptor. J. Biol. Chem. 2001;276:45031–45040
  49. Young KA, Holcomb LA, Yazdani U, Hicks PB, German DC. Elevated neuron number in the limbic thalamus in major depression. Am. J. Psychiatry. 2004;161:1270–1277
  50. Zezula J, Casaccia-Bonnefil P, Ezhevsky SA, Osterhout DJ, Levine JM, Dowdy SF, et al. p21cip1 is required for the differentiation of oligodendrocytes independently of cell cycle withdrawal. EMBO Rep. 2001;2:27–34
  51. Zhong W, Jiang MM, Weinmaster G, Jan LY, Jan YN. Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development. 1997;124:1887–1897

PII: S0920-9964(10)01265-X

doi: 10.1016/j.schres.2010.04.012

Schizophrenia Research
Volume 120, Issue 1 , Pages 150-158 , July 2010