Schizophrenia Research
Volume 77, Issue 2 , Pages 229-239 , 15 September 2005

Characterization of olfactory bulb glomeruli in schizophrenia

  • Lise Rioux

      Affiliations

    • Department of Psychiatry, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA
    • Corresponding Author InformationCorresponding author. Present address: Laboratory for BioImaging and Anatomical Informatics, Department of Neurobiology and Anatomy, Drexel University College of Medicine, 2900 Queen Lane, Philadelphia, PA, 19129-1096, USA. Tel.: +1 215 991 8410; fax: +1 215 843 9367.
  • ,
  • Edward Isaac Gelber

      Affiliations

    • Department of Psychiatry, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA
  • ,
  • Leila Parand

      Affiliations

    • Department of Psychiatry, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA
  • ,
  • Hala Altaf Kazi

      Affiliations

    • Department of Psychiatry, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA
  • ,
  • Joannie Yeh

      Affiliations

    • Department of Psychiatry, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA
  • ,
  • Rebecca Wintering

      Affiliations

    • Department of Psychiatry, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA
  • ,
  • Warren Bilker

      Affiliations

    • Department of Biostatistics and Epidemiology, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA
  • ,
  • Steven Edward Arnold

      Affiliations

    • Department of Psychiatry, University of Pennsylvania School of Medicine, Philadelphia, PA 19104, USA

Received 11 January 2005 ,Revised 15 April 2005 ,Accepted 19 April 2005.

References 

  1. Alonzo JR, Brinón J, Crespo C, Bravo IG, Arévalo R, Alijón J. Chemical organization of the macake monkey olfactory bulb: II. Calretinin, calbindin D-28k, parvalbumin, and neurocalcin immunoreactivity. J. Comp. Neurol. 2001;432:389–407
  2. Arai H, Schmidt ML, Lee VM-Y, Hurtig HI, Greenberg BD, Adler CH, et al. Epitope analysis of senile plaque components in the hippocampus of patients with Parkinson's disease. Neurology. 1992;42:1315–1322
  3. Arnold SE, Rioux L. Challenges, status, and opportunities for studying developmental neuropathology in adult schizophrenia. Schizophr. Bull. 2001;27:395–416
  4. Arnold SE, Lee VMY, Gur RE, Trojanowski JQ. Abnormal expression of two microtubule-associated proteins (MAP2 and MAP5) in specific subfields of the hippocampal formation in schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 1991;88:10850–10854
  5. Arnold SE, Gur RE, Shapiro RM, Fisher KR, Moberg PJ, Gibney MR, et al. Prospective clinicopathologic studies of schizophrenia: accrual and assessment of patients. Am. J. Psychiatry. 1995;152:731–737
  6. Arnold SE, Han LY, Moberg PJ, Turetsky BI, Gur RE, Trojanowski JQ, et al. Dysregulation of olfactory receptor neuron lineage in schizophrenia. Arch. Gen. Psychiatry. 2001;58:829–835
  7. Bédard A, Parent A. Evidence of newly generated neurons in the human olfactory bulb. Dev. Brain Res. 2004;151:159–168
  8. Brewer WJ, Edwards J, Anderson V, Robinson T, Pantelis C. Neuropsychological, olfactory, and hygiene deficits in men with negative symptom schizophrenia. Biol. Psychiatry. 1996;40:1021–1031
  9. Brunner E, Domhof S, Langer F. Nonparametric Analysis of Longitudinal Data in Factorial Experiments. London: Wiley; 2001;288 pp.
  10. Carr VM, Walters E, Margolis FL, Farbman AI. An enhanced olfactory marker immunoreactivity in individual olfactory neurons following olfactory bulbectomy may be related to increased neurogenesis. J. Neurobiol. 1998;34:377–390
  11. Chien C-L, Lee T-H, Lu K-S. Distribution of neuronal intermediate filament proteins in the developing mouse olfactory system. J. Neurosci. Res. 1998;54:353–363
  12. Chuah MI, Farbman AI. Olfactory bulb increases marker protein in olfactory receptor cells. J. Neurosci. 1983;3:2197–2205
  13. Cotter D, Landau S, Beasley C, Stevenson R, Chana G, MacMillan L, et al. The density and spatial distribution of GABAergic neurons, labelled using calcium binding proteins, in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia. Biol. Psychiatry. 2002;51:377–386
  14. Deckner ML, Frisen J, Verge VM, Hokfelt T, Risling M. Localization of neurotrophin receptors in olfactory epithelium and bulb. NeuroReport. 1993;5:301–304
  15. DeFelipe J. Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J. Chem. Neuroanat. 1997;14:1–19
  16. Eastwood SL, Harrison PJ. Synaptic pathology in the anterior cingulate cortex in schizophrenia and mood disorders. A review and a Western blot study of synaptophysin, GAP-43 and the complexins. Brain Res. Bull. 2001;55:569–578
  17. Eastwood SL, Heffernan J, Harrison PJ. Chronic haloperidol treatment differentially affects the expression of synaptic and neuronal plasticity-associated genes. Mol. Psychiatry. 1997;2(4):322–329
  18. Ehrlich ME, Grillo M, Joh TH, Margolis FL, Baker H. Transneuronal regulation of neuronal specific gene expression in the mouse olfactory bulb. Brain Res. Mol. Brain Res. 1990;7:115–122
  19. Geddes J, Huws R, Pratt P. Olfactory acuity in the positive and negative syndromes of schizophrenia. Biol. Psychiatry. 1991;29:774–778
  20. Gomez G, Rawson NE, Hahn CG, Michaels R, Restrepo D. Characteristics of odorant elicited calcium changes in cultured human olfactory neurons. J. Neurosci. Res. 2000;62:737–749
  21. Gonzales ML, Silver J. Axon–glia interactions regulate ECM patterning in the postnatal rat olfactory bulb. J. Neurosci. 1994;14:6121–6131
  22. Halim ND, Weickert CS, McClintock BW, Hyde TM, Weinberger DR, Kleinman JE, et al. Presynaptic proteins in the prefrontal cortex of patients with schizophrenia and rats with abnormal prefrontal development. Mol. Psychiatry. 2003;8(9):797–810
  23. Hashimoto T, Bergen SE, Nguyen QL, Xu B, Monteggia LM, Pierri JN, et al. Relationship of brain-derived neurotrophic factor and its receptor trkB to altered inhibitory prefrontal circuitry in schizophrenia. J. Neurosci. 2005;25(2):372–383
  24. Henegar JR, Maruniak JA. Quantification of the effects of long-term unilateral naris closure on the olfactory bulbs of adult mice. Brain Res. 1991;568:230–234
  25. Holcomb JD, Mumm JS, Calof AL. Apoptosis in the neuronal lineage of the mouse olfactory epithelium: regulation in vivo and in vitro. Dev. Biol. 1995;172:307–323
  26. Honer WG, Young AH. Presynaptic proteins and schizophrenia. Int. Rev. Neurobiol. 2004;59:175–199
  27. Honer WG, Young C, Falkai P. Synaptic pathology. In:  Harrison P,  Roberts J editor. The Neuropathology of Schizophrenia. New York: Oxford University Press; 2000;p. 105–136
  28. Hoogland PV, van den Berg R, Huisman E. Misrouted olfactory fibres and ectopic olfactory glomeruli in normal humans and in Parkinson and Alzheimer patients. Neuropathol. Appl. Neurobiol. 2003;29:303–311
  29. Hurwitz T, Kopala LC, Clark CM, Jones B. Olfactory deficits in schizophrenia. Biol. Psychiatry. 1988;23:123–128
  30. Jojich L, Pourcho RG. Glutamate immunoreactivity in the cat retina: a quantitative study. Vis. Neurosci. 1996;13:117–133
  31. Karowski HJ, Kim H, Greer CA. Compartmental organization of the olfactory bulb glomerulus. J. Comp. Neurol. 1999;407:261–274
  32. Kawaguchi S, Hirano T. Signaling cascade regulating long-term potentiation of GABA(A) receptor responsiveness in cerebellar Purkinje neurons. J. Neurosci. 2002;22:3969–3976
  33. Klein R, Nanduri V, Jing SA, Lamballe F, Tapley P, Bryant S, et al. The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell. 1991;66:395–403
  34. Kohler CG, Moberg PJ, Gur RE, O'Connor MJ, Sperling MR, Doty RL. Olfactory dysfunction in schizophrenia and temporal lobe epilepsy. Neuropsychiatry Neuropsychol. Behav. Neurol. 2001;14:83–88
  35. Kopala LC, Good KP, Honer WG. Olfactory identification ability in pre- and postmenopausal women with schizophrenia. Biol. Psychiatry. 1995;38(1):57–63
  36. Lambert W, Agarwal R, Howe W, Clark AF, Wordinger RJ. Neurotrophin and neurotrophin expression by cells of the human lamina cribrosa. Investig. Ophthalmol. Vis. Sci. 2001;42:2315–2323
  37. Lee VM-Y, Otvos JL, Schmidt ML, Trojanowski JQ. Alzheimer disease tangles share immunological similarities with multiphosphorylation repeats in the two large neurofilament proteins. Proc. Natl. Acad. Sci. U. S. A. 1988;85:7384–7388
  38. Lidow MS, Song ZM, Caster SA, Allen PB, Greengard P, Goldman-Rakic PS. Antipsychotic treatment induces alterations in dendrite- and spine-associated proteins in dopamine-rich areas of the primate cerebral cortex. Biol. Psychiatry. 2001;49(1):1–12
  39. Linden AM, Vaisanen J, Lasko M, Nawa H, Wong G, Castren E. Expression of neurotrophins BDNF and NT-3 and their receptors in rat brain after administration of antipsychotic and psychotrophic agents. J. Mol. Neurosci. 2000;14:27–37
  40. Malaspina D, Wray AD, Friedman JH, Amador X, Yale S, Hasan A, et al. Odor discrimination deficits in schizophrenia: association with eye movement dysfunction. J. Neuropsychiatry Clin. Neurosci. 1994;6:273–278
  41. Mandairon N, Jourdan F, Didier A. Deprivation of sensory inputs to the olfactory bulb up-regulates cell death and proliferation in the subventricular zone of adult mice. Neuroscience. 2003;119:507–516
  42. Mirnics K, Middleton FA, Marquez A, Lewis DA, Levitt P. Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron. 2000;28:53–67
  43. Mirnics K, Middleton FA, Lewis DA, Levitt P. Analysis of complex brain disorders with gene expression microarrays: schizophrenia as a disease of the synapse. Trends Neurosci. 2001;24:479–486
  44. Moberg PJ, Turetsky BI. Scent of a disorder: olfactory functioning in schizophrenia. Curr. Psychiatry Rep. 2003;160:1723–1725
  45. Moberg PJ, Doty RL, Turetsky BI, Arnold SE, Mahr RN, Gur RC, et al. Olfactory identification deficits in schizophrenia: correlation with duration of illness. Am. J. Psychiatry. 1997;154:1016–1018
  46. Nabors LB, Songu-Mize E, Mize RR. Quantitative immunocytochemistry using an image analyzer: II. Concentration standards for transmitter immunocytochemistry. J. Neurosci. Methods. 1988;26:25–34
  47. Nakashima T, Kimmelman CP, Snow JBJ. Immunohistopathology of human olfactory epithelium, nerve and bulb. Laryngoscope. 1985;95:391–396
  48. Nibu K, Zhang X, Rawson NE, Restrepo D, Kaga K, Lowry LD, et al. Olfactory neuron-specific expression of NeuroD in mouse and human nasal mucosa. Cell Tissue Res. 1999;298(3):405–414
  49. Ohm TG, Mueller H, Braak E. Calbindin-D-28k-like immunoreactive structures in the olfactory bulb and anterior olfactory nucleus of the human adult: distribution and cell typology-partial complementarity to parvalbumin. Neuroscience. 1991;42:823–840
  50. Philpot BD, Lim JH, Brunjes PC. Activity-dependent regulation of calcium-binding proteins in the developing rat olfactory bulb. J. Comp. Neurol. 1997;387:12–26
  51. Quartu M, Pina Serra M, Manca A, Follesa P, Ambu R, Del Fiacco M. High affinity neurotrophin receptors in the human pre-term newborn, infant, and adult cerebellum. Int. J. Dev. Neurosci. 2003;21:309–320
  52. Rieux C, Carney R, Lupi D, DKhissi-Benyahya O, Jansen K, Chounlamountri N, et al. Analysis of immunohistochemical label of fos protein in the suprachiasmatic nucleus; comparison of different methods of quantification. J. Biol. Rhythms. 2002;17:121–136
  53. Rioux L, Ruscheinsky D, Arnold SE. Microtubules-associated protein MAP2 expression in olfactory bulb in schizophrenia. Psychiatry Res. 2004;128:1–7
  54. Roskams AJ, Bethel MA, Hurt KJ, Ronnett GV. Sequential expression of Trks A, B, and C in the regenerating olfactory neuroepithelium. J. Neurosci. 1996;16:1294–1307
  55. Roskams AJI, Cai X, Ronnett GV. Expression of neuron-specific beta-III tubulin during olfactory neurogenesis in the embryonic and adult rat. Neuroscience. 1998;83:191–200
  56. Schipper J, Tilders FJ. A new technique for studying specificity of immunocytochemical procedures: specificity of serotonin immunostaining. J. Histochem. Cytochem. 1983;31:12–18
  57. Shipley MT, Ennis M. Functional organization of olfactory system. J. Neurobiol. 1996;30:123–176
  58. Simpson PJ, Miller I, Moon C, Hanlon AL, Liebl DJ, Ronnett GV. Atrial natriuretic peptide type C induces a cell-cycle switch from proliferation to differentiation in brain-derived neurotrophic factor- or nerve growth factor-primed olfactory receptor neurons. J. Neurosci. 2002;22:5536–5551
  59. Slotnick B, Bodyak N, Davis BJ. Olfactory marker protein immunohistochemistry and the anterograde transport of horseradish peroxidase as indices of damage to the olfactory epithelium. Chem. Senses. 2001;26:605–610
  60. Smith RL, Baker H, Kolstad K, Spencer DD, Greer CA. Localization of tyrosine hydroxylase and olfactory marker protein immunoreactivity in human and macaque olfactory bulb. Brain Res. 1991;548:140–148
  61. Smutzer GS, Lee VM-Y, Trojanowski JQ, Arnold SE. Human olfactory mucosa in schizophrenia. Ann. Otol. Rhinol. Laryngol. 1998;107:349–355
  62. Takahashi M, Shirakawa O, Toyooka K, Kitamura N, Hashimoto T, Maeda K, et al. Abnormal expression of brain-derived neurotrophic factor and its receptor in the corticolimbic system of schizophrenic patients. Mol. Psychiatry. 2000;5:293–300
  63. Turetsky BI, Moberg PJ, Yousem DM, Doty RL, Arnold SE, Gur RE. Reduced olfactory bulb volume in patients with schizophrenia. Am. J. Psychiatry. 2000;157:828–830
  64. Verhaagen J, Ostreicher AB, Gispen WH, Margolis FL. The expression of the growth associated protein B50/GAP43 in the olfactory system of neonatal and adult rats. J. Neurosci. 1989;9:683–691
  65. Weickert CS, Hyde TM, Lipska BK, Herman MM, Weinberger DR, Kleinman JE. Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol. Psychiatry. 2003;8:592–610
  66. Weinberger DR. From neuropathology to neurodevelopment. Lancet. 1995;346:552–557
  67. Wiedenmann B, Franke WW. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell. 1985;41:1017–1028
  68. Yan Q, Radeke MJ, Matheson CR, Talvenheimo J, Welcher AA, Feinstein SC. Immunocytochemical localization of trkB in the central nervous system of the adult rat. J. Comp. Neurol. 1997;378:135–157

PII: S0920-9964(05)00174-X

doi: 10.1016/j.schres.2005.04.022

Schizophrenia Research
Volume 77, Issue 2 , Pages 229-239 , 15 September 2005