Ultrastructural damage of capillaries in the neocortex in schizophrenia

World Journal of Biological Psychiatry

Volumn 11, Issue 3, 2010, Pages 567-578

  Uranova, Natalya A ^a   Zimina, Ivetta S ^a   Vikhreva, Olga V ^a   Krukov, Nikolai O ^a   Rachmanova, Valentina I ^a   Orlovskaya, Diana D ^a  

^a MENTAL HEALTH RESEARCH CENTER   (Russian Federation)

Author keywords

Capillaries; Morphometry; Neocortex; Schizophrenia; Ultrastructure

Indexed keywords

ADULT; ARTICLE; ASTROCYTE; BASEMENT MEMBRANE; BLOOD BRAIN BARRIER; BRAIN CORTEX LESION; CAPILLARY; CELL ULTRASTRUCTURE; CELL VACUOLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; FEMALE; HUMAN; HUMAN TISSUE; MALE; NEOCORTEX; PATHOGENESIS; PREFRONTAL CORTEX; SCHIZOPHRENIA; VISUAL CORTEX; AGED; MICROGLIA; MIDDLE AGED; OLIGODENDROGLIA; PATHOLOGY; PHYSIOLOGY; ULTRASTRUCTURE; VASCULAR ENDOTHELIUM; VASCULARIZATION;

ADULT; AGED; ASTROCYTES; BASEMENT MEMBRANE; BLOOD-BRAIN BARRIER; CAPILLARIES; CYTOPLASM; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; MALE; MICROGLIA; MICROSCOPY, ELECTRON; MIDDLE AGED; NEOCORTEX; OLIGODENDROGLIA; PREFRONTAL CORTEX; SCHIZOPHRENIA; VACUOLES; VISUAL CORTEX;

EID: 77953635931     PISSN: 15622975     EISSN: 18141412     Source Type: Journal    
DOI: 10.3109/15622970903414188     Document Type: Article

References (73)

1. Alba C, Vidal L, Diaz F, Villena A, de Vargas IP. 2004. Ultrastructural and quantitative age-related changes in capillaries of the dorsal lateral geniculate nucleus. Brain Res Bull 30:145-153.
2. Afonso PV, Ozden S, Cumont MC, Seilhean D, Cartier L, et al 2008. Alteration of blood-brain barrier integrity by retroviral infection. PLoS Pathog 4(11):e1000205 [Epub 14 November 2008].
3. Andreasen NC, O'Leary DS, Flaum M, Nopoulos P, Watkins GL, et al 1997. Hypofrontality in schizophrenia: distributed dysfunctional circuits in neuroleptic-naive patients. Lancet 349:1730-1734.
4. Andreasen NC, Calage CA, O'Leary DS. 2008. Theory of mind and schizophrenia: a positron emission tomography study of medication-free patients. Schizophr Bull 34:708-719.
5. Andreone N, Tansella M, Cerini R, Versace A, Rambaldelli G, et al 2007. Cortical white matter microstructure in schizophrenia. Diffusion imaging study. British J Psychiatry 191:113-119.
6. Butler PD, Javitt DC. 2005. Early-stage visual processing deficits in schizophrenia. Curr Opin Psychiatry 18:151-157.
7. Bradbury M. 1979. The concept of a blood-brain barrier. London: Wiley.
8. Buchsbaum MS, Nenadic I, Hazlett EA, Spiegel-Cohen J, Fleischman MB, et al 2002. Differential metabolic rates in prefrontal and temporal Brodmann areas in schizophrenia and schizotypal personality disorder. Schizophr Res 54:141-150.
9. Buretić-Tomljanović A, Giacometti J, Nadalin S, Rubesa G, Vulin M, et al 2008. Phospholipid membrane abnormalities and reduced niacin skin flush response in schizophrenia. Psychiatr Danub 20:372-383.
10. Curtis CE, Iacono WG, Beiser M.1999. Relationship between nailfold plexus visibility and clinical, neuropsychological, and brain structural measures in schizophrenia. Biol Psychiatry 46:102-109.
11. Davis JM. 1974. Dose equivalence of the antipsychotic drugs. J Psychiatr Res 11:65-69.
12. Dean B, Laws SM, Hone E, Taddei K, Scarr E, et al 2003. Increased levels of apolipoprotein E in the frontal cortex of subjects with schizophrenia. Biol Psychiatry 54:616-622.
13. Dorph-Petersen KA, Pierri JN, Wu Q, Sampson AR, Lewis DA. 2007. Primary visual cortex volume and total neuron number are reduced in schizophrenia. J Comp Neurol 501:290-301.
14. Erhardt S, Blennow K, Nordin C, Skogh E, Lindström LH, et al 2001. Kynurenic acid levels are elevated in the cerebrospinal fluid of patients with schizophrenia. Neurosci Lett 313: 96-98.
15. Garver DL, Nair TR, Christensen JD, Holcomb JA, Kingsbury SJ. 2000. Brain and ventricle instability during psychotic episodes of the schizophrenias. Schizophr Res 44:11-23.
16. Gonul AS, Kula M, Esel E, Tutus A, Sofuoglu S. 2003. A Tc-99m HMPAO SPECT study of regional cerebral blood flow in drugfree schizophreniapatients with deficit and non-deficit syndrome. Psychiatry Res 123:199-205.
17. Gooding DC, Miller MD. 1998. Nailfold capillary plexus visibility in relation to schizotypy. Schizophr Res 32:207-212.
18. Farkas E, Süle Z, Tóth-Szuki V, Mátyás A, Antal P, et al 2006. Tumor necrosis factor-alpha increases cerebral blood flow and ultrastructural capillary damage through the release of nitric oxide in the rat brain. Microvasc Res 72:113-119.
19. Filosa JA, Blanco VM. 2007. Neurovascular coupling in the mammalian brain. Exp Physiol 92:641-646.
20. Hanson DR, Gottesman II. 2005. Theories of schizophrenia: a genetic-inflammatory-vascular synthesis. BMC Med Genet 6:7.
21. Haorah J, Ramirez SH, Schall K, Smith D, Pandya R, et al 2007. Oxidative stress activates protein tyrosine kinase and matrix metalloproteinases leading to blood-brain barrier dysfunction. J Neurochem 101:566-576.
22. Harrison RV, Harel N, Panesar J, Mount RJ. 2002. Blood capillary distribution correlates with hemodynamic-based functional imaging in cerebral cortex. Cereb Cortex 12:225-233.
23. Hoshi Y, Shinba T, Sato C, Doi N. 2006. Resting hypofrontality in schizophrenia: a study using near-infrared time-resolved spectroscopy. Schizophr Res 84:411-420.
24. Kamada H, Yu F, Nito C, Chan PH. 2007. Influence of hyperglycemia on oxidative stress and matrix metalloproteinase-9 activation after focal cerebral ischemia/reperfusion in rats: relation to blood-brain barrier dysfunction. Stroke 38: 1044-1049.
25. Karlsson H, Bachmann S, Schröder J, McArthur J, Torrey EF, et al 2001. Retroviral RNA identified in the cerebrospinal fluids and brains of individuals with schizophrenia. Proc Natl Acad Sci USA 98:4634-4639.
26. Kreczmanski P, Schmidt-Kastner R, Heinsen H, Steinbusch HW, Hof PR, et al 2005. Stereological studies of capillary length density in the frontal cortex of schizophrenics. Acta Neuropathol (Berlin) 109(5):510-518.
27. Kreczmanski P, Heinsen H, Mantua V, Woltersdorf F, Masson T, et al 2009. Microvessel length density, total length, and length per neuron in five subcortical regions in schizophrenia. Acta Neuropathol 117:409-421.
28. Li X, Tang J, Wu Z, Zhao G, Liu C, et al 2005. SPECT study of Chinese schizophrenia patients suggests that cerebral hypoperfusion and laterality exist in different ethnic groups. World J Biol Psychiatry 6:98-106.
29. Mchedlishvili G., Cervos-Navarro, Hossmann K-A. 1986. Brain edema. A pathogenetic analysis. Budapest: Akademia Kiado.
30. Moreno-Iñiguez M, Ortuño F, Arbizu J, Millán M, Soutullo C, et al 2005. Regional cerebral blood flow SPECT study, at rest and during Wisconsin Card Sorting Test (WCST) performance, in schizophrenia naive patients or treated with atypical neuroleptics. Actas Esp Psiquiatr 33:343-351.
31. Muller N, Ackenheil M. 1995. Immunoglobulin and albumin content of cerebrospinal fluid in schizophrenia patients: relationship to negative symptomatology. Schizophr Res 14: 223-228.
32. Navarro A, Del Valle E, Tolivia J. 2004. Differential expression of apolipoprotein d in human astroglial and oligodendroglial cells. J Histochem Cytochem 52:1031-1036.
33. O'Brien SM, Scully P, Dinan TG. 2008. Increased tumor necrosis factor-alpha concentrations with interleukin-4 concentrations in exacerbations of schizophrenia. Psychiatry Res 160: 256-262.
34. Oǐfa AI, Uranova NA. 1991. Electron-microscopic analysis of cytoarchitectonic disorders in the cerebral cortex in schizophrenia. Zh Nevropatol Psikhiatr Im S S Korsakova 91:48-52 (in Russian).
35. Orlovskaia DD, Solov'eva ZhV. 1976. Changes in the ultra-fine structure of capillaries of the embryonic brain in the presence of schizophrenia in the mother. Zh Nevropatol Psikhiatr Im S S Korsakova 76:1043-1046 (in Russian).
36. Parellada E, Catafau AM, Bernardo M, Lomena F, Catarineu S, et al 1998. The resting and activation issue of hypofrontality: a single photon emission computed tomography study in neuroleptic-naive and neuroleptic-free schizophrenia female patients. Biol Psychiatry 44:787-790.
37. Pardridge WM. 2007. Blood-brain barrier genomics. Stroke 38:686-690.
38. Paterson GJ, Ohashi Y, Reynolds GP, Pratt JA, Morris BJ. 2006. Selective increases in the cytokine, TNFalpha, in the prefrontal cortex of PCP-treated rats and human schizophrenia subjects: influence of antipsychotic drugs. J Psychopharmacol 20: 636-642.
39. Persidsky Y, Ramirez SH, Haorah J, Kanmogne GD. 2006. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol 1:223-236.
40. Peters A. 1976. The fine structure of the nervous system. The neurons and supporting cells. Philadelphia, London, Toronto: WB Saunders. p. 296-302.
41. Peters A, Josephson K, Vincent SL. 1991. Effects of aging on the neuroglial cells and pericytes within area 17 of the rhesus monkey cerebral cortex. Anat Rec 229:384-398.
42. Potkin SG, Alva G, Fleming K, Anand R, Keator D, et al 2002. A PET study of the pathophysiology of negative symptoms in schizophrenia. Positron emission tomography. Am J Psychiatry 159:227-237.
43. Prabakaran S, Swatton JE, Ryan MM, Huffaker SJ, Huang JT, et al 2004. Mitochondrial dysfunction in schizophrenia: evidence for compromised brain metabolism and oxidative stress. Mol Psychiatry 9:684-697, 643.
44. Ragland JD, Gur RC, Glahn DC, Censits DM, Smith RJ, et al 1998. Frontotemporal cerebral blood flow change during executive and declarative memory tasks in schizophrenia: a positron emission tomography study. Neuropsychology 12:399-413.
45. Reddy R, Keshavan MS.2003. Phosphorus magnetic resonance spectroscopy: its utility in examining the membrane hypothesis of schizophrenia. Prostaglandins Leukot Essent Fatty Acids 69:401-405.
46. Roberts RC, Du F, McCarthy KE, Okuno E, Schwarcz R. 1992. Immunocytochemical localization of kynurenine aminotransferase in the rat striatum: a light and electron microscopic study. J Comp Neurol 326:82-90.
47. Ross BM, Hughes B, Turenne S, Seeman M, Warsh JJ. 2004. Reduced vasodilatory response to methylnicotinate in schizophrenia as assessed by laser Doppler flowmetry. Eur Neuropsychopharmacol 14:191-197.
48. Schultz SK, O'Leary DS, Boles Ponto LL, Arndt S, Magnotta, et al 2002. Age and regional cerebral blood flow in schizophrenia: age effects in anterior cingulate, frontal, and parietal cortex. J Neuropsychiatry Clin Neurosci 14:19-24.
49. Schwarcz R, Rassoulpour A, Wu HQ, Medoff D, Tamminga CA, et al 2001. Increased cortical kynurenate content in schizophrenia. Biol Psychiatry 50:521-530.
50. Schwarz E, Prabakaran S, Whitfield P, Major H, Leweke FM, et al 2008. High throughput lipidomic profiling of schizophrenia and bipolar disorder brain tissue reveals alterations of free fatty acids, phosphatidylcholines, and ceramides. J Proteome Res 7:4266-4277.
51. Senitz D, Winkelmann E. 1991. Neuronal structure abnormality in the orbito-frontal cortex of schizophrenics. J Hirnforsch 32:149-158.
52. Semkovska M, Bedard MA, Stip E. 2001. Hypofrontality and negative symptoms in schizophrenia: synthesis of anatomic and neuropsychological knowledge and ecological perspectives. Encephale 27:405-415.
53. Shcherbakova I, Neshkova E, Dotsenko V, Platonova T, Shcherbakova E, et al 1999. The possible role of plasma kallikrein-kinin system and leukocyte elastase in pathogenesis of schizophrenia. Immunopharmacology 43:273-279.
54. Shin YW, Kwon JS, Ha TH, Park HJ, Kim DJ, et al 2006. Increased water diffusivity in the frontal and temporal cortices of schizophrenia patients. Neuroimage 30:1285-1291.
55. Shusta EV. 2005. Blood-brain barrier genomics, proteomics, and new transporter discovery. NeuroRx 2:151-161.
56. Simard M, Arcuino G, Takano T, Liu QS, Nedergaard M. 2003. Signaling at the gliovascular interface. J Neurosci 23: 9254-9262.
57. Song XQ, Lv LX, Li WQ, Hao YH, Zhao JP. 2009. The interaction of nuclear factor-kappa B and cytokines is associated with schizophrenia. Biol Psychiatry 65:481-488.
58. Suzuki M, Nohara S, Hagino H, Takahashi T, Kawasaki Y, et al 2005. Prefrontal abnormalities in patients with simple schizophrenia: structural and functional brain-imaging studies in five cases. Psychiatry Res 140:157-171.
59. Taylor SF, Phan KL, Britton JC, Liberzon I. 2005. Neural response to emotional salience in schizophrenia. Neuropsychopharmacology 30:984-995.
60. Theoharides TC, Konstantinidou AD. 2007. Corticotropinreleasing hormone and the blood-brain barrier. Front Biosci 12:1615-1628.
61. Ueno M, Sakamoto H, Kanenishi K, Onodera M, Akiguchi I, et al 2001. Ultrastructural and permeability features of microvessels in the periventricular area of senescence-accelerated mice (SAM). Microsc Res Tech 53:232-238.
62. Ueno M, Tomimoto H, Akiguchi I, Wakita H, Sakamoto H. 2002. Blood-brain barrier disruption in white matter lesions in a rat model of chronic cerebral hypoperfusion. J Cereb Blood Flow Metab 22:97-104.
63. Uranova N, Orlovskaya D, Vikhreva O, Zimina I, Kolomeets N, et al 2001. Electron microscopy of oligodendroglia in severe mental illness. Brain Res Bull 55:597-610.
64. Uranova NA, Vostrikov VM, Vikhreva OV, Zimina IS, Kolomeets NS, et al 2007. The role of oligodendrocyte pathology in schizophrenia. Int J Neuropsychopharmacol 10:537-545.
65. Vita A, Bressi S, Perani D, Invernizzi G, Giobbio GM, et al 1995. High-resolution SPECT study of regional cerebral blood flow in drug-free and drug-naive schizophrenia patients. Am J Psychiatry 152:876-882.
66. Vostrikov V, Orlovskaya D, Uranova N. 2008. Deficit of pericapillary oligodendrocytes in the prefrontal cortex in schizophrenia. World J Biol Psychiatry 9:34-42.
67. Wang CS, Yang YK, Chen M, Chiu NT, Yeh TL, et al 2003. Negative symptoms and regional cerebral blood flow in patients with schizophrenia: a single photon emission computed tomography study. Kaohsiung J Med Sci 19:464-469.
68. Webster MJ, Knable MB, Johnston-Wilson N, Nagata K, Inagaki M, et al 2001. Immunohistochemical localization of phosphorylated glial fibrillary acidic protein in the prefrontal cortex and hippocampus from patients with schizophrenia, bipolar disorder, and depression. Brain Behav Immun 15: 388-400.
69. Weinberger DR, Berman KF, Zec RF. 1986. Physiology dysfunction of dorsolateral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow evidence. Arch Gen Psychiatry 43:114-124.
70. Wu JS, Chen XC, Chen H, Shi YQ. 2006. A study on blood-brain barrier ultrastructural changes induced by cerebral hypoperfusion of different stages. Neurol Res 28:50-58.
71. Yolken RH, Karlsson H, Yee F, Johnston-Wilson NL, Torrey EF. 2000. Endogenous retroviruses and schizophrenia. Brain Res Brain Res Rev 31:193-199.
72. Zhao J, He X, Liu Z, Yang D. 2006. The effects of clozapine on cognitive function and regional cerebral blood flow in the negative symptom profile schizophrenia. Int J Psychiatry Med 36: 171-81.
73. del Zoppo GJ, Hallenbeck JM. 2000. Advances in the vascular pathophysiology of ischemic stroke. Thromb Res 98: 73-81.