Imaging neuroinflammation in gray and white matter in schizophrenia: An in-vivo PET study with [18 F]-FEPPA

Schizophrenia Bulletin

Volumn 41, Issue 1, 2015, Pages 85-93

  Kenk, Miran ^a   Selvanathan, Thiviya ^a   Rao, Naren ^a   Suridjan, Ivonne ^a   Rusjan, Pablo ^a   Remington, Gary ^a   Meyer, Jeffrey H ^a   Wilson, Alan A ^a   Houle, Sylvain ^a   Mizrahi, Romina ^a  

^a PET Centre   (Canada)

Author keywords

inflammation; microglia; positron emission tomography; psychosis; rs6971 polymorphism; translocator protein 18kDa (TSPO)

Indexed keywords

ATYPICAL ANTIPSYCHOTIC AGENT; N ACETYL N (2 FLUOROETHOXYBENZYL) 2 PHENOXY 5 PYRIDINAMINE F 18; NEUROLEPTIC AGENT; RADIOLIGAND; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; ANILIDE; N-(2-((N-(4-PHENOXYPYRIDIN-3-YL)ACETAMIDO)METHYL)PHENOXY)ETHYL FLUORIDE; PYRIDINE DERIVATIVE; RADIOPHARMACEUTICAL AGENT; TSPO PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; BRAIN SIZE; CLINICAL ARTICLE; CLINICAL EVALUATION; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE CLASSIFICATION; DISEASE COURSE; DISEASE SEVERITY; FEMALE; GRAY MATTER; HUMAN; IN VIVO STUDY; MALE; NERVOUS SYSTEM INFLAMMATION; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PET SCANNER; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PSYCHOSIS; SCHIZOPHRENIA; VOLUME OF DISTRIBUTION; WHITE MATTER; CASE CONTROL STUDY; IMMUNOLOGY; INFLAMMATION; METABOLISM; MICROGLIA; MIDDLE AGED; SCINTISCANNING;

ADULT; ANILIDES; CASE-CONTROL STUDIES; CROSS-SECTIONAL STUDIES; FEMALE; GRAY MATTER; HUMANS; INFLAMMATION; MALE; MICROGLIA; MIDDLE AGED; POSITRON-EMISSION TOMOGRAPHY; PYRIDINES; RADIOPHARMACEUTICALS; RECEPTORS, GABA; SCHIZOPHRENIA; WHITE MATTER;

EID: 84928798486     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbu157     Document Type: Article

References (74)

1. Theodoropoulou S, Spanakos G, Baxevanis CN, et al. Cytokine serum levels, autologous mixed lymphocyte reaction and surface marker analysis in never medicated and chronically medicated schizophrenic patients. Schizophr Res. 2001;47:13-25.
2. Zhang XY, Zhou DF, Zhang PY, Wu GY, Cao LY, Shen YC. Elevated interleukin-2, interleukin-6 and interleukin-8 serum levels in neuroleptic-free schizophrenia: association with psychopathology. Schizophr Res. 2002;57:247-258.
3. Akiyama K. Serum levels of soluble IL-2 receptor alpha, IL-6 and IL-1 receptor antagonist in schizophrenia before and during neuroleptic administration. Schizophr Res. 1999;37:97-106.
4. van Kammen DP, McAllister-Sistilli CG, Kelley ME, Gurklis JA, Yao JK. Elevated interleukin-6 in schizophrenia. Psychiatry Res. 1999;87:129-136.
5. Kaiya H, Uematsu M, Ofuji M, et al. Elevated plasma prostaglandin E2 levels in schizophrenia. J Neural Transm. 1989;77:39-46.
6. Dickerson F, Stallings C, Origoni A, Boronow J, Yolken R. C-reactive protein is associated with the severity of cognitive impairment but not of psychiatric symptoms in individuals with schizophrenia. Schizophr Res. 2007;93:261-265.
7. Fan X, Goff DC, Henderson DC. Inflammation and schizophrenia. Expert Rev Neurother. 2007;7:789-796.
8. Müller N, Riedel M, Scheppach C, et al. Beneficial antipsychotic effects of celecoxib add-on therapy compared to risperidone alone in schizophrenia. Am J Psychiatry. 2002;159:1029-1034.
9. Akhondzadeh S, Tabatabaee M, Amini H, Ahmadi Abhari SA, Abbasi SH, Behnam B. Celecoxib as adjunctive therapy in schizophrenia: a double-blind, randomized and placebocontrolled trial. Schizophr Res. 2007;90:179-185.
10. Müller N, Riedel M, Schwarz MJ, Engel RR. Clinical effects of COX-2 inhibitors on cognition in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2005;255:149-151.
11. Brown AS, Derkits EJ. Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am J Psychiatry. 2010;167:261-280.
12. Venneti S, Lopresti BJ, Wiley CA. The peripheral benzodiazepine receptor (Translocator protein 18kDa) in microglia: from pathology to imaging. Prog Neurobiol. 2006;80:308-322.
13. Davalos D, Grutzendler J, Yang G, et al. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci. 2005;8:752-758.
14. Denes A, Vidyasagar R, Feng J, et al. Proliferating resident microglia after focal cerebral ischaemia in mice. J Cereb Blood Flow Metab. 2007;27:1941-1953.
15. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci. 2007;10:1387-1394.
16. Cosenza-Nashat M, Zhao ML, Suh HS, et al. Expression of the translocator protein of 18 kDa by microglia, macrophages and astrocytes based on immunohistochemical localization in abnormal human brain. Neuropathol Appl Neurobiol. 2009;35:306-328.
17. Cagnin A, Myers R, Gunn RN, et al. In vivo visualization of activated glia by [11C] ®-PK11195-PET following herpes encephalitis reveals projected neuronal damage beyond the primary focal lesion. Brain. 2001;124:2014-2027.
18. Jaworski T, Lechat B, Demedts D, et al. Dendritic degeneration, neurovascular defects, and inflammation precede neuronal loss in a mouse model for tau-mediated neurodegeneration. Am J Pathol. 2011;179:2001-2015.
19. Gao HM, Zhang F, Zhou H, Kam W, Wilson B, Hong JS. Neuroinflammation and α-synuclein dysfunction potentiate each other, driving chronic progression of neurodegeneration in a mouse model of Parkinson's disease. Environ Health Perspect. 2011;119:807-814.
20. Takahashi K, Funata N, Ikuta F, Sato S. Neuronal apoptosis and inflammatory responses in the central nervous system of a rabbit treated with Shiga toxin-2. J Neuroinflammation. 2008;5:11.
21. Lieberman J, Chakos M, Wu H, et al. Longitudinal study of brain morphology in first episode schizophrenia. Biol Psychiatry. 2001;49:487-499.
22. Wright IC, Rabe-Hesketh S, Woodruff PW, David AS, Murray RM, Bullmore ET. Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry. 2000;157:16-25.
23. Lawrie SM, Abukmeil SS. Brain abnormality in schizophrenia. A systematic and quantitative review of volumetric magnetic resonance imaging studies. Br J Psychiatry. 1998;172:110-120.
24. Pedersen A, Diedrich M, Kaestner F, et al. Memory impairment correlates with increased S100B serum concentrations in patients with chronic schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry. 2008;32:1789-1792.
25. Dickerson F, Stallings C, Origoni A, Vaughan C, Khushalani S, Yolken R. Additive effects of elevated C-reactive protein and exposure to Herpes Simplex Virus type 1 on cognitive impairment in individuals with schizophrenia. Schizophr Res. 2012;134:83-88.
26. Patel S, Mahon K, Wellington R, Zhang J, Chaplin W, Szeszko PR. A meta-analysis of diffusion tensor imaging studies of the corpus callosum in schizophrenia. Schizophr Res. 2011;129:149-155.
27. Yao L, Lui S, Deng W, et al. Association of white matter deficits with clinical symptoms in antipsychotic-naive firstepisode schizophrenia: an optimized VBM study using 3T. MAGMA. 2014;27:283-290.
28. Chiapponi C, Piras F, Fagioli S, Piras F, Caltagirone C, Spalletta G. Age-related brain trajectories in schizophrenia: a systematic review of structural MRI studies. Psychiatry Res. 2013;214:83-93.
29. Holleran L, Ahmed M, Anderson-Schmidt H, et al. Altered interhemispheric and temporal lobe white matter microstructural organization in severe chronic schizophrenia. Neuropsychopharmacology. 2014;39:944-954.
30. Bayer TA, Buslei R, Havas L, Falkai P. Evidence for activation of microglia in patients with psychiatric illnesses. Neurosci Lett. 1999;271:126-128.
31. Radewicz K, Garey LJ, Gentleman SM, Reynolds R. Increase in HLA-DR immunoreactive microglia in frontal and temporal cortex of chronic schizophrenics. J Neuropathol Exp Neurol. 2000;59:137-150.
32. Busse S, Busse M, Schiltz K, et al. Different distribution patterns of lymphocytes and microglia in the hippocampus of patients with residual versus paranoid schizophrenia: further evidence for disease course-related immune alterations? Brain Behav Immun. 2012;26:1273-1279.
33. Wierzba-Bobrowicz T, Lewandowska E, Lechowicz W, Stepień T, Pasennik E. Quantitative analysis of activated microglia, ramified and damage of processes in the frontal and temporal lobes of chronic schizophrenics. Folia Neuropathol. 2005;43:81-89.
34. Steiner J, Mawrin C, Ziegeler A, et al. Distribution of HLADR-positive microglia in schizophrenia reflects impaired cerebral lateralization. Acta Neuropathol. 2006;112:305-316.
35. Arnold SE, Trojanowski JQ, Gur RE, Blackwell P, Han LY, Choi C. Absence of neurodegeneration and neural injury in the cerebral cortex in a sample of elderly patients with schizophrenia. Arch Gen Psychiatry. 1998;55:225-232.
36. Falke E, Han LY, Arnold SE. Absence of neurodegeneration in the thalamus and caudate of elderly patients with schizophrenia. Psychiatry Res. 2000;93:103-110.
37. Kurumaji A, Wakai T, Toru M. Decreases in peripheral-type benzodiazepine receptors in postmortem brains of chronic schizophrenics. J Neural Transm. 1997;104:1361-1370.
38. van Berckel BN, Bossong MG, Boellaard R, et al. Microglia activation in recent-onset schizophrenia: a quantitative ®-[11C]PK11195 positron emission tomography study. Biol Psychiatry. 2008;64:820-822.
39. Doorduin J, de Vries EF, Willemsen AT, de Groot JC, Dierckx RA, Klein HC. Neuroinflammation in schizophrenia-related psychosis: a PET study. J Nucl Med. 2009;50:1801-1807.
40. Takano A, Arakawa R, Ito H, et al. Peripheral benzodiazepine receptors in patients with chronic schizophrenia: a PET study with [11C]DAA1106. Int J Neuropsychopharmacol. 2010;13:943-950.
41. Yoder KK, Nho K, Risacher SL, Kim S, Shen L, Saykin AJ. Influence of TSPO genotype on 11C-PBR28 standardized uptake values. J Nucl Med. 2013;54:1320-1322.
42. Kreisl WC, Lyoo CH, McGwier M, et al. In vivo radioligand binding to translocator protein correlates with severity of Alzheimer's disease. Brain. 2013;136:2228-2238.
43. Owen DR, Yeo AJ, Gunn RN, et al. An 18-kDa translocator protein (TSPO) polymorphism explains differences in binding affinity of the PET radioligand PBR28. J Cereb Blood Flow Metab. 2012;32:1-5.
44. Mizrahi R, Rusjan PM, Kennedy J, et al. Translocator protein (18 kDa) polymorphism (rs6971) explains in-vivo brain binding affinity of the PET radioligand [(18)F]-FEPPA. J Cereb Blood Flow Metab. 2012;32:968-972.
45. Wilson AA, Garcia A, Parkes J, et al. Radiosynthesis and initial evaluation of [18F]-FEPPA for PET imaging of peripheral benzodiazepine receptors. Nucl Med Biol. 2008;35:305-314.
46. Rusjan PM, Wilson AA, Bloomfield PM, et al. Quantitation of translocator protein binding in human brain with the novel radioligand [18F]-FEPPA and positron emission tomography. J Cereb Blood Flow Metab. 2011;31:1807-1816.
47. First M, Spitzer R, Gibbon M, Williams J. Structured Clinical Interview for DSM-IV Axis I Disorders: Patient Edition (SCIDI/P). Version 2.0. New York: Biometric Research, New York State Psychiatric Institute; 1995.
48. Müller N, Schwarz MJ. A psychoneuroimmunological perspective to Emil Kraepelins dichotomy: schizophrenia and major depression as inflammatory CNS disorders. Eur Arch Psychiatry Clin Neurosci. 2008;258(suppl 2):97-106.
49. Kay SR, Fiszbein A, Opler LA. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull. 1987;13:261-276.
50. Yamagishi H, Kawaguchi M. Characterization of centraland peripheral-type benzodiazepine receptors in rat salivary glands. Biochem Pharmacol. 1998;55:209-214.
51. Kalk NJ, Owen DR, Tyacke RJ, et al. Are prescribed benzodiazepines likely to affect the availability of the 18 kDa translocator protein (TSPO) in PET studies? Synapse. 2013;67:909-912.
52. Danovich L, Veenman L, Leschiner S, et al. The influence of clozapine treatment and other antipsychotics on the 18 kDa translocator protein, formerly named the peripheraltype benzodiazepine receptor, and steroid production. Eur Neuropsychopharmacol. 2008;18:24-33.
53. Krueger KE. Peripheral-type benzodiazepine receptors: a second site of action for benzodiazepines. Neuropsychopharmacology. 1991;4:237-244.
54. Randolph C. Repeatable Battery for the Assessment of Neuropsychological Status. San Antonio, TX: Psychological Corporation (Harcourt); 1998.
55. Wilk CM, Gold JM, Humber K, Dickerson F, Fenton WS, Buchanan RW. Brief cognitive assessment in schizophrenia: normative data for the Repeatable Battery for the Assessment of Neuropsychological Status. Schizophr Res. 2004;70:175-186.
56. Rusjan P, Mamo D, Ginovart N, et al. An automated method for the extraction of regional data from PET images. Psychiatry Res. 2006;147:79-89.
57. Mizrahi R, Addington J, Rusjan PM, et al. Increased stressinduced dopamine release in psychosis. Biol Psychiatry. 2012;71:561-567.
58. Suridjan I, Rusjan PM, Kenk M, et al. Quantitative imaging of neuroinflammation in human white matter: a positron emission tomography study with translocator protein 18 kDa radioligand, [(18) F]-FEPPA. Synapse. 2014;68:536-547.
59. Leenders KL, Perani D, Lammertsma AA, et al. Cerebral blood flow, blood volume and oxygen utilization. Normal values and effect of age. Brain. 1990;113(pt 1):27-47.
60. Müller-Gärtner HW, Links JM, Prince JL, et al. Measurement of radiotracer concentration in brain gray matter using positron emission tomography: MRI-based correction for partial volume effects. J Cereb Blood Flow Metab. 1992;12:571-583.
61. Lahiri DK, Bye S, Nurnberger JI Jr, Hodes ME, Crisp M. A non-organic and non-enzymatic extraction method gives higher yields of genomic DNA from whole-blood samples than do nine other methods tested. J Biochem Biophys Methods. 1992;25:193-205.
62. Schweitzer PJ, Fallon BA, Mann JJ, Kumar JS. PET tracers for the peripheral benzodiazepine receptor and uses thereof. Drug Discov Today. 2010;15:933-942.
63. Kreisl WC, Jenko KJ, Hines CS, et al. A genetic polymorphism for translocator protein 18 kDa affects both in vitro and in vivo radioligand binding in human brain to this putative biomarker of neuroinflammation. J Cereb Blood Flow Metab. 2013;33:53-58.
64. van Velden FH, Kloet RW, van Berckel BN, et al. HRRT versus HR+ human brain PET studies: an interscanner testretest study. J Nucl Med. 2009;50:693-702.
65. Leroy C, Comtat C, Trébossen R, Syrota A, Martinot JL, Ribeiro MJ. Assessment of 11C-PE2I binding to the neuronal dopamine transporter in humans with the high-spatial-resolution PET scanner HRRT. J Nucl Med. 2007;48:538-546.
66. Rizzo G, Veronese M, Tonietto M, Zanotti-Fregonara P, Turkheimer FE, Bertoldo A. Kinetic modeling without accounting for the vascular component impairs the quantification of [(11)C]PBR28 brain PET data. J Cereb Blood Flow Metab. 2014;34:1060-1069.
67. Ellison-Wright I, Nathan PJ, Bullmore ET, et al. Distribution of tract deficits in schizophrenia. BMC Psychiatry. 2014;14:99.
68. Zipursky RB, Lambe EK, Kapur S, Mikulis DJ. Cerebral gray matter volume deficits in first episode psychosis. Arch Gen Psychiatry. 1998;55:540-546.
69. Moncrieff J, Leo J. A systematic review of the effects of antipsychotic drugs on brain volume. Psychol Med. 2010;40:1409-1422.
70. Deng MY, McAlonan GM, Cheung C, et al. A naturalistic study of grey matter volume increase after early treatment in anti-psychotic naïve, newly diagnosed schizophrenia. Psychopharmacology (Berl). 2009;206:437-446.
71. Li M, Chen Z, Deng W, et al. Volume increases in putamen associated with positive symptom reduction in previously drug-naive schizophrenia after 6 weeks antipsychotic treatment. Psychol Med. 2012;42:1475-1483.
72. Hou Y, Wu CF, Yang JY, et al. Effects of clozapine, olanzapine and haloperidol on nitric oxide production by lipopolysaccharide-activated N9 cells. Prog Neuropsychopharmacol Biol Psychiatry. 2006;30:1523-1528.
73. Bian Q, Kato T, Monji A, et al. The effect of atypical antipsychotics, perospirone, ziprasidone and quetiapine on microglial activation induced by interferon-gamma. Prog Neuropsychopharmacol Biol Psychiatry. 2008;32:42-48.
74. Innis RB, Cunningham VJ, Delforge J, et al. Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J Cereb Blood Flow Metab. 2007;27:1533-1539.