Microglial activation in the rat brain following chronic antipsychotic treatment at clinically relevant doses

European Neuropsychopharmacology

Volumn 25, Issue 11, 2015, Pages 2098-2107

  Cotel, Marie Caroline ^a   Lenartowicz, Ewelina M ^a   Natesan, Sridhar ^a   Modo, Michel M ^a   Cooper, Jonathan D ^a   Williams, Steven C R ^a   Kapur, Shitij ^a   Vernon, Anthony C ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Antipsychotic; Haloperidol; Inflammation; Microglia; Olanzapine; Schizophrenia

Indexed keywords

HALOPERIDOL; NEUROLEPTIC AGENT; OLANZAPINE; PROTEIN; PROTEIN IBA 1; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; AIF1 PROTEIN, RAT; BENZODIAZEPINE DERIVATIVE; CALCIUM BINDING PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; BRAIN REGION; CELL ACTIVATION; CELL DENSITY; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; CORPUS STRIATUM; DRUG EFFECT; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; MALE; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; SCHIZOPHRENIA; SECONDARY SOMATOSENSORY CORTEX; TREATMENT DURATION; ANIMAL; BRAIN; CELL COUNT; DRUG EFFECTS; IMMUNOLOGY; IMMUNOMODULATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIPSYCHOTIC AGENTS; BENZODIAZEPINES; BRAIN; CALCIUM-BINDING PROTEINS; CELL COUNT; CELL PROLIFERATION; HALOPERIDOL; IMMUNOHISTOCHEMISTRY; MALE; MICROFILAMENT PROTEINS; MICROGLIA; NEUROIMMUNOMODULATION; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY;

EID: 84947492780     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2015.08.004     Document Type: Article

References (51)

1. Arnold S.E., Trojanowski J.Q., Gur R.E., Blackwell P., Han L.Y., 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.
2. Banati R.B. Visualising microglial activation in vivo. Glia 2002, 40:206-217.
3. Bayer T.A., Buslei R., Havas L., Falkai P. Evidence for activation of microglia in patients with psychiatric illnesses. Neurosci. Lett. 1999, 271:126-128.
4. Boonstra G., van Haren N.E., Schnack H.G., Cahn W., Burger H., Boersma M., de Kroon B., Grobbee D.E., Hulshoff Pol H.E., Kahn R.S. Brain volume changes after withdrawal of atypical antipsychotics in patients with first-episode schizophrenia. J. Clin. Psychopharmacol. 2011, 31:146-153.
5. Brown A.S., Derkits E.J. Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am. J. Psychiatry 2010, 167:261-280.
6. Busse S., Busse M., Schiltz K., Bielau H., Gos T., Brisch R., Mawrin C., Schmitt A., Jordan W., Muller U.J., Bernstein H.G., Bogerts B., Steiner J. 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.
7. Cazorla M., de Carvalho F.D., Chohan M.O., Shegda M., Chuhma N., Rayport S., Ahmari S.E., Moore H., Kellendonk C. Dopamine D2 receptors regulate the anatomical and functional balance of basal ganglia circuitry. Neuron 2014, 81:153-164.
8. 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.
9. 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.
10. Doorduin J., de Vries E.F., Willemsen A.T., de Groot J.C., Dierckx R.A., Klein H.C. Neuroinflammation in schizophrenia-related psychosis: a PET study. J. Nucl. Med. 2009, 50:1801-1807.
11. Dorph-Petersen K.A., Pierri J.N., Perel J.M., Sun Z., Sampson A.R., Lewis D.A. The influence of chronic exposure to antipsychotic medications on brain size before and after tissue fixation: a comparison of haloperidol and olanzapine in macaque monkeys. Neuropsychopharmacology 2005, 30:1649-1661.
12. Falke E., Han L.Y., Arnold S.E. Absence of neurodegeneration in the thalamus and caudate of elderly patients with schizophrenia. Psychiatry Res. 2000, 93:103-110.
13. Fillman S.G., Cloonan N., Catts V.S., Miller L.C., Wong J., McCrossin T., Cairns M., Weickert C.S. Increased inflammatory markers identified in the dorsolateral prefrontal cortex of individuals with schizophrenia. Mol. Psychiatry 2013, 18:206-214.
14. Fusar-Poli P., Smieskova R., Kempton M.J., Ho B.C., Andreasen N.C., Borgwardt S. Progressive brain changes in schizophrenia related to antipsychotic treatment? A meta-analysis of longitudinal MRI studies. Neurosci. Biobehav. Rev. 2013, 37:1680-1691.
15. Ho B.C., Andreasen N.C., Ziebell S., Pierson R., Magnotta V. Long-term antipsychotic treatment and brain volumes: a longitudinal study of first-episode schizophrenia. Arch. Gen. Psychiatry 2011, 68:128-137.
16. Kahn R.S., Sommer I.E. The neurobiology and treatment of first-episode schizophrenia. Mol. Psychiatry 2014.
17. Kapur S., VanderSpek S.C., Brownlee B.A., Nobrega J.N. Antipsychotic dosing in preclinical models is often unrepresentative of the clinical condition: a suggested solution based on in vivo occupancy. J. Pharmacol. Exp. Ther. 2003, 305:625-631.
18. Kato T.A., Monji A., Mizoguchi Y., Hashioka S., Horikawa H., Seki Y., Kasai M., Utsumi H., Kanba S. Anti-Inflammatory properties of antipsychotics via microglia modulations: are antipsychotics a 'fire extinguisher' in the brain of schizophrenia?. Mini Rev. Med. Chem. 2011, 11:565-574.
19. 18F]-FEPPA. Schizophr. Bull. 2015, 41:85-93.
20. Kettenmann H., Kirchhoff F., Verkhratsky A. Microglia: new roles for the synaptic stripper. Neuron 2013, 77:10-18.
21. Konopaske G.T., Dorph-Petersen K.A., Sweet R.A., Pierri J.N., Zhang W., Sampson A.R., Lewis D.A. Effect of chronic antipsychotic exposure on astrocyte and oligodendrocyte numbers in macaque monkeys. Biol. Psychiatry 2008, 63:759-765.
22. 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.
23. Lieberman J., Chakos M., Wu H., Alvir J., Hoffman E., Robinson D., Bilder R. Longitudinal study of brain morphology in first episode schizophrenia. Biol. Psychiatry 2001, 49:487-499.
24. Lieberman J.A., Tollefson G.D., Charles C., Zipursky R., Sharma T., Kahn R.S., Keefe R.S., Green A.I., Gur R.E., McEvoy J., Perkins D., Hamer R.M., Gu H., Tohen M. Antipsychotic drug effects on brain morphology in first-episode psychosis. Arch. Gen. Psychiatry 2005, 62:361-370.
25. Martins-de-Souza D., Gattaz W.F., Schmitt A., Rewerts C., Maccarrone G., Dias-Neto E., Turck C.W. Prefrontal cortex shotgun proteome analysis reveals altered calcium homeostasis and immune system imbalance in schizophrenia. Eur. Arch. Psychiatry Clin. Neurosci. 2009, 259:151-163.
26. Maxeiner H.G., Marion Schneider E., Kurfiss S.T., Brettschneider J., Tumani H., Bechter K. Cerebrospinal fluid and serum cytokine profiling to detect immune control of infectious and inflammatory neurological and psychiatric diseases. Cytokine 2014, 69:62-67.
27. Miller B.J., Buckley P., Seabolt W., Mellor A., Kirkpatrick B. Meta-analysis of cytokine alterations in schizophrenia: clinical status and antipsychotic effects. Biol. Psychiatry 2011, 70:663-671.
28. Miller B.J., Culpepper N., Rapaport M.H., Buckley P. Prenatal inflammation and neurodevelopment in schizophrenia: a review of human studies. Prog. Neuropsychopharmacol. Biol. Psychiatry 2013, 42:92-100.
29. Miller B.J., Gassama B., Sebastian D., Buckley P., Mellor A. Meta-analysis of lymphocytes in schizophrenia: clinical status and antipsychotic effects. Biol. Psychiatry 2013, 73:993-999.
30. Montero-Menei C.N., Sindji L., Garcion E., Mege M., Couez D., Gamelin E., Darcy F. Early events of the inflammatory reaction induced in rat brain by lipopolysaccharide intracerebral injection: relative contribution of peripheral monocytes and activated microglia. Brain Res. 1996, 724:55-66.
31. Papadopoulos V., Baraldi M., Guilarte T.R., Knudsen T.B., Lacapere J.J., Lindemann P., Norenberg M.D., Nutt D., Weizman A., Zhang M.R., Gavish M. Translocator protein (18kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol. Sci. 2006, 27:402-409.
32. Paxinos, G., Watson, C., 2007. The Rat Brain in Stereotaxic Coordinates, Sixth Edition, Elsevier, 84 Theobald's Road, London WC1X 8RR, UK.
33. Pedersen A., Diedrich M., Kaestner F., Koelkebeck K., Ohrmann P., Ponath G., Kipp F., Abel S., Siegmund A., Suslow T., von Eiff C., Arolt V., Rothermundt M. Memory impairment correlates with increased S100B serum concentrations in patients with chronic schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 2008, 32:1789-1792.
34. Radewicz K., Garey L.J., Gentleman S.M., Reynolds R. Increase in HLA-DR immunoreactive microglia in frontal and temporal cortex of chronic schizophrenics. J. Neuropathol. Exp. Neurol. 2000, 59:137-150.
35. Rizzo G., Veronese M., Tonietto M., Zanotti-Fregonara P., Turkheimer F.E., 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.
36. Schmitz C., Hof P.R. Design-based stereology in neuroscience. Neuroscience 2005, 130:813-831.
37. Shin H., Song J.H. Antipsychotics, chlorpromazine and haloperidol inhibit voltage-gated proton currents in BV2 microglial cells. Eur. J. Pharmacol. 2014, 738:256-262.
38. Sommer I.E., van Westrhenen R., Begemann M.J., de Witte L.D., Leucht S., Kahn R.S. Efficacy of anti-inflammatory agents to improve symptoms in patients with schizophrenia: an update. Schizophr. Bull. 2014, 40:181-191.
39. Steiner J., Bielau H., Brisch R., Danos P., Ullrich O., Mawrin C., Bernstein H.G., Bogerts B. Immunological aspects in the neurobiology of suicide: elevated microglial density in schizophrenia and depression is associated with suicide. J. Psychiatr. Res. 2008, 42:151-157.
40. Steiner J., Mawrin C., Ziegeler A., Bielau H., Ullrich O., Bernstein H.G., Bogerts B. Distribution of HLA-DR-positive microglia in schizophrenia reflects impaired cerebral lateralization. Acta Neuropathol. 2006, 112:305-316.
41. 11C]DAA1106. Int. J. Neuropsychopharmacol. 2010, 13:943-950.
42. 11C]PK11195 positron emission tomography study. Biol. Psychiatry 2008, 64:820-822.
43. Venneti S., Lopresti B.J., Wiley C.A. The peripheral benzodiazepine receptor (Translocator protein 18kDa) in microglia: from pathology to imaging. Prog. Neurobiol. 2006, 80:308-322.
44. Vernon A.C., Crum W.R., Lerch J.P., Chege W., Natesan S., Modo M., Cooper J.D., Williams S.C., Kapur S. Reduced cortical volume and elevated astrocyte density in rats chronically treated with antipsychotic drugs-linking magnetic resonance imaging findings to cellular pathology. Biol. Psychiatry 2014, 75:982-990.
45. Vernon A.C., Natesan S., Crum W.R., Cooper J.D., Modo M., Williams S.C., Kapur S. Contrasting effects of haloperidol and lithium on rodent brain structure: a magnetic resonance imaging study with postmortem confirmation. Biol. Psychiatry 2012, 71:855-863.
46. Vernon A.C., Natesan S., Modo M., Kapur S. Effect of chronic antipsychotic treatment on brain structure: a serial magnetic resonance imaging study with ex vivo and postmortem confirmation. Biol. Psychiatry 2011, 69:936-944.
47. Wake H., Moorhouse A.J., Jinno S., Kohsaka S., Nabekura J. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 2009, 29:3974-3980.
48. Wierzba-Bobrowicz T., Lewandowska E., Lechowicz W., Stepien 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.
49. Wright I.C., Rabe-Hesketh S., Woodruff P.W., David A.S., Murray R.M., Bullmore E.T. Meta-analysis of regional brain volumes in schizophrenia. Am. J. Psychiatry 2000, 157:16-25.
50. Zatorre R.J., Fields R.D., Johansen-Berg H. Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat. Neurosci. 2012, 15:528-536.
51. Zhu F., Zheng Y., Ding Y.Q., Liu Y., Zhang X., Wu R., Guo X., Zhao J. Minocycline and risperidone prevent microglia activation and rescue behavioral deficits induced by neonatal intrahippocampal injection of lipopolysaccharide in rats. PLoS One 2014, 9:e93966.