Morphological features of microglial cells in the hippocampal dentate gyrus of Gunn rat: A possible schizophrenia animal model

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Liaury, Kristian ^a,b   Miyaoka, Tsuyoshi ^a   Tsumori, Toshiko ^a   Furuya, Motohide ^a   Wake, Rei ^a   Ieda, Masa ^a   Tsuchie, Keiko ^a   Taki, Michiyo ^a   Ishihara, Kotomi ^a   Tanra, Andi J ^b   Horiguchi, Jun ^a  

^a SHIMANE UNIVERSITY FACULTY OF MEDICINE   (Japan)

^b HASANUDDIN UNIVERSITY   (Indonesia)

Author keywords

Dentate gyrus; Gunn rats; Microglial cells; Schizophrenia

Indexed keywords

BILIRUBIN; CD11B ANTIGEN; ACTIN BINDING PROTEIN; AIF1 PROTEIN, RAT; CALCIUM BINDING PROTEIN; ENOLASE;

ADULT ANIMAL; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ANTIGEN EXPRESSION; ARTICLE; CELL ACTIVATION; CELL COUNT; CELL INTERACTION; CELL PHAGOCYTOSIS; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOARCHITECTURE; DENTATE GYRUS; DENTATE HILUS; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; NERVE CELL DIFFERENTIATION; NONHUMAN; ORGANELLE SIZE; RAT; SCHIZOPHRENIA; ANIMAL; CYTOLOGY; GUNN RAT; METABOLISM; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WISTAR RAT;

ANIMALS; ANTIGENS, CD11B; CALCIUM-BINDING PROTEINS; CELL COUNT; DENTATE GYRUS; MALE; MICROFILAMENT PROTEINS; MICROGLIA; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; PHOSPHOPYRUVATE HYDRATASE; RATS; RATS, GUNN; RATS, WISTAR;

EID: 84858260810     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-56     Document Type: Article

References (49)

1. Saha S, Chant D, Welham J, McGrath J. A systematic review of the prevalence of schizophrenia. PLoS Med 2005, 2:413-433.
2. Monji A, Kato T, Kanba S. Cytokines and schizophrenia: microglia hypothesis of schizophrenia. Psychiatry Clin Neurosci 2009, 63:257-265. 10.1111/j.1440-1819.2009.01945.x, 19579286.
3. Stefansson H, Ophoff RA, Steinberg S, Andreassen OA, Cichon S, Rujescu D, Werge T, Pietiläinen OP, Mors O, Mortensen PB, Sigurdsson E, Gustafsson O, Nyegaard M, Tuulio-Henriksson A, Ingason A, Hansen T, Suvisaari J, Lonnqvist J, Paunio T, Børglum AD, Hartmann A, Fink-Jensen A, Nordentoft M, Hougaard D, Norgaard-Pedersen B, Böttcher Y, Olesen J, Breuer R, Möller HJ, Giegling I, et al. Common variants conferring risk of schizophrenia. Nature 2009, 460:744-748. 3077530, 19571808.
4. Miller BJ, Buckley P, Seabott W, Mellor A, Kirkpatrick B. Meta-analysis of cytokine alterations in schizophrenia: clinical studies and antipsychotic effects. Biol Psychiatry 2011, 70:663-671. 10.1016/j.biopsych.2011.04.013, 21641581.
5. Drexhage RC, Knijff EM, Padmos RC, Heul-Nieuwenhuijzen L, Beumer W, Versnel MA, Drexhage HA. The mononuclear phagocyte system and its cytokine inflammatory networks in schizophrenia and bipolar disorder. Expert Rev Neurother 2010, 10:59-76. 10.1586/ern.09.144, 20021321.
6. Steiner J, Mawrin C, Ziegeler A, Bielau H, Ullrich O, Bernstein HG, Bogerts B. Distribution of HLA-DR-positive microglia in schizophrenia reflects impaired cerebral lateralization. Acta Neuropathol 2006, 112:305-316. 10.1007/s00401-006-0090-8, 16783554.
7. Steiner J, Bielau H, Brisch R, Danos P, Ullrich O, Mawrin C, Bernstein HG, 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. 10.1016/j.jpsychires.2006.10.013, 17174336.
8. Muller N, Myint AM, Schwarz MJ. Kynurenine pathway in schizophrenia: pathophysiological and therapeutic aspects. Curr Pharm Des 2011, 17:130-136. 10.2174/138161211795049552, 21361867.
9. Steiner J, Bogerts B, Sarnyai Z, Walter M, Gos T, Bernstein HG, Myint AM. Bridging the gap between the immune and glutamate hypotheses of schizophrenia and major depression: potential role of glial NMDA receptor modulators and impaired blood-brain barrier integrity. World J Biol Psychiatry
10. Muller N, Schiller P, Ackenheil M. Coincidence of schizophrenia and hyperbilirubinemia. Pharmacopsychiatry 1991, 24:225-228. 10.1055/s-2007-1014472, 1812499.
11. Miyaoka T, Seno H, Itoga M, Iijima M, Inagaki T, Horiguchi J. Schizophrenia-associated idiopathic unconjugated bilirubinemia (Gilbert's syndrome). J Clin Psychiatry 2000, 61:868-871. 10.4088/JCP.v61n1110, 11105741.
12. Radhakrishnan R, Kanigere M, Menon J, Calvin S, Janish A, Srinivasan K. Association between unconjugated bilirubin and schizophrenia. Psychiatry Res 2011, 189:480-482. 10.1016/j.psychres.2011.03.003, 21470692.
13. Miyaoka T, Yasukawa R, Mizuno S, Sukegawa T, Inagaki T, Horiguchi J, Seno H, Oda K, Kitagaki H. Proton magnetic resonance spectroscopy (1H-MRS) of hippocampus, basal ganglia, and vermis of cerebellum in schizophrenia associated with idiopathic unconjugated hyperbilirubinemia (Gilbert's syndrome). J Psychiatr Res 2005, 39:29-34. 10.1016/j.jpsychires.2004.05.003, 15504421.
14. Yasukawa R, Miyaoka T, Mizuno S, Inagaki T, Horiguchi J, Oda K, Kitagaki H. Proton magnetic resonance spectroscopy of the anterior cingulated gyrus, insular cortex and thalamus in schizophrenia associated with idiopathic unconjugated hyperbilirubinemia (Gilbert's syndrome). J Psychiatry Neurosci 2005, 30:416-422. 1277024, 16327875.
15. Miyaoka T, Yasukawa R, Mihara T, Mizuno S, Yasuda H, Sukegawa T, Hayashida M, Inagaki T, Horiguchi J. Fluid-attenuated inversion-recovery MR imaging in schizophrenia-associated with idiopathic unconjugated hyperbilirubinemia (Gilbert's syndrome). Eur Psychiatry 2005, 20:327-331. 10.1016/j.eurpsy.2004.12.012, 16018925.
16. Wake R, Miyaoka T, Tsuchie K, Kawakami K, Nishida A, Inagaki T, Horiguchi J. Abnormalities in MRI signal intensity in schizophrenia associated with idiopathic unconjugated hyperbilirubinemia. Aus N Z J Psychiatry 2009, 43:1057-1069.
17. Dennery PA, Seidman DS, Stevenson DK. Neonatal hyperbilirubinemia. N Engl J Med 2001, 344:581-590. 10.1056/NEJM200102223440807, 11207355.
18. Hansen TWR. Mechanism of bilirubin toxicity: clinical implications. Clin Perinatol 2002, 29:765-778. 10.1016/S0095-5108(02)00053-2, 12516745.
19. Porter ML, Dennis BL. Hyperbilirubinemia in the term newborn. Am Fam Physician 2002, 65:599-606.
20. Shapiro SM. Definition of the clinical spectrum of kernicterus and bilirubin-induced neurologic dysfunction (BIND). J Perinatol 2005, 25:54-59. 10.1038/sj.jp.7211157, 15578034.
21. Dalman C, Cullberg J. Neonatal hyperbilirubinemia-vulnerability factor for mental disorder?. Acta Psychiatr Scand 1999, 100:469-471. 10.1111/j.1600-0447.1999.tb10899.x, 10626927.
22. Hayashida M, Miyaoka T, Tsuchie K, Yasuda H, Wake R, Nishida A, Inagaki T, Toga T, Hagami H, Oda T, Horiguchi J. Hyperbilirubinemia-related behavioral and neuropathological changes in rats: a possible schizophrenia animal model. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33:581-588. 10.1016/j.pnpbp.2009.02.013, 19249333.
23. Gunn CK. Hereditary acholuric jaundice in the rat. Can Med Assoc J 1944, 50:230-237. 1581738, 20323028.
24. Silva RFM, Rodriques CM, Brites D. Rat cultured neuronal and glial cells respond differently to toxicity of unconjugated bilirubin. Pediatr Res 2002, 51:535-541. 10.1203/00006450-200204000-00022, 11919342.
25. Gordo AC, Falcão AS, Fernandes A, Brito MA, Slva RFM, Brites D. Unconjugated bilirubin activates and damages microglia. J Neurosci Res 2006, 84:194-201. 10.1002/jnr.20857, 16612833.
26. Silva SL, Vaz AR, Barateiro A, Falcão AS, Fernandes A, Brito MA, Silva RFM, Brites D. Features of bilirubin-induced reactive microglia: from phagocytosis to inflammation. Neurobiol Dis 2010, 40:663-675. 10.1016/j.nbd.2010.08.010, 20727973.
27. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates 2007, London: Elsevier Inc, 6.
28. Streit WJ, Graeber MB, Kreutzberg GW. Functional plasticity of microglia: a review. Glia 1988, 1:301-307. 10.1002/glia.440010502, 2976393.
29. Nimmerjahn A, Kirchhcoff F, Helmchen F. Resting microglia cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318. 10.1126/science.1110647, 15831717.
30. Shapiro LA, Perez ZD, Foresti ML, Arisi GM, Ribak CE. Morphological and ultrastructural features of Iba1-immunolabeled microglial cells in the hippocampal dentate gyrus. Brain Res 2009, 1266:29-36. 2677570, 19249294.
31. Sierra A, Encinas JM, Deudero JJP, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, Tsirka SE, Maletic-Savatic M. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 2010, 7:483-495. 10.1016/j.stem.2010.08.014, 20887954.
32. Rossum VD, Hanisch UK. Microglia. Metab Brain Dis 2004, 19:393-411.
33. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007, 10:1387-1394. 10.1038/nn1997, 17965659.
34. Graeber MB. Changing face of microglia. Science 2010, 330:783-788. 10.1126/science.1190929, 21051630.
35. Streit WJ, Walter SA, Pennel NA. Reactive microgliosis. Prog Neurobiol 1999, 57:563-581. 10.1016/S0301-0082(98)00069-0, 10221782.
36. Bessis A, Béchade C, Bernard D, Roumier A. Microglial control of neuronal death and synaptic properties. Glia 2007, 55:233-238. 10.1002/glia.20459, 17106878.
37. Ladeby R, Wirenfeldt M, Garcia-Overejo D, Fenger C, Dissing Olsen L, Dalmau I, Finsen B. Microglial cell population dynamics in the injured adult central nervous system. Brain Res Rev 2005, 48:196-206. 10.1016/j.brainresrev.2004.12.009, 15850658.
38. Hailer NP, Grampp A, Nitsch R. Proliferation of microglia and astrocytes in the dentate gyrus following entohirnal cortex lesion: a quantitative bromodeoxyuridine-labelling study. Eur J Neurosci 1999, 11:3359-3364. 10.1046/j.1460-9568.1999.00808.x, 10510203.
39. Ahdab-Barmada M, Moossy J. The neuropathology of kernicterus in the premature neonate: diagnostic problems. J Neuropathol Exp Neurol 1984, 43:45-52. 10.1097/00005072-198401000-00004, 6693927.
40. Johnson L, Sarmiento F, Blanc WA, Day R. Kernicterus in rats with inherited deficiency of glucuronyl transferase. AMA J Dis Child 1959, 97:591-608.
41. McDonald JW, Shapiro SM, Silverstein FS, Johnston MV. Role of glutamate receptor-mediated excitotoxicity in bilirubin-induced brain injury in the Gunn rat model. Exp Neurol 1998, 150:21-29. 10.1006/exnr.1997.6762, 9514835.
42. Ekdahl CT, Kokaia Z, Lindvall O. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 2009, 158:1021-1029. 10.1016/j.neuroscience.2008.06.052, 18662748.
43. Doorduin J, de Vries EFJ, Willemsen ATM, de Groot JC, Dierckx RA, Klein HC. Neuroinflammation in schizophrenia-related psychosis: a PET study. J Nucl Med 2009, 50:1801-1807. 10.2967/jnumed.109.066647, 19837763.
44. Lin A, Kenis G, Bignotti S, Tura GJ, de Jong R, Bosmans E, Pioli R, Altamura C, Scharpé S, Maes M. The inflammatory response system in treatment-resistant schizophrenia: increased serum interleukin-6. Schizophr Res 1998, 32:9-15. 10.1016/S0920-9964(98)00034-6, 9690329.
45. Zhang XY, Zhou DF, Cao LY, Zhang PY, Wu GY, Shen YC. Changes in serum interleukin-2, -6, and -8 levels before and during treatment with risperidone and haloperidol: relationship to outcome in schizophrenia. J Clin Psychiatry 2004, 65:940-947. 10.4088/JCP.v65n0710, 15291683.
46. Akhondzadeh S, Tabatabaee M, Amini H, Ahmadi Abhari SA, Abbasi SH, Behnam B. Celecoxib as adjunctive therapy in schizophrenia: a double-blind, randomized, and placebo-controlled trial. Schizophr Res 2007, 90:179-185. 10.1016/j.schres.2006.11.016, 17208413.
47. Miyaoka T, Yasukawa R, Yasuda H, Hayashida M, Inagaki T, Horiguchi J. Minocycline as adjunctive therapy for schizophrenia: an open-label study. Clin Neuropharmacol 2008, 315:287-292.
48. Kato T, Monji A, Hashioka S, Kanba S. Risperidone significantly inhibits interferon-gamma-induced microglial activation in vitro. Schizophr Res 2007, 92:108-115. 10.1016/j.schres.2007.01.019, 17363222.
49. Bian Q, Kato T, Monji A, Hashioka S, Mizoguchi Y, Horikawa H, Kanba S. The effect of atypical antipsychotics, perospirone, ziprasidone, and quetiapine on microglial activation induced by interferon-gamma. Prog Neuropsychopharmacol Biol Psychiatry 2008, 32:42-48. 10.1016/j.pnpbp.2007.06.031, 17716796.