Translocator protein (18 kDa) (TSPO) is expressed in reactive retinal microglia and modulates microglial inflammation and phagocytosis

Journal of Neuroinflammation

Volumn 11, Issue , 2014, Pages

  Karlstetter, Marcus ^a   Nothdurfter, Caroline ^b   Aslanidis, Alexander ^a   Moeller, Katharina ^a   Horn, Felicitas ^a   Scholz, Rebecca ^a   Neumann, Harald ^c   Weber, Bernhard H F ^b   Rupprecht, Rainer ^b   Langmann, Thomas ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

Microglia; Phagocytosis; Retinal degeneration; Translocator protein (18 kDa)

Indexed keywords

CASPASE 3; CASPASE 7; EMAPUNIL; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; LATEX; LIPOPOLYSACCHARIDE; MESSENGER RNA; MITOCHONDRIAL PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; NITRITE; RETINOSCHISIN; SHORT HAIRPIN RNA; TRANSLOCATOR PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; ANIMAL CELL; ARTICLE; CELL ASSAY; CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ANALYSIS; EXPLANT; FILOPODIUM; FLUORESCENCE ACTIVATED CELL SORTING; GLIOSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROGLIA; MIDDLE AGED; MOUSE; NEUROTOXICITY; NONHUMAN; PERINATAL PERIOD; PHAGOCYTOSIS; PHENOTYPE; PHOTORECEPTOR CELL; PLURIPOTENT STEM CELL; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RETINA CELL; RETINA DEGENERATION; RETINA DYSTROPHY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; UPREGULATION;

AGED; ANIMALS; CELL PROLIFERATION; DNA-BINDING PROTEINS; ENZYME INHIBITORS; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, KNOCKOUT; MICROGLIA; MIDDLE AGED; PHAGOCYTES; PSEUDOPODIA; PURINES; RECEPTORS, GABA; RETINA; TISSUE CULTURE TECHNIQUES; WOUND HEALING;

EID: 84892174249     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-11-3     Document Type: Article

References (41)

1. Papadopoulos V, Baraldi M, Guilarte TR, Knudsen TB, Lacapere JJ, Lindemann P, Norenberg MD, Nutt D, Weizman A, Zhang MR, Gavish M. Translocator protein (18 kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 2006, 27:402-409. 10.1016/j.tips.2006.06.005, 16822554.
2. McEnery MW, Snowman AM, Trifiletti RR, Snyder SH. Isolation of the mitochondrial benzodiazepine receptor: association with the voltage-dependent anion channel and the adenine nucleotide carrier. Proc Natl Acad Sci U S A 1992, 89:3170-3174. 10.1073/pnas.89.8.3170, 48827, 1373486.
3. Papadopoulos V, Liu J, Culty M. Is there a mitochondrial signaling complex facilitating cholesterol import?. Mol Cell Endocrinol 2007, 265-266:59-64.
4. Rupprecht R, Papadopoulos V, Rammes G, Baghai TC, Fan J, Akula N, Groyer G, Adams D, Schumacher M. Translocator protein (18 kDa) (TSPO) as a therapeutic target for neurological and psychiatric disorders. Nat Rev Drug Discov 2010, 9:971-988. 10.1038/nrd3295, 21119734.
5. Kuhlmann AC, Guilarte TR. Cellular and subcellular localization of peripheral benzodiazepine receptors after trimethyltin neurotoxicity. J Neurochem 2000, 74:1694-1704.
6. Maeda J, Higuchi M, Inaji M, Ji B, Haneda E, Okauchi T, Zhang MR, Suzuki K, Suhara T. Phase-dependent roles of reactive microglia and astrocytes in nervous system injury as delineated by imaging of peripheral benzodiazepine receptor. Brain Res 2007, 1157:100-111.
7. Veiga S, Azcoitia I, Garcia-Segura LM. Extragonadal synthesis of estradiol is protective against kainic acid excitotoxic damage to the hippocampus. Neuroreport 2005, 16:1599-1603. 10.1097/01.wnr.0000179081.39659.7d, 16148753.
8. Papadopoulos V, Berkovich A, Krueger KE, Costa E, Guidotti A. Diazepam binding inhibitor and its processing products stimulate mitochondrial steroid biosynthesis via an interaction with mitochondrial benzodiazepine receptors. Endocrinology 1991, 129:1481-1488. 10.1210/endo-129-3-1481, 1651852.
9. Girard C, Liu S, Adams D, Lacroix C, Sineus M, Boucher C, Papadopoulos V, Rupprecht R, Schumacher M, Groyer G. Axonal regeneration and neuroinflammation: roles for the translocator protein 18 kDa. J Neuroendocrinol 2012, 24:71-81. 10.1111/j.1365-2826.2011.02215.x, 21951109.
10. Chen MK, Guilarte TR. Translocator protein 18 kDa (TSPO): molecular sensor of brain injury and repair. Pharmacol Ther 2008, 118:1-17. 10.1016/j.pharmthera.2007.12.004, 2453598, 18374421.
11. Barron AM, Garcia-Segura LM, Caruso D, Jayaraman A, Lee JW, Melcangi RC, Pike CJ. Ligand for translocator protein reverses pathology in a mouse model of Alzheimer's disease. J Neurosci 2013, 33:8891-8897. 10.1523/JNEUROSCI.1350-13.2013, 3733563, 23678130.
12. Daugherty DJ, Selvaraj V, Chechneva OV, Liu XB, Pleasure DE, Deng W. A TSPO ligand is protective in a mouse model of multiple sclerosis. EMBO Mol Med 2013, 5:891-903. 10.1002/emmm.201202124, 3779450, 23681668.
13. Wei XH, Wei X, Chen FY, Zang Y, Xin WJ, Pang RP, Chen Y, Wang J, Li YY, Shen KF, Zhou LJ, Liu XG. The upregulation of translocator protein (18 kDa) promotes recovery from neuropathic pain in rats. J Neurosci 2013, 33:1540-1551. 10.1523/JNEUROSCI.0324-12.2013, 23345228.
14. Rupprecht R, Rammes G, Eser D, Baghai TC, Schule C, Nothdurfter C, Troxler T, Gentsch C, Kalkman HO, Chaperon F, Uzunov V, McAllister KH, Bertaina-Anglade V, La Rochelle CD, Tuerck D, Floesser A, Kiese B, Schumacher M, Landgraf R, Holsboer F, Kucher K. Translocator protein (18 kD) as target for anxiolytics without benzodiazepine-like side effects. Science 2009, 325:490-493. Erratum in: Science 2009, 325:1072. Dosage error in article text, 10.1126/science.1175055, 19541954.
15. Nothdurfter C, Rammes G, Baghai TC, Schule C, Schumacher M, Papadopoulos V, Rupprecht R. Translocator protein (18 kDa) as a target for novel anxiolytics with a favourable side-effect profile. J Neuroendocrinol 2012, 24:82-92. 10.1111/j.1365-2826.2011.02166.x, 21609361.
16. Nothdurfter C, Baghai TC, Schule C, Rupprecht R. Translocator protein (18 kDa) (TSPO) as a therapeutic target for anxiety and neurologic disorders. Eur Arch Psychiatry Clin Neurosci 2012, 262(Suppl 2):S107-S112.
17. Berger W, Kloeckener-Gruissem B, Neidhardt J. The molecular basis of human retinal and vitreoretinal diseases. Prog Retin Eye Res 2010, 29:335-375. 10.1016/j.preteyeres.2010.03.004, 20362068.
18. Langmann T. Microglia activation in retinal degeneration. J Leukoc Biol 2007, 81:1345-1351. 10.1189/jlb.0207114, 17405851.
19. Weber BH, Schrewe H, Molday LL, Gehrig A, White KL, Seeliger MW, Jaissle GB, Friedburg C, Tamm E, Molday RS. Inactivation of the murine X-linked juvenile retinoschisis gene, Rs1h, suggests a role of retinoschisin in retinal cell layer organization and synaptic structure. Proc Natl Acad Sci U S A 2002, 99:6222-6227. 10.1073/pnas.092528599, 122930, 11983912.
20. Gehrig A, Langmann T, Horling F, Janssen A, Bonin M, Walter M, Poths S, Weber BH. Genome-wide expression profiling of the retinoschisin-deficient retina in early postnatal mouse development. Invest Ophthalmol Vis Sci 2007, 48:891-900. 10.1167/iovs.06-0641, 17251492.
21. Ebert S, Weigelt K, Walczak Y, Drobnik W, Mauerer R, Hume DA, Weber BH, Langmann T. Docosahexaenoic acid attenuates microglial activation and delays early retinal degeneration. J Neurochem 2009, 110:1863-1875. 10.1111/j.1471-4159.2009.06286.x, 19627444.
22. Sasmono RT, Oceandy D, Pollard JW, Tong W, Pavli P, Wainwright BJ, Ostrowski MC, Himes SR, Hume DA. A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood 2003, 101:1155-1163. 10.1182/blood-2002-02-0569, 12393599.
23. Ebert S, Schoeberl T, Walczak Y, Stoecker K, Stempfl T, Moehle C, Weber BH, Langmann T. Chondroitin sulfate disaccharide stimulates microglia to adopt a novel regulatory phenotype. J Leukoc Biol 2008, 84:736-740. 10.1189/jlb.0208138, 18550791.
24. Beutner C, Roy K, Linnartz B, Napoli I, Neumann H. Generation of microglial cells from mouse embryonic stem cells. Nat Protoc 2010, 5:1481-1494. 10.1038/nprot.2010.90, 20725065.
25. Roy K, Beutner C, Neumann H. Perspectives of stem cell-derived microglia for medicine. Embryonic Stem Cells - Recent Advances in Pluripotent Stem Cell-Based Regenerative Medicine 2011, 171-188. Rijeka, Croatia: InTech Europe, Atwook C, Atwook C.
26. Da Settimo F, Simorini F, Taliani S, La Motta C, Marini AM, Salerno S, Bellandi M, Novellino E, Greco G, Cosimelli B, Da Pozzo E, Costa B, Simola N, Morelli M, Martini C. Anxiolytic-like effects of N, N-dialkyl-2-phenylindol-3-ylglyoxylamides by modulation of translocator protein promoting neurosteroid biosynthesis. J Med Chem 2008, 51:5798-5806. 10.1021/jm8003224, 18729350.
27. Chauveau F, Boutin H, Van Camp N, Dollé F, Tavitian B. Nuclear imaging of neuroinflammation: a comprehensive review of [11C]PK11195 challengers. Eur J Nucl Med Mol Imaging 2008, 35:2304-2319. 10.1007/s00259-008-0908-9, 18828015.
28. Venneti S, Lopresti BJ, Wiley CA. Molecular imaging of microglia/macrophages in the brain. Glia 2013, 61:10-23. 10.1002/glia.22357, 3580157, 22615180.
29. Karlstetter M, Walczak Y, Weigelt K, Ebert S, Van den Brulle J, Schwer H, Fuchshofer R, Langmann T. The novel activated microglia/macrophage WAP domain protein, AMWAP, acts as a counter-regulator of proinflammatory response. J Immunol 2010, 185:3379-3390. 10.4049/jimmunol.0903300, 20709948.
30. Chen MK, Baidoo K, Verina T, Guilarte TR. Peripheral benzodiazepine receptor imaging in CNS demyelination: functional implications of anatomical and cellular localization. Brain 2004, 127:1379-1392. 10.1093/brain/awh161, 15069023.
31. Chen MK, Guilarte TR. Imaging the peripheral benzodiazepine receptor response in central nervous system demyelination and remyelination. Toxicol Sci 2006, 91:532-539. 10.1093/toxsci/kfj172, 16554315.
32. Choi HB, Khoo C, Ryu JK, van Breemen E, Kim SU, McLarnon JG. Inhibition of lipopolysaccharide-induced cyclooxygenase-2, tumor necrosis factor-alpha and [Ca2+]i responses in human microglia by the peripheral benzodiazepine receptor ligand PK11195. J Neurochem 2002, 83:546-555. 10.1046/j.1471-4159.2002.01122.x, 12390516.
33. Ryu JK, Choi HB, McLarnon JG. Peripheral benzodiazepine receptor ligand PK11195 reduces microglial activation and neuronal death in quinolinic acid-injected rat striatum. Neurobiol Dis 2005, 20:550-561. 10.1016/j.nbd.2005.04.010, 15916899.
34. Cascio C, Brown RC, Liu Y, Han Z, Hales DB, Papadopoulos V. Pathways of dehydroepiandrosterone formation in rat brain glia. J Steroid Biochem Mol Biol 2000, 75:177-186. 10.1016/S0960-0760(00)00163-1, 11226834.
35. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318. 10.1126/science.1110647, 15831717.
36. Sierra A, Abiega O, Shahraz A, Neumann H. Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis. Front Cell Neurosci 2013, 7:6. 3558702, 23386811.
37. Ruff MR, Pert CB, Weber RJ, Wahl LM, Wahl SM, Paul SM. Benzodiazepine receptor-mediated chemotaxis of human monocytes. Science 1985, 229:1281-1283. 10.1126/science.2994216, 2994216.
38. Cosentino M, Marino F, Cattaneo S, Di Grazia L, Francioli C, Fietta AM, Lecchini S, Frigo G. Diazepam-binding inhibitor-derived peptides induce intracellular calcium changes and modulate human neutrophil function. J Leukoc Biol 2000, 67:637-643.
39. Marino F, Cattaneo S, Cosentino M, Rasini E, Di Grazia L, Fietta AM, Lecchini S, Frigo G. Diazepam stimulates migration and phagocytosis of human neutrophils: possible contribution of peripheral-type benzodiazepine receptors and intracellular calcium. Pharmacology 2001, 63:42-49. 10.1159/000056111, 11408831.
40. Rechichi M, Salvetti A, Chelli B, Costa B, Da Pozzo E, Spinetti F, Lena A, Evangelista M, Rainaldi G, Martini C, Gremigni V, Rossi L. TSPO over-expression increases motility, transmigration and proliferation properties of C6 rat glioma cells. Biochim Biophys Acta 2008, 1782:118-125. 10.1016/j.bbadis.2007.12.001, 18190798.
41. Guidotti A, Forchetti CM, Corda MG, Konkel D, Bennett CD, Costa E. Isolation, characterization, and purification to homogeneity of an endogenous polypeptide with agonistic action on benzodiazepine receptors. Proc Natl Acad Sci U S A 1983, 80:3531-3535. 10.1073/pnas.80.11.3531, 394079, 6304714.