Cited by 192Neuroinflammation and Neurodegeneration MechanismsPharmacological Receptor Mechanisms and EffectsMedical Imaging Techniques and Applications

Cellular sources of TSPO expression in healthy and diseased brain

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Nutma, Erik, Ceyzériat, Kelly, Amor, Sandra, Tsartsalis, Stergios, Millet, Philippe, Owen, David R., Papadopoulos, Vassilios, Tournier, Benjamin B.·2021·European Journal of Nuclear Medicine and Molecular Imaging

Abstract

The 18 kDa translocator protein (TSPO) is a highly conserved protein located in the outer mitochondrial membrane. TSPO binding, as measured with positron emission tomography (PET), is considered an in vivo marker of neuroinflammation. Indeed, TSPO expression is altered in neurodegenerative, neuroinflammatory, and neuropsychiatric diseases. In PET studies, the TSPO signal is often viewed as a marker of microglial cell activity. However, there is little evidence in support of a microglia-specific TSPO expression. This review describes the cellular sources and functions of TSPO in animal models of disease and human studies, in health, and in central nervous system diseases. A discussion of methods of analysis and of quantification of TSPO is also presented. Overall, it appears that the alterations of TSPO binding, their cellular underpinnings, and the functional significance of such alterations depend on many factors, notably the pathology or the animal model under study, the disease stage, and the involved brain regions. Thus, further studies are needed to fully determine how changes in TSPO binding occur at the cellular level with the ultimate goal of revealing potential therapeutic pathways.

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  • TSPO is expressed in almost all CNS cells, including astrocytes, neurons and endothelial cells.

    “Although increased TSPO expression has historically been mostly associated with microglial activation, TSPO is now known to be expressed in almost all CNS cells including astrocytes, neurons and endothelial cells [21–27], all of which may also be involved in, or be affected by neuroinflammation [28].”

    From Pharmacological modulation of TSPO in microglia/macrophages and neurons in a chronic neurodegenerative model of prion disease (2023) · cites this paper as [22]

    The Introduction and Conclusion say TSPO occurs in astrocytes and endothelial cells as well as microglia. But the Wild-type section says its expression varies by brain region and that neurons generally lack TSPO in the mouse brain, while noting particular neuronal exceptions. The source therefore does not support the unqualified claim that TSPO is expressed in almost all CNS cells. (LLM, conf=0.88)

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  1. [1]Guilarte TR TSPO in diverse CNS pathologies and psychiatric disease: a critical review and a way forward Pharmacol Ther 2019 194 44 58 10.1016/j.pharmthera.2018.09.003 30189290 PMC6348013 · DOI · Paper page
  2. [2]Guilarte TR. TSPO in diverse CNS pathologies and psychiatric disease: a critical review and a way forward. Pharmacol Ther. 2018. 10.1016/j.pharmthera.2018.09.003. PMC6348013 30189290 · DOI · Paper page
  3. [4]Gui Y Marks JD Das S Hyman BT Serrano-Pozo A Characterization of the 18 kDa translocator protein (TSPO) expression in post-mortem normal and Alzheimer’s disease brains Brain Pathol 2020 30 151 164 10.1111/bpa.12763 31276244 PMC6904423 · DOI · Paper page
  4. [8]Ahmad R Koole M Evens N Serdons K Verbruggen A Bormans G Whole-body biodistribution and radiation dosimetry of the cannabinoid type 2 receptor ligand [11C]-NE40 in healthy subjects Mol Imaging Biol 2013 15 384 390 10.1007/s11307-013-0626-y 23508466 · DOI
  5. [9]Attili B Celen S Ahamed M Koole M Haute CVD Vanduffel W Preclinical evaluation of [(18) F]MA3: a CB(2) receptor agonist radiotracer for PET Br J Pharmacol 2019 176 1481 1491 10.1111/bph.14564 30588600 PMC6487560 · DOI
  6. [10]Kumar JSD Prabhakaran J Molotkov A Sattiraju A Kim J Doubrovin M Radiosynthesis and evaluation of [(18)F]FMTP, a COX-2 PET ligand Pharmacol Rep 2020 72 1433 1440 10.1007/s43440-020-00124-z 32632914 · DOI
  7. [11]Shrestha S Kim MJ Eldridge M Lehmann ML Frankland M Liow JS PET measurement of cyclooxygenase-2 using a novel radioligand: upregulation in primate neuroinflammation and first-in-human study J Neuroinflammation 2020 17 140 10.1186/s12974-020-01804-6 32359360 PMC7195739 · DOI
  8. [12]Hosoya T Fukumoto D Kakiuchi T Nishiyama S Yamamoto S Ohba H In vivo TSPO and cannabinoid receptor type 2 availability early in post-stroke neuroinflammation in rats: a positron emission tomography study J Neuroinflammation 2017 14 69 10.1186/s12974-017-0851-4 28356120 PMC5372312 · DOI
  9. [13]Pottier G Gómez-Vallejo V Padro D Boisgard R Dollé F Llop J PET imaging of cannabinoid type 2 receptors with [(11)C]A-836339 did not evidence changes following neuroinflammation in rats J Cereb Blood Flow Metab 2017 37 1163 1178 10.1177/0271678×16685105 28079433 PMC5363492 · DOI
  10. [14]Territo PR Meyer JA Peters JS Riley AA McCarthy BP Gao M Characterization of (11)C-GSK1482160 for targeting the P2X7 receptor as a biomarker for neuroinflammation J Nucl Med 2017 58 458 465 10.2967/jnumed.116.181354 27765863 · DOI
  11. [15]Berdyyeva T Xia C Taylor N He Y Chen G Huang C PET Imaging of the P2X7 ion channel with a novel tracer [(18)F]JNJ-64413739 in a rat model of neuroinflammation Mol Imaging Biol 2019 21 871 878 10.1007/s11307-018-01313-2 30632003 · DOI
  12. [16]Kolb HC Barret O Bhattacharya A Chen G Constantinescu C Huang C Preclinical evaluation and nonhuman primate receptor occupancy study of (18)F-JNJ-64413739, a PET radioligand for P2X7 receptors J Nucl Med 2019 60 1154 1159 10.2967/jnumed.118.212696 30733317 · DOI
  13. [17]Liu H Jin H Yue X Luo Z Liu C Rosenberg AJ PET imaging study of S1PR1 expression in a rat model of multiple sclerosis Mol Imaging Biol 2016 18 724 732 10.1007/s11307-016-0944-y 26975859 PMC5297893 · DOI
  14. [18]Weng CC Carlin S Hou C Metz T Li S Lee H Correlation analysis of [(18)F]ROStrace using ex vivo autoradiography and dihydroethidium fluorescent imaging in lipopolysaccharide-treated animals Biochem Biophys Res Commun 2019 516 397 401 10.1016/j.bbrc.2019.06.062 31221481 · DOI
  15. [19]Horti AG Naik R Foss CA Minn I Misheneva V Du Y PET imaging of microglia by targeting macrophage colony-stimulating factor 1 receptor (CSF1R) Proc Natl Acad Sci U S A 2019 116 1686 1691 10.1073/pnas.1812155116 30635412 PMC6358677 · DOI
  16. [20]Papadopoulos V Baraldi M Guilarte TR Knudsen TB Lacapere JJ Lindemann P 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 · DOI
  17. [21]Rupprecht R Papadopoulos V Rammes G Baghai TC Fan J Akula N 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 · DOI · Paper page
  18. [22]Veenman L Papadopoulos V Gavish M Channel-like functions of the 18-kDa translocator protein (TSPO): regulation of apoptosis and steroidogenesis as part of the host-defense response Curr Pharm Des 2007 13 2385 2405 10.2174/138161207781368710 17692008 · DOI
  19. [24]Austin CJ Kahlert J Kassiou M Rendina LM The translocator protein (TSPO): a novel target for cancer chemotherapy Int J Biochem Cell Biol 2013 45 1212 1216 10.1016/j.biocel.2013.03.004 23518318 · DOI
  20. [25]Batarseh A, Papadopoulos V. Regulation of translocator protein 18 kDa (TSPO) expression in health and disease states. Mol Cell Endocrinol. 2010;327(1-12). 10.1016/j.mce.2010.06.013. PMC2922062 20600583 · DOI
  21. [26]Caballero B Veenman L Gavish M Role of mitochondrial translocator protein (18 kDa) on mitochondrial-related cell death processes Recent Pat Endocr Metab Immune Drug Discovery 2013 7 86 101 10.2174/1872214811307020002 23368281 · DOI
  22. [27]Papadopoulos V Peripheral-type benzodiazepine/diazepam binding inhibitor receptor: biological role in steroidogenic cell function Endocr Rev 1993 14 222 240 10.1210/edrv-14-2-222 8391980 · DOI · Paper page
  23. [28]Veenman L Gavish M The peripheral-type benzodiazepine receptor and the cardiovascular system. Implications for drug development Pharmacol Ther 2006 110 503 524 10.1016/j.pharmthera.2005.09.007 16337685 · DOI
  24. [29]Galiegue S Casellas P Kramar A Tinel N Simony-Lafontaine J Immunohistochemical assessment of the peripheral benzodiazepine receptor in breast cancer and its relationship with survival Clin Cancer Res 2004 10 2058 2064 10.1158/1078-0432.ccr-03-0988 15041726 · DOI
  25. [30]Tonon MC, Vaudry H, Chuquet J, Guillebaud F, Fan J, Masmoudi-Kouki O, et al. Endozepines and their receptors: structure, functions and pathophysiological significance. Pharmacol Ther. 2019:107386. 10.1016/j.pharmthera.2019.06.008. 31283949 · DOI
  26. [31]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 18374421 PMC2453598 · DOI · Paper page
  27. [32]Taliani S Da Settimo F Da Pozzo E Chelli B Martini C Translocator protein ligands as promising therapeutic tools for anxiety disorders Curr Med Chem 2009 16 3359 3380 10.2174/092986709789057653 19548867 · DOI
  28. [33]Liu GJ Middleton RJ Hatty CR Kam WW Chan R Pham T The 18 kDa translocator protein, microglia and neuroinflammation Brain Pathol 2014 24 631 653 10.1111/bpa.12196 25345894 PMC8029074 · DOI
  29. [34]Wang HJ Fan J Papadopoulos V Translocator protein (Tspo) gene promoter-driven green fluorescent protein synthesis in transgenic mice: an in vivo model to study Tspo transcription Cell Tissue Res 2012 350 261 275 10.1007/s00441-012-1478-5 22868914 PMC3740157 · DOI
  30. [35]Bribes E Carriere D Goubet C Galiegue S Casellas P Simony-Lafontaine J Immunohistochemical assessment of the peripheral benzodiazepine receptor in human tissues J Histochem Cytochem 2004 52 19 28 10.1177/002215540405200103 14688214 · DOI · Paper page
  31. [36]Katz Y Ben-Baruch G Kloog Y Menczer J Gavish M Increased density of peripheral benzodiazepine-binding sites in ovarian carcinomas as compared with benign ovarian tumours and normal ovaries Clin Sci (Lond) 1990 78 155 158 10.1042/cs0780155 2155741 · DOI
  32. [37]Bhoola NH, Mbita Z, Hull R, Dlamini Z. Translocator protein (TSPO) as a potential biomarker in human cancers. Int J Mol Sci. 2018;19. 10.3390/ijms19082176. PMC6121633 30044440 · DOI
  33. [38]Han Z Slack RS Li W Papadopoulos V Expression of peripheral benzodiazepine receptor (PBR) in human tumors: relationship to breast, colorectal, and prostate tumor progression J Recept Signal Transduct Res 2003 23 225 238 10.1081/rrs-120025210 14626449 · DOI
  34. [39]Batarseh A Barlow KD Martinez-Arguelles DB Papadopoulos V Functional characterization of the human translocator protein (18 kDa) gene promoter in human breast cancer cell lines Biochim Biophys Acta 2012 1819 38 56 10.1016/j.bbagrm.2011.09.001 21958735 PMC3249510 · DOI
  35. [40]Hardwick M Cavalli LR Barlow KD Haddad BR Papadopoulos V Peripheral-type benzodiazepine receptor (PBR) gene amplification in MDA-MB-231 aggressive breast cancer cells Cancer Genet Cytogenet 2002 139 48 51 10.1016/s0165-4608(02)00604-0 12547158 · DOI
  36. [41]Anholt RR Pedersen PL De Souza EB Snyder SH The peripheral-type benzodiazepine receptor. Localization to the mitochondrial outer membrane J Biol Chem 1986 261 576 583 10.1016/S0021-9258(17)36131-8 3001071 · DOI
  37. [42]Garnier M Boujrad N Oke BO Brown AS Riond J Ferrara P Diazepam binding inhibitor is a paracrine/autocrine regulator of Leydig cell proliferation and steroidogenesis: action via peripheral-type benzodiazepine receptor and independent mechanisms Endocrinology. 1993 132 444 458 10.1210/endo.132.1.8380386 8380386 · DOI
  38. [43]Hardwick M Fertikh D Culty M Li H Vidic B Papadopoulos V Peripheral-type benzodiazepine receptor (PBR) in human breast cancer: correlation of breast cancer cell aggressive phenotype with PBR expression, nuclear localization, and PBR-mediated cell proliferation and nuclear transport of cholesterol Cancer Res 1999 59 831 842 10029072
  39. [44]Doble A Ferris O Burgevin MC Menager J Uzan A Dubroeucq MC Photoaffinity labeling of peripheral-type benzodiazepine-binding sites Mol Pharmacol 1987 31 42 49 3027525
  40. [45]Antkiewicz-Michaluk L Mukhin AG Guidotti A Krueger KE Purification and characterization of a protein associated with peripheral-type benzodiazepine binding sites J Biol Chem 1988 263 17317 17321 10.1016/S0021-9258(19)77838-7 2846560 · DOI
  41. [46]Riond J Vita N Le Fur G Ferrara P Characterization of a peripheral-type benzodiazepine-binding site in the mitochondria of Chinese hamster ovary cells FEBS Lett 1989 245 238 244 10.1016/0014-5793(89)80229-7 2538361 · DOI
  42. [47]Sprengel R Werner P Seeburg PH Mukhin AG Santi MR Grayson DR Molecular cloning and expression of cDNA encoding a peripheral-type benzodiazepine receptor J Biol Chem 1989 264 20415 20421 10.1016/S0021-9258(19)47078-6 2555358 · DOI
  43. [48]Riond J Mattei MG Kaghad M Dumont X Guillemot JC Le Fur G Molecular cloning and chromosomal localization of a human peripheral-type benzodiazepine receptor Eur J Biochem 1991 195 305 311 10.1111/j.1432-1033.1991.tb15707.x 1847678 · DOI
  44. [49]Chang YJ McCabe RT Rennert H Budarf ML Sayegh R Emanuel BS The human “peripheral-type” benzodiazepine receptor: regional mapping of the gene and characterization of the receptor expressed from cDNA DNA Cell Biol 1992 11 471 480 10.1089/dna.1992.11.471 1326278 · DOI
  45. [50]Parola AL Stump DG Pepperl DJ Krueger KE Regan JW Laird HE 2nd Cloning and expression of a pharmacologically unique bovine peripheral-type benzodiazepine receptor isoquinoline binding protein J Biol Chem 1991 266 14082 14087 10.1016/S0021-9258(18)92812-7 1649835 · DOI
  46. [52]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 1373486 PMC48827 · DOI · Paper page
  47. [53]Levitt D Gramicidin, VDAC, porin and perforin channels Curr Opin Cell Biol 1990 2 689 694 10.1016/0955-0674(90)90112-r 1701307 · DOI
  48. [54]Le Fur G Vaucher N Perrier ML Flamier A Benavides J Renault C Differentiation between two ligands for peripheral benzodiazepine binding sites, [3H]RO5-4864 and [3H]PK 11195, by thermodynamic studies Life Sci 1983 33 449 457 10.1016/0024-3205(83)90794-4 6308375 · DOI
  49. [55]Rone MB Liu J Blonder J Ye X Veenstra TD Young JC Targeting and insertion of the cholesterol-binding translocator protein into the outer mitochondrial membrane Biochemistry. 2009 48 6909 6920 10.1021/bi900854z 19552401 PMC2748833 · DOI
  50. [57]Li F Liu J Liu N Kuhn LA Garavito RM Ferguson-Miller S Translocator protein 18 kDa (TSPO): an old protein with new functions? Biochemistry. 2016 55 2821 2831 10.1021/acs.biochem.6b00142 27074410 PMC5125027 · DOI
  51. [60]Issop L Rone MB Papadopoulos V Organelle plasticity and interactions in cholesterol transport and steroid biosynthesis Mol Cell Endocrinol 2013 371 34 46 10.1016/j.mce.2012.12.003 23246788 · DOI
  52. [61]Aghazadeh Y Zirkin BR Papadopoulos V Pharmacological regulation of the cholesterol transport machinery in steroidogenic cells of the testis Vitam Horm 2015 98 189 227 10.1016/bs.vh.2014.12.006 25817870 · DOI
  53. [62]Oke BO Suarez-Quian CA Riond J Ferrara P Papadopoulos V Cell surface localization of the peripheral-type benzodiazepine receptor (PBR) in adrenal cortex Mol Cell Endocrinol 1992 87 R1 R6 10.1016/0303-7207(92)90248-5 1332905 · DOI
  54. [63]Hirsch JD Beyer CF Malkowitz L Beer B Blume AJ Mitochondrial benzodiazepine receptors mediate inhibition of mitochondrial respiratory control Mol Pharmacol 1989 35 157 163 2464128
  55. [64]Larcher JC Vayssiere JL Le Marquer FJ Cordeau LR Keane PE Bachy A Effects of peripheral benzodiazepines upon the O2 consumption of neuroblastoma cells Eur J Pharmacol 1989 161 197 202 10.1016/0014-2999(89)90843-1 2542045 · DOI
  56. [65]Lejri I Grimm A Halle F Abarghaz M Klein C Maitre M TSPO ligands boost mitochondrial function and pregnenolone synthesis J Alzheimers Dis 2019 72 1045 1058 10.3233/JAD-190127 31256132 PMC6971832 · DOI
  57. [66]Papadopoulos V Aghazadeh Y Fan J Campioli E Zirkin B Midzak A Translocator protein-mediated pharmacology of cholesterol transport and steroidogenesis Mol Cell Endocrinol 2015 408 90 98 10.1016/j.mce.2015.03.014 25818881 PMC4417383 · DOI
  58. [67]Papadopoulos V, Fan J, Zirkin B. Translocator protein (18 kDa): an update on its function in steroidogenesis. J Neuroendocrinol. 2018;30. 10.1111/jne.12500. PMC5748373 28667781 · DOI
  59. [68]Costa E Auta J Guidotti A Korneyev A Romeo E The pharmacology of neurosteroidogenesis J Steroid Biochem Mol Biol 1994 49 385 389 10.1016/0960-0760(94)90284-4 8043504 · DOI
  60. [69]Papadopoulos V Guarneri P Kreuger KE Guidotti A Costa E Pregnenolone biosynthesis in C6-2B glioma cell mitochondria: regulation by a mitochondrial diazepam binding inhibitor receptor Proc Natl Acad Sci U S A 1992 89 5113 5117 10.1073/pnas.89.11.5113 1317581 PMC49239 · DOI
  61. [70]Arbo BD Benetti F Garcia-Segura LM Ribeiro MF Therapeutic actions of translocator protein (18 kDa) ligands in experimental models of psychiatric disorders and neurodegenerative diseases J Steroid Biochem Mol Biol 2015 154 68 74 10.1016/j.jsbmb.2015.07.007 26200949 · DOI
  62. [71]Porcu P Barron AM Frye CA Walf AA Yang SY He XY Neurosteroidogenesis today: novel targets for neuroactive steroid synthesis and action and their relevance for translational research J Neuroendocrinol 2016 28 12351 10.1111/jne.12351 26681259 PMC4769676 · DOI
  63. [72]Falchi AM Battetta B Sanna F Piludu M Sogos V Serra M Intracellular cholesterol changes induced by translocator protein (18 kDa) TSPO/PBR ligands Neuropharmacology. 2007 53 318 329 10.1016/j.neuropharm.2007.05.016 17631921 · DOI
  64. [73]Chung JY, Chen H, Papadopoulos V, Zirkin B. Cholesterol accumulation, lipid droplet formation, and steroid production in Leydig cells: role of translocator protein (18-kDa). Andrology. 2019. 10.1111/andr.12733. 31738001 · DOI
  65. [74]Lacapere JJ Duma L Finet S Kassiou M Papadopoulos V Insight into the structural features of TSPO: implications for drug development Trends Pharmacol Sci 2020 41 110 122 10.1016/j.tips.2019.11.005 31864680 PMC7021566 · DOI
  66. [75]Costa B Da Pozzo E Giacomelli C Barresi E Taliani S Da Settimo F TSPO ligand residence time: a new parameter to predict compound neurosteroidogenic efficacy Sci Rep 2016 6 18164 10.1038/srep18164 26750656 PMC4707509 · DOI
  67. [76]Costa B Cavallini C Da Pozzo E Taliani S Da Settimo F Martini C The anxiolytic etifoxine binds to TSPO Ro5-4864 binding site with long residence time showing a high neurosteroidogenic activity ACS Chem Neurosci 2017 8 1448 1454 10.1021/acschemneuro.7b00027 28362078 · DOI
  68. [77]Hatty CR Banati RB Protein-ligand and membrane-ligand interactions in pharmacology: the case of the translocator protein (TSPO) Pharmacol Res 2015 100 58 63 10.1016/j.phrs.2015.07.029 26238176 · DOI
  69. [78]Kletsas D Li W Han Z Papadopoulos V Peripheral-type benzodiazepine receptor (PBR) and PBR drug ligands in fibroblast and fibrosarcoma cell proliferation: role of ERK, c-Jun and ligand-activated PBR-independent pathways Biochem Pharmacol 2004 67 1927 1932 10.1016/j.bcp.2004.01.021 15130769 · DOI
  70. [79]Bader S Wolf L Milenkovic VM Gruber M Nothdurfter C Rupprecht R Differential effects of TSPO ligands on mitochondrial function in mouse microglia cells Psychoneuroendocrinology. 2019 106 65 76 10.1016/j.psyneuen.2019.03.029 30954920 · DOI
  71. [80]Veenman L Shandalov Y Gavish M VDAC activation by the 18 kDa translocator protein (TSPO), implications for apoptosis J Bioenerg Biomembr 2008 40 199 205 10.1007/s10863-008-9142-1 18670869 · DOI
  72. [81]Veenman L Alten J Linnemannstons K Shandalov Y Zeno S Lakomek M Potential involvement of F0F1-ATP(synth)ase and reactive oxygen species in apoptosis induction by the antineoplastic agent erucylphosphohomocholine in glioblastoma cell lines: a mechanism for induction of apoptosis via the 18 kDa mitochondrial translocator protein Apoptosis. 2010 15 753 768 10.1007/s10495-010-0460-5 20107899 PMC3128697 · DOI
  73. [82]Veenman L Gavish M The role of 18 kDa mitochondrial translocator protein (TSPO) in programmed cell death, and effects of steroids on TSPO expression Curr Mol Med 2012 12 398 412 10.2174/1566524011207040398 22348610 · DOI
  74. [83]Azarashvili T Grachev D Krestinina O Evtodienko Y Yurkov I Papadopoulos V The peripheral-type benzodiazepine receptor is involved in control of Ca2+-induced permeability transition pore opening in rat brain mitochondria Cell Calcium 2007 42 27 39 10.1016/j.ceca.2006.11.004 17174393 · DOI
  75. [84]Zulian A Sileikyte J Petronilli V Bova S Dabbeni-Sala F Cargnelli G The translocator protein (peripheral benzodiazepine receptor) mediates rat-selective activation of the mitochondrial permeability transition by norbormide Biochim Biophys Acta 2011 1807 1600 1605 10.1016/j.bbabio.2011.08.007 21889488 · DOI
  76. [85]Galiegue S Tinel N Casellas P The peripheral benzodiazepine receptor: a promising therapeutic drug target Curr Med Chem 2003 10 1563 1572 10.2174/0929867033457223 12871127 · DOI
  77. [86]Katz Y Eitan A Gavish M Increase in peripheral benzodiazepine binding sites in colonic adenocarcinoma Oncology. 1990 47 139 142 10.1159/000226806 2156202 · DOI
  78. [87]Lacapere JJ, Duma L, Finet S, Kassiou M, Papadopoulos V. Insight into the structural features of TSPO: implications for drug development. Trends Pharmacol Sci. 2019. 10.1016/j.tips.2019.11.005. PMC7021566 31864680 · DOI
  79. [88]Li H Papadopoulos V Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern Endocrinology 1998 139 4991 4997 10.1210/endo.139.12.6390 9832438 · DOI
  80. [89]Li H Yao Z Degenhardt B Teper G Papadopoulos V Cholesterol binding at the cholesterol recognition/interaction amino acid consensus (CRAC) of the peripheral-type benzodiazepine receptor and inhibition of steroidogenesis by an HIV TAT-CRAC peptide Proc Natl Acad Sci U S A 2001 98 1267 1272 10.1073/pnas.031461598 11158628 PMC14743 · DOI
  81. [90]Jamin N Neumann JM Ostuni MA Vu TK Yao ZX Murail S Characterization of the cholesterol recognition amino acid consensus sequence of the peripheral-type benzodiazepine receptor Mol Endocrinol 2005 19 588 594 10.1210/me.2004-0308 15528269 · DOI
  82. [91]Jaipuria G Leonov A Giller K Vasa SK Jaremko L Jaremko M Cholesterol-mediated allosteric regulation of the mitochondrial translocator protein structure Nat Commun 2017 8 14893 10.1038/ncomms14893 28358007 PMC5379104 · DOI
  83. [92]Jaremko L Jaremko M Giller K Becker S Zweckstetter M Structure of the mitochondrial translocator protein in complex with a diagnostic ligand Science. 2014 343 1363 1366 10.1126/science.1248725 24653034 PMC5650047 · DOI
  84. [93]Li F Liu J Zheng Y Garavito RM Ferguson-Miller S Protein structure. Crystal structures of translocator protein (TSPO) and mutant mimic of a human polymorphism Science 2015 347 555 558 10.1126/science.1260590 25635101 PMC5125025 · DOI · Paper page
  85. [94]Korkhov VM Sachse C Short JM Tate CG Three-dimensional structure of TspO by electron cryomicroscopy of helical crystals Structure. 2010 18 677 687 10.1016/j.str.2010.03.001 20541505 PMC2911597 · DOI
  86. [95]Iatmanen-Harbi S, Senicourt L, Papadopoulos V, Lequin O, Lacapere JJ. Characterization of the high-affinity drug ligand binding site of mouse recombinant TSPO. Int J Mol Sci. 2019;20. 10.3390/ijms20061444. PMC6470738 30901938 · DOI
  87. [96]Guo Y Kalathur RC Liu Q Kloss B Bruni R Ginter C Protein structure. Structure and activity of tryptophan-rich TSPO proteins Science 2015 347 551 555 10.1126/science.aaa1534 25635100 PMC4341906 · DOI · Paper page
  88. [97]Jaipuria G Giller K Leonov A Becker S Zweckstetter M Insights into cholesterol/membrane protein interactions using paramagnetic solid-state NMR Chemistry. 2018 24 17606 17611 10.1002/chem.201804550 30255522 · DOI
  89. [98]Taylor JM Allen AM Graham A Targeting mitochondrial 18 kDa translocator protein (TSPO) regulates macrophage cholesterol efflux and lipid phenotype Clin Sci (Lond) 2014 127 603 613 10.1042/CS20140047 24814875 · DOI
  90. [99]Biswas L Zhou X Dhillon B Graham A Shu X Retinal pigment epithelium cholesterol efflux mediated by the 18 kDa translocator protein, TSPO, a potential target for treating age-related macular degeneration Hum Mol Genet 2017 26 4327 4339 10.1093/hmg/ddx319 28973423 · DOI
  91. [100]Elustondo P Martin LA Karten B Mitochondrial cholesterol import Biochim Biophys Acta Mol Cell Biol Lipids 2017 1862 90 101 10.1016/j.bbalip.2016.08.012 27565112 · DOI
  92. [101]Rone MB Fan J Papadopoulos V Cholesterol transport in steroid biosynthesis: role of protein-protein interactions and implications in disease states Biochim Biophys Acta 2009 1791 646 658 10.1016/j.bbalip.2009.03.001 19286473 PMC2757135 · DOI · Paper page
  93. [102]Mari M Morales A Colell A Garcia-Ruiz C Fernandez-Checa JC Mitochondrial glutathione, a key survival antioxidant Antioxid Redox Signal 2009 11 2685 2700 10.1089/ARS.2009.2695 19558212 PMC2821140 · DOI
  94. [103]Gatliff J Campanella M TSPO is a REDOX regulator of cell mitophagy Biochem Soc Trans 2015 43 543 552 10.1042/BST20150037 26551691 · DOI
  95. [104]Gatliff J East DA Singh A Alvarez MS Frison M Matic I A role for TSPO in mitochondrial Ca(2+) homeostasis and redox stress signaling Cell Death Dis 2017 8 e2896 10.1038/cddis.2017.186 28640253 PMC5520880 · DOI
  96. [105]Sileikyte J Blachly-Dyson E Sewell R Carpi A Menabo R Di Lisa F Regulation of the mitochondrial permeability transition pore by the outer membrane does not involve the peripheral benzodiazepine receptor (translocator protein of 18 kDa (TSPO)) J Biol Chem 2014 289 13769 13781 10.1074/jbc.M114.549634 24692541 PMC4022851 · DOI
  97. [106]Morohaku K Pelton SH Daugherty DJ Butler WR Deng W Selvaraj V Translocator protein/peripheral benzodiazepine receptor is not required for steroid hormone biosynthesis Endocrinology. 2014 155 89 97 10.1210/en.2013-1556 24174323 PMC3868810 · DOI
  98. [107]Tu LN Morohaku K Manna PR Pelton SH Butler WR Stocco DM Peripheral benzodiazepine receptor/translocator protein global knock-out mice are viable with no effects on steroid hormone biosynthesis J Biol Chem 2014 289 27444 27454 10.1074/jbc.M114.578286 24936060 PMC4183784 · DOI · Paper page
  99. [108]Banati RB Middleton RJ Chan R Hatty CR Kam WW Quin C Positron emission tomography and functional characterization of a complete PBR/TSPO knockout Nat Commun 2014 5 5452 10.1038/ncomms6452 25406832 PMC4263137 · DOI · Paper page
  100. [110]Owen DR Fan J Campioli E Venugopal S Midzak A Daly E TSPO mutations in rats and a human polymorphism impair the rate of steroid synthesis Biochem J 2017 474 3985 3999 10.1042/BCJ20170648 29074640 PMC5697202 · DOI
  101. [111]Barron AM Ji B Kito S Suhara T Higuchi M Steroidogenic abnormalities in translocator protein knockout mice and significance in the aging male Biochem J 2018 475 75 85 10.1042/BCJ20170645 29127254 · DOI
  102. [112]Barron AM, Higuchi M, Hattori S, Kito S, Suhara T, Ji B. Regulation of anxiety and depression by mitochondrial translocator protein-mediated steroidogenesis: the role of neurons. Mol Neurobiol. 2020. 10.1007/s12035-020-02136-5. 32989676 · DOI
  103. [114]Kelly-Hershkovitz E Weizman R Spanier I Leschiner S Lahav M Weisinger G Effects of peripheral-type benzodiazepine receptor antisense knockout on MA-10 Leydig cell proliferation and steroidogenesis J Biol Chem 1998 273 5478 5483 10.1074/jbc.273.10.5478 9488670 · DOI
  104. [115]Tu LN Zhao AH Stocco DM Selvaraj V PK11195 effect on steroidogenesis is not mediated through the translocator protein (TSPO) Endocrinology. 2015 156 1033 1039 10.1210/en.2014-1707 25535830 PMC4330312 · DOI
  105. [116]Fan J Wang K Zirkin B Papadopoulos V CRISPR/Cas9 mediated Tspo gene mutations lead to reduced mitochondrial membrane potential and steroid formation in MA-10 mouse tumor Leydig cells Endocrinology 2018 159 1130 1146 10.1210/en.2017-03065 29300865 PMC5793793 · DOI
  106. [117]Verma A Facchina SL Hirsch DJ Song SY Dillahey LF Williams JR Photodynamic tumor therapy: mitochondrial benzodiazepine receptors as a therapeutic target Mol Med 1998 4 40 45 10.1007/BF03401728 9513188 PMC2230262 · DOI
  107. [118]Verma A Nye JS Snyder SH Porphyrins are endogenous ligands for the mitochondrial (peripheral-type) benzodiazepine receptor Proc Natl Acad Sci U S A 1987 84 2256 2260 10.1073/pnas.84.8.2256 3031675 PMC304628 · DOI
  108. [120]Zhao AH Tu LN Mukai C Sirivelu MP Pillai VV Morohaku K Mitochondrial translocator protein (TSPO) function is not essential for heme biosynthesis J Biol Chem 2016 291 1591 1603 10.1074/jbc.M115.686360 26627829 PMC4722442 · DOI
  109. [121]Milenkovic VM, Slim D, Bader S, Koch V, Heinl ES, Alvarez-Carbonell D, et al. CRISPR-Cas9 mediated TSPO gene knockout alters respiration and cellular metabolism in human primary microglia cells. Int J Mol Sci. 2019;20. 10.3390/ijms20133359. PMC6651328 31323920 · DOI
  110. [122]Urbani A Giorgio V Carrer A Franchin C Arrigoni G Jiko C Purified F-ATP synthase forms a Ca(2+)-dependent high-conductance channel matching the mitochondrial permeability transition pore Nat Commun 2019 10 4341 10.1038/s41467-019-12331-1 31554800 PMC6761146 · DOI
  111. [123]Owen DR Yeo AJ Gunn RN Song K Wadsworth G Lewis A 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 10.1038/jcbfm.2011.147 22008728 PMC3323305 · DOI · Paper page
  112. [124]Costa B Pini S Martini C Abelli M Gabelloni P Landi S Ala147Thr substitution in translocator protein is associated with adult separation anxiety in patients with depression Psychiatr Genet 2009 19 110 111 10.1097/YPG.0b013e32832080f6 19668118 · DOI
  113. [125]Nakamura K Yamada K Iwayama Y Toyota T Furukawa A Takimoto T Evidence that variation in the peripheral benzodiazepine receptor (PBR) gene influences susceptibility to panic disorder Am J Med Genet B Neuropsychiatr Genet 2006 141B 222 226 10.1002/ajmg.b.30211 16511838 · DOI
  114. [126]Colasanti A Owen DR Grozeva D Rabiner EA Matthews PM Craddock N Bipolar disorder is associated with the rs6971 polymorphism in the gene encoding 18 kDa translocator protein (TSPO) Psychoneuroendocrinology. 2013 38 2826 2829 10.1016/j.psyneuen.2013.07.007 23942012 PMC3820042 · DOI · Paper page
  115. [127]Da Pozzo E Costa B Martini C Translocator protein (TSPO) and neurosteroids: implications in psychiatric disorders Curr Mol Med 2012 12 426 442 10.2174/156652412800163451 22348611 · DOI
  116. [129]Owen DR Lewis AJ Reynolds R Rupprecht R Eser D Wilkins MR Variation in binding affinity of the novel anxiolytic XBD173 for the 18 kDa translocator protein in human brain Synapse. 2011 65 257 259 10.1002/syn.20884 21132812 · DOI
  117. [131]Prossin AR Chandler M Ryan KA Saunders EF Kamali M Papadopoulos V Functional TSPO polymorphism predicts variance in the diurnal cortisol rhythm in bipolar disorder Psychoneuroendocrinology 2018 89 194 202 10.1016/j.psyneuen.2018.01.013 29414032 PMC6048960 · DOI
  118. [132]Fan J Lindemann P Feuilloley MG Papadopoulos V Structural and functional evolution of the translocator protein (18 kDa) Curr Mol Med 2012 12 369 386 10.2174/1566524011207040369 22364126 · DOI
  119. [133]Yeliseev AA Kaplan S A sensory transducer homologous to the mammalian peripheral-type benzodiazepine receptor regulates photosynthetic membrane complex formation in Rhodobacter sphaeroides 2.4.1 J Biol Chem 1995 270 21167 21175 10.1074/jbc.270.36.21167 7673149 · DOI
  120. [134]Yeliseev AA Krueger KE Kaplan S A mammalian mitochondrial drug receptor functions as a bacterial “oxygen” sensor Proc Natl Acad Sci U S A 1997 94 5101 5106 10.1073/pnas.94.10.5101 9144197 PMC24638 · DOI
  121. [135]Fan J Rone MB Papadopoulos V Translocator protein 2 is involved in cholesterol redistribution during erythropoiesis J Biol Chem 2009 284 30484 30497 10.1074/jbc.M109.029876 19729679 PMC2781603 · DOI
  122. [137]Gong J Szego EM Leonov A Benito E Becker S Fischer A Translocator protein ligand protects against neurodegeneration in the MPTP mouse model of Parkinsonism J Neurosci 2019 39 3752 3769 10.1523/JNEUROSCI.2070-18.2019 30796158 PMC6510339 · DOI
  123. [138]Lavisse S Guillermier M Herard AS Petit F Delahaye M Van Camp N Reactive astrocytes overexpress TSPO and are detected by TSPO positron emission tomography imaging J Neurosci 2012 32 10809 10818 10.1523/JNEUROSCI.1487-12.2012 22875916 PMC6621018 · DOI
  124. [140]Chiang T, Messing RO, Chou WH. Mouse model of middle cerebral artery occlusion. J Vis Exp. 2011. 10.3791/2761. PMC3197421 21372780 · DOI
  125. [141]Pulagam KR Colas L Padro D Plaza-Garcia S Gomez-Vallejo V Higuchi M Evaluation of the novel TSPO radiotracer [(18)F] VUIIS1008 in a preclinical model of cerebral ischemia in rats EJNMMI Res 2017 7 93 10.1186/s13550-017-0343-7 29177913 PMC5701906 · DOI
  126. [142]Rojas S Martin A Arranz MJ Pareto D Purroy J Verdaguer E Imaging brain inflammation with [(11)C]PK11195 by PET and induction of the peripheral-type benzodiazepine receptor after transient focal ischemia in rats J Cereb Blood Flow Metab 2007 27 1975 1986 10.1038/sj.jcbfm.9600500 17457364 · DOI
  127. [143]Li HD Li M Shi E Jin WN Wood K Gonzales R A translocator protein 18 kDa agonist protects against cerebral ischemia/reperfusion injury J Neuroinflammation 2017 14 151 10.1186/s12974-017-0921-7 28754131 PMC5534039 · DOI
  128. [144]Constantinescu CS Farooqi N O'Brien K Gran B Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS) Br J Pharmacol 2011 164 1079 1106 10.1111/j.1476-5381.2011.01302.x 21371012 PMC3229753 · DOI · Paper page
  129. [145]Torkildsen O Brunborg LA Myhr KM Bo L The cuprizone model for demyelination Acta Neurol Scand Suppl 2008 188 72 76 10.1111/j.1600-0404.2008.01036.x 18439226 · DOI · Paper page
  130. [146]Banati RB Newcombe J Gunn RN Cagnin A Turkheimer F Heppner F The peripheral benzodiazepine binding site in the brain in multiple sclerosis: quantitative in vivo imaging of microglia as a measure of disease activity Brain 2000 123 Pt 11 2321 2337 10.1093/brain/123.11.2321 11050032 · DOI · Paper page
  131. [148]Zinnhardt B Belloy M Fricke IB Orije J Guglielmetti C Hermann S Molecular imaging of immune cell dynamics during de- and remyelination in the cuprizone model of multiple sclerosis by [(18)F]DPA-714 PET and MRI Theranostics. 2019 9 1523 1537 10.7150/thno.32461 31037121 PMC6485187 · DOI · Paper page
  132. [150]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 23681668 PMC3779450 · DOI
  133. [151]Esquerda-Canals G Montoliu-Gaya L Guell-Bosch J Villegas S Mouse models of Alzheimer’s disease J Alzheimers Dis 2017 57 1171 1183 10.3233/JAD-170045 28304309 · DOI · Paper page
  134. [152]James ML Belichenko NP Nguyen TV Andrews LE Ding Z Liu H PET imaging of translocator protein (18 kDa) in a mouse model of Alzheimer’s disease using N-(2,5-dimethoxybenzyl)-2-18F-fluoro-N-(2-phenoxyphenyl)acetamide J Nucl Med 2015 56 311 316 10.2967/jnumed.114.141648 25613536 PMC4866832 · DOI
  135. [155]Mirzaei N Tang SP Ashworth S Coello C Plisson C Passchier J In vivo imaging of microglial activation by positron emission tomography with [(11)C]PBR28 in the 5XFAD model of Alzheimer’s disease Glia 2016 64 993 1006 10.1002/glia.22978 26959396 · DOI · Paper page
  136. [156]Rapic S Backes H Viel T Kummer MP Monfared P Neumaier B Imaging microglial activation and glucose consumption in a mouse model of Alzheimer’s disease Neurobiol Aging 2013 34 351 354 10.1016/j.neurobiolaging.2012.04.016 22651996 · DOI
  137. [157]Sacher C, Blume T, Beyer L, Peters F, Eckenweber F, Sgobio C, et al. Longitudinal PET monitoring of amyloidosis and microglial activation in a second generation amyloid-beta mouse model. J Nucl Med. 2019. 10.2967/jnumed.119.227322. PMC6894380 31302633 · DOI
  138. [158]Serriere S Tauber C Vercouillie J Mothes C Pruckner C Guilloteau D Amyloid load and translocator protein 18 kDa in APPswePS1-dE9 mice: a longitudinal study Neurobiol Aging 2015 36 1639 1652 10.1016/j.neurobiolaging.2014.11.023 25680265 · DOI
  139. [159]Tournier BB Tsartsalis S Rigaud D Fossey C Cailly T Fabis F TSPO and amyloid deposits in sub-regions of the hippocampus in the 3xTgAD mouse model of Alzheimer’s disease Neurobiol Dis 2019 121 95 105 10.1016/j.nbd.2018.09.022 30261283 · DOI · Paper page
  140. [161]Notter T Coughlin JM Gschwind T Weber-Stadlbauer U Wang Y Kassiou M Translational evaluation of translocator protein as a marker of neuroinflammation in schizophrenia Mol Psychiatry 2018 23 323 334 10.1038/mp.2016.248 28093569 · DOI
  141. [162]Beckers L Ory D Geric I Declercq L Koole M Kassiou M Increased expression of translocator protein (TSPO) marks pro-inflammatory microglia but does not predict neurodegeneration Mol Imaging Biol 2018 20 94 102 10.1007/s11307-017-1099-1 28695372 · DOI
  142. [164]Tong J, Williams B, Rusjan PM, Mizrahi R, Lacapere JJ, Mccluskey T, et al. Concentration, distribution, and influence of aging on the 18 kDa translocator protein in human brain: implications for brain imaging studies. J Cereb Blood Flow Metab. 2019:271678X19858003. 10.1177/0271678X19858003. PMC7181090 31220997 · DOI
  143. [165]Yokokura M Terada T Bunai T Nakaizumi K Takebayashi K Iwata Y Depiction of microglial activation in aging and dementia: positron emission tomography with [(11)C]DPA713 versus [(11)C](R)PK11195 J Cereb Blood Flow Metab 2017 37 877 889 10.1177/0271678X16646788 27117856 PMC5363467 · DOI
  144. [166]Paul S Gallagher E Liow JS Mabins S Henry K Zoghbi SS Building a database for brain 18 kDa translocator protein imaged using [(11)C]PBR28 in healthy subjects J Cereb Blood Flow Metab 2019 39 1138 1147 10.1177/0271678X18771250 29749279 PMC6547185 · DOI
  145. [168]Werry EL, Bright FM, Piguet O, Ittner LM, Halliday GM, Hodges JR, et al. Recent developments in TSPO PET imaging as a biomarker of neuroinflammation in neurodegenerative disorders. Int J Mol Sci. 2019;20. 10.3390/ijms20133161. PMC6650818 31261683 · DOI
  146. [171]Zhang D Hu X Qian L O'Callaghan JP Hong JS Astrogliosis in CNS pathologies: is there a role for microglia? Mol Neurobiol 2010 41 232 241 10.1007/s12035-010-8098-4 20148316 PMC3629545 · DOI
  147. [172]Gui Y, Marks JD, Das S, Hyman BT, Serrano-Pozo A. Characterization of the 18 kDa translocator protein (TSPO) expression in post-mortem normal and Alzheimer’s disease brains. Brain Pathol. 2019. 10.1111/bpa.12763. PMC6904423 31276244 · DOI · Paper page
  148. [173]Xu J Sun J Perrin RJ Mach RH Bales KR Morris JC Translocator protein in late stage Alzheimer’s disease and dementia with Lewy bodies brains Ann Clin Transl Neurol 2019 6 1423 1434 10.1002/acn3.50837 31402620 PMC6689696 · DOI
  149. [174]Kuszpit K Hollidge BS Zeng X Stafford RG Daye S Zhang X [(18)F]DPA-714 PET imaging reveals global neuroinflammation in Zika virus-infected mice Mol Imaging Biol 2018 20 275 283 10.1007/s11307-017-1118-2 28900831 PMC5862915 · DOI
  150. [175]Doorduin J Klein HC Dierckx RA James M Kassiou M de Vries EF [11C]-DPA-713 and [18F]-DPA-714 as new PET tracers for TSPO: a comparison with [11C]-(R)-PK11195 in a rat model of herpes encephalitis Mol Imaging Biol 2009 11 386 398 10.1007/s11307-009-0211-6 19330384 PMC2763079 · DOI
  151. [176]Parente A Feltes PK Vallez Garcia D Sijbesma JW Moriguchi Jeckel CM Dierckx RA Pharmacokinetic analysis of 11C-PBR28 in the rat model of herpes encephalitis: comparison with (R)-11C-PK11195 J Nucl Med 2016 57 785 791 10.2967/jnumed.115.165019 26823567 · DOI
  152. [177]Vallez Garcia D de Vries EF Toyohara J Ishiwata K Hatano K Dierckx RA Evaluation of [(11)C]CB184 for imaging and quantification of TSPO overexpression in a rat model of herpes encephalitis Eur J Nucl Med Mol Imaging 2015 42 1106 1118 10.1007/s00259-015-3021-x 25771904 PMC4424274 · DOI
  153. [178]Iaccarino L Moresco RM Presotto L Bugiani O Iannaccone S Giaccone G An in vivo (11)C-(R)-PK11195 PET and in vitro pathology study of microglia activation in Creutzfeldt-Jakob disease Mol Neurobiol 2018 55 2856 2868 10.1007/s12035-017-0522-6 28455699 · DOI
  154. [179]De Picker LJ Morrens M Chance SA Boche D Microglia and brain plasticity in acute psychosis and schizophrenia illness course: a meta-review Front Psychiatry 2017 8 238 10.3389/fpsyt.2017.00238 29201010 PMC5696326 · DOI
  155. [180]Plaven-Sigray P, Matheson GJ, Coughlin JM, Hafizi S, Laurikainen H, Ottoy J, et al. Meta-analysis of the glial marker TSPO in psychosis revisited: reconciling inconclusive findings of patient-control differences. Biol Psychiatry. 2020. 10.1016/j.biopsych.2020.05.028. PMC7899168 32682565 · DOI
  156. [181]Plaven-Sigray P Cervenka S Meta-analytic studies of the glial cell marker TSPO in psychosis - a question of apples and pears? Psychol Med 2019 49 1624 1628 10.1017/S003329171800421X 30739609 PMC6601355 · DOI
  157. [182]Plaven-Sigray P Matheson GJ Collste K Ashok AH Coughlin JM Howes OD Positron emission tomography studies of the glial cell marker translocator protein in patients with psychosis: a meta-analysis using individual participant data Biol Psychiatry 2018 84 433 442 10.1016/j.biopsych.2018.02.1171 29653835 PMC7893597 · DOI
  158. [183]Meyer JH Cervenka S Kim MJ Kreisl WC Henter ID Innis RB Neuroinflammation in psychiatric disorders: PET imaging and promising new targets Lancet Psychiatry 2020 7 1064 1074 10.1016/S2215-0366(20)30255-8 33098761 PMC7893630 · DOI
  159. [184]Holmes SE Hinz R Conen S Gregory CJ Matthews JC Anton-Rodriguez JM Elevated translocator protein in anterior cingulate in major depression and a role for inflammation in suicidal thinking: a positron emission tomography study Biol Psychiatry 2018 83 61 69 10.1016/j.biopsych.2017.08.005 28939116 · DOI · Paper page
  160. [185]Setiawan E Attwells S Wilson AA Mizrahi R Rusjan PM Miler L Association of translocator protein total distribution volume with duration of untreated major depressive disorder: a cross-sectional study Lancet Psychiatry 2018 5 339 347 10.1016/S2215-0366(18)30048-8 29496589 · DOI
  161. [186]Li H Sagar AP Keri S Translocator protein (18 kDa TSPO) binding, a marker of microglia, is reduced in major depression during cognitive-behavioral therapy Prog Neuro-Psychopharmacol Biol Psychiatry 2018 83 1 7 10.1016/j.pnpbp.2017.12.011 29269262 · DOI
  162. [187]Scaini G Barichello T Fries GR Kennon EA Andrews T Nix BR TSPO upregulation in bipolar disorder and concomitant downregulation of mitophagic proteins and NLRP3 inflammasome activation Neuropsychopharmacology. 2019 44 1291 1299 10.1038/s41386-018-0293-4 30575805 PMC6785146 · DOI
  163. [188]Weidner LD Kannan P Mitsios N Kang SJ Hall MD Theodore WH The expression of inflammatory markers and their potential influence on efflux transporters in drug-resistant mesial temporal lobe epilepsy tissue Epilepsia. 2018 59 1507 1517 10.1111/epi.14505 30030837 PMC6356105 · DOI
  164. [189]Tournier BB Tsartsalis S Ceyzeriat K Medina Z Fraser BH Gregoire MC Fluorescence-activated cell sorting to reveal the cell origin of radioligand binding J Cereb Blood Flow Metab 2020 40 1242 1255 10.1177/0271678X19860408 31242048 PMC7238369 · DOI
  165. [190]Tournier BB, Tsartsalis S, Ceyzeriat K, Fraser BH, Gregoire MC, Kovari E, et al. Astrocytic TSPO upregulation appears before microglial TSPO in Alzheimer’s disease. J Alzheimers Dis. 2020. 10.3233/JAD-200136. PMC7683091 32804124 · DOI · Paper page
  166. [191]Notter T, Coughlin JM, Gschwind T, Weber-Stadlbauer U, Wang Y, Kassiou M, et al. Translational evaluation of translocator protein as a marker of neuroinflammation in schizophrenia. Mol Psychiatry. 2017. 10.1038/mp.2016.248. 28093569 · DOI

Cited by

Sorted by citations

Authors
Nutma, E., Ceyzériat, K., Amor, S., Tsartsalis, S., Millet, P., Owen, D. R., Papadopoulos, V., & Tournier, B. B.
Affiliations
  • Amsterdam University Medical Centers (NL)
  • University Hospital of Geneva (CH)
  • Queen Mary University of London (GB)
  • University of Geneva (CH)
  • Imperial College London (GB)
  • University of Southern California (US)
Corresponding author
Tournier, Benjamin B.
Venue
European Journal of Nuclear Medicine and Molecular Imaging
Published
2021-01-12
Volume
49
Issue
1
Pages
146-163
ISSN
  • 1619-7070 (ISSN-L)
  • 1619-7089
OpenAlex
W3119647162
Cited by
192
References
25
Citations by year
2026: 28 · 2025: 36 · 2024: 41 · 2023: 39 · 2022: 31 · 2021: 17
FWCI
3.89
Type
journal article
Language
en
Open access
Locations
  • European Journal of Nuclear Medicine and Molecular Imaging (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion, other-oa)
  • Archive ouverte UNIGE (University of Geneva) (publishedVersion, other-oa)
  • Pure Amsterdam UMC (submittedVersion, cc-by)
  • Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders
Université de Genève
Topics
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pharmacological Receptor Mechanisms and Effects
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Medical Imaging Techniques and Applications
Keywords
translocator protein (TSPO), neuroinflammation, microglia, TSPO PET imaging, mitochondrial outer membrane, neurodegenerative diseases, neuropsychiatric disorders, animal models of disease
MeSH terms
Animals, Brain, Humans, Tomography, X-Ray Computed, Microglia, Receptors, GABA, Positron-Emission Tomography

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