Detection and quantification of remote microglial activation in rodent models of focal ischaemia using the TSPO radioligand CLINDE

European Journal of Nuclear Medicine and Molecular Imaging

Volumn 37, Issue 12, 2010, Pages 2371-2380

  Arlicot, Nicolas ^a   Petit, Edwige ^b   Katsifis, Andrew ^c   Toutain, Jérôme ^b   Divoux, Didier ^b   Bodard, Sylvie ^a   Roussel, Simon ^b   Guilloteau, Denis ^a   Bernaudin, Myriam ^b   Chalon, Sylvie ^a  

^a UNIVERSITÉ DE TOURS   (France)

^b UNIVERSITÉ DE CAEN   (France)

^c AUSTRALIAN NUCLEAR SCIENCE AND TECHNOLOGY ORGANISATION   (Australia)

Author keywords

Cerebral ischaemia; Middle cerebral artery occlusion; Molecular imaging; SPECT; Stroke

Indexed keywords

CARRIER PROTEIN; CLINDE IODINE 125; FLUMAZENIL; IODINE 125; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; RADIOLIGAND; TRANSLOCATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BRAIN CORTEX; BRAIN DAMAGE; CELL ACTIVATION; CEREBROVASCULAR ACCIDENT; CORPUS STRIATUM; CORRELATION ANALYSIS; DRUG BINDING; GRAY MATTER; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; QUANTITATIVE ANALYSIS; RAT; SUBSTANTIA NIGRA; THALAMUS;

ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; HUMANS; MALE; MICE; MICROGLIA; RADIOPHARMACEUTICALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 78649788110     PISSN: 16197070     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00259-010-1598-7     Document Type: Article

References (54)

1. S Venneti BJ Lopresti CA Wiley 2006 The peripheral benzodiazepine receptor (translocator protein 18 kDa) in microglia: from pathology to imaging Prog Neurobiol 80 6 308 322 1:CAS:528:DC%2BD2sXntlyhtg%3D%3D 10.1016/j.pneurobio.2006.10.002 17156911 (Pubitemid 46107737)
2. VL Feigin CM Lawes DA Bennett SL Barker-Collo V Parag 2009 Worldwide stroke incidence and early case fatality reported in 56 population-based studies: a systematic review Lancet Neurol 8 4 355 369 10.1016/S1474-4422(09) 70025-0 19233729
3. MK Chen TR Guilarte 2008 Translocator protein 18 kDa (TSPO): molecular sensor of brain injury and repair Pharmacol Ther 118 1 1 17 1:CAS:528: DC%2BD1cXlvVSqsb0%3D 10.1016/j.pharmthera.2007.12.004 18374421
4. J Doorduin EF de Vries RA Dierckx HC Klein 2008 PET imaging of the peripheral benzodiazepine receptor: monitoring disease progression and therapy response in neurodegenerative disorders Curr Pharm Des 14 31 3297 3315 1:CAS:528:DC%2BD1MXmtV2qtg%3D%3D 10.2174/138161208786549443 19075709
5. V Papadopoulos M Baraldi TR Guilarte TB Knudsen JJ Lacapère P Lindemann, et al. 2006 Translocator protein (18 kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function Trends Pharmacol Sci 27 8 402 409 1:CAS:528:DC%2BD28XntVylsr8%3D 10.1016/j.tips.2006.06.005 16822554 (Pubitemid 44069585)
6. MW McEnery AM Snowman RR Trifiletti SH Snyder 1992 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 89 8 3170 3174 1:CAS:528:DyaK38XksVShsLc%3D 10.1073/pnas.89.8.3170 1373486
7. N Jamin JM Neumann MA Ostuni TK Vu ZX Yao S Murail, et al. 2005 Characterization of the cholesterol recognition amino acid consensus sequence of the peripheral-type benzodiazepine receptor Mol Endocrinol 19 3 588 594 1:CAS:528:DC%2BD2MXit1Sruro%3D 10.1210/me.2004-0308 15528269 (Pubitemid 40349433)
8. JJ Lacapère V Papadopoulos 2003 Peripheral-type benzodiazepine receptor: structure and function of a cholesterol-binding protein in steroid and bile acid biosynthesis Steroids 68 7-8 569 585 10.1016/S0039-128X(03)00101-6 12957662 (Pubitemid 37075920)
9. AP Sutter K Maaser M Höpfner B Barthel P Grabowski S Faiss, et al. 2002 Specific ligands of the peripheral benzodiazepine receptor induce apoptosis and cell cycle arrest in human esophageal cancer cells Int J Cancer 102 4 318 327 1:CAS:528:DC%2BD38Xos1ajtL8%3D 10.1002/ijc.10724 12402299 (Pubitemid 35265870)
10. J Benavides D Quarteronet F Imbault C Malgouris A Uzan C Renault, et al. 1983 Labelling of "peripheral-type" benzodiazepine binding sites in the rat brain by using [3H]PK 11195, an isoquinoline carboxamide derivative: kinetic studies and autoradiographic localization J Neurochem 41 6 1744 1750 1:CAS:528:DyaL2cXhslWqsQ%3D%3D 10.1111/j.1471-4159.1983.tb00888.x 6315880
11. A Gerhard J Schwarz R Myers R Wise RB Banati 2005 Evolution of microglial activation in patients after ischemic stroke: a [11C](R)-PK11195 PET study Neuroimage 24 2 591 595 10.1016/j.neuroimage.2004.09.034 15627603 (Pubitemid 41359057)
12. S Pappata M Levasseur RN Gunn R Myers C Crouzel A Syrota, et al. 2000 Thalamic microglial activation in ischemic stroke detected in vivo by PET and [11C]PK1195 Neurology 55 7 1052 1054 1:STN:280:DC%2BD3crgvVyjtA%3D%3D 11061271
13. CJ Price D Wang DK Menon JV Guadagno M Cleij T Fryer, et al. 2006 Intrinsic activated microglia map to the peri-infarct zone in the subacute phase of ischemic stroke Stroke 37 7 1749 1753 10.1161/01.STR.0000226980.95389.0b 16763188 (Pubitemid 44297724)
14. S Rojas A Martín MJ Arranz D Pareto J Purroy E Verdaguer, et al. 2007 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 27 12 1975 1986 1:CAS:528:DC%2BD2sXhtlWqurrE 10.1038/sj.jcbfm.9600500 17457364 (Pubitemid 350129165)
15. M Schroeter MA Dennin M Walberer H Backes B Neumaier GR Fink, et al. 2009 Neuroinflammation extends brain tissue at risk to vital peri-infarct tissue: a double tracer [11C]PK11195- and [18F]FDG-PET study J Cereb Blood Flow Metab 29 6 1216 1225 1:CAS:528:DC%2BD1MXntVyku7s%3D 10.1038/jcbfm.2009.36 19352400
16. M Imaizumi HJ Kim SS Zoghbi E Briard J Hong JL Musachio, et al. 2007 PET imaging with [11C]PBR28 can localize and quantify upregulated peripheral benzodiazepine receptors associated with cerebral ischemia in rat Neurosci Lett 411 3 200 205 1:CAS:528:DC%2BD28Xht1KgurvL 10.1016/j.neulet.2006.09.093 17127001 (Pubitemid 44828275)
17. A Martín R Boisgard B Thézé N Van Camp B Kuhnast A Damont, et al. 2010 Evaluation of the PBR/TSPO radioligand [(18)F]DPA-714 in a rat model of focal cerebral ischemia J Cereb Blood Flow Metab 30 230 241 10.1038/jcbfm.2009.205 19794397
18. MC Petit-Taboué JC Baron L Barré JM Travère D Speckel R Camsonne, et al. 1991 Brain kinetics and specific binding of [11C]PK 11195 to omega 3 sites in baboons: positron emission tomography study Eur J Pharmacol 200 2-3 347 351 10.1016/0014-2999(91)90594-G 1782994
19. F Shah SP Hume VW Pike S Ashworth J McDermott 1994 Synthesis of the enantiomers of [N-methyl-11C]PK 11195 and comparison of their behaviours as radioligands for PK binding sites in rats Nucl Med Biol 21 4 573 581 1:CAS:528:DyaK2cXlslCjtbo%3D 10.1016/0969-8051(94)90022-1 9234314 (Pubitemid 24173248)
20. F Dollé C Luus A Reynolds M Kassiou 2009 Radiolabelled molecules for imaging the translocator protein (18 kDa) using positron emission tomography Curr Med Chem 16 22 2899 2923 10.2174/092986709788803150 19689272
21. S Venneti G Wang J Nguyen CA Wiley 2008 The positron emission tomography ligand DAA1106 binds with high affinity to activated microglia in human neurological disorders J Neuropathol Exp Neurol 67 10 1001 1010 10.1097/NEN.0b013e318188b204 18800007
22. B Gulyás B Makkai P Kása K Gulya L Bakota S Várszegi, et al. 2009 A comparative autoradiography study in post mortem whole hemisphere human brain slices taken from Alzheimer patients and age-matched controls using two radiolabelled DAA1106 analogues with high affinity to the peripheral benzodiazepine receptor (PBR) system Neurochem Int 54 1 28 36 10.1016/j.neuint.2008.10.001 18984021
23. A Takano R Arakawa H Ito A Tateno H Takahashi R Matsumoto, et al. 2010 Peripheral benzodiazepine receptors in patients with chronic schizophrenia: a PET study with [11C]DAA1106 Int J Neuropsychopharmacol 13 943 950 1:CAS:528:DC%2BC3cXpt1Gjsbc%3D 10.1017/S1461145710000313 20350336
24. H Boutin F Chauveau C Thominiaux MC Grégoire ML James R Trebossen, et al. 2007 11C-DPA-713: a novel peripheral benzodiazepine receptor PET ligand for in vivo imaging of neuroinflammation J Nucl Med 48 4 573 581 1:CAS:528:DC%2BD2sXhtVert7nK 10.2967/jnumed.106.036764 17401094 (Pubitemid 47571413)
25. ML James RR Fulton J Vercoullie DJ Henderson L Garreau S Chalon, et al. 2008 DPA-714, a new translocator protein-specific ligand: synthesis, radiofluorination, and pharmacologic characterization J Nucl Med 49 5 814 822 1:CAS:528:DC%2BD1cXmvVSju7s%3D 10.2967/jnumed.107.046151 18413395 (Pubitemid 351717548)
26. CJ Endres MG Pomper M James O Uzuner DA Hammoud CC Watkins, et al. 2009 Initial evaluation of 11C-DPA-713, a novel TSPO PET ligand, in humans J Nucl Med 50 8 1276 1282 1:CAS:528:DC%2BD1MXhtVymtrrL 10.2967/jnumed.109.062265 19617321
27. A Le Pogam J Vercouillie P Corcia J Praline D Guilloteau J Baulieu, et al. 2008 Preliminary results of PET with [18F]DPA 714 in humans for detection of microglial activation in amyotrophic lateral sclerosis (ALS) J Nucl Med 49 231P
28. F Mattner K Mardon A Katsifis 2008 Pharmacological evaluation of [123I]-CLINDE: a radioiodinated imidazopyridine-3-acetamide for the study of peripheral benzodiazepine binding sites (PBBS) Eur J Nucl Med Mol Imaging 35 4 779 789 1:CAS:528:DC%2BD1cXjsVCksrw%3D 10.1007/s00259-007-0645-5 18057934
29. N Arlicot A Katsifis L Garreau F Mattner J Vergote S Duval, et al. 2008 Evaluation of CLINDE as potent translocator protein (18 kDa) SPECT radiotracer reflecting the degree of neuroinflammation in a rat model of microglial activation Eur J Nucl Med Mol Imaging 35 12 2203 2211 10.1007/s00259-008-0834-x 18536913
30. F Mattner A Katsifis M Staykova P Ballantyne DO Willenborg 2005 Evaluation of a radiolabelled peripheral benzodiazepine receptor ligand in the central nervous system inflammation of experimental autoimmune encephalomyelitis: a possible probe for imaging multiple sclerosis Eur J Nucl Med Mol Imaging 32 5 557 563 1:STN:280:DC%2BD2M3jslWhug%3D%3D 10.1007/s00259-004-1690-y 15875181 (Pubitemid 41214198)
31. M Bernaudin HH Marti S Roussel D Divoux A Nouvelot ET MacKenzie, et al. 1999 A potential role for erythropoietin in focal permanent cerebral ischemia in mice J Cereb Blood Flow Metab 19 6 643 651 1:CAS:528:DC%2BD3cXksVCqt7w%3D 10.1097/00004647-199906000-00007 10366194
32. EZ Longa PR Weinstein S Carlson R Cummins 1989 Reversible middle cerebral artery occlusion without craniectomy in rats Stroke 20 1 84 91 1:STN:280:DyaL1M7gtFWhuw%3D%3D 2643202
33. Franklin K, Paxinos G. The mouse brain in stereotaxic coordinates. San Diego: Academic; 1997.
34. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. New York: Academic; 1986.
35. Y Watanabe T Nakano K Yutani H Nishimura H Kusuoka H Nakamura, et al. 2000 Detection of viable cortical neurons using benzodiazepine receptor imaging after reversible focal ischaemia in rats: comparison with regional cerebral blood flow Eur J Nucl Med 27 3 308 313 1:CAS:528:DC%2BD3cXhsVWns7g%3D 10.1007/s002590050038 10774883
36. T Freret V Bouet C Leconte S Roussel L Chazalviel D Divoux, et al. 2009 Behavioral deficits after distal focal cerebral ischemia in mice: usefulness of adhesive removal test Behav Neurosci 123 1 224 230 10.1037/a0014157 19170448
37. MD Ginsberg 2003 Adventures in the pathophysiology of brain ischemia: penumbra, gene expression, neuroprotection: the 2002 Thomas Willis Lecture Stroke 34 1 214 223 10.1161/01.STR.0000048846.09677.62 12511777 (Pubitemid 36070826)
38. J Kriz M Lalancette-Hébert 2009 Inflammation, plasticity and real-time imaging after cerebral ischemia Acta Neuropathol 117 5 497 509 1:CAS:528:DC%2BD1MXjvFOnsr4%3D 10.1007/s00401-009-0496-1 19225790
39. F Binkofski RJ Seitz S Arnold J Classen R Benecke HJ Freund 1996 Thalamic metabolism and corticospinal tract integrity determine motor recovery in stroke Ann Neurol 39 4 460 470 1:STN:280:DyaK287os1yhtw%3D%3D 10.1002/ana.410390408 8619524 (Pubitemid 26118001)
40. RJ Seitz NP Azari U Knorr F Binkofski H Herzog HJ Freund 1999 The role of diaschisis in stroke recovery Stroke 30 9 1844 1850 1:STN:280: DyaK1MvgtV2gug%3D%3D 10471434
41. J Van Beek P Chan M Bernaudin E Petit ET MacKenzie M Fontaine 2000 Glial responses, clusterin, and complement in permanent focal cerebral ischemia in the mouse Glia 31 1 39 50 10.1002/(SICI)1098-1136(200007)31:1<39::AID- GLIA40>3.0.CO;2-1 10816605 (Pubitemid 30410872)
42. K Rupalla PR Allegrini D Sauer C Wiessner 1998 Time course of microglia activation and apoptosis in various brain regions after permanent focal cerebral ischemia in mice Acta Neuropathol 96 2 172 178 1:STN:280:DyaK1czmvVygsw%3D%3D 10.1007/s004010050878 9705133 (Pubitemid 28356531)
43. DT Stephenson DA Schober EB Smalstig RE Mincy DR Gehlert JA Clemens 1995 Peripheral benzodiazepine receptors are colocalized with activated microglia following transient global forebrain ischemia in the rat J Neurosci 15 7 Pt 2 5263 5274 1:CAS:528:DyaK2MXmvFCrsLc%3D 7623150
44. R Myers LG Manjil RS Frackowiak JE Cremer 1991 [3H]PK 11195 and the localisation of secondary thalamic lesions following focal ischaemia in rat motor cortex Neurosci Lett 133 1 20 24 1:CAS:528:DyaK38XhtVeksr8%3D 10.1016/0304-3940(91)90047-W 1791992
45. BA Radlinska SA Ghinani P Lyon D Jolly JP Soucy J Minuk, et al. 2009 Multimodal microglia imaging of fiber tracts in acute subcortical stroke Ann Neurol 66 6 825 832 10.1002/ana.21796 20035510
46. C Justicia P Ramos-Cabrer M Hoehn 2008 MRI detection of secondary damage after stroke: chronic iron accumulation in the thalamus of the rat brain Stroke 39 5 1541 1547 10.1161/STROKEAHA.107.503565 18323485
47. N Nighoghossian M Wiart S Cakmak Y Berthezène L Derex TH Cho, et al. 2007 Inflammatory response after ischemic stroke: a USPIO-enhanced MRI study in patients Stroke 38 2 303 307 10.1161/01.STR.0000254548.30258.f2 17170357 (Pubitemid 46184299)
48. ML Block JS Hong 2005 Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism Prog Neurobiol 76 2 77 98 1:CAS:528:DC%2BD2MXpvFemu7o%3D 10.1016/j.pneurobio.2005.06.004 16081203 (Pubitemid 41242883)
49. M Dihné F Block 2001 Focal ischemia induces transient expression of IL-6 in the substantia nigra pars reticulata Brain Res 889 1-2 165 173 10.1016/S0006-8993(00)03129-2 11166700 (Pubitemid 32146278)
50. M Loos M Dihné F Block 2003 Tumor necrosis factor-alpha expression in areas of remote degeneration following middle cerebral artery occlusion of the rat Neuroscience 122 2 373 380 1:CAS:528:DC%2BD3sXovVWhur4%3D 10.1016/S0306-4522(03)00498-6 14614903 (Pubitemid 37410167)
51. S Revital B Hagai G Gadi 2008 Evidence for the coexistence of segregated and integrated functional connections from the striatum to the substantia nigra in rats Neuroimage 40 2 451 457 10.1016/j.neuroimage.2007.12.017 18221893
52. H Hara K Harada T Sukamoto 1993 Chronological atrophy after transient middle cerebral artery occlusion in rats Brain Res 618 2 251 260 1:STN:280:DyaK3szos1Clug%3D%3D 10.1016/0006-8993(93)91273-U 8374756 (Pubitemid 23207964)
53. MM Zaleska ML Mercado J Chavez GZ Feuerstein MN Pangalos A Wood 2009 The development of stroke therapeutics: promising mechanisms and translational challenges Neuropharmacology 56 2 329 341 1:CAS:528:DC%2BD1MXhtVGjtbg%3D 10.1016/j.neuropharm.2008.10.006 19007799
54. J Jordán T Segura D Brea MF Galindo J Castillo 2008 Inflammation as therapeutic objective in stroke Curr Pharm Des 14 33 3549 3564 10.2174/138161208786848766 19075732