In vivo imaging of brain lesions with [11C]CLINME, a new PET radioligand of peripheral benzodiazepine receptors

GLIA

Volumn 55, Issue 14, 2007, Pages 1459-1468

  Boutin, Hervé ^a,b,c   Chauveau, Fabien ^a,b   Thominiaux, Cyrille ^a   Kuhnast, Bertrand ^a   Grégoire, Marie Claude ^a,d   Jan, Sébastien ^a   Trebossen, Régine ^a   Dollé, Frédéric ^a   Tavitian, Bertrand ^a,b   Mattner, Filomena ^d   Katsifis, Andrew ^d  

^a DIF   (France)

^b INSERM   (France)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d AUSTRALIAN NUCLEAR SCIENCE AND TECHNOLOGY ORGANISATION   (Australia)

Author keywords

Benzodiazepine receptor; Gliosis; Inflammation; Peripheral; PK11195; Positron emission tomography

Indexed keywords

2 (6 CHLORO 2 (4 IODOPHENYL) IMIDAZO(1,2 A)PYRIDIN 3 YL) N ETHYL N METHYL ACETAMIDE; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; TRACER; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN DAMAGE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RAT;

ACETAMIDES; ANIMALS; ANTINEOPLASTIC AGENTS; BINDING, COMPETITIVE; BRAIN; CARBON RADIOISOTOPES; DISEASE MODELS, ANIMAL; ENCEPHALITIS; GLIOSIS; ISOQUINOLINES; LIGANDS; MICROGLIA; POSITRON-EMISSION TOMOGRAPHY; PYRIDINES; RADIOLIGAND ASSAY; RATS; RATS, WISTAR; RECEPTORS, GABA-A;

EID: 34648822769     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20562     Document Type: Article

References (63)

1. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, O'Banion MK, Pachter J, Pasinetti G, Plata-Salaman C, Rogers J, Rydel R, Shen Y, Streit W, Strohmeyer R, Tooyoma I, Van Muiswinkel FL, Veerhuis R, Walker D, Webster S, Wegrzyniak B, Wenk G, Wyss-Coray T. 2000. Inflammation and Alzheimer's disease. Neurobiol Aging 21:383-421.
2. Ali C, Nicole O, Docagne F, Lesne S, MacKenzie ET, Nouvelot A, Buisson A, Vivien D. 2000. Ischemia-induced interleukin-6 as a potential endogenous neuroprotective cytokine against NMDA receptor-mediated excitotoxicity in the brain. J Cereb Blood Flow Metab 20:956-966.
3. Banati RB, Newcombe J, Gunn RN, Cagnin A, Turkheimer F, Heppner F, Price G, Wegner F, Giovannoni G, Miller DH, Perkin GD, Smith T, Hewson AK, Bydder G, Kreutzberg GW, Jones T, Cuzner ML, Myers R. 2000. The peripheral benzodiazepine binding site in the brain in multiple sclerosis: Quantitative in vivo imaging of microglia as a measure of disease activity. Brain 123:2321-2337.
4. Belloli S, Moresco RM, Matarrese M, Biella G, Sanvito F, Simonelli P, Turolla E, Olivieri S, Cappelli A, Vomero S, Galli-Kienle M, Fazio F. 2004. Evaluation of three quinoline-carboxamide derivatives as potential radioligands for the in vivo pet imaging of neurodegeneration. Neurochem Int 44:433-440.
5. 3 site ligand: A critical analysis of animal models of cerebral ischaemia and neurodegeneration. Brain Res 522:275-289.
6. Bertram L, Tanzi RE. 2005. The genetic epidemiology of neurodegenerative disease. J Clin Invest 115:1449-1457.
7. Boutin H, LeFeuvre RA, Horai R, Asano M, Iwakura Y, Rothwell NJ. 2001. Role of IL-1α and IL-1β in ischemic brain damage. J Neurosci 21:5528-5534.
8. Cagnin A, Brooks DJ, Kennedy AM, Gunn RN, Myers R, Turkheimer FE, Jones T, Banati RB. 2001. In-vivo measurement of activated microglia in dementia. Lancet 358:461-467.
9. Cagnin A, Kassiou M, Meikle SR, Banati RB. 2006. In vivo evidence for microglial activation in neurodegenerative dementia. Acta Neurol Scand Suppl 185:107-114.
10. Cicchetti F, Brownell AL, Williams K, Chen YI, Livni E, Isacson O. 2002. Neuroinflammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging. Eur J Neurosci 15:991-998.
11. Ferri CP, Prince M, Brayne C, Brodaty H, Fratiglioni L, Ganguli M, Hall K, Hasegawa K, Hendrie H, Huang Y, Jorm A, Mathers C, Menezes PR, Rimmer E, Scazufca M. 2005. Global prevalence of dementia: A Delphi consensus study. Lancet 366:2112-2117.
12. Gerhard A, Banati RB, Goerres GB, Cagnin A, Myers R, Gunn RN, Turkheimer F, Good CD, Mathias CJ, Quinn N, Schwarz J, Brooks DJ. 2003. [(11)C](R)-PK11195 PET imaging of microglial activation in multiple system atrophy. Neurology 61:686-689.
13. Gerhard A, Pavese N, Hotton G, Turkheimer F, Es M, Hammers A, Eggert K, Oertel W, Banati RB, Brooks DJ. 2006. In vivo imaging of microglial activation with [(11)C](R)-PK11195 PET in idiopathic Parkinson's disease. Neurobiol Dis 21:404-412.
14. Gerhard A, Schwarz J, Myers R, Wise R, Banati RB. 2005. Evolution of microglial activation in patients after ischemic stroke: A [(11)C](R)- PK11195 PET study. Neuroimage 24:591-595.
15. Gerhard A, Watts J, Trender-Gerhard I, Turkheimer F, Banati RB, Bhatia K, Brooks DJ. 2004. In vivo imaging of microglial activation with [(11)C](R)-PK11195 PET in corticobasal degeneration. Mov Disord 19:1221-1226.
16. Gotti B, Benavides J, MacKenzie ET, Scatton B. 1990. The pharmacotherapy of focal ischaemia in the mouse. Brain Res 522:290-307.
17. Grilli M, Barbieri I, Basudev H, Brusa R, Casati C, Lozza G, Ongini E. 2000. Interleukin-10 modulates neuronal threshold of vulnerability to ischaemic damage. Eur J Neurosci 12:2265-2272.
18. Groom GN, Junck L, Foster NL, Frey KA, Kuhl DE. 1995. PET of peripheral benzodiazepine binding sites in the microgliosis of Alzheimer's disease. J Nucl Med 36:2207-2210.
19. Gulyas B, Halldin C, Vas A, Banati RB, Shchukin E, Finnema S, Tarkainen J, Tihanyi K, Szilagyi G, Farde L. 2005. [11C]Vinpocetine: A prospective peripheral benzodiazepine receptor ligand for primate PET studies. J Neurol Sci 229/230:219-223.
20. Heiss WD, Herholz K. 2006. Brain receptor imaging. J Nucl Med 47:302-312.
21. Hirsch EC, Hunot S, Hartmann A. 2005. Neuroinflammatory processes in Parkinson's disease. Parkinsonism Relat Disord 11 (Suppl 1):S9-S15.
22. Ikoma Y, Yasuno F, Ito H, Suhara T, Ota M, Toyama H, Fujimura Y, Takano A, Maeda J, Zhang MR, Nakao R, Suzuki K. 2007. Quantitative analysis for estimating binding potential of the peripheral benzodiazepine receptor with [(11)C]DAA1106. J Cereb Blood Flow Metab 27:173-184.
23. James ML, Selleri S, Kassiou M. 2006. Development of ligands for the peripheral benzodiazepine receptor. Curr Med Chem 13:1991-2001.
24. Jander S, Schroeter M, Stoll G. 2002. Interleukin-18 expression after focal ischemia of the rat brain: Association with the late-stage inflammatory response. J Cereb Blood Flow Metab 22:62-70.
25. Jander S, Stoll G. 1998. Differential induction of interleukin-12, interleukin-18, and interleukin-1β converting enzyme mRNA in experimental autoimmune encephalomyelitis of the Lewis rat. J Neuroimmunol 91:93-99.
26. Koistinaho M, Koistinaho J. 2005. Interactions between Alzheimer's disease and cerebral ischemia - Focus on inflammation. Brain Res Brain Res Rev 48:240-250.
27. Kropholler MA, Boellaard R, Schuitemaker A, Folkersma H, van Berckel BN, Lammertsma AA. 2006. Evaluation of reference tissue models for the analysis of [11C](R)-PK11195 studies. J Cereb Blood Flow Metab 26:1431-1441.
28. Kropholler MA, Boellaard R, Schuitemaker A, van Berckel BN, Luurtsema G, Windhorst AD, Lammertsma AA. 2005. Development of a tracer kinetic plasma input model for (R)-[11C]PK11195 brain studies. J Cereb Blood Flow Metab 25:842-851.
29. Lammertsma AA, Hume SP. 1996. Simplified reference tissue model for PET receptor studies. Neuroimage 4:153-158.
30. Lang S. 2002. The role of peripheral benzodiazepine receptors (PBRs) in CNS pathophysiology. Curr Med Chem 9:1411-1415.
31. Lindberg C, Chromek M, Ahrengart L, Brauner A, Schultzberg M, Garlind A. 2005. Soluble interleukin-1 receptor type II,IL-18 and caspase-1 in mild cognitive impairment and severe Alzheimer's disease Neurochem Int 46:551-557.
32. Lockhart A, Davis B, Matthews JC, Rahmoune H, Hong G, Gee A, Earnshaw D, Brown J. 2003. The peripheral benzodiazepine receptor ligand PK11195 binds with high affinity to the acute phase reactant α1-acid glycoprotein: Implications for the use of the ligand as a CNS inflammatory marker. Nucl Med Biol 30:199-206.
33. Maeda J, Suhara T, Zhang MR, Okauchi T, Yasuno F, Ikoma Y, Inaji M, Nagai Y, Takano A, Obayashi S, Suzuki K. 2004. Novel peripheral benzodiazepine receptor ligand [11C]DAA1106 for PET: An imaging tool for glial cells in the brain. Synapse 52:283-291.
34. Maier B, Schwerdtfeger K, Mautes A, Holanda M, Muller M, Steudel WI, Marzi I. 2001. Differential release of interleukines 6, 8, and 10 in cerebrospinal fluid and plasma after traumatic brain injury. Shock 15:421-426.
35. Mattner F, Katsifis A, Staykova M, Ballantyne P, Willenborg DO. 2005. Evaluation of a radiolabeled 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 32:557-563.
36. Ooboshi H, Ibayashi S, Shichita T, Kumai Y, Takada J, Ago T, Arakawa S, Sugimori H, Kamouchi M, Kitazono T, Iida M. 2005. Postischemic gene transfer of interleukin-10 protects against both focal and global brain ischemia. Circulation 111:913-919.
37. Osborne KA, Shigeno T, Balarsky A-M, Ford I, McCulloch J, Teasdale GM, Graham DI. 1987. Quantitative assessment of early brain damage in a rat model of focal cerebral ischemia. J Neurol Neurosurg Psychiatry 50:402-410.
38. Ouchi Y, Yoshikawa E, Sekine Y, Futatsubashi M, Kanno T, Ogusu T, Torizuka T. 2005. Microglial activation and dopamine terminal loss in early Parkinson's disease. Ann Neurol 57:168-175.
39. Papadopoulos V, Baraldi M, Guilarte TR, Knudsen TB, Lacapere JJ, Lindemann P, Norenberg MD, Nutt D, Weizman A, Zhang MR, Gavish M. 2006. Translocator protein (18 kDa): New nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 27:402-409.
40. Pappata S, Cornu P, Samson Y, Prenant C, Benavides J, Scatton B, Crouzel C, Hauw JJ, Syrota A. 1991. PET study of carbon-11-PK 11195 binding to peripheral type benzodiazepine sites in glioblastoma: A case report. J Nucl Med 32:1608-1610.
41. Pappata S, Levasseur M, Gunn RN, Myers R, Crouzel C, Syrota A, Jones T, Kreutzberg GW, Banati RB. 2000. Thalamic microglial activation in ischemic stroke detected in vivo by PET, [11C]PK11195. Neurology 55:1052-1054.
42. Perini F, Morra M, Alecci M, Galloni E, Marchi M, Toso V. 2001. Temporal profile of serum anti-inflammatory and pro-inflammatory interleukins in acute ischemic stroke patients. Neurol Sci 22:289-296.
43. 3 sites in baboons: Positron emission tomography study. Eur J Pharmacol 200:347-351.
44. Pinteaux E, Rothwell NJ, Boutin H. 2006. Neuroprotective actions of endogenous interleukin-1 receptor antagonist (IL-1ra) are mediated by glia. Glia 53:551-556.
45. Planas AM, Crouzel C, Hinnen F, Jobert A, Ne F, DiGiamberardino L, Tavitian B. 1994. Rat brain acetylcholinesterase visualized with [11C]physostigmine. Neuroimage 1:173-180.
46. Price CJ, Wang D, Menon DK, Guadagno JV, Cleij M, Fryer T, Aigbirhio F, Baron JC, Warburton EA. 2006. Intrinsic activated microglia map to the peri-infarct zone in the subacute phase of ischemic stroke. Stroke 37:1749-1753.
47. Rao VL, Bowen KK, Rao AM, Dempsey RJ. 2001. Up-regulation of the peripheral-type benzodiazepine receptor expression and [(3)H] PK11195 binding in gerbil hippocampus after transient forebrain ischemia. J Neurosci Res 64:493-500.
48. Rothwell N, Allan S, Toulmond S. 1997. The role of interleukin 1 in acute neurodegeneration and stroke: Pathophysiological and therapeutic implications. J Clin Invest 100:2648-2652.
49. Shah F, Hume SP, Pike VW, Ashworth S, McDermott J. 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 21:573-581.
50. Stephenson DT, Schober DA, Smalstig EB, Mincy RE, Gehlert DR, Clemens JA. 1995. Peripheral benzodiazepine receptors are colocalized with activated microglia following transient global forebrain ischemia in the rat. J Neurosci 15:5263-5274.
51. Stoll G, Jander S, Schroeter M. 1998. Inflammation and glial responses in ischemic brain lesions. Prog Neurobiol 56:149-171.
52. Swartz KR, Liu F, Sewell D, Schochet T, Campbell I, Sandor M, Fabry Z. 2001. Interleukin-6 promotes post-traumatic healing in the central nervous system. Brain Res 896:86-95.
53. Tai YF, Pavese N, Gerhard A, Tabrizi SJ, Barker RA, Brooks DJ, Piccini P. 2007. Microglial activation in presymptomatic Huntington's disease gene carriers. Brain 130:1759-1766.
54. 11C]CLINME, a novel radioligand for imaging the peripheral benzodiazepine receptors with PET. J Labelled Compd Ratiopharm 50:229-236.
55. Touzani O, Boutin H, Lefeuvre RA, Parker LC, Miller A, Luheshi GN, Rothwell NJ. 2002. Interleukin-1 influences ischemic brain damage in the mouse independently of the interleukin-1 type I receptor. J Neurosci 22:38-43.
56. Tuppo EE, Arias HR. 2005. The role of inflammation in Alzheimer's disease. Int J Biochem Cell Biol 37:289-305.
57. Turner MR, Cagnin A, Turkheimer FE, Miller CC, Shaw CE, Brooks DJ, Leigh PN, Banati RB. 2004. Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: An [11C](R)-PK11195 positron emission tomography study. Neurobiol Dis 15:601-609.
58. Vowinckel E, Reutens D, Becher B, Verge G, Evans A, Owens T, Antel JP. 1997. PK11195 binding to the peripheral benzodiazepine receptor as a marker of microglia activation in multiple sclerosis and experimental autoimmune encephalomyelitis. J Neurosci Res 50:345-353.
59. Wilms H, Claasen J, Rohl C, Sievers J, Deuschl G, Lucius R. 2003. Involvement of benzodiazepine receptors in neuroinflammatory and neurodegenerative diseases: Evidence from activated microglial cells in vitro. Neurobiol Dis 14:417-424.
60. Yu AC, Lau LT. 2000. Expression of interleukin-1α, tumor necrosis factor α and interleukin-6 genes in astrocytes under ischemic injury. Neurochem Int 36:369-377.
61. Zhang MR, Kida T, Noguchi J, Furutsuka K, Maeda J, Suhara T, Suzuki K. 2003a. [(11)C]DAA1106: Radiosynthesis and in vivo binding to peripheral benzodiazepine receptors in mouse brain. Nucl Med Biol 30:513-519.
62. 18F]FEDAA1106: Two positron-emitter labeled ligands for peripheral benzodiazepine receptor (PBR). Bioorg Med Chem Lett 20:201-204.
63. 18F]fluoroethyl-5- methoxybenzyl)acetamide, for pet imaging of peripheral benzodiazepine receptor in primate brain. J Med Chem 47:2228-2235.