In vivo PET imaging of the α4β2 nicotinic acetylcholine receptor as a marker for brain inflammation after cerebral ischemia

Journal of Neuroscience

Volumn 35, Issue 15, 2015, Pages 5998-6009

  Martín, Abraham ^a   Szczupak, Boguslaw ^a   Gómez Vallejo, Vanessa ^a   Domercq, Maria ^b,c,d   Cano, Ainhoa ^a   Padro, Daniel ^a   Muñoz, Clara ^a   Higuchi, Makoto ^e   Matute, Carlos ^b,c,d   Llop, Jordi ^a  

^a CIC BIOMAGUNE   (Spain)

^b UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^c ACHUCARRO BASQUE CENTER FOR NEUROSCIENCE   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^e NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

Author keywords

2 18F fluoro A85380; Cerebral ischemia; PET; TSPO; 11C PK11195; 4 2

Indexed keywords

3 (2 AZETIDINYLMETHOXY) PYRIDINE; BIOLOGICAL MARKER; CARBON 11; CD11B ANTIGEN; DIHYDRO BETA ERYTHROIDINE; FLUORODEOXYGLUCOSE F 18; GLIAL FIBRILLARY ACIDIC PROTEIN; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; NICOTINIC RECEPTOR ALPHA4BETA2; UNCLASSIFIED DRUG; (R)-(11C)1-(2-CHLOROPHENYL)-N-METHYL-N-(1-METHYLPROPYL)-3-ISOQUINOLINECARBOXAMIDE; AMIDE; ISOQUINOLINE DERIVATIVE; NICOTINIC RECEPTOR; PROTEIN BINDING;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN ISCHEMIA; CELL COUNT; CONTROLLED STUDY; CORPUS STRIATUM; DEXTERITY TEST; DIAGNOSTIC IMAGING; ENCEPHALITIS; EXPERIMENTAL BEHAVIORAL TEST; EXPERIMENTAL STROKE; HEMISPHERE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SENSORIMOTOR FUNCTION; THALAMUS; ANIMAL; BRAIN; CEREBRAL ARTERY DISEASE; COMPLICATION; DIAGNOSTIC USE; DISEASE MODEL; DRUG EFFECTS; MENTAL DISORDERS; METABOLISM; PATHOLOGY; PSYCHOMOTOR PERFORMANCE; SCINTISCANNING; SPRAGUE DAWLEY RAT; TIME;

AMIDES; ANIMALS; ANTIGENS, CD11B; BRAIN; CELL COUNT; DIHYDRO-BETA-ERYTHROIDINE; DISEASE MODELS, ANIMAL; ENCEPHALITIS; FLUORODEOXYGLUCOSE F18; GLIAL FIBRILLARY ACIDIC PROTEIN; INFARCTION, MIDDLE CEREBRAL ARTERY; ISOQUINOLINES; MAGNETIC RESONANCE IMAGING; MALE; MENTAL DISORDERS; POSITRON-EMISSION TOMOGRAPHY; PROTEIN BINDING; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC; TIME FACTORS;

EID: 84929232376     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3670-14.2015     Document Type: Article

References (47)

1. Banati RB, Newcombe J, Gunn RN, Cagnin A, Turkheimer F, Heppner F, Price G, Wegner F, Giovannoni G, Miller DH, Perkin GD, Smith T, Hew-son 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. CrossRef Medline
2. Bartels AL, Leenders KL (2007) Neuroinflammation in the pathophysiology of Parkinson’s disease: evidence from animal models to human in vivo studies with [11C]-PK11195 PET. Mov Disord 22:1852-1856. CrossRef Medline
3. Bottlaender M, Valette H, Roumenov D, Dollé F, Coulon C, Ottaviani M, Hinnen F, Ricard M (2003) Biodistribution and radiation dosimetry of 18F-fluoro-A-85380 in healthy volunteers. J Nucl Med 44:596-601. Medline
4. Bouet V, Boulouard M, Toutain J, Divoux D, Bernaudin M, Schumann-Bard P, Freret T (2009) The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nat Protoc 4:1560-1564. CrossRef Medline
5. Burghaus L, Schütz U, Krempel U, de Vos RA, Jansen Steur EN, Wevers A, Lindstrom J, Schröder H (2000) Quantitative assessment of nicotinic acetylcholine receptor proteins in the cerebral cortex of Alzheimer patients. Brain Res Mol Brain Res 76:385-388. CrossRef Medline
6. 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. CrossRef Medline
7. Chauveau F, Boutin H, Van Camp N, Dollé F, Tavitian B (2008) Nuclear imaging of neuroinflammation: a comprehensive review of [ 11C]PK11195 challengers. Eur J Nucl Med Mol Imaging 35:2304-2319. CrossRef Medline
8. Chen MK, Guilarte TR (2008) Translocator protein 18 kDa (TSPO): molecular sensor of brain injury and repair. Pharmacol Ther 118:1-17. CrossRef Medline
9. Chen Y, Nie H, Tian L, Tong L, Yang L, Lao N, Dong H, Sang H, Xiong L (2013) Nicotine-induced neuroprotection against ischemic injury involves activation of endocannabinoid system in rats. Neurochem Res 38: 364-370. CrossRef Medline
10. Damont A, Roeda D, Dollé F (2013) The potential of carbon-11 and fluorine-18 chemistry: illustration through the development of positron emission tomography radioligands targeting the translocator protein 18 kDa. J Labelled Comp Radiopharm 56:96-104. CrossRef Medline
11. Ding YS, Fowler JS, Logan J, Wang GJ, Telang F, Garza V, Biegon A, Pareto D, Rooney W, Shea C, Alexoff D, Volkow ND, Vocci F (2004) 6-[ 18F]Fluoro-A-85380, a new PET tracer for the nicotinic acetylcholine receptor: studies in the human brain and in vivo demonstration of specific binding in white matter. Synapse 53:184-189. CrossRef Medline
12. Furukawa S, Sameshima H, Yang L, Ikenoue T (2013) Activation of acetylcholine receptors and microglia in hypoxic-ischemic brain damage in newborn rats. Brain Dev 35:607-613. CrossRef Medline
13. Gerhard A, Schwarz J, Myers R, Wise R, Banati RB (2005) Evolution of microglial activation in patients after ischemic stroke: a [ 11C] (R)-PK11195 PET study. Neuroimage 24:591-595. CrossRef Medline
14. Gotti C, Fornasari D, Clementi F (1997) Human neuronal nicotinic receptors. Prog Neurobiol 53:199-237. CrossRef Medline
15. Guan ZZ, Nordberg A, Mousavi M, Rinne JO, Hellström-Lindahl E (2002) Selective changes in the levels of nicotinic acetylcholine receptor protein and of corresponding mRNA species in the brains of patients with Parkinson’s disease. Brain Res 956:358-366. CrossRef Medline
16. Hijioka M, Matsushita H, Hisatsune A, Isohama Y, Katsuki H (2011) Therapeutic effect of nicotine in a mouse model of intracerebral hemorrhage. J Pharmacol Exp Ther 338:741-749. CrossRef Medline
17. Hogg RC, Raggenbass M, Bertrand D (2003) Nicotinic acetylcholine receptors: from structure to brain function. Rev Physiol Biochem Pharmacol 147:1-46. CrossRef Medline
18. Hughes JL, Jones PS, Beech JS, Wang D, Menon DK, Aigbirhio FI, Fryer TD, Baron JC (2012) A microPET study of the regional distribution of [ 11C]-PK11195 binding following temporary focal cerebral ischemia in the rat. Correlation with post mortem mapping of microglia activation. Neuroimage 59:2007-2016. CrossRef Medline
19. Jo S, Yarishkin O, Hwang YJ, Chun YE, Park M, Woo DH, Bae JY, Kim T, Lee J, Chun H, Park HJ, Lee da Y, Hong J, Kim HY, Oh SJ, Park SJ, Lee H, Yoon BE, Kim Y, Jeong Y, Shim I, Bae YC, Cho J, Kowall NW, Ryu H, Hwang E, Kim D, Lee CJ (2014) GABA from reactive astrocytes impairs memory in mouse models of Alzheimer’s disease. Nat Med 20:886-896. CrossRef Medline
20. Justicia C, Pérez-Asensio FJ, Burguete MC, Salom JB, Planas AM (2001) Administration of transforming growth factor-alpha reduces infarct volume after transient focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 21:1097-1104. Medline
21. Kihara T, ShimohamaS, Urushitani M, SawadaH, Kimura J, Kume T, Maeda T, Akaike A (1998) Stimulation of alpha4beta2 nicotinic acetylcholine receptors inhibits beta-amyloid toxicity. Brain Res 792:331-334. CrossRef Medline
22. Kimes AS, Horti AG, London ED, Chefer SI, Contoreggi C, Ernst M, Friello P, Koren AO, Kurian V, Matochik JA, Pavlova O, Vaupel DB, Mukhin AG (2003) 2-[ 18FJF-A-85380: PET imaging of brain nicotinic acetylcholine receptors and whole body distribution in humans. FASEB J 17:1331-1333. Medline
23. Lammertsma AA, Hume SP (1996) Simplified reference tissue model for PET receptor studies. Neuroimage 4:153-158. CrossRef Medline
24. Martín A, Boisgard R, Thézé B, Van Camp N, Kuhnast B, Damont A, Kassiou M, Dollé F, Tavitian B (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. CrossRef Medline
25. Martín A, Macé E, Boisgard R, Montaldo G, Thézé B, Tanter M, Tavitian B (2012a) Imaging of perfusion, angiogenesis, and tissue elasticity after stroke. J Cereb Blood Flow Metab 32:1496-1507. CrossRef Medline
26. Martín A, San Sebastián E, Gómez-Vallejo V, Llop J (2012b) Positron emission tomograghy with [(l)(3)N]ammonia evidences long-term cerebral hyperperfusion after 2h-transient focal ischemia. Neuroscience 213:47-53. CrossRef Medline
27. Menzies SA, Hoff JT, Betz AL (1992) Middle cerebral artery occlusion in rats: a neurological and pathological evaluation of a reproducible model. Neurosurgery 31:100-106; discussion 106-107. CrossRef Medline
28. Mudo G, Belluardo N, Fuxe K (2007) Nicotinic receptor agonists as neuro-protective/neurotrophic drugs: progress in molecular mechanisms. J Neural Transm 114:135-147. CrossRef Medline
29. Mukhin AG, Gündisch D, Horti AG, Koren AO, Tamagnan G, Kimes AS, Chambers J, Vaupel DB, King SL, Picciotto MR, Innis RB, London ED (2000) 5-Iodo-A-85380, an alpha4beta2 subtype-selective ligand for nicotinic acetylcholine receptors. Mol Pharmacol 57:642-649. Medline
30. Nirogi R, Kandikere V, Bhyrapuneni G, Saralaya R, Muddana N, Ajjala DR (2012) Rat thalamic alpha(4)beta(2) neuronal nicotinic acetylcholine receptor occupancy assay using LC-MS/MS. J Pharmacol Toxicol Methods 65:136-141. CrossRef Medline
31. Nizri E, Hamra-Amitay Y, Sicsic C, Lavon I, Brenner T (2006) Antiinflammatory properties of cholinergic up-regulation: A new role for acetylcholinesterase inhibitors. Neuropharmacology 50:540-547. CrossRef Medline
32. Nizri E, Irony-Tur-Sinai M, Faranesh N, Lavon I, Lavi E, Weinstock M, Brenner T (2008) Suppression of neuroinflammation and immuno-modulation by the acetylcholinesterase inhibitor rivastigmine. J Neuro-immunol 203:12-22. CrossRef Medline
33. O’Neill MJ, Murray TK, Lakics V, Visanji NP, Duty S (2002) The role of neuronal nicotinic acetylcholine receptors in acute and chronic neurodegeneration. Curr Drug Targets CNS Neurol Disord 1:399-411. CrossRef Medline
34. 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 and [11CJPK1195. Neurology 55:1052-1054. CrossRef Medline
35. Park HJ, Lee PH, Ahn YW, Choi YJ, Lee G, Lee DY, Chung ES, Jin BK (2007) Neuroprotective effect of nicotine on dopaminergic neurons by antiinflammatory action. Eur J Neurosci 26:79-89. CrossRef Medline
36. 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. CrossRef Medline
37. Rojas S, Martín A, Arranz MJ, Pareto D, Purroy J, Verdaguer E, Llop J, Gómez V, Gispert JD, Millán O, Chamorro A, Planas AM (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 27:1975-1986. CrossRef Medline
38. Rossini PM, Calautti C, Pauri F, Baron JC (2003) Post-stroke plastic reorganisation in the adult brain. Lancet Neurol 2:493-502. CrossRef Medline
39. Schmaljohann J, Minnerop M, Karwath P, Gündisch D, Falkai P, Guhlke S, Wüllner U (2004) Imaging of central nAChReceptors with 2-[18F]F-A85380: optimized synthesis and in vitro evaluation in Alzheimer’s disease. Appl Radiat Isot 61:1235-1240. CrossRef Medline
40. Schmaljohann J, Gündisch D, Minnerop M, Bucerius J, Joe A, Reinhardt M, Guhlke S, Bier sack HJ, Wüllner U (2006) In vitro evaluation of nicotinic acetylcholine receptors with 2-[18F]F-A85380 in Parkinson’s disease. Nucl Med Biol 33:305-309. CrossRef Medline
41. Schroeter M, Dennin MA, Walberer M, Backes H, Neumaier B, Fink GR, Graf R (2009) Neuroinflammation extends brain tissue at risk to vital peri-infarct tissue: a double tracer [ 11C]PK11195-and [ 18FJFDG-PET study. J Cereb Blood Flow Metab 29:1216-1225. CrossRef Medline
42. Shimohama S, Greenwald DL, Shafron DH, Akaika A, Maeda T, Kaneko S, Kimura J, Simpkins CE, Day AL, Meyer EM (1998) Nicotinic alpha 7 receptors protect against glutamate neurotoxicity and neuronal ischemic damage. Brain Res 779:359-363. CrossRef Medline
43. Shytle RD, Mori T, Townsend K, Vendrame M, Sun N, Zeng J, Ehrhart J, Silver AA, Sanberg PR, Tan J (2004) Cholinergic modulation of microglial activation by alpha 7 nicotinic receptors. J Neurochem 89:337-343. CrossRef Medline
44. Valette H, Bottlaender M, Dollé F, Guenther I, Fuseau C, Coulon C, Ottaviani M, Crouzel C (1999) Imaging central nicotinic acetylcholine receptors in baboons with [18F]fluoro-A-85380. J Nucl Med 40:1374-1380. Medline
45. Wang H, Yu M, Ochani M, Amelia CA, Tanovic M, Susarla S, Li JH, Wang H, Yang H, Ulloa L, Al-Abed Y, Czura CJ, Tracey KJ (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421:384-388. CrossRef Medline
46. Winkeler A, Boisgard R, Martín A, Tavitian B (2010) Radioisotopic imaging of neuroinflammation. J Nucl Med 51:1-4. CrossRef Medline
47. Zanotti-Fregonara P, Maroy R, Peyronneau MA, Trebossen R, Bottlaender M (2012) Minimally invasive input function for 2-18F-fluoro-A-85380 brain PET studies. Eur J Nucl Med Mol Imaging 39:651-659. CrossRef Medline