Evaluation of [123I]-CLINDE as a potent SPECT radiotracer to assess the degree of astroglia activation in cuprizone-induced neuroinflammation

European Journal of Nuclear Medicine and Molecular Imaging

Volumn 38, Issue 8, 2011, Pages 1516-1528

  Mattner, Filomena ^a   Bandin, David Linares ^b   Staykova, Maria ^b   Berghofer, Paula ^a   Gregoire, Marie Claude ^a   Ballantyne, Patrice ^a   Quinlivan, Mitchell ^a   Fordham, Susan ^b   Pham, Tien ^a   Willenborg, David O ^b   Katsifis, Andrew ^a  

^a ANSTO LifeSciences   (Australia)

^b CANBERRA HOSPITAL   (Australia)

Author keywords

Astroglia activation; Cuprizone; Keywords Translocator protein; Peripheral benzodiazepine receptor; SPECT imaging

Indexed keywords

CARRIER PROTEIN; CLINDE I 123; CUPRIZONE; TRACER; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; 6 CHLORO 2 (4' IODOPHENYL) 3 (N,N DIETHYL)IMIDAZO(1,2 A)PYRIDINE 3 ACETAMIDE; 6-CHLORO-2-(4'-IODOPHENYL)-3-(N,N-DIETHYL)IMIDAZO(1,2-A)PYRIDINE-3-ACETAMIDE; BZRP PROTEIN, MOUSE; DIAGNOSTIC AGENT; FUSED HETEROCYCLIC RINGS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; AUTORADIOGRAPHY; CELL ACTIVATION; CONTROLLED STUDY; CORPUS CALLOSUM; DEMYELINATING DISEASE; DISEASE ASSOCIATION; DRUG DISTRIBUTION; DRUG UPTAKE; FEASIBILITY STUDY; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MACROGLIA; MALE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OLFACTORY BULB; PROTEIN EXPRESSION; PUTAMEN; REAL TIME POLYMERASE CHAIN REACTION; REMYELINIZATION; SENSITIVITY ANALYSIS; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; EVALUATION; GENETICS; INFLAMMATION; MACROPHAGE; METABOLISM; METHODOLOGY; PATHOLOGY; SCINTISCANNING; UPREGULATION;

ANIMALS; ASTROCYTES; BICYCLO COMPOUNDS, HETEROCYCLIC; CORPUS CALLOSUM; CUPRIZONE; INFLAMMATION; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; RADIOACTIVE TRACERS; RECEPTORS, GABA; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON; UP-REGULATION;

EID: 80052566963     PISSN: 16197070     EISSN: 16197089     Source Type: Journal    
DOI: 10.1007/s00259-011-1784-2     Document Type: Article

References (54)

1. Vowinckel E, Reutens D, Becher B, Verge G, Evans A, Owens T, et al. PK11195 binding to the peripheral benzodiazepine receptor as a marker of microglia activation in multiple sclerosis and experimental autoimmune encephalomyelitis. J Neurosci Res 1997;50:345-53. (Pubitemid 27473649)
2. Banati RB, Newcombe J, Gunn RN, Cagnin A, Turkheimer F, Heppner F, et al. 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;123:2321-37.
3. Nair A, Frederick TJ, Miller SD. Astrocytes in multiple sclerosis: A product of their environment. Cell Mol Life Sci 2008;65:2702-20.
4. Cagnin A, Brooks DJ, Kennedy AM, Gunn RN, Myers R, Turkheimer FE, et al. In-vivo measurement of activated microglia in dementia. Lancet 2001;358:461-7. (Pubitemid 32769854)
5. Wisniewski HM, Wegiel J. The role of perivascular and microglial cells in fibrillogenesis of beta-amyloid and PrP protein in Alzheimer's disease and scrapie. Res Immunol 1992;143:642-5.
6. Messmer K, Reynolds GP. Increased peripheral benzodiazepine binding sites in the brain of patients with Huntington's disease. Neurosci Lett 1998;241:53-6. (Pubitemid 28079032)
7. Dheen ST, Kaur C, Ling EA. Microglial activation and its implications in the brain diseases. Curr Med Chem 2007;14:1189-97. (Pubitemid 46739320)
8. O'Brien K, Fitzgerald DC, Naiken K, Alugupalli KR, Rostami AM, Gran B. Role of the innate immune system in autoimmune inflammatory demyelination. Curr Med Chem 2008;15:1105-15. (Pubitemid 352002979)
9. Laird MD, Vender JR, Dhandapani KM. Opposing roles for reactive astrocytes following traumatic brain injury. Neurosignals 2008;16:154-64. (Pubitemid 351263222)
10. Sofroniew MV. Reactive astrocytes in neural repair and protection. Neuroscientist 2005;11:400-7. (Pubitemid 41339226)
11. Williams A, Piaton G, Lubetzki C. Astrocytes-friends or foes in multiple sclerosis? Glia 2007;55:1300-12.
12. Beckers C, Jeukens X, Ribbens C, André B, Marcelis S, Leclercq P, et al. (18)F-FDG PET imaging of rheumatoid knee synovitis correlates with dynamic magnetic resonance and sonographic assessments as well as with the serum level of metalloproteinase-3. Eur J Nucl Med Mol Imaging 2006;33:275-80.
13. Burdette JE. In vivo imaging of molecular targets and their function in endocrinology. J Mol Endocrinol 2008;40:253-61. (Pubitemid 351865033)
14. Silverman DH, Hoh CK, Seltzer MA, Schiepers C, Cuan GS, Gambhir SS, et al. Evaluating tumor biology and oncological disease with positron-emission tomography. Semin Radiat Oncol 1998;8:183-96. (Pubitemid 28323477)
15. Bakshi R, Minagar A, Jaisani Z, Wolinsky JS. Imaging of multiple sclerosis: Role in neurotherapeutics. NeuroRx 2005;2:277-303. (Pubitemid 40471438)
16. Mattner F, Katsifis A, Staykova M, Ballantyne P, Willenborg DO. 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 2005;32:557-63. (Pubitemid 41214198)
17. Radu CG, Shu CJ, Shelly SM, Phelps ME, Witte ON. Positron emission tomography with computed tomography imaging of neuroinflammation in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 2007;104:1937-42. (Pubitemid 46239882)
18. Klem B, Lappin G, Nicholson S, van de Wetering J, de Vries DE, Oosterhuis B, et al. Determination of the bioavailability of [14C]- hexaminolevulinate using accelerator mass spectrometry after intravesical administration to human volunteers. J Clin Pharmacol 2006;46:456-60.
19. Papadopoulos V, Baraldi M, Guilarte TR, Knudsen TB, Lacapére JJ, Lindemann P, et al. Translocator protein (18 kDa): New nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 2006;27:402-9. (Pubitemid 44069585)
20. Venneti S, Lopresti BJ, Wiley CA. The peripheral benzodiazepine receptor (translocator protein 18 kDa) in microglia: From pathology to imaging. Prog Neurobiol 2006;80:308-22. (Pubitemid 46107737)
21. Garnier M, Boujrad N, Ogwuegbu SO, Hudson JRJ, Papadopoulos V. The polypeptide diazepam-binding inhibitor and a higher affinity mitochondrial peripheral-type benzodiazepine receptor sustain constitutive steroidogenesis in the R2C Leydig tumor cell line. J Biol Chem 1994;269:22105-12. (Pubitemid 24282135)
22. Papadopoulos V. In search of the function of the peripheral-type benzodiazepine receptor. Endocr Res 2004;30:677-84. (Pubitemid 40070152)
23. Papadopoulos V, Amri H, Boujrad N, Cascio C, Culty M, Garnier M, et al. Peripheral benzodiazepine receptor in cholesterol transport and steroidogenesis. Steroids 1997;62:21-8. (Pubitemid 27066980)
24. 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;13:2385-405. (Pubitemid 47321571)
25. Casellas P, Galiegue S, Basile AS. Peripheral benzodiazepine receptors and mitochondrial function. Neurochem Int 2002;40:475-86. (Pubitemid 34159148)
26. Myers R, Manjil LG, Cullen BM, Price GW, Frackowiak RS, Cremer JE. Macrophage and astrocyte populations in relation to [3H]PK 11195 binding in rat cerebral cortex following a local ischaemic lesion. J Cereb Blood Flow Metab 1991;11:314-22.
27. Stephenson DT, Schober DA, Smalstig EB, Mincy RE, Gehlert DR, Clemens JA. Peripheral benzodiazepine receptors are colocalized with activated microglia following transient global forebrain ischemia in the rat. J Neurosci 1995;15:5263-74.
28. Belloli S, Moresco RM, Matarrese M, Biella G, Sanvito F, Simonelli P, et al. Evaluation of three quinoline-carboxamide derivatives as potential radioligands for the in vivo pet imaging of neurodegeneration. Neurochem Int 2004;44:433-40. (Pubitemid 37548408)
29. Lockhart A, Davis B, Matthews JC, Rahmoune H, Hong G, Gee A, et al. The peripheral benzodiazepine receptor ligand PK11195 binds with high affinity to the acute phase reactant alpha1-acid glycoprotein: Implications for the use of the ligand as a CNS inflammatory marker. Nucl Med Biol 2003;30:199-206. (Pubitemid 36293722)
30. Shah F, Hume SP, Pike VW, Ashworth S, McDermott J. 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 1994;21:573-81. (Pubitemid 24173248)
31. Petit-Taboué MC, Baron JC, Barré L, Travére JM, Speckel D, Camsonne R, et al. Brain kinetics and specific binding of [11C]PK 11195 to omega 3 sites in baboons: Positron emission tomography study. Eur J Pharmacol 1991;200:347-51.
32. Arlicot N, Katsifis A, Garreau L, Mattner F, Vergote J, Duval S, et al. 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 2008;35:2203-11.
33. Arlicot N, Petit E, Katsifis A, Toutain J, Divoux D, Bodard S, et al. Detection and quantification of remote microglial activation in rodent models of focal ischaemia using the TSPO radioligand CLINDE. Eur J Nucl Med Mol Imaging 2010;37:2371-80. doi:10.1007/s00259-010-1598-7.
34. Mattner F, Mardon K, Katsifis A. 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 2008;35:779-89.
35. Petronilli V, Zoratti M. A characterization of cuprizone-induced giant mouse liver mitochondria. J Bioenerg Biomembr 1990;22:663-77. doi:10.1007/bf00809070. (Pubitemid 20362626)
36. Tandler B,Hoppel CL. Studies on giant mitochondria. Ann NYAcad Sci 1986;488:65-81. doi:10.1111/j.1749-6632.1986.tb54394.x.
37. Pirko I, Johnson AJ. Neuroimaging of demyelination and remyelination models. Curr Top Microbiol Immunol 2008;318:241-66.
38. Torkildsen O, Brunborg LA, Myhr KM, Bø L. The cuprizone model for demyelination. Acta Neurol Scand Suppl 2008;188:72-6. (Pubitemid 351606183)
39. Chen MK, Guilarte TR. Translocator protein 18 kDa (TSPO): Molecular sensor of brain injury and repair. Pharmacol Ther 2008;118:1-17.
40. Mana P, Liñares D, Fordham S, Staykova M, Willenborg D. Deleterious role of IFNgamma in a toxic model of central nervous system demyelination. Am J Pathol 2006;168:1464-73.
41. Katsifis A, Mattner F, Dikic B, Papazian V. Synthesis of substituted [123I]imidazo[1,2-a]pyridines as potential probes for the study of the peripheral benzodiazepine receptors using SPECT. Radiochim Acta 2000;88:229-32.
42. McElroy DP, MacDonald LR, Beekman FJ, Yuchuan W, Patt BE, Iwanczyk JS, et al. Performance evaluation of A-SPECT: A high resolution desktop pinhole SPECT system for imaging small animals. IEEE Trans Nucl Sci 2002;49:2139-47. (Pubitemid 35443066)
43. Paxinos G, Franklin KBJ. The mouse brain. 2nd ed. San Diego: Academic; 2001.
44. Maña P, Fordham SA, Staykova MA, Correcha M, Silva D, Willenborg DO, et al. Demyelination caused by the copper chelator cuprizone halts T cell mediated autoimmune neuroinflammation. J Neuroimmunol 2009;210:13-21.
45. Taylor LC, Gilmore W, Matsushima GK. SJL mice exposed to cuprizone intoxication reveal strain and gender pattern differences in demyelination. Brain Pathol 2009;19:467-79.
46. Yang HJ, Wang H, Zhang Y, Xiao L, Clough RW, Browning R, et al. Region-specific susceptibilities to cuprizone-induced lesions in the mouse forebrain: Implications for the pathophysiology of schizophrenia. Brain Res 2009;1270:121-30.
47. Pott F, Gingele S, Clarner T, Dang J, Baumgartner W, Beyer C, et al. Cuprizone effect on myelination, astrogliosis and microglia attraction in the mouse basal ganglia. Brain Res 2009;1305:137-49.
48. Skripuletz T, Lindner M, Kotsiari A, Garde N, Fokuhl J, Linsmeier F, et al. Cortical demyelination is prominent in the murine cuprizone model and is strain-dependent. Am J Pathol 2008;172:1053-61. (Pubitemid 351520001)
49. Chen MK, Guilarte TR. Imaging the peripheral benzodiazepine receptor response in central nervous system demyelination and remyelination. Toxicol Sci 2006;91:532-9. (Pubitemid 43827305)
50. Zhang MR, Ogawa M, Maeda J, Ito T, Noguchi J, Kumata K, et al. [2-11C]isopropyl-, [1-11C]ethyl-, and [11C]methyl-labeled phenoxyphenyl acetamide derivatives as positron emission tomography ligands for the peripheral benzodiazepine receptor: Radiosynthesis, uptake, and in vivo binding in brain. J Med Chem 2006;49:2735-42.
51. Cosenza-Nashat M, Zhao ML, Suh HS, Morgan J, Natividad R, Morgello S, et al. Expression of the translocator protein of 18 kDa by microglia, macrophages and astrocytes based on immunohistochemical localization in abnormal human brain. Neuropathol Appl Neurobiol 2009;35:306-28.
52. Chen MK, Baidoo K, Verina T, Guilarte TR. Peripheral benzodiazepine receptor imaging in CNS demyelination: Functional implications of anatomical and cellular localization. Brain 2004;127:1379-92.
53. Guilarte TR, Kuhlmann AC, O'Callaghan JP, Miceli RC. Enhanced expression of peripheral benzodiazepine receptors in trimethyltin-exposed rat brain: A biomarker of neurotoxicity. Neurotoxicology 1995;16:441-50.
54. Kuhlmann AC, Guilarte TR. Cellular and subcellular localization of peripheral benzodiazepine receptors after trimethyltin neurotoxicity. J Neurochem 2000;74:1694-704. (Pubitemid 30163992)