Login Register Cart 0
Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Review Article

Essential Principles and Recent Progress in the Development of TSPO PET Ligands for Neuroinflammation Imaging

Author(s): Monica Viviano, Elisabetta Barresi, Fabrice G. Siméon, Barbara Costa, Sabrina Taliani, Federico Da Settimo, Victor W. Pike and Sabrina Castellano*

Volume 29, Issue 28, 2022

Published on: 12 May, 2022

Page: [4862 - 4890] Pages: 29

DOI: 10.2174/0929867329666220329204054

Price: $65

Open Access Journals Promotions 2
Abstract

The translocator protein 18kDa (TSPO) is expressed in the outer mitochondrial membrane and is implicated in several functions, including cholesterol transport and steroidogenesis. Under normal physiological conditions, TSPO is present in very low concentrations in the human brain but is markedly upregulated in response to brain injury and inflammation. This upregulation is strongly associated with activated microglia. Therefore, TSPO is particularly suited for assessing active gliosis associated with brain lesions following injury or disease. For over three decades, TSPO has been studied as a biomarker. Numerous radioligands for positron emission tomography (PET) that target TSPO have been developed for imaging inflammatory progression in the brain. Although [11C]PK11195, the prototypical first-generation PET radioligand, is still widely used for in vivo studies, mainly now as its single more potent R-enantiomer, it has severe limitations, including low sensitivity and poor amenability to quantification. Second-generation radioligands are characterized by higher TSPO specific signals but suffer from other drawbacks, such as sensitivity to the TSPO single nucleotide polymorphism (SNP) rs6971. Therefore, their applications in human studies have the burden of needing to genotype subjects. Consequently, recent efforts are focused on developing improved radioligands that combine the optimal features of the second generation with the ability to overcome the differences in binding affinities across the population. This review presents essential principles in the design and development of TSPO PET ligands and discusses prominent examples among the main chemotypes.

Keywords: TSPO, neuroinflammation, imaging, PET, radioligand, drug development, diagnostic marker.

« Previous
[1]
Papadopoulos, V.; Baraldi, M.; Guilarte, T.R.; Knudsen, T.B.; Lacapère, J.J.; Lindemann, P.; Norenberg, M.D.; Nutt, D.; Weizman, A.; Zhang, M.R.; Gavish, M. Translocator protein (18kDa): New nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol. Sci., 2006, 27(8), 402-409.
[http://dx.doi.org/10.1016/j.tips.2006.06.005] [PMID: 16822554]
[2]
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(12), 4991-4997.
[http://dx.doi.org/10.1210/endo.139.12.6390] [PMID: 9832438]
[3]
Lacapère, J.J.; Delavoie, F.; Li, H.; Péranzi, G.; Maccario, J.; Papadopoulos, V.; Vidic, B. Structural and functional study of reconstituted peripheral benzodiazepine receptor. Biochem. Biophys. Res. Commun., 2001, 284(2), 536-541.
[http://dx.doi.org/10.1006/bbrc.2001.4975] [PMID: 11394915]
[4]
Gatliff, J.; Campanella, M. TSPO: kaleidoscopic 18-kDa amid biochemical pharmacology, control and targeting of mitochondria. Biochem. J., 2016, 473(2), 107-121.
[http://dx.doi.org/10.1042/BJ20150899] [PMID: 26733718]
[5]
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(6177), 1363-1366.
[http://dx.doi.org/10.1126/science.1248725] [PMID: 24653034]
[6]
Jaremko, M.; Jaremko, Ł.; Jaipuria, G.; Becker, S.; Zweckstetter, M. Structure of the mammalian TSPO/PBR protein. Biochem. Soc. Trans., 2015, 43(4), 566-571.
[http://dx.doi.org/10.1042/BST20150029] [PMID: 26551694]
[7]
Jaremko, Ł.; Jaremko, M.; Giller, K.; Becker, S.; Zweckstetter, M. Conformational flexibility in the transmembrane protein TSPO. Chemistry, 2015, 21(46), 16555-16563.
[http://dx.doi.org/10.1002/chem.201502314] [PMID: 26394723]
[8]
Li, F.; Liu, J.; Zheng, Y.; Garavito, R.M.; Ferguson-Miller, S. Protein structure. Crystal structures of translocator protein (TSPO) and mutant mimic of a human polymorphism. Science, 2015, 347(6221), 555-558.
[http://dx.doi.org/10.1126/science.1260590] [PMID: 25635101]
[9]
Guo, Y.; Kalathur, R.C.; Liu, Q.; Kloss, B.; Bruni, R.; Ginter, C.; Kloppmann, E.; Rost, B.; Hendrickson, W.A. Protein structure. Structure and activity of tryptophan-rich TSPO proteins. Science, 2015, 347(6221), 551-555.
[http://dx.doi.org/10.1126/science.aaa1534] [PMID: 25635100]
[10]
Papadopoulos, V.; Lecanu, L. Translocator protein (18 kDa) TSPO: An emerging therapeutic target in neurotrauma. Exp. Neurol., 2009, 219(1), 53-57.
[http://dx.doi.org/10.1016/j.expneurol.2009.04.016] [PMID: 19409385]
[11]
Costa, B.; Da Pozzo, E.; Martini, C. Translocator protein as a promising target for novel anxiolytics. Curr. Top. Med. Chem., 2012, 12(4), 270-285.
[http://dx.doi.org/10.2174/156802612799078720] [PMID: 22204481]
[12]
Da Pozzo, E.; Giacomelli, C.; Barresi, E.; Costa, B.; Taliani, S.; Passetti, Fda.S.; Martini, C. Targeting the 18-kDa translocator protein: Recent perspectives for neuroprotection. Biochem. Soc. Trans., 2015, 43(4), 559-565.
[http://dx.doi.org/10.1042/BST20150028] [PMID: 26551693]
[13]
Veenman, L.; Gavish, M. The peripheral-type benzodiazepine receptor and the cardiovascular system. Implications for drug development. Pharmacol. Ther., 2006, 110(3), 503-524.
[http://dx.doi.org/10.1016/j.pharmthera.2005.09.007] [PMID: 16337685]
[14]
Maaser, K.; Grabowski, P.; Oezdem, Y.; Krahn, A.; Heine, B.; Stein, H.; Buhr, H.; Zeitz, M.; Scherübl, H. Up-regulation of the peripheral benzodiazepine receptor during human colorectal carcinogenesis and tumor spread. Clin. Cancer Res., 2005, 11(5), 1751-1756.
[http://dx.doi.org/10.1158/1078-0432.CCR-04-1955] [PMID: 15755996]
[15]
Hauet, T.; Yao, Z.X.; Bose, H.S.; Wall, C.T.; Han, Z.; Li, W.; Hales, D.B.; Miller, W.L.; Culty, M.; Papadopoulos, V. Peripheral-type benzodiazepine receptor-mediated action of steroidogenic acute regulatory protein on cholesterol entry into leydig cell mitochondria. Mol. Endocrinol., 2005, 19(2), 540-554.
[http://dx.doi.org/10.1210/me.2004-0307] [PMID: 15498831]
[16]
Ritsner, M.; Modai, I.; Gibel, A.; Leschiner, S.; Silver, H.; Tsinovoy, G.; Weizman, A.; Gavish, M. Decreased platelet peripheral-type benzodiazepine receptors in persistently violent schizophrenia patients. J. Psychiatr. Res., 2003, 37(6), 549-556.
[http://dx.doi.org/10.1016/S0022-3956(03)00055-4] [PMID: 14563387]
[17]
Banati, R.B. Visualising microglial activation in vivo. Glia, 2002, 40(2), 206-217.
[http://dx.doi.org/10.1002/glia.10144] [PMID: 12379908]
[18]
Trapani, A.; Palazzo, C.; de Candia, M.; Lasorsa, F.M.; Trapani, G. Targeting of the translocator protein 18 kDa (TSPO): a valuable approach for nuclear and optical imaging of activated microglia. Bioconjug. Chem., 2013, 24(9), 1415-1428.
[http://dx.doi.org/10.1021/bc300666f] [PMID: 23837837]
[19]
Nutma, E.; Ceyzériat, K.; Amor, S.; Tsartsalis, S.; Millet, P.; Owen, D.R.; Papadopoulos, V.; Tournier, B.B. Cellular sources of TSPO expression in healthy and diseased brain. Eur. J. Nucl. Med. Mol. Imaging, 2021, 49(1), 146-163.
[http://dx.doi.org/10.1007/s00259-020-05166-2] [PMID: 33433698]
[20]
Dupont, A.C.; Largeau, B.; Santiago Ribeiro, M.J.; Guilloteau, D.; Tronel, C.; Arlicot, N. Translocator Protein-18 kDa (TSPO) Positron Emission Tomography (PET) Imaging and Its Clinical Impact in Neurodegenerative Diseases. Int. J. Mol. Sci., 2017, 18(4), 785-821.
[http://dx.doi.org/10.3390/ijms18040785] [PMID: 28387722]
[21]
Meyer, J.H.; Cervenka, S.; Kim, M.J.; Kreisl, W.C.; Henter, I.D.; Innis, R.B. Neuroinflammation in psychiatric disorders: PET imaging and promising new targets. Lancet Psychiatry, 2020, 7(12), 1064-1074.
[http://dx.doi.org/10.1016/S2215-0366(20)30255-8] [PMID: 33098761]
[22]
Notter, T.; Coughlin, J.M.; Gschwind, T.; Weber-Stadlbauer, U.; Wang, Y.; Kassiou, M.; Vernon, A.C.; Benke, D.; Pomper, M.G.; Sawa, A.; Meyer, U. Translational evaluation of translocator protein as a marker of neuroinflammation in schizophrenia. Mol. Psychiatry, 2018, 23(2), 323-334.
[http://dx.doi.org/10.1038/mp.2016.248] [PMID: 28093569]
[23]
Zhang, X.Y.; Wei, W.; Zhang, Y.Z.; Fu, Q.; Mi, W.D.; Zhang, L.M.; Li, Y.F. The 18 kDa Translocator Protein (TSPO) overexpression in hippocampal dentate gyrus elicits anxiolytic-like effects in a mouse model of post-traumatic stress disorder. Front. Pharmacol., 2018, 9, 1364-1374.
[http://dx.doi.org/10.3389/fphar.2018.01364] [PMID: 30532709]
[24]
Attwells, S.; Setiawan, E.; Wilson, A.A.; Rusjan, P.M.; Mizrahi, R.; Miler, L.; Xu, C.; Richter, M.A.; Kahn, A.; Kish, S.J.; Houle, S.; Ravindran, L.; Meyer, J.H. Inflammation in the neurocircuitry of obsessive-compulsive disorder. JAMA Psychiatry, 2017, 74(8), 833-840.
[http://dx.doi.org/10.1001/jamapsychiatry.2017.1567] [PMID: 28636705]
[25]
Favreau, F.; Rossard, L.; Zhang, K.; Desurmont, T.; Manguy, E.; Belliard, A.; Fabre, S.; Liu, J.; Han, Z.; Thuillier, R.; Papadopoulos, V.; Hauet, T. Expression and modulation of translocator protein and its partners by hypoxia reoxygenation or ischemia and reperfusion in porcine renal models. Am. J. Physiol. Renal Physiol., 2009, 297(1), F177-F190.
[http://dx.doi.org/10.1152/ajprenal.90422.2008] [PMID: 19386723]
[26]
Ran, C.; Albrecht, D.S.; Bredella, M.A.; Yang, J.; Yang, J.; Liang, S.H.; Cypess, A.M.; Loggia, M.L.; Atassi, N.; Moore, A. PET imaging of human brown adipose tissue with the TSPO Tracer [11C]PBR28. Mol. Imaging Biol., 2018, 20(2), 188-193.
[http://dx.doi.org/10.1007/s11307-017-1129-z] [PMID: 28983743]
[27]
Herranz, E.; Giannì, C.; Louapre, C.; Treaba, C.A.; Govindarajan, S.T.; Ouellette, R.; Loggia, M.L.; Sloane, J.A.; Madigan, N.; Izquierdo-Garcia, D.; Ward, N.; Mangeat, G.; Granberg, T.; Klawiter, E.C.; Catana, C.; Hooker, J.M.; Taylor, N.; Ionete, C.; Kinkel, R.P.; Mainero, C. Neuroinflammatory component of gray matter pathology in multiple sclerosis. Ann. Neurol., 2016, 80(5), 776-790.
[http://dx.doi.org/10.1002/ana.24791] [PMID: 27686563]
[28]
Zürcher, N.R.; Loggia, M.L.; Lawson, R.; Chonde, D.B.; Izquierdo-Garcia, D.; Yasek, J.E.; Akeju, O.; Catana, C.; Rosen, B.R.; Cudkowicz, M.E.; Hooker, J.M.; Atassi, N. Increased in vivo glial activation in patients with amyotrophic lateral sclerosis: assessed with [11C]-PBR28. Neuroimage Clin., 2015, 7, 409-414.
[http://dx.doi.org/10.1016/j.nicl.2015.01.009] [PMID: 25685708]
[29]
Kreisl, W.C.; Lyoo, C.H.; Liow, J.S.; Snow, J.; Page, E.; Jenko, K.J.; Morse, C.L.; Zoghbi, S.S.; Pike, V.W.; Turner, R.S.; Innis, R.B. Distinct patterns of increased translocator protein in posterior cortical atrophy and amnestic Alzheimer’s disease. Neurobiol. Aging, 2017, 51, 132-140.
[http://dx.doi.org/10.1016/j.neurobiolaging.2016.12.006] [PMID: 28068564]
[30]
Notter, T.; Coughlin, J.M.; Sawa, A.; Meyer, U. Reconceptualization of translocator protein as a biomarker of neuroinflammation in psychiatry. Mol. Psychiatry, 2018, 23(1), 36-47.
[http://dx.doi.org/10.1038/mp.2017.232] [PMID: 29203847]
[31]
Wyatt, S.K.; Manning, H.C.; Bai, M.; Bailey, S.N.; Gallant, P.; Ma, G.; McIntosh, L.; Bornhop, D.J. Molecular imaging of the translocator protein (TSPO) in a pre-clinical model of breast cancer. Mol. Imaging Biol., 2010, 12(3), 349-358.
[http://dx.doi.org/10.1007/s11307-009-0270-8] [PMID: 19949989]
[32]
Jiemy, W.F.; Heeringa, P.; Kamps, J.A.A.M.; van der Laken, C.J.; Slart, R.H.J.A.; Brouwer, E. Positron emission tomography (PET) and single photon emission computed tomography (SPECT) imaging of macrophages in large vessel vasculitis: Current status and future prospects. Autoimmun. Rev., 2018, 17(7), 715-726.
[http://dx.doi.org/10.1016/j.autrev.2018.02.006] [PMID: 29729443]
[33]
Ametamey, S.M.; Honer, M.; Schubiger, P.A. Molecular imaging with PET. Chem. Rev., 2008, 108(5), 1501-1516.
[http://dx.doi.org/10.1021/cr0782426] [PMID: 18426240]
[34]
Kreisl, W.C.; Kim, M.J.; Coughlin, J.M.; Henter, I.D.; Owen, D.R.; Innis, R.B. PET imaging of neuroinflammation in neurological disorders. Lancet Neurol., 2020, 19(11), 940-950.
[http://dx.doi.org/10.1016/S1474-4422(20)30346-X] [PMID: 33098803]
[35]
Narayanaswami, V.; Dahl, K.; Bernard-Gauthier, V.; Josephson, L.; Cumming, P.; Vasdev, N. Emerging PET radiotracers and targets for imaging of neuroinflammation in neurodegenerative diseases: Outlook beyond TSPO. Mol. Imaging, 2018, 17, 1536012118792317.
[http://dx.doi.org/10.1177/1536012118792317] [PMID: 30203712]
[36]
Lagarde, J.; Sarazin, M.; Bottlaender, M. In vivo PET imaging of neuroinflammation in Alzheimer's disease. J. Neural Trans. , 2018, 125(5), 847-867.
[37]
Werry, E.L.; Bright, F.M.; Piguet, O.; Ittner, L.M.; Halliday, G.M.; Hodges, J.R.; Kiernan, M.C.; Loy, C.T.; Kril, J.J.; Kassiou, M. Recent developments in TSPO PET imaging as a biomarker of neuroinflammation in neurodegenerative disorders. Int. J. Mol. Sci., 2019, 20(13), 3161-3181.
[http://dx.doi.org/10.3390/ijms20133161] [PMID: 31261683]
[38]
Patel, S.; Gibson, R. In vivo site-directed radiotracers: A mini-review. Nucl. Med. Biol., 2008, 35(8), 805-815.
[http://dx.doi.org/10.1016/j.nucmedbio.2008.10.002] [PMID: 19026942]
[39]
Laruelle, M.; Slifstein, M.; Huang, Y. Relationships between radiotracer properties and image quality in molecular imaging of the brain with positron emission tomography. Mol. Imaging Biol., 2003, 5(6), 363-375.
[http://dx.doi.org/10.1016/j.mibio.2003.09.009] [PMID: 14667491]
[40]
Waterhouse, R.N. Determination of lipophilicity and its use as a predictor of blood-brain barrier penetration of molecular imaging agents. Mol. Imaging Biol., 2003, 5(6), 376-389.
[http://dx.doi.org/10.1016/j.mibio.2003.09.014] [PMID: 14667492]
[41]
Pike, V.W. Considerations in the development of reversibly binding PET radioligands for brain imaging. Curr. Med. Chem., 2016, 23(18), 1818-1869.
[http://dx.doi.org/10.2174/0929867323666160418114826] [PMID: 27087244]
[42]
Hall, M.D.; Pike, V.W. Avoiding barriers to PET radioligand development: Cellular assays of brain efflux transporters. J. Nuclear Med., 2011, 52(3), 338-340.
[43]
Pike, V.W. PET radiotracers: crossing the blood-brain barrier and surviving metabolism. Trends Pharmacol. Sci., 2009, 30(8), 431-440.
[http://dx.doi.org/10.1016/j.tips.2009.05.005] [PMID: 19616318]
[44]
Kreisl, W.C.; Fujita, M.; Fujimura, Y.; Kimura, N.; Jenko, K.J.; Kannan, P.; Hong, J.; Morse, C.L.; Zoghbi, S.S.; Gladding, R.L.; Jacobson, S.; Oh, U.; Pike, V.W.; Innis, R.B. Comparison of [11C]-(R)-PK 11195 and [11C]PBR28, two radioligands for translocator protein (18 kDa) in human and monkey: Implications for positron emission tomographic imaging of this inflammation biomarker. Neuroimage, 2010, 49(4), 2924-2932.
[http://dx.doi.org/10.1016/j.neuroimage.2009.11.056] [PMID: 19948230]
[45]
Zhang, L.; Villalobos, A.; Beck, E.M.; Bocan, T.; Chappie, T.A.; Chen, L.; Grimwood, S.; Heck, S.D.; Helal, C.J.; Hou, X.; Humphrey, J.M.; Lu, J.; Skaddan, M.B.; McCarthy, T.J.; Verhoest, P.R.; Wager, T.T.; Zasadny, K. Design and selection parameters to accelerate the discovery of novel central nervous system positron emission tomography (PET) ligands and their application in the development of a novel phosphodiesterase 2A PET ligand. J. Med. Chem., 2013, 56(11), 4568-4579.
[http://dx.doi.org/10.1021/jm400312y] [PMID: 23651455]
[46]
Cho, Z.H.; Chan, J.K.; Ericksson, L.; Singh, M.; Graham, S.; MacDonald, N.S.; Yano, Y. Positron ranges obtained from biomedically important positron-emitting radionuclides. J. Nuclear Med., 1975, 16(12), 1174-1176.
[47]
Carter, L.M.; Kesner, A.L.; Pratt, E.C.; Sanders, V.A.; Massicano, A.V.F.; Cutler, C.S.; Lapi, S.E.; Lewis, J.S. The impact of positron range on PET resolution, evaluated with phantoms and PHITS Monte Carlo simulations for conventional and non-conventional radionuclides. Mol. Imaging Biol., 2020, 22(1), 73-84.
[http://dx.doi.org/10.1007/s11307-019-01337-2] [PMID: 31001765]
[48]
Zanotti-Fregonara, P.; Lammertsma, A.A.; Innis, R.B. 11C dosimetry scans should be abandoned. J. Nuclear Med., 2021, 62(2), 158-159.
[49]
Patani, G.A.; LaVoie, E.J. Bioisosterism: A rational approach in drug design. Chem. Rev., 1996, 96(8), 3147-3176.
[http://dx.doi.org/10.1021/cr950066q] [PMID: 11848856]
[50]
Meanwell, N.A. Synopsis of some recent tactical application of bioisosteres in drug design. J. Med. Chem., 2011, 54(8), 2529-2591.
[http://dx.doi.org/10.1021/jm1013693] [PMID: 21413808]
[51]
Meanwell, N.A. Fluorine and fluorinated motifs in the design and application of bioisosteres for drug design. J. Med. Chem., 2018, 61(14), 5822-5880.
[http://dx.doi.org/10.1021/acs.jmedchem.7b01788] [PMID: 29400967]
[52]
Fujita, M.; Imaizumi, M.; Zoghbi, S.S.; Fujimura, Y.; Farris, A.G.; Suhara, T.; Hong, J.; Pike, V.W.; Innis, R.B. Kinetic analysis in healthy humans of a novel positron emission tomography radioligand to image the peripheral benzodiazepine receptor, a potential biomarker for inflammation. Neuroimage, 2008, 40(1), 43-52.
[http://dx.doi.org/10.1016/j.neuroimage.2007.11.011] [PMID: 18093844]
[53]
Owen, D.R.; Howell, O.W.; Tang, S.P.; Wells, L.A.; Bennacef, I.; Bergstrom, M.; Gunn, R.N.; Rabiner, E.A.; Wilkins, M.R.; Reynolds, R.; Matthews, P.M.; Parker, C.A. Two binding sites for [3H]PBR28 in human brain: Implications for TSPO PET imaging of neuroinflammation. J. Cereb. Blood Flow Metab., 2010, 30(9), 1608-1618.
[http://dx.doi.org/10.1038/jcbfm.2010.63] [PMID: 20424634]
[54]
Owen, D.R.; Yeo, A.J.; Gunn, R.N.; Song, K.; Wadsworth, G.; Lewis, A.; Rhodes, C.; Pulford, D.J.; Bennacef, I.; Parker, C.A.; StJean, P.L.; Cardon, L.R.; Mooser, V.E.; Matthews, P.M.; Rabiner, E.A.; Rubio, J.P. 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), 1-5.
[http://dx.doi.org/10.1038/jcbfm.2011.147] [PMID: 22008728]
[55]
Owen, D.R.; Guo, Q.; Rabiner, E.A.; Gunn, R.N. The impact of the rs6971 polymorphism in TSPO for quantification and study design. Clin. Transl. Imaging, 2015, 3(6), 417-422.
[http://dx.doi.org/10.1007/s40336-015-0141-z]
[56]
Taliani, S.; Pugliesi, I.; Da Settimo, F. Structural requirements to obtain highly potent and selective 18 kDa Translocator Protein (TSPO) Ligands. Curr. Top. Med. Chem., 2011, 11(7), 860-886.
[http://dx.doi.org/10.2174/156802611795165142] [PMID: 21291396]
[57]
Junck, L.; Olson, J.M.; Ciliax, B.J.; Koeppe, R.A.; Watkins, G.L.; Jewett, D.M.; McKeever, P.E.; Wieland, D.M.; Kilbourn, M.R.; Starosta-Rubinstein, S. PET imaging of human gliomas with ligands for the peripheral benzodiazepine binding site. Ann. Neurol., 1989, 26(6), 752-758.
[http://dx.doi.org/10.1002/ana.410260611] [PMID: 2557794]
[58]
Farges, R.; Joseph-Liauzun, E.; Shire, D.; Caput, D.; Le Fur, G.; Ferrara, P. Site-directed mutagenesis of the peripheral benzodiazepine receptor: Identification of amino acids implicated in the binding site of Ro5-4864. Mol. Pharmacol., 1994, 46(6), 1160-1167.
[PMID: 7808437]
[59]
Van Dort, M.E.; Ciliax, B.J.; Gildersleeve, D.L.; Sherman, P.S.; Rosenspire, K.C.; Young, A.B.; Junck, L.; Wieland, D.M. Radioiodinated benzodiazepines: Agents for mapping glial tumors. J. Med. Chem., 1988, 31(11), 2081-2086.
[http://dx.doi.org/10.1021/jm00119a005] [PMID: 2846836]
[60]
Camsonne, R.; Crouzel, C.; Comar, D.; Mazière, M.; Prenant, C.; Sastre, J.; Moulin, M.; Syrota, A. Synthesis of N-(11C) methyl, N-(methyl-1 propyl), (chloro-2 phenyl)-1 isoquinoleine carboxamide-3 (PK 11195): A new ligand for peripheral benzodiazepine receptors. 1984, 21(10), 985-991.
[61]
Shah, F.; Hume, S.P.; Pike, V.W.; 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(4), 573-581.
[http://dx.doi.org/10.1016/0969-8051(94)90022-1] [PMID: 9234314]
[62]
Tondo, G.; Boccalini, C.; Caminiti, S.P.; Presotto, L.; Filippi, M.; Magnani, G.; Frisoni, G.B.; Iannaccone, S.; Perani, D. Brain metabolism and microglia activation in mild cognitive impairment: A combined [18F]FDG and [11C]-(R)-PK11195 PET study. J. Alzheimers Dis., 2021, 80(1), 433-445.
[http://dx.doi.org/10.3233/JAD-201351] [PMID: 33579848]
[63]
Tondo, G.; Iaccarino, L.; Cerami, C.; Vanoli, G.E.; Presotto, L.; Masiello, V.; Coliva, A.; Salvi, F.; Bartolomei, I.; Mosca, L.; Lunetta, C.; Perani, D. 11 C-PK11195 PET-based molecular study of microglia activation in SOD1 amyotrophic lateral sclerosis. Ann. Clin. Transl. Neurol., 2020, 7(9), 1513-1523.
[http://dx.doi.org/10.1002/acn3.51112] [PMID: 32762033]
[64]
van der Doef, T.F.; de Witte, L.D.; Sutterland, A.L.; Jobse, E.; Yaqub, M.; Boellaard, R.; de Haan, L.; Eriksson, J.; Lammertsma, A.A.; Kahn, R.S.; van Berckel, B.N. In vivo (R)-[11C]PK11195 PET imaging of 18kDa translocator protein in recent onset psychosis. NPJ Schizophr., 2016, 2(1), 16031-16035.
[http://dx.doi.org/10.1038/npjschz.2016.31] [PMID: 27602389]
[65]
Seo, S.; Jung, Y.H.; Lee, D.; Lee, W.J.; Jang, J.H.; Lee, J.Y.; Choi, S.H.; Moon, J.Y.; Lee, J.S.; Cheon, G.J.; Kang, D.H. Abnormal neuroinflammation in fibromyalgia and CRPS using [11C]-(R)-PK11195 PET. PLoS One, 2021, 16(2), e0246152.
[http://dx.doi.org/10.1371/journal.pone.0246152] [PMID: 33556139]
[66]
Iaccarino, L.; Moresco, R.M.; Presotto, L.; Bugiani, O.; Iannaccone, S.; Giaccone, G.; Tagliavini, F.; Perani, D. An in vivo11C-(R)-PK11195 PET and in vitro pathology study of microglia activation in creutzfeldt-jakob disease. Mol. Neurobiol., 2018, 55(4), 2856-2868.
[http://dx.doi.org/10.1007/s12035-017-0522-6] [PMID: 28455699]
[67]
Chauveau, F.; Boutin, H.; Van Camp, N.; Dollé, F.; Tavitian, B. Nuclear imaging of neuroinflammation: A comprehensive review of [11C]PK11195 challengers. Eur. J. Nucl. Med. Mol. Imaging, 2008, 35(12), 2304-2319.
[http://dx.doi.org/10.1007/s00259-008-0908-9] [PMID: 18828015]
[68]
Schuitemaker, A.; van Berckel, B.N.; Kropholler, M.A.; Veltman, D.J.; Scheltens, P.; Jonker, C.; Lammertsma, A.A.; Boellaard, R. SPM analysis of parametric (R)-[11C]PK11195 binding images: plasma input versus reference tissue parametric methods. Neuroimage, 2007, 35(4), 1473-1479.
[http://dx.doi.org/10.1016/j.neuroimage.2007.02.013] [PMID: 17363280]
[69]
Parente, A.; Feltes, P.K.; Vállez García, D.; Sijbesma, J.W.; Moriguchi Jeckel, C.M.; Dierckx, R.A.; de Vries, E.F.; Doorduin, J. Pharmacokinetic analysis of 11C-PBR28 in the rat model of herpes encephalitis: Comparison with (R)-11C-PK11195. J. Nuclear Med., 2016, 57(5), 785-791.
[70]
Pascali, C.; Luthra, S.K.; Pike, V.W.; Price, G.W.; Ahier, R.G.; Hume, S.P.; Myers, R.; Manjil, L.; Cremer, J.E. The radiosynthesis of [18F]PK 14105 as an alternative radioligand for peripheral type benzodiazepine binding sites. Int. J. Rad. Appl. Instrum. [A], 1990, 41(5), 477-482.
[http://dx.doi.org/10.1016/0883-2889(90)90008-5] [PMID: 2166014]
[71]
Price, G.W.; Ahier, R.G.; Hume, S.P.; Myers, R.; Manjil, L.; Cremer, J.E.; Luthra, S.K.; Pascali, C.; Pike, V.; Frackowiak, R.S. In vivo binding to peripheral benzodiazepine binding sites in lesioned rat brain: Comparison between [3H]PK11195 and [18F]PK14105 as markers for neuronal damage. J. Neurochem., 1990, 55(1), 175-185.
[http://dx.doi.org/10.1111/j.1471-4159.1990.tb08836.x] [PMID: 2355218]
[72]
Matarrese, M.; Moresco, R.M.; Cappelli, A.; Anzini, M.; Vomero, S.; Simonelli, P.; Verza, E.; Magni, F.; Sudati, F.; Soloviev, D.; Todde, S.; Carpinelli, A.; Kienle, M.G.; Fazio, F. Labeling and evaluation of N-[11C]methylated quinoline-2-carboxamides as potential radioligands for visualization of peripheral benzodiazepine receptors. J. Med. Chem., 2001, 44(4), 579-585.
[http://dx.doi.org/10.1021/jm001004h] [PMID: 11170647]
[73]
Belloli, S.; Moresco, R.M.; Matarrese, M.; Biella, G.; Sanvito, F.; Simonelli, P.; Turolla, E.; Olivieri, S.; Cappelli, A.; Vomero, S.; Galli-Kienle, M.; Fazio, F. Evaluation of three quinoline-carboxamide derivatives as potential radioligands for the in vivo pet imaging of neurodegeneration. Neurochem. Int., 2004, 44(6), 433-440.
[http://dx.doi.org/10.1016/j.neuint.2003.08.006] [PMID: 14687608]
[74]
Cappelli, A.; Matarrese, M.; Moresco, R.M.; Valenti, S.; Anzini, M.; Vomero, S.; Turolla, E.A.; Belloli, S.; Simonelli, P.; Filannino, M.A.; Lecchi, M.; Fazio, F. Synthesis, labeling, and biological evaluation of halogenated 2-quinolinecarboxamides as potential radioligands for the visualization of peripheral benzodiazepine receptors. Bioorg. Med. Chem., 2006, 14(12), 4055-4066.
[http://dx.doi.org/10.1016/j.bmc.2006.02.004] [PMID: 16495062]
[75]
Di Grigoli, G.; Monterisi, C.; Belloli, S.; Masiello, V.; Politi, L.S.; Valenti, S.; Paolino, M.; Anzini, M.; Matarrese, M.; Cappelli, A.; Moresco, R.M. Radiosynthesis and preliminary biological evaluation of [18F]VC701, a Radioligand for translocator protein. Mol. Imaging, 2015, 14(6), 14-22.
[http://dx.doi.org/10.2310/7290.2015.00007] [PMID: 26044669]
[76]
Castellano, S.; Taliani, S.; Milite, C.; Pugliesi, I.; Da Pozzo, E.; Rizzetto, E.; Bendinelli, S.; Costa, B.; Cosconati, S.; Greco, G.; Novellino, E.; Sbardella, G.; Stefancich, G.; Martini, C.; Da Settimo, F. Synthesis and biological evaluation of 4-phenylquinazoline-2-carboxamides designed as a novel class of potent ligands of the translocator protein. J. Med. Chem., 2012, 55(9), 4506-4510.
[http://dx.doi.org/10.1021/jm201703k] [PMID: 22489952]
[77]
Castellano, S.; Taliani, S.; Viviano, M.; Milite, C.; Da Pozzo, E.; Costa, B.; Barresi, E.; Bruno, A.; Cosconati, S.; Marinelli, L.; Greco, G.; Novellino, E.; Sbardella, G.; Da Settimo, F.; Martini, C. Structure-activity relationship refinement and further assessment of 4-phenylquinazoline-2-carboxamide translocator protein ligands as antiproliferative agents in human glioblastoma tumors. J. Med. Chem., 2014, 57(6), 2413-2428.
[http://dx.doi.org/10.1021/jm401721h] [PMID: 24580635]
[78]
Zanotti-Fregonara, P.; Zhang, Y.; Jenko, K.J.; Gladding, R.L.; Zoghbi, S.S.; Fujita, M.; Sbardella, G.; Castellano, S.; Taliani, S.; Martini, C.; Innis, R.B.; Da Settimo, F.; Pike, V.W. Synthesis and evaluation of translocator 18 kDa protein (TSPO) positron emission tomography (PET) radioligands with low binding sensitivity to human single nucleotide polymorphism rs6971. ACS Chem. Neurosci., 2014, 5(10), 963-971.
[http://dx.doi.org/10.1021/cn500138n] [PMID: 25123416]
[79]
Ikawa, M.; Lohith, T.G.; Shrestha, S.; Telu, S.; Zoghbi, S.S.; Castellano, S.; Taliani, S.; Da Settimo, F.; Fujita, M.; Pike, V.W.; Innis, R.B. 11c-er176, a radioligand for 18-kda translocator protein, has adequate sensitivity to robustly image all three affinity genotypes in human brain. J. Nuclear Med., 2017, 58(2), 320-325.
[80]
Zanotti-Fregonara, P.; Pascual, B.; Veronese, M.; Yu, M.; Beers, D.; Appel, S.H.; Masdeu, J.C. Head-to-head comparison of 11C-PBR28 and 11C-ER176 for quantification of the translocator protein in the human brain. Eur. J. Nucl. Med. Mol. Imaging, 2019, 46(9), 1822-1829.
[http://dx.doi.org/10.1007/s00259-019-04349-w] [PMID: 31152207]
[81]
Fujita, M.; Kobayashi, M.; Ikawa, M.; Gunn, R.N.; Rabiner, E.A.; Owen, D.R.; Zoghbi, S.S.; Haskali, M.B.; Telu, S.; Pike, V.W.; Innis, R.B. Comparison of four 11C-labeled PET   ligands   to   quantify  translocator  protein  18 kDa (TSPO) in human brain: (R)-PK11195, PBR28, DPA-713, and ER176-based on recent publications that measured specific-to-non-displaceable ratios. EJNMMI Res., 2017, 7(1), 84-88.
[http://dx.doi.org/10.1186/s13550-017-0334-8] [PMID: 29038960]
[82]
Downer, O.M.; Marcus, R.E.G.; Zürcher, N.R.; Hooker, J.M. Tracing the history of the human translocator protein to recent neurodegenerative and psychiatric imaging. ACS Chem. Neurosci., 2020, 11(15), 2192-2200.
[http://dx.doi.org/10.1021/acschemneuro.0c00362] [PMID: 32662626]
[83]
Hong, J.; Telu, S.; Zhang, Y.; Miller, W.H.; Shetty, H.U.; Morse, C.L.; Pike, V.W. Translation of 11C-labeled tracer synthesis to a CGMP environment as exemplified by [11C]ER176 for PET imaging of human TSPO. Nat. Protoc., 2021, 16(9), 4419-4445.
[http://dx.doi.org/10.1038/s41596-021-00584-4] [PMID: 34363068]
[84]
Siméon, F.G.; Lee, J.H.; Morse, C.L.; Stukes, I.; Zoghbi, S.S.; Manly, L.S.; Liow, J.S.; Gladding, R.L.; Dick, R.M.; Yan, X.; Taliani, S.; Costa, B.; Martini, C.; Da Settimo, F.; Castellano, S.; Innis, R.B.; Pike, V.W. Synthesis and screening in mice of fluorine-containing PET radioligands for TSPO: discovery of a promising 18F-labeled ligand. J. Med. Chem., 2021, 64(22), 16731-16745.
[http://dx.doi.org/10.1021/acs.jmedchem.1c01562] [PMID: 34756026]
[85]
Okuyama, S.; Chaki, S.; Yoshikawa, R.; Ogawa, S.; Suzuki, Y.; Okubo, T.; Nakazato, A.; Nagamine, M.; Tomisawa, K. Neuropharmacological profile of peripheral benzodiazepine receptor agonists, DAA1097 and DAA1106. Life Sci., 1999, 64(16), 1455-1464.
[http://dx.doi.org/10.1016/S0024-3205(99)00079-X] [PMID: 10321725]
[86]
Zhang, M.R.; Kida, T.; Noguchi, J.; Furutsuka, K.; Maeda, J.; Suhara, T.; Suzuki, K. [11C]DAA1106: Radiosynthesis and in vivo binding to peripheral benzodiazepine receptors in mouse brain. Nucl. Med. Biol., 2003, 30(5), 513-519.
[http://dx.doi.org/10.1016/S0969-8051(03)00016-7] [PMID: 12831989]
[87]
Venneti, S.; Lopresti, B.J.; Wang, G.; Slagel, S.L.; Mason, N.S.; Mathis, C.A.; Fischer, M.L.; Larsen, N.J.; Mortimer, A.D.; Hastings, T.G.; Smith, A.D.; Zigmond, M.J.; Suhara, T.; Higuchi, M.; Wiley, C.A. A comparison of the high-affinity peripheral benzodiazepine receptor ligands DAA1106 and (R)-PK11195 in rat models of neuroinflammation: implications for PET imaging of microglial activation. J. Neurochem., 2007, 102(6), 2118-2131.
[http://dx.doi.org/10.1111/j.1471-4159.2007.04690.x] [PMID: 17555551]
[88]
Venneti, S.; Wang, G.; Nguyen, J.; Wiley, C.A. The positron emission tomography ligand DAA1106 binds with high affinity to activated microglia in human neurological disorders. J. Neuropathol. Exp. Neurol., 2008, 67(10), 1001-1010.
[http://dx.doi.org/10.1097/NEN.0b013e318188b204] [PMID: 18800007]
[89]
Yasuno, F.; Ota, M.; Kosaka, J.; Ito, H.; Higuchi, M.; Doronbekov, T.K.; Nozaki, S.; Fujimura, Y.; Koeda, M.; Asada, T.; Suhara, T. Increased binding of peripheral benzodiazepine receptor in Alzheimer’s disease measured by positron emission tomography with [11C]DAA1106. Biol. Psychiatry, 2008, 64(10), 835-841.
[http://dx.doi.org/10.1016/j.biopsych.2008.04.021] [PMID: 18514164]
[90]
Takano, A.; Arakawa, R.; Ito, H.; Tateno, A.; Takahashi, H.; Matsumoto, R.; Okubo, Y.; Suhara, T. Peripheral benzodiazepine receptors in patients with chronic schizophrenia: a PET study with [11C]DAA1106. Int. J. Neuropsychopharmacol., 2010, 13(7), 943-950.
[http://dx.doi.org/10.1017/S1461145710000313] [PMID: 20350336]
[91]
Brody, A.L.; Hubert, R.; Enoki, R.; Garcia, L.Y.; Mamoun, M.S.; Okita, K.; London, E.D.; Nurmi, E.L.; Seaman, L.C.; Mandelkern, M.A. Effect of cigarette smoking on a marker for neuroinflammation: A [11C]DAA1106 Positron Emission Tomography study. Neuropsychopharmacology, 2017, 42(8), 1630-1639.
[92]
Brody, A.L.; Gehlbach, D.; Garcia, L.Y.; Enoki, R.; Hoh, C.; Vera, D.; Kotta, K.K.; London, E.D.; Okita, K.; Nurmi, E.L.; Seaman, L.C.; Mandelkern, M.A. Effect of overnight smoking abstinence on a marker for microglial activation: A [11C]DAA1106 positron emission tomography study. Psychopharmacology (Berl.), 2018, 235(12), 3525-3534.
[http://dx.doi.org/10.1007/s00213-018-5077-3] [PMID: 30343364]
[93]
Zhang, M.R.; Maeda, J.; Furutsuka, K.; Yoshida, Y.; Ogawa, M.; Suhara, T.; Suzuki, K. [18F]FMDAA1106 and [18F]FEDAA1106: two positron-emitter labeled ligands for peripheral benzodiazepine receptor (PBR). Bioorg. Med. Chem. Lett., 2003, 13(2), 201-204.
[http://dx.doi.org/10.1016/S0960-894X(02)00886-7] [PMID: 12482423]
[94]
Zhang, M.R.; Maeda, J.; Ogawa, M.; Noguchi, J.; Ito, T.; Yoshida, Y.; Okauchi, T.; Obayashi, S.; Suhara, T.; Suzuki, K. Development of a new radioligand, N-(5-fluoro-2-phenoxyphenyl)-N-(2-[18F]fluoroethyl-5-methoxybenzyl)acetamide, for pet imaging of peripheral benzodiazepine receptor in primate brain. J. Med. Chem., 2004, 47(9), 2228-2235.
[http://dx.doi.org/10.1021/jm0304919] [PMID: 15084121]
[95]
Fujimura, Y.; Ikoma, Y.; Yasuno, F.; Suhara, T.; Ota, M.; Matsumoto, R.; Nozaki, S.; Takano, A.; Kosaka, J.; Zhang, M.R.; Nakao, R.; Suzuki, K.; Kato, N.; Ito, H. Quantitative analyses of 18F-FEDAA1106 binding to peripheral benzodiazepine receptors in living human brain. Journal of nuclear medicine , 2006, 47(1), 43-50.
[96]
Varrone, A.; Mattsson, P.; Forsberg, A.; Takano, A.; Nag, S.; Gulyás, B.; Borg, J.; Boellaard, R.; Al-Tawil, N.; Eriksdotter, M.; Zimmermann, T.; Schultze-Mosgau, M.; Thiele, A.; Hoffmann, A.; Lammertsma, A.A.; Halldin, C. In vivo imaging of the 18-kDa translocator protein (TSPO) with [18F]FEDAA1106 and PET does not show increased binding in Alzheimer’s disease patients. Eur. J. Nucl. Med. Mol. Imaging, 2013, 40(6), 921-931.
[http://dx.doi.org/10.1007/s00259-013-2359-1] [PMID: 23436070]
[97]
Briard, E.; Zoghbi, S.S.; Siméon, F.G.; Imaizumi, M.; Gourley, J.P.; Shetty, H.U.; Lu, S.; Fujita, M.; Innis, R.B.; Pike, V.W. Single-step high-yield radiosynthesis and evaluation of a sensitive 18F-labeled ligand for imaging brain peripheral benzodiazepine receptors with PET. J. Med. Chem., 2009, 52(3), 688-699.
[http://dx.doi.org/10.1021/jm8011855] [PMID: 19119848]
[98]
Fujimura, Y.; Kimura, Y.; Siméon, F.G.; Dickstein, L.P.; Pike, V.W.; Innis, R.B.; Fujita, M. Biodistribution and radiation dosimetry in humans of a new PET ligand, 18F-PBR06, to image translocator protein (18 kDa). J. Nuclear Med., 2010, 51(1), 145-149.
[99]
Imaizumi, M.; Briard, E.; Zoghbi, S.S.; Gourley, J.P.; Hong, J.; Musachio, J.L.; Gladding, R.; Pike, V.W.; Innis, R.B.; Fujita, M. Kinetic evaluation in nonhuman primates of two new PET ligands for peripheral benzodiazepine receptors in brain. Synapse, 2007, 61(8), 595-605.
[http://dx.doi.org/10.1002/syn.20394] [PMID: 17455247]
[100]
Simmons, D.A.; James, M.L.; Belichenko, N.P.; Semaan, S.; Condon, C.; Kuan, J.; Shuhendler, A.J.; Miao, Z.; Chin, F.T.; Longo, F.M. TSPO-PET imaging using [18F]PBR06 is a potential translatable biomarker for treatment response in Huntington’s disease: preclinical evidence with the p75NTR ligand LM11A-31. Hum. Mol. Genet., 2018, 27(16), 2893-2912.
[http://dx.doi.org/10.1093/hmg/ddy202] [PMID: 29860333]
[101]
Lartey, F.M.; Ahn, G.O.; Ali, R.; Rosenblum, S.; Miao, Z.; Arksey, N.; Shen, B.; Colomer, M.V.; Rafat, M.; Liu, H.; Alejandre-Alcazar, M.A.; Chen, J.W.; Palmer, T.; Chin, F.T.; Guzman, R.; Loo, B.W., Jr; Graves, E. The relationship between serial [18 F]PBR06 PET imaging of microglial activation and motor function following stroke in mice. Mol. Imaging Biol., 2014, 16(6), 821-829.
[http://dx.doi.org/10.1007/s11307-014-0745-0] [PMID: 24865401]
[102]
Briard, E.; Zoghbi, S.S.; Imaizumi, M.; Gourley, J.P.; Shetty, H.U.; Hong, J.; Cropley, V.; Fujita, M.; Innis, R.B.; Pike, V.W. Synthesis and evaluation in monkey of two sensitive 11C-labeled aryloxyanilide ligands for imaging brain peripheral benzodiazepine receptors in vivo. J. Med. Chem., 2008, 51(1), 17-30.
[http://dx.doi.org/10.1021/jm0707370] [PMID: 18067245]
[103]
Imaizumi, M.; Briard, E.; Zoghbi, S.S.; Gourley, J.P.; Hong, J.; Fujimura, Y.; Pike, V.W.; Innis, R.B.; Fujita, M. Brain and whole-body imaging in nonhuman primates of [11C]PBR28, a promising PET radioligand for peripheral benzodiazepine receptors. Neuroimage, 2008, 39(3), 1289-1298.
[http://dx.doi.org/10.1016/j.neuroimage.2007.09.063] [PMID: 18024084]
[104]
Kreisl, W.C.; Lyoo, C.H.; Liow, J.S.; Wei, M.; Snow, J.; Page, E.; Jenko, K.J.; Morse, C.L.; Zoghbi, S.S.; Pike, V.W.; Turner, R.S.; Innis, R.B. 11C-PBR28 binding to translocator protein increases with progression of Alzheimer’s disease. Neurobiol. Aging, 2016, 44, 53-61.
[http://dx.doi.org/10.1016/j.neurobiolaging.2016.04.011] [PMID: 27318133]
[105]
Zou, J.; Tao, S.; Johnson, A.; Tomljanovic, Z.; Polly, K.; Klein, J.; Razlighi, Q.R.; Brickman, A.M.; Lee, S.; Stern, Y.; Kreisl, W.C. Microglial activation, but not tau pathology, is independently associated with amyloid positivity and memory impairment. Neurobiol. Aging, 2020, 85, 11-21.
[http://dx.doi.org/10.1016/j.neurobiolaging.2019.09.019] [PMID: 31698286]
[106]
Barletta, V.T.; Herranz, E.; Treaba, C.A.; Ouellette, R.; Mehndiratta, A.; Loggia, M.L.; Klawiter, E.C.; Ionete, C.; Jacob, S.A.; Mainero, C. Evidence of diffuse cerebellar neuroinflammation in multiple sclerosis by 11C-PBR28 MR-PET. Mult. Scler., 2020, 26(6), 668-678.
[http://dx.doi.org/10.1177/1352458519843048] [PMID: 30973800]
[107]
Zürcher, N.R.; Loggia, M.L.; Mullett, J.E.; Tseng, C.; Bhanot, A.; Richey, L.; Hightower, B.G.; Wu, C.; Parmar, A.J.; Butterfield, R.I.; Dubois, J.M.; Chonde, D.B.; Izquierdo-Garcia, D.; Wey, H.Y.; Catana, C.; Hadjikhani, N.; McDougle, C.J.; Hooker, J.M. [11C]PBR28 MR-PET imaging reveals lower regional brain expression of translocator protein (TSPO) in young adult males with autism spectrum disorder. Mol. Psychiatry, 2021, 26(5), 1659-1669.
[http://dx.doi.org/10.1038/s41380-020-0682-z] [PMID: 32076115]
[108]
Lois, C.; González, I.; Izquierdo-García, D.; Zürcher, N.R.; Wilkens, P.; Loggia, M.L.; Hooker, J.M.; Rosas, H.D. Neuroinflammation in Huntington’s Disease: New Insights with 11C-PBR28 PET/MRI. ACS Chem. Neurosci., 2018, 9(11), 2563-2571.
[http://dx.doi.org/10.1021/acschemneuro.8b00072] [PMID: 29719953]
[109]
Forsberg, A.; Lampa, J.; Estelius, J.; Cervenka, S.; Farde, L.; Halldin, C.; Lekander, M.; Olgart Höglund, C.; Kosek, E. Disease activity in rheumatoid arthritis is inversely related to cerebral TSPO binding assessed by [11C]PBR28 positron emission tomography. J. Neuroimmunol., 2019, 334, 577000-577008.
[http://dx.doi.org/10.1016/j.jneuroim.2019.577000] [PMID: 31260948]
[110]
Hillmer, A.T.; Matuskey, D.; Huang, Y.; Nabulsi, N.; Ropchan, J.; Carson, R.E.; O’Malley, S.S.; Cosgrove, K.P. Tobacco smoking in people is not associated with altered 18-kDa translocator protein levels: A PET Study. J. Nuclear Med., 2020, 61(8), 1200-1204.
[111]
Owen, D.R.; Gunn, R.N.; Rabiner, E.A.; Bennacef, I.; Fujita, M.; Kreisl, W.C.; Innis, R.B.; Pike, V.W.; Reynolds, R.; Matthews, P.M.; Parker, C.A. Mixed-affinity binding in humans with 18-kDa translocator protein ligands. J. Nuclear Med., 2011, 52(1), 24-32.
[112]
Moon, B.S.; Kim, B.S.; Park, C.; Jung, J.H.; Lee, Y.W.; Lee, H.Y.; Chi, D.Y.; Lee, B.C.; Kim, S.E. [11F]Fluoromethyl-PBR28 as a potential radiotracer for TSPO: preclinical comparison with [11C]PBR28 in a rat model of neuroinflammation. Bioconjug. Chem., 2014, 25(2), 442-450.
[http://dx.doi.org/10.1021/bc400556h] [PMID: 24400917]
[113]
Kim, G.R.; Paeng, J.C.; Jung, J.H.; Moon, B.S.; Lopalco, A.; Denora, N.; Lee, B.C.; Kim, S.E. Assessment of TSPO in a rat experimental autoimmune myocarditis model: A comparison study between [11F]Fluoromethyl-PBR28 and [11F]CB251. Int. J. Mol. Sci., 2018, 19(1), 276-285.
[http://dx.doi.org/10.3390/ijms19010276]
[114]
Wilson, A.A.; Garcia, A.; Parkes, J.; McCormick, P.; Stephenson, K.A.; Houle, S.; Vasdev, N. Radiosynthesis and initial evaluation of [18F]-FEPPA for PET imaging of peripheral benzodiazepine receptors. Nucl. Med. Biol., 2008, 35(3), 305-314.
[http://dx.doi.org/10.1016/j.nucmedbio.2007.12.009] [PMID: 18355686]
[115]
Rusjan, P.M.; Wilson, A.A.; Bloomfield, P.M.; Vitcu, I.; Meyer, J.H.; Houle, S.; Mizrahi, R. Quantitation of translocator protein binding in human brain with the novel radioligand [18F]-FEPPA and positron emission tomography. J. Cereb. Blood Flow Metab., 2011, 31(8), 1807-1816.
[http://dx.doi.org/10.1038/jcbfm.2011.55] [PMID: 21522163]
[116]
Mizrahi, R.; Rusjan, P.M.; Kennedy, J.; Pollock, B.; Mulsant, B.; Suridjan, I.; De Luca, V.; Wilson, A.A.; Houle, S. Translocator protein (18 kDa) polymorphism (rs6971) explains in-vivo brain binding affinity of the PET radioligand [11F]-FEPPA. J. Cereb. Blood Flow Metab., 2012, 32(6), 968-972.
[http://dx.doi.org/10.1038/jcbfm.2012.46] [PMID: 22472607]
[117]
Ghadery, C.; Koshimori, Y.; Christopher, L.; Kim, J.; Rusjan, P.; Lang, A.E.; Houle, S.; Strafella, A.P. The interaction between neuroinflammation and β-Amyloid in cognitive decline in Parkinson’s Disease. Mol. Neurobiol., 2020, 57(1), 492-501.
[http://dx.doi.org/10.1007/s12035-019-01714-6] [PMID: 31385228]
[118]
Suridjan, I.; Pollock, B.G.; Verhoeff, N.P.; Voineskos, A.N.; Chow, T.; Rusjan, P.M.; Lobaugh, N.J.; Houle, S.; Mulsant, B.H.; Mizrahi, R. In-vivo imaging of grey and white matter neuroinflammation in Alzheimer’s disease: A positron emission tomography study with a novel radioligand, [18F]-FEPPA. Mol. Psychiatry, 2015, 20(12), 1579-1587.
[http://dx.doi.org/10.1038/mp.2015.1] [PMID: 25707397]
[119]
Hafizi, S.; Da Silva, T.; Meyer, J.H.; Kiang, M.; Houle, S.; Remington, G.; Prce, I.; Wilson, A.A.; Rusjan, P.M.; Sailasuta, N.; Mizrahi, R. Interaction between TSPO-a neuroimmune marker-and redox status in clinical high risk for psychosis: A PET-MRS study. Neuropsychopharmacology, 2018, 43(8), 1700-1705.
[120]
Damont, A.; Boisgard, R.; Kuhnast, B.; Lemée, F.; Raggiri, G.; Scarf, A.M.; Da Pozzo, E.; Selleri, S.; Martini, C.; Tavitian, B.; Kassiou, M.; Dollé, F. Synthesis of 6-[¹⁸F]fluoro-PBR28, a novel radiotracer for imaging the TSPO 18 kDa with PET. Bioorg. Med. Chem. Lett., 2011, 21(16), 4819-4822.
[http://dx.doi.org/10.1016/j.bmcl.2011.06.048] [PMID: 21741237]
[121]
Boutin, H.; Chauveau, F.; Thominiaux, C.; Kuhnast, B.; Grégoire, M.C.; Jan, S.; Trebossen, R.; Dollé, F.; Tavitian, B.; Mattner, F.; Katsifis, A. In vivo imaging of brain lesions with [11C]CLINME, a new PET radioligand of peripheral benzodiazepine receptors. Glia, 2007, 55(14), 1459-1468.
[http://dx.doi.org/10.1002/glia.20562] [PMID: 17680643]
[122]
Mattner, F.; Bandin, D.L.; Staykova, M.; Berghofer, P.; Gregoire, M.C.; Ballantyne, P.; Quinlivan, M.; Fordham, S.; Pham, T.; Willenborg, D.O.; Katsifis, A. Evaluation of [¹²³I]-CLINDE as a potent SPECT radiotracer to assess the degree of astroglia activation in cuprizone-induced neuroinflammation. Eur. J. Nucl. Med. Mol. Imaging, 2011, 38(8), 1516-1528.
[http://dx.doi.org/10.1007/s00259-011-1784-2] [PMID: 21484375]
[123]
Bourdier, T.; Henderson, D.; Fookes, C.J.; Lam, P.; Mattner, F.; Fulham, M.; Katsifis, A. Synthesis of [¹¹C]PBR170, a novel imidazopyridine, for imaging the translocator protein with PET. Appl. Radiat. Isotopes, 2014, 90, 46-52.
[124]
Sekimata, K.; Hatano, K.; Ogawa, M.; Abe, J.; Magata, Y.; Biggio, G.; Serra, M.; Laquintana, V.; Denora, N.; Latrofa, A.; Trapani, G.; Liso, G.; Ito, K. Radiosynthesis and in vivo evaluation of N-[11C]methylated imidazopyridineacetamides as PET tracers for peripheral benzodiazepine receptors. Nucl. Med. Biol., 2008, 35(3), 327-334.
[http://dx.doi.org/10.1016/j.nucmedbio.2007.12.005] [PMID: 18355688]
[125]
Fookes, C.J.; Pham, T.Q.; Mattner, F.; Greguric, I.; Loc’h, C.; Liu, X.; Berghofer, P.; Shepherd, R.; Gregoire, M.C.; Katsifis, A. Synthesis and biological evaluation of substituted [18F]imidazo[1,2-a]pyridines and [18F]pyrazolo[1,5-a]pyrimidines for the study of the peripheral benzodiazepine receptor using positron emission tomography. J. Med. Chem., 2008, 51(13), 3700-3712.
[http://dx.doi.org/10.1021/jm7014556] [PMID: 18557607]
[126]
Perrone, M.; Moon, B.S.; Park, H.S.; Laquintana, V.; Jung, J.H.; Cutrignelli, A.; Lopedota, A.; Franco, M.; Kim, S.E.; Lee, B.C.; Denora, N. A novel PET imaging probe for the detection and monitoring of translocator protein 18 kDa expression in pathological disorders. Sci. Rep., 2016, 6, 20422-20434.
[http://dx.doi.org/10.1038/srep20422] [PMID: 26853260]
[127]
Callaghan, P.D.; Wimberley, C.A.; Rahardjo, G.L.; Berghofer, P.J.; Pham, T.Q.; Jackson, T.; Zahra, D.; Bourdier, T.; Wyatt, N.; Greguric, I.; Howell, N.R.; Siegele, R.; Pastuovic, Z.; Mattner, F.; Loc’h, C.; Gregoire, M.C.; Katsifis, A. Comparison of in vivo binding properties of the 18-kDa translocator protein (TSPO) ligands [11F]PBR102 and [ 18F]PBR111 in a model of excitotoxin-induced neuroinflammation. Eur. J. Nucl. Med. Mol. Imaging, 2015, 42(1), 138-151.
[http://dx.doi.org/10.1007/s00259-014-2895-3] [PMID: 25231248]
[128]
Colasanti, A.; Guo, Q.; Muhlert, N.; Giannetti, P.; Onega, M.; Newbould, R.D.; Ciccarelli, O.; Rison, S.; Thomas, C.; Nicholas, R.; Muraro, P.A.; Malik, O.; Owen, D.R.; Piccini, P.; Gunn, R.N.; Rabiner, E.A.; Matthews, P.M. In vivo assessment of brain white matter inflammation in multiple sclerosis with 18F-PBR111 PET. J. Nuclear Med., 2014, 55(7), 1112-1118.
[129]
Guo, Q.; Colasanti, A.; Owen, D.R.; Onega, M.; Kamalakaran, A.; Bennacef, I.; Matthews, P.M.; Rabiner, E.A.; Turkheimer, F.E.; Gunn, R.N. Quantification of the specific translocator protein signal of 18F-PBR111 in healthy humans: A genetic polymorphism effect on in vivo binding. J. Nuclear Med., 2013, 54(11), 1915-1923.
[130]
Kim, K.; Kim, H.; Bae, S.H.; Lee, S.Y.; Kim, Y.H.; Na, J.; Lee, C.H.; Lee, M.S.; Ko, G.B.; Kim, K.Y.; Lee, S.H.; Song, I.H.; Cheon, G.J.; Kang, K.W.; Kim, S.E.; Chung, J.K.; Kim, E.E.; Paek, S.H.; Lee, J.S.; Lee, B.C.; Youn, H. [18F]CB251 PET/MR imaging probe targeting translocator protein (TSPO) independent of its polymorphism in a neuroinflammation model. Theranostics, 2020, 10(20), 9315-9331.
[http://dx.doi.org/10.7150/thno.46875] [PMID: 32802194]
[131]
James, M.L.; Fulton, R.R.; Henderson, D.J.; Eberl, S.; Meikle, S.R.; Thomson, S.; Allan, R.D.; Dolle, F.; Fulham, M.J.; Kassiou, M. Synthesis and in vivo evaluation of a novel peripheral benzodiazepine receptor PET radioligand. Bioorg. Med. Chem., 2005, 13(22), 6188-6194.
[http://dx.doi.org/10.1016/j.bmc.2005.06.030] [PMID: 16039131]
[132]
James, M.L.; Fulton, R.R.; Vercoullie, J.; Henderson, D.J.; Garreau, L.; Chalon, S.; Dolle, F.; Costa, B.; Guilloteau, D.; Kassiou, M. DPA-714, a new translocator protein-specific ligand: synthesis, radiofluorination, and pharmacologic characterization. J. Nuclear Med., 2008, 49(5), 814-822.
[133]
Chaney, A.; Cropper, H.C.; Johnson, E.M.; Lechtenberg, K.J.; Peterson, T.C.; Stevens, M.Y.; Buckwalter, M.S.; James, M.L. 11C-DPA-713 versus18F-GE-180: A preclinical comparison of translocator protein 18 kDa PET tracers to visualize acute and chronic neuroinflammation in a mouse model of ischemic stroke. J. Nuclear Med., 2019, 60(1), 122-128.
[134]
Kobayashi, M.; Jiang, T.; Telu, S.; Zoghbi, S.S.; Gunn, R.N.; Rabiner, E.A.; Owen, D.R.; Guo, Q.; Pike, V.W.; Innis, R.B.; Fujita, M. 11C-DPA-713 has much greater specific binding to translocator protein 18 kDa (TSPO) in human brain than 11C-( R)-PK11195. J. Cereb. Blood Flow Metab., 2018, 38(3), 393-403.
[http://dx.doi.org/10.1177/0271678X17699223] [PMID: 28322082]
[135]
Chauveau, F.; Van Camp, N.; Dollé, F.; Kuhnast, B.; Hinnen, F.; Damont, A.; Boutin, H.; James, M.; Kassiou, M.; Tavitian, B. Comparative evaluation of the translocator protein radioligands 11C-DPA-713, 18F-DPA-714, and 11C-PK11195 in a rat model of acute neuroinflammation. J. Nuclear Med., 2009, 50(3), 468-476.
[136]
Zinnhardt, B.; Müther, M.; Roll, W.; Backhaus, P.; Jeibmann, A.; Foray, C.; Barca, C.; Döring, C.; Tavitian, B.; Dollé, F.; Weckesser, M.; Winkeler, A.; Hermann, S.; Wagner, S.; Wiendl, H.; Stummer, W.; Jacobs, A.H.; Schäfers, M.; Grauer, O.M. TSPO imaging-guided characterization of the immunosuppressive myeloid tumor microenvironment in patients with malignant glioma. Neuro-oncol., 2020, 22(7), 1030-1043.
[http://dx.doi.org/10.1093/neuonc/noaa023] [PMID: 32047908]
[137]
Foray, C.; Valtorta, S.; Barca, C.; Winkeler, A.; Roll, W.; Müther, M.; Wagner, S.; Gardner, M.L.; Hermann, S.; Schäfers, M.; Grauer, O.M.; Moresco, R.M.; Zinnhardt, B.; Jacobs, A.H. Imaging temozolomide-induced changes in the myeloid glioma microenvironment. Theranostics, 2021, 11(5), 2020-2033.
[http://dx.doi.org/10.7150/thno.47269] [PMID: 33500706]
[138]
Golla, S.S.; Boellaard, R.; Oikonen, V.; Hoffmann, A.; van Berckel, B.N.; Windhorst, A.D.; Virta, J.; Haaparanta-Solin, M.; Luoto, P.; Savisto, N.; Solin, O.; Valencia, R.; Thiele, A.; Eriksson, J.; Schuit, R.C.; Lammertsma, A.A.; Rinne, J.O. Quantification of [18F]DPA-714 binding in the human brain: initial studies in healthy controls and Alzheimer’s disease patients. J. Cereb. Blood Flow Metab., 2015, 35(5), 766-772.
[http://dx.doi.org/10.1038/jcbfm.2014.261] [PMID: 25649991]
[139]
Hagens, M.H.J.; Golla, S.V.; Wijburg, M.T.; Yaqub, M.; Heijtel, D.; Steenwijk, M.D.; Schober, P.; Brevé, J.J.P.; Schuit, R.C.; Reekie, T.A.; Kassiou, M.; van Dam, A.M.; Windhorst, A.D.; Killestein, J.; Barkhof, F.; van Berckel, B.N.M.; Lammertsma, A.A. In vivo assessment of neuroinflammation in progressive multiple sclerosis: a proof of concept study with [18F]DPA714 PET. J. Neuroinflammation, 2018, 15(1), 314-323.
[http://dx.doi.org/10.1186/s12974-018-1352-9] [PMID: 30424780]
[140]
Niu, N.; Xing, H.; Wang, X.; Ding, J.; Hao, Z.; Ren, C.; Ba, J.; Zheng, L.; Fu, C.; Zhao, H.; Huo, L. Comparative [18F]FDG and [18F]DPA714 PET imaging and time-dependent changes of brown adipose tissue in tumour-bearing mice. Adipocyte, 2020, 9(1), 542-549.
[http://dx.doi.org/10.1080/21623945.2020.1814546] [PMID: 32902340]
[141]
Lavisse, S.; García-Lorenzo, D.; Peyronneau, M.A.; Bodini, B.; Thiriez, C.; Kuhnast, B.; Comtat, C.; Remy, P.; Stankoff, B.; Bottlaender, M. Optimized quantification of translocator protein radioligand 11F-DPA-714 uptake in the brain of genotyped healthy volunteers. J. Nuclear Med., 2015, 56(7), 1048-1054.
[142]
Peyronneau, M.A.; Saba, W.; Goutal, S.; Damont, A.; Dollé, F.; Kassiou, M.; Bottlaender, M.; Valette, H. Metabolism and quantification of [11F]DPA-714, a new TSPO positron emission tomography radioligand. Drug Metab. Dispos., 2013, 41(1), 122-131.
[http://dx.doi.org/10.1124/dmd.112.046342] [PMID: 23065531]
[143]
Wang, L.; Cheng, R.; Fujinaga, M.; Yang, J.; Zhang, Y.; Hatori, A.; Kumata, K.; Yang, J.; Vasdev, N.; Du, Y.; Ran, C.; Zhang, M.R.; Liang, S.H. A facile radiolabeling of [18F]FDPA via spirocyclic iodonium ylides: Preliminary PET imaging studies in preclinical models of neuroinflammation. J. Med. Chem., 2017, 60(12), 5222-5227.
[http://dx.doi.org/10.1021/acs.jmedchem.7b00432] [PMID: 28530834]
[144]
Keller, T.; Krzyczmonik, A.; Forsback, S.; Picón, F.R.L.; Kirjavainen, A.K.; Takkinen, J.; Rajander, J.; Cacheux, F.; Damont, A.; Dollé, F.; Rinne, J.O.; Haaparanta-Solin, M.; Solin, O. Radiosynthesis and preclinical evaluation of [18F]F-DPA, a novel pyrazolo[1,5a]pyrimidine Acetamide TSPO radioligand, in healthy sprague dawley rats. Mol. Imaging Biol., 2017, 19(5), 736-745.
[http://dx.doi.org/10.1007/s11307-016-1040-z] [PMID: 28083825]
[145]
Keller, T.; López-Picón, F.R.; Krzyczmonik, A.; Forsback, S.; Kirjavainen, A.K.; Takkinen, J.S.; Alzghool, O.; Rajander, J.; Teperi, S.; Cacheux, F.; Damont, A.; Dollé, F.; Rinne, J.O.; Solin, O.; Haaparanta-Solin, M. [18F]F-DPA for the detection of activated microglia in a mouse model of Alzheimer’s disease. Nucl. Med. Biol., 2018, 67, 1-9.
[http://dx.doi.org/10.1016/j.nucmedbio.2018.09.001] [PMID: 30317069]
[146]
Keller, T.; López-Picón, F.R.; Krzyczmonik, A.; Forsback, S.; Takkinen, J.S.; Rajander, J.; Teperi, S.; Dollé, F.; Rinne, J.O.; Haaparanta-Solin, M.; Solin, O. Comparison of high and low molar activity TSPO tracer [18F]F-DPA in a mouse model of Alzheimer’s disease. J. Cereb. Blood Flow Metab., 2020, 40(5), 1012-1020.
[http://dx.doi.org/10.1177/0271678X19853117] [PMID: 31142224]
[147]
Tang, D.; McKinley, E.T.; Hight, M.R.; Uddin, M.I.; Harp, J.M.; Fu, A.; Nickels, M.L.; Buck, J.R.; Manning, H.C. Synthesis and structure-activity relationships of 5,6,7-substituted pyrazolopyrimidines: discovery of a novel TSPO PET ligand for cancer imaging. J. Med. Chem., 2013, 56(8), 3429-3433.
[http://dx.doi.org/10.1021/jm4001874] [PMID: 23521048]
[148]
Tang, D.; Nickels, M.L.; Tantawy, M.N.; Buck, J.R.; Manning, H.C. Preclinical imaging evaluation of novel TSPO-PET ligand 2-(5,7-Diethyl-2-(4-(2-[11F]fluoroethoxy) phenyl)pyrazolo[1,5-a]pyrimidin-3-yl)-N,N-diethylacetamide ([ 18F]VUIIS1008) in glioma. Mol. Imaging Biol., 2014, 16(6), 813-820.
[http://dx.doi.org/10.1007/s11307-014-0743-2] [PMID: 24845529]
[149]
Pulagam, K.R.; Colás, L.; Padro, D.; Plaza-García, S.; Gómez-Vallejo, V.; Higuchi, M.; Llop, J.; Martín, A. Evaluation of the novel TSPO radiotracer [18F] VUIIS1008 in a preclinical model of cerebral ischemia in rats. EJNMMI Res., 2017, 7(1), 93-105.
[http://dx.doi.org/10.1186/s13550-017-0343-7] [PMID: 29177913]
[150]
Tang, D.; Fujinaga, M.; Hatori, A.; Zhang, Y.; Yamasaki, T.; Xie, L.; Mori, W.; Kumata, K.; Liu, J.; Manning, H.C.; Huang, G.; Zhang, M.R. Evaluation of the novel TSPO radiotracer 2-(7-butyl-2-(4-(2-([18F]fluoroethoxy)phenyl)-5- methylpyrazolo[1,5-a]pyrimidin-3-yl)-N,N-diethylacetamide in a preclinical model of neuroinflammation. Eur. J. Med. Chem., 2018, 150, 1-8.
[http://dx.doi.org/10.1016/j.ejmech.2018.02.076] [PMID: 29505933]
[151]
Tang, D.; Li, J.; Nickels, M.L.; Huang, G.; Cohen, A.S.; Manning, H.C. Preclinical evaluation of a novel TSPO PET Ligand 2-(7-Butyl-2-(4-(2-[18F]Fluoroethoxy) phenyl)-5-methylpyrazolo[1,5-a]pyrimidin-3-yl)-N,N-diethylacetamide (18F-VUIIS1018A) to image glioma. Mol. Imaging Biol., 2019, 21(1), 113-121.
[http://dx.doi.org/10.1007/s11307-018-1198-7] [PMID: 29869061]
[152]
Kozikowski, A.P.; Ma, D.; Brewer, J.; Sun, S.; Costa, E.; Romeo, E.; Guidotti, A. Chemistry, binding affinities, and behavioral properties of a new class of “antineophobic” mitochondrial DBI receptor complex (mDRC) ligands. J. Med. Chem., 1993, 36(20), 2908-2920.
[http://dx.doi.org/10.1021/jm00072a010] [PMID: 8411007]
[153]
Primofiore, G.; Da Settimo, F.; Taliani, S.; Simorini, F.; Patrizi, M.P.; Novellino, E.; Greco, G.; Abignente, E.; Costa, B.; Chelli, B.; Martini, C. N,N-dialkyl-2-phenylindol-3-ylglyoxylamides. A new class of potent and selective ligands at the peripheral benzodiazepine receptor. J. Med. Chem., 2004, 47(7), 1852-1855.
[http://dx.doi.org/10.1021/jm030973k] [PMID: 15027878]
[154]
Da Settimo, F.; Simorini, F.; Taliani, S.; La Motta, C.; Marini, A.M.; Salerno, S.; Bellandi, M.; Novellino, E.; Greco, G.; Cosimelli, B.; Da Pozzo, E.; Costa, B.; Simola, N.; Morelli, M.; Martini, C. Anxiolytic-like effects of N,N-dialkyl-2-phenylindol-3-ylglyoxylamides by modulation of translocator protein promoting neurosteroid biosynthesis. J. Med. Chem., 2008, 51(18), 5798-5806.
[http://dx.doi.org/10.1021/jm8003224] [PMID: 18729350]
[155]
Pike, V.W.; Taliani, S.; Lohith, T.G.; Owen, D.R.; Pugliesi, I.; Da Pozzo, E.; Hong, J.; Zoghbi, S.S.; Gunn, R.N.; Parker, C.A.; Rabiner, E.A.; Fujita, M.; Innis, R.B.; Martini, C.; Da Settimo, F. Evaluation of novel N1-methyl-2-phenylindol-3-ylglyoxylamides as a new chemotype of 18 kDa translocator protein-selective ligand suitable for the development of positron emission tomography radioligands. J. Med. Chem., 2011, 54(1), 366-373.
[http://dx.doi.org/10.1021/jm101230g] [PMID: 21133364]
[156]
Ferzaz, B.; Brault, E.; Bourliaud, G.; Robert, J.P.; Poughon, G.; Claustre, Y.; Marguet, F.; Liere, P.; Schumacher, M.; Nowicki, J.P.; Fournier, J.; Marabout, B.; Sevrin, M.; George, P.; Soubrie, P.; Benavides, J.; Scatton, B. SSR180575 (7-chloro-N,N,5-trimethyl-4-oxo-3-phenyl- 3,5-dihydro-4H-pyridazino[4,5-b]indole-1-acetamide), a peripheral benzodiazepine receptor ligand, promotes neuronal survival and repair. J. Pharmacol. Exp. Ther., 2002, 301(3), 1067-1078.
[http://dx.doi.org/10.1124/jpet.301.3.1067] [PMID: 12023539]
[157]
Thominiaux, C.; Damont, A.; Kuhnast, B.; Demphel, S.; Le Helleix, S.; Boisnard, S.; Rivron, L.; Chauveau, F.; Boutin, H.; Van Camp, N.; Boisgard, R.; Roy, S.; Allen, J.; Rooney, T.; Benavides, J.; Hantraye, P.; Tavitian, B.; Dollé, F. Radiosynthesis of 7-chloro-N,N-dimethyl-5-[11C] methyl-4-oxo-3-phenyl-3,5-dihydro-4H-pyridazino[4, 5-b]indole-1-acetamide, [11C]SSR180575, a novel radioligand for imaging the TSPO (peripheral benzodiazepine receptor) with PET. J. Labelled Comp. Radiopharm., 2010, 53(13), 767-773.
[http://dx.doi.org/10.1002/jlcr.1794]
[158]
Chauveau, F.; Boutin, H.; Van Camp, N.; Thominiaux, C.; Hantraye, P.; Rivron, L.; Marguet, F.; Castel, M.N.; Rooney, T.; Benavides, J.; Dollé, F.; Tavitian, B. In vivo imaging of neuroinflammation in the rodent brain with [11C]SSR180575, a novel indoleacetamide radioligand of the translocator protein (18 kDa). Eur. J. Nucl. Med. Mol. Imaging, 2011, 38(3), 509-514.
[http://dx.doi.org/10.1007/s00259-010-1628-5] [PMID: 20936410]
[159]
Cheung, Y.Y.; Nickels, M.L.; Tang, D.; Buck, J.R.; Manning, H.C. Facile synthesis of SSR180575 and discovery of 7-chloro-N,N,5-trimethyl-4-oxo-3(6-[11F]fluoropyridin-2- yl)-3,5-dihydro-4H-pyridazino[4,5-b]indole-1-acetamide, a potent pyridazinoindole ligand for PET imaging of TSPO in cancer. Bioorg. Med. Chem. Lett., 2014, 24(18), 4466-4471.
[http://dx.doi.org/10.1016/j.bmcl.2014.07.091] [PMID: 25172419]
[160]
Okubo, T.; Yoshikawa, R.; Chaki, S.; Okuyama, S.; Nakazato, A. Design, synthesis, and structure-activity relationships of novel tetracyclic compounds as peripheral benzodiazepine receptor ligands. Bioorg. Med. Chem., 2004, 12(13), 3569-3580.
[http://dx.doi.org/10.1016/j.bmc.2004.04.025] [PMID: 15186841]
[161]
Wadsworth, H.; Jones, P.A.; Chau, W.F.; Durrant, C.; Fouladi, N.; Passmore, J.; O’Shea, D.; Wynn, D.; Morisson-Iveson, V.; Ewan, A.; Thaning, M.; Mantzilas, D.; Gausemel, I.; Khan, I.; Black, A.; Avory, M.; Trigg, W. [¹⁸F]GE-180: a novel fluorine-18 labelled PET tracer for imaging Translocator protein 18 kDa (TSPO). Bioorg. Med. Chem. Lett., 2012, 22(3), 1308-1313.
[http://dx.doi.org/10.1016/j.bmcl.2011.12.084] [PMID: 22244939]
[162]
Chau, W.F.; Black, A.M.; Clarke, A.; Durrant, C.; Gausemel, I.; Khan, I.; Mantzilas, D.; Oulie, I.; Rogstad, A.; Trigg, W.; Jones, P.A. Exploration of the impact of stereochemistry on the identification of the novel translocator protein PET imaging agent [11F]GE-180. Nucl. Med. Biol., 2015, 42(9), 711-719.
[http://dx.doi.org/10.1016/j.nucmedbio.2015.05.004] [PMID: 26072270]
[163]
Dickens, A.M.; Vainio, S.; Marjamäki, P.; Johansson, J.; Lehtiniemi, P.; Rokka, J.; Rinne, J.; Solin, O.; Haaparanta-Solin, M.; Jones, P.A.; Trigg, W.; Anthony, D.C.; Airas, L. Detection of microglial activation in an acute model of neuroinflammation using PET and radiotracers 11C-(R)-PK11195 and 18F-GE-180. J. Nuclear Med., 2014, 55(3), 466-472.
[164]
Boutin, H.; Murray, K.; Pradillo, J.; Maroy, R.; Smigova, A.; Gerhard, A.; Jones, P.A.; Trigg, W. 18F-GE-180: A novel TSPO radiotracer compared to 11C-R-PK11195 in a preclinical model of stroke. Eur. J. Nucl. Med. Mol. Imaging, 2015, 42(3), 503-511.
[http://dx.doi.org/10.1007/s00259-014-2939-8] [PMID: 25351507]
[165]
Liu, B.; Le, K.X.; Park, M.A.; Wang, S.; Belanger, A.P.; Dubey, S.; Frost, J.L.; Holton, P.; Reiser, V.; Jones, P.A.; Trigg, W.; Di Carli, M.F.; Lemere, C.A. In vivo detection of age- and disease-related increases in neuroinflammation by 18F-GE180 TSPO MicroPET imaging in wild-type and Alzheimer’s transgenic mice. J. Neurosci., 2015, 35(47), 15716-15730.
[http://dx.doi.org/10.1523/JNEUROSCI.0996-15.2015] [PMID: 26609163]
[166]
Feeney, C.; Scott, G.; Raffel, J.; Roberts, S.; Coello, C.; Jolly, A.; Searle, G.; Goldstone, A.P.; Brooks, D.J.; Nicholas, R.S.; Trigg, W.; Gunn, R.N.; Sharp, D.J. Kinetic analysis of the translocator protein positron emission tomography ligand [18F]GE-180 in the human brain. Eur. J. Nucl. Med. Mol. Imaging, 2016, 43(12), 2201-2210.
[http://dx.doi.org/10.1007/s00259-016-3444-z] [PMID: 27349244]
[167]
Fan, Z.; Calsolaro, V.; Atkinson, R.A.; Femminella, G.D.; Waldman, A.; Buckley, C.; Trigg, W.; Brooks, D.J.; Hinz, R.; Edison, P. Flutriciclamide (18F-GE180) PET: First-in-Human PET study of novel third-generation in vivo marker of human translocator protein. J. Nuclear Med., 2016, 57(11), 1753-1759.
[168]
Unterrainer, M.; Mahler, C.; Vomacka, L.; Lindner, S.; Havla, J.; Brendel, M.; Böning, G.; Ertl-Wagner, B.; Kümpfel, T.; Milenkovic, V.M.; Rupprecht, R.; Kerschensteiner, M.; Bartenstein, P.; Albert, N.L. TSPO PET with [18F]GE-180 sensitively detects focal neuroinflammation in patients with relapsing-remitting multiple sclerosis. Eur. J. Nucl. Med. Mol. Imaging, 2018, 45(8), 1423-1431.
[http://dx.doi.org/10.1007/s00259-018-3974-7] [PMID: 29523925]
[169]
Albert, N.L.; Unterrainer, M.; Fleischmann, D.F.; Lindner, S.; Vettermann, F.; Brunegraf, A.; Vomacka, L.; Brendel, M.; Wenter, V.; Wetzel, C.; Rupprecht, R.; Tonn, J.C.; Belka, C.; Bartenstein, P.; Niyazi, M. TSPO PET for glioma imaging using the novel ligand 18F-GE-180: first results in patients with glioblastoma. Eur. J. Nucl. Med. Mol. Imaging, 2017, 44(13), 2230-2238.
[http://dx.doi.org/10.1007/s00259-017-3799-9] [PMID: 28821920]
[170]
Unterrainer, M.; Fleischmann, D.F.; Diekmann, C.; Vomacka, L.; Lindner, S.; Vettermann, F.; Brendel, M.; Wenter, V.; Ertl-Wagner, B.; Herms, J.; Wetzel, C.; Rupprecht, R.; Tonn, J.C.; Belka, C.; Bartenstein, P.; Niyazi, M.; Albert, N.L. Comparison of 18F-GE-180 and dynamic 18F-FET PET in high grade glioma: A double-tracer pilot study. Eur. J. Nucl. Med. Mol. Imaging, 2019, 46(3), 580-590.
[http://dx.doi.org/10.1007/s00259-018-4166-1] [PMID: 30244386]
[171]
Unterrainer, M.; Fleischmann, D.F.; Lindner, S.; Brendel, M.; Rupprecht, R.; Tonn, J.C.; Belka, C.; Bartenstein, P.; Niyazi, M.; Albert, N.L. Detection of cerebrospinal fluid dissemination of recurrent glioblastoma using TSPO-PET With 18F-GE-180. Clin. Nucl. Med., 2018, 43(7), 518-519.
[http://dx.doi.org/10.1097/RLU.0000000000002113] [PMID: 29742608]
[172]
Unterrainer, M.; Fleischmann, D.F.; Vettermann, F.; Ruf, V.; Kaiser, L.; Nelwan, D.; Lindner, S.; Brendel, M.; Wenter, V.; Stöcklein, S.; Herms, J.; Milenkovic, V.M.; Rupprecht, R.; Tonn, J.C.; Belka, C.; Bartenstein, P.; Niyazi, M.; Albert, N.L. TSPO PET, tumour grading and molecular genetics in histologically verified glioma: a correlative 18F-GE-180 PET study. Eur. J. Nucl. Med. Mol. Imaging, 2020, 47(6), 1368-1380.
[http://dx.doi.org/10.1007/s00259-019-04491-5] [PMID: 31486876]
[173]
Roncaroli, F.; Su, Z.; Herholz, K.; Gerhard, A.; Turkheimer, F.E. TSPO expression in brain tumours: Is TSPO a target for brain tumour imaging? Clin. Transl. Imaging, 2016, 4, 145-156.
[http://dx.doi.org/10.1007/s40336-016-0168-9] [PMID: 27077069]
[174]
Zanotti-Fregonara, P.; Pascual, B.; Rizzo, G.; Yu, M.; Pal, N.; Beers, D.; Carter, R.; Appel, S.H.; Atassi, N.; Masdeu, J.C. Head-to-Head Comparison of 11C-PBR28 and 18F-GE180 for quantification of the translocator protein in the human brain. J. Nuclear Med., 2018, 59(8), 1260-1266.
[175]
Zanotti-Fregonara, P.; Pascual, B.; Rostomily, R.C.; Rizzo, G.; Veronese, M.; Masdeu, J.C.; Turkheimer, F. Anatomy of 18F-GE180, a failed radioligand for the TSPO protein. Eur. J. Nucl. Med. Mol. Imaging, 2020, 47(10), 2233-2236.
[http://dx.doi.org/10.1007/s00259-020-04732-y] [PMID: 32088848]
[176]
Qiao, L.; Fisher, E.; McMurray, L.; Milicevic Sephton, S.; Hird, M.; Kuzhuppilly-Ramakrishnan, N.; Williamson, D.J.; Zhou, X.; Werry, E.; Kassiou, M.; Luthra, S.; Trigg, W.; Aigbirhio, F.I. Radiosynthesis of (R,S)-[18 F]GE387: A Potential PET Radiotracer for Imaging Translocator Protein 18 kDa (TSPO) with low binding sensitivity to the human gene polymorphism rs6971. ChemMedChem, 2019, 14(9), 982-993.
[http://dx.doi.org/10.1002/cmdc.201900023] [PMID: 30900397]
[177]
Zhang, M.R.; Kumata, K.; Maeda, J.; Yanamoto, K.; Hatori, A.; Okada, M.; Higuchi, M.; Obayashi, S.; Suhara, T.; Suzuki, K. 11C-AC-5216: A novel PET ligand for peripheral benzodiazepine receptors in the primate brain. J. Nuclear Med., 2007, 48(11), 1853-1861.
[178]
Maeda, J.; Zhang, M.R.; Okauchi, T.; Ji, B.; Ono, M.; Hattori, S.; Kumata, K.; Iwata, N.; Saido, T.C.; Trojanowski, J.Q.; Lee, V.M.; Staufenbiel, M.; Tomiyama, T.; Mori, H.; Fukumura, T.; Suhara, T.; Higuchi, M. In vivo positron emission tomographic imaging of glial responses to amyloid-beta and tau pathologies in mouse models of Alzheimer’s disease and related disorders. J. Neurosci., 2011, 31(12), 4720-4730.
[http://dx.doi.org/10.1523/JNEUROSCI.3076-10.2011] [PMID: 21430171]
[179]
Rupprecht, R.; Papadopoulos, V.; Rammes, G.; Baghai, T.C.; Fan, J.; Akula, N.; Groyer, G.; Adams, D.; Schumacher, M. Translocator protein (18 kDa) (TSPO) as a therapeutic target for neurological and psychiatric disorders. Nat. Rev. Drug Discov., 2010, 9(12), 971-988.
[http://dx.doi.org/10.1038/nrd3295] [PMID: 21119734]
[180]
Gong, J.; Szego, É.M.; Leonov, A.; Benito, E.; Becker, S.; Fischer, A.; Zweckstetter, M.; Outeiro, T.; Schneider, A. Translocator protein ligand protects against neurodegeneration in the MPTP mouse model of parkinsonism. J. Neurosci., 2019, 39(19), 3752-3769.
[http://dx.doi.org/10.1523/JNEUROSCI.2070-18.2019] [PMID: 30796158]
[181]
Owen, D.R.; Lewis, A.J.; Reynolds, R.; Rupprecht, R.; Eser, D.; Wilkins, M.R.; Bennacef, I.; Nutt, D.J.; Parker, C.A. Variation in binding affinity of the novel anxiolytic XBD173 for the 18 kDa translocator protein in human brain. Synapse, 2011, 65(3), 257-259.
[http://dx.doi.org/10.1002/syn.20884] [PMID: 21132812]
[182]
Yanamoto, K.; Yamasaki, T.; Kumata, K.; Yui, J.; Odawara, C.; Kawamura, K.; Hatori, A.; Inoue, O.; Yamaguchi, M.; Suzuki, K.; Zhang, M.R. Evaluation of N-benzyl-N-[11C]methyl-2- (7-methyl-8-oxo-2-phenyl-7,8-dihydro-9H-purin-9-yl)acetamide ([11C]DAC) as a novel translocator protein (18 kDa) radioligand in kainic acid-lesioned rat. Synapse, 2009, 63(11), 961-971.
[http://dx.doi.org/10.1002/syn.20678] [PMID: 19593823]
[183]
Yui, J.; Hatori, A.; Kawamura, K.; Yanamoto, K.; Yamasaki, T.; Ogawa, M.; Yoshida, Y.; Kumata, K.; Fujinaga, M.; Nengaki, N.; Fukumura, T.; Suzuki, K.; Zhang, M.R. Visualization of early infarction in rat brain after ischemia using a translocator protein (18 kDa) PET ligand [11C]DAC with ultra-high specific activity. Neuroimage, 2011, 54(1), 123-130.
[http://dx.doi.org/10.1016/j.neuroimage.2010.08.010] [PMID: 20705143]
[184]
Yanamoto, K.; Kumata, K.; Yamasaki, T.; Odawara, C.; Kawamura, K.; Yui, J.; Hatori, A.; Suzuki, K.; Zhang, M.R. [18F]FEAC and [18F]FEDAC: Two novel positron emission tomography ligands for peripheral-type benzodiazepine receptor in the brain. Bioorg. Med. Chem. Lett., 2009, 19(6), 1707-1710.
[http://dx.doi.org/10.1016/j.bmcl.2009.01.093] [PMID: 19217778]
[185]
Yui, J.; Maeda, J.; Kumata, K.; Kawamura, K.; Yanamoto, K.; Hatori, A.; Yamasaki, T.; Nengaki, N.; Higuchi, M.; Zhang, M.R. 18F-FEAC and 18F-FEDAC: PET of the monkey brain and imaging of translocator protein (18 kDa) in the infarcted rat brain. J. Nuclear Med., 2010, 51(8), 1301-1309.
[186]
Chung, S.J.; Yoon, H.J.; Youn, H.; Kim, M.J.; Lee, Y.S.; Jeong, J.M.; Chung, J.K.; Kang, K.W.; Xie, L.; Zhang, M.R.; Cheon, G.J. 18F-FEDAC as a targeting agent for activated macrophages in DBA/1 mice with collagen-induced arthritis: Comparison with 18F-FDG. J. Nuclear Med., 2018, 59(5), 839-845.
[187]
Tiwari, A.K.; Yui, J.; Fujinaga, M.; Kumata, K.; Shimoda, Y.; Yamasaki, T.; Xie, L.; Hatori, A.; Maeda, J.; Nengaki, N.; Zhang, M.R. Characterization of a novel acetamidobenzoxazolone-based PET ligand for translocator protein (18 kDa) imaging of neuroinflammation in the brain. J. Neurochem., 2014, 129(4), 712-720.
[http://dx.doi.org/10.1111/jnc.12670] [PMID: 24484439]
[188]
Tiwari, A.K.; Fujinaga, M.; Yui, J.; Yamasaki, T.; Xie, L.; Kumata, K.; Mishra, A.K.; Shimoda, Y.; Hatori, A.; Ji, B.; Ogawa, M.; Kawamura, K.; Wang, F.; Zhang, M.R. Synthesis and evaluation of new 18F-labelled acetamidobenzoxazolone-based radioligands for imaging of the translocator protein (18 kDa, TSPO) in the brain. Org. Biomol. Chem., 2014, 12(47), 9621-9630.
[http://dx.doi.org/10.1039/C4OB01933D] [PMID: 25339090]
[189]
Tiwari, A.K.; Ji, B.; Yui, J.; Fujinaga, M.; Yamasaki, T.; Xie, L.; Luo, R.; Shimoda, Y.; Kumata, K.; Zhang, Y.; Hatori, A.; Maeda, J.; Higuchi, M.; Wang, F.; Zhang, M.R. [18F]FEBMP: Positron Emission Tomography Imaging of TSPO in a model of neuroinflammation in rats, and in vitro autoradiograms of the human brain. Theranostics, 2015, 5(9), 961-969.
[http://dx.doi.org/10.7150/thno.12027] [PMID: 26155312]
[190]
Fujinaga, M.; Luo, R.; Kumata, K.; Zhang, Y.; Hatori, A.; Yamasaki, T.; Xie, L.; Mori, W.; Kurihara, Y.; Ogawa, M.; Nengaki, N.; Wang, F.; Zhang, M.R. Development of a 18F-Labeled radiotracer with improved brain kinetics for positron emission tomography imaging of translocator protein (18 kDa) in ischemic brain and glioma. J. Med. Chem., 2017, 60(9), 4047-4061.
[http://dx.doi.org/10.1021/acs.jmedchem.7b00374] [PMID: 28422499]

Rights & Permissions Print Cite
Article Metrics
51
1
Wayfinder Image
Open Access Journals Promotions
World Antimicrobial Awareness Week
© 2024 Bentham Science Publishers | Privacy Policy