In Vivo Detection of Age- and Disease-Related Increases in Neuroinflammation by18F-GE180 TSPO MicroPET Imaging in Wild-Type and Alzheimer's Transgenic Mice

Liu, Bin; Le, Kevin X.; Park, Mi-Ae; Wang, Shuyan; Belanger, Anthony P.; Dubey, Shipra; Frost, Jeffrey L.; Holton, Peter; Reiser, Vladimir; Jones, Paul A.; Trigg, William; Di Carli, Marcelo F.; Lemere, Cynthia. A.

doi:10.1523/jneurosci.0996-15.2015

Cited by 114Neuroinflammation and Neurodegeneration MechanismsAlzheimer's disease research and treatmentsMedical Imaging Techniques and Applications

In Vivo Detection of Age- and Disease-Related Increases in Neuroinflammation by18F-GE180 TSPO MicroPET Imaging in Wild-Type and Alzheimer's Transgenic Mice

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Liu, Bin, Le, Kevin X., Park, Mi-Ae, Wang, Shuyan, Belanger, Anthony P., Dubey, Shipra, Frost, Jeffrey L., Holton, Peter +5 more·2015·The Journal of Neuroscience

DOI 10.1523/jneurosci.0996-15.2015PMC PMC6705465

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Abstract

Alzheimer's disease (AD) is the most common cause of dementia. Neuroinflammation appears to play an important role in AD pathogenesis. Ligands of the 18 kDa translocator protein (TSPO), a marker for activated microglia, have been used as positron emission tomography (PET) tracers to reflect neuroinflammation in humans and mouse models. Here, we used the novel TSPO-targeted PET tracer 18 F-GE180 (flutriciclamide) to investigate differences in neuroinflammation between young and old WT and APP/PS1dE9 transgenic (Tg) mice.In vivo PET scans revealed an overt age-dependent elevation in whole-brain uptake of 18 F-GE180 in both WT and Tg mice, and a significant increase in whole-brain uptake of 18 F-GE180 (peak-uptake and retention) in old Tg mice compared with young Tg mice and all WT mice. Similarly, the 18 F-GE180 binding potential in hippocampus was highest to lowest in old Tg > old WT > young Tg > young WT mice using MRI coregistration.Ex vivo PET and autoradiography analysis further confirmed our in vivo PET results: enhanced uptake and specific binding (SUV 75%) of 18 F-GE180 in hippocampus and cortex was highest in old Tg mice followed by old WT, young Tg, and finally young WT mice.18 F-GE180 specificity was confirmed by an in vivo cold tracer competition study. We also examined 18 F-GE180 metabolites in 4-month-old WT mice and found that, although total radioactivity declined over 2 h, of the remaining radioactivity, ∼90% was due to parent 18 F-GE180. In conclusion,18 F-GE180 PET scans may be useful for longitudinal monitoring of neuroinflammation during AD progression and treatment. SIGNIFICANCE STATEMENT Microglial activation, a player in Alzheimer's disease (AD) pathogenesis, is thought to reflect neuroinflammation. Using in vivo microPET imaging with a novel TSPO radioligand,18 F-GE180, we detected significantly enhanced neuroinflammation during normal aging in WT mice and in response to AD-associated pathology in APP/PS1dE9 Tg mice, an AD mouse model. Increased uptake and specific binding of 18 F-GE180 in whole brain and hippocampus were confirmed by ex vivo PET and autoradiography. The binding specificity and stability of 18 F-GE180 was further confirmed by a cold tracer competition study and a metabolite study, respectively. Therefore,18 F-GE180 PET imaging may be useful for longitudinal monitoring of neuroinflammation during AD progression and treatment and may also be useful for other neurodegenerative diseases.

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In models of Alzheimer's-like neurodegeneration, TSPO positive microglia, astrocytes and endothelium are all increased.
“Similarly, others have found that TSPO positive microglia, astrocytes and endothelium are all increased in models of Alzheimer’s-like neurodegeneration [48–51] and in postmortem human Alzheimer’s disease brains [27].”
From Pharmacological modulation of TSPO in microglia/macrophages and neurons in a chronic neurodegenerative model of prion disease (2023) · cites this paper as [49]
The colocalization results (page not available) show TSPO-positive microglia associated with amyloid plaques in APP/PS1dE9 mice. They report only rare overlap between TSPO and the astrocyte marker GFAP, and the passages examined do not establish an increase in TSPO-positive endothelium. The source therefore does not support the claim that all three cell types are increased. (LLM, conf=0.88)
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Wickstrøm, T., Clarke, A., Gausemel, I., Horn, E., Jørgensen, K., Khan, I. A., Mantzilas, D., Rajanayagam, T., Veld, D. J. I., & Trigg, W. (2013) · Journal of Labelled Compounds and Radiopharmaceuticals · doi:10.1002/jlcr.3112 · Cited by 59 · see citing works
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Imaging microglial activation and glucose consumption in a mouse model of Alzheimer's disease
Rapic, S., Backes, H., Viel, T., Kummer, M. P., Monfared, P., Neumaier, B., Vollmar, S., Hoehn, M., der Linden, A. V., Heneka, M. T., et al. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.04.016 · Cited by 52 · see citing works
PET Imaging of Translocator Protein (18 kDa) in a Mouse Model of Alzheimer's Disease UsingN-(2,5-Dimethoxybenzyl)-2-18F-Fluoro-N-(2-Phenoxyphenyl)Acetamide
James, M. L., Belichenko, N. P., Nguyen, T. V., Andrews, L., Ding, Z., Liu, H., Bodapati, D., Arksey, N., Shen, B., Cheng, Z., et al. (2015) · Journal of Nuclear Medicine · doi:10.2967/jnumed.114.141648 · Cited by 52 · see citing works
PET Imaging of Stroke-Induced Neuroinflammation in Mice Using [18F]PBR06
Lartey, F. M., Ahn, G., Shen, B., Cord, K.-T., Smith, T. N., Chua, J. Y., Rosenblum, S., Liu, H., James, M. L., Chernikova, S. B., et al. (2013) · Molecular Imaging and Biology · doi:10.1007/s11307-013-0664-5 · Cited by 51 · see citing works
Biodistribution and Radiation Dosimetry in Humans of a New PET Ligand, 18F-PBR06, to Image Translocator Protein (18 kDa)
Fujimura, Y., Kimura, Y., Siméon, F. G., Dickstein, L. P., Pike, V. W., Innis, R. B., & Fujita, M. (2009) · Journal of Nuclear Medicine · doi:10.2967/jnumed.109.068064 · Cited by 47 · see citing works
Human biodistribution and radiation dosimetry of 11C-(R)-PK11195, the prototypic PET ligand to image inflammation
Hirvonen, J., Roivainen, A., Virta, J. R., Helin, S., Någren, K., & Rinne, J. O. (2009) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-009-1298-3 · Cited by 46 · see citing works
Central Nervous System Expression and PET Imaging of the Translocator Protein in Relapsing–Remitting Experimental Autoimmune Encephalomyelitis
Mattner, F., Staykova, M. A., Berghofer, P., Wong, H. J., Fordham, S. A., Callaghan, P. D., Jackson, T. W., Pham, T. Q., Grégoire, M., Zahra, D., et al. (2013) · Journal of Nuclear Medicine · doi:10.2967/jnumed.112.108894 · Cited by 39 · see citing works
Inflammation in the Alzheimer's disease cascade: culprit or innocent bystander?
Tan, Z. S., & Seshadri, S. (2010) · Alzheimer's Research & Therapy · doi:10.1186/alzrt29 · Cited by 39 · see citing works
Molecular cloning, chromosomal localization of human peripheral‐type benzodiazepine receptor‐ and protein kinase A regulatory subunit type 1A (PRKAR1A)‐associated protein PAP7 and studies in PRKAR1A mutant cells and tissues
Liu, J., Matyakhina, L., Han, Z. J., Sandrini, F., Bei, T. A., Stratakis, C. A., & Papadopoulos, V. (2003) · The FASEB Journal · doi:10.1096/fj.02-1066fje · Cited by 36 · see citing works
Radiation Dosimetry and Biodistribution of the TSPO Ligand11C-DPA-713 in Humans
Endres, C. J., Coughlin, J. M., Gage, K. L., Watkins, C. C., Kassiou, M., & Pomper, M. G. (2012) · Journal of Nuclear Medicine · doi:10.2967/jnumed.111.094565 · Cited by 31 · see citing works
Radiosynthesis and in vivo evaluation of N-[11C]methylated imidazopyridineacetamides as PET tracers for peripheral benzodiazepine receptors
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Postnatal development of peripheral-type benzodiazepine receptors in rat brain and peripheral tissues
Kurumaji, A., & Toru, M. (1996) · Developmental Brain Research · doi:10.1016/s0165-3806(96)00150-2 · Cited by 10 · see citing works

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sTREM2 cerebrospinal fluid levels are a potential biomarker for microglia activity in early‐stage Alzheimer's disease and associate with neuronal injury markers
Suárez‐Calvet, M., Kleinberger, G., Araque Caballero, M. Á., Brendel, M., Rominger, A., Alcolea, D., Fortea, J., Lleó, A., Blesa, R., Gispert, J. D., et al. (2016) · EMBO Molecular Medicine · doi:10.15252/emmm.201506123 · Cited by 522 · see citing works
NLRP3 inflammasome in neurological diseases, from functions to therapies
Song, L., Pei, L., Yao, S., Wu, Y., & Shang, Y. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00063 · Cited by 467 · see citing works
Radiopharmaceuticals for PET and SPECT Imaging: A Literature Review over the Last Decade
Crișan, G., Moldovean-Cioroianu, N. S., Timaru, D.-G., Andrieș, G., Căinap, C., & Chiș, V. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23095023 · Cited by 283 · see citing works
Myocardial Inflammation Predicts Remodeling and Neuroinflammation After Myocardial Infarction
Thackeray, J. T., Hupe, H. C., Wang, Y., Bankstahl, J. P., Berding, G., Roß, T. L., Bauersachs, J. K., Wollert, K. C., & Bengel, F. M. (2018) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2017.11.024 · Cited by 302 · see citing works
Recent Developments in TSPO PET Imaging as A Biomarker of Neuroinflammation in Neurodegenerative Disorders
Werry, E. L., Bright, F., Piguet, O., Ittner, L. M., Halliday, G. M., Hodges, J. R., Kiernan, M. C., Loy, C. T., Kril, J. J., & Kassiou, M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20133161 · Cited by 282 · see citing works
Early changes in CSF sTREM2 in dominantly inherited Alzheimer’s disease occur after amyloid deposition and neuronal injury
Suárez-Calvet, M., Araque Caballero, M. Á., Kleinberger, G., Bateman, R. J., Fagan, A. M., Morris, J. C., Levin, J., Danek, A., Ewers, M., Haass, C., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aag1767 · Cited by 272 · see citing works
The FTD‐like syndrome causing TREM2 T66M mutation impairs microglia function, brain perfusion, and glucose metabolism
Kleinberger, G., Brendel, M., Mracsko, E. Z., Wefers, B., Groeneweg, L., Xiang, X., Focke, C., Deußing, M., Suárez‐Calvet, M., Mazaheri, F., et al. (2017) · The EMBO Journal · doi:10.15252/embj.201796516 · Cited by 244 · see citing works
Cellular sources of TSPO expression in healthy and diseased brain
Nutma, E., Ceyzériat, K., Amor, S., Tsartsalis, S., Millet, P., Owen, D. R., Papadopoulos, V., & Tournier, B. B. (2021) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-020-05166-2 · Cited by 192 · see citing works
Recent developments on PET radiotracers for TSPO and their applications in neuroimaging
Zhang, L., Hu, K., Shao, T., Hou, L., Zhang, S., Ye, W., Josephson, L., Meyer, J. H., Zhang, M., Vasdev, N., et al. (2020) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2020.08.006 · Cited by 187 · see citing works
TSPO in diverse CNS pathologies and psychiatric disease: a critical review and a way forward
Guilarte, T. R. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.09.003 · Cited by 173 · see citing works
PET Imaging of Neuroinflammation in Alzheimer’s Disease
Zhou, R., Ji, B., Kong, Y., Qin, L., Ren, W., Guan, Y., & Ni, R. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.739130 · Cited by 150 · see citing works
Glial Activation and Glucose Metabolism in a Transgenic Amyloid Mouse Model: A Triple-Tracer PET Study
Brendel, M., Probst, F., Jaworska, A. M., Overhoff, F., Korzhova, V., Albert, N. L., Beck, R., Lindner, S., Gildehaus, F., Baumann, K., et al. (2016) · Journal of Nuclear Medicine · doi:10.2967/jnumed.115.167858 · Cited by 145 · see citing works
A quantitative neuropathological assessment of translocator protein expression in multiple sclerosis
Nutma, E., Stephenson, J. A., Gorter, R. P., de Bruin, J., Boucherie, D. M., Donat, C. K., Breur, M., van der Valk, P., Matthews, P. M., Owen, D. R., et al. (2019) · Brain · doi:10.1093/brain/awz287 · Cited by 138 · see citing works
“…et al. , 2016; Israel et al. , 2016; Nguyen et al. , 2018), only a few have examined astrocytic expression of TSPO in the human CNS (Kaunzner et al. , 2019), and these descriptions have been qualitative rather than quantitative (Cosenza-Nashat et al. , 2009; Maeda et al. , 2011; Liu et al. , 2015).”
Microglia-Mediated Neuroprotection, TREM2, and Alzheimer’s Disease: Evidence From Optical Imaging
Condello, C., Yuan, P., & Grutzendler, J. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.007 · Cited by 131 · see citing works
Opposite microglial activation stages upon loss of PGRN or TREM2 result in reduced cerebral glucose metabolism
Götzl, J. K., Brendel, M., Werner, G., Parhizkar, S., Monasor, L. S., Kleinberger, G., Colombo, A.-V., Deußing, M., Wagner, M., Winkelmann, J., et al. (2019) · EMBO Molecular Medicine · doi:10.15252/emmm.201809711 · Cited by 124 · see citing works
Characterization of the 18 kDa translocator protein (TSPO) expression in post‐mortem normal and Alzheimer's disease brains
Gui, Y., Marks, J. D., Das, S., Hyman, B. T., & Serrano‐Pozo, A. (2020) · Brain Pathology · doi:10.1111/bpa.12763 · Cited by 126 · see citing works
In vivo molecular imaging of neuroinflammation in Alzheimer's disease
Chaney, A. M., Williams, S. R., & Boutin, H. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14615 · Cited by 116 · see citing works
VDAC1 and the TSPO: Expression, Interactions, and Associated Functions in Health and Disease States
Shoshan‐Barmatz, V., Pittala, S., & Mizrachi, D. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20133348 · Cited by 106 · see citing works
Environmental Enrichment Improves Cognitive Deficits, AD Hallmarks and Epigenetic Alterations Presented in 5xFAD Mouse Model
Griñán-Ferré, C., Izquierdo, V., Otero, E., Puigoriol-Illamola, D., Corpas, R., Sanfeliu, C., Ortuño-Sahagún, D., & Pallàs, M. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00224 · Cited by 94 · see citing works
Loss of TREM2 rescues hyperactivation of microglia, but not lysosomal deficits and neurotoxicity in models of progranulin deficiency
Reifschneider, A., Robinson, S., van Lengerich, B., Gnörich, J., Logan, T., Heindl, S., Vogt, M. A., Weidinger, E., Riedl, L., Wind, K., et al. (2022) · The EMBO Journal · doi:10.15252/embj.2021109108 · Cited by 89 · see citing works
In vivo Imaging of Glial Activation in Alzheimer's Disease
Edison, P., Donat, C. K., & Sastre, M. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00625 · Cited by 86 · see citing works
In vivo imaging of microglial activation by positron emission tomography with <scp>[11C]PBR28</scp> in the <scp>5XFAD</scp> model of <scp>A</scp>lzheimer's disease
Mirzaei, N., Tang, S. P., Ashworth, S., Coello, C., Plisson, C., Passchier, J., Selvaraj, V., Tyacke, R. J., Nutt, D. J., & Sastre, M. (2016) · Glia · doi:10.1002/glia.22978 · Cited by 82 · see citing works
In Vivo TSPO Signal and Neuroinflammation in Alzheimer’s Disease
Tournier, B. B., Tsartsalis, S., Ceyzériat, K., Garibotto, V., & Millet, P. (2020) · Cells · doi:10.3390/cells9091941 · Cited by 79 · see citing works
Comparative Evaluation of Three TSPO PET Radiotracers in a LPS-Induced Model of Mild Neuroinflammation in Rats
Sridharan, S., Lepelletier, F.-X., Trigg, W., Banister, S. D., Reekie, T. A., Kassiou, M., Gerhard, A., Hinz, R., & Boutin, H. (2016) · Molecular Imaging and Biology · doi:10.1007/s11307-016-0984-3 · Cited by 78 · see citing works
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Circular RNA NF1-419 enhances autophagy to ameliorate senile dementia by binding Dynamin-1 and Adaptor protein 2 B1 in AD-like mice
Diling, C., Guo, Y., Qi, L., Xiaocui, T., Liu, Y., Xin, Y., Guoyan, H., Shuai, O., Yong, T., Wang, D., et al. (2019) · Aging · doi:10.18632/aging.102529 · Cited by 78 · see citing works
Retracted
Impact of 40 Hz Transcranial Alternating Current Stimulation on Cerebral Tau Burden in Patients with Alzheimer’s Disease: A Case Series
Dhaynaut, M., Sprugnoli, G., Cappon, D., Macone, J., Sanchez, J. S., Normandin, M. D., Guehl, N. J., Koch, G., Paciorek, R., Connor, A., et al. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-215072 · Cited by 79 · see citing works
Effects of intermittent fasting on cognitive health and Alzheimer’s disease
Elias, A., Padinjakara, N., & Lautenschlager, N. T. (2023) · Nutrition Reviews · doi:10.1093/nutrit/nuad021 · Cited by 81 · see citing works
Space-like 56Fe irradiation manifests mild, early sex-specific behavioral and neuropathological changes in wildtype and Alzheimer’s-like transgenic mice
Liu, B., Hinshaw, R. G., Le, K. X., Park, M.-A., Wang, S., Belanger, A. P., Dubey, S., Frost, J. L., Shi, Q., Holton, P., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-48615-1 · Cited by 73 · see citing works
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[18F]GE-180 PET Detects Reduced Microglia Activation After LM11A-31 Therapy in a Mouse Model of Alzheimer's Disease
James, M. L., Belichenko, N. P., Shuhendler, A. J., Höhne, A., Andrews, L., Condon, C., Nguyen, T. V., Reiser, V., Jones, P. A., Trigg, W., et al. (2017) · Theranostics · doi:10.7150/thno.17666 · Cited by 73 · see citing works
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Diagnostic and Therapeutic Potential of TSPO Studies Regarding Neurodegenerative Diseases, Psychiatric Disorders, Alcohol Use Disorders, Traumatic Brain Injury, and Stroke: An Update
Dimitrova‐Shumkovska, J., Krstanoski, L., & Veenman, L. (2020) · Cells · doi:10.3390/cells9040870 · Cited by 70 · see citing works
The Brain–Gut Axis, an Important Player in Alzheimer and Parkinson Disease: A Narrative Review
Caradonna, E., Nemni, R., Bifone, A., Gandolfo, P., Costantino, L., Giordano, L., Mormone, E., Macula, A., Cuomo, M., Difruscolo, R., et al. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13144130 · Cited by 75 · see citing works
Increase of TREM2 during Aging of an Alzheimer’s Disease Mouse Model Is Paralleled by Microglial Activation and Amyloidosis
Brendel, M., Kleinberger, G., Probst, F., Jaworska, A., Overhoff, F., Blume, T., Albert, N. L., Carlsen, J., Lindner, S., Gildehaus, F. J., et al. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00008 · Cited by 66 · see citing works
Brain energy metabolism and neuroinflammation in ageing APP/PS1-21 mice using longitudinal 18 F-FDG and 18 F-DPA-714 PET imaging
Helin, J. S., Lopez‐Picon, F. R., Majidi, R. A., Eskola, O., Krzyczmonik, A., Keller, T., Löyttyniemi, E., Solin, O. H., Rinne, J. O., & Haaparanta‐Solin, M. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16677990 · Cited by 66 · see citing works
Astrocytic TSPO upregulation appears before microglial TSPO in Alzheimer’s disease
Tournier, B. B., Tsartsalis, S., Ceyzériat, K., Fraser, B. H., Grégoire, M.-C., Kövari, E., & Millet, P. (2020) · Journal of Alzheimer’s Disease · doi:10.3233/jad-200136 · Cited by 65 · see citing works
In Vivo Assessment of Neuroinflammation in <scp>4‐Repeat</scp> Tauopathies
Palleis, C., Sauerbeck, J., Beyer, L., Harris, S., Schmitt, J., Morenas‐Rodriguez, E., Finze, A., Nitschmann, A., Ruch‐Rubinstein, F., Eckenweber, F., et al. (2021) · Movement Disorders · doi:10.1002/mds.28395 · Cited by 62 · see citing works
TSPO and amyloid deposits in sub-regions of the hippocampus in the 3xTgAD mouse model of Alzheimer’s disease
Tournier, B. B., Tsartsalis, S., Rigaud, D., Fossey, C., Cailly, T., Fabis, F., Pham, T., Grégoire, M.-C., Kövari, E., Moulin-Sallanon, M., et al. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.09.022 · Cited by 62 · see citing works
Age and Sex Influence the Neuro-inflammatory Response to a Peripheral Acute LPS Challenge
Murtaj, V., Belloli, S., Di Grigoli, G., Pannese, M., Ballarini, E., Rodriguez-Menendez, V., Marmiroli, P., Cappelli, A., Masiello, V., Monterisi, C., et al. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00299 · Cited by 58 · see citing works
A Facile Radiolabeling of [18F]FDPA via Spirocyclic Iodonium Ylides: Preliminary PET Imaging Studies in Preclinical Models of Neuroinflammation
Wang, L., Cheng, R., Fujinaga, M., Yang, J., Zhang, Y., Hatori, A., Kumata, K., Yang, J., Vasdev, N., Du, Y., et al. (2017) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.7b00432 · Cited by 56 · see citing works
Alcohol-Induced Neuroinflammatory Response and Mitochondrial Dysfunction on Aging and Alzheimer’s Disease
León, B. E., Kang, S., Franca-Solomon, G., Shang, P., & Choi, D. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.778456 · Cited by 52 · see citing works
Effector function of anti-pyroglutamate-3 Aβ antibodies affects cognitive benefit, glial activation and amyloid clearance in Alzheimer’s-like mice
Crehan, H., Liu, B., Kleinschmidt, M., Rahfeld, J., Le, K. X., Caldarone, B. J., Frost, J. L., Hettmann, T., Hutter‐Paier, B., O’Nuallain, B., et al. (2020) · Alzheimer s Research & Therapy · doi:10.1186/s13195-019-0579-8 · Cited by 48 · see citing works
Self-citation
Early and Longitudinal Microglial Activation but Not Amyloid Accumulation Predicts Cognitive Outcome in PS2APP Mice
Focke, C., Blume, T., Zott, B., Shi, Y., Deußing, M., Peters, F., Schmidt, C., Kleinberger, G., Lindner, S., Gildehaus, F., et al. (2018) · Journal of Nuclear Medicine · doi:10.2967/jnumed.118.217703 · Cited by 48 · see citing works
Neuroinflammation Appears Early on PET Imaging and Then Plateaus in a Mouse Model of Alzheimer Disease
Lopez‐Picon, F. R., Snellman, A., Eskola, O., Helin, S., Solin, O. H., Haaparanta‐Solin, M., & Rinne, J. O. (2017) · Journal of Nuclear Medicine · doi:10.2967/jnumed.117.197608 · Cited by 48 · see citing works
Implicating neuroinflammation in hippocampus, prefrontal cortex and amygdala with cognitive deficit: a narrative review
Blossom, V., Ullal, S. D., D’Souza, M. M., Ranade, A. V., Kumar, N. A., & Rai, R. (2025) · 3 Biotech · doi:10.1007/s13205-025-04468-2 · Cited by 54 · see citing works
Microglial response to increasing amyloid load saturates with aging: a longitudinal dual tracer in vivo μPET-study
Blume, T., Focke, C., Peters, F., Deußing, M., Albert, N. L., Lindner, S., Gildehaus, F., von Ungern‐Sternberg, B., Ozmen, L., Baumann, K., et al. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1347-6 · Cited by 45 · see citing works
Time Courses of Cortical Glucose Metabolism and Microglial Activity Across the Life Span of Wild-Type Mice: A PET Study
Brendel, M., Focke, C., Blume, T., Peters, F., Deußing, M., Probst, F., Jaworska, A. M., Overhoff, F., Albert, N. L., Lindner, S., et al. (2017) · Journal of Nuclear Medicine · doi:10.2967/jnumed.117.195107 · Cited by 45 · see citing works
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
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. (2018) · Human Molecular Genetics · doi:10.1093/hmg/ddy202 · Cited by 44 · see citing works
Regulation of Mitochondrial, Cellular, and Organismal Functions by TSPO
Gavish, M., & Veenman, L. (2017) · Advances in pharmacology · doi:10.1016/bs.apha.2017.09.004 · Cited by 43 · see citing works
A binge high sucrose diet provokes systemic and cerebral inflammation in rats without inducing obesity
Patkar, O. L., Mohamed, A. Z., Narayanan, A., Mardon, K., Cowin, G., Bhalla, R., Stimson, D. H. R., Kassiou, M., Beecher, K., Belmer, A., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-90817-z · Cited by 32 · see citing works
Neurite orientation dispersion and density imaging reveals white matter and hippocampal microstructure changes produced by Interleukin-6 in the TgCRND8 mouse model of amyloidosis
Colon-Perez, L. M., Ibanez, K. R., Suarez, M., Torroella, K., Acuna, K., Ofori, E., Levites, Y., Vaillancourt, D. E., Golde, T. E., Chakrabarty, P., et al. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116138 · Cited by 41 · see citing works
Recent Developments in Diagnosis of Epilepsy: Scope of MicroRNA and Technological Advancements
Bandopadhyay, R., Singh, T., Ghoneim, M. M., Alshehri, S., Angelopoulou, E., Paudel, Y. N., Piperi, C., Ahmad, J., Alhakamy, N. A., Alfaleh, M. A., et al. (2021) · Biology · doi:10.3390/biology10111097 · Cited by 43 · see citing works
Microglial Activation Imaging Using 18 F-DPA-714 PET/MRI for Detecting Autoimmune Encephalitis
Zhang, M., Meng, H., Zhou, Q., Chunyu, H., He, L., Meng, H., Wang, H., Wang, Y., Sun, C., Xi, Y., et al. (2024) · Radiology · doi:10.1148/radiol.230397 · Cited by 39 · see citing works
TSPO Radioligands for Neuroinflammation: An Overview
Salerno, S., Viviano, M., Baglini, E., Poggetti, V., Giorgini, D., Castagnoli, J., Barresi, E., Castellano, S., Settimo, F. D., & Taliani, S. (2024) · Molecules · doi:10.3390/molecules29174212 · Cited by 33 · see citing works
Imaging Translocator Protein as a Biomarker of Neuroinflammation in Dementia
Kreisl, W. C., Henter, I. D., & Innis, R. B. (2017) · Advances in pharmacology · doi:10.1016/bs.apha.2017.08.004 · Cited by 39 · see citing works
Longitudinal translocator protein-18 kDa–positron emission tomography imaging of peripheral and central myeloid cells in a mouse model of complex regional pain syndrome
Cropper, H. C., Johnson, E. M., Haight, E. S., Cordonnier, S. A., Chaney, A. M., Forman, T. E., Biswal, A., Stevens, M. Y., James, M. L., & Tawfik, V. L. (2019) · Pain · doi:10.1097/j.pain.0000000000001607 · Cited by 37 · see citing works
Coupling between physiological TSPO expression in brain and myocardium allows stabilization of late-phase cerebral [18F]GE180 PET quantification
Deußing, M., Blume, T., Kaiser, L., Mahler, C. F., Focke, C., Todica, A. S., Unterrainer, M., Albert, N. L., Lindner, S., von Ungern‐Sternberg, B., et al. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.10.006 · Cited by 37 · see citing works
Longitudinal investigation of neuroinflammation and metabolite profiles in the APP swe× PS 1Δe9 transgenic mouse model of Alzheimer's disease
Chaney, A. M., Bauer, M., Bochicchio, D., Smigova, A., Kassiou, M., Davies, K. E., Williams, S. R., & Boutin, H. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14251 · Cited by 37 · see citing works
Essential Principles and Recent Progress in the Development of TSPO PET Ligands for Neuroinflammation Imaging
Viviano, M., Barresi, E., Siméon, F. G., Costa, B., Taliani, S., Settimo, F. D., Pike, V. W., & Castellano, S. (2022) · Current Medicinal Chemistry · doi:10.2174/0929867329666220329204054 · Cited by 34 · see citing works
In vivo PET imaging of the neuroinflammatory response in rat spinal cord injury using the TSPO tracer [18F]GE-180 and effect of docosahexaenoic acid
Tremoleda, J. L., Thau‐Zuchman, O., Davies, M., Foster, J., Khan, I., Vadivelu, K. C., Yip, P. K., Sosabowski, J. K., Trigg, W., & Michael-Titus, A. T. (2016) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-016-3391-8 · Cited by 34 · see citing works
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[O3–09–06]: MICROGLIAL ACTIVATION IN ALZHEIMER's DISEASE DETECTED BY NOVEL THIRD GENERATION TRANSLOCATOR PROTEIN TRACER FLUTRICICLAMIDE ([18F]GE180)
Calsolaro, V., Fan, Z., Femminella, G. D., Veronese, M., Pasqualetti, G., Trigg, W., Turkheimer, F., Gentleman, S., Brooks, D. J., Hinz, R., et al. (2017) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2017.07.355
Self-citation

Authors: 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.
Affiliations: Harvard University (US)
Brigham and Women's Hospital (US)
ORCID: Liu, Bin
Le, Kevin X.
Park, Mi-Ae
Wang, Shuyan
Belanger, Anthony P.
Dubey, Shipra
Jones, Paul A.
Trigg, William
Lemere, Cynthia. A.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2015-11-25
Volume: 35
Issue: 47
Pages: 15716-15730
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.0996-15.2015
PMC: PMC6705465
OpenAlex: W2253390436
Cited by: 114
References: 73
Citations by year: 2026: 3 · 2025: 4 · 2024: 12 · 2023: 8 · 2022: 10 · 2021: 13 · 2020: 13 · 2019: 11 · 2018: 14 · 2017: 17 · 2016: 9
FWCI: 7.13
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 182 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Aging (R01AG040092)
National Institute of Neurological Disorders and Stroke (R01NS136122)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Medical Imaging Techniques and Applications
Keywords: Alzheimer's disease, neuroinflammation, microglial activation, aging, hippocampus, microPET imaging, binding potential, tracer metabolism, Alzheimer's disease biomarkers
MeSH terms: Aging, Alzheimer Disease, Animals, Carbazoles, Fluorine Radioisotopes, Humans, Inflammation, Male, Mice, Inbred C57BL, Mice, Transgenic, Receptors, GABA, Disease Progression, Positron-Emission Tomography, Mice

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In Vivo Detection of Age- and Disease-Related Increases in Neuroinflammation by18F-GE180 TSPO MicroPET Imaging in Wild-Type and Alzheimer's Transgenic Mice

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