Age and disease related changes in the translocator protein (TSPO) system in the human brain: Positron emission tomography measurements with [11C]vinpocetine
Abstract
Backgrounds and purpose The main objectives of the present study were (i) to measure density changes of activated microglia and the peripheral benzodiazepine receptor/translocator protein (TSPO) system during normal ageing in the human brain with positron emission tomography (PET) using the TSPO molecular imaging biomarker [(11)C]vinpocetine and (ii) to compare the level and pattern of TSPO in Alzheimer (AD) patients with age matched healthy subjects, in order to assess the biomarker's usefulness as a diagnostic imaging marker in normal (ageing) and pathological (AD) up-regulation of microglia.Methods and subjects PET measurements were made in healthy volunteers, aged between 25 and 78 years, and AD patients, aged between 67 and 82 years, using [(11)C]vinpocetine as the tracer. Global and regional quantitative parameters of tracer uptake and binding, including time activity curves (TAC) of standard uptake values (%SUV), binding affinity parameters, intensity spectrum and homogeneity of the uptake distribution were measured and analysed.Results Both %SUV and binding values increased with age linearly in the whole brain and in all brain regions. There were no significant differences between the %SUV values of the AD patients and age matched control subjects. There were, however, significant differences in %SUV values in a large number of brain regions between young subjects and old subjects, as well as young subjects and AD patients. The intensity spectrum analysis and homogeneity analysis of the voxel data show that the homogeneity of the %SUV values decreases with ageing and during the disease, whereas the centre of the intensity spectrum is shifted to higher %SUV values. These data indicate an inhomogeneous up-regulation of the TSPO system during ageing and AD. These changes were significant between the group of young subjects and old subjects, as well as young subjects and AD patients, but not between old subjects and AD patients.Conclusions The present data indicate that [(11)C]vinpocetine may serve as a molecular imaging biomarker of the activity of the TSPO system and, consequently, of the up-regulation of microglia during ageing and in neuroinflammatory diseases. However, the global and regional brain %SUV values between AD patients and age matched controls are not different from each other. The disease specific changes, measured with [(11)C]vinpocetine in AD, are significantly different from those measured in age matched controls only if the inhomogeneities in the uptake pattern are explored with advanced mathematical techniques. For this reason, PET studies using [(11)C]vinpocetine, as molecular imaging biomarker, can efficiently visualise the activation of microglia and the up-regulation of TSPO during ageing and in diseased brains with the help of an appropriate inhomogeneity analysis of the radioligand's brain uptake pattern.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Several PET scan studies have revealed increased receptor binding of the TSPO ligands, R-[11C]PK11195 and [11C]vinpocetine, in the cortical and subcortical brain regions of healthy elderly participants.
“Several PET scan studies have revealed increased receptor binding of the TSPO ligands, R-[ 11 C]PK11195 and [ 11 C]vinpocetine, in the cortical and subcortical brain regions of healthy elderly participants (Gulyas et al, 2011;Schuitemaker et al, 2012).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Gulyas et al, 2011
Cites
Distribution Volume Ratios without Blood Sampling from Graphical Analysis of PET Data
Logan, J., Fowler, J. S., Volkow, N. D., Wang, G., Ding, Y., & Alexoff, D. L. (1996) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199609000-00008 · Cited by 1,515 · see citing works
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., et al. (2006) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2006.06.005 · Cited by 1,389 · see citing works
In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson's disease
Gerhard, A., Pavese, N., Hotton, G., Turkheimer, F., Es, M., Hammers, A., Eggert, K., Oertel, W., Banati, R. B., & Brooks, D. J. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.08.002 · Cited by 1,200 · see citing works
In-vivo measurement of activated microglia in dementia
Cagnin, A., Brooks, D. J., Kennedy, A. M., Gunn, R. N., Myers, R., Turkheimer, F. E., Jones, T., & Banati, R. B. (2001) · The Lancet · doi:10.1016/s0140-6736(01)05625-2 · Cited by 1,054 · see citing works
Blood–brain barrier: Ageing and microvascular disease – systematic review and meta-analysis
Farrall, A. J., & Wardlaw, J. M. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.07.015 · Cited by 882 · see citing works
Immune activation in brain aging and neurodegeneration: too much or too little?
Lucin, K. M., & Wyss-Coray, T. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.039 · Cited by 679 · see citing works
The peripheral benzodiazepine binding site in the brain in multiple sclerosis
Banati, R. B., Newcombe, J., Gunn, R. N., Cagnin, A., Turkheimer, F., Heppner, F., Price, G., Wegner, F., Giovannoni, G., Miller, D. H., et al. (2000) · Brain · doi:10.1093/brain/123.11.2321 · Cited by 661 · see citing works
Blood brain barrier: ageing and microvascular disease-systematic review and meta-analysis
Farrall, A., & Wardlaw, J. M. (2009) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2009.02.089 · Cited by 639 · see citing works
Glia and their cytokines in progression of neurodegeneration
Mrak, R. E., & Griffin, W. S. T. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.05.010 · Cited by 592 · see citing works
Wienhard, K., Dahlbom, M. L., Eriksson, L., Michel, C. J., Bruckbauer, T., Pietrzyk, U., & Heiss, W. (1994) · Journal of Computer Assisted Tomography · doi:10.1097/00004728-199401000-00023 · Cited by 561 · see citing works
Conversion of amyloid positive and negative MCI to AD over 3 years
Okello, A., Koivunen, J., Edison, P., Archer, H. A., Turkheimer, F., Någren, K., Bullock, R. M., Walker, Z., Kennedy, A. M., Fox, N. C., et al. (2009) · Neurology · doi:10.1212/wnl.0b013e3181b23564 · Cited by 522 · see citing works
Visualising microglial activation in vivo
Banati, R. B. (2002) · Glia · doi:10.1002/glia.10144 · Cited by 428 · see citing works
Nuclear imaging of neuroinflammation: a comprehensive review of [11C]PK11195 challengers
Chauveau, F., Boutin, H., Camp, N. V., Dollé, F., & Tavitian, B. (2008) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-008-0908-9 · Cited by 419 · see citing works
Microglial senescence: does the brain's immune system have an expiration date?
Streit, W. J. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.07.001 · Cited by 397 · see citing works
Expansion of the calcium hypothesis of brain aging and Alzheimer's disease: minding the store
Thibault, O., Gant, J. C., & Landfield, P. W. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00295.x · Cited by 379 · see citing works
Venneti, S., Lopresti, B. J., & Wiley, C. A. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.10.002 · Cited by 373 · see citing works
Microglial activation and amyloid deposition in mild cognitive impairment: A PET study
Okello, A., Edison, P., Archer, H. A., Turkheimer, F. E., Kennedy, J., Bullock, R., Walker, Z., Kennedy, A., Fox, N., Rossor, M., et al. (2009) · Neurology · doi:10.1212/01.wnl.0000338622.27876.0d · Cited by 367 · see citing works
Conde, J. R., & Streit, W. J. (2006) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/01.jnen.0000202887.22082.63 · Cited by 344 · see citing works
Age and gender effects on microglia and astrocyte numbers in brains of mice
Mouton, P. R., Long, J. M., Lei, D.-L., Howard, V., Jucker, M., Calhoun, M. E., & Ingram, D. K. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03475-3 · Cited by 320 · see citing works
m, M. B., thius, J. B., Eriksson, L., Greitz, T. V. B., Ribbe, T., & Wid�n, L. (1981) · Journal of Computer Assisted Tomography · doi:10.1097/00004728-198102000-00027 · Cited by 315 · see citing works
Vascular basis for brain degeneration: faltering controls and risk factors for dementia
Kalaria, R. N. (2010) · Nutrition Reviews · doi:10.1111/j.1753-4887.2010.00352.x · Cited by 291 · see citing works
Evolution of microglial activation in patients after ischemic stroke: a [11C](R)-PK11195 PET study
Gerhard, A., Schwarz, J., Myers, R., Wise, R. J. S., & Banati, R. B. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.09.034 · Cited by 286 · see citing works
James, M. L., Fulton, R., Vercouillie, J., Henderson, D., Garreau, L., Chalon, S., Dollé, F., Selleri, S., Guilloteau, D., & Kassiou, M. (2008) · Journal of Nuclear Medicine · doi:10.2967/jnumed.107.046151 · Cited by 283 · see citing works
Kreisl, W. C., Fujita, M., Fujimura, Y., Kimura, N., Jenko, K. J., Kannan, P., Hong, J. S., Morse, C. L., Zoghbi, S. S., Gladding, R. L., et al. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.11.056 · Cited by 275 · see citing works
Adenosine Receptors and the Central Nervous System
Sebastião, A. M., & Ribeiro, J. A. (2009) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-89615-9_16 · Cited by 271 · see citing works
Aging‐dependent changes of microglial cells and their relevance for neurodegenerative disorders
Von Bernhardi, R., Tichauer, J. E., & Eugenín, J. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06537.x · Cited by 258 · see citing works
Ca2+–Zn2+ permeable AMPA or kainate receptors: possible key factors in selective neurodegeneration
Weiss, J. H., & Sensi, S. L. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01610-6 · Cited by 255 · see citing works
Human brain atlas: For high‐resolution functional and anatomical mapping
Roland, P. E., Graufelds, C. J., Wahlin, J.-P., Ingelman, L., Andersson, M., Ledberg, A., Pedersen, J. R., Åkerman, S., Dabringhaus, A., & Zilles, K. (1994) · Human Brain Mapping · doi:10.1002/hbm.460010303 · Cited by 253 · see citing works
[ 11 C]( R )-PK11195 PET imaging of microglial activation in multiple system atrophy
Gerhard, A., Banati, R. B., Goerres, G. B., Cagnin, A., Myers, R., Gunn, R. N., Turkheimer, F., Good, C. D., Mathias, C. J., Quinn, N. P., et al. (2003) · Neurology · doi:10.1212/01.wnl.0000078192.95645.e6 · Cited by 247 · see citing works
Vinpocetine inhibits NF-κB–dependent inflammation via an IKK-dependent but PDE-independent mechanism
Jeon, K., Xu, X., Aizawa, T., Lim, J. H., Jono, H., Kwon, D.-S., Abe, J., Berk, B. C., Li, J., & Chen, Y. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914414107 · Cited by 242 · see citing works
Chauveau, F., Camp, N. V., Dollé, F., Kühnast, B., Hinnen, F., Damont, A., Boutin, H., James, M. L., Kassiou, M., & Tavitian, B. (2009) · Journal of Nuclear Medicine · doi:10.2967/jnumed.108.058669 · Cited by 236 · see citing works
The channel hypothesis of Alzheimer’s disease: current status
Kagan, B. L., Hirakura, Y., Azimov, R., Azimova, R., & Lin, M. (2002) · Peptides · doi:10.1016/s0196-9781(02)00067-0 · Cited by 230 · see citing works
Fujita, M., Imaizumi, M., Zoghbi, S. S., Fujimura, Y., Farris, A. G., Suhara, T., Hong, J. S., Pike, V. W., & Innis, R. B. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.11.011 · Cited by 213 · see citing works
Adenosine Receptors and Neurological Disease: Neuroprotection and Neurodegeneration
Stone, T. W., Ceruti, S., & Abbracchio, M. P. (2009) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-89615-9_17 · Cited by 211 · see citing works
Owen, D. R., Howell, O. W., Tang, S.-P., Wells, L. A., Bennacef, I., Bergström, M., Gunn, R. N., Rabiner, E. A., Wilkins, M. R., Reynolds, R., et al. (2010) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2010.63 · Cited by 211 · see citing works
Martín, A., Boisgard, R., Thézé, B., Van Camp, N., Kuhnast, B., Damont, A., Kassiou, M., Dollé, F., & Tavitian, B. (2010) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.205 · Cited by 206 · cited 1× · see citing works
“…[11C]DAA1106, [18F]FEDAA1106, [11C]DPA713, and [18F]DPA714 (Boutin et al., 2007; Doorduin et al., 2010; Endres et al., 2009; Fujimura et al., 2006; Higuchi, 2009; James et al., 2008; Kassiou et al., 2005; Martin et al., 2010; Okello et al., 2009a,b; Fujimura et al., 2010; Takano et al., 2010).”
Intrinsic Activated Microglia Map to the Peri-infarct Zone in the Subacute Phase of Ischemic Stroke
Price, C., Wang, D., Menon, D. K., Guadagno, J., Cleij, M. C., Fryer, T. D., Aigbirhio, F. I., Baron, J., & Warburton, E. A. (2006) · Stroke · doi:10.1161/01.str.0000226980.95389.0b · Cited by 201 · see citing works
Deshmukh, R. R., Sharma, V., Mehan, S., Sharma, N., & Bedi, K. L. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.08.027 · Cited by 195 · see citing works
Blood-brain barrier disturbance in patients with Alzheimer's disease is related to vascular factors
Blennow, K., Wallin, A., Fredman, P., Karlsson, I., Gottfries, C. G., & Svennerholm, L. T. (2009) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1990.tb01563.x · Cited by 185 · see citing works
Angulo-Pueyo, E., Casadó, V., Mallol, J., Canela, E. I., Viñals, F., Ferrer, I., Lluís, C., & Franco, R. (2003) · Brain Pathology · doi:10.1111/j.1750-3639.2003.tb00475.x · Cited by 179 · see citing works
RESEARCH ARTICLE: Up‐regulation of Adenosine Receptors in the Frontal Cortex in Alzheimer's Disease
Albasanz, J. L., Perez, S., Barrachina, M., Ferrer, I., & Martı́n, M. (2008) · Brain Pathology · doi:10.1111/j.1750-3639.2007.00112.x · Cited by 177 · see citing works
Takano, A., Arakawa, R., Ito, H., Tateno, A., Takahashi, H., Matsumoto, R., Okubo, Y., & Suhara, T. (2010) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145710000313 · Cited by 174 · see citing works
Self-citationGerhard, A., Trender‐Gerhard, I., Turkheimer, F., Quinn, N. P., Bhatia, K. P., & Brooks, D. J. (2006) · Movement Disorders · doi:10.1002/mds.20668 · Cited by 171 · see citing works
Boutin, H., Chauveau, F., Thominiaux, C., Grégoire, M., James, M. L., Trébossen, R., Hantraye, P., Dollé, F., Tavitian, B., & Kassiou, M. (2007) · Journal of Nuclear Medicine · doi:10.2967/jnumed.106.036764 · Cited by 161 · see citing works
Microglial degeneration in the aging brain - bad news for neurons?
Streit, W. (2008) · Frontiers in Bioscience · doi:10.2741/2937 · Cited by 150 · see citing works
Role of sodium channel inhibition in neuroprotection: effect of vinpocetine
Bönöczk, P., Gulyás, B. Z., Ádám‐Vizi, V., et al. (2000) · Brain Research Bulletin · doi:10.1016/s0361-9230(00)00354-3 · Cited by 136 · see citing works
Self-citationDollé, F., Luus, C., Reynolds, A. J., & Kassiou, M. (2009) · Current Medicinal Chemistry · doi:10.2174/092986709788803150 · Cited by 133 · see citing works
Kreisl, W. C., Liow, J., Kimura, N., Seneca, N. M., Zoghbi, S. S., Morse, C. L., Herscovitch, P., Pike, V. W., & Innis, R. B. (2010) · Journal of Nuclear Medicine · doi:10.2967/jnumed.109.070151 · Cited by 131 · see citing works
Initial Evaluation of 11C-DPA-713, a Novel TSPO PET Ligand, in Humans
Endres, C. J., Pomper, M. G., James, M. L., Uzuner, Ö., Hammoud, D. A., Watkins, C. C., Reynolds, A., Hilton, J., Dannals, R. F., & Kassiou, M. (2009) · Journal of Nuclear Medicine · doi:10.2967/jnumed.109.062265 · Cited by 131 · see citing works
The blood-brain barrier and cerebral microcirculation in Alzheimer disease.
Kalaria, R. N. (1992) · PubMed · Cited by 130 · see citing works
Head fixation system for integration of radiodiagnostic and therapeutic procedures
Greitz, T. V. B., Bergström, M., Boethius, J., et al. (1980) · Neuroradiology · doi:10.1007/bf00369080 · Cited by 120 · see citing works
Eburnamine derivatives and the brain
Vas, Á., & Gulyás, B. Z. (2005) · Medicinal Research Reviews · doi:10.1002/med.20043 · Cited by 117 · see citing works
Self-citationChapter 36 Structural changes in the normally aging cerebral cortex of primates
Peters, A. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)36038-2 · Cited by 114 · see citing works
Tomasi, G., Edison, P., Bertoldo, A., Roncaroli, F., Singh, P., Gerhard, A., Cobelli, C., Brooks, D. J., & Turkheimer, F. E. (2008) · Journal of Nuclear Medicine · doi:10.2967/jnumed.108.050583 · Cited by 97 · see citing works
Fujimura, Y., Ikoma, Y., Yasuno, F., Suhara, T., Ota, M., Matsumoto, R., Nozaki, S., Takano, A., Kosaka, J., Zhang, M., et al. (2006) · PubMed · Cited by 95 · see citing works
Self-citationPET Studies with Carbon-11 Radioligands in Neuropsychopharmacological Drug Development
Halldin, C., Gulyás, B. Z., & Farde, L. (2001) · Current Pharmaceutical Design · doi:10.2174/1381612013396871 · Cited by 95 · see citing works
Self-citationEvaluation of Reference Tissue Models for the Analysis of [ 11 C]( R )-PK11195 Studies
Kropholler, M. A., Boellaard, R., Schuitemaker, A., Folkersma, H., van Berckel, B. N. M., & Lammertsma, A. A. (2006) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600289 · Cited by 94 · see citing works
11C-AC-5216: A Novel PET Ligand for Peripheral Benzodiazepine Receptors in the Primate Brain
Zhang, M.-R., Kumata, K., Maeda, J., Yanamoto, K., Hatori, A., Okada, M., Higuchi, M., Obayashi, S., Suhara, T., & Suzuki, K. (2007) · Journal of Nuclear Medicine · doi:10.2967/jnumed.107.043505 · Cited by 86 · see citing works
Vinpocetine as a potent antiinflammatory agent
Medina, A. E. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005138107 · Cited by 84 · see citing works
Development of a Tracer Kinetic Plasma Input Model for (R)-[11C]PK11195 Brain Studies
Kropholler, M. A., Boellaard, R., Schuitemaker, A., van Berckel, B. N. M., Luurtsema, G., Windhorst, A. D., & Lammertsma, A. A. (2005) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600092 · Cited by 81 · see citing works
Fujimura, Y., Zoghbi, S. S., Siméon, F. G., Taku, A. K., Pike, V. W., Innis, R. B., & Fujita, M. (2009) · Journal of Nuclear Medicine · doi:10.2967/jnumed.108.060186 · Cited by 78 · see citing works
Luijten, J. A. F. M., & de la Faille-Kuyper, E. H. B. (1972) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(72)90009-3 · Cited by 77 · see citing works
Cselényi, Z., Olsson, H., Halldin, C., Gulyás, B. Z., & Farde, L. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.02.053 · Cited by 77 · see citing works
Self-citationAlterations of the blood-brain barrier in cerebral white matter lesions in the ageing brain
Simpson, J. E., Wharton, S. B., Cooper, J., Gelsthorpe, C., Baxter, L., Forster, G., Shaw, P. J., Savva, G., Matthews, F. E., Brayne, C., et al. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.09.063 · Cited by 77 · see citing works
Vas, Á., Shchukin, Y., Karrenbauer, V. D., Cselényi, Z., Kostulas, K., Hillert, J. A., Savić, I., Takano, A., Halldin, C., & Gulyás, B. Z. (2007) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2007.07.018 · Cited by 71 · see citing works
Self-citationVarrone, A., Tóth, M., Steiger, C., et al. (2010) · Journal of Nuclear Medicine · doi:10.2967/jnumed.110.077651 · Cited by 61 · see citing works
Self-citationPET studies on the brain uptake and regional distribution of [11C]vinpocetine in human subjects
Gulyás, B. Z., Halldin, C., Sandell, J., Karlsson, P., Sóvágó, J., Kárpáti, E., Kiss, B., Vas, Á., Cselényi, Z., & Farde, L. (2002) · Acta Neurologica Scandinavica · doi:10.1034/j.1600-0404.2002.01302.x · Cited by 59 · see citing works
Self-citationFukumitsu, N., Ishii, K., Kimura, Y., Oda, K., Hashimoto, M., Suzuki, M., & Ishiwata, K. (2008) · Annals of Nuclear Medicine · doi:10.1007/s12149-008-0185-5 · Cited by 50 · see citing works
Vinpocetine for acute ischaemic stroke
Bereczki, D., & Fekete, I. (2008) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd000480.pub2 · Cited by 50 · see citing works
Szilágyi, G., Nagy, Z., Balkay, L., Boros, I., Emri, M., Lehel, S., Márián, T., Molnár, T., Szakáll, S., Trón, L., et al. (2005) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2004.11.053 · Cited by 49 · see citing works
Self-citationGulyás, B. Z., Halldin, C., Sóvágó, J., et al. (2002) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-002-0823-4 · Cited by 49 · see citing works
Self-citation[11C]Vinpocetine: a prospective peripheral benzodiazepine receptor ligand for primate PET studies
Gulyás, B. Z., Halldin, C., Vas, Á., Banati, R. B., Shchukin, E., Finnema, S. J., Tarkainen, J., Tihanyi, K., Szilágyi, G., & Farde, L. (2004) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2004.11.032 · Cited by 49 · see citing works
Self-citationRole of Microglia in Age-Related Changes to the Nervous System
Brown, D. R. (2009) · The Scientific World JOURNAL · doi:10.1100/tsw.2009.111 · Cited by 48 · see citing works
Nyakas, C., Felszeghy, K., Szabó, R., Keijser, J. N., Luiten, P. G. M., Szombathelyi, Z., & Tihanyi, K. (2009) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2009.00078.x · Cited by 46 · see citing works
The Role of Peripheral Benzodiazepine Receptors (PBRs) in CNS Pathophysiology
Lang, S.-Y. (2002) · Current Medicinal Chemistry · doi:10.2174/0929867023369745 · Cited by 45 · see citing works
Cerebral Effects of a Single Dose of Intravenous Vinpocetine in Chronic Stroke Patients: A PET Study
Szakáll, S., Boros, I., Balkay, L., et al. (1998) · Journal of Neuroimaging · doi:10.1111/jon199884197 · Cited by 43 · see citing works
Ligands for peripheral benzodiazepine binding sites in glial cells
Kassiou, M., Meikle, S. R., & Banati, R. B. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.12.010 · Cited by 40 · see citing works
Peripheral benzodiazepine receptor: structure and function in health and disease.
Papadopoulos, V. D. (2003) · PubMed · Cited by 39 · see citing works
Synthesis of [125I]iodoDPA-713: A new probe for imaging inflammation
Wang, H., Pullambhatla, M., Guilarte, T. R., Mease, R. C., & Pomper, M. G. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.08.102 · Cited by 38 · see citing works
Characterization of inhibitors of phosphodiesterase 1C on a human cellular system
Dunkern, T. R., & Hatzelmann, A. (2007) · FEBS Journal · doi:10.1111/j.1742-4658.2007.06001.x · Cited by 36 · see citing works
Effects of Vinpocetine on mitochondrial function and neuroprotection in primary cortical neurons
Tárnok, K., Kiss, E., Luiten, P. G. M., Nyakas, C. J., Tihanyi, K., Schlett, K., & Eisel, U. L. M. (2008) · Neurochemistry International · doi:10.1016/j.neuint.2008.08.003 · Cited by 36 · see citing works
Visualization of Brain Amyloid and Microglial Activation in Mouse Models of Alzheimers Disease
Higuchi, M. (2009) · Current Alzheimer Research · doi:10.2174/156720509787602906 · Cited by 34 · see citing works
Mazák, K., Vámos, J., Nemes, A., et al. (2003) · Journal of Chromatography A · doi:10.1016/s0021-9673(03)00617-4 · Cited by 34 · see citing works
Doorduin, J., Klein, H. C., de Jong, J. R., et al. (2009) · Nuclear Medicine and Biology · doi:10.1016/j.nucmedbio.2009.09.002 · Cited by 32 · see citing works
Gulyás, B. Z., Halldin, C., Karlsson, P., et al. (1999) · Journal of Neuroimaging · doi:10.1111/jon199994217 · Cited by 31 · see citing works
Self-citationVas, Á., Gulyás, B. Z., Szabó, Z. R., et al. (2002) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(02)00301-5 · Cited by 31 · see citing works
Self-citationChanges at the focus of experimental ischemic stroke treated with neuroprotective agents
Onishchenko, L. S., Gaikova, O. N., & Yanishevskii, S. N. (2007) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-008-0007-1 · Cited by 28 · see citing works
A Novel PDE2A Reporter Cell Line: Characterization of the Cellular Activity of PDE Inhibitors
Wunder, F., Gnoth, M. J., Geerts, A., et al. (2008) · Molecular Pharmaceutics · doi:10.1021/mp800127n · Cited by 25 · see citing works
Positron Emission Tomography: A Critical Assessment of Recent Trends
Gulyás, B. Z., & Müller‐Gärtner, H. W. (1998) · Springer eBooks · doi:10.1007/978-94-011-4996-9 · Cited by 24 · see citing works
Self-citationThe Concept of In Vivo Imaging of Neuroinflammation with [11C](R)-PK11195 PET
Cagnin, A., Gerhard, A., & Banati, R. B. (2002) · Springer eBooks · doi:10.1007/978-3-662-05073-6_10 · Cited by 20 · see citing works
Investigation of the Metabolites of (S,S)-[11C]MeNER in Humans, Monkeys and Rats
Schou, M., Zoghbi, S. S., Shetty, H. U., et al. (2008) · Molecular Imaging and Biology · doi:10.1007/s11307-008-0175-y · Cited by 19 · see citing works
Takano, A., Gulyás, B. Z., Varrone, A., et al. (2009) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-009-1194-x · Cited by 15 · see citing works
Self-citationVinpocetine for acute ischaemic stroke
Bereczki, D., & Fekete, I. (1997) · doi:10.1002/14651858.cd000480 · Cited by 13 · see citing works
Fehér, G., Koltai, K., Késmárky, G., et al. (2009) · Phytomedicine · doi:10.1016/j.phymed.2008.10.014 · Cited by 12 · see citing works
Adám-Vizi (2000) · PubMed · Cited by 12 · see citing works
Halldin, C., Gulyás, B. Z., & Farde, L. (2004) · Springer eBooks · doi:10.1007/978-3-662-07310-0_5 · Cited by 8 · see citing works
Self-citationAutoradiographic evaluation of [11C]vinpocetine binding in the humanpostmortembrain
Hall, H., Varnäs, K., Sandell, J., et al. (2002) · Acta Biologica Hungarica · doi:10.1556/abiol.53.2002.1-2.7 · Cited by 8 · see citing works
Cselényi, Z. (2004) · Neurochemistry International · doi:10.1016/j.neuint.2003.12.005 · Cited by 7 · see citing works
Self-citationNeuroprotection in Ischemic/Hypoxic Disorders
Nagy, Z., & Simon, L. (2004) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-8969-7_3 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Microglia in Neuroinflammation and Neurodegeneration: From Understanding to Therapy
Muzio, L., Viotti, A., & Martino, G. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.742065 · Cited by 581 · see citing works
Microglia Priming with Aging and Stress
Niraula, A., Sheridan, J. F., & Godbout, J. P. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.185 · Cited by 398 · see citing works
Microglia in Aging and Alzheimer’s Disease: A Comparative Species Review
Edler, M. K., Mhatre-Winters, I., & Richardson, J. R. (2021) · Cells · doi:10.3390/cells10051138 · Cited by 126 · see citing works
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., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.0996-15.2015 · Cited by 114 · 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
Cerami, C., Iaccarino, L., & Perani, D. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18050993 · Cited by 75 · see citing works
Suridjan, I., Rusjan, P. M., Voineskos, A. N., Selvanathan, T., Setiawan, E., Strafella, A. P., Wilson, A. A., Meyer, J. H., Houle, S., & Mizrahi, R. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2013.09.021 · Cited by 71 · see citing works
Microglial Activation and Connectivity in Alzheimer Disease and Aging
Rauchmann, B., Brendel, M., Franzmeier, N., Trappmann, L., Zaganjori, M., Ersoezlue, E., Morenas‐Rodriguez, E., Guersel, S., Burow, L., Kurz, C., et al. (2022) · Annals of Neurology · doi:10.1002/ana.26465 · Cited by 61 · see citing works
Jung, M. E., Metzger, D. B., & Hall, J. (2020) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.172873 · Cited by 8 · see citing works
- Authors
- Gulyás, B., Vas, Á., Tóth, M., Takano, A., Varrone, A., Cselényi, Z., Schain, M., Mattsson, P., & Halldin, C.
- Affiliations
- Karolinska Institutet (SE)
- Gedeon Richter (Hungary) (HU)
- Corresponding author
- Gulyás, Balázs
- ORCID
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2011-06
- Volume
- 56
- Issue
- 3
- Pages
- 1111-1121
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W2099480013
- Cited by
- 94
- References
- 99
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 5 · 2023: 3 · 2022: 8 · 2021: 9 · 2020: 6 · 2019: 8 · 2018: 7 · 2017: 8 · 2016: 7 · 2015: 9 · 2014: 8 · 2013: 5 · 2012: 5
- FWCI
- 3.54
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- translocator protein (TSPO), Alzheimer's disease, brain aging, microglial activation, neuroinflammation, molecular imaging biomarkers, neurodegeneration biomarkers
- MeSH terms
- Adult, Aged, Aged, 80 and over, Aging, Alzheimer Disease, Brain, Data Interpretation, Statistical, Female, Humans, Image Processing, Computer-Assisted, Isotope Labeling, Male, Middle Aged, Vinca Alkaloids, Receptors, GABA, Radiopharmaceuticals, Positron-Emission Tomography
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review