Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)-PK11195 positron emission tomography study

Turner, M.R; Cagnin, A; Turkheimer, F.E; Miller, C.C.J; Shaw, C.E; Brooks, D.J; Leigh, P.N; Banati, R.B

doi:10.1016/j.nbd.2003.12.012

Cited by 737Amyotrophic Lateral Sclerosis ResearchNeuroinflammation and Neurodegeneration MechanismsMultiple Sclerosis Research Studies

Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)-PK11195 positron emission tomography study

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Turner, M.R, Cagnin, A, Turkheimer, F.E, Miller, C.C.J, Shaw, C.E, Brooks, D.J, Leigh, P.N, Banati, R.B·2004·Neurobiology of Disease

DOI 10.1016/j.nbd.2003.12.012

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Abstract

Microglial activation is implicated in the pathogenesis of ALS and can be detected in animal models of the disease that demonstrate increased survival when treated with anti-inflammatory drugs. PK11195 is a ligand for the "peripheral benzodiazepine binding site" expressed by activated microglia. Ten ALS patients and 14 healthy controls underwent [(11)C](R)-PK11195 PET of the brain. Volumes of interest were defined to obtain [(11)C](R)-PK11195 regional binding potential values for motor and "extra-motor" regions. Significantly increased binding was found in motor cortex (P = 0.003), pons (P = 0.004), dorsolateral prefrontal cortex (P = 0.010) and thalamus (P = 0.005) in the ALS patients, with significant correlation between binding in the motor cortex and the burden of upper motor neuron signs clinically (r = 0.73, P = 0.009). These findings indicate that cerebral microglial activation can be detected in vivo during the evolution of ALS, and support the previous observations that cerebral pathology is widespread. They also argue for the development of therapeutic strategies aimed at inflammatory pathways.

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Elevated macrophage markers in ALS CSF are presumably due to increased CNS microglia or their activation.
“presumably due to increased CNS microglia or their activation, as suggested by positron emission tomography (PET) imaging using radiotracers specific for activated microglia [423,424].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [424]
Postmortem and in vivo PET studies revealed widespread cerebral microglial activation in patients with ALS and even in pre-symptomatic ALS-related mutation carriers.
“Postmortem studies308–310 and in vivo PET studies311–313 revealed widespread cerebral microglial activation in patients with ALS,308–312 and even in pre-symptomatic ALS-related mutation carriers.309,313”
From Microglia in neurodegenerative diseases: mechanism and potential therapeutic targets (2023) · cites this paper as [311]
Microglial activation in middle frontal and superior or middle temporal gyrus regions was also highly found in in vivo PET imaging studies in humans.
“Microglial activation in middle frontal and superior or middle temporal gyrus regions was also highly found in vivo PET imaging studies in humans”
From Microglia in neurodegenerative diseases: mechanism and potential therapeutic targets (2023) · cites this paper as [311]

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Neuroinflammation in neurodegenerative disorders: the roles of microglia and astrocytes
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Translocator protein (18 kDa) (TSPO) as a therapeutic target for neurological and psychiatric disorders
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Microglia Induce Motor Neuron Death via the Classical NF-κB Pathway in Amyotrophic Lateral Sclerosis
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Blood-Brain Barrier Dysfunction Amplifies the Development of Neuroinflammation: Understanding of Cellular Events in Brain Microvascular Endothelial Cells for Prevention and Treatment of BBB Dysfunction
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Microglia in Neuroinflammation and Neurodegeneration: From Understanding to Therapy
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Microbiome–microglia connections via the gut–brain axis
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An Inflammation-Centric View of Neurological Disease: Beyond the Neuron
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Endogenous regulatory T lymphocytes ameliorate amyotrophic lateral sclerosis in mice and correlate with disease progression in patients with amyotrophic lateral sclerosis
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Nuclear imaging of neuroinflammation: a comprehensive review of [11C]PK11195 challengers
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Role of Neuroinflammation in Amyotrophic Lateral Sclerosis: Cellular Mechanisms and Therapeutic Implications
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The peripheral benzodiazepine receptor (Translocator protein 18kDa) in microglia: From pathology to imaging
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Microglia in ALS: The Good, The Bad, and The Resting
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The resolution of neuroinflammation in neurodegeneration: leukocyte recruitment via the choroid plexus
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Novel threshold tracking techniques suggest that cortical hyperexcitability is an early feature of motor neuron disease
Vucic, S. (2006) · Brain · doi:10.1093/brain/awl172 · Cited by 334 · see citing works
Inflammation in ALS/FTD pathogenesis
McCauley, M. E., & Baloh, R. H. (2018) · Acta Neuropathologica · doi:10.1007/s00401-018-1933-9 · Cited by 324 · see citing works
Neuroinflammation in Neurodegenerative Disorders-a Review
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RETRACTED: Neuroinflammatory Markers: Key Indicators in the Pathology of Neurodegenerative Diseases
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Microglia-mediated recovery from ALS-relevant motor neuron degeneration in a mouse model of TDP-43 proteinopathy
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Neuroglia in neurodegeneration
Heneka, M. T., Rodriguez, J. J., & Verkhratsky, A. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.11.004 · Cited by 303 · see citing works
Immune-mediated Mechanisms in the Pathoprogression of Amyotrophic Lateral Sclerosis
Zhao, W., Beers, D. R., & Appel, S. H. (2013) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-013-9489-x · Cited by 298 · see citing works
Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis
Filippini, N., Douaud, G., Mackay, C. E., Knight, S., Talbot, K., & Turner, M. R. (2010) · Neurology · doi:10.1212/wnl.0b013e3181fb84d1 · Cited by 280 · see citing works
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Protective and Toxic Neuroinflammation in Amyotrophic Lateral Sclerosis
Hooten, K. G., Beers, D. R., Zhao, W., & Appel, S. H. (2015) · Neurotherapeutics · doi:10.1007/s13311-014-0329-3 · Cited by 287 · see citing works
Microglial Activation Correlates with Disease Progression and Upper Motor Neuron Clinical Symptoms in Amyotrophic Lateral Sclerosis
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Neuritic Beading Induced by Activated Microglia Is an Early Feature of Neuronal Dysfunction Toward Neuronal Death by Inhibition of Mitochondrial Respiration and Axonal Transport
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Immune aging, dysmetabolism, and inflammation in neurological diseases
Deleidi, M., JÃ¤ggle, M., & Rubino, G. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00172 · Cited by 260 · see citing works
Molecular Imaging of Microglial Activation in Amyotrophic Lateral Sclerosis
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Glial cells in amyotrophic lateral sclerosis
Philips, T., & Rothstein, J. D. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.05.015 · Cited by 255 · see citing works
Neuroimaging in amyotrophic lateral sclerosis: insights into structural and functional changes
Chiò, A., Pagani, M., Agosta, F., Calvo, A., Cistaro, A., & Filippi, M. (2014) · The Lancet Neurology · doi:10.1016/s1474-4422(14)70167-x · Cited by 253 · see citing works
Mast cells, glia and neuroinflammation: partners in crime?
Skaper, S. D., Facci, L., & Giusti, P. (2013) · Immunology · doi:10.1111/imm.12170 · Cited by 251 · see citing works
PET Imaging of Neuroinflammation in Neurological Disorders
Kreisl, W., Kim, M.-J., Coughlin, J. M., Henter, I., Owen, D. R., & Innis, R. (2020) · Lancet Neurology · doi:10.1016/s1474-4422(20)30346-x · Cited by 180 · see citing works
Noninvasive Molecular Imaging of Neuroinflammation
Jacobs, A. H., Tavitian, B., & the INMiND consortium (2012) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2012.53 · Cited by 245 · see citing works
TDP-43 activates microglia through NF-κB and NLRP3 inflammasome
Zhao, W., Beers, D. R., Bell, S., Wang, J., Wen, S., Baloh, R. H., & Appel, S. H. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.07.019 · Cited by 241 · see citing works
The methodology of TSPO imaging with positron emission tomography
Turkheimer, F. E., Rizzo, G., Bloomfield, P. S., Howes, O., Zanotti-Fregonara, P., Bertoldo, A., & Veronese, M. (2015) · Biochemical Society Transactions · doi:10.1042/bst20150058 · Cited by 238 · see citing works
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The Role of Immune and Inflammatory Mechanisms in ALS
McCombe, P., & Henderson, R. D. (2011) · Current Molecular Medicine · doi:10.2174/156652411795243450 · Cited by 234 · see citing works
Increased in vivo glial activation in patients with amyotrophic lateral sclerosis: Assessed with [11C]-PBR28
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“This finding is consistent with the first microglial PET study in ALS patients (Turner et al., 2004), as well as histopathological studies reporting increased activated microglia near degenerating motor neurons (Brettschneider et al., 2012; Henkel et al., 2004; Kawamata et al., 1992), suggesting…”
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Diversity and plasticity of microglial cells in psychiatric and neurological disorders
Nakagawa, Y., & Chiba, K. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.06.010 · Cited by 208 · see citing works
Sensitivity and specificity of threshold tracking transcranial magnetic stimulation for diagnosis of amyotrophic lateral sclerosis: a prospective study
Menon, P., Geevasinga, N., Yiannikas, C., Howells, J., Kiernan, M. C., & Vucic, S. (2015) · The Lancet Neurology · doi:10.1016/s1474-4422(15)00014-9 · Cited by 207 · see citing works
The CB2 cannabinoid agonist AM‐1241 prolongs survival in a transgenic mouse model of amyotrophic lateral sclerosis when initiated at symptom onset
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Friends or foes: matrix metalloproteinases and their multifaceted roles in neurodegenerative diseases
Brkic, M., Balusu, S., Libert, C., & Vandenbroucke, R. E. (2015) · Mediators of Inflammation · doi:10.1155/2015/620581 · Cited by 205 · see citing works
Microglia as potential contributors to motor neuron injury in amyotrophic lateral sclerosis
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Functional pattern of brain FDG-PET in amyotrophic lateral sclerosis
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Correlation of Peripheral Immunity With Rapid Amyotrophic Lateral Sclerosis Progression
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Autophagy and ALS: mechanistic insights and therapeutic implications
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Adaptive Immune Neuroprotection in G93A-SOD1 Amyotrophic Lateral Sclerosis Mice
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Multifaceted Role of Matrix Metalloproteinases in Neurodegenerative Diseases: Pathophysiological and Therapeutic Perspectives
Behl, T., Kaur, G., Sehgal, A., Bhardwaj, S., Singh, S., Buhaș, C. L., Pusta, C. T. J., Uivaroșan, D., Munteanu, M. A., & BUNGAU, S. G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22031413 · Cited by 192 · see citing works
Widespread grey matter pathology dominates the longitudinal cerebral MRI and clinical landscape of amyotrophic lateral sclerosis
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The impact of high and low dose ionising radiation on the central nervous system
Betlazar, C., Middleton, R., Banati, R., & Liu, G.-J. (2016) · Redox Biology · doi:10.1016/j.redox.2016.08.002 · Cited by 126 · see citing works
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Translocator Protein-18 kDa (TSPO) Positron Emission Tomography (PET) Imaging and Its Clinical Impact in Neurodegenerative Diseases
Dupont, A.-C., Largeau, B., Santiago Ribeiro, M., Guilloteau, D., Tronel, C., & Arlicot, N. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18040785 · Cited by 182 · see citing works
RETRACTED: Gut-brain axis: A cutting-edge approach to target neurological disorders and potential synbiotic application
Ashique, S., Mohanto, S., Ahmed, M. G., Mishra, N., Garg, A., Chellappan, D. K., Omara, T., Iqbal, S., & Kahwa, I. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e34092 · Cited by 201 · see citing works
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Microglia and C9orf72 in neuroinflammation and ALS and frontotemporal dementia
Lall, D., & Baloh, R. H. (2017) · Journal of Clinical Investigation · doi:10.1172/jci90607 · Cited by 175 · see citing works
Basal ganglia involvement in amyotrophic lateral sclerosis
Bede, P., Elamin, M., Byrne, S., McLaughlin, R. L., Kenna, K. P., Vajda, A., Pender, N. P., Bradley, D. G., & Hardiman, O. M. (2013) · Neurology · doi:10.1212/01.wnl.0000437313.80913.2c · Cited by 177 · see citing works
Inflammation and neurovascular changes in amyotrophic lateral sclerosis
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Characterization of Gene Expression Phenotype in Amyotrophic Lateral Sclerosis Monocytes
Zhao, W., Beers, D. R., Hooten, K. G., Sieglaff, D. H., Zhang, A., Sundaram, S. K., Traini, C., Halsey, W. S., Hughes, A. M., Sathe, G. M., et al. (2017) · JAMA Neurology · doi:10.1001/jamaneurol.2017.0357 · Cited by 176 · see citing works
IL-17A is increased in the serum and in spinal cord CD8 and mast cells of ALS patients
Fiala, M., Chattopadhay, M., Cava, A. L., Tse, E., Liu, G., Lourenço, E. V., Eskin, A., Liu, P. T., Magpantay, L. I., Tse, S., et al. (2010) · Journal of Neuroinflammation · doi:10.1186/1742-2094-7-76 · Cited by 174 · 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
Widespread sensorimotor and frontal cortical atrophy in Amyotrophic Lateral Sclerosis
Großkreutz, J., Kaufmann, J., Frädrich, J., Dengler, R., Heinze, H., & Peschel, T. (2006) · BMC Neurology · doi:10.1186/1471-2377-6-17 · Cited by 172 · see citing works
Brain hypermetabolism in amyotrophic lateral sclerosis: a FDG PET study in ALS of spinal and bulbar onset
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Imaging Microglial Activation During Neuroinflammation and Alzheimer’s Disease
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Mechanisms, models and biomarkers in amyotrophic lateral sclerosis
Turner, M. R., Bowser, R. P., Bruijn, L. I., Dupuis, L., Ludolph, A. C., McGrath, M. S., Manfredi, G., Maragakis, N. J., Miller, R. G., Pullman, S. L., et al. (2013) · Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration · doi:10.3109/21678421.2013.778554 · Cited by 168 · see citing works
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Exosomes: Origins and Therapeutic Potential for Neurodegenerative Disease
Sarko, D. K., & McKinney, C. E. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00082 · Cited by 170 · see citing works
Innate immune activation in neurodegenerative diseases
Castro‐Gomez, S., & Heneka, M. T. (2024) · Immunity · doi:10.1016/j.immuni.2024.03.010 · Cited by 165 · see citing works
The microglial component of amyotrophic lateral sclerosis
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The widening spectrum of C9ORF72-related disease; genotype/phenotype correlations and potential modifiers of clinical phenotype
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The P2X7 Receptor: Central Hub of Brain Diseases
Andrejew, R., Oliveira-Giacomelli, Á., Ribeiro, D. E., Glaser, T., Arnaud-Sampaio, V. F., Lameu, C., & Ulrich, H. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00124 · Cited by 162 · see citing works
11C-DPA-713: A Novel Peripheral Benzodiazepine Receptor PET Ligand for In Vivo Imaging of Neuroinflammation
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
Distinct cerebral lesions in sporadic and ‘D90A’ SOD1 ALS: studies with [11C]flumazenil PET
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Peripheral monocytes are functionally altered and invade the CNS in ALS patients
Zondler, L., Müller, K., Khalaji, S., Bliederhäuser, C., Ruf, W. P., Grozdanov, V., Thiemann, M., Fundel-Clemes, K., Freischmidt, A., Holzmann, K., et al. (2016) · Acta Neuropathologica · doi:10.1007/s00401-016-1548-y · Cited by 154 · see citing works
Glia in the pathogenesis of neurodegenerative diseases
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A TSPO ligand is protective in a mouse model of multiple sclerosis
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Quantifying disease progression in amyotrophic lateral sclerosis
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Authors: Turner, M. R., Cagnin, A., Turkheimer, F. E., Miller, C. C. J., Shaw, C. E., Brooks, D. J., Leigh, P. N., & Banati, R. B.
Affiliations: King's College London (GB)
University of Padua (IT)
Hammersmith Hospital (GB)
Corresponding author: Turner, M.R
ORCID: Turner, M.R
Turkheimer, F.E
Miller, C.C.J
Shaw, C.E
Brooks, D.J
Banati, R.B
Venue: Neurobiology of Disease
Publisher: Elsevier BV
Published: 2004-04
Volume: 15
Issue: 3
Pages: 601-609
ISSN: 0969-9961 (ISSN-L)
DOI: 10.1016/j.nbd.2003.12.012
OpenAlex: W2019706623
Cited by: 737
References: 90
Citations by year: 2026: 15 · 2025: 23 · 2024: 37 · 2023: 31 · 2022: 40 · 2021: 52 · 2020: 52 · 2019: 43 · 2018: 43 · 2017: 44 · 2016: 42 · 2015: 42 · 2014: 47 · 2013: 42 · 2012: 27
FWCI: 15.87
Type: journal article
Language: en
Open access: green
doaj.org
Licence: cc-by-sa
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neurobiology of Disease (publishedVersion)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Research Portal (King's College London) (submittedVersion)
Padua Research Archive (University of Padova) (submittedVersion, other-oa)
Topics: Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
Keywords: amyotrophic lateral sclerosis, microglial activation, [11C]PK11195, positron emission tomography, translocator protein (TSPO), motor cortex, passive optical networks, dorsolateral prefrontal cortex, thalamus, upper motor neuron signs, neuroinflammation, neuropathology
MeSH terms: Adult, Amyotrophic Lateral Sclerosis, Brain, Female, Humans, Isoquinolines, Male, Middle Aged, Tomography, Emission-Computed, Microglia

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Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)-PK11195 positron emission tomography study

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