Increased in vivo glial activation in patients with amyotrophic lateral sclerosis: Assessed with [11C]-PBR28
Open accessAbstract
Evidence from human post mortem, in vivo and animal model studies implicates the neuroimmune system and activated microglia in the pathology of amyotrophic lateral sclerosis. The study aim was to further evaluate in vivo neuroinflammation in individuals with amyotrophic lateral sclerosis using [(11)C]-PBR28 positron emission tomography. Ten patients with amyotrophic lateral sclerosis (seven males, three females, 38-68 years) and ten age- and [(11)C]-PBR28 binding affinity-matched healthy volunteers (six males, four females, 33-65 years) completed a positron emission tomography scan. Standardized uptake values were calculated from 60 to 90 min post-injection and normalized to whole brain mean. Voxel-wise analysis showed increased binding in the motor cortices and corticospinal tracts in patients with amyotrophic lateral sclerosis compared to healthy controls (p FWE < 0.05). Region of interest analysis revealed increased [(11)C]-PBR28 binding in the precentral gyrus in patients (normalized standardized uptake value = 1.15) compared to controls (1.03, p < 0.05). In patients those values were positively correlated with upper motor neuron burden scores (r = 0.69, p < 0.05), and negatively correlated with the amyotrophic lateral sclerosis functional rating scale (r = -0.66, p < 0.05). Increased in vivo glial activation in motor cortices, that correlates with phenotype, complements previous histopathological reports. Further studies will determine the role of [(11)C]-PBR28 as a marker of treatments that target neuroinflammation.
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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 [312]
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BackgroundThe neuroinflammatory component of negative affect in patients with chronic pain
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“tex, extra-motor frontotemporal areas, thalamus, midbrain, pons, and subcortical WM of patients with ALS [73,74].”
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Update on recent advances in amyotrophic lateral sclerosis
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“…Suridjan et al, 2015; Varrone et al, 2015; Yasuno et al, 2008, 2012), Lewy body dementia (Surendranathan et al, 2015), amyotrophic lateral sclerosis (Zurcher et al, 2015), stroke (Lartey et al, 2014), and non-smokers with major depression (Setiawan et al, 2015), but not Parkinson’s disease…”
BackgroundMethodImmune mechanisms and shared immune targets in neurodegenerative diseases
Weiner, H. L. (2024) · Nature Reviews Neurology · doi:10.1038/s41582-024-01046-7 · Cited by 63 · see citing works
“TSPO PET has revealed microglial activation 50,51 in cortical and subcortical structures in the brain of people with ALS, and this activation was also apparent in people who were carriers of SOD1 mutations but were presymptomatic 52 .”
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Self-citationUltra high-field (7tesla) magnetic resonance spectroscopy in Amyotrophic Lateral Sclerosis
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Self-citationTSPO Versus P2X7 as a Target for Neuroinflammation: An In Vitro and In Vivo Study
Weehaeghe, D. V., Schoor, E. V., Vocht, J. D., Koole, M. J. B., Attili, B. N. N. R., Celen, S., Declercq, L., Thal, D. R., Damme, P. V., Bormans, G. M., et al. (2019) · Journal of Nuclear Medicine · doi:10.2967/jnumed.119.231985 · Cited by 58 · see citing works
The involvement of NLRP3 inflammasome in the treatment of neurodegenerative diseases
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“More recent studies involving second-generation TSPO tracers, that is, (18)F-DPA-714 and (11)C-PBR28, confirmed increased microglial activation in primary motor and supplementary motor cortices, which correlated with markers of degeneration in the same regions, including atrophy and white matter changes,(65) and with…”
BackgroundSelvaraj, S., Bloomfield, P. S., Bo, C., Veronese, M., Turkheimer, F., & Howes, O. (2017) · Schizophrenia Research · doi:10.1016/j.schres.2017.08.063 · Cited by 50 · see citing works
“…inter- subject blood binding, typical of TSPO targeting tracers (Albrecht et al., 2016; Lockhart et al., 2003; Turkheimer et al., 2015b), regional distribution volume estimates were normalized for whole brain activity in agreement with previous studies (Loggia et al., 2015; Zürcher et al., 2015).”
ResultMarshall, J., Nietupski, J. B., Park, H. J., Cao, J. H., Bangari, D. S., Silvescu, C. I., Wilper, T., Randall, K. L., Tietz, D., Wang, B., et al. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2019.05.018 · Cited by 55 · see citing works
Neuroepigenetic signatures of age and sex in the living human brain
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Self-citationInterplay between immunity and amyotrophic lateral sclerosis: Clinical impact
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Self-citationEvidence for an early innate immune response in the motor cortex of ALS
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Principles of Simultaneous PET/MR Imaging
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“Moreover, our findings are in agreement with those of previous studies in humans showing an increased [(11)C](R)PK11195 PET signal in the pons of ALS patients [22], and with those of a more recent study showing increased PBR28 uptake in the brainstem of individuals with bulbar-onset ALS [24].”
BackgroundResultKinetic modeling and parameter estimation of TSPO PET imaging in the human brain
Wimberley, C., Lavisse, S., Hillmer, A. T., Hinz, R., Turkheimer, F., & Zanotti‐Fregonara, P. (2021) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-021-05248-9 · Cited by 49 · see citing works
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“Prolonged glial cell accumulation surrounding motor neurons in the spinal cord of wobbler mice, rats, and mice expressing the ALS-linked SOD1 mutation and even in post mortem studies is also well established to proceed the degeneration and subsequent paralysis of affected animals and ALS patients [34, 39, 40].”
BackgroundA PET/CT approach to spinal cord metabolism in amyotrophic lateral sclerosis
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Pseudoreference Regions for Glial Imaging with 11C-PBR28: Investigation in 2 Clinical Cohorts
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“WB voxelwise SUVR analyses were also performed for comparison with the SUVRWB data previously reported (14,17).”
BackgroundMethodInfluentialSelf-citationAmyotrophic lateral sclerosis: The complement and inflammatory hypothesis
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Thalamic neuroinflammation as a reproducible and discriminating signature for chronic low back pain
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Self-citationNeuroinflammation in amyotrophic lateral sclerosis: pathogenic insights and therapeutic implications
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Ultra-High Field Proton MR Spectroscopy in Early-Stage Amyotrophic Lateral Sclerosis
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Considerations for Amyotrophic Lateral Sclerosis (ALS) Clinical Trial Design
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The Skeletal Muscle Emerges as a New Disease Target in Amyotrophic Lateral Sclerosis
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“As an example, ALS patients carrying SOD1 mutations displayed microglial activation [35,36].”
BackgroundVarghese, A. M., Ghosh, M., Bhagat, S. K., Vijayalakshmi, K., Preethish‐Kumar, V., Vengalil, S., Pradeep-Chandra-Reddy, C., Nashi, S., Polavarapu, K., Sharma, M., et al. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01909-y · Cited by 44 · see citing works
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Positron Emission Tomography Molecular Imaging Biomarkers for Amyotrophic Lateral Sclerosis
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Self-citationSupervised clustering for TSPO PET imaging
Schubert, J., Tonietto, M., Turkheimer, F., Zanotti-Fregonara, P., & Veronese, M. (2021) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-021-05309-z · Cited by 40 · see citing works
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“…been applied in the assessment of neuroinflammation in patients with several neuropathological conditions that are accompanied by cognitive impairment (Batarseh and Papadopoulos, 2010; Colasanti et al., 2014; Rissanen et al., 2014; Suridjan et al., 2015; Zurcher et al., 2015; Wang et al., 2016).”
BackgroundImaging in amyotrophic lateral sclerosis: MRI and PET
Kassubek, J., & Pagani, M. (2019) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000728 · Cited by 40 · see citing works
Gliosis and Neurodegenerative Diseases: The Role of PET and MR Imaging
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Frontotemporal Pathology in Motor Neuron Disease Phenotypes: Insights From Neuroimaging
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Ibudilast (MN-166) in amyotrophic lateral sclerosis- an open label, safety and pharmacodynamic trial
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Self-citationClinical Applications of Small-molecule PET Radiotracers: Current Progress and Future Outlook
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Imaging Translocator Protein as a Biomarker of Neuroinflammation in Dementia
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“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript approaches with a different radioligand without first validating it against kinetic modeling (Bloomfield et al., 2016; Zurcher et al., 2015).”
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A pilot trial of RNS60 in amyotrophic lateral sclerosis
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“Neuroinflammation is increasingly implicated in ALS pathogenesis, including activation of circulating monocytes, lymphocytic infiltration,(14) and microglial activation in the central nervous system (CNS).(7,8) Mouse models of ALS show that activation of microglia and influx of T-lymphocytes into the CNS occur before…”
InfluentialSelf-citationA Novel Interaction of Translocator Protein 18 kDa (TSPO) with NADPH Oxidase in Microglia
Loth, M. K., Guariglia, S. R., Ré, D. B., Perez, J., de Paiva, V. N., McGlothan, J. L., Chambers, J. W., Azzam, D. J., & Guilarte, T. R. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-02042-w · Cited by 35 · see citing works
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Imaging of glia activation in people with primary lateral sclerosis
Paganoni, S., Alshikho, M. J., Zürcher, N. R., Cernasov, P., Babu, S., Loggia, M. L., Chan, J. G. M., Chonde, D. B., Izquierdo‐Garcia, D., Catana, C., et al. (2017) · NeuroImage Clinical · doi:10.1016/j.nicl.2017.10.024 · Cited by 36 · see citing works
“Abbreviations: Ala = alanine; ALSFRS-R = amyotrophic lateral sclerosis functional rating scale revised; HC = healthy control; PLS = primary lateral sclerosis; SD = standard deviation; Thr = threonine; TSPO = translocator protein; UMNB = upper motor neuron burden scale.”
InfluentialSelf-citationArbo, B. D., Benetti, F., García-Segura, L., & Ribeiro, M. (2015) · Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2015.07.007 · Cited by 35 · see citing works
“injury and inflammation, as well as in several neur opathological conditions including stroke and neurodegenerative disorders such as Alzh eimer’s disease (AD), Parkinson’s disease, Huntington’s disease, multiple sclerosis a nd amyotrophic lateral sclerosis [2, 41-43].”
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“Details on the PET acquisition were previously published (7).”
BackgroundSelf-citation
- Authors
- 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.
- Affiliations
- Harvard University (US)
- Corresponding author
- Hooker, Jacob M.
- Atassi, Nazem
- ORCID
- Venue
- NeuroImage: Clinical
- Publisher
- Elsevier BV
- Published
- 2015
- Volume
- 7
- Pages
- 409-414
- ISSN
- 2213-1582 (ISSN-L)
- PMC
- PMC4310932
- OpenAlex
- W1969387798
- Cited by
- 226
- References
- 31
- Citations by year
- 2026: 6 · 2025: 15 · 2024: 27 · 2023: 15 · 2022: 11 · 2021: 26 · 2020: 25 · 2019: 21 · 2018: 19 · 2017: 27 · 2016: 26 · 2015: 8
- FWCI
- 18.79
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- NeuroImage Clinical (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Harvard NeuroDiscovery Center
- Muscular Dystrophy Association
- American Academy of Neurology
- Anne Young Fellowship
- NINDS (1K23NS083715-01A1)
- Topics
- Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- amyotrophic lateral sclerosis, glial activation, neuroinflammation, microglial activation, [11C]PBR28, positron emission tomography, motor cortex, corticospinal tract, ALSFRS-R, neuroimmune system
- MeSH terms
- Acetamides, Adult, Aged, Amyotrophic Lateral Sclerosis, Brain, Carbon Radioisotopes, Female, Humans, Male, Middle Aged, Neuroglia, Pyridines, Radiographic Image Interpretation, Computer-Assisted, 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 ›
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