Noninvasive Molecular Imaging of Neuroinflammation

Jacobs, Andreas H; Tavitian, Bertrand; the INMiND consortium

doi:10.1038/jcbfm.2012.53

Cited by 245Neuroinflammation and Neurodegeneration MechanismsMedical Imaging Techniques and ApplicationsNeurological Disease Mechanisms and Treatments

Noninvasive Molecular Imaging of Neuroinflammation

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Jacobs, Andreas H, Tavitian, Bertrand, the INMiND consortium·2012·Journal of Cerebral Blood Flow & Metabolism

DOI 10.1038/jcbfm.2012.53PMC PMC3390799

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Abstract

Inflammation is a highly dynamic and complex adaptive process to preserve and restore tissue homeostasis. Originally viewed as an immune-privileged organ, the central nervous system (CNS) is now recognized to have a constant interplay with the innate and the adaptive immune systems, where resident microglia and infiltrating immune cells from the periphery have important roles. Common diseases of the CNS, such as stroke, multiple sclerosis (MS), and neurodegeneration, elicit a neuroinflammatory response with the goal to limit the extent of the disease and to support repair and regeneration. However, various disease mechanisms lead to neuroinflammation (NI) contributing to the disease process itself. Molecular imaging is the method of choice to try to decipher key aspects of the dynamic interplay of various inducers, sensors, transducers, and effectors of the orchestrated inflammatory response in vivo in animal models and patients. Here, we review the basic principles of NI with emphasis on microglia and common neurologic disease mechanisms, the molecular targets which are being used and explored for imaging, and molecular imaging of NI in frequent neurologic diseases, such as stroke, MS, neurodegeneration, epilepsy, encephalitis, and gliomas.

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The spatial distribution of neuroinflammation is dependent on the deposition of protein aggregates specific to each disease.
“First, the spatial distribution of neuroinflammation is dependent on the deposition of protein aggregates specific to each disease [107].”
From Glial contributions to neurodegeneration in tauopathies (2017) · cites this paper as [107]
Signals secreted by microglia, such as IL-1β, TNF-α, IL-6, and C1q, co-activate astrocytes leading to neuronal dysfunction and death.
“Furthermore, signals secreted by microglia, such as IL-1β, TNF-α, IL-6, and C1q have been shown to co-activate astrocytes leading to neuronal dysfunction and death [107].”
From Glial contributions to neurodegeneration in tauopathies (2017) · cites this paper as [107]

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Gulyás, B. Z., Pavlova, E. L., Kása, P., Gulya, K., Bakota, L., Várszegi, S., Keller, É., Horváth, M. C., Nag, S., Hermecz, I., et al. (2010) · Neurochemistry International · doi:10.1016/j.neuint.2010.10.013 · Cited by 203 · see citing works
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
Intracellular Nanoparticle Coating Stability Determines Nanoparticle Diagnostics Efficacy and Cell Functionality
Soenen, S. J., Himmelreich, U., Nuytten, N., Pisanic, T. R., Ferrari, A., & Cuyper, M. D. (2010) · Small · doi:10.1002/smll.201000763 · Cited by 189 · see citing works
Minocycline 1‐year therapy in multiple‐system‐atrophy: Effect on clinical symptoms and [ 11 C] (R) ‐PK11195 PET (MEMSA‐trial)
Dodel, R. C., Spottke, A. E., Gerhard, A., Reuß, A., Reinecker, S., Schimke, N., Trenkwalder, C., Sixel‐Döring, F., Herting, B., Kamm, C., et al. (2009) · Movement Disorders · doi:10.1002/mds.22732 · Cited by 187 · see citing works
In vivo detection of microglial activation in frontotemporal dementia
Cagnin, A., Rossor, M., Sampson, E. L., MacKinnon, T., & Banati, R. B. (2004) · Annals of Neurology · doi:10.1002/ana.20332 · Cited by 187 · cited 1× · see citing works
“In patients with frontotemporal dementia, PET showed [11C](R)PK11195 binding in the frontal, medial temporal, and subcortical regions (Cagnin et al, 2004).”
Background
Pluriformity of inflammation in multiple sclerosis shown by ultra-small iron oxide particle enhancement
Vellinga, M. M., Oude Engberink, R. D., Seewann, A., Pouwels, P. J. W., Wattjes, M. P., van der Pol, S. M. A., Pering, C., Polman, C. H., de Vries, H. E., Geurts, J. J. G., et al. (2008) · Brain · doi:10.1093/brain/awn009 · Cited by 183 · see citing works
[11C]-PK11195 PET: Quantification of neuroinflammation and a monitor of anti-inflammatory treatment in Parkinson's disease?
Bartels, A. L., Willemsen, A. T. M., Doorduin, J., de Vries, E. F. J., Dierckx, R. A., & Leenders, K. L. (2009) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2009.05.005 · Cited by 181 · see citing works
PET imaging with [11C]PBR28 can localize and quantify upregulated peripheral benzodiazepine receptors associated with cerebral ischemia in rat
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Toll‐like receptors 2 and 4 mediate Aβ(1–42) activation of the innate immune response in a human monocytic cell line
Udan, M. L. D., Ajit, D., Crouse, N. R., & Nichols, M. R. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.05001.x · Cited by 175 · see citing works
In vivo changes in microglial activation and amyloid deposits in brain regions with hypometabolism in Alzheimer’s disease
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Adoptive Immunotherapy of Experimental Autoimmune Encephalomyelitis Via T Cell Delivery of the IL-12 p40 Subunit
Costa, G. L., Sandora, M. R., Nakajima, A., et al. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.4.2379 · Cited by 172 · see citing works
In vivo visualization of activated glia by[11C] (R)-PK11195-PET following herpes encephalitis reveals projected neuronal damage beyond the primary focal lesion
Cagnin, A. (2001) · Brain · doi:10.1093/brain/124.10.2014 · Cited by 169 · see citing works
The Temporal Dynamics of Poststroke Neuroinflammation: A Longitudinal Diffusion Tensor Imaging–Guided PET Study with 11C-PK11195 in Acute Subcortical Stroke
Thiel, A., Radlinska, B. A., Paquette, C., Sidel, M., Soucy, J., Schirrmacher, R., & Minuk, J. (2010) · Journal of Nuclear Medicine · doi:10.2967/jnumed.110.076612 · Cited by 167 · see citing works
Taking Advantage of the Systemic Immune System to Cure Brain Diseases
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Positron emission tomography-based imaging of transgene expression mediated by replication-conditional, oncolytic herpes simplex virus type 1 mutant vectors in vivo.
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Microglial Involvement in Neuroplastic Changes Following Focal Brain Ischemia in Rats
Madinier, A., Bertrand, N., Mossiat, C. M., Prigent‐Tessier, A., Beley, A., Marie, C., & Garnier, P. E. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008101 · Cited by 154 · see citing works
Evidence of activated microglia in focal cortical dysplasia
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Imaging Brain Inflammation with [11C]PK11195 by PET and Induction of the Peripheral-Type Benzodiazepine Receptor after Transient Focal Ischemia in Rats
Rojas, S., Martín, A., Arranz, M. J., Pareto, D., Purroy, J., Verdaguer, E., Llop, J., Gómez‐Vallejo, V., Gispert, J. D., Milián, O., et al. (2007) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600500 · Cited by 146 · see citing works
Positron emission tomography imaging and clinical progression in relation to molecular pathology in the first Pittsburgh Compound B positron emission tomography patient with Alzheimer’s disease
Kadir, A., Marutle, A., Gonzalez, D., Schöll, M., Almkvist, O., Mousavi, M. T., Mustafiz, T., Darreh‐Shori, T., Nennesmo, I., & Nordberg, A. K. (2010) · Brain · doi:10.1093/brain/awq349 · Cited by 139 · see citing works
PK11195 labels activated microglia in Alzheimer's disease and in vivo in a mouse model using PET
Venneti, S., Lopresti, B. J., Wang, G., Hamilton, R. L., Mathis, C. A., Klunk, W. E., Apte, U. M., & Wiley, C. A. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.11.005 · Cited by 138 · see citing works
Radiolabelled Molecules for Imaging the Translocator Protein (18 kDa) Using Positron Emission Tomography
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Live Imaging of Neuroinflammation Reveals Sex and Estrogen Effects on Astrocyte Response to Ischemic Injury
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Microglia dynamics and function in the CNS
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[11C]-DPA-713 and [18F]-DPA-714 as New PET Tracers for TSPO: A Comparison with [11C]-(R)-PK11195 in a Rat Model of Herpes Encephalitis
Doorduin, J., Klein, H. C., Dierckx, R., James, M. L., Kassiou, M., & de Vries, E. F. J. (2009) · Molecular Imaging and Biology · doi:10.1007/s11307-009-0211-6 · Cited by 131 · see citing works
Inflammatory Response After Ischemic Stroke
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Neuroinflammation Extends Brain Tissue at Risk to Vital Peri-Infarct Tissue: A Double Tracer [ 11 C]PK11195- and [ 18 F]FDG-PET Study
Schroeter, M., Dennin, M. A., Walberer, M., Backes, H., Neumaier, B., Fink, G. R., & Graf, R. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.36 · Cited by 129 · see citing works
Neuronal regulation of immune responses in the central nervous system
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Microglial imaging with positron emission tomography and atrophy measurements with magnetic resonance imaging in multiple sclerosis: a correlative study
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In Vivo Imaging of64Cu-Labeled Polymer Nanoparticles Targeted to the Lung Endothelium
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Translocator protein (18 kDa)/peripheral benzodiazepine receptor specific ligands induce microglia functions consistent with an activated state
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Functional and Molecular Ultrasound Imaging: Concepts and Contrast Agents
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Functional Coexpression of HSV-1 Thymidine Kinase and Green Fluorescent Protein: Implications for Noninvasive Imaging of Transgene Expression
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Glia-dependent TGF-β signaling, acting independently of the TH17 pathway, is critical for initiation of murine autoimmune encephalomyelitis
Luo, J., Ho, P. P.-K., Buckwalter, M. S., Hsu, T., Lee, L. Y., Zhang, H., Kim, D., Kim, S., Gambhir, S. S., Steinman, L., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31763 · Cited by 115 · see citing works
Imaging Microglial/Macrophage Activation in Spinal Cords of Experimental Autoimmune Encephalomyelitis Rats by Positron Emission Tomography Using the Mitochondrial 18 kDa Translocator Protein Radioligand [18F]DPA-714
Abourbeh, G., Thezé, B., Maroy, R., Dubois, A., Brulon, V., Fontyn, Y., Dollé, F., Tavitian, B., & Boisgard, R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2900-11.2012 · Cited by 112 · see citing works
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In vivo imaging of neuroinflammation
Cagnin, A. (2002) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(02)00107-4 · Cited by 110 · see citing works
Myeloperoxidase-targeted imaging of active inflammatory lesions in murine experimental autoimmune encephalomyelitis
Chen, J. W., Breckwoldt, M. O., Aikawa, E. R., Chiang, G. C.-Y., & Weissleder, R. (2008) · Brain · doi:10.1093/brain/awn004 · Cited by 110 · see citing works
Synthesis and biodistribution of [11C]A-836339, a new potential radioligand for PET imaging of cannabinoid type 2 receptors (CB2)
Horti, A. G., Gao, Y., Ravert, H. T., Finley, P. A., Valentine, H., Wong, D. F., Endres, C. J., Savonenko, A. V., & Dannals, R. F. (2010) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2010.05.058 · Cited by 108 · see citing works
Image-guided, noninvasive, spatiotemporal control of gene expression
Deckers, R., Quesson, B., Arsaut, J., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806936106 · Cited by 102 · see citing works
Treatment with minocycline after disease onset alters astrocyte reactivity and increases microgliosis in SOD1 mutant mice
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Calpain 2 Controls Turnover of LFA-1 Adhesions on Migrating T Lymphocytes
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Novel Reference Region Model Reveals Increased Microglial and Reduced Vascular Binding of 11C-(R)-PK11195 in Patients with Alzheimer's Disease
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
PET/CT in diagnosis of dementia
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The translocator protein ligand [18F]DPA-714 images glioma and activated microglia in vivo
Winkeler, A., Boisgard, R., Awde, A. R., Dubois, A., Thezé, B., Zheng, J., Ciobanu, L., Dollé, F., Viel, T., Jacobs, A. H., et al. (2012) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-011-2041-4 · Cited by 95 · see citing works
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In Vivo Expression of Cyclooxygenase-1 in Activated Microglia and Macrophages During Neuroinflammation Visualized by PET with 11C-Ketoprofen Methyl Ester
Shukuri, M., Takashima‐Hirano, M., Tokuda, K., Takashima, T., Matsumura, K., Inoue, O., Doi, H., Suzuki, M., Watanabe, Y., & Onoe, H. (2011) · Journal of Nuclear Medicine · doi:10.2967/jnumed.110.084046 · Cited by 93 · see citing works
Quantitative Autoradiographic Mapping of Herpes Simplex Virus Encephalitis with a Radiolabeled Antiviral Drug
Saito, Y., Price, R. W., Rottenberg, D. A., et al. (1982) · Science · doi:10.1126/science.7112121 · Cited by 88 · see citing works
Positron emission tomography with computed tomography imaging of neuroinflammation in experimental autoimmune encephalomyelitis
Radu, C. G., Shu, C. J., Shelly, S. M., Phelps, M. E., & Witte, O. N. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610544104 · Cited by 87 · see citing works
Evaluation of [11C]rofecoxib as PET tracer for cyclooxygenase 2 overexpression in rat models of inflammation
de Vries, E. F. J., Doorduin, J., Dierckx, R., & van Waarde, A. (2007) · Nuclear Medicine and Biology · doi:10.1016/j.nucmedbio.2007.07.015 · Cited by 87 · see citing works
Imaging Inflammation in a Patient with Epilepsy Due to Focal Cortical Dysplasia
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Molecular and cellular immune mediators of neuroprotection
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In vivo imaging
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Molecular Magnetic Resonance Imaging of Acute Vascular Cell Adhesion Molecule-1 Expression in a Mouse Model of Cerebral Ischemia
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Imipramine, in Part through Tumor Necrosis Factor α Inhibition, Prevents Cognitive Decline and β-Amyloid Accumulation in a Mouse Model of Alzheimer's Disease
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In vivo imaging of neuroinflammation: a comparative study between [18F]PBR111, [11C]CLINME and [11C]PK11195 in an acute rodent model
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Two-photon laser scanning microscopy imaging of intact spinal cord and cerebral cortex reveals requirement for CXCR6 and neuroinflammation in immune cell infiltration of cortical injury sites
Kim, J. V., Jiang, N., Tadokoro, C. E., Liu, L., Ransohoff, R. M., Lafaille, J. J., & Dustin, M. L. (2009) · Journal of Immunological Methods · doi:10.1016/j.jim.2009.09.007 · Cited by 72 · see citing works
Synthesis and biological evaluation of carbon-11- and fluorine-18-labeled 2-oxoquinoline derivatives for type 2 cannabinoid receptor positron emission tomography imaging
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Functional neuroimaging in multiple sclerosis with radiolabelled glia markers: Preliminary comparative PET studies with [11C]vinpocetine and [11C]PK11195 in patients
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
Radioisotopic Imaging of Neuroinflammation: FIGURE 1.
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Early-Stage Investigations of Ultrasmall Superparamagnetic Iron Oxide-Induced Signal Change After Permanent Middle Cerebral Artery Occlusion in Mice
Desestret, V., Brisset, J., Moucharrafie, S., Devillard, E., Nataf, S., Honnorat, J., Nighoghossian, N., Berthezène, Y., & Wiart, M. (2009) · Stroke · doi:10.1161/strokeaha.108.531269 · Cited by 69 · see citing works
Multimodal microglia imaging of fiber tracts in acute subcortical stroke
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125I-Labeled Gold Nanorods for Targeted Imaging of Inflammation
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Novel Fluorinated Derivatives of the Broad-Spectrum MMP Inhibitors N-Hydroxy-2(R)-[[(4-methoxyphenyl)sulfonyl](benzyl)- and (3-picolyl)-amino]-3-methyl-butanamide as Potential Tools for the Molecular Imaging of Activated MMPs with PET
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Reduced PBR/TSPO Expression After Minocycline Treatment in a Rat Model of Focal Cerebral Ischemia: A PET Study Using [18F]DPA-714
Martín, A., Boisgard, R., Kassiou, M., Dollé, F., & Tavitian, B. (2010) · Molecular Imaging and Biology · doi:10.1007/s11307-010-0324-y · Cited by 68 · see citing works
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In Vivo Analysis of Uropod Function during Physiological T Cell Trafficking
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Toll-like receptors 7 and 8 expression is associated with poor outcome and greater inflammatory response in acute ischemic stroke
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Methods to monitor gene therapy with molecular imaging
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Non-invasive visualization of CNS inflammation with nuclear and optical imaging
Wunder, A. P., Klohs, J., & Dirnagl, U. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.10.005 · Cited by 64 · see citing works
In Vivo Imaging Reveals Distinct Inflammatory Activity of CNS Microglia versus PNS Macrophages in a Mouse Model for ALS
Dibaj, P., Steffens, H., Zschüntzsch, J., Nadrigny, F., Schomburg, E. D., Kirchhoff, F., & Neusch, C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017910 · Cited by 63 · see citing works
Quantitative Preclinical Imaging of TSPO Expression in Glioma Using N,N-Diethyl-2-(2-(4-(2-18F-Fluoroethoxy)Phenyl)-5,7-Dimethylpyrazolo[1,5-a]Pyrimidin-3-yl)Acetamide
Tang, D., Hight, M. R., McKinley, E. T., Fu, A., Buck, J. R., Smith, R. A., Tantawy, M. N., Peterson, T. E., Colvin, D. C., Ansari, M. S., et al. (2012) · Journal of Nuclear Medicine · doi:10.2967/jnumed.111.095653 · Cited by 63 · see citing works
Neuron-Microglia Dialogue and Hippocampal Neurogenesis in the Aged Brain.
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Translocator protein (18 kDa) is involved in the regulation of reactive gliosis
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Knocking at the brain’s door: intravital two-photon imaging of autoreactive T cell interactions with CNS structures
Kawakami, N., & Flügel, A. (2010) · Seminars in Immunopathology · doi:10.1007/s00281-010-0216-x · Cited by 62 · see citing works
Bioluminescence in vivo imaging of autoimmune encephalomyelitis predicts disease
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In vivo imaging of neuroinflammation in the rodent brain with [11C]SSR180575, a novel indoleacetamide radioligand of the translocator protein (18 kDa)
Chauveau, F., Boutin, H., Camp, N. V., Thominiaux, C., Hantraye, P., Rivron, L., Marguet, F., Castel, M., Rooney, T., Bénavidès, J., et al. (2010) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-010-1628-5 · Cited by 61 · see citing works
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Quantitative, Preclinical PET of Translocator Protein Expression in Glioma Using 18F-N-Fluoroacetyl-N-(2,5-Dimethoxybenzyl)-2-Phenoxyaniline
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A PET Brain Reporter Gene System Based on Type 2 Cannabinoid Receptors
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Positron emission tomography imaging of peripheral benzodiazepine receptor binding in human immunodeficiency virus–infected subjects with and without cognitive impairment
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Authors: Jacobs, A. H., Tavitian, B., & the INMiND consortium
Affiliations: University of Münster (DE)
Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
Corresponding author: Jacobs, Andreas H
ORCID: Jacobs, Andreas H
Tavitian, Bertrand
Venue: Journal of Cerebral Blood Flow & Metabolism
Publisher: SAGE Publications
Published: 2012-05-02
Volume: 32
Issue: 7
Pages: 1393-1415
ISSN: 0271-678X (ISSN-L)
1559-7016
DOI: 10.1038/jcbfm.2012.53
PMC: PMC3390799
OpenAlex: W2158232675
Cited by: 245
References: 188
Citations by year: 2026: 3 · 2025: 8 · 2024: 8 · 2023: 7 · 2022: 7 · 2021: 23 · 2020: 20 · 2019: 17 · 2018: 30 · 2017: 27 · 2016: 23 · 2015: 26 · 2014: 27 · 2013: 17 · 2012: 2
FWCI: 2.14
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
journals.sagepub.com/page/policies/text-and-data-mining-license (tdm)
Locations: Journal of Cerebral Blood Flow & Metabolism (publishedVersion, cc-by-nc-nd)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Open Repository and Bibliography (University of Luxembourg) (submittedVersion, cc-by-nc-nd)
Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by-nc-nd)
Lirias (KU Leuven) (submittedVersion)
Pure Amsterdam UMC (submittedVersion)
Research Explorer (The University of Manchester) (submittedVersion)
URN:NBN Resolver for Germany & Switzerland (German National Library) (submittedVersion, cc-by-nc-nd)
Data Archiving and Networked Services (DANS) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders: University of Southampton
Imperial College London
University of Manchester
University of Sydney
Universiteit van Amsterdam
Semmelweis Egyetem
Gentofte Hospital
Karolinska Institutet
Turun Yliopisto
Université François-Rabelais
Universiteit Antwerpen
Paracelsus Medizinische Privatuniversität
Institut d’Investigacions Biomèdiques August Pi i Sunyer, Universitat de Barcelona
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Medical Imaging Techniques and Applications
Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
Keywords: neuroinflammation, noninvasive molecular imaging, microglia, central nervous system, stroke, multiple sclerosis, neurodegeneration, epilepsy, encephalitis, glioma
MeSH terms: Animals, Brain, Humans, Inflammation, Spinal Cord, Molecular Imaging, Neuroimaging

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