Imaging robust microglial activation after lipopolysaccharide administration in humans with PET

Neuroinflammation is associated with a broad spectrum of neurodegenerative and psychiatric diseases. The core process in neuroinflammation is activation of microglia, the innate immune cells of the brain. We measured the neuroinflammatory response produced by a systemic administration of theEscheric...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 112; no. 40; pp. 12468 - 12473
Main Authors Sandiego, Christine M., Gallezot, Jean-Dominique, Pittman, Brian, Nabulsi, Nabeel, Lim, Keunpoong, Lin, Shu-Fei, Matuskey, David, Lee, Jae-Yun, O’Connor, Kevin C., Huang, Yiyun, Carson, Richard E., Hannestad, Jonas, Cosgrove, Kelly P.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 06.10.2015
National Acad Sciences
Subjects
Acetamides - metabolism
Acetamides - pharmacokinetics
Adult
Binding sites
Biological Sciences
Biomarkers
Biomarkers - metabolism
Brain - immunology
Brain - metabolism
Carbon Radioisotopes - metabolism
Carbon Radioisotopes - pharmacokinetics
Cytokines - blood
Cytokines - metabolism
E coli
Endotoxins
Escherichia coli
Humans
Inflammation
Inflammation Mediators - blood
Inflammation Mediators - metabolism
Lipopolysaccharides - administration & dosage
Lipopolysaccharides - immunology
Male
Microglia - immunology
Microglia - metabolism
Neurodegeneration
Positron-Emission Tomography - methods
Protein Binding
Pyridines - metabolism
Pyridines - pharmacokinetics
Radioactive tracers
Radiopharmaceuticals - metabolism
Radiopharmaceuticals - pharmacokinetics
Receptors, GABA - metabolism
Reproducibility of Results
Tomography
Young Adult
PBR28
cytokines
neuroinflammation
microglia
endotoxin
Online AccessGet full text

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Abstract Neuroinflammation is associated with a broad spectrum of neurodegenerative and psychiatric diseases. The core process in neuroinflammation is activation of microglia, the innate immune cells of the brain. We measured the neuroinflammatory response produced by a systemic administration of theEscherichia colilipopolysaccharide (LPS; also called endotoxin) in humans with the positron emission tomography (PET) radiotracer [11C]PBR28, which binds to translocator protein, a molecular marker that is up-regulated by microglial activation. In addition, inflammatory cytokines in serum and sickness behavior profiles were measured before and after LPS administration to relate brain microglial activation with systemic inflammation and behavior. Eight healthy male subjects each had two 120-min [11C]PBR28 PET scans in 1 d, before and after an LPS challenge. LPS (1.0 ng/kg, i.v.) was administered 180 min before the second [11C]PBR28 scan. LPS administration significantly increased [11C]PBR28 binding 30–60%, demonstrating microglial activation throughout the brain. This increase was accompanied by an increase in blood levels of inflammatory cytokines, vital sign changes, and sickness symptoms, well-established consequences of LPS administration. To our knowledge, this is the first demonstration in humans that a systemic LPS challenge induces robust increases in microglial activation in the brain. This imaging paradigm to measure brain microglial activation with [11C]PBR28 PET provides an approach to test new medications in humans for their putative antiinflammatory effects.
AbstractList Neuroinflammation is associated with a broad spectrum of neurodegenerative and psychiatric diseases. The core process in neuroinflammation is activation of microglia, the innate immune cells of the brain. We measured the neuroinflammatory response produced by a systemic administration of the Escherichia coli lipopolysaccharide (LPS; also called endotoxin) in humans with the positron emission tomography (PET) radiotracer [...C]PBR28, which binds to translocator protein, a molecular marker that is up-regulated by microglial activation. In addition, inflammatory cytokines in serum and sickness behavior profiles were measured before and after LPS administration to relate brain microglial activation with systemic inflammation and behavior. Eight healthy male subjects each had two 120-min [...C]PBR28 PET scans in 1 d, before and after an LPS challenge. LPS (1.0 ng/kg, i.v.) was administered 180 min before the second [...C]PBR28 scan. LPS administration significantly increased [...C]PBR28 binding 30-60%, demonstrating microglial activation throughout the brain. This increase was accompanied by an increase in blood levels of inflammatory cytokines, vital sign changes, and sickness symptoms, well-established consequences of LPS administration. To our knowledge, this is the first demonstration in humans that a systemic LPS challenge induces robust increases in microglial activation in the brain. This imaging paradigm to measure brain microglial activation with [...C]PBR28 PET provides an approach to test new medications in humans for their putative antiinflammatory effects. (ProQuest: ... denotes formulae/symbols omitted.)
Neuroinflammation is associated with a broad spectrum of neurodegenerative and psychiatric diseases. The core process in neuroinflammation is activation of microglia, the innate immune cells of the brain. We measured the neuroinflammatory response produced by a systemic administration of theEscherichia colilipopolysaccharide (LPS; also called endotoxin) in humans with the positron emission tomography (PET) radiotracer [11C]PBR28, which binds to translocator protein, a molecular marker that is up-regulated by microglial activation. In addition, inflammatory cytokines in serum and sickness behavior profiles were measured before and after LPS administration to relate brain microglial activation with systemic inflammation and behavior. Eight healthy male subjects each had two 120-min [11C]PBR28 PET scans in 1 d, before and after an LPS challenge. LPS (1.0 ng/kg, i.v.) was administered 180 min before the second [11C]PBR28 scan. LPS administration significantly increased [11C]PBR28 binding 30–60%, demonstrating microglial activation throughout the brain. This increase was accompanied by an increase in blood levels of inflammatory cytokines, vital sign changes, and sickness symptoms, well-established consequences of LPS administration. To our knowledge, this is the first demonstration in humans that a systemic LPS challenge induces robust increases in microglial activation in the brain. This imaging paradigm to measure brain microglial activation with [11C]PBR28 PET provides an approach to test new medications in humans for their putative antiinflammatory effects.
Neuroinflammation is a brain immune response that is associated with neurodegenerative diseases and is primarily driven by activation of microglia, the brain’s resident macrophages. Dysfunctional microglial activation may contribute to the behavioral changes observed in neurodegenerative diseases. Upon activation, microglia express translocator protein, which can be imaged with the radiotracer [ 11 C]PBR28 and positron emission tomography (PET) in the living human brain. We imaged healthy human subjects with [ 11 C]PBR28 and PET before and after i.v. administration of lipopolysaccharide (LPS), a potent immune activator. LPS produced a marked increase in brain microglial activation, peripheral inflammatory cytokine levels, and self-reported sickness symptoms. This imaging paradigm can provide a direct approach to test new medications for their potential to reduce acute neuroinflammation. Neuroinflammation is associated with a broad spectrum of neurodegenerative and psychiatric diseases. The core process in neuroinflammation is activation of microglia, the innate immune cells of the brain. We measured the neuroinflammatory response produced by a systemic administration of the Escherichia coli lipopolysaccharide (LPS; also called endotoxin) in humans with the positron emission tomography (PET) radiotracer [ 11 C]PBR28, which binds to translocator protein, a molecular marker that is up-regulated by microglial activation. In addition, inflammatory cytokines in serum and sickness behavior profiles were measured before and after LPS administration to relate brain microglial activation with systemic inflammation and behavior. Eight healthy male subjects each had two 120-min [ 11 C]PBR28 PET scans in 1 d, before and after an LPS challenge. LPS (1.0 ng/kg, i.v.) was administered 180 min before the second [ 11 C]PBR28 scan. LPS administration significantly increased [ 11 C]PBR28 binding 30–60%, demonstrating microglial activation throughout the brain. This increase was accompanied by an increase in blood levels of inflammatory cytokines, vital sign changes, and sickness symptoms, well-established consequences of LPS administration. To our knowledge, this is the first demonstration in humans that a systemic LPS challenge induces robust increases in microglial activation in the brain. This imaging paradigm to measure brain microglial activation with [ 11 C]PBR28 PET provides an approach to test new medications in humans for their putative antiinflammatory effects.
Neuroinflammation is associated with a broad spectrum of neurodegenerative and psychiatric diseases. The core process in neuroinflammation is activation of microglia, the innate immune cells of the brain. We measured the neuroinflammatory response produced by a systemic administration of the Escherichia coli lipopolysaccharide (LPS; also called endotoxin) in humans with the positron emission tomography (PET) radiotracer [11C]PBR28, which binds to translocator protein, a molecular marker that is up-regulated by microglial activation. In addition, inflammatory cytokines in serum and sickness behavior profiles were measured before and after LPS administration to relate brain microglial activation with systemic inflammation and behavior. Eight healthy male subjects each had two 120-min [11C]PBR28 PET scans in 1 d, before and after an LPS challenge. LPS (1.0 ng/kg, i.v.) was administered 180 min before the second [11C]PBR28 scan. LPS administration significantly increased [11C]PBR28 binding 30-60%, demonstrating microglial activation throughout the brain. This increase was accompanied by an increase in blood levels of inflammatory cytokines, vital sign changes, and sickness symptoms, well-established consequences of LPS administration. To our knowledge, this is the first demonstration in humans that a systemic LPS challenge induces robust increases in microglial activation in the brain. This imaging paradigm to measure brain microglial activation with [11C]PBR28 PET provides an approach to test new medications in humans for their putative antiinflammatory effects.Neuroinflammation is associated with a broad spectrum of neurodegenerative and psychiatric diseases. The core process in neuroinflammation is activation of microglia, the innate immune cells of the brain. We measured the neuroinflammatory response produced by a systemic administration of the Escherichia coli lipopolysaccharide (LPS; also called endotoxin) in humans with the positron emission tomography (PET) radiotracer [11C]PBR28, which binds to translocator protein, a molecular marker that is up-regulated by microglial activation. In addition, inflammatory cytokines in serum and sickness behavior profiles were measured before and after LPS administration to relate brain microglial activation with systemic inflammation and behavior. Eight healthy male subjects each had two 120-min [11C]PBR28 PET scans in 1 d, before and after an LPS challenge. LPS (1.0 ng/kg, i.v.) was administered 180 min before the second [11C]PBR28 scan. LPS administration significantly increased [11C]PBR28 binding 30-60%, demonstrating microglial activation throughout the brain. This increase was accompanied by an increase in blood levels of inflammatory cytokines, vital sign changes, and sickness symptoms, well-established consequences of LPS administration. To our knowledge, this is the first demonstration in humans that a systemic LPS challenge induces robust increases in microglial activation in the brain. This imaging paradigm to measure brain microglial activation with [11C]PBR28 PET provides an approach to test new medications in humans for their putative antiinflammatory effects.
Neuroinflammation is associated with a broad spectrum of neurodegenerative and psychiatric diseases. The core process in neuroinflammation is activation of microglia, the innate immune cells of the brain. We measured the neuroinflammatory response produced by a systemic administration of the Escherichia coli lipopolysaccharide (LPS; also called endotoxin) in humans with the positron emission tomography (PET) radiotracer [11C]PBR28, which binds to translocator protein, a molecular marker that is up-regulated by microglial activation. In addition, inflammatory cytokines in serum and sickness behavior profiles were measured before and after LPS administration to relate brain microglial activation with systemic inflammation and behavior. Eight healthy male subjects each had two 120-min [11C]PBR28 PET scans in 1 d, before and after an LPS challenge. LPS (1.0 ng/kg, i.v.) was administered 180 min before the second [11C]PBR28 scan. LPS administration significantly increased [11C]PBR28 binding 30-60%, demonstrating microglial activation throughout the brain. This increase was accompanied by an increase in blood levels of inflammatory cytokines, vital sign changes, and sickness symptoms, well-established consequences of LPS administration. To our knowledge, this is the first demonstration in humans that a systemic LPS challenge induces robust increases in microglial activation in the brain. This imaging paradigm to measure brain microglial activation with [11C]PBR28 PET provides an approach to test new medications in humans for their putative antiinflammatory effects.
Author Lee, Jae-Yun
O’Connor, Kevin C.
Hannestad, Jonas
Nabulsi, Nabeel
Carson, Richard E.
Matuskey, David
Pittman, Brian
Huang, Yiyun
Lim, Keunpoong
Sandiego, Christine M.
Cosgrove, Kelly P.
Gallezot, Jean-Dominique
Lin, Shu-Fei
Author_xml – sequence: 1
  givenname: Christine M.
  surname: Sandiego
  fullname: Sandiego, Christine M.
  organization: PET Center, Diagnostic Radiology, Yale University, New Haven, CT 06520
– sequence: 2
  givenname: Jean-Dominique
  surname: Gallezot
  fullname: Gallezot, Jean-Dominique
  organization: PET Center, Diagnostic Radiology, Yale University, New Haven, CT 06520
– sequence: 3
  givenname: Brian
  surname: Pittman
  fullname: Pittman, Brian
  organization: Department of Psychiatry, Yale University, New Haven, CT 06511
– sequence: 4
  givenname: Nabeel
  surname: Nabulsi
  fullname: Nabulsi, Nabeel
  organization: PET Center, Diagnostic Radiology, Yale University, New Haven, CT 06520
– sequence: 5
  givenname: Keunpoong
  surname: Lim
  fullname: Lim, Keunpoong
  organization: PET Center, Diagnostic Radiology, Yale University, New Haven, CT 06520
– sequence: 6
  givenname: Shu-Fei
  surname: Lin
  fullname: Lin, Shu-Fei
  organization: PET Center, Diagnostic Radiology, Yale University, New Haven, CT 06520
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  givenname: David
  surname: Matuskey
  fullname: Matuskey, David
  organization: PET Center, Diagnostic Radiology, Yale University, New Haven, CT 06520
– sequence: 8
  givenname: Jae-Yun
  surname: Lee
  fullname: Lee, Jae-Yun
  organization: Department of Neurology, Yale University, New Haven, CT 06511
– sequence: 9
  givenname: Kevin C.
  surname: O’Connor
  fullname: O’Connor, Kevin C.
  organization: Department of Neurology, Yale University, New Haven, CT 06511
– sequence: 10
  givenname: Yiyun
  surname: Huang
  fullname: Huang, Yiyun
  organization: PET Center, Diagnostic Radiology, Yale University, New Haven, CT 06520
– sequence: 11
  givenname: Richard E.
  surname: Carson
  fullname: Carson, Richard E.
  organization: PET Center, Diagnostic Radiology, Yale University, New Haven, CT 06520
– sequence: 12
  givenname: Jonas
  surname: Hannestad
  fullname: Hannestad, Jonas
  organization: UCB Pharma, Braine-l’Alleud, Belgium
– sequence: 13
  givenname: Kelly P.
  surname: Cosgrove
  fullname: Cosgrove, Kelly P.
  organization: PET Center, Diagnostic Radiology, Yale University, New Haven, CT 06520
BackLink https://www.ncbi.nlm.nih.gov/pubmed/26385967$$D View this record in MEDLINE/PubMed
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Author contributions: J.H. and K.P.C. designed research; C.M.S., N.N., K.L., S.-F.L., D.M., J.-Y.L., K.C.O., Y.H., R.E.C., and K.P.C. performed research; C.M.S., J.-D.G., and B.P. analyzed data; D.M. is the medical doctor (M.D.) on study; K.C.O. provided immunology expertise; Y.H. senior radiochemist; R.E.C. checked analysis and helped with writing; and C.M.S. and K.P.C. wrote the paper.
Edited by Joanna S. Fowler, Brookhaven National Laboratory, Upton, NY, and approved August 4, 2015 (received for review June 4, 2015)
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Snippet Neuroinflammation is associated with a broad spectrum of neurodegenerative and psychiatric diseases. The core process in neuroinflammation is activation of...
Neuroinflammation is a brain immune response that is associated with neurodegenerative diseases and is primarily driven by activation of microglia, the brain’s...
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StartPage 12468
SubjectTerms Acetamides - metabolism
Acetamides - pharmacokinetics
Adult
Binding sites
Biological Sciences
Biomarkers
Biomarkers - metabolism
Brain - immunology
Brain - metabolism
Carbon Radioisotopes - metabolism
Carbon Radioisotopes - pharmacokinetics
Cytokines - blood
Cytokines - metabolism
E coli
Endotoxins
Escherichia coli
Humans
Inflammation
Inflammation Mediators - blood
Inflammation Mediators - metabolism
Lipopolysaccharides - administration & dosage
Lipopolysaccharides - immunology
Male
Microglia - immunology
Microglia - metabolism
Neurodegeneration
Positron-Emission Tomography - methods
Protein Binding
Pyridines - metabolism
Pyridines - pharmacokinetics
Radioactive tracers
Radiopharmaceuticals - metabolism
Radiopharmaceuticals - pharmacokinetics
Receptors, GABA - metabolism
Reproducibility of Results
Tomography
Young Adult
Title Imaging robust microglial activation after lipopolysaccharide administration in humans with PET
URI https://www.jstor.org/stable/26465378
http://www.pnas.org/content/112/40/12468.abstract
https://www.ncbi.nlm.nih.gov/pubmed/26385967
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https://www.proquest.com/docview/1720451434
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https://pubmed.ncbi.nlm.nih.gov/PMC4603509
Volume 112
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