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Analysis of Fractalkine Receptor CX3CR1 Function by Targeted Deletion and Green Fluorescent Protein Reporter Gene Insertion
Open accessAbstract
The seven-transmembrane receptor CX(3)CR1 is a specific receptor for the novel CX(3)C chemokine fractalkine (FKN) (neurotactin). In vitro data suggest that membrane anchoring of FKN, and the existence of a shed, soluble FKN isoform allow for both adhesive and chemoattractive properties. Expression on activated endothelium and neurons defines FKN as a potential target for therapeutic intervention in inflammatory conditions, particularly central nervous system diseases. To investigate the physiological function of CX(3)CR1-FKN interactions, we generated a mouse strain in which the CX(3)CR1 gene was replaced by a green fluorescent protein (GFP) reporter gene. In addition to the creation of a mutant CX(3)CR1 locus, this approach enabled us to assign murine CX(3)CR1 expression to monocytes, subsets of NK and dendritic cells, and the brain microglia. Analysis of CX(3)CR1-deficient mice indicates that CX(3)CR1 is the only murine FKN receptor. Yet, defying anticipated FKN functions, absence of CX(3)CR1 interferes neither with monocyte extravasation in a peritonitis model nor with DC migration and differentiation in response to microbial antigens or contact sensitizers. Furthermore, a prominent response of CX(3)CR1-deficient microglia to peripheral nerve injury indicates unimpaired neuronal-glial cross talk in the absence of CX(3)CR1.
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“Cx3cr1-CreERT2 developed by Jung et al. (2000) was reported to drive microglia-specific expression.”
From Targeting Microglia Using Cx3cr1-Cre Lines: Revisiting the Specificity (2019) · cites this paper as Jung et al. (2000)
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“The inducible Cx3cr1-CreERT2 line developed by Jung et al. (2000), displayed some basal cre activity without tamoxifen treatment, but this expression was restricted to microglia.”
From Targeting Microglia Using Cx3cr1-Cre Lines: Revisiting the Specificity (2019) · cites this paper as Jung et al. (2000)
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“The inducible Cx3cr1-CreERT2 line developed by Jung et al. (2000), displayed some basal cre activity without tamoxifen treatment, but this expression was restricted to microglia.”
From Targeting Microglia Using Cx3cr1-Cre Lines: Revisiting the Specificity (2019) · cites this paper as Jung et al. (2000)
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“According to the description on The Jackson Laboratory website, the constitutive Cx3cr1-Cre line created by Jung et al. (2000), displays leakiness into neurons when crossed with a yellow fluorescent protein (YFP) reporter line.”
From Targeting Microglia Using Cx3cr1-Cre Lines: Revisiting the Specificity (2019) · cites this paper as Jung et al. (2000)
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“Thus, the cre activity in this line is not fully dependent on tamoxifen.”
From Targeting Microglia Using Cx3cr1-Cre Lines: Revisiting the Specificity (2019) · cites this paper as Jung et al. (2000)
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“The partial tamoxifen-independent cre activity observed in the Cx3cr1-CreERT2 line developed by Jung et al. (2000), indicates potential embryonic deletion of TSC1 in a fraction”
From Targeting Microglia Using Cx3cr1-Cre Lines: Revisiting the Specificity (2019) · cites this paper as Jung et al. (2000)
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“Microglia were labeled using the CX3CR1+/GFP mouse line in which all microglia express EGFP under the control of fractalkine receptor, CX3CR1, expression (Figure 1, S1, and S5) (Cardona et al., 2006; Jung et al., 2000; Saederup et al., 2010).”
From Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner (2012) · cites this paper as Jung et al., 2000
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“CX3CR1 is exclusively expressed by microglia within the brain”
From CX3CR1 Deficiency Alters Microglial Activation and Reduces Beta-Amyloid Deposition in Two Alzheimer's Disease Mouse Models (2010) · cites this paper as [15]
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“If the YFP reporter line has no spontaneous leakiness, then the constitutive Cx3cr1-Cre line developed by Jung et al. (2000), and which is now available at The Jackson Laboratory, is not microglia specific.”
From Targeting Microglia Using Cx3cr1-Cre Lines: Revisiting the Specificity (2019) · cites this paper as Jung et al. (2000)
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“The YFP reporter line was used to verify two inducible Cx3cr1-CreERT2 lines (Jung et al., 2000; Parkhurst et al., 2013).”
From Targeting Microglia Using Cx3cr1-Cre Lines: Revisiting the Specificity (2019) · cites this paper as Jung et al., 2000
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“Nevertheless, tamoxifen treatment led to broad expression of GFP reporter in microglia, without significant leakage into neurons.”
From Targeting Microglia Using Cx3cr1-Cre Lines: Revisiting the Specificity (2019) · cites this paper as Jung et al. (2000)
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“In Cx3Cr1‐eGFP mice, GFP is expressed by CNS‐resident macrophages (Jung et al. 2000), which, as noted above, are predominantly represented by microglia (Zhao et al. 2023).”
From Depletion of Microglia Increases Cortical Oligodendrocyte Density During Remyelination (2026) · cites this paper as Jung et al. 2000
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“the P2ry12 signal co-localized on CX3CR1GFP microglia in which GFP is expressed in resident microglia17,23 (Fig. 4e).”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [23]
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“Escape behavior is considered to be an active defensive response dependent on increased PVN-CRH+ neuron activity20.”
From Constitutive expression of CX3CR1-BAC-Cre introduces minimal off-target effects in microglia (2026) · cites this paper as [20]
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“The looming-shadow threat task assesses a mouse’s response to a predator-like threat20.”
From Constitutive expression of CX3CR1-BAC-Cre introduces minimal off-target effects in microglia (2026) · cites this paper as [20]
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“No leakiness was reported in those studies.”
From Targeting Microglia Using Cx3cr1-Cre Lines: Revisiting the Specificity (2019) · cites this paper as Jung et al., 2000
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“which may explain the differences in seizure susceptibility observed in these two studies (Jung et al., 2000; Zhang et al., 2018; Zhao et al., 2018).”
From Targeting Microglia Using Cx3cr1-Cre Lines: Revisiting the Specificity (2019) · cites this paper as Jung et al., 2000
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“Notably, myeloid priming occurs in cells which express the TFs PU.1 and/or C/EBPα32.”
From Single-cell analysis of mixed-lineage states leading to a binary cell fate choice (2016) · cites this paper as [32]
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Systematic Review of the Neurobiological Relevance of Chemokines to Psychiatric Disorders
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Modulation of Microglial Process Convergence Toward Neuronal Dendrites by Extracellular Calcium
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Koenigsknecht-Talboo, J., Meyer-Luehmann, M., Parsadanian, M., Garcia-Alloza, M., Finn, M. B., Hyman, B. T., Bacskai, B. J., & Holtzman, D. M. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4147-08.2008 · Cited by 149
Selective suppression of the α isoform of p38 MAPK rescues late-stage tau pathology
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Jung, K., Heishi, T., Incio, J., Huang, Y., Beech, E. Y., Pinter, M., Ho, W. W., Kawaguchi, K., Rahbari, N. N., Chung, E., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1710754114 · Cited by 138
Oligodendroglial fatty acid metabolism as a central nervous system energy reserve
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The brain’s best friend: microglial neurotoxicity revisited
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Cerebellar microglia are dynamically unique and survey Purkinje neurons in vivo
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Microglia: unique and common features with other tissue macrophages
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Microglia: A Central Player in Depression
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Inflammatory Osteoclasts Prime TNFα-Producing CD4+ T Cells and Express CX3CR1
Ibáñez, L., Abou-Ezzi, G., Ciucci, T., Amiot, V., Belaïd, N., Obino, D., Mansour, A., Rouleau, M., Wakkach, A., & Blin-Wakkach, C. (2016) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2868 · Cited by 117
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Temporally distinct myeloid cell responses mediate damage and repair after cerebrovascular injury
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Time-dependent effects of CX3CR1 in a mouse model of mild traumatic brain injury
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“Indeed, deleting CX3CR1 [4] exacerbates microglial neurotoxicity induced by systemic inflammation in rodent models of Parkinson’s disease and amyotrophic lateral sclerosis [5].”
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“The CX3CR1/GFP / mouse (Jung et al., 2000) was a gift from Dr. Brent Berwin (Geisel School of Medicine at Dartmouth).”
MethodAn Engulfment Assay: A Protocol to Assess Interactions Between CNS Phagocytes and Neurons
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“Cx3cr1 -de fi cient mice, in which both copies of Cx3cr1 are disrupted by the gene for eGFP (Jung et al, 2000), were initially obtained from The Jackson Laboratory and then bred to maintain them on the C57Bl/6J background.”
InfluentialSystemic inflammation in early neonatal mice induces transient and lasting neurodegenerative effects
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A2E accumulation influences retinal microglial activation and complement regulation
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“The fractalkine receptor in these mice has been replaced by a green fluorescent protein (GFP) reporter gene by targeted deletion via homologous recombination in embryonic stem cells (Jung et al. 2000; Davalos et al. 2005).”
BackgroundWhite matter microglia heterogeneity in the CNS
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Metadata
- Authors
- Jung, S., Aliberti, J., Graemmel, P., Sunshine, M. J., Kreutzberg, G. W., Sher, A., & Littman, D. R.
- Affiliations
- Howard Hughes Medical Institute (US)
- Immunobiology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
- Max Planck Institute of Neurobiology (DE)
- National Institutes of Health (US)
- Corresponding author
- Jung, Steffen
- Venue
- Molecular and Cellular Biology
- Publisher
- Informa UK Limited
- Published
- 2000-06-01
- Volume
- 20
- Issue
- 11
- Pages
- 4106-4114
- ISSN
- 0270-7306 (ISSN-L)
- 1098-5549
- PMC
- PMC85780
- OpenAlex
- W2161057248
- Cited by
- 2,632
- References
- 20
- Citations by year
- 2026: 87 · 2025: 132 · 2024: 172 · 2023: 138 · 2022: 135 · 2021: 192 · 2020: 174 · 2019: 162 · 2018: 136 · 2017: 147 · 2016: 142 · 2015: 140 · 2014: 163 · 2013: 128 · 2012: 95
- FWCI
- 11.19
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Molecular and Cellular Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- Topics
- Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Keywords
- CX3CR1, fractalkine, CX3C chemokines, G protein-coupled receptors, monocytes, dendritic cells, natural killer cells, microglia, monocyte extravasation, peritonitis, dendritic cell migration, peripheral nerve injury, neuroinflammation
- MeSH terms
- CX3C Chemokine Receptor 1, Animals, Luminescent Proteins, Mice, Mutant Strains, Phenotype, Receptors, HIV, Gene Expression, Mutagenesis, Insertional, Genes, Reporter, Receptors, Cytokine, Gene Targeting, Green Fluorescent Proteins, Mice
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