Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice
Open accessAbstract
BACKGROUND: Monocyte subpopulations distinguished by differential expression of chemokine receptors CCR2 and CX3CR1 are difficult to track in vivo, partly due to lack of CCR2 reagents. METHODOLOGY/PRINCIPAL FINDINGS: We created CCR2-red fluorescent protein (RFP) knock-in mice and crossed them with CX3CR1-GFP mice to investigate monocyte subset trafficking. In mice with experimental autoimmune encephalomyelitis, CCR2 was critical for efficient intrathecal accumulation and localization of Ly6C(hi)/CCR2(hi) monocytes. Surprisingly, neutrophils, not Ly6C(lo) monocytes, largely replaced Ly6C(hi) cells in the central nervous system of these mice. CCR2-RFP expression allowed the first unequivocal distinction between infiltrating monocytes/macrophages from resident microglia. CONCLUSION/SIGNIFICANCE: These results refine the concept of monocyte subsets, provide mechanistic insight about monocyte entry into the central nervous system, and present a novel model for imaging and quantifying inflammatory myeloid populations.
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In double-heterozygous Ccr2rfp::Cx3cr1gfp mice with EAE, GFP is expressed by CD45dim/Ly6C− microglia, whereas RFP is restricted to CD45high/Ly6C+ monocytes.
“When F4/80+ macrophages were isolated from CNS and analyzed by flow cytometry using cells from double-heterozygous Ccr2rfp::Cx3cr1gfp mice with EAE, GFP was expressed by CD45dim/Ly6C− microglia, whereas RFP was restricted to CD45high/Ly6C+ monocytes (Saederup et al., 2010; Mizutani et al., 2012).”
From Differential roles of microglia and monocytes in the inflamed central nervous system (2014) · cites this paper as Saederup et al., 2010
The Results section (Infiltration by CD115+ monocytes; page not supplied) reports GFP-high, RFP-negative CD45-low microglia at peak EAE, supporting the microglial part of the claim. But the Discussion reports RFP-low Ly6C-low cells in the diseased CNS, and the Results (Three color imaging with a myeloid marker) identifies RFP-positive cells likely to be Ly6C-low monocytes or T cells. RFP is therefore not restricted to Ly6C-positive monocytes as claimed. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn Ccr2rfp/rfp::Cx3cr1gfp/+ mice, MDMs were virtually absent from inflamed EAE tissues and replaced in large part by neutrophils.
“To address the role of MDMs in demyelination at EAE onset, we investigated clinical characteristics in relation to node pathology and demyelination in Ccr2rfp/rfp::Cx3cr1gfp/+ mice in which MDMs were virtually absent from inflamed EAE tissues and replaced in large part by neutrophils (Saederup et al., 2010).”
From Differential roles of microglia and monocytes in the inflamed central nervous system (2014) · cites this paper as Saederup et al., 2010
The Discussion (page unavailable) says Ly6Chi monocytes were virtually absent from the CNS of these mice and that neutrophils replaced them. The Results section on CD115+ infiltration reports markedly fewer monocytes/macrophages, but also says Ly6Clo cells remained; it does not establish that all monocyte-derived macrophages (MDMs) were virtually absent. (LLM, conf=0.84)
Experimental — accuracy not yet measuredCCR2+Ly6C+ cells constitute the vast majority of infiltrating monocytes at EAE onset.
“CCR2+Ly6C+ cells constitute the vast majority of infiltrating monocytes at EAE onset (Saederup et al., 2010; Mizutani et al., 2012).”
From Differential roles of microglia and monocytes in the inflamed central nervous system (2014) · cites this paper as Saederup et al., 2010
The Results (Figure 4D) report that 88% of CD115+ monocyte-lineage cells in the CNS were Ly6Chi, and another Results passage (Figure 4E) identifies this subset as CCR2+. These measurements were made at peak EAE severity, not at EAE onset, so the cited paper does not establish the claim's timing. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn ccr2RFP∷cx3cr1GFP double heterozygous mice, adult resident microglia exhibit a ccr2RFP−/cx3cr1GFP+ pattern, whereas peripheral monocytes recruited in response to inflammation are characterized by a ccr2RFP+/cx3cr1GFP− pattern.
“We took advantage of ccr2RFP∷ cx3cr1GFP double heterozygous mice 35 in which adult resident microglia exhibit a ccr2RFP−/cx3cr1GFP+ pattern35, 36, whereas peripheral monocytes, which are recruited in response to inflammation, are characterized by a ccr2RFP+/cx3cr1GFP− pattern35–37.”
From Social stress induces neurovascular pathology promoting depression (2017) · cites this paper as [35]
The Discussion identifies resident microglia as GFP-only and infiltrating monocyte-derived cells as RFP-positive. It does not characterize the recruited monocytes as uniformly GFP-negative: the Discussion says they have varying degrees of GFP expression, and the Results report RFP/GFP double-positive monocytes entering inflamed brain tissue. (LLM, conf=0.90)
Experimental — accuracy not yet measuredMicroglia were labeled using the CX3CR1+/GFP mouse line in which all microglia express EGFP under CX3CR1.
“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 Saederup et al., 2010
There was an increase in CD39−CD11bHi cells which express Ly6C in CNS-TGFβ1−/− mice.
“we found an increase in CD39−CD11bHi cells which express Ly6C (Fig. 7g) and which represent peripherally infiltrating monocytes9,12.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [9]
Microglia can be distinguished from monocytes using red-green mice in which microglia and monocyte-derived macrophages are labeled with CX3CR1 (GFP) and CCR2 (RFP) respectively.
“microglia can be distinguished from monocytes using red-green mice in which microglia and monocyte-derived macrophages are labeled with CX3CR1 (GFP) and CCR2 (RFP) respectively9.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [9]
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Self-citation
- Authors
- Saederup, N., Cardona, A. E., Croft, K., Mizutani, M., Cotleur, A. C., Tsou, C.-L., Ransohoff, R. M., & Charo, I. F.
- Affiliations
- Gladstone Institutes (US)
- Cleveland Clinic (US)
- Corresponding author
- Ransohoff, Richard M.
- Charo, Israel F.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2010-10-27
- Volume
- 5
- Issue
- 10
- Pages
- e13693
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2965160
- OpenAlex
- W2104003768
- Cited by
- 599
- References
- 46
- Citations by year
- 2026: 19 · 2025: 28 · 2024: 60 · 2023: 32 · 2022: 22 · 2021: 38 · 2020: 49 · 2019: 54 · 2018: 42 · 2017: 51 · 2016: 44 · 2015: 49 · 2014: 46 · 2013: 30 · 2012: 17
- FWCI
- 9.81
- Type
- journal article
- Language
- en
- Update notices
- correction (2017-04-27)
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Multiple Sclerosis Society
- Multiple Sclerosis Society
- National Institutes of Health
- National Heart, Lung, and Blood Institute (R01HL063894, R01HL052773, HL 52773, HL63894)
- National Institute of Neurological Disorders and Stroke (R01NS32151, R01NS032151)
- Topics
- Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Keywords
- CCR2, CX3CR1, monocyte subsets, monocyte trafficking, experimental autoimmune encephalomyelitis, Ly6C, neutrophils, microglia, red fluorescent protein
- MeSH terms
- Red Fluorescent Protein, Animals, Central Nervous System, Luminescent Proteins, Mice, Receptors, CCR2
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