Oligodendrocyte precursor cells express a functional chemokine receptor CCR3: Implications for myelination
Abstract
Myelination in the central nervous system requires an accurate interplay between oligodendrocyte precursor cells (OPC) and axons. By as yet not fully understood mechanisms, OPC proliferate, migrate to the axon to be myelinated and finally differentiate into mature oligodendrocytes. The recent finding that OPC express CXC chemokine receptors led us to the investigation of the expression and functional importance of CC chemokine receptors. Using RT-PCR, we show that primary OPC from neonatal rats express CCR3, while CCR1, CCR2, CCR4, CCR5, and CCR7 are not expressed. Immunofluorescence staining of OPC could further demonstrate protein expression of CCR3. A rise of intracellular Ca2+ upon stimulation with the appropriate ligand CCL11 showed that this receptor is functional. Moreover, CCL11 led to a concentration specific increase in proliferation, inhibition of migration, and augmentation of differentiation in primary OPC. Thus, CCR3 may influence the process of myelination. This is of general importance for both developmental tissue patterning and for repair processes in demyelinating diseases like multiple sclerosis.
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OPCs have been suggested to express the primary CCL11 receptor CCR3, and elevated CCL11 levels are associated with MS disease duration and severity.
“Moreover, OPCs have been suggested to express the primary CCL11 receptor, CCR360 and elevated CCL11 levels are associated with MS disease duration and severity61,62.”
From Senescent-like microglia limit remyelination through the senescence associated secretory phenotype (2025) · cites this paper as [60]
Cites
Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue
Mccarthy, K., & de Vellis, J. (1980) · Journal of Cell Biology · doi:10.1083/jcb.85.3.890 · Cited by 3,915 · see citing works
Zlotnik, A., & Yoshie, O. (2000) · Immunity · doi:10.1016/s1074-7613(00)80165-x · Cited by 3,859 · see citing works
Chemokines and leukocyte traffic
Baggiolini, M. (1998) · Nature · doi:10.1038/33340 · Cited by 2,685 · see citing works
Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development
Zou, Y.-R., Kottmann, A. H., Kuroda, M., Taniuchi, I., & Littman, D. R. (1998) · Nature · doi:10.1038/31269 · Cited by 2,494 · see citing works
Biology of Oligodendrocyte and Myelin in the Mammalian Central Nervous System
Baumann, N., & Pham-Dinh, D. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.871 · Cited by 1,828 · see citing works
Lock, C., Hermans, G., Pedotti, R., Brendolan, A., Schadt, E. E., Garren, H., Langer-Gould, A. M., Strober, S., Cannella, B., Allard, J. D., et al. (2002) · Nature Medicine · doi:10.1038/nm0502-500 · Cited by 1,659 · see citing works
Neves, S. R., Ram, P. T., & Iyengar, R. (2002) · Science · doi:10.1126/science.1071550 · Cited by 1,300 · see citing works
Why does remyelination fail in multiple sclerosis?
Franklin, R. J. M. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn917 · Cited by 837 · see citing works
Dancing to the tune of chemokines
Thelen, M. (2001) · Nature Immunology · doi:10.1038/84224 · Cited by 620 · see citing works
Tsai, H., Frost, E. E., To, V., Robinson, S., ffrench‐Constant, C., Geertman, R. T., Ransohoff, R. M., & Miller, R. H. (2002) · Cell · doi:10.1016/s0092-8674(02)00838-3 · Cited by 388 · see citing works
Bajetto, A., Bonavia, R., Barbero, S., & Schettini, G. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.01091.x · Cited by 318 · see citing works
Depletion of CXCR2 Inhibits Tumor Growth and Angiogenesis in a Murine Model of Lung Cancer
Keane, M. P., Belperio, J. A., Xue, Y., Burdick, M. D., & Strieter, R. M. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.5.2853 · Cited by 305 · see citing works
A role for CXCR4 signaling in survival and migration of neural and oligodendrocyte precursors
Dziembowska, M., Tham, T. N., Lau, P., Vitry, S., Lazarini, F., & Dubois-Dalcq, M. (2005) · Glia · doi:10.1002/glia.20170 · Cited by 233 · see citing works
Robinson, S., Tani, M., Strieter, R. M., Ransohoff, R. M., & Miller, R. H. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10457.1998 · Cited by 229 · see citing works
Chemokines and Glial Cells: A Complex Network in the Central Nervous System
Ambrosini, E., & Aloisi, F. (2004) · Neurochemical Research · doi:10.1023/b:nere.0000021246.96864.89 · Cited by 219 · see citing works
CXC chemokine receptors on human oligodendrocytes: implications for multiple sclerosis
Omari, K. M., John, G. R., Sealfon, S. C., & Raine, C. S. (2005) · Brain · doi:10.1093/brain/awh479 · Cited by 196 · see citing works
Astrocytes express functional chemokine receptors
Dorf, M. E., Berman, M. A., Tanabe, S., Heesen, M. A., & Luo, Y. (2000) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(00)00371-4 · Cited by 193 · see citing works
Baranzini, S. E., Elfstrom, C., Chang, S.-Y. P., Butunoi, C., Murray, R. S., Higuchi, R., & Oksenberg, J. R. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.11.6576 · Cited by 157 · see citing works
Fryer, A. D. (2005) · Journal of Clinical Investigation · doi:10.1172/jci25423 · Cited by 155 · see citing works
Role for CXCR2 and CXCL1 on glia in multiple sclerosis
Omari, K. M., John, G. R., Lango, R., & Raine, C. S. (2005) · Glia · doi:10.1002/glia.20246 · Cited by 137 · see citing works
Remyelinating strategies for the treatment of multiple sclerosis
Stangel, M., & Hartung, H.-P. (2002) · Progress in Neurobiology · doi:10.1016/s0301-0082(02)00105-3 · Cited by 126 · see citing works
Self-citationExpression of the chemokine receptors CXCR1 and CXCR2 in rat oligodendroglial cells
Nguyen, D., & Stangel, M. (2001) · Developmental Brain Research · doi:10.1016/s0165-3806(01)00128-6 · Cited by 96 · see citing works
Self-citationHöpfner, M., Maaser, K., Barthel, B., Lampe, B., HANSKI, C., Riecken, E. O., Zeitz, M., & Scherübl, H. (2001) · International Journal of Colorectal Disease · doi:10.1007/s003840100302 · Cited by 92 · see citing works
Self-citationMulti-faceted strategies to combat disease by interference with the chemokine system
Johnson, Z., Schwarz, M. K., Power, C., Wells, T. N. C., & Proudfoot, A. E. I. (2005) · Trends in Immunology · doi:10.1016/j.it.2005.03.001 · Cited by 89 · see citing works
Chemokine receptors and HIV-1: the fusion of two major research fields
Horuk, R. (1999) · Immunology Today · doi:10.1016/s0167-5699(98)01396-6 · Cited by 81 · see citing works
Kadi, L., Selvaraju, R. K., de Lys, P., Proudfoot, A. E. I., Wells, T. N. C., & Boschert, U. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2006.01.011 · Cited by 78 · see citing works
Axonal Signals and Oligodendrocyte Differentiation
Bozzali, M., & Wrabetz, L. G. (2004) · Neurochemical Research · doi:10.1023/b:nere.0000021242.12455.75 · Cited by 57 · see citing works
Stangel, M., Compston, A., & Scolding, N. J. (2000) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00241-6 · Cited by 47 · see citing works
Self-citationAsakura, K., Hunter, S. F., & Rodriguez, M. (1997) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1997.68062281.x · Cited by 46 · see citing works
Nguyen, D., Höpfner, M., Zobel, F., Henke, U., Scherübl, H., & Stangel, M. (2003) · Neuroscience Letters · doi:10.1016/j.neulet.2003.07.014 · Cited by 16 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Deverman, B. E., & Patterson, P. H. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.002 · Cited by 865 · see citing works
Redefining the heterogeneity of peripheral nerve cells in health and autoimmunity
Wolbert, J., Li, X., Heming, M., Mausberg, A. K., Akkermann, D., Frydrychowicz, C., Fledrich, R., Groeneweg, L., Schulz, C., Stettner, M., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1912139117 · Cited by 137 · see citing works
Cytokines and Myelination in the Central Nervous System
Schmitz, T., & Chew, L. (2008) · The Scientific World JOURNAL · doi:10.1100/tsw.2008.140 · Cited by 137 · see citing works
CCL5 induces a pro-inflammatory profile in microglia in vitro
Škuljec, J., Sun, H., Pul, R., Bénardais, K., Ragancokova, D., Moharregh-Khiabani, D., Kotsiari, A., Trebst, C., & Stangel, M. (2011) · Cellular Immunology · doi:10.1016/j.cellimm.2011.05.001 · Cited by 118 · see citing works
Self-citationOmari, K. M., Lutz, S. E., Santambrogio, L., Lira, S. A., & Raine, C. S. (2008) · American Journal Of Pathology · doi:10.2353/ajpath.2009.080350 · Cited by 103 · see citing works
In vivo spatiotemporal dynamics of NG2 glia activity caused by neural electrode implantation
Wellman, S. M., & Kozai, T. D. Y. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.02.037 · Cited by 67 · see citing works
Psenicka, M. W., Smith, B. C., Tinkey, R. A., & Williams, J. L. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.654284 · Cited by 69 · see citing works
Biancotti, J. C., Kumar, S., & de Vellis, J. (2008) · Neurochemical Research · doi:10.1007/s11064-008-9792-8 · Cited by 69 · see citing works
Senescent-like microglia limit remyelination through the senescence associated secretory phenotype
Gross, P. S., Durán-Laforet, V., Ho, L. T., Melchor, G. S., Zia, S., Manavi, Z., Barclay, W. E., Lee, S. H., Shults, N., Selva, S., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-57632-w · Cited by 62 · see citing works
“Moreover, OPCs have been suggested to express the primary CCL11 receptor, CCR3 60 and elevated CCL11 levels are associated with MS disease duration and severity 61,62 .”
Cheung, G. T. Y., Kann, O., Kohsaka, S., Färber, K., & Kettenmann, H. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.163923 · Cited by 41 · see citing works
CCL11 promotes migration and proliferation of mouse neural progenitor cells
Wang, F., Baba, N., Shen, Y., Yamashita, T., Tsuru, E., Tsuda, M., Maeda, N., & Sagara, Y. (2017) · Stem Cell Research & Therapy · doi:10.1186/s13287-017-0474-9 · Cited by 34 · see citing works
Raphael, I., Gomez‐Rivera, F., Raphael, R. A., Robinson, R. R., Nalawade, S. A., & Forsthuber, T. G. (2019) · JCI Insight · doi:10.1172/jci.insight.132527 · Cited by 24 · see citing works
The Age of Cortical Neural Networks Affects Their Interactions with Magnetic Nanoparticles
Tay, A. K. P., Kunze, A., Jun, D., Hoek, E. M. V., & Carlo, D. D. (2016) · Small · doi:10.1002/smll.201600673 · Cited by 23 · see citing works
The progress of chemokines and chemokine receptors in autism spectrum disorders
Ye, J.-R., Wang, H., Cui, L., Chu, S., & Chen, N. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.05.024 · Cited by 19 · see citing works
Schoderboeck, L., Adzemovic, M. Z., Nicolussi, E.-M., Crupinschi, C., Hochmeister, S., Fischer, M.-T., Lassmann, H., & Bradl, M. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.05.026 · Cited by 19 · see citing works
CCL11 Differentially Affects Post-Stroke Brain Injury and Neuroregeneration in Mice Depending on Age
Lieschke, S., Zechmeister, B., Haupt, M., Zheng, X., Jin, F., Hein, K., Weber, M. S., Hermann, D. M., Bähr, M., Kılıç, E., et al. (2019) · Cells · doi:10.3390/cells9010066 · Cited by 18 · see citing works
Factors Regulating Oligodendrocyte Progenitor Cell Migration: From Development to Remyelination
Cao, M., Boltze, J., & Li, S. (2025) · Glia · doi:10.1002/glia.70051 · Cited by 11 · see citing works
The Healthy and Diseased Microenvironments Regulate Oligodendrocyte Properties
Leferink, P. S., & Heine, V. M. (2017) · American Journal Of Pathology · doi:10.1016/j.ajpath.2017.08.030 · Cited by 11 · see citing works
Inflammatory proteins and vestibular neuronitis: A Mendelian randomization study
He, Y., Guo, T., Dai, T., Zhou, B., & Xie, H. (2024) · Medicine · doi:10.1097/md.0000000000041081 · Cited by 6 · see citing works
Gene regulation in the rat prefrontal cortex after learning with or without cholinergic insult
Paban, V., Chambon, C., Farioli, F., & Alescio‐Lautier, B. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.02.005 · Cited by 5 · see citing works
Periasamy, R., Surbek, D., & Schoeberlein, A. (2018) · Tissue and Cell · doi:10.1016/j.tice.2018.04.002 · Cited by 3 · see citing works
Rad, A., Weigl, L. G., Steinecker-Frohnwieser, B., Stadlmayr, S., Millesi, F., Haertinger, M., Borger, A., Supper, P., Semmler, L., Wolf, S., et al. (2024) · Cells · doi:10.3390/cells13181544 · Cited by 2 · see citing works
Johnstone, S. A. (2015) · Enlighten: Theses (The University of Glasgow) · Cited by 1 · see citing works
Gallego, J., Nevin, M., & Eisenstat, D. D. (2023) · Springer eBooks · doi:10.1007/978-3-031-20792-1_7
- Authors
- Maysami, S., Nguyen, D., Zobel, F., Heine, S., Höpfner, M., & Stangel, M.
- Affiliations
- Medizinische Hochschule Hannover (DE)
- Stiftung Charité (DE)
- Venue
- Journal of Neuroimmunology
- Publisher
- Elsevier BV
- Published
- 2006-09
- Volume
- 178
- Issue
- 1-2
- Pages
- 17-23
- ISSN
- 0165-5728 (ISSN-L)
- OpenAlex
- W2134505623
- Cited by
- 25
- References
- 30
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 1 · 2021: 3 · 2020: 1 · 2019: 2 · 2018: 2 · 2017: 2 · 2016: 1 · 2015: 1
- FWCI
- 0.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroimmunology (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Keywords
- oligodendrocyte precursor cells, CCR3, CC chemokine receptors, myelination, eotaxin, oligodendrocyte differentiation, cell proliferation, cell migration, intracellular calcium signaling, demyelinating disease, multiple sclerosis, central nervous system development
- MeSH terms
- Animals, Cell Differentiation, Cell Movement, Cells, Cultured, Immunohistochemistry, Myelin Sheath, Oligodendroglia, RNA, Messenger, Stem Cells, Rats, Sprague-Dawley, Receptors, Chemokine, Chemokines, CC, Reverse Transcriptase Polymerase Chain Reaction, Cell Proliferation, Rats, Receptors, CCR3, Chemokine CCL11
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