The DOI matches its Crossref record; 71 of the 71 references it cites were found in a registry or an index.
Induction and blockage of oligodendrogenesis by differently activated microglia in an animal model of multiple sclerosis
Open accessAbstract
The role of activated microglia (MG) in demyelinating neurodegenerative diseases such as multiple sclerosis is controversial. Here we show that high, but not low, levels of IFN-gamma (a cytokine associated with inflammatory autoimmune diseases) conferred on rodent MG a phenotype that impeded oligodendrogenesis from adult neural stem/progenitor cells. IL-4 reversed the impediment, attenuated TNF-alpha production, and overcame blockage of IGF-I production caused by IFN-gamma. In rodents with acute or chronic EAE, injection of IL-4-activated MG into the cerebrospinal fluid resulted in increased oligodendrogenesis in the spinal cord and improved clinical symptoms. The newly formed oligodendrocytes were spatially associated with MG expressing MHC class II proteins and IGF-I. These results point to what we believe to be a novel role for MG in oligodendrogenesis from the endogenous stem cell pool.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cited source says what the claim attributes to it.
In the citing paper
“We found that M1 microglia express a high level of inflammatory-related transcripts including Ccl2, Ccl3, Ccl5, whereas M2 microglia express genes including IGF-1 (Supplementary Fig. 10a,b), which play a role in tissue development and neural cell renewal28.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [28]
The check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“CD11c+ microglia are known to increase in chronic inflammatory and neurodegenerative conditions as well as during development [76–83]”
From PLCγ2 deficiency compromises systemic immune tolerance and erodes myelin homeostasis while enhancing oxidative metabolism in the mouse brain (2026) · cites this paper as [76]
Experimental — accuracy not yet measuredThe check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“We found that M1 microglia express a high level of inflammatory-related transcripts including Ccl2, Ccl3, Ccl5, whereas M2 microglia express genes including IGF-1 (Supplementary Fig. 10a,b), which play a role in tissue development and neural cell renewal28.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [28]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Molecular Mechanisms of Depression: Perspectives on New Treatment Strategies
Lang, U. E., & Borgwardt, S. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350094 · Cited by 8,526
Glutamate neurotoxicity and diseases of the nervous system
Choi, D. W. (1988) · Neuron · doi:10.1016/0896-6273(88)90162-6 · Cited by 8,188
Neurogenesis in the adult human hippocampus
Eriksson, P. S., Perfilieva, E., Björk-Eriksson, T., Alborn, A.-M., Nordborg, C., Peterson, D. A., & Gage, F. H. (1998) · Nature Medicine · doi:10.1038/3305 · Cited by 6,369
ATP mediates rapid microglial response to local brain injury in vivo
Davalos, D., Grutzendler, J., Yang, G., Kim, J. V., Zuo, Y., Jung, S., Littman, D. R., Dustin, M. L., & Gan, W.-B. (2005) · Nature Neuroscience · doi:10.1038/nn1472 · Cited by 3,913
Blood Monocytes Consist of Two Principal Subsets with Distinct Migratory Properties
Geissmann, F., Jung, S., & Littman, D. R. (2003) · Immunity · doi:10.1016/s1074-7613(03)00174-2 · Cited by 3,504
Jung, S., Aliberti, J., Graemmel, P., Sunshine, M. J., Kreutzberg, G. W., Sher, A., & Littman, D. R. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.11.4106-4114.2000 · Cited by 2,632
Regulation of neuronal survival by the serine-threonine protein kinase Akt
Dudek, H., Datta, S. R., Franke, T. F., Birnbaum, M. J., Yao, R., Cooper, G. M., Segal, R. A., Kaplan, D. R., & Greenberg, M. E. (1997) · Science · doi:10.1126/science.275.5300.661 · Cited by 2,436
Inflammatory Blockade Restores Adult Hippocampal Neurogenesis
Monje, M. L., Toda, H., & Palmer, T. D. (2003) · Science · doi:10.1126/science.1088417 · Cited by 2,426
Jung, S., Unutmaz, D., Wong, P., Sano, G., Santos, K. D. L., Sparwasser, T., Wu, S., Vuthoori, S., Ko, K., Zavala, F., et al. (2002) · Immunity · doi:10.1016/s1074-7613(02)00365-5 · Cited by 1,953
Prevention of experimental autoimmune encephalomyelitis by antibodies against α4βl integrin
Yednock, T. A., Cannon, C., Fritz, L. C., Sánchez‐Madrid, F., Steinman, L., & Karin, N. (1992) · Nature · doi:10.1038/356063a0 · Cited by 1,737
Flagged first, then by citations
Cited by
Sorted by citations
Items 201–262 of 262
Bao, Z., Hao, J., Li, Y., & Feng, F. (2020) · Molecular Medicine Reports · doi:10.3892/mmr.2020.11042 · Cited by 8
Lin, X., Zhao, T., Walker, M. J., Ding, A.-S., Lin, S., Cao, Y., Zheng, J., Liu, X., Geng, M., Xu, X., et al. (2016) · Cell Transplantation · doi:10.3727/096368916x692636 · Cited by 6
Microglia in the Physiology and Pathology of Brain
Nagayach, A., Patro, N., & Patro, I. K. (2015) · Proceedings of the National Academy of Sciences India Section B Biological Sciences · doi:10.1007/s40011-015-0585-y · Cited by 6
Mouhi, S., Pio, T., & Andersen, J. (2025) · Trends in Cell Biology · doi:10.1016/j.tcb.2025.11.003 · Cited by 7
HPGD: An Intermediate Player in Microglial Polarization and Multiple Sclerosis Regulated by Nr4a1
Sun, M., Liu, Y., Wang, X., & Wang, L. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04280-8 · Cited by 6
Zhang, Q., Sun, W., Zheng, M., & Zhang, N. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1452390 · Cited by 5
Kim, J., Lee, K. S., & Chang, Y. P. (2019) · Folia Neuropathologica · doi:10.5114/fn.2019.83828 · Cited by 3
Park, S.-M., Oh, Y.-H., Lim, G.-H., An, J.-H., Lee, J., Gwag, B.-J., Won, S., Seo, K.-W., & Youn, H. (2025) · BMC Neuroscience · doi:10.1186/s12868-024-00920-w · Cited by 3
Effect of Anesthesia on Oligodendrocyte Development in the Brain
Fu, N., Zhu, R., Zeng, S., Li, N., & Zhang, J. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2022.848362 · Cited by 3
Neuroprotection Versus Neurotoxicity
Biber, K. P. H., & Block, M. L. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1429-6_6 · Cited by 3
Ryu, J., Wang, Z., Fan, D., Han, S., Do, S.-H., & Zuo, Z. (2016) · Neuroreport · doi:10.1097/wnr.0000000000000668 · Cited by 3
Functional properties of microglia in mouse models of Alzheimer’s disease
Saiepour, N. (2017) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6117 · Cited by 3
Zhou, Y., Lu, X., Zhang, Y., Li, C., Bai, Y., & Zhang, Z. (2022) · Combinatorial Chemistry & High Throughput Screening · doi:10.2174/1386207326666221111093915 · Cited by 2
Multiple sclerosis: Glial cell activation – Biomarker advances and their translational significance
Zeng, W., Wu, H., & Huang, Y. (2025) · Science Progress · doi:10.1177/00368504251390710 · Cited by 2
Rolando, C., Boda, E., & Buffo, A. (2012) · InTech eBooks · doi:10.5772/31823 · Cited by 2
Macrophages, Microglia, and Dendritic C
Ghorpade, A., Gendelman, H. E., & Kipnis, J. (2008) · Springer eBooks · doi:10.1007/978-0-387-72573-4_9 · Cited by 2
Microglia Colonization Associated with Angiogenesis and Neural Cell Development
Harry, G. J. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-55529-9_10 · Cited by 2
Developmental Vascularization, Neurogenesis, Myelination, and Astrogliogenesis
Harry, G. J., & Pont‐Lezica, L. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1429-6_8 · Cited by 2
Huang, L., Huang, Q., & Zhang, Z. (2026) · European Journal of Neuroscience · doi:10.1111/ejn.70398 · Cited by 1
Garcia, J. C., Bueno, R. J., Salla, M., Serra, I. M., Seeger, B., Akbari, N., Sperber, P. S., Stachelscheid, H., Infante‐Duarte, C., Paul, F., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-57066-2 · Cited by 1
Neural Functions of Hematopoietic‐derived Cells
Derecki, N. C., & Kipnis, J. (2013) · Wiley eBooks · doi:10.1002/9781118314814.ch6 · Cited by 1
Protective and Regenerative Autoimmunity in CNS Injury
Kipnis, J., & Schwartz, M. (2008) · Springer eBooks · doi:10.1007/978-0-387-72573-4_45 · Cited by 1
Réparation du système nerveux central : les stratégies actuelles de thérapie cellulaire
Feron, F. P. (2007) · Revue Neurologique · doi:10.1016/s0035-3787(07)92156-6 · Cited by 1
Brain Inflammation and the Neuronal Fate: from Neurogenesis to Neurodegeneration
Ajmone‐Cat, M. A., Cacci, E., & Minghetti, L. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195326697.003.0013 · Cited by 1
Gutierrez-Kuri, E., Marie Garcia-Rogers, J. L., Perez, J., Smith, S., Kenwood, M. R., Archuleta, K. S., Xiao, Y., Campos, G., Barannikov, S., Wang, H., et al. (2026) · doi:10.64898/2026.07.13.738356
Immune Modulation in Glaucoma – Can Manipulation of Microglial Activation Help?
Chiu, K., So, K., & Chuen-Chung, R. (2011) · InTech eBooks · doi:10.5772/20077
Gozzelino, R. (2007) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas)
Mikroglia bei Alzheimer-Demenz
Wiltfang, J. (2014) · Nervenheilkunde · doi:10.1055/s-0038-1627748
FEATURES OF ADULT NEURAL PROGENITOR CELLS
Arvidsson, L. (2013) · Figshare
N-3 Polyunsaturated Fatty Acid and Neuroinflammation in Aging: Role in Cognition
Layé, S., Madore, C., Delpech, J.-C., Joffre, C., & Nadjar, A. (2014) · AAPS advances in the pharmaceutical sciences series · doi:10.1007/978-3-319-06151-1_6
Ghrelin Suppression of Autoimmune Encephalomyelitis
Miyake, S., & Yamamura, T. (2012) · Humana Press eBooks · doi:10.1007/978-1-61779-903-7_14
Development of Immunization Approaches to Amyotrophic Lateral Sclerosis
Gros‐Louis, F., Gowing, G., & Julien, J. (2009) · Future Neurology · doi:10.2217/fnl.09.21
Adult neural stem cells in neuroinflammation
Covacu, R. (2008) · Figshare
Differential Reactivity of Microglia in Two Mouse Models of Multiple Sclerosis
Hartley, R. K. (2016) · VCU Scholars Compass (Virginia Commonwealth University) · doi:10.25772/8pqb-mw19
Jáňová, H. (2014) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-4704
Lawford‐Smith, H. (2015)
Giannetti, P. (2015) · Spiral (Imperial College London) · doi:10.25560/34680
45and Regenerative Autoimmunity in CNS Injury
Kipnis, J., & Schwartz, M. (2008)
On the role of macrophages, microglia and the extracellular matrix in remyelination
Wang, P. (2018) · University of Groningen research database (University of Groningen / Centre for Information Technology)
Deftu, A., & Suter, M. R. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.24214-4
Distinct Myeloid Cell Subsets with Divergent Functions in Central Nervous System Autoimmunity
Giles, D. A. (2020) · Deep Blue (University of Michigan)
Nave, K., & Werner, H. B. (2007) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1065969.518931
Autologous Macrophages for Central Nervous System Repair
Schwartz, M., & Yoles, E. (2008) · Springer eBooks · doi:10.1007/978-3-540-29678-2_467
(2008) · Springer eBooks · doi:10.1007/978-3-540-29678-2_1
Gu, J., Sun, J. Y., Zhang, Y., Wang, X., Fu, L.-L., Li, L., Wang, D., Wang, X., Yu, L., & Han, X. (2022) · Expert Review of Clinical Immunology · doi:10.1080/1744666x.2022.2117160
Vanherle, S., Guns, J., Loix, M., Mingneau, F., Dierckx, T., Vangansewinkel, T., Wolfs, E., Lins, P. M. P., Bronckaers, A., Lambrichts, I., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.23.521775
Sajjad, M., Zahoor, I., Rashid, F., Rattan, R., & Giri, S. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.19.533192
Microglia in multiple sclerosis
Borst, K., & Prinz, M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-823848-6.00006-3
Ivan, D. C., Berve, K., Walthert, S., Monaco, G., Borst, K., Bouillet, E., Ferreira, F. M., Lee, H., Steudler, J., Buch, T., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22624240
Ivan, D. C., Berve, K., Walthert, S., Monaco, G., Borst, K., Bouillet, E., Ferreira, F. M., Lee, H., Steudler, J., Buch, T., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22624237
Ivan, D. C., Berve, K., Walthert, S., Monaco, G., Borst, K., Bouillet, E., Ferreira, F. M., Lee, H., Steudler, J., Buch, T., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22624234
Sanson, C. (2017) · theses.fr (ABES) · doi:10.70675/205f3741zaac1z422eza6aeza2902010260f · Cited by 1
Jaouën, A. (2017) · doi:10.70675/32a64946zb1b6z4f2dza493zac9994e9782d
Macrophage activation profiles of multiple sclerosis patients
Fransson, J. (2019) · theses.fr (ABES) · doi:10.70675/361929ebz66c2z48dbz83a1z8955d8b54716
Microglia-nodes of Ranvier interaction during repair
Roux, T. (2020) · theses.fr (ABES) · doi:10.70675/a1319259z2b39z4d4ez9c05z261e4533646b
Microglial PD-1/PD-L1 axis in CNS demyelinating diseases: a dual immunoregulatory perspective
Zhou, M., Yao, X., Liu, L., Gao, Y., Chen, W. K., Zheng, K., Li, H., & Meng, Q. (2026) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2026.1815351
Metadata
- Authors
- Butovsky, O.
- Affiliations
- Weizmann Institute of Science (IL)
- Corresponding author
- Butovsky, O.
- ORCID
- Butovsky, O.
- Venue
- Journal of Clinical Investigation
- Published
- 2006-03-23
- Volume
- 116
- Issue
- 4
- Pages
- 905-915
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC1409740
- OpenAlex
- W2145533845
- Cited by
- 261
- References
- 71
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 11 · 2023: 15 · 2022: 8 · 2021: 7 · 2020: 14 · 2019: 18 · 2018: 10 · 2017: 11 · 2016: 15 · 2015: 16 · 2014: 16 · 2013: 16 · 2012: 16
- FWCI
- 13.58
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- microglia, oligodendrogenesis, multiple sclerosis, experimental autoimmune encephalomyelitis, interferon-gamma, IL-4, TNF-α, insulin-like growth factor I, neural stem/progenitor cells, demyelination, MHC class II, oligodendrocytes, cerebrospinal fluid injection, neuroinflammation
- MeSH terms
- Animals, Cells, Cultured, Cerebral Ventricles, Disease Models, Animal, Encephalomyelitis, Autoimmune, Experimental, Interferon-gamma, Male, Mice, Inbred C57BL, Multiple Sclerosis, Oligodendroglia, Rats, Inbred Lew, Recombinant Proteins, Stem Cells, Interleukin-4, Microglia, Mice, Knockout, Mice, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review