GM‐CSF promotes migration of human monocytes across the blood brain barrier
Open accessAbstract
Multiple sclerosis (MS) is a chronic inflammatory demyelinating disease of the central nervous system (CNS). Infiltration of monocytes into the CNS is crucial for disease onset and progression. Animal studies indicate that granulocyte‐macrophages colony‐stimulating factor (GM‐CSF) may play an essential role in this process, possibly by acting on the migratory capacities of myeloid cells across the blood–brain barrier. This study describes the effect of GM‐CSF on human monocytes, macrophages, and microglia. Furthermore, the expression of GM‐CSF and its receptor was investigated in the CNS under healthy and pathological conditions. We show that GM‐CSF enhances monocyte migration across human blood–brain barrier endothelial cells in vitro. Next, immunohistochemical analysis on human brain tissues revealed that GM‐CSF is highly expressed by microglia and macrophages in MS lesions. The GM‐CSF receptor is expressed by neurons in the rim of combined gray/white matter lesions and astrocytes. Finally, the effect of GM‐CSF on human macrophages was determined, revealing an intermediate activation status, with a phenotype similar to that observed in active MS lesions. Together our data indicate that GM‐CSF is a powerful stimulator of monocyte migration, and is abundantly present in the inflamed CNS where it may act as an activator of macrophages and microglia.
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
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?
CSF-2 promotes migration of blood-borne monocytes across the blood-brain barrier, which then differentiate into macrophages in the presence of CSF-1 and CSF-2.
“CSF-2 promotes migration of blood-borne monocytes across the blood-brain barrier, which then differentiate into macrophages in the presence of CSF-1 and CSF-2 [16, 17, 26, 52].”
From Loss of homeostatic microglial phenotype in CSF1R-related Leukoencephalopathy (2020) · cites this paper as [52]
The Discussion reports that GM-CSF (CSF-2) increased human monocyte migration across a blood-brain-barrier endothelial layer in vitro, and says monocytes mature into macrophages after entering the CNS. The Introduction and Human macrophages methods describe GM-CSF-associated maturation and macrophage culture, but do not establish that the migrated monocytes subsequently differentiate in the presence of both CSF-1 and CSF-2. Page numbers are unavailable in our copy. (LLM, conf=0.88)
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.
Cites
The M1 and M2 paradigm of macrophage activation: Time for reassessment
Martinez, F. O., & Gordon, S. (2014) · F1000Prime Reports · doi:10.12703/p6-13 · Cited by 4,689 · see citing works
Macrophage activation and polarization
Martinez, F. O. (2008) · Frontiers in Bioscience · doi:10.2741/2692 · Cited by 3,160 · see citing works
M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination
Miron, V. E., Boyd, A., Zhao, J.-W., Yuen, T. J., Ruckh, J. M., Shadrach, J. L., van Wijngaarden, P., Wagers, A. J., Williams, A., Franklin, R. J. M., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3469 · Cited by 1,788 · see citing works
Blood‐brain barrier‐specific properties of a human adult brain endothelial cell line
Weksler, B. B., Subileau, E.-A., Perrière, N., Charneau, P., Holloway, K. E., Leveque, M., Tricoire-Leignel, H., Nicotra, A., Bourdoulous, S., Turowski, P., et al. (2005) · The FASEB Journal · doi:10.1096/fj.04-3458fje · Cited by 1,325 · see citing works
Colony-stimulating factors in inflammation and autoimmunity
Hamilton, J. A. (2008) · Nature reviews. Immunology · doi:10.1038/nri2356 · Cited by 1,305 · see citing works
Codarri, L., Gyülvészi, G., Tosevski, V., Hesske, L., Fontana, A., Magnenat, L., Suter, T., & Becher, B. (2011) · Nature Immunology · doi:10.1038/ni.2027 · Cited by 1,191 · see citing works
Verreck, F. A. W., de Boer, T., Langenberg, D. M. L., Hoeve, M. A., Kramer, M., Vaisberg, E., Kastelein, R., Kolk, A. H. J., Malefyt, R. D. W., & Ottenhoff, T. H. M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400983101 · Cited by 969 · see citing works
Kuhlmann, T., Lingfeld, G., Bitsch, A., Schuchardt, J., & Brück, W. (2002) · Brain : a journal of neurology · doi:10.1093/brain/awf235 · Cited by 851 · see citing works
Oxidative damage in multiple sclerosis lesions
Haider, L., Fischer, M. T., Frischer, J., Bauer, J., Höftberger, R., Botond, G., Esterbauer, H., Binder, C., Witztum, J., & Lassmann, H. (2011) · Brain : a journal of neurology · doi:10.1093/brain/awr128 · Cited by 754 · see citing works
Cc Chemokine Receptor 2 Is Critical for Induction of Experimental Autoimmune Encephalomyelitis
Fife, B. T., Huffnagle, G. B., Kuziel, W. A., & Karpus, W. J. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.6.899 · Cited by 511 · see citing works
Huitinga, I., van Rooijen, N., de Groot, C. J., Uitdehaag, B. M., & Dijkstra, C. D. (1990) · The Journal of experimental medicine · doi:10.1084/jem.172.4.1025 · Cited by 506 · see citing works
Self-citationMacrophages in inflammatory multiple sclerosis lesions have an intermediate activation status
Vogel, D. Y., Vereyken, E. J., Glim, J. E., Heijnen, P. D., Moeton, M., van der Valk, P., Amor, S., Teunissen, C. E., van Horssen, J., & Dijkstra, C. D. (2013) · Journal of Neuroinflammation · doi:10.1186/1742-2094-10-35 · Cited by 479 · see citing works
Self-citationGranulocyte Macrophage Colony-Stimulating Factor
McQualter, J. L., Darwiche, R., Ewing, C., Onuki, M., Kay, T. W., Hamilton, J. A., Reid, H. H., & Bernard, C. C. A. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.194.7.873 · Cited by 477 · see citing works
Comparison of polarization properties of human adult microglia and blood‐derived macrophages
Durafourt, B. A., Moore, C. S., Zammit, D., Johnson, T., Zaguia, F., Guiot, M., Bar‐Or, A., & Antel, J. P. (2012) · Glia · doi:10.1002/glia.22298 · Cited by 470 · see citing works
Human macrophage polarization in vitro: maturation and activation methods compared.
Vogel, D., Glim, J. E., Stavenuiter, A. W., Breur, M., Heijnen, P., Amor, S., Dijkstra, C., & Beelen, R. (2014) · Immunobiology · doi:10.1016/j.imbio.2014.05.002 · Cited by 431 · see citing works
Self-citationSystematic validation of specific phenotypic markers for in vitro polarized human macrophages
Ambarus, C. A., Krausz, S., van Eijk, M., Hamann, J., Radstake, T. R. D. J., Reedquist, K. A., Tak, P. P., & Baeten, D. L. P. (2012) · Journal of Immunological Methods · doi:10.1016/j.jim.2011.10.013 · Cited by 411 · see citing works
Tran, E., Hoekstra, K., van Rooijen, N., Dijkstra, C., & Owens, T. (1998) · Journal of Immunology · doi:10.4049/jimmunol.161.7.3767 · Cited by 373 · see citing works
Self-citationDihydrorhodamine 123: a fluorescent probe for superoxide generation?
HENDERSON, L. M., & Chappell, J. (1993) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1993.tb18328.x · Cited by 371 · see citing works
Verreck, F. A. W., de Boer, T., Langenberg, D. M. L., van der Zanden, L., & Ottenhoff, T. H. M. (2005) · Journal of Leukocyte Biology · doi:10.1189/jlb.0105015 · Cited by 370 · see citing works
Mikita, J., Dubourdieu-Cassagno, N., Deloire, M. S., Vekris, A., Biran, M., Raffard, G., Brochet, B., Canron, M.-H., Franconi, J.-M., Boiziau, C., et al. (2011) · Multiple Sclerosis Journal · doi:10.1177/1352458510379243 · Cited by 358 · see citing works
Ponomarev, E. D., Shriver, L. P., Maresz, K., Pedras-Vasconcelos, J., Verthelyi, D. I., & Dittel, B. N. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.1.39 · Cited by 357 · see citing works
van Horssen, J., Schreibelt, G., Drexhage, J., Hazes, T., Dijkstra, C. D., van der Valk, P., & de Vries, H. E. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.09.023 · Cited by 316 · see citing works
Self-citationBrück, W. (2005) · Journal of Neurology · doi:10.1007/s00415-005-5002-7 · Cited by 307 · see citing works
Groot, C. J. A. D. (2001) · Brain · doi:10.1093/brain/124.8.1635 · Cited by 285 · see citing works
Shechter, R., & Schwartz, M. (2012) · The Journal of Pathology · doi:10.1002/path.4106 · Cited by 225 · see citing works
Hamilton, J. A., & Anderson, G. P. (2004) · Growth Factors · doi:10.1080/08977190412331279881 · Cited by 224 · see citing works
Enhanced number and activity of mitochondria in multiple sclerosis lesions
Witte, M. E., Bø, L., Rodenburg, R. J., Beliën, J. A. M., Musters, R. J. P., Hazes, T., Wintjes, L. T., Smeitink, J. A. M., Geurts, J. J. G., de Vries, H. E., et al. (2009) · The Journal of Pathology · doi:10.1002/path.2582 · Cited by 222 · see citing works
GM‐CSF promotes proliferation of human fetal and adult microglia in primary cultures
Lee, S. C., Liu, W., Brosnan, C. F., & Dickson, D. W. (1994) · Glia · doi:10.1002/glia.440120407 · Cited by 209 · see citing works
Functions of Granulocyte-Macrophage Colony-Stimulating Factor
Fleetwood, A. J., Cook, A. D., & Hamilton, J. A. (2005) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.v25.i5.50 · Cited by 205 · see citing works
The Impact of Microglia-Derived Cytokines upon Gliosis in the CNS
Giulian, D., Li, J., Li, X., George, J., & Rutecki, P. A. (1994) · Developmental Neuroscience · doi:10.1159/000112099 · Cited by 194 · see citing works
Reactive oxygen species are required for the phagocytosis of myelin by macrophages
van der Goes, A., Brouwer, J. P., Hoekstra, K., Roos, D., van den Berg, T. K., & Dijkstra, C. D. (1998) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(98)00175-1 · Cited by 180 · see citing works
Self-citationMacrophages migrate in an activation-dependent manner to chemokines involved in neuroinflammation
Vogel, D. Y. S., Heijnen, P. D. A. M., Breur, M., de Vries, H. E., Tool, A. T. J., Amor, S., & Dijkstra, C. D. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-23 · Cited by 180 · see citing works
Self-citationLacombe, P., Mathews, P. M., Schmidt, S., Breidert, T., Heneka, M., Landreth, G., Feinstein, D. L., & Galea, E. (2004) · Journal of Neuroinflammation · doi:10.1186/1742-2094-1-11 · Cited by 179 · see citing works
Qin, H., Wilson, C. A., Lee, S. J., Zhao, X., & Benveniste, E. N. (2005) · Blood · doi:10.1182/blood-2005-02-0759 · Cited by 175 · see citing works
Schäbitz, W.-R., Krüger, C., Pitzer, C., Weber, D., Laage, R., Gaßler, N., Aronowski, J. A., Mier, W., Kirsch, F., Dittgen, T., et al. (2007) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600496 · Cited by 168 · see citing works
Reactive oxygen species enhance the migration of monocytes across the blood‐brain barrier in vitro
van der Goes, A., Wouters, D., van der Pol, S. M. A., Huizinga, R., Ronken, E., Adamson, P., Greenwood, J., Dijkstra, C. D., & de Vries, H. E. (2001) · The FASEB Journal · doi:10.1096/fj.00-0881fje · Cited by 162 · see citing works
Self-citationCarrieri, P. B., Provitera, V., Rosa, T. D., Tartaglia, G. G., Gorga, F., & Perrella, O. (1998) · Immunopharmacology and Immunotoxicology · doi:10.3109/08923979809034820 · Cited by 155 · see citing works
Natalizumab: Targeting α4-Integrins in Multiple Sclerosis
Engelhardt, B., & Kappos, L. (2007) · Neurodegenerative Diseases · doi:10.1159/000109933 · Cited by 154 · see citing works
Phenotyping primary human microglia: tight regulation of LPS responsiveness
Melief, J., Koning, N., Schuurman, K. G., Van De Garde, M. D. B., Smolders, J., Hoek, R. M., Van Eijk, M., Hamann, J., & Huitinga, I. (2012) · Glia · doi:10.1002/glia.22370 · Cited by 132 · see citing works
McLay, R. N. (1997) · Brain · doi:10.1093/brain/120.11.2083 · Cited by 109 · see citing works
Potsch, C., Voehringer, D., & Pircher, H. (1999) · European Journal of Immunology · doi:10.1002/(sici)1521-4141(199911)29:11 · Cited by 92 · see citing works
Kooij, G., Mizee, M. R., van Horssen, J., Reijerkerk, A., Witte, M. E., Drexhage, J. A. R., van der Pol, S. M. A., van het Hof, B., Scheffer, G., Scheper, R., et al. (2011) · Brain · doi:10.1093/brain/awq330 · Cited by 90 · see citing works
Self-citationRho kinase inhibitor fasudil regulates microglia polarization and function
Zhang, H., Li, Y., Yu, J., Guo, M., Meng, J., Liu, C., Xie, Y., Feng, L., Xiao, B., & Ma, C. (2013) · Neuroimmunomodulation · doi:10.1159/000351221 · Cited by 90 · see citing works
Lisi, L., Stigliano, E., Lauriola, L., Navarra, P., & Russo, C. D. (2014) · ASN NEURO · doi:10.1042/an20130045 · Cited by 89 · see citing works
Chemokine CCL2 and chemokine receptor CCR2 in early active multiple sclerosis
Sørensen, T. L., Ransohoff, R. M., Strieter, R. M., & Sellebjerg, F. T. (2004) · European Journal of Neurology · doi:10.1111/j.1468-1331.2004.00796.x · Cited by 88 · see citing works
Groot, C. J. A. D., Montagne, L., Janssen, I., Ravid, R., van der Valk, P., & Veerhuis, R. (2000) · Brain Research Protocols · doi:10.1016/s1385-299x(99)00059-8 · Cited by 76 · see citing works
Matrix metalloproteinase‐19 is highly expressed in active multiple sclerosis lesions
van Horssen, J., Vos, C. M. P., Admiraal, L., van Haastert, E. S., Montagne, L., van der Valk, P., & de Vries, H. E. (2006) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2006.00766.x · Cited by 64 · see citing works
Ha, Y. S., Kim, Y. S., Cho, J. M., Yoon, S. H., Park, S. R., Yoon, D. H., Kim, E. Y., & Park, H. C. (2005) · Journal of Neurosurgery Spine · doi:10.3171/spi.2005.2.1.0055 · Cited by 64 · see citing works
P-glycoprotein regulates trafficking of CD8+ T cells to the brain parenchyma
Kooij, G., Kroon, J., Paul, D., Reijerkerk, A., Geerts, D., van der Pol, S. M. A., Hof, B. V. H., Drexhage, J., van Vliet, S. J., Hekking, L. H. P., et al. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1244-8 · Cited by 53 · see citing works
Self-citationDame, J. B., Christensen, R. D., & Juul, S. E. (1999) · Pediatric Research · doi:10.1203/00006450-199910000-00002 · Cited by 51 · see citing works
Wiggins-Dohlvik, K. C., Merriman, M., Shaji, C. A., Alluri, H., Grimsley, M., Davis, M. L., Smith, R. W., & Tharakan, B. (2014) · The American Journal of Surgery · doi:10.1016/j.amjsurg.2014.08.014 · Cited by 49 · see citing works
Marušić, S., Miyashiro, J. S., Douhan, J., Konz, R. F., Xuan, D., Pelker, J. W., Ling, V., Leonard, J. P., & Jacobs, K. A. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)00947-3 · Cited by 41 · see citing works
Laminar fate specification in the cerebral cortex
Gaspard, N., & Vanderhaeghen, P. (2011) · F1000 Biology Reports · doi:10.3410/b3-6 · Cited by 36 · see citing works
The helminth Trichuris suis suppresses TLR4-induced inflammatory responses in human macrophages
Ottow, M., Klaver, E. J., Kraan, T. C. T. M. V. D. P., Heijnen, P. D. A. M., Laan, L. C., Kringel, H., Vogel, D. Y. S., Dijkstra, C. D., Kooij, G., & van Die, I. (2014) · Genes and Immunity · doi:10.1038/gene.2014.38 · Cited by 35 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition)
Cossarizza, A., Chang, H., Radbruch, A., Acs, A., Adam, D., Adam‐Klages, S., Agace, W. W., Aghaeepour, N., Akdiş, M., Allez, M., et al. (2019) · European Journal of Immunology · doi:10.1002/eji.201970107 · Cited by 982 · see citing works
Macrophage polarization in pathology
Sica, A., Erreni, M., Allavena, P., & Porta, C. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1995-y · Cited by 673 · see citing works
Guidelines for the use of flow cytometry and cell sorting in immunological studies *
Cossarizza, A., Chang, H., Radbruch, A., Akdiş, M., Andrä, I., Annunziato, F., Bächer, P., Barnaba, V., Battistini, L., Bauer, W. M., et al. (2017) · European Journal of Immunology · doi:10.1002/eji.201646632 · Cited by 572 · see citing works
The Role of Monocytes and Macrophages in Autoimmune Diseases: A Comprehensive Review
Ma, W., Gao, F., Gu, K., & Chen, D. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01140 · Cited by 360 · see citing works
GM-CSF: A Double-Edged Sword in Cancer Immunotherapy
Kumar, A., Khani, A. T., Ortiz, A. S., & Swaminathan, S. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.901277 · Cited by 277 · see citing works
Roles of GM-CSF in the Pathogenesis of Autoimmune Diseases: An Update
Lotfi, N., Thomé, R., Rezaei, N., Zhang, G., Rezaei, A., Rostami, A. M., & Esmaeil, N. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01265 · Cited by 229 · see citing works
van Langelaar, J., de Vries, R. M. V. D. V., Janssen, M., Wierenga‐Wolf, A. F., Spilt, I. M., Siepman, T. A. M., Dankers, W., Verjans, G. M. G. M., de Vries, H. E., Lubberts, E., et al. (2018) · Brain · doi:10.1093/brain/awy069 · Cited by 224 · see citing works
Deep insight into cytokine storm: from pathogenesis to treatment
Nie, J., Zhou, L., Tian, W., Liu, X., Yang, L., Yang, X., Zhang, Y., Wei, S., Wang, D. W., & Wei, J. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02178-y · Cited by 224 · see citing works
Kalinski, A. L., Yoon, C., Huffman, L. D., Duncker, P. C., Kohen, R., Passino, R., Hafner, H., Johnson, C. N., Kawaguchi, R., Carbajal, K. S., et al. (2020) · eLife · doi:10.7554/elife.60223 · Cited by 160 · see citing works
Sachdeva, M., Duchateau, P. N., Depil, S., Poirot, L., & Valton, J. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ac119.007558 · Cited by 162 · see citing works
Anti-colony-stimulating factor therapies for inflammatory and autoimmune diseases
Hamilton, J. A., Cook, A. D., & Tak, P. P. (2016) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2016.231 · Cited by 160 · see citing works
GM-CSF: A Promising Target in Inflammation and Autoimmunity
Lee, M.-C., Achuthan, A. A., & Hamilton, J. A. (2020) · ImmunoTargets and Therapy · doi:10.2147/itt.s262566 · Cited by 146 · see citing works
Unique and shared inflammatory profiles of human brain endothelia and pericytes
Smyth, L. C. D., Rustenhoven, J., Park, T., Schweder, P. M., Jansson, D., Heppner, P. A., O’Carroll, S. J., Mee, E. W., Faull, R. L. M., Curtis, M. A., et al. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1167-8 · Cited by 137 · see citing works
Kooij, G., Troletti, C. D., Leuti, A., Norris, P. C., Riley, I. R., Albanese, M., Ruggieri, S., Libreros, S., van der Pol, S. M. A., Hof, B. V. H., et al. (2019) · Haematologica · doi:10.3324/haematol.2019.219519 · Cited by 120 · see citing works
Self-citationMacrophage, the potential key mediator in CAR-T related CRS
Hao, Z., Li, R., Li, M., Han, Z., & Hong, Z. (2020) · Experimental Hematology and Oncology · doi:10.1186/s40164-020-00171-5 · Cited by 104 · see citing works
The role of human mast cells in allergy and asthma
Banafea, G. H., Bakhashab, S., Alshaibi, H. F., Pushparaj, P. N., & Rasool, M. (2022) · Bioengineered · doi:10.1080/21655979.2022.2044278 · Cited by 93 · see citing works
The potential role of synovial cells in the progression and treatment of osteoarthritis
Zou, Z., Li, H., Yu, K., Ma, K., Wang, Q., Tang, J., Liu, G., Lim, K. S., Hooper, G. J., Woodfield, T. B. F., et al. (2023) · Exploration · doi:10.1002/exp.20220132 · Cited by 82 · see citing works
Syndecan-1 facilitates breast cancer metastasis to the brain
Sayyad, M. R., Puchalapalli, M., Vergara, N. G., Wangensteen, S. M., Moore, M., Mu, L., Edwards, C., Anderson, A., Kall, S. L., Sullivan, M. E., et al. (2019) · Breast Cancer Research and Treatment · doi:10.1007/s10549-019-05347-0 · Cited by 81 · see citing works
Spampinato, S. F., Bortolotto, V., Canonico, P. L., Sortino, M. A., & Grilli, M. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.01346 · Cited by 79 · see citing works
Loss of homeostatic microglial phenotype in CSF1R-related Leukoencephalopathy
Kempthorne, L., Yoon, H., Madore, C., Smith, S., Wszolek, Z. K., Rademakers, R., Kim, J., Butovsky, O., & Dickson, D. W. (2020) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-00947-0 · Cited by 77 · see citing works
“Thus, it might be interesting to further investigate whether alteration in CSF-2 or IL-34 mediated pathways account for, or compensate, the phenotypic changes in brain regions less vulnerable to pathology in HDLS.”
BackgroundInfluentialDelbridge, A. R. D., Huh, D., Brickelmaier, M., Burns, J. C., Roberts, C., Challa, R., Raymond, N., Cullen, P., Carlile, T. M., Ennis, K. A., et al. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.592005 · Cited by 72 · see citing works
Shang, D., Yang, Y., Zhang, H., Li, T. X., Jiang, J. S., Dong, Y., Zhang, K., Li, B., Zhao, W., Fang, W., et al. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16660983 · Cited by 67 · see citing works
Borriello, F., Iannone, R., Somma, S. D., Loffredo, S., Scamardella, E., Galdiero, M. R., Varricchi, G., Granata, F., Portella, G., & Marone, G. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00680 · Cited by 65 · see citing works
GM-CSF: Master regulator of the T cell-phagocyte interface during inflammation
Ingelfinger, F., De Feo, D., & Becher, B. (2021) · Seminars in Immunology · doi:10.1016/j.smim.2021.101518 · Cited by 61 · see citing works
Alpha-hemolysin of uropathogenic Escherichia coli induces GM-CSF-mediated acute kidney injury
Wang, C., Li, Q., Lv, J., Sun, X., Cao, Y., Yu, K., Miao, C., Zhang, Z., Yao, Z., & Wang, Q. (2019) · Mucosal Immunology · doi:10.1038/s41385-019-0225-6 · Cited by 61 · see citing works
Colony stimulating factors in the nervous system
Chiţu, V., Biundo, F., & Stanley, E. R. (2021) · Seminars in Immunology · doi:10.1016/j.smim.2021.101511 · Cited by 55 · see citing works
Dwellers and Trespassers: Mononuclear Phagocytes at the Borders of the Central Nervous System
Ivan, D. C., Walthert, S., Berve, K., Steudler, J., & Locatelli, G. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.609921 · Cited by 53 · see citing works
Evaluation of the effect of GM-CSF blocking on the phenotype and function of human monocytes
Lotfi, N., Zhang, G., Esmaeil, N., & Rostami, A. M. (2020) · Scientific Reports · doi:10.1038/s41598-020-58131-2 · Cited by 52 · see citing works
Liu, Z., Zhang, H., Xia, H., Wang, B., Zhang, R., Zeng, Q., Guo, L., Shen, K., Wang, B., Zhong, Y., et al. (2019) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2019.03.002 · Cited by 53 · see citing works
Targeting the GM-CSF receptor for the treatment of CNS autoimmunity
Ifergan, I., Davidson, T. S., Kébir, H., Xu, D., Palacios-Macapagal, D., Cann, J. A., Rodgers, J. M., Hunter, Z. N., Pittet, C. L., Beddow, S. A., et al. (2017) · Journal of Autoimmunity · doi:10.1016/j.jaut.2017.06.005 · Cited by 51 · see citing works
Mehrzad, J., Hosseinkhani, S., & Malvandi, A. M. (2018) · NeuroImmunoModulation · doi:10.1159/000493528 · Cited by 50 · see citing works
The Network of Cytokines in Brain Metastases
Fares, J., Cordero, Á., Kanojia, D., & Lesniak, M. S. (2021) · Cancers · doi:10.3390/cancers13010142 · Cited by 46 · see citing works
Muls, N., Nasr, Z., Dang, H. A., Sindic, C., & Pesch, V. V. (2017) · PLoS ONE · doi:10.1371/journal.pone.0173780 · Cited by 46 · see citing works
Aarts, S. A. B. M., Seijkens, T. T. P., Kusters, P. J. H., van der Pol, S. M. A., Zarzycka, B. A., Heijnen, P. D. A. M., Beckers, L., den Toom, M., Gijbels, M. J., Boon, L., et al. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0875-9 · Cited by 40 · see citing works
Self-citationImitola, J., Rasouli, J., Watanabe, F., Mahajan, K., Sharan, A. D., Ćirić, B., Zhang, G., & Rostami, A. M. (2017) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2017.12.017 · Cited by 38 · see citing works
ZO-1 expression is suppressed by GM-CSF via miR-96/ERG in brain microvascular endothelial cells
Zhang, H., Zhang, S., Zhang, J., Liu, D., Wei, J., Fang, W., Zhao, W., Chen, Y., & Shang, D. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17702668 · Cited by 37 · see citing works
Dohlman, T. H., Ding, J. X., Dana, R., & Chauhan, S. K. (2017) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.16-20789 · Cited by 38 · see citing works
Microglia and metastases to the central nervous system: victim, ravager, or something else?
Caffarel, M. M., & Braza, M. S. (2022) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-022-02535-7 · Cited by 37 · see citing works
iNKT Cells in Secondary Progressive Multiple Sclerosis Patients Display Pro-inflammatory Profiles
Biasi, S. D., Simone, A. M., Nasi, M., Bianchini, E., Ferraro, D., Vitetta, F., Gibellini, L., Pinti, M., Giovane, C. D., Sola, P., et al. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00555 · Cited by 35 · see citing works
Mordoh, J., Pampena, M. B., Aris, M., Blanco, P. A., Lombardo, M., von Euw, E. M., Keon, S. M., Crow, M. Y., Bravo, A., O’Connor, J. M., et al. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00625 · Cited by 36 · see citing works
Chorioamnionitis, IL‐17A, and fetal origins of neurologic disease
Lawrence, S. M., & Wynn, J. L. (2017) · American Journal of Reproductive Immunology · doi:10.1111/aji.12803 · Cited by 33 · see citing works
The Role of Granulocyte-Macrophage Colony-Stimulating Factor in Murine Models of Multiple Sclerosis
Monaghan, K. L., & Wan, E. C. K. (2020) · Cells · doi:10.3390/cells9030611 · Cited by 35 · see citing works
The Mechanisms of Altered Blood–Brain Barrier Permeability in CD19 CAR T–Cell Recipients
Pinto, S., & Krenciute, G. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25010644 · Cited by 31 · see citing works
DONATIEN, P. D., Anand, U., Yiangou, Y., Sinisi, M., Fox, M., MacQuillan, A. H. F., Quick, T., Korchev, Y. E., & Anand, P. (2018) · PAIN Reports · doi:10.1097/pr9.0000000000000676 · Cited by 29 · see citing works
Nguyen, V. T. T., König, S., Eggert, S., Endres, K., & Kins, S. (2021) · Biological Chemistry · doi:10.1515/hsz-2021-0214 · Cited by 28 · see citing works
Bombeiro, A. L., Pereira, B. T. N., & de Oliveira, A. L. R. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14106 · Cited by 27 · see citing works
Fu, X., Cheng, D., Luo, Z., Wagner, A. M., Fitting, S., Cong, X. S., Xu, W., Maas, K. R., Wan, Z., Zhu, J. K., et al. (2021) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-021-10007-6 · Cited by 24 · see citing works
Fiedler, S. E., Spain, R., Kim, E., & Salinthone, S. (2020) · Immunology and Cell Biology · doi:10.1111/imcb.12392 · Cited by 24 · see citing works
Granulocyte-Macrophage Colony-Stimulating Factor as a Therapeutic Target in Multiple Sclerosis
Aram, J., Francis, A. G., Tănăsescu, R., & Constantinescu, C. S. (2018) · Neurology and Therapy · doi:10.1007/s40120-018-0120-1 · Cited by 22 · see citing works
Guo, H., Qian, L., & Cui, J. (2021) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2021.0087 · Cited by 22 · see citing works
Microglia-mediated neuroimmune suppression in PTSD is associated with anhedonia
Bonomi, R. E., Hillmer, A. T., Woodcock, E. A., Bhatt, S., Rusowicz, A., Angarita, G. A., Carson, R. E., Davis, M. T., Esterlis, I., Nabulsi, N., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2406005121 · Cited by 21 · see citing works
Mansouri, V., Yazdanpanah, N., & Rezaei, N. (2021) · International Reviews of Immunology · doi:10.1080/08830185.2021.1984449 · Cited by 21 · see citing works
Granulocyte-macrophage colony-stimulating factor as a mediator of autoimmunity in multiple sclerosis
Kostić, M. S., Živković, N., Cvetanović, A., & Stojanović, I. R. (2018) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2018.07.002 · Cited by 20 · see citing works
Human Monocytes Plasticity in Neurodegeneration
Savinetti, I., Papagna, A., & Foti, M. (2021) · Biomedicines · doi:10.3390/biomedicines9070717 · Cited by 19 · see citing works
Roles of CSF2 as a modulator of inflammation during retinal degeneration
Saita, K., Moriuchi, Y., Iwagawa, T., Aihara, M., Takai, Y., Uchida, K., & Watanabe, S. (2022) · Cytokine · doi:10.1016/j.cyto.2022.155996 · Cited by 15 · see citing works
Mei, X., Ouyang, H., Zhang, H., Jia, W., Lü, B., Zhang, J., & Ji, L. (2023) · Biochemical Pharmacology · doi:10.1016/j.bcp.2023.115808 · Cited by 15 · see citing works
Checkpoints to the Brain: Directing Myeloid Cell Migration to the Central Nervous System
Harrison‐Brown, M., Liu, G. J., & Banati, R. B. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17122030 · Cited by 14 · see citing works
de Fàbregues, O., Sellés, M. C., Ramos-Vicente, D., Roch, G., Vila, M., & Bové, J. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106308 · Cited by 13 · see citing works
Therapeutic potential of natural killer cells in neuroimmunological diseases
Zhang, Q., Lin, J., Yang, M., Li, Z., Zhang, M., & Bu, B. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.116371 · Cited by 13 · see citing works
Geranmayeh, M. H., Nourazarian, A., Avcı, Ç. B., Rahbarghazi, R., & Farhoudi, M. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0286-4 · Cited by 12 · see citing works
Shafiei, M., & Mozhgani, S. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03303-0 · Cited by 11 · see citing works
Zeng, K., Huang, M., Lyu, M.-A., Khoury, J. D., Ahmed, S., Patel, K. K., Dropulić, B., Reese‐Koc, J., Caimi, P. F., Sadeghi, T., et al. (2023) · Cells · doi:10.3390/cells12141880 · Cited by 9 · see citing works
Lo, Y.-F., Wang, S., Wu, Y., Ho, M., Yeh, C., Wu, T.-Y., Peng, J.-J., Lin, Y.-N., Ding, J.-Y., Shih, H.-P., et al. (2024) · Journal of Clinical Immunology · doi:10.1007/s10875-024-01775-w · Cited by 8 · see citing works
Profiling migration of human monocytes in response to chemotactic and barotactic guidance cues
Hall, C. K., Barr, O. M., Delamare, A., Burkholder, A., Tsai, A., Tian, Y., Ellett, F. E., Li, B. M., Tanzi, R. E., & Jorfi, M. (2024) · Cell Reports Methods · doi:10.1016/j.crmeth.2024.100846 · Cited by 9 · see citing works
Li, J., Xu, X., Zhao, Y., Wu, X., Chen, S., Xu, J., Xiao, R., Tang, J. P., Hong, X., Chen, S., et al. (2025) · Advanced Healthcare Materials · doi:10.1002/adhm.202502808 · Cited by 8 · see citing works
Gardner, R. S., Kyle, M. M., Hughes, K., & Zhao, L. (2024) · Biomolecules · doi:10.3390/biom14070827 · Cited by 7 · see citing works
Maria, Z., Turner, E., Agasing, A. M., Kumar, G., & Axtell, R. C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22062924 · Cited by 8 · see citing works
A Pan-RNase Inhibitor Enabling CRISPR-mRNA Platforms for Engineering of Primary Human Monocytes
Laoharawee, K., Johnson, M. J., Lahr, W. S., Sipe, C. J., Kleinboehl, E., Peterson, J. J., Lonetree, C.-L., Bell, J. B., Slipek, N. J., Crane, A. T., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23179749 · Cited by 7 · see citing works
Jiang, Y., Feng, D., Wang, C., Zhang, Y., Zhao, C., Su, L., Qin, Y., Chang, A. H., & Zhu, J. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.1042501 · Cited by 7 · see citing works
Chiou, H.-Y. C., Huang, S., Hung, C., Tsai, S.-M., Kuo, H.-R., Huang, Y.-R., Wang, J., Chen, S., Kuo, C., Wu, D., et al. (2021) · Biomedicines · doi:10.3390/biomedicines9080943 · Cited by 5 · see citing works
Peripheral Inflammatory Cytokine Signature Mirrors Motor Deficits in Mucolipidosis IV
Misko, A. L., Weinstock, L. D., Sankar, S. B., Furness, A., Grishchuk, Y., & Wood, L. B. (2022) · Cells · doi:10.3390/cells11030546 · Cited by 4 · see citing works
Neuromuscular complications associated with cancer immunotherapy
Xiong, G., Lomen‐Hoerth, C., Richman, D. P., & Li, T. (2025) · Journal of the National Cancer Center · doi:10.1016/j.jncc.2025.05.004 · Cited by 5 · see citing works
Crossing Barriers: In Vitro Cancer Model for Studying Monocyte Migration across Endothelial Barriers
Marway, M. K., Bhagentsang, D., Venugopal, C., Singh, S. K., Wylie, R. G., & Zhang, B. (2025) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.5c00783 · Cited by 4 · see citing works
Immunological correlates of suicidality among adolescents with internalizing symptoms
Roske, C., Nguyen, T. N. B., Schwartz, J. J., Erulker, A., Nie, K., Xie, H., Kim‐Schulze, S., Ely, B. A., Tobe, R. H., Mowrey, W. B., et al. (2024) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2024.100866 · Cited by 3 · see citing works
Microglial Regulation of Neural Networks in Neuropsychiatric Disorders
Cao, Z.-L., Zhu, L., Wang, H., & Zhu, L. (2025) · The Neuroscientist · doi:10.1177/10738584251316558 · Cited by 2 · see citing works
Role of A1 Adenosinergic System in Multiple Sclerosis and Possible Therapeutic Strategy
Justin, A., Basavaraj, M., Murugan, D., Rao, G. N., & Jeyabalan, J. B. (2022) · Research Journal of Pharmacy and Technology · doi:10.52711/0974-360x.2022.00505 · Cited by 2 · see citing works
Granulocyte-Macrophage Colony-Stimulating Factor in Central Nervous System Autoimmunity
Ćirić, B., Rasouli, J., & Rostami, A. M. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800763-1.00005-1 · Cited by 1 · see citing works
Turğut, E., Alpua, M., & Ergün, U. (2025) · Kırıkkale Üniversitesi Tıp Fakültesi Dergisi · doi:10.24938/kutfd.1643896 · Cited by 1 · see citing works
Rahman, S. S., Hussein, N. A., Galfrè, S. G., Gaertner, F., Macaubas, C., Chan, A. L., Columbo, L. A., Gao, J., Galehdari, S., Bayram, B., et al. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03549-6 · Cited by 1 · see citing works
Adrenergic signaling during parasitic infections
Gardias, P., & Bąska, P. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1691005 · Cited by 1 · see citing works
Bakhashab, S., Banafea, G. H., Ahmed, F., Alsolami, R., Schulten, H.-J., Gauthaman, K., Naseer, M. I., & Pushparaj, P. N. (2024) · PLoS ONE · doi:10.1371/journal.pone.0311981 · Cited by 1 · see citing works
McFarlane, A., Fyfe, P. K., & Moraga, I. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-820472-6.00112-2 · Cited by 1 · see citing works
Mury, P., Dupuis, J., & Thorin, É. (2020) · Canadian Journal of Cardiology · doi:10.1016/j.cjca.2020.02.068 · Cited by 1 · see citing works
Colombo, S. L., Frakich, N., & Constantinescu, C. S. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-85841-0.00012-2
Jiang, H., & Lü, J. (2025) · Psychoradiology · doi:10.1093/psyrad/kkaf004
A 3D Human Neuron‐on‐Chip Platform to Monitor Neuronal Injury Responses
Tang, R., Latchoumane, C.-F. V., Chopra, A., Sarkar, M. M., Kim, C., Gonsalves, N., Wu, H., Sentmanat, J. C., Liu, A., Mhatre‐Winters, I., et al. (2026) · Advanced Healthcare Materials · doi:10.1002/adhm.202503457
Milner, O., Fisher, R. A., Asby, D. J., Cross, S., Boche, D., & Miners, J. S. (2025) · Brain Pathology · doi:10.1111/bpa.70052
Inflammatory Mediators Both Directly and Indirectly Promote Microglial Proliferation
Hammond, B. P., Hahn, E., Lee, K. V., Kerr, B. J., & Plemel, J. R. (2026) · Glia · doi:10.1002/glia.70150
Deciphering the regulatory role of ADAM8 in the PDAC tumor microenvironment
Zandieh, K., Cook, L., Zhao, K., Nagl, C., Gao, Y., Fazio, P. D., Bartsch, D. K., Bauer, U., Meixner, M., Yildiz, D., et al. (2026) · Cellular Oncology · doi:10.1007/s13402-026-01266-7
- Authors
- Vogel, D. Y. S., Kooij, G., Heijnen, P. D. A. M., Breur, M., Peferoen, L. A. N., van der Valk, P., de Vries, H. E., Amor, S., & Dijkstra, C. D.
- Affiliations
- Amsterdam Neuroscience (NL)
- Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
- Department of Pathology, VU University Medical Center Amsterdam Amsterdam The Netherlands
- Department of Molecular Cell Biology and Immunology VU University Medical Center Amsterdam, Neuroscience Campus Amsterdam The Netherlands
- Queen Mary University of London (GB)
- Corresponding author
- Dijkstra, Christine D.
- Venue
- European Journal of Immunology
- Publisher
- Wiley
- Published
- 2015-05-03
- Volume
- 45
- Issue
- 6
- Pages
- 1808-1819
- ISSN
- 0014-2980 (ISSN-L)
- 1521-4141
- OpenAlex
- W2131992889
- Cited by
- 94
- References
- 54
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 8 · 2023: 6 · 2022: 8 · 2021: 14 · 2020: 9 · 2019: 11 · 2018: 8 · 2017: 10 · 2016: 5 · 2015: 2
- FWCI
- 6.62
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- European Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Dutch MS Research Foundation (09-358d)
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Keywords
- GM-CSF, monocyte migration, blood-brain barrier, multiple sclerosis, microglia, macrophages, GM-CSF receptor, myeloid cell infiltration, neuroinflammation, astrocytes, macrophage activation
- MeSH terms
- Adult, Aged, Aged, 80 and over, Blood-Brain Barrier, Brain, Cells, Cultured, Female, Humans, Macrophage Activation, Macrophages, Male, Middle Aged, Monocytes, Multiple Sclerosis, Gene Expression, Granulocyte-Macrophage Colony-Stimulating Factor, Receptors, Granulocyte-Macrophage Colony-Stimulating Factor, Cytokines, Reactive Oxygen Species, Microglia, Endothelial Cells, Transendothelial and Transepithelial Migration
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