Classically and alternatively activated bone marrow derived macrophages differ in cytoskeletal functions and migration towards specific CNS cell types
Open accessAbstract
Background: Macrophages play an important role in neuroinflammatory diseases such as multiple sclerosis (MS) and spinal cord injury (SCI), being involved in both damage and repair. The divergent effects of macrophages might be explained by their different activation status: classically activated (CA/M1), pro-inflammatory, macrophages and alternatively activated (AA/M2), growth promoting, macrophages. Little is known about the effect of macrophages with these phenotypes in the central nervous system (CNS) and how they influence pathogenesis. The aim of this study was therefore to determine the characteristics of these phenotypically different macrophages in the context of the CNS in an in vitro setting. Results: Here we show that bone marrow derived CA and AA macrophages have a distinct migratory capacity towards medium conditioned by various cell types of the CNS. AA macrophages were preferentially attracted by the low weight (< 10 kD) fraction of neuronal conditioned medium, while CA macrophages were attracted in higher numbers by astrocyte- and oligodendrocyte conditioned medium. Intrinsic motility was twice as high in AA macrophages compared to CA macrophages. The adhesion to extracellular matrix molecules (ECM) was significantly enhanced in CA macrophages compared to control and AA macrophages. The actin cytoskeleton was differentially organized between CA and AA macrophages, possibly due to greater activity of the GTPases RhoA and Rac in CA macrophages. Phagocytosis of myelin and neuronal fragments was increased in CA macrophages compared to AA macrophages. The increase in myelin phagocytosis was associated with higher expression of CR3/MAC-1 in CA macrophages. Conclusion: In conclusion, since AA macrophages are more motile and are attracted by NCM, they are prone to migrate towards neurons in the CNS. CA macrophages have a lower motility and a stronger adhesion to ECM. In neuroinflammatory diseases the restricted migration and motility of CA macrophages might limit lesion size due to bystander damage.
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Pro-inflammatory M1 macrophages appear large and round-shaped, while anti-inflammatory M2 macrophages show an elongated shape.
“Previous studies indicated that pro-inflammatory M1 macrophages appeared large, round-shape morphology, while anti-inflammatory M2 macrophages showed elongated shape [49, 50].”
From A tailored bioactive 3D porous poly(lactic-acid)-exosome scaffold with osteo-immunomodulatory and osteogenic differentiation properties (2022) · cites this paper as [50]
The Results (Actin cytoskeleton of CA and AA macrophages, Figure 4; page not provided) describe CA/M1 macrophages as rounded and AA/M2 macrophages as elongated. The Discussion repeats this distinction, but our copy does not describe the M1 cells as large. (LLM, conf=0.86)
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“Interestingly, human AA macrophages have increased expression levels of CXCR4, the receptor for CXCL12 which is expressed in cultured neurons [52] and in normal brain [53], while CA macrophages have higher expression levels of CCR7 [54].”
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“In rat macrophages myelin phagocytosis was ROS dependent [68].”
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“Macrophage adhesion to plastic and several extracellular matrix molecules (ECM) was determined as described previously [47].”
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“Our findings were in line with a previous study, observing that glucocorticoid stimulated murine monocytes, which display some features of AA macrophages, adhered less and were more motile than control cells [64].”
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“In vitro these multipotent adult progenitor cells induced an AA phenotype in macrophages [79].”
Backgroundvan Zwam, M., Huizinga, R., Melief, M., Wierenga‐Wolf, A. F., van Meurs, M., Voerman, J. S. A., Biber, K. P. H., Boddeke, H. W. G. M., Höpken, U. E., Meisel, C., et al. (2008) · Journal of Molecular Medicine · doi:10.1007/s00109-008-0421-4 · Cited by 144 · cited 1× · see citing works
“since macrophages in cervical lymph nodes of MS patients contained neuronal antigens [51].”
BackgroundNewman, T. A. (2001) · Brain · doi:10.1093/brain/124.11.2203 · Cited by 143 · see citing works
Gleichmann, M., Gillen, C., Czardybon, M., Bosse, F., Greiner–Petter, R., Auer, J., & Müller, H. W. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00048.x · Cited by 133 · cited 1× · see citing works
“Interestingly, human AA macrophages have increased expression levels of CXCR4, the receptor for CXCL12 which is expressed in cultured neurons [52] and in normal brain [53], while CA macrophages have higher expression levels of CCR7 [54].”
BackgroundLee, W.-J., Wu, L.-F., Chen, W.-K., Wang, C., & Tseng, T. (2006) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2006.01.002 · Cited by 131 · cited 1× · see citing works
“Luteolin has effects on the actin cytoskeleton [73,74] through Rho and Rac [75] and could thereby affect phagocytosis.”
BackgroundFlavonoids inhibit myelin phagocytosis by macrophages; a structure–activity relationship study
Hendriks, J. J. A., de Vries, H. E., van der Pol, S. M. A., van den Berg, T. K., van Tol, E. A. F., & Dijkstra, C. D. (2003) · Biochemical Pharmacology · doi:10.1016/s0006-2952(02)01609-x · Cited by 115 · cited 2× · see citing works
“Previously, myelin phagocytosis was blocked after exposure to quercetin and luteolin in a macrophage cell line [69].”
BackgroundSelf-citationSchiffmann, E. (1982) · Annual Review of Physiology · doi:10.1146/annurev.ph.44.030182.003005 · Cited by 107 · cited 1× · see citing works
“Both fMLP and MCP-1 are potent chemoattractants [57,58].”
BackgroundActivating ROCK1 somatic mutations in human cancer
Lochhead, P. A., Wickman, G., Mezna, M., & Olson, M. F. (2010) · Oncogene · doi:10.1038/onc.2010.3 · Cited by 94 · cited 1× · see citing works
“Adhesion can also be influenced by the cytoskeletal organization [62,63].”
BackgroundLourbopoulos, A. I., Grigoriadis, N., Lagoudaki, R., Touloumi, O., Polyzoidou, E., Mavromatis, I., Tascos, N., Breuer, A., Ovadia, H., Karussis, D., et al. (2011) · Brain Research · doi:10.1016/j.brainres.2011.03.020 · Cited by 91 · cited 1× · see citing works
“2-arachidonoylglycerol [81], which were found to skew macrophages to an alternatively activated phenotype, increased the presence of AA macrophages in the lesions and ameliorated EAE disease course.”
BackgroundChristophi, G. P., Panos, M., Hudson, C. A., Christophi, R. L., Gruber, R. C., Mersich, A. T., Blystone, S. D., Jubelt, B., & Massa, P. T. (2009) · Laboratory Investigation · doi:10.1038/labinvest.2009.32 · Cited by 85 · cited 9× · see citing works
“AA macrophages were prepared by exposure to 10 ng/ml IL-4 (Invitrogen) in the culture medium [3,43].”
BackgroundInfluentialTransfused Macrophages Ameliorate Pancreatic and Renal Injury in Murine Diabetes Mellitus
Zheng, D., Wang, Y., Cao, Q., Lee, V. W., Zheng, G., Sun, Y., Tan, T. K., Wang, Y., Alexander, S. I., & Harris, D. C. H. (2011) · Nephron Experimental Nephrology · doi:10.1159/000321034 · Cited by 82 · cited 1× · see citing works
“In vitro generated AA macrophages reduced renal and pancreatic injury in a model for murine diabetes [77].”
BackgroundHeeroma, J. H., Roelandse, M., Wierda, K. D. B., van Aerde, K. I., Toonen, R. F. G., Hensbroek, R. A., Brussaard, A. B., Matus, A. I., & Verhage, M. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03503.x · Cited by 71 · cited 1× · see citing works
“Neuronal fragments were made by roughly pipetting 2 day old neuronal cultures, prepared as described previously [48], and labeling them with the lipophilic fluorescent dye 1,1’,di-octadecyl-3,3,3’3’-tetramethylindocarbocyanine perchlorate (DiI) (SigmaAldrich).”
MethodMaier, O., van der Heide, T., van Dam, A., Baron, W., de Vries, H., & Hoekstra, D. (2004) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2004.09.012 · Cited by 69 · cited 1× · see citing works
“rat oligodendrocytes were cultured as described previously [44].”
MethodSelf-citationSHP-1 deficiency and increased inflammatory gene expression in PBMCs of multiple sclerosis patients
Christophi, G. P., Hudson, C. A., Gruber, R. C., Christophi, C. P., Mihai, C., Mejico, L. J., Jubelt, B., & Massa, P. T. (2008) · Laboratory Investigation · doi:10.1038/labinvest.3700720 · Cited by 67 · cited 9× · see citing works
“AA macrophages were prepared by exposure to 10 ng/ml IL-4 (Invitrogen) in the culture medium [3,43].”
BackgroundInfluentialIannotti, C. A., Clark, M., Horn, K. P., van Rooijen, N., Silver, J., & Steinmetz, M. P. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.03.010 · Cited by 63 · see citing works
A method for the derivation and continuous propagation of cloned murine bone marrow macrophages
Johnson, C. R., Kitz, D. J., & Little, J. R. (1983) · Journal of Immunological Methods · doi:10.1016/0022-1759(83)90127-8 · Cited by 63 · cited 1× · see citing works
“Bone marrow derived macrophages were generated as described previously [42].”
MethodInhibitory effect of luteolin on osteoclast differentiation and function
Lee, J., Ahn, J.-Y., Hasegawa, S., Cha, B., Yonezawa, T., Nagai, K., Seo, H.-J., Jeon, W., & Woo, J. (2009) · Cytotechnology · doi:10.1007/s10616-010-9253-5 · Cited by 62 · cited 1× · see citing works
“Luteolin has effects on the actin cytoskeleton [73,74] through Rho and Rac [75] and could thereby affect phagocytosis.”
BackgroundDogan, R.-N. E., Long, N. C., Forde, E., Dennis, K. L., Kohm, A. P., Miller, S. D., & Karpus, W. J. (2010) · Journal of Leukocyte Biology · doi:10.1189/jlb.0810442 · Cited by 59 · cited 1× · see citing works
“Treatment with anti-CCL22 [80] and Vereyken et al.”
MethodJee, Y., Yoon, W. K., Okura, Y., Tanuma, N., & Matsumoto, Y. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00147-9 · Cited by 55 · see citing works
BCL2 inhibits cell adhesion, spreading, and motility by enhancing actin polymerization
Ke, H., Parron, V. I., Reece, J. M., Zhang, J. Y., Akiyama, S. K., & French, J. E. (2010) · Cell Research · doi:10.1038/cr.2010.21 · Cited by 45 · cited 1× · see citing works
“Adhesion can also be influenced by the cytoskeletal organization [62,63].”
BackgroundGoebeler, M., Roth, J., Kunz, M., & Sorg, C. (1993) · Immunobiology · doi:10.1016/s0171-2985(11)80495-x · Cited by 26 · cited 1× · see citing works
“The increased expression of adhesion receptors in macrophages stimulated with IFN-g and LPS is in line with previous studies [49,65] and with our current finding that CA macrophages adhere better when compared to AA macrophages.”
ResultHespanhol, M. R., & Mantovani, B. (2002) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2002000300015 · Cited by 11 · cited 1× · see citing works
“Quercetin could also mediate its effects due to the inhibition of protein tyrosine kinases, which are involved in the signaling of the engulfment phase of CR3 mediated phagocytosis [72].”
BackgroundPourshafie, M. R., & Sonnenfeld, G. (1997) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.1997.17.69 · Cited by 8 · cited 8× · see citing works
“The expression of Mac-1, F4/80 and MR was determined using FACS analysis.”
BackgroundResultInfluentialBos, H. J., Boorsma, D. M., Tuk, C. W., de Veld, J. C., van den Muysenberg, A. J. C., Helmerhorst, T. J. M., Struijk, D. G., van Bronswijk, H., & Beelen, R. H. J. (1990) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1990.tb01901.x · Cited by 7 · see citing works
Bos, H. J., BOORSMA, D. M., Tuk, C. W., et al. (1990) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1990.tb01926.x · Cited by 6 · cited 1× · see citing works
“The migratory capacity of CA and AA macrophages was studied using a 48-wells micro chemotaxis chamber (Neuro Probe, Gaithersburg, USA) as described previously [46] with some modifications.”
MethodZujovic (2000) · doi:10.1002/(sici)1098-1136(20000215)29:4
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- van der Laan LJ Ruuls SR Weber KS Lodder IJ Dopp EA Dijkstra CD Macrophage phagocytosis of myelin in vitro determined by flow cytometry: phagocytosis is mediated by CR3 and induces production of tumor necrosis factor-alpha and nitric oxide J Neuroimmunol 1996 70 145 152 10.1016/S0165-5728(96)00110-5 8898723 · DOI
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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-citationPhysical and mechanical regulation of macrophage phenotype and function
McWhorter, F. Y., Davis, C. T., & Liu, W. F. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1796-8 · Cited by 437 · see citing works
“LPS or M1-like activation has been demonstrated to enhance cell adhesion in both human and murine macrophages [49, 64, 67].”
BackgroundResultInfluentialMacrophage biology in the peripheral nervous system after injury
Zigmond, R. E., & Echevarría, F. D. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.12.001 · Cited by 369 · see citing works
“With respect to Wallerian degeneration, Vereyken et al. (2011) showed that M(LPS-IFNγ) macrophages consumed a greater amount of fluorescent myelin than M(IL-4) macrophages, suggesting that M(LPS-IFNγ) have a greater propensity for myelin phagocytosis.”
Function of microglia and macrophages in secondary damage after spinal cord injury
Ren, Y., Zhou, X., & He, X. (2014) · Neural Regeneration Research · doi:10.4103/1673-5374.143423 · Cited by 317 · see citing works
“Several macrophage subsets have been classified based on the expression of cell surface markers, intracellular enzymes, and secreted molecules, including M1 (classical activation), M2 (alternative activation), regulatory macrophages, tumor-associated macrophages (TAM), myeloid-derived suppressor cells (MDSC), and so f…”
Natrajan, M. S., de la Fuente, A. G., Crawford, A. H., Linehan, E., Núñez, V., Johnson, K. R., Wu, T., Fitzgerald, D. C., Ricote, M., Bielekova, B., et al. (2015) · Brain · doi:10.1093/brain/awv289 · Cited by 217 · see citing works
Differential regulation of macrophage inflammatory activation by fibrin and fibrinogen
Hsieh, J., Smith, T. D., Meli, V., Trần, T. N. L., Botvinick, E., & Liu, W. F. (2016) · Acta Biomaterialia · doi:10.1016/j.actbio.2016.09.024 · Cited by 206 · see citing works
Macrophage polarization in response to epigenetic modifiers during infection and inflammation
Patel, U., Rajasingh, S., Samanta, S., Cao, T., Dawn, B., & Rajasingh, J. (2016) · Drug Discovery Today · doi:10.1016/j.drudis.2016.08.006 · Cited by 216 · see citing works
“During lung inflammation, the M1 and M2 macrophages are two distinct phenotypes with important roles in producing inflammatory and anti-inflammatory factors, respectively, to combat the injury [74,75].”
BackgroundMa, S., Chen, Y.-J., Zhang, J., Shen, L., Wang, R., Zhou, J.-S., Hu, J., & Lü, H. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.11.007 · Cited by 201 · see citing works
“IL-6, NO, and TNF-a levels were markedly higher in M1 than in M0 and M2 cell cultures (P 0.01), whereas M2 cells produced higher levels of IL-10 and TGF-b than the other macrophage subtypes (P < 0.01) (Fig.”
InfluentialQian, Y., Lin, H., Yan, Z., Shi, J., & Fan, C. (2021) · Materials Today · doi:10.1016/j.mattod.2021.09.014 · Cited by 193 · see citing works
Image based Machine Learning for identification of macrophage subsets
Rostam, H. M., Reynolds, P. M., Alexander, M. R., Gadegaard, N., & Ghaemmaghami, A. M. (2017) · Scientific Reports · doi:10.1038/s41598-017-03780-z · Cited by 196 · see citing works
“Their data suggested that M1 macrophages appeared large, rounded and flat while M2 macrophages were stretched and elongated cells 36 .”
BackgroundMicroglia in central nervous system repair after injury
Jin, X., & Yamashita, T. (2016) · The Journal of Biochemistry · doi:10.1093/jb/mvw009 · Cited by 191 · see citing works
Macrophages 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-citationElectric fields are novel determinants of human macrophage functions
Hoare, J. I., Rajnicek, A. M., McCaig, C., Barker, R. N., & Wilson, H. M. (2015) · Journal of Leukocyte Biology · doi:10.1189/jlb.3a0815-390r · Cited by 164 · see citing works
Acidity promotes tumour progression by altering macrophage phenotype in prostate cancer
El-Kenawi, A., Gatenbee, C., Robertson‐Tessi, M., Bravo, R., Dhillon, J., Balagurunathan, Y., Berglund, A., Vishvakarma, N. K., Ibrahim‐Hashim, A., Choi, J. W., et al. (2019) · British Journal of Cancer · doi:10.1038/s41416-019-0542-2 · Cited by 147 · see citing works
Bannon, P., Wood, S., Restivo, T., Campbell, L., Hardman, M., & Mace, K. (2013) · Disease Models & Mechanisms · doi:10.1242/dmm.012237 · Cited by 154 · see citing works
“Pro-inflammatory, classically activated macrophages have been shown to be more adherent than alternatively activated macrophages in a variety of assays (Gordon, 2003; Vereyken et al., 2011).”
BackgroundCougoule, C., Goethem, E. V., Cabec, V. L., Lafouresse, F., Dupré, L., Mehraj, V., Mège, J., Lastrucci, C., & Maridonneau‐Parini, I. (2012) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2012.07.002 · Cited by 127 · see citing works
The Thyroid Hormone Triiodothyronine Controls Macrophage Maturation and Functions
Perrotta, C., Buldorini, M., Assi, E., Cazzato, D., Palma, C. D., Clementi, E., & Cervia, D. (2013) · American Journal Of Pathology · doi:10.1016/j.ajpath.2013.10.006 · Cited by 128 · see citing works
Díez-Tercero, L., Delgado, L. M., Bosch-Rué, È., & Pérez, R. A. (2021) · Scientific Reports · doi:10.1038/s41598-021-91070-0 · Cited by 129 · see citing works
Macrophage-Derived Cholesterol Contributes to Therapeutic Resistance in Prostate Cancer
El-Kenawi, A., Dominguez‐Viqueira, W., Liu, M., Awasthi, S., Abraham-Miranda, J., Keske, A., Steiner, K. K., Noel, L. C., Serna, A. N., Dhillon, J., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-4028 · Cited by 114 · see citing works
“Primary cells: Bone marrow-derived macrophages (BMDMs) were generated as described previously (15,16).”
MethodHeinrich, F., Lehmbecker, A., Raddatz, B. B., Kegler, K., Tipold, A., Stein, V. M., Kalkuhl, A., Deschl, U., Baumgärtner, W., Ulrich, R., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0183572 · Cited by 110 · see citing works
Immunoregulation of macrophages by dynamic ligand presentation via ligand–cation coordination
Kang, H., Yang, B., Zhang, K., Pan, Q., Yuan, W., Li, G., & Bian, L. (2019) · Nature Communications · doi:10.1038/s41467-019-09733-6 · Cited by 106 · see citing works
The roles of microglia and astrocytes in myelin phagocytosis in the central nervous system
Xu, T., Liu, C., Deng, S., Gan, L., Zhang, Z., Yang, G., Tian, H., & Tang, Y. (2022) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x221137762 · Cited by 106 · see citing works
Activation of pial and dural macrophages and dendritic cells by cortical spreading depression
Schain, A. J., Melo‐Carrillo, A., Borsook, D., Grutzendler, J., Strassman, A. M., & Burstein, R. (2018) · Annals of Neurology · doi:10.1002/ana.25169 · Cited by 105 · see citing works
“Existing literature supports the notion that macrophages adopt a rounded shape when activated.(37,38) Based on this body of evidence and on our observation that exposure to LPS also caused the meningeal macrophages to retract their processes, we interpret the findings as suggesting that CSD activates pial macrophages…”
ResultChuquimia, O. D., Petursdottír, D. H., Períolo, N., & Fernández, C. (2012) · Infection and Immunity · doi:10.1128/iai.00950-12 · Cited by 102 · see citing works
Kang, H., Kim, S., Wong, D. S. H., Jung, H. J., Lin, S., Zou, K., Li, R., Li, G., Dravid, V. P., & Bian, L. (2017) · Nano Letters · doi:10.1021/acs.nanolett.7b03405 · Cited by 94 · see citing works
Kang, H., Jung, H. J., Kim, S., Wong, S. H. D., Lin, S., Li, G., Dravid, V. P., & Bian, L. (2018) · ACS Nano · doi:10.1021/acsnano.8b02226 · Cited by 86 · see citing works
Glial hemichannels and their involvement in aging and neurodegenerative diseases
Orellana, J. A., Rommy von Bernhardi, M., Giaume, C., & Sáez, J. C. (2012) · Reviews in the Neurosciences · doi:10.1515/revneuro-2011-0065 · Cited by 86 · see citing works
Chen, K.-H. E., Lainez, N. M., & Coss, D. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.2000490 · Cited by 73 · see citing works
Macrophages in microgravity: the impact of space on immune cells
Ludtka, C., Silberman, J., Moore, E., & Allen, J. B. (2021) · npj Microgravity · doi:10.1038/s41526-021-00141-z · Cited by 73 · see citing works
Cell engineering: Biophysical regulation of the nucleus
Song, Y., Soto, J., Chen, B., Yang, L., & Li, S. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2019.119743 · Cited by 68 · see citing works
Singleton, H., Graham, S. P., Bodman-Smith, K. B., Frossard, J., & Steinbach, F. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00832 · Cited by 66 · see citing works
Cathepsin Inhibition Modulates Metabolism and Polarization of Tumor-Associated Macrophages
Oelschlägel, D., Sadan, T. W., Salpeter, S. J., Krug, S., Blum, G., Schmitz, W., Schulze, A., & Michl, P. (2020) · Cancers · doi:10.3390/cancers12092579 · Cited by 63 · see citing works
“This correlates with differences in actin organization between M1 and M2 macrophages [56,59].”
BackgroundKartikasari, N., Yamada, M., Watanabe, J., Tiskratok, W., He, X., Kamano, Y., & Egusa, H. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.10.019 · Cited by 55 · see citing works
Sikkema, A. H., Stoffels, J. M. J., Wang, P., Basedow, F. J., Bulsink, R., Bajramovic, J. J., & Baron, W. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1238-x · Cited by 58 · see citing works
Self-citationThe shift in macrophages polarisation after tendon injury: A systematic review
Xu, H.-T., Lee, C., Li, R. M. Y., Wang, Y.-F., Yung, P. S., & Lee, O. K. (2019) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2019.11.009 · Cited by 56 · see citing works
“Previous studies have demonstrated that the migration speed of Mφs is inversely correlated to intracellular tensions [76], andM2 primaryMφs has been shown to be muchmore shifting than M1 Mφs in the absence of chemoattractant in murine [77].”
BackgroundMoran, C. S., Jose, R. J., Moxon, J. V., Roomberg, A., Norman, P. E., Rush, C. M., Körner, H., & Golledge, J. (2013) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.112.301006 · Cited by 52 · see citing works
“Increased production of superoxide anions, and oxygen and nitrogen radicals is characteristic of classical activation and M1 differentiation, whereas CD206 (mannose receptor) is a signature marker for alternative activation and the M2 phenotype.(40) In vitro, an M1 phenotype can be induced in macrophages by exposure t…”
BackgroundTaniguchi, K., Hikiji, H., Okinaga, T., Hashidate‐Yoshida, T., Shindou, H., Ariyoshi, W., Shimizu, T., Tominaga, K., & Nishihara, T. (2015) · Journal of Cellular Biochemistry · doi:10.1002/jcb.25230 · Cited by 50 · see citing works
“JOURNAL OF CELLULAR BIOCHEMISTRY LPCAT3 REGULATES M1M2-MACROPHAGE POLARIZATION 2845 2015], surface antigen presentation, production of chemokines and cytokines [Biswas et al., 2006; Umemura et al., 2008], and phagocytic activity [Vereyken et al., 2011].”
BackgroundShin, T., Ahn, M., Moon, C., Kim, S., & Sim, K. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8398-6 · Cited by 47 · see citing works
Tyteca, D., Nishino, T., Debaix, H., Smissen, P. V. D., N’Kuli, F., Hoffmann, D., Cnops, Y., Rabolli, V., Loo, G., Beyaert, R., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117398 · Cited by 45 · see citing works
“Among these features for M2 are: cell elongation [27], formation of lamellipodia [48,49], and increased migration [26].”
BackgroundZhang, Y., Huo, M., Wang, Y., Xiao, L., Wu, J., Ma, Y., Zhang, D., Lang, X., & Wang, X. (2022) · Journal of Biological Engineering · doi:10.1186/s13036-022-00301-z · Cited by 43 · see citing works
“macrophages showed elongated shape [49, 50].”
Lang, J., Cheng, Y., Rolfe, A. J., Hammack, C., Vera, D. L., Kyle, K. E., Wang, J., Meissner, T. B., Ren, Y., Cowan, C. A., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.06.006 · Cited by 41 · see citing works
CSF-1R Signaling in Health and Disease: A Focus on the Mammary Gland
Dwyer, A. R., & Pixley, F. J. (2014) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-014-9320-1 · Cited by 40 · see citing works
“In addition, an IL-4-induced M2 phenotype is a necessary element of the paracrine interaction and IL-4 treated macrophages move significantly faster than control macrophages [23,110].”
BackgroundLi, Q., Zhou, L., Wang, L., Li, S., Xu, G., Gu, H., Li, D., Liu, M., Fang, L., Wang, Z., et al. (2020) · European Journal of Immunology · doi:10.1002/eji.201948299 · Cited by 39 · see citing works
SDF-1/CXCL12: Its role in spinal cord injury
Järve, A., Bosse, F., & Müller, H. W. (2011) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2011.11.023 · Cited by 36 · see citing works
Patel, D. K., Ganguly, K., Dutta, S. D., Patil, T. V., & Lim, K. (2022) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2022.120464 · Cited by 33 · see citing works
Herrmann, I., Gotovina, J., Fazekas, J., Fischer, M. B., Hufnagl, K., Bianchini, R., & Jensen‐Jarolim, E. (2018) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2018.01.005 · Cited by 31 · see citing works
Macrophages undergo a behavioural switch during wound healing in zebrafish.
Sipka, T., Park, S.-A., Ozbilgic, R., Balas, L., Durand, T., Mikula, K., Lutfalla, G., & Nguyen-Chi, M. (2022) · Free Radical Biology & Medicine · doi:10.1016/j.freeradbiomed.2022.09.021 · Cited by 27 · see citing works
Tan, H., Zhong, Y., Shen, X. P., Cheng, Y., Qin, J., & Deng, L. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.037 · Cited by 28 · see citing works
Modulation of actin dynamics as potential macrophage subtype-targeting anti-tumour strategy
Pergola, C., Schubert, K., Pace, S., Ziereisen, J., Nikels, F., Scherer, O., Hüttel, S., Stefan Zahler, A., Vollmar, A. M., Weinigel, C., et al. (2017) · Scientific Reports · doi:10.1038/srep41434 · Cited by 28 · see citing works
“Note that mouse bone-marrow-derived M2 possess a higher intrinsic motility than M1, seemingly related to different cytoskeletal functions 39 .”
The Effects of Simulated Microgravity on Macrophage Phenotype
Ludtka, C., Moore, E., & Allen, J. B. (2021) · Biomedicines · doi:10.3390/biomedicines9091205 · Cited by 26 · see citing works
“Work has shown that cytoskeletal actin arrangement enables both M1 and M2 functionalities [52].”
BackgroundMicroenvironments‐Modulated Biomaterials Enhance Spinal Cord Injury Therapy
Li, Y., Zhang, Q., Liu, Z., Fu, C., & Ding, J. (2024) · Advanced Functional Materials · doi:10.1002/adfm.202403900 · Cited by 25 · see citing works
Sex-specific impact of maternal obesity on fetal placental macrophages and cord blood triglycerides
Shook, L. L., James, K. E., Roberts, D. J., Powe, C. E., Perlis, R. H., Thornburg, K. L. R., O’Tierney-Ginn, P. F., & Edlow, A. G. (2023) · Placenta · doi:10.1016/j.placenta.2023.08.001 · Cited by 25 · see citing works
Hotter, G., Mastora, C., Jung, M., Brüne, B., Carbonell, T., Josa‐Laorden, C., Pérez‐Calvo, J. I., Cruzado, J. M., Guiteras, R., & Solà, A. (2020) · Scientific Reports · doi:10.1038/s41598-020-72342-7 · Cited by 23 · see citing works
Computational modeling of cytokine signaling in microglia
Anderson, W. D., Makadia, H. K., Greenhalgh, A. D., Schwaber, J. S., David, S., & Vadigepalli, R. (2015) · Molecular BioSystems · doi:10.1039/c5mb00488h · Cited by 25 · see citing works
Polypharmacologic Reprogramming of Tumor-Associated Macrophages toward an Inflammatory Phenotype
Nishida‐Aoki, N., & Gujral, T. S. (2021) · Cancer Research · doi:10.1158/0008-5472.can-21-1428 · Cited by 24 · see citing works
The Topography of Silica Films Modulates Primary Macrophage Morphology and Function
Makaremi, S., Luu, H., Boyle, J. P., Zhu, Y., Cerson, C., Bowdish, D. M. E., & Moran-Mirabal, J. M. (2019) · Advanced Materials Interfaces · doi:10.1002/admi.201900677 · Cited by 23 · see citing works
Boghdadi, A. G., Spurrier, J. M., Teo, L., Li, M., Škarica, M., Cao, B., Kwan, W. C., Merson, T. D., Nilsson, S. K., Šestan, N., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-27245-0 · Cited by 25 · see citing works
Agmatine Modulates the Phenotype of Macrophage Acute Phase after Spinal Cord Injury in Rats
Kim, J. Y., Kim, J. Y., Mun, C. H., Suh, M., & Lee, J. E. (2017) · Experimental Neurobiology · doi:10.5607/en.2017.26.5.278 · Cited by 20 · see citing works
“3F) and it was reported that M1-to-M2 switch is promoted by IL10 [5, 22, 23].”
BackgroundWang, X., Cheng, Z., Tai, W., Shi, M., Ayazi, M., Liu, Y., Sun, L. J., Yu, C., Fan, Z., Bin, G., et al. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.04.013 · Cited by 19 · see citing works
“4 A ), consistent with the characteristic features of M1 M ϕ activation (McWhorter et al., 2013; Vereyken et al., 2011).”
BackgroundImprinting of maternal thyroid hormones in the offspring
Opazo, M. C., Haensgen, H., Böhmwald, K., Venegas, L. F., Boudin, H., Elorza, Á. A., Simón, F., Fardella, C., Bueno, S. M., Kalergis, A. M., et al. (2017) · International Reviews of Immunology · doi:10.1080/08830185.2016.1277216 · Cited by 19 · see citing works
“Furthermore, addition of T3 to cultures inhibits the migratory capacity of macrophages, which is consistent with previous observations in murine M1 macrophages [140].”
ResultP2Y6 Receptors Regulate CXCL10 Expression and Secretion in Mouse Intestinal Epithelial Cells
Salem, M., Tremblay, A., Pelletier, J., Robaye, B., & Sévigny, J. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00149 · Cited by 19 · see citing works
“The migrated macrophages were collected from the bottom chambers and counted with a hemocytometer, as detailed in previous studies (Vereyken et al., 2011; Unver et al., 2015).”
MethodChung, E., Choi, H., Lim, J. E., & Son, Y. (2014) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-013-1113-x · Cited by 19 · see citing works
Schain, A. J., Melo‐Carrillo, A., Ashina, S., Strassman, A. M., & Burstein, R. (2019) · Pain · doi:10.1097/j.pain.0000000000001789 · Cited by 18 · see citing works
“recently that CSD causes pial and dural macrophages, which are present mainly around blood vessels, to retract their podia (cytoplasmic processes), and interpreted this behavior as an indication of activation.(37,50,51) Timewise, we noted that although pial macrophages became activated minutes after occurrence of CSD,…”
BackgroundPark, Y., Zhang, Q., Wiegertjes, G. F., Fernandes, J. M. O., & Kiron, V. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.580848 · Cited by 17 · see citing works
Divergent results induced by different types of septic shock in transglutaminase 2 knockout mice
Yoo, H. J., Ahn, E.-R., Kim, S.-J., Lee, S.-H., Oh, S. H., & Kim, S. (2012) · Amino Acids · doi:10.1007/s00726-012-1412-x · Cited by 17 · see citing works
Wang, Y., Sun, L., Song, Z., Wang, D., Bao, Y., & Li, Y. (2017) · Molecular Immunology · doi:10.1016/j.molimm.2016.12.021 · Cited by 16 · see citing works
“Likely, decreased hagocytosis is protective because the respiratory burst caused by hagocytosis may produce ROS that harm the tumor microenvironent (Vernon and Tang, 2013).”
BackgroundLi, Q., Feng, C., Li, L., Xu, G., Gu, H., Li, S., Li, D., Liu, M., Han, S., & Zheng, B. Q. (2021) · The Journal of Immunology · doi:10.4049/jimmunol.2000231 · Cited by 16 · see citing works
Czapla, J., Cichoń, T., Pilny, E., Jarosz–Biej, M., Matuszczak, S., Drzyzga, A., Krakowczyk, Ł., & Smolarczyk, R. (2020) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2020.173354 · Cited by 13 · see citing works
ATF2 orchestrates macrophage differentiation and activation to promote antibacterial responses
Rajabalee, N., Siushansian, H., Weerapura, M., Berton, S., Berbatovci, F., Hooks, B. G., Geoffrion, M., Yang, D., Harper, M., Rayner, K. J., et al. (2023) · Journal of Leukocyte Biology · doi:10.1093/jleuko/qiad076 · Cited by 12 · see citing works
Bowman, R. L., Wang, D., & Eom, D. S. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112818 · Cited by 12 · see citing works
Petursdottír, D. H., Chuquimia, O. D., Freidl, R., & Fernández, C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103411 · Cited by 12 · see citing works
“[7,12,13].”
Achita, A. B. P. (2015) · Journal of Clinical & Cellular Immunology · doi:10.4172/2155-9899.1000318 · Cited by 13 · see citing works
“1 cell line [27], and in human M(IFNγ+LPS) and M(IL-4) macrophages [31,32].”
BackgroundBertola, L., Pellizzoni, B., Giudice, C., Grieco, V., Ferrari, R., Chiti, L. E., Stefanello, D., Manfredi, M., Zani, D. D., & Recordati, C. (2024) · Veterinary Pathology · doi:10.1177/03009858241244851 · Cited by 10 · see citing works
Luo, Y., Qu, J., He, Z., Zhang, M., Zou, Z., Li, L., Zhang, Y., & Ye, J. (2023) · Cell Transplantation · doi:10.1177/09636897231210069 · Cited by 9 · see citing works
“Although immune infiltration is critical for removal of harmful cells and myelin debris 40 , inflammatory consequences may exacerbate secondary neuronal cell death.”
Drab, D., Santocki, M., Opydo‐Chanek, M., & Kołaczkowska, E. (2023) · Cell and Tissue Research · doi:10.1007/s00441-023-03832-z · Cited by 9 · see citing works
“Although at this point, we do not know why flow cytometric analyses indicated lower expression of F4/80 than immunocy-tochemical one, the surface presence of LFA-1 confirmed the expected differentiation and is in line with literature on BMDMs (Vereyken et al. 2011).”
ResultCreatine promotes the repair of peripheral nerve injury by affecting macrophage polarization
Li, Y., Jin, X., Yang, X., Zhang, L., & Qi, Z. (2022) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2022.03.047 · Cited by 8 · see citing works
Navrátilová, P., Emmer, J., Tomas, T., Ryba, L., Burda, J., Loja, T., Veverková, J., Válková, L., & Goldbergová, M. P. (2023) · Environmental Science and Pollution Research · doi:10.1007/s11356-023-31430-7 · Cited by 8 · see citing works
“Thanks to this, we can confirm the theory that the round morphology of the cells could actually correspond to the M1 phenotype, which is in accordance with other studies (Vereyken et al. 2011; McWhorter et al. 2013; Tarique et al. 2015).”
Tan, H., Kang, X., Zhong, Y., Shen, X. P., Cheng, Y., Qin, J., & Deng, L. (2012) · Europe PMC (PubMed Central) · doi:10.3969/j.issn.1673-5374.2012.04.010 · Cited by 8 · see citing works
“Activated macrophages secrete numerous factors that are neuroprotective for RGCs and which promote axonal regeneration [42-43] .”
BackgroundEngineering physical microenvironments to study innate immune cell biophysics
Kalashnikov, N., & Moraes, C. (2022) · APL Bioengineering · doi:10.1063/5.0098578 · Cited by 7 · see citing works
Single-nucleus RNA-seq dissection of choroid plexus tumor cell heterogeneity
Hill, A. D., Okonechnikov, K., Herr, M., Thomas, C., Thongjuea, S., Hasselblatt, M., & Patrizi, A. (2024) · The EMBO Journal · doi:10.1038/s44318-024-00283-2 · Cited by 6 · see citing works
“This morphology suggests a wound healing/anti-in fl ammatory bias (Costa et al, 2023; Donadon et al, 2020; McWhorter et al, 2013; Rostam et al, 2017; Vereyken et al, 2011).”
Escarrat, V., Pérez-Sánchez, J., Waly, B. E., Collazos-Castro, J. E., & Debarbieux, F. C. (2023) · Cells · doi:10.3390/cells12060839 · Cited by 6 · see citing works
“Ramified morphology is associated with pro-healing activated microglia and round morphology with pro-inflammatory phagocytic microglia, consistent with the need for cell debris clearance prior to the stimulation of axonal regeneration [37,38].”
BackgroundPrimate-specific response of astrocytes to stroke limits peripheral macrophage infiltrationPreprint
Boghdadi, A. G., Spurrier, J. M., Teo, L., Li, M., Škarica, M., Cao, B., Kwan, W. C., Merson, T. D., Nilsson, S. K., Šestan, N., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.08.083501 · Cited by 6 · see citing works
Exogenous Ubiquitin Differentially Modulates the Phenotype and Function of M1 and M2 Macrophages
Shook, P. L., Wang‐Heaton, H., Casteel, J. L., Dalal, S., Singh, M., Yakubenko, V. P., & Singh, K. (2025) · Cells · doi:10.3390/cells14120879 · Cited by 5 · see citing works
“Macrophages, which are known to be heterogeneous cells, are capable of changing their morphology depending on environmental and molecular cues [20].”
Rahim, M. I., Baseer, S., Paasch, D., Steglich, M., Waqas, S. F., Lachmann, N., Falk, C. S., & Stiesch, M. (2026) · Acta Biomaterialia · doi:10.1016/j.actbio.2026.01.017 · Cited by 5 · see citing works
Kasica, N., & Kaleczyc, J. (2024) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2024.116809 · Cited by 6 · see citing works
The significance of M1 macrophage should be highlighted in peripheral nerve regeneration.
Feng, R., & Zhang, P. (2023) · PubMed · doi:10.14670/hh-18-591 · Cited by 5 · see citing works
OnabotulinumtoxinA alters pro- and anti-inflammatory dural macrophage response to CSD in female mice
Schain, A. J., Fajardo, D. D., Strassman, A. M., Kulkarni, S., Broide, R. S., Brideau-Andersen, A. D., Adams, A. M., Brin, M. F., & Burstein, R. (2025) · Cephalalgia · doi:10.1177/03331024251378730 · Cited by 4 · see citing works
“Macrophages in their non-activated state (M0) can be polarized into the pro-in fl ammatory “ classically ” activated M1 pathway, which can be associated with a contracting shape change (49 – 51), and secretion of multiple pro-nociceptive molecules such as IL6, IL12, TNF-α , and IL1 β (21,25 – 27).”
Pu, Z., Luo, D., Shuai, B., Xu, Y., Liu, M., & Zhao, J. (2025) · Neurochemical Research · doi:10.1007/s11064-025-04347-5 · Cited by 2 · see citing works
“IL-10, notably, catalyzes the trans - differentiation from an M1 to an M2 phenotype [49 ].”
Isolation of Human Osteal Macrophages
Bousch, J. F., Lichtenberg, S., Schnitker, M., Schlösser, J., Suschek, C. V., Maus, U. M., & Beyersdorf, C. (2026) · Life · doi:10.3390/life16030376 · Cited by 1 · see citing works
Kizhakkanoodan, K. S., Inigo, V. J., Laxminarayana, S. L. K., Seetharam, R. N., Guruprasad, K. P., & Guru, B. R. (2026) · Clinical and Experimental Medicine · doi:10.1007/s10238-026-02190-8 · Cited by 1 · see citing works
“While IFN-γ/LPS-treated M1 cells often adopt a “fried-egg” appearance with perinuclear actin clus - tering, IL-4-treated M2 types display spindle-shaped forms with actin localized at the cell periphery [ 13].”
Polypharmacological Re-programming of Tumor-associated Macrophages Restores Antitumor ImmunityPreprint
Nishida‐Aoki, N., & Gujral, T. S. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.10.439265 · Cited by 1 · see citing works
“strongly with pro-tumor phenotypes (Benner et al., 2019; Cabanel et al., 2015; Chen et al., 2017; Hollmen et al., 2015; Hu et al., 2021; Porcheray et al., 2005; Su et al., 2014; Vereyken et al., 2011), we adopted cellular elongation quantified by live-cell imaging as an indicator of TAM polarization (Figure 1A).”
MethodData from Macrophage-Derived Cholesterol Contributes to Therapeutic Resistance in Prostate Cancer
El-Kenawi, A., Dominguez‐Viqueira, W., Liu, M., Awasthi, S., Abraham-Miranda, J., Keske, A., Steiner, K. K., Noel, L. C., Serna, A. N., Dhillon, J., et al. (2023) · doi:10.1158/0008-5472.c.6513003 · Cited by 1 · see citing works
Modelling Multiple Sclerosis In Vitro and the Influence of Activated Macrophages
Vereyken, E. J. F., Dijkstra, C. D., & Teunisse, C. E. (2011) · InTech eBooks · doi:10.5772/30525
“Our studies have shown that macrophage migration towards CNS cell types differs upon skewing [Vereyken et al., 2011] and that migration of macrophages in spheroids is limited and varies with skewing of the macrophages (Figure 4E).”
BackgroundMethodResultInfluentialSelf-citationEffects of Macrophages and Monocytes in Remyelination of the CNS
Natrajan, M. S., Bielekova, B., & Franklin, R. J. M. (2015) · Wiley eBooks · doi:10.1002/9781118732748.ch13
The role of syndecan-1 in the resolution of chronic inflammatory responses
Angsana, J. (2013) · SMARTech Repository (Georgia Institute of Technology)
ПОЛЯРИЗАЦИЯ МАКРОФАГОВ В СОВРЕМЕННОЙ КОНЦЕПЦИИ ФОРМИРОВАНИЯ ИММУННОГО ОТВЕТА
Lyamina, S., Malyshev, I. Y., & Evdokimov, A. I. (2014) · CyberLeninK (CyberLeninka)
Macrophage Polarization and Function in Cystic Fibrosis
Tarique, A. A. (2016) · The University of Queensland · doi:10.14264/uql.2016.680
“C57BL/6 mice were mostly used for macrophage polarization studies (41, 85-87).”
MethodRole of alveolar epithelial cells in macrophage responses against mycobacterial infections
Flores, C., & Daniela, O. (2013)
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)
- Authors
- Vereyken, E. J., Heijnen, P. D., Baron, W., de Vries, E. H., Dijkstra, C. D., & Teunissen, C. E.
- Affiliations
- Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
- University Medical Center Groningen (NL)
- Corresponding author
- Dijkstra, Christine D
- Venue
- Journal of Neuroinflammation
- Published
- 2011-05-26
- Volume
- 8
- Issue
- 1
- Pages
- 58-58
- ISSN
- 1742-2094 (ISSN-L)
- PMC
- PMC3123187
- OpenAlex
- W2165155335
- Cited by
- 108
- References
- 85
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 5 · 2023: 11 · 2022: 6 · 2021: 11 · 2020: 8 · 2019: 5 · 2018: 8 · 2017: 7 · 2016: 5 · 2015: 7 · 2014: 9 · 2013: 6 · 2012: 6
- FWCI
- 4.06
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Journal of Neuroinflammation (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, cc-by)
- Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Pure Amsterdam UMC (submittedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (016.056.024)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Keywords
- macrophage polarization, M1 macrophages, M2 macrophages, bone marrow-derived macrophages, macrophage migration, conditioned medium, actin cytoskeleton, RhoA, Rac GTPase, extracellular matrix adhesion, phagocytosis, myelin phagocytosis, astrocytes, oligodendrocytes, neurons, neuroinflammation, multiple sclerosis, spinal cord injury
- MeSH terms
- Actins, Animals, Cell Movement, Cells, Cultured, Central Nervous System, Cytoskeleton, Flavonoids, Macrophages, Mice, Inbred C57BL, Myelin Sheath, Neuroglia, Neurons, Phagocytosis, Phenotype, Culture Media, Conditioned, Mice
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