Cited by 108Neuroinflammation and Neurodegeneration MechanismsMultiple Sclerosis Research StudiesImmune cells in cancer

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Classically and alternatively activated bone marrow derived macrophages differ in cytoskeletal functions and migration towards specific CNS cell types

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Vereyken, Elly JF, Heijnen, Priscilla DAM, Baron, Wia, de Vries, Elga HE, Dijkstra, Christine D, Teunissen, Charlotte E·2011·Journal of Neuroinflammation

DOI 10.1186/1742-2094-8-58PMC PMC3123187

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Abstract

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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Figure 1 Analysis of macrophage phenotype. A) Using FACS analysis the expression of markers for the differently activated phenotype was determined. CA macrophages expressed significantly more MAC-1 and F4/80 compared to AA and control macrophages. MR expression was significantly higher on AA macrophages compared to control and CA macrophages. B) NO production was undetectable in both control and AA macrophages. CA macrophages did produce NO.CC BY · PubMed Central

Figure 2 Migration of macrophages towards conditioned medium from several CNS cell types. Migration towards conditioned medium from various CNS cell types and chemokines by in vitro stimulated bone marrow derived macrophages was studied using a 48-wells micro chemotaxis chamber. The data are expressed as the mean of 4 separate experiments (n = 4) ± SEM. A) AA macrophages migrate in significantly higher numbers towards NCM compared to control medium, 191 and 77 respectively and also compared to CA macrophages, 57. * = p < 0.05. B) AA macrophages migrated in significantly higher numbers towards the fraction of the NCM containing proteins smaller than 10 kD compared to CA macrophages. Both the fractions containing proteins smaller than 10 kD and between 10 and 50 kD significantly enhanced migration of AA macrophages compared to control medium. * = p < 0.05. C) CA macrophages migrate in significantly higher numbers towards ACM compared to control medium, 92 and 59 macrophages respectively. AA macrophages did not specifically migrate towards ACM. No difference was seen in the number of migrated macrophages towards ACM between CA and AA macrophages. * = p < 0.05. D) The fraction of the ACM containing proteins smaller than 10 kD significantly enhanced the migration of CA macrophages compared to control medium and AA macrophages. * = p < 0.05. E) The different stages of oligodendrocyte development conditioned medium significantly enhanced migration of both CA and AA macrophages compared to oligodendrocyte control medium, however CA macrophages migrated in significantly higher numbers compared to AA and control macrophages. * = p < 0.05 is significantly different from control medium; # is p < 0.05 different from AA and control macrophages.CC BY · PubMed Central

Figure 3 Motility and migratory capacity. Motility of in vitro stimulated bone marrow derived macrophages was determined by timelapse video microscopy. Speed and distance covered were determined using TrackIt software. The migration towards fMLP and MCP-1 was used as a measure for migratory capacity of in vitro stimulated bone marrow derived macrophages. Adhesion was determined by plating fluorescently labeled macrophages on (un)coated 96 wells plates, washing the plates after 2 h and measuring fluorescence. Data are the mean of 3 separate experiments (n = 3) ± SEM. *= p < 0.05. A) During the recorded time the average distance AA macrophages covered was significantly enhanced twofold compared to CA macrophages. The distance was recorded in μm. B) AA macrophages had a twofold higher speed compared to CA macrophages. Speed was recorded in μm/sec. C) No difference in migration was seen between the different macrophage phenotypes when comparing migration towards either fMLP or MCP-1. D) CA macrophages displayed a trend towards higher adherence on plastic compared to control and AA macrophages. On fibronectin and collagen adherence of CA macrophages was twofold higher compared to both control and AA macrophages. E) The expression of adhesion receptors was higher in CA macrophages compared to both AA and control macrophages.CC BY · PubMed Central

Figure 4 Cytoskeleton of differently activated macrophages. A-C) Visualization of actin cytoskeleton, red: actin (rhodamine phalloidin); blue: nuclear staining (Hoechst). Representative pictures are shown. CA macrophages appear flattened and rounded. AA macrophages are more stretched and elongated. Control macrophages appear to possess morphology in between the two extremes, with some cells being more elongated while others are more rounded. The scale bar is 50 μm and a 40 times magnification was used. D) Rac and Rho activity. In CA macrophages small GTPases are more activated compared to both control and AA macrophages.CC BY · PubMed Central

Figure 5 Phagocytosis of myelin by differently activated macrophages. Phagocytosis of fluorescently labeled myelin by activated bone marrow derived macrophages and expression of CR3 was determined using flow cytometry. MFI was measured and data are the mean of 4 separate experiments (n = 4) ± SEM. *= p < 0.05 and #= p < 0.05. A) CA macrophages phagocytosed significantly more myelin compared to control and AA macrophages. B-D) Visualization of myelin internalization by phagocytosis, red: DiI labeled myelin; green: Mac-1 on macrophage membrane. Representative images, taken on a confocal microscope, are shown. Red myelin is seen inside the green labeled membrane of the differently activated macrophages. All macrophage phenotypes appear to have taken up myelin. A 20 times magnification was used. E) Using anti-MAC-1 antibody, phagocytosis of myelin by CA and control macrophages could be blocked significantly, as indicated by #. Anti-MAC-1 antibody did not affect myelin phagocytosis by AA macrophages.CC BY · PubMed Central

Figure 6 Influence of DPI and flavonoids on phagocytosis of myelin. To determine the influence of DPI, a NADPH oxidase blocker, and flavonoids on myelin phagocytosis, these substances were added together with fluorescently labeled myelin. Phagocytosis is determined as MFI of the macrophages. Data are the mean of 4 separate experiments (n = 4) ± SEM. *= p < 0.05. Both luteolin and quercetin significantly blocked phagocytosis of myelin by control, CA and AA macrophages. DPI only significantly reduced phagocytosis of myelin by control and AA macrophages. DPI did not significantly decrease phagocytosis of myelin by CA macrophages.CC BY · PubMed Central

Figure 7 Phagocytosis of neuronal fragments by differently activated macrophages. Phagocytosis of fluorescently labeled neuronal fragments by activated bone marrow derived macrophages was determined using flow cytometry. Phagocytosis was blocked using anti-MAC-1 antibodies, luteolin, quercetin and DPI. Data are the mean of 4 separate experiments (n = 4) ± SEM. *= p < 0.05 and #= p < 0.05. A) CA macrophages phagocytosed significantly more neuronal fragments compared to control and AA macrophages. B-D) Visualization of neuronal fragment internalization by phagocytosis, red: DiI labeled neuronal fragments; green: Mac-1 on macrophage membrane. Representative images, taken on a confocal microscope (Leica TCS SP2), are shown. Red labelled neuronal fragments are clearly present within the green labelled membrane of the differently activated macrophages. Some binding is also present, with the neuronal fragments being present outside the membrane. A 20 times magnification was used. E) To determine whether phagocytosis could be blocked macrophages were exposed to luteolin, quercetin, MAC-1 (anti-CR3 antibody) or DPI (NADPH oxidase blocker). Phagocytosis of neuronal fragments by all types of macrophages was significantly reduced by exposure to luteolin and quercetin. Using MAC-1 antibody did not reduce neuronal fragment phagocytosis. DPI led to a significant reduction in control macrophages, however, CA and AA macrophages did not reduce phagocytosis significantly.CC BY · PubMed Central

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In Vitro-Derived Alternatively Activated Macrophages Reduce Colonic Inflammation in Mice
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Alternatively Activated Macrophages Differentially Express Fibronectin and Its Splice Variants and the Extracellular Matrix Protein βIG‐H3
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BackgroundInfluential
Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord
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Activated Macrophage/Microglial Cells Can Promote the Regeneration of Sensory Axons into the Injured Spinal Cord
Prewitt, C. M., Niesman, I. R., Kane, C. J. M., & Houlé, J. D. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6694 · Cited by 260 · cited 7×
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BackgroundInfluential
Requirement of Myeloid Cells for Axon Regeneration
Barrette, B., Hébert, M.-A., Filali, M., Lafortune, K., Vallières, N., Gowing, G., Julien, J., & Lacroix, S. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1447-08.2008 · Cited by 256 · cited 7×
“However, macrophages can also create a growth-permissive environment in which axonal regeneration can take place during SCI [36-38].”
BackgroundInfluential
The Expression of Tissue-type Plasminogen Activator, Matrix Metalloproteases and Endogenous Inhibitors in the Central Nervous System in Multiple Sclerosis
Cuzner, M. L., Gveric, D. O., Strand, C., Loughlin, J., Paemen, L. R., Opdenakker, G., & Newcombe, J. (1996) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199612000-00002 · Cited by 251 · cited 1×
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Background
Macrophages and neurodegeneration
Hendriks, J. J. A., Teunissen, C. E., de Vries, H. E., & Dijkstra, C. D. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.12.008 · Cited by 247 · cited 1×
“Activated macrophages secrete many products that could contribute to axonal and oligodendrocyte damage seen in MS lesions, such as matrix metalloproteinases (MMPs) [15], NO and glutamate, [16-22].”
BackgroundSelf-citation
Localization of monocyte chemoattractant peptide-1 expression in the central nervous system in experimental autoimmune encephalomyelitis and trauma in the rat
Berman, J. W., Guida, M. P., Warren, J. S., Amat, J., & Brosnan, C. F. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.156.8.3017 · Cited by 245 · cited 1×
“MCP-1 expression is mainly found in reactive astrocytes and macrophages [60,61].”
Background
Laminin-2/integrin interactions enhance myelin membrane formation by oligodendrocytes.
Buttery, P., & ffrench-Constant, C. (1999) · Molecular and cellular neurosciences · doi:10.1006/mcne.1999.0781 · Cited by 217 · cited 1×
“Briefly, oligodendrocyte precursors were cultured on poly-l-lysine coated cell culture plates for 2 days in a defined SATO medium [45] containing platelet derived growth factor-AA (PDGF-AA) and fibroblast growth factor-2 (FGF-2) in order to synchronize precursors to the bipolar oligodendrocyte-type II astrocyte (O2A)…”
Method
Myelin-mediated inhibition of oligodendrocyte precursor differentiation can be overcome by pharmacological modulation of Fyn-RhoA and protein kinase C signalling
Baer, A. S., Syed, Y. A., Kang, S. U., Mitteregger, D., Vig, R., ffrench-Constant, C., Franklin, R. J. M., Altmann, F., Lubec, G., & Kotter, M. R. (2009) · Brain · doi:10.1093/brain/awn334 · Cited by 211
Alternative activation of macrophages by IL-4 impairs phagocytosis of pathogens but potentiates microbial-induced signalling and cytokine secretion
Varin, A., Mukhopadhyay, S., Herbein, G., & Gordon, S. (2009) · Blood · doi:10.1182/blood-2009-08-236711 · Cited by 194 · cited 1×
“AA macrophages were prepared by exposure to 10 ng/ml IL-4 (Invitrogen) in the culture medium [3,43].”
Method
Flavonoids Influence Monocytic GTPase Activity and Are Protective in Experimental Allergic Encephalitis
Hendriks, J. J. A., Alblas, J., van der Pol, S. M. A., van Tol, E. A. F., Dijkstra, C. D., & de Vries, H. E. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20040819 · Cited by 191 · cited 7×
“RhoA and Rac activity in differently activated macrophages was determined using G-LISA activation assay kit (Cytoskeleton, Denver, USA) according to the manufacturer’s description.”
BackgroundInfluentialSelf-citation
Remyelination in multiple sclerosis
Lassmann, H., Brück, W., Lucchinetti, C., & Rodriguez, M. (1997) · Multiple Sclerosis Journal · doi:10.1177/135245859700300213 · Cited by 191
Neuronal Chemokines: Versatile Messengers In Central Nervous System Cell Interaction
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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].”
Background
Differences in angiogenic potential of classically vs alternatively activated macrophages
Kodelja, V., Müller, C., Tenorio, S., Schebesch, C., Orfanos, C. E., & Goerdt, S. (1997) · Immunobiology · doi:10.1016/s0171-2985(97)80080-0 · Cited by 186 · cited 3×
“They produce growth factors, such as platelet derived growth factor (PDGF), vascular endothelial growth factor (VEGF) and fibroblast growth factor (FGF) [5-7].”
Background
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 · cited 1×
“In rat macrophages myelin phagocytosis was ROS dependent [68].”
BackgroundSelf-citation
Excitatory Amino Acids and Multiple Sclerosis: Evidence From Cerebrospinal Fluid
Sarchielli, P., Greco, L., Floridi, A., Floridi, A., & Gallai, V. (2003) · Archives of Neurology · doi:10.1001/archneur.60.8.1082 · Cited by 168 · cited 1×
“Activated macrophages secrete many products that could contribute to axonal and oligodendrocyte damage seen in MS lesions, such as matrix metalloproteinases (MMPs) [15], NO and glutamate, [16-22].”
Background
Macrophage phagocytosis of myelin in vitro determined by flow cytometry: phagocytosis is mediated by CR3 and induces production of tumor necrosis factor-α and nitric oxide
van der Laan, L. J. W., Ruuls, S. R., Weber, K. S., Lodder, I. J., Döpp, E. A., & Dijkstra, C. D. (1996) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(96)00110-5 · Cited by 166 · cited 1×
“CR3 is implicated in myelin phagocytosis [67].”
Self-citation
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 · cited 1×
“Macrophage adhesion to plastic and several extracellular matrix molecules (ECM) was determined as described previously [47].”
BackgroundSelf-citation
Glucocorticoids induce an activated, anti-inflammatory monocyte subset in mice that resembles myeloid-derived suppressor cells
Varga, G., Ehrchen, J. M., Tsianakas, A., Tenbrock, K., Rattenholl, A., Seeliger, S., Mack, M., Roth, J., & Sunderkötter, C. H. (2008) · Journal of Leukocyte Biology · doi:10.1189/jlb.1107768 · Cited by 160 · cited 1×
“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].”
Result
Brain antigens in functionally distinct antigen-presenting cell populations in cervical lymph nodes in MS and EAE
van 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 148 · cited 1×
“since macrophages in cervical lymph nodes of MS patients contained neuronal antigens [51].”
Background
Multipotent Adult Progenitor Cells Prevent Macrophage-Mediated Axonal Dieback and Promote Regrowth after Spinal Cord Injury
Busch, S. A., Hamilton, J. A., Horn, K. P., Cuascut, F. X., Cutrone, R., Lehman, N., Deans, R., Ting, A. E., Mays, R. W., & Silver, J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3566-10.2011 · Cited by 145 · cited 2×
“In vitro these multipotent adult progenitor cells induced an AA phenotype in macrophages [79].”
Background
T-cell- and macrophage-mediated axon damage in the absence of a CNS-specific immune response: involvement of metalloproteinases
Newman, T. A. (2001) · Brain · doi:10.1093/brain/124.11.2203 · Cited by 143
Cloning and characterization of SDF‐1γ, a novel SDF‐1 chemokine transcript with developmentally regulated expression in the nervous system
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×
“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].”
Background
Inhibitory effect of luteolin on hepatocyte growth factor/scatter factor-induced HepG2 cell invasion involving both MAPK/ERKs and PI3K–Akt pathways
Lee, 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×
“Luteolin has effects on the actin cytoskeleton [73,74] through Rho and Rac [75] and could thereby affect phagocytosis.”
Background
Flavonoids 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×
“Previously, myelin phagocytosis was blocked after exposure to quercetin and luteolin in a macrophage cell line [69].”
BackgroundSelf-citation
Leukocyte Chemotaxis
Schiffmann, E. (1982) · Annual Review of Physiology · doi:10.1146/annurev.ph.44.030182.003005 · Cited by 107 · cited 1×
“Both fMLP and MCP-1 are potent chemoattractants [57,58].”
Background
Activating 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×
“Adhesion can also be influenced by the cytoskeletal organization [62,63].”
Background
Administration of 2-arachidonoylglycerol ameliorates both acute and chronic experimental autoimmune encephalomyelitis
Lourbopoulos, 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×
“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.”
Background
Macrophages of multiple sclerosis patients display deficient SHP-1 expression and enhanced inflammatory phenotype
Christophi, 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×
“AA macrophages were prepared by exposure to 10 ng/ml IL-4 (Invitrogen) in the culture medium [3,43].”
BackgroundInfluential
Transfused 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×
“In vitro generated AA macrophages reduced renal and pancreatic injury in a model for murine diabetes [77].”
Background
Trophic support delays but does not prevent cell‐intrinsic degeneration of neurons deficient for munc18‐1
Heeroma, 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×
“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).”
Method
Alteration of the extracellular matrix interferes with raft association of neurofascin in oligodendrocytes. Potential significance for multiple sclerosis?
Maier, 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×
“rat oligodendrocytes were cultured as described previously [44].”
MethodSelf-citation
SHP-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×
“AA macrophages were prepared by exposure to 10 ng/ml IL-4 (Invitrogen) in the culture medium [3,43].”
BackgroundInfluential
Inhibitory 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 64 · cited 1×
“Luteolin has effects on the actin cytoskeleton [73,74] through Rho and Rac [75] and could thereby affect phagocytosis.”
Background
A combination immunomodulatory treatment promotes neuroprotection and locomotor recovery after contusion SCI
Iannotti, 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
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×
“Bone marrow derived macrophages were generated as described previously [42].”
Method
CCL22 regulates experimental autoimmune encephalomyelitis by controlling inflammatory macrophage accumulation and effector function
Dogan, 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×
“Treatment with anti-CCL22 [80] and Vereyken et al.”
Method
Upregulation of monocyte chemotactic protein-1 and CC chemokine receptor 2 in the central nervous system is closely associated with relapse of autoimmune encephalomyelitis in Lewis rats
Jee, 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
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×
“Adhesion can also be influenced by the cytoskeletal organization [62,63].”
Background
Expression of intercellular adhesion molecule-1 by murine macrophages is up-regulated during differentiation and inflammatory activation
Goebeler, M., Roth, J., Kunz, M., & Sorg, C. (1993) · Immunobiology · doi:10.1016/s0171-2985(11)80495-x · Cited by 26 · cited 1×
“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.”
Result
Phagocytosis by macrophages mediated by receptors for denatured proteins - dependence on tyrosine protein kinases
Hespanhol, M. R., & Mantovani, B. (2002) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2002000300015 · Cited by 11 · cited 1×
“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].”
Background
Treatment of an Infected Murine Macrophage Cell Line (J774A.1) with Interferon-γ but Not Tumor Necrosis Factor-α or Live Mycobacterium intracellulare Alone Modulates the Expression of Adhesion Molecules
Pourshafie, M. R., & Sonnenfeld, G. (1997) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.1997.17.69 · Cited by 8 · cited 8×
“The expression of Mac-1, F4/80 and MR was determined using FACS analysis.”
BackgroundResultInfluential
Chemotaxis of the peritoneal cells and the detection of a chemo‐attractant in the effluent from peritoneal dialysis patients
Bos, 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
Chemotaxis of the peritoneal cells and the detection of a chemo‐attractant in the effluent from peritoneal dialysis patients
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×
“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.”
Method
Untitled work
Zujovic (2000) · doi:10.1002/(sici)1098-1136(20000215)29:4
Untitled work
(2000) · doi:10.1002/1531-8249(200012)48:6

Research works printed but not linked: 1

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. · DOI

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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
ORCID: Baron, Wia
Teunissen, Charlotte E
Venue: Journal of Neuroinflammation
Publisher: Springer Science and Business Media LLC
Published: 2011-05-26
Volume: 8
Issue: 1
Pages: 58-58
ISSN: 1742-2094 (ISSN-L)
DOI: 10.1186/1742-2094-8-58
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 › Clinical Neurology › 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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Classically and alternatively activated bone marrow derived macrophages differ in cytoskeletal functions and migration towards specific CNS cell types

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