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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“macrophages showed elongated shape [49, 50].”
An hPSC-Derived Tissue-Resident Macrophage Model Reveals Differential Responses of Macrophages to ZIKV and DENV Infection
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 40
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
“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].”
Background
Bcl6 modulates innate immunity by controlling macrophage activity and plays critical role in experimental autoimmune encephalomyelitis
Li, 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 38
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
Cellulose nanocrystals vs. cellulose nanospheres: A comparative study of cytotoxicity and macrophage polarization potential
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 34
Canine macrophages can like human macrophages be in vitro activated toward the M2a subtype relevant in allergy
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
Macrophages undergo a behavioural switch during wound healing in zebrafish
Sipka, T., Park, S. A., Özbilgiç, R., Balas, L., Durand, T., Mikula, K., Lutfalla, G., & Chi, M. N. (2022) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2022.09.021 · Cited by 30
Erythropoietin promotes axonal regeneration after optic nerve crush in vivo by inhibition of RhoA/ROCK signaling pathway
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
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., Zahler, S., Vollmar, A. M., Weinigel, C., et al. (2017) · Scientific Reports · doi:10.1038/srep41434 · Cited by 29
“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
“Work has shown that cytoskeletal actin arrangement enables both M1 and M2 functionalities [52].”
Background
Microenvironments‐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 26
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 26
The influenza virus NS1A binding protein gene modulates macrophages response to cytokines and phagocytic potential in inflammation
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
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
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
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
NogoA-expressing astrocytes limit peripheral macrophage infiltration after ischemic brain injury in primates
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
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
“3F) and it was reported that M1-to-M2 switch is promoted by IL10 [5, 22, 23].”
Background
Targeting foamy macrophages by manipulating ABCA1 expression to facilitate lesion healing in the injured spinal cord
Wang, 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
“4 A ), consistent with the characteristic features of M1 M ϕ activation (McWhorter et al., 2013; Vereyken et al., 2011).”
Background
Imprinting 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 20
“Furthermore, addition of T3 to cultures inhibits the migratory capacity of macrophages, which is consistent with previous observations in murine M1 macrophages [140].”
Result
P2Y6 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
“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).”
Method
Development of skin inflammation test model by co-culture of reconstituted 3D skin and RAW264.7 cells
Chung, E., Choi, H., Lim, J. E., & Son, Y. (2014) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-013-1113-x · Cited by 19
Celecoxib reduces cortical spreading depression–induced macrophage activation and dilatation of dural but not pial arteries in rodents: implications for mechanism of action in terminating migraine attacks
Schain, A. J., Melo‐Carrillo, A., Ashina, S., Strassman, A. M., & Burstein, R. (2019) · Pain · doi:10.1097/j.pain.0000000000001789 · Cited by 18
“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,…”
Background
Adherent Intestinal Cells From Atlantic Salmon Show Phagocytic Ability and Express Macrophage-Specific Genes
Park, 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
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
Maspin inhibits macrophage phagocytosis and enhances inflammatory cytokine production via activation of NF-κB signaling
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
“Likely, decreased hagocytosis is protective because the respiratory burst caused by hagocytosis may produce ROS that harm the tumor microenvironent (Vernon and Tang, 2013).”
Background
Lipid Receptor G2A-Mediated Signal Pathway Plays a Critical Role in Inflammatory Response by Promoting Classical Macrophage Activation
Li, 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
Adipose tissue-derived stromal cells stimulated macrophages-endothelial cells interactions promote effective ischemic muscle neovascularization
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
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
A Matrix Metalloproteinase-9 Dependent Macrophage Subpopulation Promotes Airineme-Mediated Intercellular Communication
Bowman, R. L., Wang, D., & Eom, D. S. (2022) · Cell Reports · doi:10.1016/j.celrep.2023.112818 · Cited by 12
Macrophage Control of Phagocytosed Mycobacteria Is Increased by Factors Secreted by Alveolar Epithelial Cells through Nitric Oxide Independent Mechanisms
Petursdottír, D. H., Chuquimia, O. D., Freidl, R., & Fernández, C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103411 · Cited by 12
“[7,12,13].”
Immortalized Murine Macrophage Cell Line as a Model for Macrophage Polarization into Classically Activated M(IFNγ+LPS) or Alternatively Activated M(IL-4) Macrophages
Achita, A. B. P. (2015) · Journal of Clinical & Cellular Immunology · doi:10.4172/2155-9899.1000318 · Cited by 13
“1 cell line [27], and in human M(IFNγ+LPS) and M(IL-4) macrophages [31,32].”
Background
Tumor-associated macrophages and tumor-infiltrating lymphocytes in canine cutaneous and subcutaneous mast cell tumors
Bertola, 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
Human Umbilical Cord Mesenchymal Stem Cells Improve the Status of Hypoxic/Ischemic Cerebral Palsy Rats by Downregulating NogoA/NgR/Rho Pathway
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
“Although immune infiltration is critical for removal of harmful cells and myelin debris 40 , inflammatory consequences may exacerbate secondary neuronal cell death.”
Impact of endogenous and exogenous nitrogen species on macrophage extracellular trap (MET) formation by bone marrow–derived macrophages
Drab, D., Santocki, M., Opydo‐Chanek, M., & Kołaczkowska, E. (2023) · Cell and Tissue Research · doi:10.1007/s00441-023-03832-z · Cited by 9
“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).”
Result
Creatine 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
Plastic response of macrophages to metal ions and nanoparticles in time mimicking metal implant body environment
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
“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).”
Erythropoietin upregulates growth associated protein-43 expression and promotes retinal ganglion cell axonal regeneration in vivo after optic nerve crush.
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
“Activated macrophages secrete numerous factors that are neuroprotective for RGCs and which promote axonal regeneration [42-43] .”
Background
Engineering physical microenvironments to study innate immune cell biophysics
Kalashnikov, N., & Moraes, C. (2022) · APL Bioengineering · doi:10.1063/5.0098578 · Cited by 8
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 7
“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).”
Composite Fibrin and Carbon Microfibre Implant to Modulate Postraumatic Inflammation after Spinal Cord Injury
Escarrat, V., Pérez-Sánchez, J., Waly, B. E., Collazos-Castro, J. E., & Debarbieux, F. C. (2023) · Cells · doi:10.3390/cells12060839 · Cited by 6
“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].”
Background
Primate-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
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
“Macrophages, which are known to be heterogeneous cells, are capable of changing their morphology depending on environmental and molecular cues [20].”
Commensal microflora coating endows implants with biofilm-repellent, immunomodulatory and osteogenic properties
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
Xanthohumol, a prenylated flavonoid from hops (Humulus lupulus L.) exerts multidirectional pro-healing properties towards damaged zebrafish hair cells by regulating the innate immune response.
Kasica, N., & Kaleczyc, J. (2024) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2024.116809 · Cited by 6
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
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
“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).”
Focusing on Formyl Peptide Receptors after Traumatic Spinal Cord Injury: from Immune Response to Neurogenesis
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
“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
Morpho-functional plasticity of tumour-associated macrophages: linking cell shape, ultrastructure, and immune regulation in cancer
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
“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
“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).”
Method
Data 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
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-citation
Effects 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 · Cited by 1
“C57BL/6 mice were mostly used for macrophage polarization studies (41, 85-87).”
Method
Role 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)
Regulation of inflammation in canine species: a role for macrophages and Hsp70
Lyu, Q. (2021) · Utrecht University Repository (Utrecht University) · doi:10.33540/882

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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