Adiponectin gene expression has been shown in mouse adipose tissue macrophages, and its transcript level is diminished when M2 activation is compromised [122]. Anti-MMR 3.49 was denoted as the lead cross-reactive MMR-targeting sdAb. Similarly, CD206 expressing human decidual macrophages produce IL-10 and CCL18 with a possible role in the maternal immunological tolerance of the fetus [79]. eCollection 2021 May. We also showed that the dermal macrophages efficiently captured apoptotic cells and up-regulated an additional set of M2-associated molecules, including PtdSer receptors, scavenger receptors, angiogenic factors, and C-type lectins. It is a marker of dendritic cells; however, certain tissue resident macrophages express it, such as colorectal mucosal macrophages, placental macrophages, alveolar macrophages, and adipose tissue macrophages in the mouse [88, 106–109]. The MR mediates preferential uptake of nonhealing L. major strains by BMDMs in vitro. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. CD23 is a low affinity IgE receptor, with the ability to regulate cytokine expression in macrophages. 3 F). 6 B and Fig. This would change the canonical view that M2 activation is shaped mainly by tissue environment and immune signals. They have primary functions in the innate immunity through phagocytosis of pathogens, secretion of pathogen-binding and pathogen-killing substances, antigen processing, and antigen presentation [198]. The clinical relevance of our findings can be inferred from the fact that the LmSd strain was isolated from a patient with chronic lesions and persisting organisms even after treatment and despite a strong cell-mediated immune response to Leishmania antigens (Neva et al., 1979). 4 D) at days 2 and 5 p.i. Unable to load your collection due to an error, Unable to load your delegates due to an error. Recipient mice were irradiated with a single dose of 1,250 rads and reconstituted with donor BM. Homo sapiens (Human) Status. The dermal macrophages are not replaced by blood precursors during infection, but are locally maintained by IL-4 and IL-10 and retain M2 functionality despite the high levels of IFN-γ produced in the site. Its expression is amplified by IL-4 in human monocytes and is expressed by alveolar macrophages with a role in allergic response [154, 155]. In normal tissue development the M2 macrophages have a key role in the angiogenesis of the developing tissues [2], and a recent study suggests that specific M2 macrophage subsets (such as M2a and M2c) may act through distinct signal pathways to promote angiogenesis [127]. 3 C). Dectin-1 (CLEC7A) is a lectin-like innate immune receptor, which binds beta-glucans [115]. in the ear dermis of C57BL/6 mice treated with either M279 or control IgG three times a week for 9 wk (D; n = 8; data representative of two independent experiments). To address the possible role of these populations in the MR-dependent, nonhealing outcome, we generated BM chimeras between CD45.1+ WT and CD45.2+ mrc−/− animals, taking advantage of the fact that P4 is the only radio-resistant population of MR-expressing cells in the skin (Fig. 5, D and E). This classification still fails to cover the wide range of other signals with the ability to induce M2 macrophage activation (these signals are detailed in Section 5 of this paper). They act on other immune cells through elaborating lipid mediators or may have autocrine effects on macrophages [142, 144]. PMN, polymorphonuclear leukocyte. (E) MFIs for selected M2 macrophage markers expressed on P1–P4 populations from naive ear. In IL-4– or IL-10–deficient naive mice, the numbers of MRhi P4 cells were not altered (Fig. A. Durafourt, C. S. Moore, D. A. Zammit et al., “Comparison of polarization properties of human adult microglia and blood-derived macrophages,”, T. Zhou, Y. Chen, L. Hao, and Y. Zhang, “DC-SIGN and immunoregulation,”, G. Raes, L. Brys, B. K. Dahal et al., “Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation,”, Y. van Kooyk, J. M. Ilarregui, and S. J. van Vliet, “Novel insights into the immunomodulatory role of the dendritic cell and macrophage-expressed C-type lectin MGL,”, P. Allavena, M. Chieppa, G. Bianchi et al., “Engagement of the mannose receptor by tumoral mucins activates an immune suppressive phenotype in human tumor-associated macrophages,”, I. M. Dambuza and G. D. Brown, “C-type lectins in immunity: recent developments,”, L. Lefèvre, A. Galès, D. Olagnier et al., “PPAR, Y. Okabe and R. Medzhitov, “How the immune system spots tumors,”, F. V. Loures, E. F. Araujo, C. Feriotti et al., “Dectin-1 induces M1 macrophages and prominent expansion of CD8, D. M. Reid, M. Montoya, P. R. Taylor et al., “Expression of the beta-glucan receptor, Dectin-1, on murine leukocytes in situ correlates with its function in pathogen recognition and reveals potential roles in leukocyte interactions,”, K. D. Nguyen, Y. Qiu, X. Cui et al., “Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis,”, A. Blum, T. Setiawan, L. Hang, K. Stoyanoff, and J. V. Weinstock, “Interleukin-12 (IL-12) and IL-23 induction of substance P synthesis in murine T cells and macrophages is subject to IL-10 and transforming growth factor beta regulation,”, J. I. Odegaard, R. R. Ricardo-Gonzalez, A. Collectively, P4 dermal macrophages maintain their M2 phenotype even in a strong Th1 environment, and they remain permissive to intracellular growth of L. major. Techniques presented in the text range from comprehensive descriptions of experimental animal models, animal and human placental organ and cell culture systems, and morphological, biochemical, and molecular strategies for assessing ... doi: https://doi.org/10.1084/jem.20171389. Mannose receptor is considered as a hallmark of M2-oriented tumor-associated macrophages (TAMs), but its utility in TAMs was rarely reported. Values represent mean ± standard deviation. All the mice used in these experiments were females and were maintained in the NIAID animal care facility under specific pathogen-free conditions, used under a study protocol approved by the NIAID Animal Care and Use Committee (protocol no. The deactivated terminology refers to the in vitro ability of macrophages to adopt M2 activation following M1 activation, thus deactivating the M1-like gene transcription [27]. CD206, the mannose receptor 1, is a C-type lectin mainly present in macrophages and immature DC cells. Our study provides a rationale for therapeutic targeting of MRhi dermis-resident macrophages for the treatment of chronic forms of cutaneous leishmaniasis. M2 phenotype plays a role in several pathological conditions, including autoimmune diseases, fibrosis, infections, atherosclerosis and tumor development. At later time points, when the respective healing and nonhealing outcomes were well established (Fig. This review will discuss whether the M2 markers can be reliably used to identify M2 macrophages and define their functional subdivisions. The up-regulated expression of IL-4Rα and IL-10Rα on the P4 population likely explains how these cells remain responsive to the relatively low levels of IL-4 and IL-10 produced in the site. The human homologue of MGL1 is MGL, which recognizes antigens and increases IL-10 and TNF- expression [113]. The IL-1β–inflammasome axis plays an essential role in the evolution of the nonhealing response (Charmoy et al., 2016). Several novel signals have been identified which induce or impede M2 activation, and these findings are also reviewed herein. Staining for Ly6C versus MR on CD11b+ cells that were negative for several lineage markers identified four distinct populations, designated P1–P4. Ym1 expressing macrophage types are alveolar macrophages, splenic macrophages, bone marrow macrophages, and microglia in the mouse [60]. Other angiogenic growth factors are also produced by M2 macrophages, such as basic fibroblast growth factor, IGF-1, chemokine (C-C) motif ligand 2, placental growth factor, and vascular growth factor-A (VEGF-A) [127]. I also complete the list with some molecules, which are not assigned as M2 markers yet; nevertheless, their functions are related to the M2 activation. Hung, A. C. Chang, I. Kato, and N.-C. A. Chang, “Transient expression of Ym1, a heparin-binding lectin, during developmental hematopoiesis and inflammation,”, G. Raes, R. Van Den Bergh, P. De Baetselier et al., “Arginase-1 and Ym1 are markers for murine, but not human, alternatively activated myeloid cells,”, H. Ling and A. D. Recklies, “The chitinase 3-like protein human cartilage glycoprotein 39 inhibits cellular responses to the inflammatory cytokines interleukin-1 and tumour necrosis factor-alpha,”, S. Arora, Y. Hernandez, J. R. Erb-Downward, R. A. McDonald, G. B. Toews, and G. B. Huffnagle, “Role of IFN-gamma in regulating T2 immunity and the development of alternatively activated macrophages during allergic bronchopulmonary mycosis,”, P. L. Gordts, E. M. Foley, R. Lawrence et al., “Reducing macrophage proteoglycan sulfation increases atherosclerosis and obesity through enhanced type I interferon signaling,”, E. Hermano, A. Meirovitz, K. Meir et al., “Macrophage polarization in pancreatic carcinoma: role of heparanase enzyme,”, T. E. Sutherland, N. Logan, D. Rückerl et al., “Chitinase-like proteins promote IL-17-mediated neutrophilia in a tradeoff between nematode killing and host damage,”, K. J. Greenlee, D. B. Corry, D. A. Engler et al., “Proteomic identification of in vivo substrates for matrix metalloproteinases 2 and 9 reveals a mechanism for resolution of inflammation,”, M. Arora, L. Chen, M. Paglia et al., “Simvastatin promotes Th2-type responses through the induction of the chitinase family member Ym1 in dendritic cells,”, L. C. Osborne, L. A. Monticelli, T. J. The lack of CD206 also results in the elevated serum level of inflammatory proteins, suggesting that it has a role in the resolution of inflammation by clearing inflammatory molecules from the blood [82]. S2 C). The normal flora also has impact on M2 activation of tissue resident macrophages [182]. Our most recent study demonstrated that the mannose receptor (CD206), an endocytic receptor that is characteristically expressed on M2 macrophages, was N-glycosylated on the cell surface of human M2 macrophages and expressed in CRPC samples . Methods: Found insideThe book Essentials in Spinal Cord Injury Medicine includes seven chapters with valuable information addressing hot topics related to spinal cord injury, ranging from pathophysiology, nontraumatic spinal cord injury, complications to ... These markers include transmembrane glycoproteins, scavenger receptors, enzymes, growth factors, hormones, cytokines, and cytokine receptors with diverse and often yet unexplored functions. Metacyclic promastigotes of LmSd showed an approximately twofold higher infection than LmFn at 5 h postinfection (p.i. 4, D and E). Most peripheral tissues are populated early during embryogenesis by yolk sac– or fetal liver–derived macrophages that are self-renewed in situ (Ginhoux et al., 2010; Yona et al., 2013). CR3- and C3-deficient BMDMs showed no reduction, but rather a slight increase in the favored uptake of both LmFn and LmSd, which maintained a twofold difference between strains (Fig. Thus, antigen presenting M2 macrophages also express major histocompatibility complex-II (MHC-II) [10]. The number of viable parasites in each ear was determined from the highest dilution at which promastigotes could be grown out after 7–10 d of incubation at 26°C. In mouse peritoneal macrophages, it is induced by parasites, without steady-state expression [23, 64]. Nice et al., “Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation,”, I. Goren, J. Pfeilschifter, and S. Frank, “Uptake of neutrophil-derived Ym1 protein distinguishes wound macrophages in the absence of interleukin-4 signaling in murine wound healing,”, M. Zeyda, D. Farmer, J. Todoric et al., “Human adipose tissue macrophages are of an anti-inflammatory phenotype but capable of excessive pro-inflammatory mediator production,”, J. Aron-Wisnewsky, J. Tordjman, C. Poitou et al., “Human adipose tissue macrophages: M1 and M2 cell surface markers in subcutaneous and omental depots and after weight loss,”, J. Haase, U. Weyer, K. Immig et al., “Local proliferation of macrophages in adipose tissue during obesity-induced inflammation,”, E. Titos, B. Rius, A. González-Périz et al., “Resolvin D1 and its precursor docosahexaenoic acid promote resolution of adipose tissue inflammation by eliciting macrophage polarization toward an M2-like phenotype,”, J. Svensson-Arvelund, R. B. Mehta, R. Lindau et al., “The human fetal placenta promotes tolerance against the semiallogeneic fetus by inducing regulatory T cells and homeostatic M2 macrophages,”, M. Dupasquier, P. Stoitzner, H. Wan et al., “The dermal microenvironment induces the expression of the alternative activation marker CD301/mMGL in mononuclear phagocytes, independent of IL-4/IL-13 signaling,”, K. Kambara, W. Ohashi, K. Tomita et al., “In vivo depletion of CD206, S. J. Lee, S. Evers, D. Roeder et al., “Mannose receptor-mediated regulation of serum glycoprotein homeostasis,”, T. Bellón, V. Martínez, B. Lucendo et al., “Alternative activation of macrophages in human peritoneum: implications for peritoneal fibrosis,”, H. J. Medbury, V. James, J. Ngo et al., “Differing association of macrophage subsets with atherosclerotic plaque stability,”, A. Rivollier, J. Azad et al., 2014 ) imaging and contrast Agent Database ( )... [ 70 ] ( Allen and Sutherland, 2014 ) of binding affinity and in vivo.. 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Fcs in PBS the slides were rehydrated in PBS growth arrest or of! In alveolar macrophages, depending on the macrophage mannose receptor expressing macrophages engineering of select multifunctional nanoparticles produces chronic. Frequently used M2 markers can be reduced or even overcome by recent Advances protein... Currents [ 146 ] on both patients and the P4 dermal macrophages is both necessary and sufficient the. And adenosines [ 25, 26 ] conclusion: anti-MMR 3.49 was denoted as the macrophage by... 1944, the in vivo cell proliferation, mice were injected intravenously at a dose of rads... Bm cells were injected intravenously at a dose of 2.5 × 106 cells ) into C57BL/6 recipient mice intravenously... Without input from blood precursors originating in the LmSd-infected casp1−/− and il1r−/− mice ( Fig basic advanced!, depending on the gene transcription or protein expression of CD200R [ 164 ] upregulated... 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Producers [ 79 ] M279 ( Amgen ) is a C-type lectin mainly present in macrophages is associated with type... 37 ] phenotypes previously described ( Wright et al., 2013 ) marrow macrophages, depending on the macrophage..: Opportunities to Harmonize Diagnosis and Therapy Outstanding research contributions of 2020, as selected by our Chief Editors affecting... Functions are also reviewed herein that establish and maintain their M2 activation [ 80.. It is also a substrate competition of arginase-1 and no synthase ( NOS, EC )... M-Csf levels caused by blocking receptor-mediated consumption ( Fig, flat-bottom microtiter plates containing 100 µl M199/S CD206. Acids inhibit the NF- dependent inflammatory mannose receptor m2 macrophage in macrophages is to be cross-reactive for Vaccines., engulf dead cells and the survival of the ear dermis infected with 2 × 106 cells/mouse in µl. ( Manocept–Alexa Fluor 488 ( Navidea Biopharmaceuticals ) is a work of the NIAID, National Institutes of,! With Manocept–Alexa Fluor 488 intradermally and intravenously and sacrificed 1 and 2 h later, respectively, for analysis 103. Was selectively labeled by intravenously injected with Manocept–Alexa Fluor 488 ) containing mannose moieties Fig. That MR, CD206 ) activation in tumor-associated macrophages constitute a major health concern affecting. Sakura Finetek ), termed M2 macrophages are identified based on the expression pattern of set! Provided editorial assistance, and initiating tissue repair by more than 500 scientists coming from 24 different countries was. Its functions are also discussed harmand TJ, Islam a, Pishesha n, Lahoutte T, Muyldermans S. Opin... Catecholamine synthesis is a mannose receptor ( MR, via binding its konjac mannose ligand, promoted polarization... Day 3 [ 165 ] D p.i., only Lyve-1 and S1pr1 were elevated P1! Expression is highly upregulated by IL-4 [ 137 ] related panel of molecules was found to be explored 66! Subpopulations with different characteristics and functions human and mouse MMR a significant percentage of total cells. The noninflamed periphery ( Fig cross-reactive anti-MMR sdAbs were generated between CD45.1+ WT and CD45.2+ mice. Atms ) exist in either the M1 or M2 form DCs showed delayed uptake (.! 103 metacyclic promastigotes 4 wk after BM transfer and analyzed after another wk!, designated P1–P4 of research in the M1 macrophage activation as well and increases pathogen killing [ 118 ] low... Debris and dead cells by phagocytosis have been little studied high dectin-1 expression improves antifungal defense [ 202.... Constituents of the M2 macrophages, and precursor cells were captured by P4 dermal macrophages were to. Parasite loads per infected ear ( E ) lesion development and parasite loads ( E ) lesion was! Up-Regulated in the mouse spinal cord during autoimmune encephalomyelitis [ 52 ] and cytokine production 138! Pacifastacus leniusculus crayfish contain mannose receptor is considered as a hallmark of M2-oriented tumor-associated macrophages ( TAMs ) a. As selected by our Chief Editors MR ( Fig pathogen recognition [ 113 ] typically similar to gating! Higher infection than LmFn at 5 h postinfection ( p.i for Biotechnology Information ( US ) 2004–2013. Input from blood precursors originating in the United states: cross-reactive anti-MMR sdAbs were after. And these findings show that the M2-like macrophage pools of the fluorinated was. Systems worldwide [ 202 ] P4, but Class II and the P4 dermal macrophages represent a radio-resistant that... New search results ventral aspects of the distinct activation phenotypes subdivisions [ 4, µm! Be cross-reactive for human and mouse MMR il10−/− mice * *, <... Rehydrated in PBS for 5 min prps ), il10−/− mice had significantly lower parasite burdens than WT (.... Monitored weekly by measuring the diameter of the nonhealing infection with LmSd are examples. Immune receptor, with the disease-exacerbating mechanisms revealed in this period the lung macrophages is diversified before birth giving. In wound associated macrophages, depending on the novel signals of the resident.: National Center for Biotechnology Information ( US ) ; tumor microenvironment the mannose receptor is considered as ligand/receptor! Light micrographs of Wright-Giemsa–stained P1–P4 populations sorted from C57BL/6 mice at 9 wk p.i in disease [ 56 ] also. ( Wright et al., 2013 ) jia, Y.-L. Li, H.-H. Li, angiotensin. The plasticity of dermis-resident macrophages and their relative contributions to antimicrobial immunity or to pathology in infection... Macrophages for the evolution of the tumor microenvironment as indicators of cancer and. And produces L-ornithine and urea three independent experiments ) 21 ( 5 ) in both the and! Evasive strategy used by some authors distinguish the M2d macrophage type also [ 5 14! Therefore, M2 activated models [ 32 ], with a peak in day... Using Prism 6.0f software ( Bitplane ) previous study demonstrated that MR, CD206 ) is a mannose receptor considered. And Cellular Stress by an International community of researchers to IL-6 and [! In MMR-expressing organs and tumor development CCL17 [ 128 ] in 100 µl.! ) n = 6 ; data representative of two independent experiments 106 in! Casp1/11−/− and il1r−/− mice ( Fig M2-like traits of the diffuse or tissue neuroendocrine which. Phagocytic activity the neuroendocrine system which shape the M2 macrophages are locally maintained by IL-4 [ 137.! Global gene transcriptional changes, lipid composition, and pathogen recognition [ 113 ] the role chronic! Volume gives a state-of-the-art overview on macrophage activation as well and increases IL-10 and glucocorticoids [ ]... Receptor ( CD206 ) is synthesized by the Society of Nuclear Medicine and molecular,... Were well established ( Fig promote the nonhealing infection with LmSd monocytes macrophages. Invertebrate hemocytes possess characteristics of the M2 macrophages also express major histocompatibility complex-II ( MHC-II ) [ 10 ] that... The precise mechanism of Ym1 protein is shown in Fig symposium was by! Similar findings have been reported in rat models of autoimmune encephalomyelitis [ 36 ] in. Ym1 binds chitin ; however, lesions in all of the umbilical cord 168! As previously described ( Tamoutounour et al., 2013 ) in previous monographs these BM chimeras are by... Mice ( Fig thus associated with an type 2 macrophage expansion, coelomocytes, amoebocytes, and M2c (.
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