LacdiNAc-glycans constitute a parasite pattern for galectin-3-mediated immune recognition
Abstract
Although Galβ1–4GlcNAc (LacNAc) moieties are the most common constituents of N-linked glycans on vertebrate proteins, GalNAcβ1–4GlcNAc (LacdiNAc, LDN)-containing glycans are widespread in invertebrates, such as helminths. We postulated that LDN might be a molecular pattern for recognition of helminth parasites by the immune system. Using LDN-based affinity chromatography and mass spectrometry, we have identified galectin-3 as the major LDN-binding protein in macrophages. By contrast, LDN binding was not observed with galectin-1. Surface plasmon resonance (SPR) analysis and a solid phase binding assay demonstrated that galectin-3 binds directly to neoglycoconjugates carrying LDN glycans. In addition, galectin-3 bound to Schistosoma mansoni soluble egg Ags and a mAb against the LDN glycan inhibited this binding, suggesting that LDN glycans within S. mansoni soluble egg Ags contribute to galectin-3 binding. Immunocytochemistry demonstrated high levels of galectin-3 in liver granulomas of S. mansoni-infected hamsters, and a colocalization of galectin-3 and LDN glycans was observed on the parasite eggshells. Finally, we demonstrate that galectin-3 can mediate recognition and phagocytosis of LDN-coated particles by macrophages. These findings provide evidence that LDN-glycans constitute a parasite pattern for galectin-3-mediated immune recognition.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The schistosome-specific GalNAc-di-GalNAc (LDN) motif is bound by soluble galectin-3.
“The schistosome-specific GalNAc-di-GalNAc (LDN) motif is bound by soluble galectin-3”
From Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules (2018) · cites this paper as van den Berg et al., 2004
Cites
Galectins: A family of animal β-galactoside-binding lectins
Barondes, S. H., Castronovo, V., Cooper, D. N. W., Cummings, R. D., Drickamer, K., Felzi, T., Gitt, M. A., Hirabayashi, J., Hughes, C., Kasai, K.-I., et al. (1994) · Cell · doi:10.1016/0092-8674(94)90498-7 · Cited by 1,223 · cited 1× · see citing works
“of mammalian -galactoside binding lectins (14, 15).”
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Galectin-3: An open-ended story
Dumić, J., Dabelić, S., & Flögel, M. (2006) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2005.12.020 · Cited by 1,171 · see citing works
Turning 'sweet' on immunity: galectin–glycan interactions in immune tolerance and inflammation
Rabinovich, G. A., & Toscano, M. A. (2009) · Nature reviews. Immunology · doi:10.1038/nri2536 · Cited by 900 · see citing works
Protein-glycan interactions in the control of innate and adaptive immune responses
van Kooyk, Y., & Rabinovich, G. A. (2008) · Nature Immunology · doi:10.1038/ni.f.203 · Cited by 800 · see citing works
Roles of galectins in infection
Vasta, G. R. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2146 · Cited by 531 · see citing works
Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules
Maizels, R. M., Smits, H. H., & McSorley, H. J. (2018) · Immunity · doi:10.1016/j.immuni.2018.10.016 · Cited by 435 · see citing works
The Role of Protein Glycosylation in Allergy
Altmann, F. (2007) · International Archives of Allergy and Immunology · doi:10.1159/000096114 · Cited by 393 · see citing works
Sato, S., St‐Pierre, C., Bhaumik, P., & Nieminen, J. (2009) · Immunological Reviews · doi:10.1111/j.1600-065x.2009.00790.x · Cited by 298 · see citing works
“64. van den Berg TK, et al. LacdiNAc-glycans constitute a parasite pattern for galectin-3- mediated immune recognition.”
BackgroundThe role of galectins in immunity and infection
Liu, F., & Stowell, S. R. (2023) · Nature reviews. Immunology · doi:10.1038/s41577-022-00829-7 · Cited by 329 · see citing works
Self-citationSurvey of the year 2003 commercial optical biosensor literature
Rich, R. L., & Myszka, D. G. (2004) · Journal of Molecular Recognition · doi:10.1002/jmr.726 · Cited by 505 · see citing works
Jouault, T., Behi, M. E. A.-E., Martínez-Esparza, M., Breuilh, L., Trinel, P., Chamaillard, M., Trottein, F., & Poulain, D. (2006) · Journal of Immunology · doi:10.4049/jimmunol.177.7.4679 · Cited by 256 · see citing works
van Vliet, S. J., van Liempt, E., Saeland, E., Aarnoudse, C. A., Appelmelk, B., Irimura, T., Geijtenbeek, T. B. H., Blixt, O., Alvarez, R., van Die, I., et al. (2005) · International Immunology · doi:10.1093/intimm/dxh246 · Cited by 238 · see citing works
Tasumi, S., & Vasta, G. (2007) · Journal of Immunology · doi:10.4049/jimmunol.179.5.3086 · Cited by 225 · see citing works
“Only a few examples of recognition of exogenous ligands by galectins have been reported, namely the binding of mammalian galectins-3 and -9 to polygalactose moieties of Leishmania major (56, 57), and the binding of galectin-3 to soluble and egg shell-associated glycans of the parasite helminth Schistosoma mansoni disp…”
BackgroundGalectin-3 Induces Death of Candida Species Expressing Specific β-1,2-Linked Mannans
Kohatsu, L., Hsu, D. K., Jegalian, A. G., Liu, F., & Baum, L. G. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.7.4718 · Cited by 221 · see citing works
“And, although galectin-3 is known to participate in phagocytosis of microbial PAMPcoated beads (29), we observed the fungicidal effect of galectin-3 in the absence of macrophages or other cells of the mammalian immune system.”
BackgroundSelf-citationSurvey of the year 2004 commercial optical biosensor literature
Rich, R. L., & Myszka, D. G. (2005) · Journal of Molecular Recognition · doi:10.1002/jmr.753 · Cited by 116 · see citing works
Glycan gimmickry by parasitic helminths: A strategy for modulating the host immune response?
van Die, I., & Cummings, R. D. (2010) · Glycobiology · doi:10.1093/glycob/cwp140 · Cited by 199 · see citing works
Self-citationRegulatory Roles of Galectins in the Immune Response
Liu, F. (2005) · International Archives of Allergy and Immunology · doi:10.1159/000084545 · Cited by 191 · see citing works
Self-citationSchistosoma mansoni egg antigens induce Treg that participate in diabetes prevention in NOD mice
Zaccone, P., Burton, O. T., Miller, N. G. A., Jones, F. M., Dunne, D. W., & Cooke, A. (2009) · European Journal of Immunology · doi:10.1002/eji.200838871 · Cited by 175 · see citing works
Tomlin, H., & Piccinini, A. M. (2018) · Immunology · doi:10.1111/imm.12972 · Cited by 198 · see citing works
Galectin-3 Is a Negative Regulator of Lipopolysaccharide-Mediated Inflammation
Li, Y., Komai‐Koma, M., Gilchrist, D. S., Hsu, D. K., Liu, F., Springall, T., & Xu, D. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.4.2781 · Cited by 163 · see citing works
“It has been suggested that galectin-3 may serve as a pathogen pattern recognition receptor to visualize PAMPs from bacteria (19, 20), parasites (21, 22), and fungi (23, 24).”
BackgroundSelf-citationGalectin-3 interacts with naïve and primed neutrophils, inducing innate immune responses
Nieminen, J., St-Pierre, C., & Sato, S. (2005) · Journal of Leukocyte Biology · doi:10.1189/jlb.1204702 · Cited by 126 · see citing works
“In addition, the expression and release of galectin-3 are suggested to be upregulated in various infection/inflammation cases, such as arthritis, hepatic cirrhosis, a murine model of asthma, diabetes, parasitic infection, and streptococcal pneumonia [16, 29–34].”
BackgroundMantelli, F., Mauris, J., & Argüeso, P. (2013) · Current Opinion in Allergy and Clinical Immunology · doi:10.1097/aci.0b013e3283645899 · Cited by 136
“It has emerged that carbohydrate-binding proteins recognize glycan antigens on allergens and parasitic helminths, which may contribute to the orchestration of immune responses [24,25].”
BackgroundRabinovich, G. A., & Gruppi, A. (2005) · Parasite Immunology · doi:10.1111/j.1365-3024.2005.00749.x · Cited by 134 · see citing works
André, S., Pei, Z., Siebert, H., Ramström, O., & Gabius, H. (2006) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2006.05.045 · Cited by 129 · see citing works
CD66b Regulates Adhesion and Activation of Human Eosinophils1
Yoon, J., Terada, A., & Kita, H. (2007) · Journal of Immunology · doi:10.4049/jimmunol.179.12.8454 · Cited by 124 · see citing works
“Galectin-3 may also decorate the cell surface carbohydrate molecules on microorganisms; this would allow eosinophils to recognize potential targets (54, 55).”
BackgroundGlycomics Analysis of Schistosoma mansoni Egg and Cercarial Secretions*S
Jang-Lee, J., Curwen, R. S., Ashton, P. D., Tissot, B., Mathieson, W., Panico, M., Dell, A., Wilson, R. A., & Haslam, S. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m700004-mcp200 · Cited by 124 · see citing works
“a whole range of lectins (39, 45, 46), to be investigated.”
BackgroundBreuilh, L., Vanhoutte, F., Fontaine, J., van Stijn, C. M. W., Tillie‐Leblond, I., Capron, M., Faveeuw, C., Jouault, T., van Die, I., Gosset, P., et al. (2007) · Infection and Immunity · doi:10.1128/iai.02006-06 · Cited by 109 · see citing works
Cerliani, J., Stowell, S., Mascanfroni, I., Arthur, C., Cummings, R., & Rabinovich, G. (2011) · Journal of Clinical Immunology · doi:10.1007/s10875-010-9494-2 · Cited by 110 · see citing works
Self-citationMutational Tuning of Galectin-3 Specificity and Biological Function
Salomonsson, E., Carlsson, M. C., Osla, V., Hendus-Altenburger, R., Kahl-Knutson, B., Öberg, C. T., Sundin, A., Nilsson, R., Karlsson, E. N., Nilsson, U. J., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.098160 · Cited by 121 · see citing works
Galectin-1 promotes HIV-1 infectivity in macrophages through stabilization of viral adsorption.
Mercier, S., St‐Pierre, C., Pelletier, I., Ouellet, M., Tremblay, M., & Sato, S. (2008) · Virology · doi:10.1016/j.virol.2007.09.034 · Cited by 106 · see citing works
“This is in contrast to its ability to facilitate the interaction between parasites and macrophages (Pelletier et al., 2003; van den Berg et al., 2004).”
Parasitic helminths: a pharmacopeia of anti-inflammatory molecules
Johnston, M. J., MacDonald, J. A., & McKay, D. M. (2008) · Parasitology · doi:10.1017/s0031182008005210 · Cited by 103 · see citing works
“This in- teraction has been implicated in granuloma formation (van den Berg et al. 2004) (recently disputed by Bickle and Helmby, 2007) and in eosinophilmediated cytotoxicity (Truong et al. 1993), although the effect on eosinophils could be reduced by the galectin-3 inhibition of IL-5 production…”
BackgroundSmit, C. H., van Diepen, A., Nguyen, D., Wuhrer, M., Hoffmann, K., Deelder, A., & Hokke, C. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m115.048280 · Cited by 101 · see citing works
Self-citationZaccone, P., Burton, O., Gibbs, S. E., Miller, N., Jones, F. M., Dunne, D., & Cooke, A. (2010) · Journal of Biomedicine and Biotechnology · doi:10.1155/2010/795210 · Cited by 100 · see citing works
Evolving Mechanistic Insights into Galectin Functions
Arthur, C. M., Dias‐Baruffi, M., Cummings, R. D., & Stowell, S. R. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1396-1_1 · Cited by 129 · see citing works
Self-citationWuhrer, M., Balog, C. I. A., Catalina, M., Jones, F. M., Schramm, G., Haas, H., Doenhoff, M., Dunne, D. W., Deelder, A., & Hokke, C. (2006) · The FEBS Journal · doi:10.1111/j.1742-4658.2006.05242.x · Cited by 92 · see citing works
Self-citationKrzeminski, M., Singh, T., André, S., Lensch, M., Wu, A. M., Bonvin, A. M. J. J., & Gabius, H. (2010) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2010.11.001 · Cited by 79 · see citing works
Galectin-3 impacts Cryptococcus neoformans infection through direct antifungal effects
Almeida, F. B. D. R., Wolf, J. M., da Silva, T. A., DeLeon‐Rodriguez, C. M., Rezende, C. P., Pessoni, A. M., Fernandes, F. F., Silva‐Rocha, R., Martínez, R., Rodrigues, M. L., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-02126-7 · Cited by 101 · see citing works
Shainheit, M. G., Smith, P. M., Bazzone, L. E., Wang, A. C., Rutitzky, L. I., & Stadecker, M. J. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.12.8559 · Cited by 74 · see citing works
Glycoconjugates in Host-Helminth Interactions
Prasanphanich, N., Mickum, M. L., Heimburg-Molinaro, J., & Cummings, R. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00240 · Cited by 85 · see citing works
Self-citationSchistosome glycans and innate immunity
Hokke, C., & Yazdanbakhsh, M. (2005) · Parasite immunology (Print) · doi:10.1111/j.1365-3024.2005.00781.x · Cited by 85 · see citing works
Self-citationGlycans modulate immune responses in helminth infections and allergy.
van Die, I., & Cummings, R. (2006) · Chemical Immunology · doi:10.1159/000088883 · Cited by 84 · see citing works
Self-citationKaltner, H., Abad‐Rodríguez, J., Corfield, A. P., Kopitz, J., & Gabius, H. (2019) · Biochemical Journal · doi:10.1042/bcj20170853 · Cited by 108 · see citing works
Yoshino, T., Dinguirard, N., Kunert, J., & Hokke, C. (2008) · Gene · doi:10.1016/j.gene.2008.01.003 · Cited by 78 · see citing works
“…of the innate immune system of vertebrates (Vasta et al., 2004a; Rabinovitch et al., 2002), such as phagocytosis (Sano et al., 2003), pattern-recognition of parasite antigens (Young and Meeusen, 2004; Van der Berg et al., 2004), and especially regulation of T-cell activation and apoptosis Gene.”
BackgroundSelf-citationCarbohydrate recognition systems in autoimmunity
Buzás, E. I., Buzás, E. I., György, B., Buzás, E. I., György, B., Pásztói, M., Jelinek, I., Falus, A., & Gabius, H. (2006) · Autoimmunity · doi:10.1080/08916930601061470 · Cited by 75 · see citing works
“helminth parasites) sensed by a member of the galectin family [25].”
Repeats of LacdiNAc and fucosylated LacdiNAc on N‐glycans of the human parasite Schistosoma mansoni
Wuhrer, M., Koeleman, C., Deelder, A., & Hokke, C. (2006) · The FEBS Journal · doi:10.1111/j.1742-4658.2005.05068.x · Cited by 77 · see citing works
Self-citationIntegrating transcriptome, proteome and glycome analyses of Schistosoma biology.
Hokke, C., Fitzpatrick, J. M., & Hoffmann, K. (2007) · Trends in Parasitology · doi:10.1016/j.pt.2007.02.007 · Cited by 76 · see citing works
Self-citationSweet complementarity: the functional pairing of glycans with lectins
Gabius, H.-J., Manning, J. C., Kopitz, J., André, S., & Kaltner, H. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2163-8 · Cited by 74 · see citing works
Singh, B. N., Hayes, G. R., Lucas, J. J., Sommer, U., Viseux, N., Mirgorodskaya, E., Trifonova, R., Sassi, R. R., Costello, C., & Fichorova, R. (2008) · Glycoconjugate Journal · doi:10.1007/s10719-008-9157-1 · Cited by 73
“Galectins are expressed in several cell types, including epithelial cells, and are known to play vital roles in host-pathogen interactions and immune recognition [50–52].”
Polarization of host immune responses by helminth‐expressed glycans
Tundup, S., Srivastava, L., & Harn, Jr. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06618.x · Cited by 71 · see citing works
Key regulators of galectin–glycan interactions
Kamili, N. A., Arthur, C. M., Gerner‐Smidt, C., Tafesse, E., Blenda, A. V., Dias‐Baruffi, M., & Stowell, S. R. (2016) · PROTEOMICS · doi:10.1002/pmic.201600116 · Cited by 87 · see citing works
“In addition to glycolipids, galectins similarly display differential recognition of other modifications to the core LacNAc structure, including the T antigen (Gal 1-3GalNAc), LacDiNAc (GalNAc 1-4GlcNAc) and type 1 (Gal 1-3GlcNac) versus type II (Gal 1-4GlcNAc) LacNAc glycan structures [80, 109, 110].”
BackgroundMicrobe–Host Interactions are Positively and Negatively Regulated by Galectin–Glycan Interactions
Baum, L., Garner, O., Schaefer, K., & Lee, B. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00284 · Cited by 69 · see citing works
“A direct role for galectin-3 in the phagocytosis of helminths such as Schistosoma mansoni has been proposed (51).”
BackgroundHomann, A., Schramm, G., & Jappe, U. (2017) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2017.04.019 · Cited by 68 · see citing works
Helminth glycomics - glycan repertoires and host-parasite interactions.
Hokke, C., & van Diepen, A. (2017) · Molecular and biochemical parasitology (Print) · doi:10.1016/j.molbiopara.2016.12.001 · Cited by 67 · see citing works
Self-citationInterplay of parasite-driven immune responses and autoimmunity
Zaccone, P., Burton, O. T., & Cooke, A. (2007) · Trends in Parasitology · doi:10.1016/j.pt.2007.10.006 · Cited by 60 · see citing works
Gender-specific expression of complex-type N-glycans in schistosomes.
Wuhrer, M., Koeleman, C., Fitzpatrick, J. M., Hoffmann, K., Deelder, A., & Hokke, C. (2006) · Glycobiology · doi:10.1093/glycob/cwl020 · Cited by 65 · see citing works
“…major targets of the humoral immune response during schistosomiasis (Omer-Ali et al., 1986; Eberl et al., 2001), and some have recently been described as ligands for lectins of the human immune system (van den Berg et al., 2004; van Liempt et al., 2004; Meyer et al., 2005; van Vliet et al., 2005).”
BackgroundSelf-citationFeng, C., Ghosh, A., Amin, M., Giomarelli, B., Shridhar, S., Banerjee, A., Fernández-Robledo, J., Bianchet, M., Wang, L.-X., Wilson, I., et al. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.476531 · Cited by 64
“Although not specific for A oligosaccharides, some galectins can recognize nonreducing terminal GalNAc moieties in exogenous ligands, such as the human galectin-3 that binds to soluble and egg shell-associated glycans of the parasite helminth Schistosoma mansoni displaying GalNAc 1–4GlcNAc (41).”
BackgroundMammalian galectins: Structure, carbohydrate specificity, and functions
Rapoport, E., Kurmyshkina, O., & Bovin, N. (2008) · Biochemistry (Moscow) · doi:10.1134/s0006297908040032 · Cited by 64 · see citing works
Design–functionality relationships for adhesion/growth-regulatory galectins
Ludwig, A.-K., Michalak, M., Xiao, Q., Gilles, U., Medrano, F., Ma, H., FitzGerald, F. G., Hasley, W. D., Melendez-Davila, A., Liu, M., et al. (2019) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1813515116 · Cited by 61 · see citing works
Debierre-Grockiego, F., Niehus, S., Coddeville, B., Elass, E., Poirier, F., Weingart, R., Schmidt, R., Mazurier, J., Guérardel, Y., & Schwarz, R. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.137588 · Cited by 61 · see citing works
van de Vijver, K. K., Deelder, A., Jacobs, W., Marck, E. V., & Hokke, C. (2006) · Glycobiology · doi:10.1093/glycob/cwj058 · Cited by 61 · see citing works
Self-citationPohleven, J., Renko, M., Magister, Š., Smith, D. F., Künzler, M., S̆trukelj, B., Turk, D., Kos, J., & Sabotič, J. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.317263 · Cited by 57
“It has been proposed that LDNglycans constitute a molecular pattern for immune recognition of parasites mediated by mammalian galectin-3 (23).”
BackgroundOliveira, F., Frazão, P., Chammas, R., Hsu, D., Liu, F.-T., Borojevic, R., Takiya, C., & El-Cheikh, M. C. (2007) · Journal of Leukocyte Biology · doi:10.1189/jlb.1206747 · Cited by 57 · see citing works
Self-citationThe roles of galectins in parasitic infections
Shi, W., Xue, C.-Y., Su, X.-Z., & Lu, F.-L. (2017) · Acta Tropica · doi:10.1016/j.actatropica.2017.09.027 · Cited by 56
Meevissen, M. H. J., Yazdanbakhsh, M., & Hokke, C. (2012) · Experimental parasitology · doi:10.1016/j.exppara.2011.05.005 · Cited by 56 · see citing works
Self-citationAn immune responsive multidomain galectin from bay scallop Argopectens irradians.
Song, X.-Y., Zhang, H., Zhao, J.-M., Wang, L.-L., Qiu, L., Mu, C.-K., Liu, X.-L., Qiu, L.-H., & Song, L.-S. (2010) · Fish and Shellfish Immunology · doi:10.1016/j.fsi.2009.11.016 · Cited by 55 · see citing works
“More importantly, galectins functioned as PRRs by binding saccharide ligands on the microbial surface or their components to trigger host immune responses both in vertebrates [10,40,41] and invertebrates [18e21].”
BackgroundDetermination of Carbohydrate‐Binding Preferences of Human Galectins with Carbohydrate Microarrays
Horlacher, T., Oberli, M. A., Werz, D. B., Kröck, L., Bufali, S., Mishra, R., Sobek, J., Simons, K., Hirashima, M., Niki, T., et al. (2010) · ChemBioChem · doi:10.1002/cbic.201000020 · Cited by 59 · see citing works
Galectin Binding to Neo-Glycoproteins: LacDiNAc Conjugated BSA as Ligand for Human Galectin-3
Böcker, S., Laaf, D., & Elling, L. (2015) · Biomolecules · doi:10.3390/biom5031671 · Cited by 52
“Due to the fact that Gal-1 does not bind to LacDiNAc [60,65,83,84], weak binding of Gal-1 to LacDiNAc-LacNAc conjugated BSA is based on recognizing the internal LacNAc unit since multiple ligands are presented.”
BackgroundToegel, S., Bieder, D., André, S., Altmann, F., Walzer, S. M., Kaltner, H., Hofstaetter, J. G., Windhager, R. H., & Gabius, H. (2013) · Arthritis Research & Therapy · doi:10.1186/ar4330 · Cited by 53 · see citing works
Meevissen, M. H. J., Balog, C., Koeleman, C., Doenhoff, M., Schramm, G., Haas, H., Deelder, A., Wuhrer, M., & Hokke, C. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m110.005710 · Cited by 52 · see citing works
Self-citationFerraz, L. C., Bernardes, E. S., Oliveira, A. F., Ruas, L. P., Fermino, M. L., Soares, S. G., Loyola, A. M., Oliver, C., Jamur, M. C., Hsu, D. K., et al. (2008) · European Journal of Immunology · doi:10.1002/eji.200737986 · Cited by 45 · see citing works
Self-citationTargeting Galectins With Glycomimetics
Bertuzzi, S., Quintana, J. I., Ardá, A., Gimeno, A., & Jiménez-Barbero, J. (2020) · Frontiers in Chemistry · doi:10.3389/fchem.2020.00593 · Cited by 49
Kawar, Z., Haslam, S., Morris, H., Dell, A., & Cummings, R. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m414273200 · Cited by 47 · see citing works
Self-citationFajka-Boja, R., Blaskó, A., Kovács-Sólyom, F., Szebeni, G. J., Tóth, G. K., & Monostori, É. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8143-x · Cited by 46
Robijn, M. L. M., Koeleman, C., Wuhrer, M., Royle, L., Geyer, R., Dwek, R., Rudd, P., Deelder, A., & Hokke, C. (2007) · Molecular and biochemical parasitology (Print) · doi:10.1016/j.molbiopara.2006.10.019 · Cited by 44 · see citing works
Self-citationPathogenic Roles of CD14, Galectin-3, and OX40 during Experimental Cerebral Malaria in Mice
Oakley, M., Majam, V., Mahajan, B., Gerald, N., Anantharaman, V., Ward, J., Faucette, L. J., Mccutchan, T., Zheng, H., Terabe, M., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006793 · Cited by 43
Differential Liver Protein Expression during Schistosomiasis
Harvie, M., Jordan, T., & Flamme, A. L. L. (2006) · Infection and Immunity · doi:10.1128/iai.01048-06 · Cited by 42 · see citing works
Regulation of expression and secretion of galectin-3 in human monocyte-derived dendritic cells.
van Stijn, C. M. W., van den Broek, M., van de Weerd, R., Visser, M., Taşdelen, I., Tefsen, B., & van Die, I. (2009) · Molecular Immunology · doi:10.1016/j.molimm.2009.07.026 · Cited by 41 · see citing works
Galectin-3 in Inflammasome Activation and Primary Biliary Cholangitis Development
Arsenijević, A., Stojanović, B., Milovanović, J., Arsenijević, D., Arsenijević, N., & Milovanović, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21145097 · Cited by 40 · see citing works
Canis, K., Anzengruber, J., Garenaux, E., Feichtinger, M., Benamara, K., Scheiflinger, F., Savoy, L., Reipert, B., & Mališauskas, M. (2018) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.14204 · Cited by 39 · see citing works
Kaltner, H., Caballero, G. G., Ludwig, A., Manning, J. C., & Gabius, H. (2018) · Histochemistry and Cell Biology · doi:10.1007/s00418-018-1676-7 · Cited by 44 · see citing works
Mukaro, V., Bylund, J., Hodge, G., Holmes, M., Jersmann, H., Reynolds, P., & Hodge, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056147 · Cited by 39 · see citing works
Rapoport, E., André, S., Kurmyshkina, O., Pochechueva, T., Severov, V., Pazynina, G., Gabius, H., & Bovin, N. (2008) · Glycobiology · doi:10.1093/glycob/cwn009 · Cited by 39 · see citing works
“Both determinants had been reported to target galectin-3 (van den Berg et al. 2004; Jin et al. 2006).”
BackgroundHirano, K., & Furukawa, K. (2022) · Biomolecules · doi:10.3390/biom12020195 · Cited by 38 · see citing works
The Mannose Receptor in Regulation of Helminth-Mediated Host Immunity
van Die, I., & Cummings, R. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01677 · Cited by 38 · see citing works
Self-citationMultivalent glycosystems for human lectins
Martínez‐Bailén, M., Rojo, J., & Ramos‐Soriano, J. (2022) · Chemical Society Reviews · doi:10.1039/d2cs00736c · Cited by 77 · see citing works
Romero, A., & Gabius, H. (2019) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2019.1675638 · Cited by 36 · see citing works
Galectins in Host-Pathogen Interactions: Structural, Functional and Evolutionary Aspects.
Vasta, G. (2020) · Advances in Experimental Medicine and Biology · doi:10.1007/978-981-15-1580-4_7 · Cited by 34 · see citing works
CD13 mediates phagocytosis in human monocytic cells
Licona-Limón, I., Garay-Canales, C., Muñoz-Paleta, O., & Ortega, E. (2015) · Journal of Leukocyte Biology · doi:10.1189/jlb.2a0914-458r · Cited by 33 · see citing works
“Importantly, galectin-3 binds to surface glycans of bacteria [73, 74], protista [75, 76], fungi [77, 78], and parasites [72].”
BackgroundHsu, T.-L., Lin, G., Koizumi, A., Brehm, K., Hada, N., Chuang, P.-K., Wong, C., Hsieh, S., & Díaz, Á. (2013) · Molecular and biochemical parasitology (Print) · doi:10.1016/j.molbiopara.2013.12.001 · Cited by 33 · see citing works
Macroparasites, innate immunity and immunoregulation: developing natural models
Friberg, I. M., Bradley, J. E., & Jackson, J. A. (2010) · Trends in Parasitology · doi:10.1016/j.pt.2010.06.010 · Cited by 30 · see citing works
Durães, F., Carvalho, N., Melo, T. T., Oliveira, S., & Fonseca, C. T. (2009) · Immunology Letters · doi:10.1016/j.imlet.2009.06.004 · Cited by 33 · see citing works
de Oliveira, F. L., Carneiro, K., Brito, J., Cabanel, M., Pereira, J. X., Paiva, L. D. A., Syn, W., Henderson, N., & El-Cheikh, M. C. (2017) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0005137 · Cited by 32 · see citing works
“As Gal-3 is highly expressed in inflammatory cells surrounding liver granulomas, it could be considered a pathogen-associated molecular pattern receptor, favoring an interactive network between macrophages and immunogenic carbohydrates [31].”
BackgroundPineda, M. A., Corvo, L., Soto, M., Fresno, M., & Bonay, P. (2014) · Glycobiology · doi:10.1093/glycob/cwu103 · Cited by 27 · see citing works
“In addition, gal-3 and -9 bind Leishmania major (Pelletier and Sato 2002; Pelletier et al. 2003; van den Berg et al. 2004).”
BackgroundGonzalez, M., Rubinstein, N., Ilarregui, J., Toscano, M., Sanjuan, N., & Rabinovich, G. (2005) · International Journal of Immunopathology and Pharmacology · doi:10.1177/039463200501800402 · Cited by 31
Alves, C., Silva, D., Azzolini, A. E. C. S., Marzocchi-Machado, C. M., Lucisano-Valim, Y., Roque-Barreira, M., & Mineo, J. R. (2012) · Parasitology · doi:10.1017/s0031182012001473 · Cited by 30
“For example, high levels of Gal-3 were found in the granulomas surrounding eggs and worms during Schistosoma mansoni infection (van den Berg et al. 2004), whereas the size of the granulomas was significantly decreased in Gal-3 deficient mice (Gal-3− /−) compared with their wild type counterparts…”
BackgroundDing, Z., Li, Z.-J., Zhang, X.-D., Li, Y.-G., Liu, C., Zhang, Y.-P., & Li, Y. (2011) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2011.11.005 · Cited by 30 · see citing works
“In addition, recent evidence indicates that galectins could facilitate pathogen internalization in phagocytic cells, such as macrophages (Van den Berg et al., 2004) .”
BackgroundCleavage and phosphorylation: important post-translational modifications of galectin-3
Gao, X.-G., Liu, J., Liu, X.-Y., Li, L.-T., & Zheng, J.-N. (2017) · Cancer Metastasis Review · doi:10.1007/s10555-017-9666-0 · Cited by 29 · see citing works
Chemo-enzymatic synthesis of LacdiNAc dimers of varying length as novel galectin ligands
Šimonová, A., Kupper, C. E., Böcker, S., Müller, A., Hofbauerová, K., Pelantová, H., Elling, L., Křen, V., & Bojarová, P. (2014) · Journal of Molecular Catalysis B Enzymatic · doi:10.1016/j.molcatb.2013.12.018 · Cited by 29 · see citing works
A Fish Galectin-8 Possesses Direct Bactericidal Activity
Zhang, T., Jiang, S., & Sun, L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010376 · Cited by 28
“For example, human Gal-3 bound Neisseria gon-orrhoeae through lipooligosaccharides [10], and hamster Gal-3 bound Schistosoma mansoni through LacdiNAc-Glycans [11].”
Hatanaka, O., Rezende, C. P., Moreno, P., Fernandes, F. F., Brito, P. M. O. O., Martinez, R., Coelho, C., Roque-Barreira, M., Casadevall, A., & Almeida, F. (2019) · Msphere · doi:10.1128/msphere.00209-19 · Cited by 28 · see citing works
Restuccia, A., Fettis, M. M., Farhadi, S., Molinaro, M., Kane, B. J., & Hudalla, G. (2018) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.8b00611 · Cited by 28
- Authors
- van den Berg, T. K., Honing, H., Franke, N., van Remoortere, A., Schiphorst, W. E. C. M., Liu, F.-T., Deelder, A. M., Cummings, R. D., Hokke, C. H., & van Die, I.
- Affiliations
- Department of Molecular Cell Biology and Immunology, Vrige University University Medical Center , Amsterdam ,
- Amsterdam University Medical Centers (NL)
- Department of Parasitology, Leiden University Medical Center, University of Leiden , Leiden ,
- Department of Dermatology, Davis School of Medicine, University of California , Sacramento, CA
- University of Oklahoma Health Sciences Center (US)
- Leiden University Medical Center (NL)
- Corresponding author
- Honing, Henk
- Franke, Niels
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2004-08-01
- Volume
- 173
- Issue
- 3
- Pages
- 1902-1907
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- OpenAlex
- W2169818746
- Cited by
- 170
- References
- 41
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 8 · 2023: 4 · 2022: 3 · 2021: 4 · 2020: 14 · 2019: 9 · 2018: 7 · 2017: 10 · 2016: 4 · 2015: 9 · 2014: 8 · 2013: 6 · 2012: 7
- FWCI
- 4.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (AI047214)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Galectins and Cancer Biology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
- Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
- Keywords
- galectin-3, galectin-1, helminths, Schistosoma mansoni, soluble egg antigen, macrophages, phagocytosis, N-glycans, liver granulomas, lectin binding
- MeSH terms
- Animals, Antigens, Helminth, Cell Line, Disaccharides, Glycoconjugates, Cricetinae, Humans, Lactose, Macrophages, Male, Mesocricetus, Phagocytosis, Polysaccharides, Protein Binding, Recombinant Fusion Proteins, Schistosoma mansoni, Schistosomiasis mansoni, Rats, Wistar, Surface Plasmon Resonance, Galectin 1, Galectin 3, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
