Volume 14 Issue 1
Jan.  2023
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James N. Arnold, Daniel A. Mitchell. Tinker, tailor, soldier, cell: the role of C-type lectins in the defense and promotion of disease[J]. Protein&Cell, 2023, 14(1): 4-16. doi: 10.1093/procel/pwac012
Citation: James N. Arnold, Daniel A. Mitchell. Tinker, tailor, soldier, cell: the role of C-type lectins in the defense and promotion of disease[J]. Protein&Cell, 2023, 14(1): 4-16. doi: 10.1093/procel/pwac012

Tinker, tailor, soldier, cell: the role of C-type lectins in the defense and promotion of disease

doi: 10.1093/procel/pwac012

D.A.M. is supported by the Howard Ostin Fund and the University Hospitals Coventry and Warwickshire Renal Medicine Department. J.N.A. is funded by a grant from Cancer Research UK (DCRPGF\100009) and is the recipient of a Cancer Research Institute/Wade F.B. Thompson CLIP grant (CRI3645).

  • Received Date: 2022-01-24
  • Rev Recd Date: 2022-04-25
  • Publish Date: 2023-01-01
  • C-type lectins (CTLs) represent a large family of soluble and membrane-bound proteins which bind calcium dependently via carbohydrate recognition domains (CRDs) to glycan residues presented on the surface of a variety of pathogens. The deconvolution of a cell’s glycan code by CTLs underpins several important physiological processes in mammals such as pathogen neutralization and opsonization, leukocyte trafficking, and the inflammatory response. However, as our knowledge of CTLs has developed it has become apparent that the role of this innate immune family of proteins can be double-edged, where some pathogens have developed approaches to subvert and exploit CTL interactions to promote infection and sustain the pathological state. Equally, CTL interactions with host glycoproteins can contribute to inflammatory diseases such as arthritis and cancer whereby, in certain contexts, they exacerbate inflammation and drive malignant progression. This review discusses the ‘dual agent’ roles of some of the major mammalian CTLs in both resolving and promoting infection, inflammation and inflammatory disease and highlights opportunities and emerging approaches for their therapeutic modulation.
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    Alon R, Feigelson SW. Chemokine-triggered leukocyte arrest:force-regulated bi-directional integrin activation in quantal adhesive contacts. Curr Opin Cell Biol 2012;24:670–676.
    Ambrus G, Gal P, Kojima M, et al. Natural substrates and inhibitors of mannan-binding lectin-associated serine protease-1 and -2: a study on recombinant catalytic fragments. J Immunol 2003;170:1374–1382.
    Amin R, Mourcin F, Uhel F, et al. DC-SIGN-expressing macrophages trigger activation of mannosylated IgM B-cell receptor in follicular lymphoma. Blood 2015;126:1911–1920.
    Amraei R, Yin W, Napoleon MA, et al. CD209L/L-SIGN and CD209/ DC-SIGN Act as Receptors for SARS-CoV-2. ACS Cent Sci 2021;7:1156–1165.
    Arnold JN, Dwek RA, Rudd PM, et al. Mannan binding lectin and its interaction with immunoglobulins in health and in disease. Immunol Lett 2006a;106:103–110.
    Arnold JN, Royle L, Dwek RA, et al. Human immunoglobulin glycosylation and the lectin pathway of complement activation. Adv Exp Med Biol 2005a;564:27–43.
    Arnold JN, Saldova R, Galligan MC, et al. Novel glycan biomarkers for the detection of lung cancer. J Proteome Res 2011;10:1755–1764.
    Arnold JN, Saldova R, Hamid UM, et al. Evaluation of the serum N-linked glycome for the diagnosis of cancer and chronic inflammation. Proteomics 2008;8:3284–3293.
    Arnold JN, Wallis R, Willis AC, et al. Interaction of mannan binding lectin with alpha2 macroglobulin via exposed oligomannose glycans: a conserved feature of the thiol ester protein family? J Biol Chem 2006b;281:6955–6963.
    Arnold JN, Wormald MR, Sim RB, et al. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu Rev Immunol 2007;25:21–50.
    Arnold JN, Wormald MR, Suter DM, et al. Human serum IgM glycosylation: identification of glycoforms that can bind to mannan-binding lectin. J Biol Chem 2005b;280:29080–29087.
    Arroyo R, Kingma PS. Surfactant protein D and bronchopulmonary dysplasia: a new way to approach an old problem. Respir Res 2021;22:141.
    Ashwell G, Harford J. Carbohydrate-specific receptors of the liver. Annu Rev Biochem 1982;51:531–554.
    Auriti C, Prencipe G, Moriondo M, et al. Mannose-binding lectin: biologic characteristics and role in the susceptibility to infections and ischemia-reperfusion related injury in critically ill neonates. J Immunol Res 2017;2017:7045630.
    Barbier V, Erbani J, Fiveash C, et al. Endothelial E-selectin inhibition improves acute myeloid leukaemia therapy by disrupting vascular niche-mediated chemoresistance. Nat Commun 2020;11:2042.
    Ben-David T, Sagi-Assif O, Meshel T, et al. The involvement of the sLe-a selectin ligand in the extravasation of human colorectal carcinoma cells. Immunol Lett 2008;116:218–224.
    Bergman MP, Engering A, Smits HH, et al. Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J Exp Med 2004;200:979–990.
    Bond A, Alavi A, Axford JS, et al. A detailed lectin analysis of IgG glycosylation, demonstrating disease specific changes in terminal galactose and N-acetylglucosamine. J Autoimmun 1997;10:77–85.
    Bradley DT, Bourke TW, Fairley DJ, et al. Genetic susceptibility to invasive meningococcal disease: MBL2 structural polymorphisms revisited in a large case-control study and a systematic review. Int J Immunogenet 2012;39:328–337.
    Breburda EE, Dambaeva SV, Slukvin II, et al. Selective distribution and pregnancy-specific expression of DC-SIGN at the maternal-fetal interface in the rhesus macaque: DC-SIGN is a putative marker of the recognition of pregnancy. Placenta 2006;27:11–21.
    Brouwer N, Dolman KM, van Houdt M, et al. Mannose-binding lectin(MBL) facilitates opsonophagocytosis of yeasts but not of bacteria despite MBL binding. J Immunol 2008;180:4124–4132.
    Brown GD, Willment JA, Whitehead L. C-type lectins in immunity and homeostasis. Nat Rev Immunol 2018;18:374–389.
    Brown KS, Keogh MJ, Owsianka AM, et al. Specific interaction of hepatitis C virus glycoproteins with mannan binding lectin inhibits virus entry. Protein Cell 2010;1:664–674.
    Cai G, Du M, Bosse Y, et al. SARS-CoV-2 impairs dendritic cells and regulates DC-SIGN gene expression in tissues. Int J Mol Sci 2021;22:9228–9248.
    Cameron PU, Freudenthal PS, Barker JM, et al. Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science 1992;257:383–387.
    Carroll MV, Sim RB, Bigi F, et al. Identification of four novel DC-SIGN ligands on Mycobacterium bovis BCG. Protein Cell 2010;1:859–870.
    Chan VS, Chan KY, Chen Y, et al. Homozygous L-SIGN (CLEC4M) plays a protective role in SARS coronavirus infection. Nat Genet 2006;38:38–46.
    Chen CB, and Wallis R. Two mechanisms for mannose-binding protein modulation of the activity of its associated serine proteases. J Biol Chem 2004;279:26058–26065.
    Chiba S, Ikushima H, Ueki H, et al. Recognition of tumor cells by Dectin-1 orchestrates innate immune cells for anti-tumor responses. Elife 2014;3:e04177.
    Clark HW. Untapped therapeutic potential of surfactant proteins: is there a case for recombinant SP-D supplementation in neonatal lung disease? Neonatology 2010;97:380–387.
    Coelho V, Krysov S, Ghaemmaghami AM, et al. Glycosylation of surface Ig creates a functional bridge between human follicular lymphoma and microenvironmental lectins. Proc Natl Acad Sci USA 2010;107:18587–18592.
    Conde P, Rodriguez M, van der Touw W, et al. DC-SIGN(+) macrophages control the induction of transplantation tolerance. Immunity 2015;42:1143–1158.
    Cummings RD, McEver RP. C-type Lectins. In Essentials of Glycobiology, nd, A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, and M.E. Etzler, eds. NY: Cold Spring Harbor, 2009.
    Curtis BM, Scharnowske S, Watson AJ. Sequence and expression of a membrane-associated C-type lectin that exhibits CD4-independent binding of human immunodeficiency virus envelope glycoprotein gp120. Proc Natl Acad Sci USA 1992;89:8356–8360.
    Damerell D, Ceroni A, Maass K, et al. The GlycanBuilder and GlycoWorkbench glycoinformatics tools: updates and new developments. Biol Chem 2012;393:1357–1362.
    Degn SE, Hansen AG, Steffensen R, et al. MAp44, a human protein associated with pattern recognition molecules of the complement system and regulating the lectin pathway of complement activation. J Immunol 2009;183:7371–7378.
    Degn SE, Jensen L, Olszowski T, et al. Co-complexes of MASP-1 and MASP-2 associated with the soluble pattern-recognition molecules drive lectin pathway activation in a manner inhibitable by MAp44. J Immunol 2013;191:1334–1345.
    Degn SE, Thiel S, Nielsen O, et al. MAp19, the alternative splice product of the MASP2 gene. J Immunol Methods 2011;373:89–101.
    DeNardo DG, Barreto JB, Andreu P, et al. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009;16:91–102.
    Dodds AW, Ren XD, Willis AC, et al. The reaction mechanism of the internal thioester in the human complement component C4.Nature 1996;379:177–179.
    Dong X, Storkus WJ, Salter RD. Binding and uptake of agalactosyl IgG by mannose receptor on macrophages and dendritic cells. J Immunol 1999;163:5427–5434.
    Downing I, Koch C, Kilpatrick DC. Immature dendritic cells possess a sugar-sensitive receptor for human mannan-binding lectin.Immunology 2003;109:360–364.
    Downing I, MacDonald SL, Turner ML, et al. Detection of an autologous ligand for mannan-binding lectin on human B lymphocytes. Scand J Immunol 2005;62:507–514.
    Drickamer K. C-type lectin-like domains. Curr Opin Struct Biol 1999;9:585–590.
    Eisen DP, Dean MM, Boermeester MA, et al. Low serum mannose-binding lectin level increases the risk of death due to pneumococcal infection. Clin Infect Dis 2008;47:510–516.
    Esposito M, Mondal N, Greco TM, et al. Bone vascular niche E-selectin induces mesenchymal-epithelial transition and Wnt activation in cancer cells to promote bone metastasis. Nat Cell Biol 2019;21:627–639.
    Faber J, Schuessler T, Finn A, et al. Age-dependent association of human mannose-binding lectin mutations with susceptibility to invasive meningococcal disease in childhood. Pediatr Infect Dis J 2007;26:243–246.
    Feinberg H, Castelli R, Drickamer K, et al. Multiple modes of binding enhance the affinity of DC-SIGN for high mannose N-linked glycans found on viral glycoproteins. J Biol Chem 2007;282:4202–4209.
    Feinberg H, Guo Y, Mitchell DA, et al. Extended neck regions stabilize tetramers of the receptors DC-SIGN and DC-SIGNR. J Biol Chem 2005;280:1327–1335.
    Feinberg H, Mitchell DA, Drickamer K, et al. Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR.Science 2001;294:2163–2166.
    Fraser DA, Bohlson SS, Jasinskiene N, et al. C1q and MBL, components of the innate immune system, influence monocyte cytokine expression. J Leukoc Biol 2006;80:107–116.
    del Fresno C, Soulat D, Roth S, et al. Interferon-beta production via Dectin-1-Syk-IRF5 signaling in dendritic cells is crucial for immunity to C. albicans. Immunity 2013;38:1176–1186.
    Gaiha GD, Dong T, Palaniyar N, et al. Surfactant protein A binds to HIV and inhibits direct infection of CD4+ cells, but enhances dendritic cell-mediated viral transfer. J Immunol 2008;181:601–609.
    Gao DN, Zhang Y, Ren YB, et al. Relationship of serum mannose-binding lectin levels with the development of sepsis: a meta-analysis. Inflammation 2015;38:338–347.
    Garcia-Manero G, Sekeres MA, Egyed M, et al. A phase 1b/2b multicenter study of oral panobinostat plus azacitidine in adults with MDS, CMML or AML with 30% blasts. Leukemia 2017;31:2799–2806.
    Garred P, Madsen HO, Marquart H, et al. Two edged role of mannose binding lectin in rheumatoid arthritis: a cross sectional study. J Rheumatol 2000;27:26–34.
    Geijtenbeek TB, Krooshoop DJ, Bleijs DA, et al. DC-SIGN-ICAM-2 interaction mediates dendritic cell trafficking. Nat Immunol 2000a;1:353–357.
    Geijtenbeek TB, Kwon DS, Torensma R, et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 2000b;100:587–597.
    Geijtenbeek TB, Torensma R, van Vliet SJ, et al. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 2000c;100:575–585.
    Geijtenbeek TB, Van Vliet SJ, Koppel EA, et al. Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 2003;197:7–17.
    van Gisbergen KP, Sanchez-Hernandez M, Geijtenbeek TB, et al.Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J Exp Med 2005;201:1281–1292.
    Green PJ, Feizi T, Stoll MS, et al. Recognition of the major cell surface glycoconjugates of Leishmania parasites by the human serum mannan-binding protein. Mol Biochem Parasitol 1994;66:319–328.
    Gringhuis SI, den Dunnen J, Litjens M, et al. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity 2007;26:605–616.
    Gringhuis SI, den Dunnen J, Litjens M, et al. Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori.Nat Immunol 2009;10:1081–1088.
    Guile GR, Rudd PM, Wing DR, et al. A rapid high-resolution high-performance liquid chromatographic method for separating glycan mixtures and analyzing oligosaccharide profiles. Anal Biochem 1996;240:210–226.
    Guo Y, Feinberg H, Conroy E, et al. Structural basis for distinct ligand-binding and targeting properties of the receptors DC-SIGN and DC-SIGNR. Nat Struct Mol Biol 2004;11:591–598.
    Heidemann F, Schildt A, Schmid K, et al. Selectins mediate small cell lung cancer systemic metastasis. PLoS One 2014;9:e92327.
    Heja D, Kocsis A, Dobo J, et al. Revised mechanism of complement lectin-pathway activation revealing the role of serine protease MASP-1 as the exclusive activator of MASP-2. Proc Natl Acad Sci U S A 2012;109:10498–10503.
    Hillaire ML, Nieuwkoop NJ, Boon AC, et al. Binding of DC-SIGN to the hemagglutinin of influenza A viruses supports virus replication in DC-SIGN expressing cells. PLoS One 2013:8;e56164.
    Hopkin SJ, Lewis JW, Krautter F, et al. Triggering the resolution of immune mediated inflammatory diseases: can targeting leukocyte migration be the answer? Front Pharmacol 2019;10:184.
    Iobst ST, Drickamer K. Binding of sugar ligands to Ca(2+)-dependent animal lectins. II. Generation of high-affinity galactose binding by site-directed mutagenesis. J Biol Chem 1994;269:15512–15519.
    Iwaki D, Kanno K, Takahashi M, et al. Small mannose-binding lectin-associated protein plays a regulatory role in the lectin complement pathway. J Immunol 2006;177:8626–8632.
    Ji X, Olinger GG, Aris S, et al. Mannose-binding lectin binds to Ebola and Marburg envelope glycoproteins, resulting in blocking of virus interaction with DC-SIGN and complement-mediated virus neutralization. J Gen Virol 2005;86:2535–2542.
    Justice JM, Sleasman JW, Lanza DC. Recalcitrant rhinosinusitis, innate immunity, and mannose-binding lectin. Ann Otol Rhinol Laryngol 2015;124:102–106.
    Kase T, Suzuki Y, Kawai T, et al. Human mannan-binding lectin inhibits the infection of influenza A virus without complement.Immunology 1999;97:385–392.
    Kjaer TR, Thiel S, Andersen GR. Toward a structure-based comprehension of the lectin pathway of complement. Mol Immunol 2013;56:222–231.
    van Kooyk Y, Appelmelk B, Geijtenbeek TB. A fatal attraction:Mycobacterium tuberculosis and HIV-1 target DC-SIGN to escape immune surveillance. Trends Mol Med 2003;9:153–159.
    Kosti P, Maher J, Arnold JN. Perspectives on chimeric antigen receptor T-cell immunotherapy for solid tumors. Front Immunol 2018;9:1104.
    Krarup A, Gulla KC, Gal P, et al. The action of MBL-associated serine protease 1 (MASP1) on factor XIII and fibrinogen. Biochim Biophys Acta 2008;1784:1294–1300.
    Krarup A, Wallis R, Presanis JS, et al. Simultaneous activation of complement and coagulation by MBL-associated serine protease 2.PLoS One 2007;2:e623.
    Kunkel EJ, Ley K. Distinct phenotype of E-selectin-deficient mice. E-selectin is required for slow leukocyte rolling in vivo. Circ Res 1996;79:1196–1204.
    Kwon DS, Gregorio G, Bitton N, et al. DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity 2002;16:135–144.
    Lamb YN. Inclisiran: first approval. Drugs 2021;81:389–395.
    Larsen F, Madsen HO, Sim RB, et al. Disease-associated mutations in human mannose-binding lectin compromise oligomerization and activity of the final protein.J Biol Chem 2004;279:21302–21311.
    Laubli H, Borsig L. Selectins promote tumor metastasis. Semin Cancer Biol 2010;20:169–177.
    Laubli H, Spanaus KS, Borsig L. Selectin-mediated activation of endothelial cells induces expression of CCL5 and promotes metastasis through recruitment of monocytes. Blood 2009;114:4583–4591.
    Le Carré, J. Tinker, tailor, soldier, spy, 1st edn. (New York, Knopf; distributed by Random House) 1974.
    Lefort CT, Ley K. Neutrophil arrest by LFA-1 activation. Front Immunol 2012;3:157.
    Li C, Xue VW, Wang QM, et al. The Mincle/Syk/NF-kappaB signaling circuit is essential for maintaining the protumoral activities of tumor-associated macrophages. Cancer Immunol Res 2020;8:1004–1017.
    Lillegard JB, Sim RB, Thorkildson P, et al. Recognition of Candida albicans by mannan-binding lectin in vitro and in vivo. J Infect Dis 2006;193:1589–1597.
    Linley A, Krysov S, Ponzoni M, et al. Lectin binding to surface Ig variable regions provides a universal persistent activating signal for follicular lymphoma cells. Blood 2015;126:1902–1910.
    Liu P, Ridilla M, Patel P, et al. Beyond attachment: Roles of DC-SIGN in dengue virus infection. Traffic 2017;18:218–231.
    Madsen J, Gaiha GD, Palaniyar N, et al. Surfactant Protein D modulates HIV infection of both T-cells and dendritic cells. PLoS One 2013;8:e59047.
    Madsen HO, Satz ML, Hogh B, et al. Different molecular events result in low protein levels of mannan-binding lectin in populations from southeast Africa and South America. J Immunol 1998;161:3169–3175.
    Malhotra R, Thiel S, Reid KB, et al. Human leukocyte C1q receptor binds other soluble proteins with collagen domains. J Exp Med 1990;172:955–959.
    Malhotra R, Wormald MR, Rudd PM, et al. Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat Med 1995;1:237–243.
    Mantovani A, Marchesi F, Malesci A, et al. Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol 2017;14:399–416.
    Mayilyan KR, Presanis JS, Arnold JN, et al. Heterogeneity of MBLMASP complexes. Mol Immunol 2006;43:1286–1292.
    McEver RP. Selectins: initiators of leucocyte adhesion and signalling at the vascular wall. Cardiovasc Res 2015;107:331–339.
    Merle NS, Church SE, Fremeaux-Bacchi V, et al. Complement system part I - molecular mechanisms of activation and regulation.Front Immunol 2015;6:262.
    Mimura Y, Katoh T, Saldova R, et al. Glycosylation engineering of therapeutic IgG antibodies: challenges for the safety, functionality and efficacy. Protein Cell 2018;9:47–62.
    Mitchell DA, Fadden AJ, Drickamer K. A novel mechanism of carbohydrate recognition by the C-type lectins DC-SIGN and DC-SIGNR.Subunit organization and binding to multivalent ligands. J Biol Chem 2001;276:28939–28945.
    Moller-Kristensen M, Thiel S, Sjoholm A, et al. Cooperation between MASP-1 and MASP-2 in the generation of C3 convertase through the MBL pathway. Int Immunol 2007;19:141–149.
    Mondal N, Silva M, Castano AP, et al. Glycoengineering of chimeric antigen receptor (CAR) T-cells to enforce E-selectin binding. J Biol Chem 2019;294:18465–18474.
    Mrksich M. An early taste of functional glycomics. Chem Biol 2004;11:739–740.
    Muliaditan T, Caron J, Okesola M, et al. Macrophages are exploited from an innate wound healing response to facilitate cancer metastasis. Nat Commun 2018;9:2951.
    Murray PJ, Allen JE, Biswas SK, et al. Macrophage activation and polarization: nomenclature and experimental guidelines.Immunity 2014;41:14–20.
    Murugaiah V, Varghese PM, Beirag N, et al. Complement proteins as soluble pattern recognition receptors for pathogenic viruses.Viruses 2021;13.
    Nair JK, Willoughby JL, Chan A, et al. Multivalent N-acetylgalactosamine-conjugated siRNA localizes in hepatocytes and elicits robust RNAi-mediated gene silencing. J Am Chem Soc 2014;136:16958–16961.
    Natoni A, Macauley MS, O’Dwyer ME. Targeting selectins and their ligands in cancer. Front Oncol 2016;6:93.
    Navarro-Sanchez E, Altmeyer R, Amara A, et al. Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep 2003;4:723–728.
    Neth O, Jack DL, Dodds AW, et al. Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition. Infect Immun 2000;68:688–693.
    Nimmerjahn F, Anthony RM, Ravetch JV. Agalactosylated IgG antibodies depend on cellular Fc receptors for in vivo activity. Proc Natl Acad Sci USA 2007;104:8433–8437.
    Nonaka M, Ma BY, Imaeda H, et al. Dendritic cell-specific intercellular adhesion molecule 3-grabbing non-integrin(DC-SIGN) recognizes a novel ligand, Mac-2-binding protein, characteristically expressed on human colorectal carcinomas.J Biol Chem 2011;286:22403–22413.
    Nonaka M, Ma BY, Murai R, et al. Glycosylation-dependent interactions of C-type lectin DC-SIGN with colorectal tumor-associated Lewis glycans impair the function and differentiation of monocyte-derived dendritic cells. J Immunol 2008;180:3347–3356.
    Ogden CA, deCathelineau A, Hoffmann PR, et al. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 2001;194:781–795.
    Opzoomer JW, Anstee JE, Dean I, et al. Macrophages orchestrate the expansion of a proangiogenic perivascular niche during cancer progression. Sci Adv 2021;7:eabg9518.
    Parekh RB, Dwek RA, Sutton BJ, et al. Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature 1985;316:452–457.
    Parekh R, Isenberg D, Rook G, et al. A comparative analysis of disease-associated changes in the galactosylation of serum IgG. J Autoimmun 1989;2:101–114.
    Pinho SS, and Reis CA. Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer 2015;15:540–555.
    Pohlmann S, Soilleux EJ, Baribaud F, et al. DC-SIGNR, a DC-SIGN homologue expressed in endothelial cells, binds to human and simian immunodeficiency viruses and activates infection in trans. Proc Natl Acad Sci U S A 2001;98:2670–2675.
    Presanis JS, Hajela K, Ambrus G, et al. Differential substrate and inhibitor profiles for human MASP-1 and MASP-2. Mol Immunol 2004;40:921–929.
    Presanis JS, Kojima M, Sim RB. Biochemistry and genetics of mannan-binding lectin (MBL). Biochem Soc Trans 2003;31:748–752.
    Radcliffe CM, Arnold JN, Suter DM, et al. Human follicular lymphoma cells contain oligomannose glycans in the antigen-binding site of the B-cell receptor. J Biol Chem 2007;282:7405–7415.
    Reid KBM. Complement component C1q: historical perspective of a functionally versatile, and structurally unusual, serum protein.Front Immunol 2018;9:764.
    Rook GA, Steele J, Brealey R, et al. Changes in IgG glycoform levels are associated with remission of arthritis during pregnancy. J Autoimmun 1991;4:779–794.
    Roos A, Bouwman LH, van Gijlswijk-Janssen DJ, et al. Human IgA activates the complement system via the mannan-binding lectin pathway. J Immunol 2001;167, 2861–2868.
    Royle L, Roos A, Harvey DJ, et al. Secretory IgA N- and O-glycans provide a link between the innate and adaptive immune systems. J Biol Chem 2003;278:20140–20153.
    Saeland E, van Vliet SJ, Backstrom M, et al. The C-type lectin MGL expressed by dendritic cells detects glycan changes on MUC1 in colon carcinoma. Cancer Immunol Immunother 2007;56:1225–1236.
    Saldova R, Royle L, Radcliffe CM, et al. Ovarian cancer is associated with changes in glycosylation in both acute-phase proteins and IgG. Glycobiology 2007;17:1344–1356.
    Santos IK, Costa CH, Krieger H, et al. Mannan-binding lectin enhances susceptibility to visceral leishmaniasis. Infect Immun 2001;69:5212–5215.
    Santulli G, Jankauskas SS, Gambardella J. Inclisiran: a new milestone on the PCSK9 road to tackle cardiovascular risk. Eur Heart J Cardiovasc Pharmacother 2021;7:e11–e12.
    Schwaeble WJ, Lynch NJ, Clark JE, et al. Targeting of mannan-binding lectin-associated serine protease-2 confers protection from myocardial and gastrointestinal ischemia/reperfusion injury.Proc Natl Acad Sci USA 2011;108:7523–7528.
    Schweitzer KM, Drager AM, van der Valk P, et al. Constitutive expression of E-selectin and vascular cell adhesion molecule-1 on endothelial cells of hematopoietic tissues. Am J Pathol 1996;148:165–175.
    Seifert L, Werba G, Tiwari S, et al. The necrosome promotes pancreatic oncogenesis via CXCL1 and Mincle-induced immune suppression. Nature 2016;532:245–249.
    Sim RB, Schwaeble W, Fujita T. Complement research in the 18th-21st centuries: Progress comes with new technology. Immunobiology 2016;221:1037–1045.
    Simmons G, Reeves JD, Grogan CC, et al. DC-SIGN and DC-SIGNR bind ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 2003;305:115–123.
    Soilleux EJ, Barten R, Trowsdale J. DC-SIGN; a related gene, DC-SIGNR; and CD23 form a cluster on 19p13. J Immunol 2000;165:2937–2942.
    Soilleux EJ, Morris LS, Lee B, et al. Placental expression of DC-SIGN may mediate intrauterine vertical transmission of HIV. J Pathol 2001;195:586–592.
    Soilleux EJ, Morris LS, Leslie G, et al. Constitutive and induced expression of DC-SIGN on dendritic cell and macrophage subpopulations in situ and in vitro. J Leukoc Biol 2002;71:445–457.
    Stover CM, Thiel S, Thelen M, et al. Two constituents of the initiation complex of the mannan-binding lectin activation pathway of complement are encoded by a single structural gene. J Immunol 1999;162:3481–3490.
    Strong P, Townsend P, Mackay R, et al. A recombinant fragment of human SP-D reduces allergic responses in mice sensitized to house dust mite allergens. Clin Exp Immunol 2003;134:181–187.
    Stuart LM, Takahashi K, Shi L, et al. Mannose-binding lectin-deficient mice display defective apoptotic cell clearance but no autoimmune phenotype. J Immunol 2005;174:3220–3226.
    Summerfield JA, Sumiya M, Levin M, et al. Association of mutations in mannose binding protein gene with childhood infection in consecutive hospital series. BMJ 1997;314:1229–1232.
    Terada M, Khoo KH, Inoue R, et al. Characterization of oligosaccharide ligands expressed on SW1116 cells recognized by mannan-binding protein. A highly fucosylated polylactosamine type N-glycan. J Biol Chem 2005;280:10897–10913.
    Thiel S, Vorup-Jensen T, Stover CM, et al. A second serine protease associated with mannan-binding lectin that activates complement. Nature 1997;386:506–510.
    Tomaiuolo R, Ruocco A, Salapete C, et al. Activity of mannose-binding lectin in centenarians. Aging Cell 2012;11:394–400.
    Tsakanova G, Stepanyan A, Nahapetyan K, et al. Serine proteases of the complement lectin pathway and their genetic variations in ischaemic stroke. J Clin Pathol 2018;71:141–147.
    Tsutsumi A, Takahashi R, Sumida T. Mannose binding lectin: genetics and autoimmune disease. Autoimmun Rev 2005;4:364–372.
    Valle-Argos B, Chiodin G, Bryant DJ, et al. DC-SIGN binding to mannosylated B-cell receptors in follicular lymphoma down-modulates receptor signaling capacity. Sci Rep 2021;11:11676.
    van Vliet SJ, Gringhuis SI, Geijtenbeek TB, et al. Regulation of effector T cells by antigen-presenting cells via interaction of the C-type lectin MGL with CD45. Nat Immunol 2006;7:1200–1208.
    Wawrzinek R, Wamhoff EC, Lefebre J, et al. A remote secondary binding pocket promotes heteromultivalent targeting of DC-SIGN. J Am Chem Soc 2021;143:18977–18988.
    Weis WI, Drickamer K, and Hendrickson WA. Structure of a C-type mannose-binding protein complexed with an oligosaccharide.Nature 1992;360:127–134.
    Wong D, Dorovini-Zis K. Regualtion by cytokines and lipopolysaccharide of E-selectin expression by human brain microvessel endothelial cells in primary culture. J Neuropathol Exp Neurol 1996;55:225–235.
    Yang SW, Cho EH, Choi SY, et al. DC-SIGN expression in Hofbauer cells may play an important role in immune tolerance in fetal chorionic villi during the development of preeclampsia. J Reprod Immunol 2017;124:30–37.
    Yang ZS, Huang SW, Wang WH, et al. Identification of Important N-Linked Glycosylation Sites in the Hemagglutinin Protein and Their Functional Impact on DC-SIGN Mediated Avian Influenza H5N1 Infection. Int J Mol Sci 2021;22:743–765.
    Yaseen S, Demopulos G, Dudler T, et al. Lectin pathway effector enzyme mannan-binding lectin-associated serine protease-2 can activate native complement C3 in absence of C4 and/or C2. FASEB J 2017;31:2210–2219.
    Zahavi D, Weiner L. Monoclonal antibodies in cancer therapy. Antibodies (Basel) 2020;9:34–54.
    Zhao N, Wu J, Xiong S, et al. Mannan-binding lectin, a serum collectin, suppresses T-cell proliferation via direct interaction with cell surface calreticulin and inhibition of proximal T-cell receptor signaling. FASEB J 2017;31:2405–2417.
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