DC-SIGN mediated internalisation of glycosylated extracellular vesicles from Schistosoma mansoni increases activation of monocyte-derived dendritic cells

References

• Colley DG, Bustinduy AL, Secor WE, et al. Human schistosomiasis. Lancet. 2014;383(9936):2253–19. .
   PubMed Web of Science ®Google Scholar
• Maizels RM, Smits HH, McSorley HJ, et al. Modulation of host immunity by helminths: the expanding repertoire of parasite effector molecules. Immunity. 2018;49(5):801–818.
   PubMed Web of Science ®Google Scholar
• Mountford AP, Trottein F. Schistosomes in the skin: a balance between immune priming and regulation. Trends Parasitol. 2004;20(5):221–226.
   Web of Science ®Google Scholar
• Maizels RM, McSorley HJ. Regulation of the host immune system by helminth parasites. J Allergy Clin Immunol. 2016;138(3):666–675.
   PubMed Web of Science ®Google Scholar
• Wu Z, Wang L, Li J, et al. Extracellular Vesicle-mediated communication within host-parasite interactions. Front Immunol. 2018;9:3066.
   PubMed Web of Science ®Google Scholar
• Nowacki FC, Swain MT, Klychnikov OI, et al. Protein and small non-coding RNA-enriched extracellular vesicles are released by the pathogenic blood fluke Schistosoma mansoni. J Extracell Vesicles. 2015;4:28665.
   PubMed Web of Science ®Google Scholar
• Sotillo J, Pearson M, Potriquet J, et al. Extracellular vesicles secreted by Schistosoma mansoni contain protein vaccine candidates. Int J Parasitol. 2016;46(1):1–5.
   PubMed Web of Science ®Google Scholar
• Samoil V, Dagenais M, Ganapathy V, et al. Vesicle-based secretion in schistosomes: analysis of protein and microRNA (miRNA) content of exosome-like vesicles derived from Schistosoma mansoni. Sci Rep. 2018;8(1):3286.
   Google Scholar
• Maizels RM, Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol. 2003;3(9):733–744.
   PubMed Web of Science ®Google Scholar
• Hogg KG, Kumkate S, Anderson S, et al. Interleukin-12 p40 secretion by cutaneous CD11c+ and F4/80+ cells is a major feature of the innate immune response in mice that develop Th1-mediated protective immunity to Schistosoma mansoni. Infect Immun. 2003;71(6):3563–3571.
   Web of Science ®Google Scholar
• Paveley RA, Aynsley SA, Cook PC, et al. Fluorescent imaging of antigen released by a skin-invading helminth reveals differential uptake and activation profiles by antigen presenting cells. PLoS Negl Trop Dis. 2009;3(10):e528.
   Web of Science ®Google Scholar
• Winkel BMF, Dalenberg MR, de Korne CM, et al. Early induction of human regulatory dermal antigen presenting cells by skin-penetrating schistosoma mansoni cercariae. Front Immunol. 2018;9:2510.
   Web of Science ®Google Scholar
• van Niel G, D’Angelo G, Raposo G, et al. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19(4):213–228.
   PubMed Web of Science ®Google Scholar
• Egesa M, Lubyayi L, Tukahebwa EM, et al. Schistosoma mansoni schistosomula antigens induce Th1/Pro-inflammatory cytokine responses. Parasite Immunol. 2018;40(12):e12592.
   Web of Science ®Google Scholar
• Jenkins SJ, Hewitson JP, Ferret-Bernard S, et al. Schistosome larvae stimulate macrophage cytokine production through TLR4-dependent and -independent pathways. Int Immunol. 2005;17(11):1409–1418.
   Web of Science ®Google Scholar
• Paveley RA, Aynsley SA, Turner JD, et al. The Mannose Receptor (CD206) is an important pattern recognition receptor (PRR) in the detection of the infective stage of the helminth Schistosoma mansoni and modulates IFNgamma production. Int J Parasitol. 2011;41(13–14):1335–1345.
   Web of Science ®Google Scholar
• van Die I, Cummings RD. The mannose receptor in regulation of helminth-mediated host immunity. Front Immunol. 2017;8:1677.
   Web of Science ®Google Scholar
• Kaisar MMM, Ritter M, Del Fresno C, et al. Dectin-1/2-induced autocrine PGE2 signaling licenses dendritic cells to prime Th2 responses. PLoS Biol. 2018;16(4):e2005504.
   Web of Science ®Google Scholar
• Bloem K, Vuist IM, van den Berk M, et al. DCIR interacts with ligands from both endogenous and pathogenic origin. Immunol Lett. 2014;158(1–2):33–41.
   Web of Science ®Google Scholar
• van Liempt E, van Vliet SJ, Engering A, et al. Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation. Mol Immunol. 2007;44(10):2605–2615.
   Web of Science ®Google Scholar
• van Die I, van Vliet SJ, Nyame AK, et al. The dendritic cell-specific C-type lectin DC-SIGN is a receptor for Schistosoma mansoni egg antigens and recognizes the glycan antigen Lewis x. Glycobiology. 2003;13(6):471–478.
   PubMed Web of Science ®Google Scholar
• Everts B, Hussaarts L, Driessen NN, et al. Schistosome-derived omega-1 drives Th2 polarization by suppressing protein synthesis following internalization by the mannose receptor. J Exp Med. 2012;209(10):1753–67, S1.
   PubMed Web of Science ®Google Scholar
• Geijtenbeek TB, Gringhuis SI. C-type lectin receptors in the control of T helper cell differentiation. Nat Rev Immunol. 2016;16(7):433–448.
   PubMed Web of Science ®Google Scholar
• Jang-Lee J, Curwen RS, Ashton PD, et al. Glycomics analysis of schistosoma mansoni egg and cercarial secretions. Mol Cell Proteomics. 2007;6(9):1485–1499.
   Web of Science ®Google Scholar
• Gerlach JQ, Griffin MD. Getting to know the extracellular vesicle glycome. Mol Biosyst. 2016;12(4):1071–1081.
   PubMedGoogle Scholar
• Williams C, Royo F, Aizpurua-Olaizola O, et al. Glycosylation of extracellular vesicles: current knowledge, tools and clinical perspectives. J Extracell Vesicles. 2018;7(1):1442985.
   PubMed Web of Science ®Google Scholar
• Freitas D, Balmaña M, Poças J, et al. Different isolation approaches lead to diverse glycosylated extracellular vesicle populations. J Extracell Vesicles. 2019;8:1.
   Web of Science ®Google Scholar
• Williams C, Pazos R, Royo F, et al. Assessing the role of surface glycans of extracellular vesicles on cellular uptake. Sci Rep. 2019;9:1.
   Web of Science ®Google Scholar
• Shimoda A, Sawada S-I, Sasaki Y, et al. Exosome surface glycans reflect osteogenic differentiation of mesenchymal stem cells: profiling by an evanescent field fluorescence-assisted lectin array system. Sci Rep. 2019;9:1.
   Web of Science ®Google Scholar
• Colley DG, Wikel SK. Schistosoma mansoni: simplified method for the production of schistosomules. Exp Parasitol. 1974;35(1):44–51.
   Web of Science ®Google Scholar
• Consortium E-T, Van Deun J, Mestdagh P, et al. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Nat Methods. 2017;14(3):228–232.
   PubMed Web of Science ®Google Scholar
• Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–682.
   PubMed Web of Science ®Google Scholar
• Hussaarts L, Smits HH, Schramm G, et al. Rapamycin and omega-1: mTOR-dependent and -independent Th2 skewing by human dendritic cells. Immunol Cell Biol. 2013;91(7):486–489.
   Web of Science ®Google Scholar
• Wilbers RHP, Westerhof LB, van Noort K, et al. Production and glyco-engineering of immunomodulatory helminth glycoproteins in plants. Sci Rep. 2017;7:1.
   Web of Science ®Google Scholar
• Smit CH, van Diepen A, Nguyen DL, et al. Glycomic analysis of life stages of the human parasite schistosoma mansoni reveals developmental expression profiles of functional and antigenic glycan motifs. Mol Cell Proteomics. 2015;14(7):1750–1769.
   Web of Science ®Google Scholar
• Ceroni A, Maass K, Geyer H, et al. Glycoworkbench: a tool for the computer-assisted annotation of mass spectra of glycans †. J Proteome Res. 2008;7(4):1650–1659.
   PubMed Web of Science ®Google Scholar
• Bustin SA, Benes V, Garson JA, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009;55(4):611–622.
   PubMed Web of Science ®Google Scholar
• Simonsen JB. Pitfalls associated with lipophilic fluorophore staining of extracellular vesicles for uptake studies. J Extracell Vesicles. 2019;8(1):1582237.
   PubMed Web of Science ®Google Scholar
• Hokke CH, van Diepen A. Helminth glycomics - glycan repertoires and host-parasite interactions. Mol Biochem Parasitol. 2017;215:47–57.
   Web of Science ®Google Scholar
• van Kooyk Y, Geijtenbeek TBH. DC-SIGN: escape mechanism for pathogens. Nat Rev Immunol. 2003;3(9):697–709.
   PubMed Web of Science ®Google Scholar
• Everts B, Perona-Wright G, Smits HH, et al. Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J Exp Med. 2009;206(8):1673–1680.
   Web of Science ®Google Scholar
• Meevissen MHJ, Driessen NN, Smits HH, et al. Specific glycan elements determine differential binding of individual egg glycoproteins of the human parasite Schistosoma mansoni by host C-type lectin receptors. Int J Parasitol. 2012;42(3):269–277.
   Web of Science ®Google Scholar
• Meyer S, van Liempt E, Imberty A, et al. DC-SIGN mediates binding of dendritic cells to authentic Pseudo-Lewis Y glycolipids of Schistosoma mansoni Cercariae, the first parasite-specific ligand of DC-SIGN. J Biol Chem. 2005;280(45):37349–37359.
   PubMed Web of Science ®Google Scholar
• Dorsey CH, Cousin CE, Lewis FA, et al. Ultrastructure of the Schistosoma mansoni cercaria. Micron. 2002;33(3):279–323.
   Web of Science ®Google Scholar
• Turner L, Bitto NJ, Steer DL, et al. Helicobacter pylori outer membrane vesicle size determines their mechanisms of host cell entry and protein content. Front Immunol. 2018;9:1466.
   Web of Science ®Google Scholar
• Liu J, Zhu L, Wang J, et al. Schistosoma japonicum extracellular vesicle miRNA cargo regulates host macrophage functions facilitating parasitism. PLoS Pathog. 2019;15(6):e1007817.
   PubMed Web of Science ®Google Scholar
• Dunne DW, Opinion CA. - A worm’s eye view of the immune system: consequences for evolution of human autoimmune disease. Nat Rev Immunol. 2005;5(5):420–426.
   Web of Science ®Google Scholar
• Kifle DW, Pearson MS, Becker L, et al. Proteomic analysis of two populations of Schistosoma mansoni-derived extracellular vesicles: 15k pellet and 120k pellet vesicles. Mol Biochem Parasitol. 2020;236:111264.
   PubMed Web of Science ®Google Scholar
• Hunter RC, Beveridge TJ. High-resolution visualization of Pseudomonas aeruginosa PAO1 biofilms by freeze-substitution transmission electron microscopy. J Bacteriol. 2005;187(22):7619–7630.
   Web of Science ®Google Scholar
• Liu Y, Hidaka E, Kaneko Y, et al. Ultrastructure of Helicobacter pylori in human gastric mucosa and H. pylori-infected human gastric mucosa using transmission electron microscopy and the high-pressure freezing-freeze substitution technique. J Gastroenterol. 2006;41(6):569–574.
   PubMed Web of Science ®Google Scholar
• Gui MJ, Dashper SG, Slakeski N, et al. Spheres of influence: porphyromonas gingivalis outer membrane vesicles. Mol Oral Microbiol. 2016;31(5):365–378.
   PubMed Web of Science ®Google Scholar
• Wang L, Li Z, Shen J, et al. Exosome-like vesicles derived by Schistosoma japonicum adult worms mediates M1 type immune- activity of macrophage. Parasitol Res. 2015;114(5):1865–1873.
   Web of Science ®Google Scholar
• Zhu L, Liu J, Dao J, et al. Molecular characterization of S. japonicum exosome-like vesicles reveals their regulatory roles in parasite-host interactions. Sci Rep. 2016;6:25885.
   PubMed Web of Science ®Google Scholar
• Zhu S, Wang S, Lin Y, et al. Release of extracellular vesicles containing small RNAs from the eggs of Schistosoma japonicum. Parasit Vectors. 2016;9(1):574.
   Google Scholar
• van Stijn CM, Meyer S, van den Broek M, et al. Schistosoma mansoni worm glycolipids induce an inflammatory phenotype in human dendritic cells by cooperation of TLR4 and DC-SIGN. Mol Immunol. 2010;47(7–8):1544–1552.
   PubMed Web of Science ®Google Scholar
• Garcia-Vallejo JJ, van Kooyk Y. The physiological role of DC-SIGN: a tale of mice and men. Trends Immunol. 2013;34(10):482–486.
   Web of Science ®Google Scholar
• Gazi U, Martinez-Pomares L. Influence of the mannose receptor in host immune responses. Immunobiology. 2009;214(7):554–561.
   PubMed Web of Science ®Google Scholar
• Horrevorts SK, Stolk DA, Ven RV, et al. Glycan-modified melanoma-derived apoptotic extracellular vesicles as antigen source for anti-tumor vaccination. Cancers (Basel). 2019;11:9.
   Web of Science ®Google Scholar
• Dusoswa SA, Horrevorts SK, Ambrosini M, et al. Glycan modification of glioblastoma-derived extracellular vesicles enhances receptor-mediated targeting of dendritic cells. J Extracell Vesicles. 2019;8(1):1648995.
   PubMed Web of Science ®Google Scholar
• Eriksson M, Serna S, Maglinao M, et al. Biological evaluation of multivalent lewis X-MGL-1 interactions. Chembiochem. 2014;15(6):844–851.
   Web of Science ®Google Scholar
• Marcelo F, Supekar N, Corzana F, et al. Identification of a secondary binding site in human macrophage galactose-type lectin by microarray studies: implications for the molecular recognition of its ligands. J Biol Chem. 2019;294(4):1300–1311.
   Web of Science ®Google Scholar
• Kaparakis M, Turnbull L, Carneiro L, et al. Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell Microbiol. 2010;12(3):372–385.
   PubMed Web of Science ®Google Scholar
• Stevenson TC, Cywes-Bentley C, Moeller TD, et al. Immunization with outer membrane vesicles displaying conserved surface polysaccharide antigen elicits broadly antimicrobial antibodies. Proc Natl Acad Sci U S A. 2018;115(14):E3106–E15.
   Web of Science ®Google Scholar
• Kuipers ME, Hokke CH, Smits HH, et al. Pathogen-derived extracellular vesicle-associated molecules that affect the host immune system: an overview. Front Microbiol. 2018;9:2182.
   PubMed Web of Science ®Google Scholar
• O’Donoghue EJ, Sirisaengtaksin N, Browning DF, et al. Lipopolysaccharide structure impacts the entry kinetics of bacterial outer membrane vesicles into host cells. PLoS Pathog. 2017;13(11):e1006760.
   Web of Science ®Google Scholar
• de la Torre-escudero E, Gerlach JQ, Bennett APS, et al. Surface molecules of extracellular vesicles secreted by the helminth pathogen Fasciola hepatica direct their internalisation by host cells. PLoS Negl Trop Dis. 2019;13(1):e0007087.
   PubMed Web of Science ®Google Scholar
• Nkurunungi G, van Diepen A, Nassuuna J, et al. Microarray assessment of N-glycan-specific IgE and IgG profiles associated with Schistosoma mansoni infection in rural and urban Uganda. Sci Rep. 2019;9(1):3522.
   Google Scholar
• van Diepen A, Smit CH, van Egmond L, et al. Differential anti-glycan antibody responses in Schistosoma mansoni-infected children and adults studied by shotgun glycan microarray. PLoS Negl Trop Dis. 2012;6(11):e1922.
   PubMed Web of Science ®Google Scholar
• Yang YY, Li XH, Brzezicka K, et al. Specific anti-glycan antibodies are sustained during and after parasite clearance in Schistosoma japonicum-infected rhesus macaques. PLoS Negl Trop Dis. 2017;11(2):e0005339.
   Web of Science ®Google Scholar
• Coakley G, McCaskill JL, Borger JG, et al. Extracellular vesicles from a helminth parasite suppress macrophage activation and constitute an effective vaccine for protective immunity. Cell Rep. 2017;19(8):1545–1557.
   PubMed Web of Science ®Google Scholar
• Engering A, Geijtenbeek TB, van Vliet SJ, et al. The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol. 2002;168(5):2118–2126.
   PubMed Web of Science ®Google Scholar
• Eichenberger RM, Ryan S, Jones L, et al. Hookworm secreted extracellular vesicles interact with host cells and prevent inducible colitis in mice. Front Immunol. 2018;9:850.
   Web of Science ®Google Scholar
• Gringhuis SI, Kaptein TM, Wevers BA, et al. Fucose-specific DC-SIGN signalling directs T helper cell type-2 responses via IKKepsilon- and CYLD-dependent Bcl3 activation. Nat Commun. 2014;5:3898.
   PubMed Web of Science ®Google Scholar
• Giera M, Kaisar MMM, Derks RJE, et al. The Schistosoma mansoni lipidome: leads for immunomodulation. Anal Chim Acta. 2018;1037:107–118.
   Web of Science ®Google Scholar
• Turner JD, Meurs L, Dool P, et al. Schistosome infection is associated with enhanced whole-blood IL-10 secretion in response to cercarial excretory/secretory products. Parasite Immunol. 2013;35(5–6):147–156.
   Web of Science ®Google Scholar
• Baribaud F, Pohlmann S, Leslie G, et al. Quantitative expression and virus transmission analysis of DC-SIGN on monocyte-derived dendritic cells. J Virol. 2002;76(18):9135–9142.
   Web of Science ®Google Scholar