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Glycans in the roles of parasitological diagnosis and host–parasite interplay

Published online by Cambridge University Press:  06 May 2019

Carolina De Marco Veríssimo ,
Carlos Graeff-Teixeira ,
Malcolm K. Jones  and
Alessandra L. Morassutti Open the ORCID record for Alessandra L. Morassutti [Opens in a new window]
Carolina De Marco Veríssimo
Affiliation:
Escola de Ciências, Pontifícia Universidade Católica do Rio Grande do Sul, Av. Ipiranga 6681, Porto Alegre RS 90619-900 Rio Grande do Sul, Brazil School of Biological Sciences, Queen's University Belfast, 2017, University Road, Belfast, BT7 1NN, Northern Ireland, UK
Carlos Graeff-Teixeira
Affiliation:
Escola de Ciências, Pontifícia Universidade Católica do Rio Grande do Sul, Av. Ipiranga 6681, Porto Alegre RS 90619-900 Rio Grande do Sul, Brazil
Malcolm K. Jones
Affiliation:
School of Veterinary Science, University of Queensland, St Lucia, Qld, 4072 Brisbane, Australia
Alessandra L. Morassutti*
Affiliation:
Escola de Ciências, Pontifícia Universidade Católica do Rio Grande do Sul, Av. Ipiranga 6681, Porto Alegre RS 90619-900 Rio Grande do Sul, Brazil
*
Author for correspondence: Alessandra Loureiro Morassutti, E-mail: [email protected]
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Abstract

The investigation of the glycan repertoire of several organisms has revealed a wide variation in terms of structures and abundance of glycan moieties. Among the parasites, it is possible to observe different sets of glycoconjugates across taxa and developmental stages within a species. The presence of distinct glycoconjugates throughout the life cycle of a parasite could relate to the ability of that organism to adapt and survive in different hosts and environments. Carbohydrates on the surface, and in excretory-secretory products of parasites, play essential roles in host–parasite interactions. Carbohydrate portions of complex molecules of parasites stimulate and modulate host immune responses, mainly through interactions with specific receptors on the surface of dendritic cells, leading to the generation of a pattern of response that may benefit parasite survival. Available data reviewed here also show the frequent aspect of parasite immunomodulation of mammalian responses through specific glycan interactions, which ultimately makes these molecules promising in the fields of diagnostics and vaccinology.

Keywords

Glycanshelminthimmune responseparasiteprotozoa
Type
Review Article
Information
Parasitology , Volume 146 , Issue 10 , September 2019 , pp. 1217 - 1232
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Copyright
Copyright © Cambridge University Press 2019 

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References

Abdulla, MH, Lim, KC, McKerrow, JH and Caffrey, CR (2011) Proteomic identification of IPSE/α-1 as a major hepatotoxin secreted by Schistosoma mansoni eggs. PLoS Neglected Tropical Diseases 5, e1368.Google Scholar
Aguirre García, M, Gutiérrez-Kobeh, L and López Vancell, R (2015) Entamoeba histolytica: adhesins and lectins in the trophozoite surface. Molecules 20, 2802–2815.Google Scholar
Akira, S (2006) TLR signaling. Current Topics in Microbiology and Immunology 311, 1–16. PMID: 17048703.Google Scholar
Alba Soto, CD, Mirkin, GA, Solana, ME and González Cappa, SM (2003) Trypanosoma cruzi infection modulates in vivo expression of major histocompatibility complex class II molecules on antigen-presenting cells and T-cell stimulatory activity of dendritic cells in a strain-dependent manner. Infection and Immunity 71, 194–199.Google Scholar
Allen, S, Richardson, JM, Mehlert, A and Ferguson, MA (2013) Structure of a complex phosphoglycan epitope from gp72 of Trypanosoma cruzi. The Journal of Biological Chemistry 288, 11093–11105.Google Scholar
Alvarez Errico, D, Medeiros, A, Míguez, M, Casaravilla, C, Malgor, R, Carmona, C, Nieto, A and Osinaga, E (2001) O-glycosylation in Echinococcus granulosus: identification and characterization of the carcinoma-associated Tn antigen. Experimental Parasitology 98, 100–109.Google Scholar
Aranzamendi, C, Tefsen, B, Jansen, M, Chiumiento, L, Bruschi, F, Kortbeek, T, Smith, DF, Cummings, RD, Pinelli, E and Van Die, I (2011) Glycan microarray profiling of parasite infection sera identifies the LDNF glycan as a potential antigen for serodiagnosis of trichinellosis. Experimental Parasitology 129, 221–226.Google Scholar
Argueta-Donohué, J, Carrillo, N, Valdés-Reyes, L, Zentella, A, Aguirre-García, M, Becker, I and Gutiérrez-Kobeh, L (2008) Leishmania mexicana: participation of NF-κB in the differential production of IL-12 in dendritic cells and monocytes induced by lipophosphoglycan (LPG). Experimental Parasitology 120, 1–9.Google Scholar
Bangs, JD (2018) Evolution of antigenic variation in African Trypanosomes: variant surface glycoprotein expression, structure, and function. Bioessays: News and Reviews in Molecular, Cellular and Developmental Biology 40, e1800181.Google Scholar
Behm, CA (1997) The role of trehalose in the physiology of nematodes. International Journal of Parasitology 27, 215–229.Google Scholar
Bennett, CL, Misslitz, A, Colledge, L, Aebischer, T and Blackburn, CC (2001) Silent infection of bone marrow-derived dendritic cells by Leishmania mexicana amastigotes. European Journal of Immunology 31, 876–883.Google Scholar
Bergwerff, AA, van Dam, GJ, Rotmans, JP, Deelder, AM, Kamerling, JP and Vliegenthart, JF (1994) The immunologically reactive part of immunopurified circulating anodic antigen from Schistosoma mansoni is a threonine-linked polysaccharide consisting of --> 6)-(beta-D-GlcpA-(1 --> 3))-beta-D-GalpNAc-(1 --> repeating units. Journal Biology Chemistry 269, 31510–7.+6)-(beta-D-GlcpA-(1+-->+3))-beta-D-GalpNAc-(1+-->+repeating+units.+Journal+Biology+Chemistry+269,+31510–7.>Google Scholar
Bhattacharya, A, Arya, R, Clark, CG and Ackers, JP (2000) Absence of lipophosphoglycan-like glycoconjugates in Entamoeba dispar. Parasitology 120, 31–35.Google Scholar
Brodskyn, C, Patricio, J, Oliveira, R, Lobo, L, Arnholdt, A, Mendonça-Previato, L, Barral, A and Barral-Netto, M (2002) Glycoinositolphospholipids from Trypanosoma cruzi interfere with macrophages and dendritic cell responses. Infection and Immunity 70, 3736–3743.Google Scholar
Bulik, DA, van Ophem, P, Manning, JM, Shen, Z, Newburg, DS and Jarroll, EL (2000) UDP-N-acetylglucosamine pyrophosphorylase, a key enzyme in encysting Giardia, is allosterically regulated. The Journal of Biological Chemistry 275, 14722–14728.Google Scholar
Caldas, IR, Campi-Azevedo, AC, Oliveira, LF, Silveira, AM, Oliveira, RC and Gazzinelli, G (2008) Human schistosomiasis mansoni: immune responses during acute and chronic phases of the infection. Acta Tropica 108, 109–117.Google Scholar
Campos, MAS, Almeida, IC, Takeuchi, O, Akira, S, Valente, EP, Procópio, DO, Travassos, LR, Smith, JA, Golenbock, DT and Gazzinelli, RT (2001) Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite. Journal of Immunology 167, 416–423.Google Scholar
Casacuberta, M, Kinunghi, S, Vennervald, BJ and Olsen, A (2016) Evaluation and optimization of the Circulating Cathodic Antigen (POC-CCA) cassette test for detecting Schistosoma mansoni infection by using image analysis in school children in Mwanza Region, Tanzania. Parasite Epidemiology and Control 1, 105–115.Google Scholar
Casaravilla, C, Freire, T, Malgor, R, Medeiros, A, Osinaga, E and Carmona, C (2003) Mucin-type O-glycosylation in helminth parasites from major taxonomic groups: evidence for widespread distribution of the Tn antigen (GalNAc-Ser/Thr) and identification of UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase activity. Journal of Parasitology 89, 709–714.Google Scholar
Chakir, H, Campos-Neto, A, Mojibian, M and Webb, JR (2003) IL-12Rβ2-deficient mice of a genetically resistant background are susceptible to Leishmania major infection and develop a parasite-specific Th2 immune response. Microbes and Infection 5, 241–249.Google Scholar
Chuah, C, Jones, MK, Burke, ML, Owen, HC, Anthony, BJ, McManus, DP, Ramm, GA and Gobert, GN (2013) Spatial and temporal transcriptomics of Schistosoma japonicum-induced hepatic granuloma formation reveals novel roles for neutrophils. Journal of Leukocyte Biology 94, 353–365.Google Scholar
Cipollo, JF, Awad, AM, Costello, CE and Hirschberg, CB (2005) N-glycans of Caenorhabditis elegans are specific to developmental stages. The Journal of Biological Chemistry 280, 26063–26072.Google Scholar
Clark, IA and Schofield, L (2000) Pathogenesis of malaria. Parasitology Today 16, 451–454.Google Scholar
Coelho-Finamore, JM, Freitas, VC, Assis, RR, Melo, MN, Novozhilova, N, Secundino, NF, Pimenta, PF, Turco, SJ and Soares, RP (2011) Leishmania infantum: lipophosphoglycan intraspecific variation and interaction with vertebrate and invertebrate hosts. International Journal for Parasitology 41, 333–342.Google Scholar
Colley, DG, Binder, S, Campbell, C, King, CH, Tchuem Tchuenté, LA, N'Goran, EK, Erko, B, Karanja, DM, Kabatereine, NB, van Lieshout, L and Rathbun, S (2013) A five-country evaluation of a point-of-care circulating cathodic antigen urine assay for the prevalence of Schistosoma mansoni. The American Journal of Tropical Medicine and Hygiene 88, 426–432.Google Scholar
Corstjens, PL, De Dood, CJ, Kornelis, D, Fat, EM, Wilson, RA, Kariuki, TM, Nyakundi, RK, Loverde, PT, Abrams, WR, Tanke, HJ, Van Lieshout, L, Deelder, AM and Van Dam, GJ (2014) Tools for diagnosis, monitoring and screening of Schistosoma infections utilizing lateral-flow based assays and upconverting phosphor labels. Parasitology 141, 1841–1855.Google Scholar
Costa, F, Franchin, G, Pereira-Chioccola, VL, Ribeirão, M, Schenkman, S and Rodrigues, MM (1998) Immunization with a plasmid DNA containing the gene of trans-sialidase reduces Trypanosoma cruzi infection in mice. Vaccine 16, 768–774.Google Scholar
Cova, M, Rodrigues, JA, Smith, TK and Izquierdo, L (2015) Sugar activation and glycosylation in Plasmodium. Malaria Journal 14, 427.Google Scholar
Cummings, RD (2009) The repertoire of glycan determinants in the human glycome. Molecular BioSystems 5, 1087–1104.Google Scholar
Cummings, RD and Nyame, AK (1996) Glycobiology of schistosomiasis. The FASEB Journal 10, 838–848.Google Scholar
Cummings, RD and Nyame, AK (1999) Schistosome glycoconjugates. Biochimica et Biophysica Acta 1455, 363–374.Google Scholar
Damerow, M, Rodrigues, JA, Wu, D, Güther, ML, Mehlert, A and Ferguson, MA (2014) Identification and functional characterization of a highly divergent N-acetylglucosaminyltransferase I (TbGnTI) in Trypanosoma brucei. The Journal of Biological Chemistry 289, 9328–9339.Google Scholar
Damerow, M, Graalfs, F, Güther, ML, Mehlert, A, Izquierdo, L and Ferguson, MA (2016) A gene of the β3-glycosyltransferase family encodes N-acetylglucosaminyltransferase II function in Trypanosoma brucei. The Journal of Biological Chemistry 291, 13834–13845.Google Scholar
Deelder, AM, Kornelis, D, Van Marck, EA, Eveleigh, PC and Van Egmond, JG (1980) Schistosoma mansoni: characterization of two circulating polysaccharide antigens and the immunological response to these antigens in mouse, hamster, and human infections. Experimetal Parasitology 50, 16–32, PMID: 7389856.Google Scholar
Del Puerto, L, Rovetta, R, Navatta, M, Fontana, C, Lin, G, Moyna, G, Dematteis, S, Brehm, K, Koziol, U, Ferreira, F and Díaz, A (2016) Negligible elongation of mucin glycans with Gal β1–3 units distinguishes the laminated layer of Echinococcus multilocularis from that of Echinococcus granulosus. International Journal for Parasitology 46, 311–321.Google Scholar
Dell, A, Haslam, SM, Morris, HR and Khoo, KH (1999) Immunogenic glycoconjugates implicated in parasitic nematode diseases. Biochimica et Biophysica Acta 1455, 353–362.Google Scholar
Descoteaux, A and Turco, SJ (1999) Glycoconjugates in Leishmania infectivity. Biochimica et Biophysica Acta 1455, 341–352.Google Scholar
de Souza, JB, Runglall, M, Corran, PH, Okell, LC, Kumar, S, Gowda, DC, Couper, KN and Riley, EM (2010) Neutralization of malaria glycosylphosphatidylinositol in vitro by serum IgG from malaria-exposed individuals. Infection and Immunity 78, 3920–3929.Google Scholar
De Veer, MJ, Curtis, JM, Baldwin, TM, Didonato, JA, Sexton, A, Mcconville, MJ, Handman, E and Schofield, L (2003) Myd88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and toll-like receptor 2 signaling. European Journal of Immunology 33, 2822–2831.Google Scholar
Díaz, A, Fontana, EC, Todeschini, AR, Soulé, S, González, H, Casaravilla, C, Portela, M, Mohana-Borges, R, Mendonça-Previato, L, Previato, JO and Ferreira, F (2009) The major surface carbohydrates of the Echinococcus granulosus cyst: mucin-type O-glycans decorated by novel galactose-based structures. Biochemistry 48, 11678–11691.Google Scholar
Diebold, SS (2009) Activation of dendritic cells by toll-like receptors and C-type lectins. Handbook of Experimental Pharmacology 188, 3–30.Google Scholar
Eberl, M, Langermans, JA, Vervenne, RA, Nyame, AK, Cummings, RD, Thomas, AW, Coulson, PS and Wilson, RA (2001) Antibodies to glycans dominate the host response to schistosome larvae and eggs: is their role protective or subversive? The Journal of Infectious Diseases 183, 1238–1247.Google Scholar
Erdmann, H, Steeg, C, Koch-Nolte, F, Fleischer, B and Jacobs, T (2009) Sialylated ligands on pathogenic Trypanosoma cruzi interact with Siglec-E (sialic acid-binding Ig-like lectin-E). Cellular Microbiology 11, 1600–1611.Google Scholar
Everts, B, Hussaarts, L, Driessen, NN, Meevissen, MHJ, Schramm, G, van der Ham, AJ, van der Hoeven, B, Scholzen, T, Burgdorf, S, Mohrs, M, Pearce, EJ, Hokke, CH, Haas, H, Smits, HH and Yazdanbakhsh, M (2012) Schistosome-derived omega-1 drives Th2 polarization by suppressing protein synthesis following internalization by the mannose receptor. The Journal of Experimental Medicine 209, 1753–1767.Google Scholar
Ferguson, MA (1999) The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. Journal of Cell Science 112, 2799–2809.Google Scholar
Ferguson, BJ, Newland, SA, Gibbs, SE, Tourlomousis, P, Fernandes dos Santos, P, Patel, MN, Hall, SW, Walczak, H, Schramm, G, Haas, H, Dunne, DW, Cooke, A and Zaccone, P (2015) The Schistosoma mansoni T2 ribonuclease omega-1 modulates inflammasome-dependent IL-1beta secretion in macrophages. International Journal for Parasitology 45, 809–813.Google Scholar
Fincher, GB (2009) Exploring the evolution of (1,3; 1,4)-β-D-glucans in plant cell walls: comparative genomics can help!. Current Opinion in Plant Biology 12, 140–147.Google Scholar
Forbes, LB, Appleyard, GD and Gajadhar, AA (2004) Comparison of synthetic tyvelose antigen with excretory-secretory antigen for the detection of trichinellosis in swine using enzyme-linked immunosorbent assay. Journal of Parasitology 90, 835–840.Google Scholar
Forestier, CL, Gao, Q and Boons, GJ (2015) Leishmania lipophosphoglycan: how to establish structure-activity relationships for this highly complex and multifunctional glycoconjugate? Frontiers in Cellular and Infection Microbiology 4, 193.Google Scholar
Freire, T, Casaravilla, C, Carmona, C and Osinaga, E (2003) Mucin type O-glycosylation in Fasciola hepatica: characterization of carcinoma associated Tn and sialyl-Tn antigens and evaluation of UDP-GalNAc: polypeptide N-acetylgalactosaminyltransferase activity. International Journal of Parasitology 33, 47–56.Google Scholar
Gala, RP, D'Souza, M and Zughaier, SM (2016) Evaluation of various adjuvant nanoparticulate formulations for meningococcal capsular polysaccharide-based vaccine. Vaccine 34, 3260–3267.Google Scholar
Garcia-Campos, A, Ravidà, A, Nguyen, DL, Cwiklinski, K, Dalton, JP, Hokke, CH, O'Neill, S and Mulcahy, G (2016) Tegument glycoproteins and cathepsins of newly excysted juvenile Fasciola hepatica carry mannosidic and paucimannosidic N-glycans. PLoS Neglected Tropical Diseases 10, e0004688.Google Scholar
Geijtenbeek, TB and Gringhuis, SI (2009) Signalling through C-type lectin receptors: shaping immune responses. Nature Reviews Immunology 9, 465–479.Google Scholar
Geijtenbeek, TB, Van Vliet, SJ, Koppel, EA, Sanchez-Hernandez, M, Vandenbroucke-Grauls, CM, Appelmelk, B and Van Kooyk, Y (2003) Mycobacteria target DC-SIGN to suppress dendritic cell function. Journal Experimental Medicine 197, 7–17.Google Scholar
Georgieva, K, Georgieva, S, Mizinska, Y and Stoitsova, SR (2012) Fasciola hepatica miracidia: lectin binding and stimulation of in vitro miracidium-to-sporocyst transformation. Acta Parasitologica 57, 46–52.Google Scholar
Giddings, OK, Eickhoff, CS, Sullivan, NL and Hoft, df (2010) Intranasal vaccinations with the trans-sialidase antigen plus CpG adjuvant induce mucosal immunity protective against conjunctival Trypanosoma cruzi challenges. Infection and Immunity 78, 1333–1338.Google Scholar
Goel, A, Vohra, H and Varshney, GC (1999) Strain-specific recognition of live Leishmania donovani promastigotes by homologous antiserum raised against a crude membrane fraction of infected macrophages. Parasitology Research 85, 19–24.Google Scholar
Gomez-Garcia, L, Lopez-Marin, LM, Saavedra, R, Reyes, JL, Rodriguez-Sosa, M and Terrazas, LI (2005) Intact glycans from cestode antigens are involved in innate activation of myeloid suppressor cells. Parasite Immunology 27, 395–405.Google Scholar
Gómez-García, L, Rivera-Montoya, I, Rodríguez-Sosa, M and Terrazas, LI (2006) Carbohydrate components of Taenia crassiceps metacestodes display Th2-adjuvant and antiinflammatory properties when co-injected with bystander antigen. Parasitology Research 99, 440–448.Google Scholar
Goodridge, HS, Marshall, FA, Else, KJ, Houston, KM, Egan, C, Al-Riyami, L, Liew, FY, Harnett, W and Harnett, MM (2005) Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine-containing secreted product, ES-62. Journal of Immunology 174, 284–293.Google Scholar
Gowda, DC and Davidson, EA (1999) Protein glycosylation in the malaria parasite. Parasitology today 15, 147–152.Google Scholar
Goyal, PK, Wheatcroft, J and Wakelin, D (2002) Tyvelose and protective responses to the intestinal stages of Trichinella spiralis. Parasitology International 51, 91–98.Google Scholar
Guha-Niyogi, A, Sullivan, DR and Turco, SJ (2001) Glycoconjugate structures of parasitic protozoa. Glycobiology 11, 45R–59R.Google Scholar
Handel, TM, Johnson, Z, Crown, SE, Lau, EK and Proudfoot, AE (2005) Regulation of protein function by glycosaminoglycans as exemplified by chemokines. Annual Review of Biochemistry 74, 385–410.Google Scholar
Haslam, SM, Coles, GC, Morris, HR and Dell, A (2000) Structural characterization of the N-glycans of Dictyocaulusviviparus: discovery of the Lewis(x) structure in a nematode. Glycobiology 10, 223–229.Google Scholar
Haslam, SM, Coles, GC, Munn, EA, Smith, TS, Smith, HF, Morris, HR and Dell, A (1996) Haemonchus contortus glycoproteins contain N-linked oligosaccharides with novel highly fucosylated core structures. The Journal of Biological Chemistry 271, 30561–30570.Google Scholar
Haslam, SM, Coles, GC, Reason, AJ, Morris, HR and Dell, A (1998) The novel core fucosylation of Haemonchus contortus N-glycans is stage specific. Molecular and Biochemical Parasitology 93, 143–147.Google Scholar
Haslam, SM, Houston, KM, Harnett, W, Reason, AJ, Morris, HR and Dell, A (1999) Structural studies of N-glycans of filarial parasites. Conservation of phosphorylcholine-substituted glycans among species and discovery of novel chito-oligomers. The Journal of Biological Chemistry 274, 20953–20960.Google Scholar
Haslam, SM, Morris, HR and Dell, A (2001) Mass spectrometric strategies: providing structural clues for helminth glycoproteins. Trends in Parasitology 17, 231–235.Google Scholar
Haslam, SM, Restrepo, BI, Obregón-Henao, A, Teale, JM, Morris, HR and Dell, A (2003) Structural characterization of the N-linked glycans from Taenia solium metacestodes. Molecular and Biochemical Parasitology 126, 103–107.Google Scholar
Hawk, MW, Shahlaie, K, Kim, KD and Theis, JH (2005) Neurocysticercosis: a review. Surgical Neurology 63, 123–132.Google Scholar
Heim, C, Hertzberg, H, Butschi, A, Bleuler-Martinez, S, Aebi, M, Deplazes, P, Künzler, M and Štefanić, S (2015) Inhibition of Haemonchus contortus larval development by fungal lectins. Parasites and Vectors 19, 425.Google Scholar
Hoft, df, Eickhoff, CS, Giddings, OK, Vasconcelos, JR and Rodrigues, MM (2007) Trans-sialidase recombinant protein mixed with CpG motif-containing oligodeoxynucleotide induces protective mucosal and systemic Trypanosoma cruzi immunity involving CD8+CTL and B cell-mediated cross-priming. The Journal of Immunology 179, 6889–6900.Google Scholar
Hokke, CH and Deelder, AM (2001) Schistosome glycoconjugates in host-parasite interplay. Glycoconjugate Journal 18, 573–587.Google Scholar
Hokke, CH and van Diepen, A (2017) Helminth glycomics – glycan repertoires and host-parasite interactions. Molecular and Biochemical Parasitology 215, 47–57.Google Scholar
Hokke, CH, Deelder, AM, Hoffmann, KF and Wuhrer, M (2007) Glycomics-driven discoveries in schistosome research. Experimental Parasitology 117, 275–283.Google Scholar
Hülsmeier, AJ, Gehrig, PM, Geyer, R, Sack, R, Gottstein, B, Deplazes, P and Köhler, P (2002) A major Echinococcus multilocularis antigen is a mucin-type glycoprotein. The Journal of Biological Chemistry 277, 5742–5748.Google Scholar
Hwa, KY and Khoo, KH (2000) Structural analysis of the asparagine-linked glycans from the procyclic Trypanosoma brucei and its glycosylation mutants resistant to Concanavalin A killing. Molecular Biochemical Parasitology 111, 173–184, PMID: 11087927.Google Scholar
Ibraim, IC, de Assis, RR, Pessoa, NL, Campos, MA, Melo, MN, Turco, SJ and Soares, RP (2013) Two biochemically distinct lipophosphoglycans from Leishmania braziliensis and Leishmania infantum trigger different innate immune responses in murine macrophages. Parasites & Vectors 6, 54–65. doi: 10.1186/1756-3305-6-54.Google Scholar
Ilg, T, Stierhof, YD, McConville, MJ and Overath, P (1995) Purification, partial characterization and immunolocalization of a proteophosphoglycan secreted by Leishmania mexicana amastigotes. European Journal of Cell Biology 66, 205–215.Google Scholar
Ingold, K, Gottstein, B and Hemphill, A (2000) High molecular mass glycans are major structural elements associated with the laminated layer of in vitro cultivated Echinococcus multilocularis metacestodes. International Journal of Parasitology 30, 207–214.Google Scholar
Ivory, CPA and Chadee, K (2007) Activation of dendritic cells by the Gal-lectin of Entamoeba histolytica drives Th1 responses in vitro and in vivo. European Journal of Immunology 37, 385–394.Google Scholar
Jacobs, W, Deelder, A and Van Marck, E (1999) Schistosomal granuloma modulation. II. Specific immunogenic carbohydrates can modulate schistosome-egg-antigen-induced hepatic granuloma formation. Parasitology Research 85, 14–18.Google Scholar
Jang-Lee, J, Curwen, RS, Ashton, PD, Tissot, B, Mathieson, W, Panico, M, Dell, A, Wilson, RA and Haslam, SM (2007) Glycomics analysis of Schistosoma mansoni egg and cercarial secretions. Molecular and Cellular Proteomics 6, 1485–1499.Google Scholar
Jaurigue, JA and Seeberger, PH (2017) Parasite carbohydrate vaccines. Frontiers in Cellular and Infection Microbiology 12, 248.Google Scholar
Jawed, JJ, Majumder, S, Bandyopadhyay, S, Biswas, S, Parveen, S and Majumdar, S (2016) SLA-PGN-primed dendritic cell-based vaccination induces Th17-mediated protective immunity against experimental visceral leishmaniasis: a crucial role of PKCβ. Pathogens and Disease 74, pii: ftw041.Google Scholar
Jebbari, H, Stagg, AJ, Davidson, RN and Knight, SC (2002) Leishmania major promastigotes inhibit dendritic cell motility in vitro. Infection and Immunity 70, 1023–1026.Google Scholar
Jones, MK, Gobert, GN, Zhang, L, Sunderland, P and McManus, DP (2004) The cytoskeleton and motor proteins of human schistosomes and their roles in surface maintenance and host-parasite interactions. Bioessays. 26, 752–765.Google Scholar
Kearney, PE, Murray, PJ, Hoy, JM, Hohenhaus, M and Kotze, A (2016) The ‘Toolbox’ of strategies for managing Haemonchus contortus in goats: What's in and what's out. Veterinaryparasitology 15, 93–107.Google Scholar
Kailemia, MJ, Ruhaak, LR, Lebrilla, CB and Amster, IJ (2014) Oligosaccharide analysis by mass spectrometry: a review of recent developments. Analytical Chemistry 86, 196–212.Google Scholar
Kane, CM, Cervi, L, Sun, J, et al. (2004) Helminth antigens modulate TLR-initiated dendritic cell activation. Journal of Immunology 173, 7454–7461.Google Scholar
Kane, CM, Jung, E and Pearce, EJ (2008) Schistosoma mansoni egg antigen-mediated modulation of toll-like receptor (TLR)-induced activation occurs independently of TLR2, TLR4, and MyD88. Infection and Immunity 76, 5754–5759.Google Scholar
Kantelhardt, SR, Wuhrer, M, Dennis, RD, Doenhoff, MJ, Bickle, Q and Geyer, R (2002) Fuc(alpha1-->3)GalNAc-: the major antigenic motif of Schistosoma mansoni glycolipids implicated in infection sera and keyhole-limpet haemocyanin cross-reactivity. Biochemical Journal 366, 217–223.3)GalNAc-:+the+major+antigenic+motif+of+Schistosoma+mansoni+glycolipids+implicated+in+infection+sera+and+keyhole-limpet+haemocyanin+cross-reactivity.+Biochemical+Journal+366,+217–223.>Google Scholar
Kapsenberg, ML (2003) Dendritic-cell control of pathogen-driven T-cell polarization. Nature Reviews. Immunology 3, 984–993.Google Scholar
Karanja, DM, Colley, DG, Nahlen, BL, Ouma, JH and Secor, WE (1997) Studies of schistosomiasis in Western Kenya: I. Evidence for immune-facilitated excretion of schistosome eggs from patients with Schistosoma mansoni and human immunodeficiency virus coinfections. The American Journal of Tropical Medicine and Hygiene 56, 515–521, PMID: 9180601.Google Scholar
Kariuki, TM, Farah, IO, Wilson, RA and Coulson, PS (2008) Antibodies elicited by the secretions from schistosome cercariae and eggs are predominantly against glycan epitopes. Parasite Immunology 30, 554–562.Google Scholar
Khan, AH, Qazi, AM, Hoessli, DC, Torred-Duarte, AP, Senaldi, G, Qazi, MH, Walker-Nasir, E and Nasir-ud-Din, (1997) Carbohydrate moiety of Plasmodium falciparum glycoproteins: the nature of the carbohydrate-peptide linkage in the MSP-2 glycoprotein. Biochemistry and Molecular Biology International 43, 655–668.Google Scholar
Khoo, KH, Maizels, RM, Page, AP, Taylor, GW, Rendell, NB and Dell, A (1991) Characterization of nematode glycoproteins: the major O-glycans of Toxocara excretory-secretory antigens are O-methylated trisaccharides. Glycobiology 1, 163–171.Google Scholar
Khoo, KH, Sarda, S, Xu, X, Caulfield, JP, McNeil, MR, Homans, SW, Morris, HR and Dell, A (1995) A unique multifucosylated-3GalNAc beta 1-->4GlcNAc beta 1-->3Gal alpha 1- motif constitutes the repeating unit of the complex O-glycans derived from the cercarial glycocalyx of Schistosoma mansoni. The Journal of Biological Chemistry 270, 17114–17123.4GlcNAc+beta+1-->3Gal+alpha+1-+motif+constitutes+the+repeating+unit+of+the+complex+O-glycans+derived+from+the+cercarial+glycocalyx+of+Schistosoma+mansoni.+The+Journal+of+Biological+Chemistry+270,+17114–17123.>Google Scholar
Khoo, KH, Nieto, A, Morris, HR and Dell, A (1997) Structural characterization of the N-glycans from Echinococcus granulosus hydatid cyst membrane and protoscoleces. Molecular and Biochemical Parasitology 86, 237–248.Google Scholar
Kimura, EA, Couto, AS, Peres, VJ, Casal, OL and Katzin, AM (1996) N-linked glycoproteins are related to schizogony of the intraerythrocytic stage in Plasmodium falciparum. The Journal of Biological Chemistry 271, 14452–14461, PMID: 8662869.Google Scholar
Ko, AI, Dräger, UC and Harn, DA (1990) A Schistosoma mansoni epitope recognized by a protective monoclonal antibody is identical to the stage-specific embryonic antigen 1. Proceedings of the National Academy of Sciences USA 87, 4159–4163.Google Scholar
Koga, R, Hamano, S, Kuwata, H, Atarashi, K, Ogawa, M, Hisaeda, H, Yamamoto, M, Akira, S, Himeno, K, Matsumoto, M and Takeda, K (2006) TLR-dependent induction of IFN-β mediates host defense against Trypanosoma cruzi. Journal of Immunology 177, 7059–7066.Google Scholar
Koizumi, A, Yamano, K, Schweizer, F, Takeda, T, Kiuchi, F and Hada, N (2011) Synthesis of the carbohydrate moiety from the parasite Echinococcus multilocularis and their antigenicity against human sera. European Journal of Medicinal Chemistry 46, 1768–1778.Google Scholar
Konecny, P, Stagg, AJ, Jebbari, H, English, N, Davidson, RN and Knight, SC (1999) Murine dendritic cells internalize Leishmania major promastigotes, produce IL-12 p40 and stimulate primary T cell proliferation in vitro. European Journal of Immunology 29, 1803–1811.Google Scholar
Kusel, JR, Al-Adhami, BH and Doenhoff, MJ (2007) The schistosome in the mammalian host: understanding the mechanisms of adaptation. Parasitology 134, 1477–1526.Google Scholar
Lauwaet, T, Oliveira, MJ, De Bruyne, G, Bruchhaus, I, Duche ne, M, Mareel, M and Leroy, A (2004) Entamoeba histolytica trophozoites transfer lipophosphopeptidoglycans to enteric cell layers. International Journal for Parasitology 34, 549–556.Google Scholar
Lee, JJ, Dissanayake, S, Panico, M, Morris, HR, Dell, A and Haslam, SM (2005) Mass spectrometric characterisation of Taenia crassiceps metacestode N-glycans. Molecular and Biochemical Parasitology 143, 245–249.Google Scholar
Lehr, T, Frank, S, Natsuka, S, Geyer, H, Beuerlein, K, Doenhoff, MJ, Hase, S and Geyer, R (2010) N-Glycosylation patterns of hemolymph glycoproteins from Biomphalaria glabrata strains expressing different susceptibility to Schistosoma mansoni infection. Experimental Parasitology 126, 592–602.Google Scholar
Lindholz, CG, Favero, V, Verissimo, CM, Candido, RRF, de Souza, RP, Dos Santos, RR, Morassutti, AL, Bittencourt, HR, Jones, MK, St Pierre, TG and Graeff-Teixeira, C (2018) Study of diagnostic accuracy of Helmintex, Kato-Katz, and POC-CCA methods for diagnosing intestinal schistosomiasis in Candeal, a low intensity transmission area in northeastern Brazil. PLoS Neglected Tropical Diseases 12, 1–16.Google Scholar
Linehan, SA, Coulson, PS, Wilson, RA, Mountford, AP, Brombacher, F, Martínez-Pomares, L and Gordon, S (2003) IL-4 receptor signaling is required for mannose receptor expression by macrophages recruited to granulomata but not resident cells in mice infected with Schistosoma mansoni. Laboratory Investigation 83, 1223–1231.Google Scholar
Liu, X, Siegrist, S, Amacker, M, Zurbriggen, R, Pluschke, G and Seeberger, PH (2006) Enhancement of the immunogenicity of synthetic carbohydrates by conjugation to virosomes: a leishmaniasis vaccine candidate. ACS Chemical Biology 1, 161–164.Google Scholar
Lochnit, G, Nispel, S, Dennis, RD and Geyer, R (1998) Structural analysis and immunohistochemical localization of two acidic glycosphingolipids from the porcine, parasitic nematode, Ascaris suum. Glycobiology 8, 891–899.Google Scholar
Lorenzo, C, Salinas, G, Brugnini, A, Wernstedt, C, Hellman, U and González-Sapienza, G (2003) Echinococcus granulosus antigen 5 is closely related to proteases of the trypsin family. Biochemical Journal 369, 191–198.Google Scholar
Magnelli, P, Cipollo, JF, Ratner, DM, Cui, J, Kelleher, D, Gilmore, R, Costello, CE, Robbins, PW and Samuelson, J (2008) Unique Asn-linked oligosaccharides of the human pathogen Entamoeba histolytica. The Journal of Biological Chemistry 283, 18355–18364.Google Scholar
Maizels, RM, Balic, A, GomezEscobar, N, Nair, M, Taylor, MD and Allen, JE (2004) Helminth parasites – masters of regulation. Immunological Reviews 201, 89–116.Google Scholar
Maldonado-Bernal, C, Kirschning, CJ, Rosenstein, Y, Rocha, LM, Rios-Sarabia, N, Espinosa-Cantellano, M, Becker, I, Estrada, I, Salazar-González, RM, López-Macías, C, Wagner, H, Sánchez, J and Isibasi, A (2005) The innate immune response to Entamoeba histolytica lipopeptidophosphoglycan is mediated by toll-like receptors 2 and 4. Parasite Immunology 27, 127–137.Google Scholar
Marinets, A, Zhang, T, Guillen, N, Gounon, P, Bohle, B, Vollmann, U, Scheiner, O, Wiedermann, G, Stanley, SL Jr and Duchene, M (1997) Protection against invasive amebiasis by a single monoclonal antibody directed against a lipophosphoglycan antigen localized on the surface of Entamoeba histolytica. The Journal of Experimental Medicine 186, 1557–1565.Google Scholar
Medeiros, A, Chiribao, ML, Ubillos, L, Festari, MF, Saldaña, J, Robello, C, Domínguez, L, Calvete, JJ and Osinaga, E (2008) Mucin-type O-glycosylation in Mesocestoides vogae (syn. corti). International Journal of Parasitology 38, 265–276.Google Scholar
Mickum, ML, Prasanphanich, NS, Heimburg-Molinaro, J, Leon, KE and Cummings, RD (2014) Deciphering the glycogenome of schistosomes. Frontiers in Genetics 5, 262.Google Scholar
Montero-Barrera, D, Valderrama-Carvajal, H, Terrazas, CA, Rojas-Hernández, S, Ledesma-Soto, Y, Vera-Arias, L, Carrasco-Yépez, M, Gómez-García, L, Martínez-Saucedo, D, Becerra-Díaz, M and Terrazas, LI (2015) The macrophages galactose-type lectin-1 (MGL1) recognizes Taenia crassiceps antigens, triggers intracellular signaling, and is critical for resistance to this infection. BioMed Research International 2015, 615865.Google Scholar
Mendonça-Previato, L, Todeschini, AR, Heise, N and Previato, JO (2003) Protozoan parasite-specific carbohydrate structures. Current Opinion in Structural Biology 15, 499–505.Google Scholar
Moody, S, Becker, S, Nuchamowitz, Y and Mirelman, D (1997) Virulent and avirulent Entamoeba histolytica and E. dispar differ in their cell surface phosphorylated glycolipids. Parasitology 114, 95–104.Google Scholar
Moody-Haupt, S, Patterson, JH, Mirelman, D and McConville, MJ (2000) The major surface antigens of Entamoeba histolytic trophozoites are GPI-anchored proteophosphoglycans. Journal of Molecular Biology 297, 409–420.Google Scholar
Morassutti, AL, Levert, K, Perelygin, A, da Silva, AJ, Wilkins, P and Graeff-Teixeira, C (2012) The 31-kDa antigen of Angiostrongylus cantonensis comprises distinct antigenic glycoproteins. Vector Borne Zoonotic Disease 12, 961–968.Google Scholar
Morelle, W, Haslam, SM, Olivier, V, Appleton, JA, Morris, HR and Dell, A (2000) Phosphorylcholine-containing N-glycans of Trichinella spiralis: identification of multiantennary lacdiNAc structures. Glycobiology 10, 941–950.Google Scholar
Mwanakasale, V, Vounatsou, P, Sukwa, TY, Ziba, M, Ernest, A and Tanner, M (2003) Interactions between Schistosoma haematobium and human immunodeficiency virus type 1: the effects of coinfection on treatment outcomes in rural Zambia. The American Journal of Tropical Medicine and Hygiene 69, 420–428, PMID: 14640503.Google Scholar
Naderer, T, Vince, J and McConville, MAJ (2004) Surface determinants Leishmania parasites and their role in infectivity in the mammalian host. Current Molecular Medicine 4, 649–665.Google Scholar
Niborski, V, Vallée, I, Fonseca-Liñán, R, Boireau, P, Enciso, A, Ortega-Pierres, G and Yépez-Mulia, L (2004) Trichinella spiralis: stimulation of mast cells by TSL-1 antigens trigger cytokine mRNA expression and release of IL-4 and TNF through an Ig-independent pathway. Experimental Parasitology 108, 101–108.Google Scholar
Norden, AP and Strand, M (1985) Identification of antigenic Schistosoma mansoni glycoproteins during the course of infection in mice and humans. The American Journal of Tropical Medicine and Hygiene 34, 495–507.Google Scholar
Nunes Dda, S, Gonzaga, HT, Ribeiro Vda, S, da Cunha, JP Jr and Costa-Cruz, J. M. (2013) Taenia saginata metacestode antigenic fractions obtained by ion-exchange chromatography: potential source of immunodominant markers applicable in the immunodiagnosis of human neurocysticercosis. Diagnostic Microbiology and Infectious Disease 76, 36–41.Google Scholar
N'Zoukoudi-N'Doundou, MY, Dirat, I, Akouala, JJ, Penchenier, L, Makuwa, M and Rey, JL (1995) Bilharziasis and human immunodeficiency virus infection in Congo. Medecine Tropicale (Mars) 55, 249–251, PMID: 8559022.Google Scholar
Nyame, AK, Debose-Boyd, R, Long, TD, Tsang, VC and Cummings, RD (1998) Expression of Lex antigen in Schistosoma japonicum and S. haematobium and immune responses to Lex in infected animals: lack of Lex expression in other trematodes and nematodes. Glycobiology 8, 615–624.Google Scholar
Nyame, AK, Yoshino, TP and Cummings, RD (2002) Differential expression of LacdiNAc, fucosylated LacdiNAc, and Lewis x glycan antigens in intramolluscan stages of Schistosoma mansoni. Journal of Parasitology 88, 890–897.Google Scholar
Nyame, AK, Lewis, FA, Doughty, BL, Correa-Oliveira, R and Cummings, RD (2003) Immunity to schistosomiasis: glycans are potential antigenic targets for immune intervention. Experimental Parasitology 104, 1–13.Google Scholar
Nyame, AK, Kawar, ZS and Cummings, RD (2004) Antigenic glycans in parasitic infections: implications for vaccines and diagnostics. Archives of Biochemistry and Biophysics 426, 182–200.Google Scholar
Okano, M, Satoskar, AR, Nishizaki, K and Harn, DA Jr (2001) Lacto-N-fucopentaose III found on Schistosoma mansoni egg antigens functions as adjuvant for proteins by inducing Th2-type response. Journal of Immunology 167, 442–450.Google Scholar
Papanastasiou, P, McConville, MJ, Ralton, J and Köhler, P (1997) The variant-specific surface protein of Giardia, VSP4A1, is a glycosylated and palmitoylated protein. Biochemical Journal 322, 49–56.Google Scholar
Paschinger, K and Wilson, IB (2015) Two types of galactosylated fucose motifis are present on N-glycans of Haemonchus contortus. Glycobiology 25, 585–590.Google Scholar
Paschinger, K, GonzalezSapienza, GG and Wilson, IBH (2012) Mass spectrometric analysis of the immunodominant glycan epitope of Echinococcus granulosus antigen Ag5. International Journal for Parasitology 42, 279–285.Google Scholar
Pereira-Chioccola, VL, Costa, F, Ribeirão, M, Soares, IS, Arena, F, Schenkman, S and Rodrigues, MM (1999) Comparison of antibody and protective immune responses against Trypanosoma cruzi infection elicited by immunization with a parasite antigen delivered as naked DNA or recombinant protein. Parasite Immunology 21, 103–110.Google Scholar
Peterson, NA, Hokke, CH, Deelder, AM and Yoshino, TP (2009) Glycotope analysis in miracidia and primary sporocysts of Schistosoma mansoni: differential expression during the miracidium-to-sporocyst transformation. International Journal of Parasitology 39, 1331–1344.Google Scholar
Peterson, NA, Anderson, TK and Yoshino, TP (2013) In silico analysis of the fucosylation-associated genome of the human blood fluke Schistosoma mansoni: cloning and characterization of the fucosyltransferase multigene family. PLoS ONE 8, e63299.Google Scholar
Petri, W Jr (1996) Amebiasis and the Entamoeba histolytica Gal/GalNAc lectin: from lab bench to bedside. Journal of Investigative Medicine 44, 24–36.Google Scholar
Pinheiro, RO, Pinto, EF, Lopes, JR, Guedes, HL, Fentanes, RF and RossiBergmann, B (2005) TGF-beta-associated enhanced susceptibility to leishmaniasis following intramuscular vaccination of mice with Leishmania amazonensis antigens. Microbes and Infection 7, 1317–1323.Google Scholar
Pinheiro, RO, Pinto, EF, de Matos Guedes, HL, Filho, OA, de Mattos, KA, Saraiva, EM, de Mendonça, SC and Rossi-Bergmann, B (2007) Protection against cutaneous leishmaniasis by intranasal vaccination with lipophosphoglycan. Vaccine 25, 2716–2722.Google Scholar
Pöltl, G, Kerner, D, Paschinger, K and Wilson, IB (2007) N-glycans of the porcine nematode parasite Ascaris suum are modified with phosphorylcholine and core fucose residues. The FEBS Journal 274, 714–726.Google Scholar
Poncini, CV, Alba Soto, CD, Batalla, E, Solana, ME and Gonzalez Cappa, SM (2008) Trypanosoma cruzi induces regulatory dendritic cells in vitro. Infection and Immunity 76, 2633–2641.Google Scholar
Prasanphanich, NS, Luyai, AE, Song, X, Heimburg-Molinaro, J, Mandalasi, M, Mickum, M, Smith, DF, Nyame, AK and Cummings, RD (2014) Immunization with recombinantly expressed glycan antigens from Schistosoma mansoni induces glycan-specific antibodies against the parasite. Glycobiology 24, 619–637.Google Scholar
Previato, JO, Gorin, PA, Mazurek, M, Xavier, MT, Fournet, B, Wieruszesk, JM and Mendonça-Previato, L (1990) Primary structure of the oligosaccharide chain of lipopeptidophosphoglycan of epimastigote forms of Trypanosoma cruzi. Journal of Biological Chemistry 265, 2518–2526.Google Scholar
Ralston, KS and Petri, WA (2011) The ways of a killer: how does Entamoeba histolytica elicit host cell death? Essays in Biochemistry 51, 193–210.Google Scholar
Ravidà, A, Aldridge, AM, Driessen, NN, Heus, FA, Hokke, CH and O'Neill, SM (2016) Fasciola hepatica surface coat glycoproteins contain mannosylated and phosphorylated N-glycans and exhibit immune modulatory properties independent of the mannose receptor. PLoS Neglected Tropical Diseases 10, e0004601.Google Scholar
Reason, AJ, Ellis, LA, Appleton, JA, Wisnewski, N, Grieve, RB, McNeil, M, Wassom, DL, Morris, HR and Dell, A (1994) Novel tyvelose-containing tri- and tetra-antennary N-glycans in the immunodominant antigens of the intracellular parasite Trichinella spiralis. Glycobiology 4, 593–603.Google Scholar
Reiner, L and Locksley, RM (1995) The regulation of immunity to Leishmania major. Annual Review of Immunology 13, 151–177.Google Scholar
Restrepo, BI, Obregón-Henao, A, Mesa, M, Gil, DL, Ortiz, BL, Mejía, JS, Villota, GE, Sanzón, F and Teale, JM (2000) Characterisation of the carbohydrate components of Taeniasolium metacestode glycoprotein antigens. International Journal of Parasitology 30, 689–696.Google Scholar
Riganò, R, Buttari, B, Profumo, E, Ortona, E, Delunardo, F, Margutti, P, Mattei, V, Teggi, A, Sorice, M and Siracusano, A (2007) Echinococcus granulosus antigen B impairs human dendritic cell differentiation and polarizes immature dendritic cell maturation towards a Th2 cell response. Infection and Immunity 75, 1667–1678.Google Scholar
Robijn, MLM, Koeleman, CAM, Hokke, CH and Deelder, AM (2007) Schistosoma mansoni eggs excrete specific free oligosaccharides that are detectable in the urine of the human host. Molecular and Biochemical Parasitology 151, 162–172.Google Scholar
Rodríguez, E, Noya, V, Cervi, L, Chiribao, ML, Brossard, N, Chiale, C, Carmona, C, Giacomini, C and Freire, T (2015) Glycans from Fasciola hepatica modulate the host immune response and TLR-induced maturation of dendritic cells. PLoS Neglected Tropical Diseases 9, e0004234.Google Scholar
Roggelin, L, Vinnemeier, CD, Fischer-Herr, J, Johnson-Weaver, BT, Rolling, T, Burchard, GD, Staats, HF and Cramer, JP (2015) Serological response following re-vaccination with Salmonella typhi Vi-capsular polysaccharide vaccines in healthy adult travellers. Vaccine 33, 4141–4145.Google Scholar
Rojas-Bernabe, A, Garcia-Hernandez, O, Maldonado-Bernal, C, DelegadoDominguez, J, Ortega, E, Gutierrez-Kobeh, L, Becker, I and Aguirre-Garcia, M (2014) Leishmania mexicana lipophosphoglycan activates ERK and p38 MAP kinase and induces production of proinflammatory cytokines in human macrophages through TLR2 and TLR4. Parasitology 141, 788–800.Google Scholar
Russell, DG and Alexander, J (1988) Effective immunization against cutaneous leishmaniasis with defined membrane antigens reconstituted into liposomes. The Journal of Immunology 140, 1274–1279.Google Scholar
San Francisco, J, Barría, I, Gutiérrez, B, Neira, I, Muñoz, C, Sagua, H, Araya, JE, Andrade, JC, Zailberger, A, Catalán, A, Remonsellez, F, Vega, JL and González, J (2017) Decreased cruzipain and gp85/trans-sialidase family protein expression contributes to loss of Trypanosoma cruzi trypomastigote virulence. Microbes and Infection 19, 55–61.Google Scholar
Schauer, R, Reuter, G, Muhlpfordt, H, Andrade, AF and Pereira, ME (1983) The occurrence of N-acetyl- and N-glycoloylneuraminic acid in Trypanosoma cruzi. Hoppe-Seyler's Zeitschritf fur Physiologische Chemie 364, 1053–1057.Google Scholar
Schofield, L, McConville, MJ, Hansen, D, Campbell, AS, Fraser-Reid, B, Grusby, MJ and Tachado, SD (1999) CD1d-restricted immunoglobulin G formation to GPI-anchored antigens mediated by NKT cells. Science 283, 225–229.Google Scholar
Schofield, L, Hewitt, MC, Evans, K, Siomos, MA and Seeberger, PH (2002) Synthetic GPI as a candidate anti-toxic vaccine in a model of malaria. Nature 418, 785–789.Google Scholar
Sher, A, Pearce, E and Kaye, P (2003) Shaping the immune response to parasites: role of dendritic cells. Current Opinion in Immunology 15, 421–429.Google Scholar
Smit, CH, van Diepen, A, Nguyen, DL, Wuhrer, M, Hoffmann, KF, Deelder, AM and Hokke, CH (2015) Glycomic analysis of life stages of the human parasite Schistosoma mansoni reveals developmental expression profiles of functional and antigenic glycan motifs. Molecular and Cellular Proteomics 14, 1750–1769.Google Scholar
Spiro, RG (2002) Protein glycosylation: nature, distribution, enzymatic formation and disease implications of glycopeptides bonds. Glycobiology 12, 43R–56R.Google Scholar
Stanley, SL Jr, Tian, K, Koester, JP and Li, E (1995) The serine-rich Entamoeba histolytica protein is a phosphorylated membrane protein containing O-linked terminal N-acetylglucosamine residues. The Journal of Biological Chemistry 270, 4121–4126.Google Scholar
Stormo, SK, Praebel, K and Elvevoll, EO (2009) Cold tolerance in sealworm (Pseudoterranova decipiens) due to heat-shock adaptations. Parasitology 136, 1317–1324.Google Scholar
Stothard, JR, Kabatereine, NB, Tukahebwa, EM, Kazibwe, F, Rollinson, D, Mathieson, W, Webster, JP and Fenwick, A (2006) Use of circulation cathodic antigen (CCA) dipsticks for detection of intestinal and urinary schistosomiasis. Acta Tropica 97, 219–228.Google Scholar
Swearingen, KE, Eng, JK, Shteynberg, D, Vigdorovich, V, Springer, TA, Mendoza, L, Sather, DN, Deutsch, EW, Kappe, SHI and Moritz, RL (2019) A tandem mass spectrometry sequence database search method for identification of O-fucosylated proteins by mass spectrometry. Journal of Proteome Research 18, 652–663.Google Scholar
Talabnin, K, Aoki, K, Saichua, P, Wongkham, S, Kaewkes, S, Boons, GJ, Sripa, B and Tiemeyer, M (2013) Stage-specific expression and antigenicity of glycoprotein glycans isolated from the human liver fluke, Opisthorchis viverrini. International Journal for Parasitology 43, 37–50.Google Scholar
Taratuto, AL and Venturiello, SM (1997) Echinococcosis. Brain Pathology 7, 673–679, PMID: 9034573.Google Scholar
Taylor, CE, Cobb, BA, RittenhouseOlson, K, Paulson, JC and Schreiber, JR (2012) Carbohydrate moieties as vaccine candidates: targeting the sweet spot in the immune response. Vaccine 30, 4409–4413.Google Scholar
Tejle, K, Lindroth, M, Magnusson, K-E and Rasmusson, B (2008) Wild-type Leishmania donovani promastigotes block maturation, increase integrin expression and inhibit detachment of human monocyte-derived dendritic cells – the influence of phosphoglycans. FEMS Microbiology Letters 279, 92–102.Google Scholar
Terrazas, CA, Terrazas, LI and Gómez-García, L (2010) Modulation of dendritic cell responses by parasites: a common strategy to survive. Journal of Biomedicine and Biotechnology 2010, 357106.Google Scholar
Thaysen-Andersen, M and Packer, NH (2014) Advances in LC-MS/MS based glycoproteomics: getting closer to system-wide site-specificmapping of the N- and O-glycoproteome. Biochimica et Biophysica Acta 1844, 1437–1452.Google Scholar
Thomas, PG, Carter, MR, Atochina, O, Da'Dara, AA, Piskorska, D, McGuire, E and Harn, DA (2003) Maturation of dendritic cell 2 phenotype by a helminth glycan uses a toll-like receptor 4-dependent mechanism. Journal of Immunology 171, 5837–5841.Google Scholar
Todeschini, AR, da Silveira, EX, Jones, C, Wait, R, Previato, JO and Mendonça-Previato, L (2001) Structure of O-glycosidically linked oligosaccharides from glycoproteins of Trypanosoma cruzi CL-Brener strain: evidence for the presence of O-linked sialyl-oligosaccharides. Glycobiology 11, 47–55.Google Scholar
Tonui, WK, Mbati, PA, Anjili, CO, Orago, AS, Turco, SJ, Githure, JI and Koech, DK (2001) Transmission blocking vaccine studies in leishmaniasis: II. Effect of immunisation using Leishmania major derived 63 kilodalton glycoprotein, lipophosphoglycan and whole parasite antigens on the course of L. major infection in BALB/c mice. East African Medical Journal 78, 90–92.Google Scholar
Tundup, S, Srivastava, L and Harn, DA (2012) Polarization of host immune responses by helminth-expressed glycans. Annals of the New York Academy of Sciences 1253, E1–13.Google Scholar
Van Dam, GJ, Bergwerff, AA, Thomas-Oates, JE, Rotmans, JP, Kamerling, JP, Vliegenthart, JF and Deelder, AM (1994) The immunologically reactive O-linked polysaccharide chains derived from circulating cathodic antigen isolated from the human blood fluke Schistosoma mansoni have Lewis x as repeating unit. European Journal of Biochemistry 225, 467–482.Google Scholar
van Dam, GJ, Wichers, JH, Ferreira, TMF, Ghati, D, van Amerongen, A and Deelder, AM (2004) Diagnosis of schistosomiasis by reagent strip test for detection of circulating cathodic antigen. Journal of Clinical Microbiology 42, 5458–5461.Google Scholar
van Die, I and Cummings, RD (2006) Glycans modulate immune responses in helminth infections and allergy. Chemical Immunology and Allergy 90, 91–112.Google Scholar
van Die, I and Cummings, RD (2010) Glycan gimmickry by parasitic helminths: a strategy for modulating the host immune response? Glycobiology 20, 2–12.Google Scholar
van Die, I, Gomord, V, Kooyman, FN, van den Berg, TK, Cummings, RD and Vervelde, L (1999) Core alpha1-->3-fucose is a common modification of N-glycans in parasitic helminths and constitutes an important epitope for IgE from Haemonchus contortus infected sheep. FEBS Letters 463, 189–193.3-fucose+is+a+common+modification+of+N-glycans+in+parasitic+helminths+and+constitutes+an+important+epitope+for+IgE+from+Haemonchus+contortus+infected+sheep.+FEBS+Letters+463,+189–193.>Google Scholar
van Liempt, E, van Vliet, SJ, Engering, A, García Vallejo, JJ, Bank, CM, Sanchez-Hernandez, M, van Kooyk, Y and van Die, I (2007) Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation. Molecular Immunology 44, 2605–2615.Google Scholar
van Stijn, CM, van den Broek, M, Vervelde, L, Alvarez, RA, Cummings, RD, Tefsen, B and van Die, I (2010) Vaccination-induced IgG response to Galalpha1–3GalNAc glycan epitopes in lambs protected against Haemonchus contortus challenge infection. International Journal for Parasitology 40, 215–222.Google Scholar
Varki, A (2017) Biological roles of glycans. Glycobiology 27, 3–49.Google Scholar
Veríssimo, CM, Morassutti, AL, von Itzstein, M, Sutov, G, Hartley-Tassell, L, McAtamney, S, Dell, A, Haslam, SM and Graeff-Teixeira, C (2016) Characterization of the N-glycans of female Angiostrongylus cantonensis worms. Experimental Parasitology 166, 137–143.Google Scholar
Vermeer, HJ, van Dam, GJ, Halkes, KM, Kamerling, JP, Vliegenthart, JF, Hokke, CH and Deelder, AM (2003) Immunodiagnostically applicable monoclonal antibodies to the circulating anodic antigen of Schistosoma mansoni bind to small, defined oligosaccharide epitopes. Parasitology Research 90, 330–336.Google Scholar
Vervelde, L, Bakker, N, Kooyman, FN, Cornelissen, AW, Bank, CM, Nyame, AK, Cummings, RD and van Die, I (2003) Vaccination induced protection of lambs against the parasitic nematode Haemonchus contortus correlates with high IgG antibody responses to the LDNF glycan antigen. Glycobiology 13, 795–804.Google Scholar
Vivanco-Cid, H, Alpuche-Aranda, C, Wong-Baeza, I, Rocha-Ramírez, LM, Rios-Sarabia, N, Estrada-Garcia, I, Villasis-Keever, MA, Lopez-Macias, C and Isibasi, A (2007) Lipopopeptidephosphoglycan from Entamoeba histolytica activates human macrophages and dendritic cells and reaches their late endosomes. Parasite Immunology 29, 467–474.Google Scholar
von Stebut, E, Belkaid, Y, Jakob, T, Sacks, DL and Udey, MC (1998) Uptake of Leishmania major amastigotes results in activation and interleukin 12 release from murine skinderived dendritic cells: implications for the initiation of anti-Leishmania immunity. Journal of Experimental Medicine 188, 1547–1552.Google Scholar
Wisnewski, N, McNeil, M, Grieve, RB and Wassom, DL (1993) Characterization of novel fucosyl- and tyvelosyl-containing glycoconjugates from Trichinella spiralis muscle stage larvae. Molecular and Biochemical Parasitology 61, 25–35.Google Scholar
World Health Organization – Leishmaniasis. (2017) Available at http://www.who.int/mediacentre/factsheets/fs375/en/ (Accessed December 2017).Google Scholar
Wuhrer, M, Grimm, C, Dennis, R, Idris, M and Geyer, R (2004) The parasitic trematode Fasciola hepatica exhibits mammalian-type glycolipids as well as Gal(beta1–6)Gal-terminating glycolipids that account for cestode serological cross-reactivity. Glycobiology 14, 115–126.Google Scholar
Wuhrer, M, Koeleman, CAM, Deelder, AM and Hokke, CH (2006) Repeats of LacdiNAc and fucosylated LacdiNAc on N-glycans of the human parasite Schistosoma mansoni. The FEBS Journal 273, 347–361.Google Scholar
Wuhrer, M, Rickhoff, S, Dennis, RD, Lochnit, G, Soboslay, PT, Baumeister, S and Geyer, R (2000) Phosphocholine-containing, zwitterionic glycosphingolipids of adult Onchocerca volvulus as highly conserved antigenic structures of parasitic nematodes. Biochemical Journal 1, 417–423.Google Scholar
Yamano, K, Goto, A, Nakamura-Uchiyama, F, Nawa, Y, Hada, N and Takeda, T (2009) Galbeta1–6Gal, antigenic epitope which accounts for serological cross-reaction in diagnosis of Echinococcus multilocularis infection. Parasite Immunology 31, 481–487.Google Scholar
Yépez-Mulia, L, Hernández-Bello, R, Arizmendi-Puga, N, Fonseca-Liñán, R and Ortega-Pierres, G (2007) Contributions to the study of Trichinella spiralis TSL-1 antigens in host immunity. Parasite Immunology 29, 661–670.Google Scholar