Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-26T09:20:35.299Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasitic helminths: a pharmacopeia of anti-inflammatory molecules

Published online by Cambridge University Press:  15 December 2008

M. J. G. JOHNSTON ,
J. A. MacDONALD  and
D. M. McKAY
M. J. G. JOHNSTON
Affiliation:
Gastrointestinal Research Group, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, Canada, T2N 1N4 Department of Physiology and Biophysics, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, Canada, T2N 1N4
J. A. MacDONALD
Affiliation:
Smooth Muscle Research Group, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, Canada, T2N 1N4 Department of Biochemistry and Molecular Biology, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, Canada, T2N 1N4
D. M. McKAY*
Affiliation:
Gastrointestinal Research Group, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, Canada, T2N 1N4 Department of Physiology and Biophysics, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, Canada, T2N 1N4
*
*Corresponding author: Health Sciences Centre, HSC 1877, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, CanadaT2N 1N4. Tel: +1 403 220 7362. Fax: +1 403 283 3028. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Infection with parasitic helminths takes a heavy toll on the health and well-being of humans and their domestic livestock, concomitantly resulting in major economic losses. Analyses have consistently revealed bioactive molecules in extracts of helminths or in their excretory/secretory products that modulate the immune response of the host. It is our view that parasitic helminths are an untapped source of immunomodulatory substances that, in pure form, could become new drugs (or models for drug design) to treat disease. Here, we illustrate the range of immunomodulatory molecules in selected parasitic trematodes, cestodes and nematodes, their impact on the immune cells in the host and how the host may recognize these molecules. There are many examples of the partial characterization of helminth-derived immunomodulatory molecules, but these have not yet translated into new drugs, reflecting the difficulty of isolating and fully characterizing proteins, glycoproteins and lipid-based molecules from small amounts of parasite material. However, this should not deter the investigator, since analytical techniques are now being used to accrue considerable structural information on parasite-derived molecules, even when only minute quantities of tissue are available. With the introduction of methodologies to purify and structurally-characterize molecules from small amounts of tissue and the application of high throughput immunological assays, one would predict that an assessment of parasitic helminths will yield a variety of novel drug candidates in the coming years.

Keywords

helminthsimmunomodulatorsanti-inflammatory drugsdrug design
Type
Review Article
Information
Parasitology , Volume 136 , Issue 2 , February 2009 , pp. 125 - 147
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abner, S. R., Parthasarathy, G., Hill, D. E. and Mansfield, L. S. (2001). Trichuris suis: detection of antibacterial activity in excretory-secretory products from adults. Experimental Parasitology 99, 26–36.Google Scholar
Al-Riyami, L., Egan, C. A., Bradley, J. E., Lustigman, S. and Harnett, W. (2008). Failure of ES-62 to inhibit T-helper type I responses to other filarial nematode antigens. Parasite Immunology 30, 304–308.Google Scholar
Anbu, K. A. and Joshi, P. (2008). Identification of a 55 kDa Haemonchus contortus excretory/secretory glycoprotein as a neutrophil inhibitory factor. Parasite Immunology 30, 23–30.CrossRefGoogle ScholarPubMed
Ando, M., Tu, W., Nishijima, K. I. and Iijima, S. (2008). Siglec-9 enhances IL-10 production in macrophages via tyrosine based motifs. Biochemical and Biophysical Research Communications 369, 878–883.CrossRefGoogle ScholarPubMed
Andrade, M. A., Siles-Lucas, M., Espinoza, E., Perez Arellano, J. L., Gottstein, B. and Muro, A. (2004). Echinococcus multilocularis laminated-layer components and the E14t 14-3-3 recombinant protein decrease NO production by activated rat macrophages in vitro. Nitric Oxide 10, 150–155.CrossRefGoogle ScholarPubMed
Antonioli, L., Fornai, M., Colucci, R., Ghisu, N., Tuccori, M., Del Tacca, M. and Blandizzi, C. (2008). Pharmacological modulation of adenosine system: novel options for treatment of inflammatory bowel disease. Inflammatory Bowel Disease 14, 566–574.CrossRefGoogle Scholar
Antony, R. M., Rutitzky, L. I., Urban, J. F. Jr., Stadecker, M. J. and Gause, W. C. (2007). Protective immune mechanism in helminth infection. Nature Reviews in Immunology 7, 975–987.Google Scholar
Apinhasmit, W., Sobhon, P., Tarasub, C., Mothong, W., Saitongdee, P., Sretarugsa, P., Wanichanon, C. and Upatham, E. S. (2000). Opisthorchis viverrini: ultrastructure and cytochemistry of the glycocalyx of the tegument. Journal of Helminthology 74, 23–29.CrossRefGoogle ScholarPubMed
Appelmelk, B. J., Van Die, I., Van Vleit, S. J., Vandenbroucke-Grauls, C. M., Geijtenbeek, T. B. and Van Kooyk, Y. (2003). Cutting edge: carbohydrate profiling identifies new pathogens that interact with dendritic cell specific ICAM-3 grabbing nonintegrin on dendritic cells. Journal of Immunology 170, 1635–1639.Google Scholar
Arechavleta, F., Mollinari, J. L. and Tato, P. (1998). A Taenia solium metacestode factor nonspecifically inhibits cytokine production. Parasitology Research 84, 117–122.CrossRefGoogle Scholar
Atochina, O. and Harn, D. (2005). LNFPIII/LeX-stimulated macrophages activate natural killer cells via CD40-CD40L interaction. Clinical and Diagnostic Laboratory Immunology 12, 1041–1049.Google Scholar
Balic, A., Harcus, Y., Holland, M. J. and Maizels, R. M. (2004). Selective maturation of dendritic cells by Nippostrongylus brasilensis-secreted proteins drives TH2 immune responses. European Journal of Immunology 34, 3047–3059.CrossRefGoogle ScholarPubMed
Bateman, K. P., White, R. L. and Thibault, P. (1998). Evaluation of adsorption preconcentration/capillary zone electrophoresis/nanoelectrospray mass spectrometry for peptide and glycoprotein analyses. Journal of Mass Spectrometry 33, 1109–1123.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Baumgart, M., Tomkins, F., Leng, J. and Hess, M. (2006). Naturally occurring CD4+Foxp3+ regulatory T cells are an essential, IL-10-independent part of the immunoregulatory network in Schistosoma mansoni egg-induced inflammation. Journal of Immunology 176, 5374–5387.Google Scholar
Belkaid, Y. and Oldenhove, G. (2008). Tuning microenvironments: induction of regulatory T cells by dendritic cells. Immunity 29, 362–371.CrossRefGoogle ScholarPubMed
Bennett, H. (1963). Morphological aspects of extracellular polysaccharides. Journal of Histochemistry and Cytochemistry 11, 14–23.CrossRefGoogle Scholar
Bickle, Q. and Helmby, H. (2007). Lack of galectin-3 involvement in murine intestinal nematode and schistosome infection. Parasite Immunology 29, 93–100.Google Scholar
Blackburn, C. C. and Selkirk, M. E. (1992). Inactivation of platelet-activating factor by a putative acetylhydrolase from the gastrointestinal nematode parasite, Nippostrongylus brasilensis. Immunology 75, 41–46.Google Scholar
Bogoevska, V., Nallau, P., Lucka, L., Grunow, D., Klampe, B., Uotila, L. M., Samsen, A., Gahmberg, C. G. and Wagener, C. (2007). DC-SIGN binds ICAM-3 isolated from peripheral human leukocytes through Lewis X residues. Glycobiology 17, 324–333.CrossRefGoogle ScholarPubMed
Breuilh, L., Vanhoutte, F., Fontaine, J., van Stijn, C. M. W., Tillie-LeBlond, I., Capron, M., Faveeuw, C., Jouault, T., van Die, I., Gosset, P. and Trottein, F. (2007). Galectin-3 modulates autoimmune and inflammatory responses during helminthic infection: impact of galectin-3 deficiency on the functions of dendritic cells. Infection and Immunity 75, 5148–5157.Google Scholar
Burger, C. J., Rikihisa, Y. and Lin, Y. C. (1986). Taenia taeniformes: inhibition of mitogen induced proliferation and interleukin-2 production in rat splenocytes by larval in vitro product. Experimental Parasitology 62, 216–222.CrossRefGoogle Scholar
Carod-Artal, F. J. (2008). Neurological complications of Schistosoma infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 107–116.CrossRefGoogle ScholarPubMed
Casaravilla, C., Friere, 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-acetlygalactosaminyltransferase activity. Journal of Parasitology 89, 709–715.CrossRefGoogle Scholar
Chen, C. C., Louie, S., McCormick, B., Walker, W. A. and Shi, H. N. (2005). Concurrent infection with an intestinal helminth parasite impairs host resistance to enteric Citrobacter rodentium and enhances Citrobacter-induced colitis is mice. Infection and Immunity 73, 5468–5481.Google Scholar
Chung, Y. B., Kita, H. and Shin, M. H. (2008). A 27 kDa cysteine protease secreted by newly excysted Paragonimus westermani metacercariae induces superoxide anion production and degranulation of human eosinophils. Korean Journal of Parasitology 46, 95–99.CrossRefGoogle ScholarPubMed
Clausen, H. and Bennett, E. (1996). A family of UDP-GalNAc: polypeptide N-acetlygalactosaminyltransferase controls the initiation of mucin type O-linked glycosylation. Glycobiology 6, 635–646.Google Scholar
Collins, B. E., Kiso, M., Hasegawa, A., Tropak, M. B., Roder, J. C., Crocker, P. R. and Schnaar, R. L. (1997). Binding specificities of the sialoadhesion family of I-type lectins. Sialic acid linkage and substructure requirements for binding of myeloid associated glycoprotein, Schwann cell myelin protein and sialoadhesion. Journal of Biological Chemistry 272, 16889–16895.CrossRefGoogle Scholar
Cornish, A. L., Freeman, S., Forbes, G., Ni, J., Zhang, M., Cepeda, M., Gentz, R., Augustus, M., Carter, K. C. and Crocker, P. R. (1998). Characterization of Siglec-5, a novel glycoprotein expressed on myeloid cells related to CD33. Blood 92, 2123–2132.Google Scholar
Corteganao, I., del Pozo, V., Cardaba, B., de Andres, B., Gallardo, S., del Amo, A., Arrieta, I., Jurado, A., Palomino, P., Liu, F. T. and Lahoz, C. (1998). Galectin-3 downregulates IL-5 gene expression on different cell types. Journal of Immunology 161, 385–389.Google Scholar
Couper, K. N., Chen, W., Houston, K. M., Harnett, W. and Johnson, L. L. (2005). ES-62 is unable to modulate Toxoplasma gondii-driven TH1 responses and pathology. Parasite Immunology 27, 147–150.CrossRefGoogle ScholarPubMed
Craig, H., Wastling, J. M. and Knox, D. P. (2006). A preliminary proteomic survey of the in vitro excretory/secretory products of fourth stage larval and adult Teladorsagia circumcincta. Parasitology 132, 535–543.Google Scholar
Culley, F. J., Brown, A., Conroy, D. M., Sabroe, I., Pritchard, D. I. and Williams, T. J. (2000). Eotaxin is specifically cleaved by hookworm metalloproteases preventing its action in vitro and in vivo. Journal of Immunology 165, 6447–6453.CrossRefGoogle ScholarPubMed
Daub, J., Loukas, A., Pritchard, D. I. and Blaxter, M. (2000). A survey of genes expressed in adults of the human hookworm, Necator americanus. Parasitology 120, 171–184.CrossRefGoogle ScholarPubMed
Deehan, M. R., Goodridge, H. S., Blair, D., Lochnit, G., Dennis, R. D., Geyer, R., Harnett, M. M. and Harnett, W. (2002). Immunomodulatory properties of Ascaris suum glycosphingolipids – phosphorylcholine and non-phosphorylcholine-dependent effects. Parasite Immunology 24, 463–469.CrossRefGoogle ScholarPubMed
Deehan, M. R., Harnett, M. M. and Harnett, W. (1997). A filarial nematode secreted product differentially modulates expression and activation of protein kinase C isoforms in B lymphocytes. Journal of Immunology 159, 6105–6111.Google Scholar
Dematteis, S., Pirotto, F., Marques, J., Nieto, A., Orn, A. and Baz, A. (2001). Modulation of the cellular immune response by a carbohydrate rich fraction from Echinococcus granulosus protoscolesces in infected or immunized Balb/c mice. Parasite Immunology 23, 1–9.CrossRefGoogle ScholarPubMed
Demelbauer, U. M., Zehl, M., Plematl, A., Allmaier, G. and Rizzi, A. (2004). Determination of glycopeptide structures by multistage mass spectrometry with low energy collision induced dissociation: comparison of electrospray ionization quadrupole ion trap and matrix assisted laser desorption ionization quadrupole ion trap reflection time of flight approaches. Rapid Communications in Mass Spectrometry 18, 1575–1582.Google Scholar
Diragahayu, P., Fukumoto, S., Tademoto, S., Kina, Y. and Hirai, K. (2004). Excretory/secretory products from plerocercoids of Spirometra erinaceieuropaei suppress interleukin-1β gene expression in murine macrophages. International Journal for Parasitology 34, 577–584.Google Scholar
Dirgahayu, P., Fukumoto, S., Miura, K. and Hirai, K. (2002). Excretory/secretory products from plerocercoids of Spirometra erinaceieuropaei suppress the TNFα gene expression by reducing phosphorylation of ERK1/2 and p38 MAPK in macrophages. International Journal for Parasitology 32, 1155–1162.Google Scholar
Dissanayake, S., Amith, R. S. and Shahin, A. (2004). Taenia crassiceps carbohydrates stimulate IL-6 expression in naive murine macrophages via Toll-like receptors (TLRs). Molecular Immunology 41, 391–398.CrossRefGoogle ScholarPubMed
Dissanayake, S. and Shahin, A. (2007). Induction of interferon-γ by Taenia crassiceps glycans and Lewis sugars in naive Balb/c spleen and peritoneal exudate cells. Molecular Immunology 44, 1623–1630.Google Scholar
Doetze, A., Satoguina, J., Buchard, G., Rau, T., Loliger, C., Flesicher, B. and Horeauf, A. (2000). Antigen specific cellular hyporesponsiveness in a chronic human helminth infection is mediated by Th3/Tr1-type cytokines IL-10 and transforming growth factor β but not by a Th1 to Th2 shift. Infection and Immunity 12, 623–630.Google Scholar
Donnelly, S., O'Neill, S. M., Sekiya, M., Mulcahy, G. and Dalton, J. P. (2005). Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infection and Immunity 73, 166–173.Google Scholar
Duvaux-Miret, O., Stefano, G. B., Smith, E. M., Dissous, C. and Capron, A. (1992). Immunosuppression in the definitive and intermediate hosts of the human parasite Schistosoma mansoni by release of immunoactive neuropeptides. Proceedings of the National Academy of Sciences, USA 89, 778–781.CrossRefGoogle ScholarPubMed
Elayoubi, F. A. and Craig, P. S. (2004). Echinococcus granulosus coproantigens: chromatographic fractionation and characterization. Parasitology 128, 455–465.Google Scholar
El-Gayash, A., Turner, R. J., Brophy, P. M. and Barrett, J. (1999). Effect of Fasciola gigantica somatic extracts and excretory/secretory products on superoxide production by activated neutrophils. Veterinary Parasitology 84, 91–100.Google Scholar
Falcone, F. H. and Pritchard, D. I. (2005). Parasite role reversal: worms on trial. Trends in Parasitology 21, 157–160.Google Scholar
Farah, I. O., Langoi, D., Nyaundi, J. and Hau, J. (2007). Schistosome-induced pathology is exacerbated and TH2 polarization is enhanced during pregnancy. In Vivo 21, 599–602.Google ScholarPubMed
Flynn, R. J. and Mulcahy, G. (2008). Possible role for Toll-like receptors in interaction of Fasciola hepatica excretory-secretory products with bovine macrophages. Infection and Immunity 76, 678–684.CrossRefGoogle ScholarPubMed
Freeman, S. D., Kelm, S., Barber, E. K. and Crocker, P. R. (1995). Characterization of CD33 as a new member of the sialoadhesion family of cellular interaction molecules. Blood 85, 2005–2012.Google Scholar
Frenoy, G. (2005). Methods for the reduction of malignant tumors by an eosinophil/helminth therapy. Free Patents Online http://www.freepatentsonline.com/7335354.htmlGoogle Scholar
Friedl, C. H., Lochnit, G., Zahringer, U., Bahr, U. and Geyer, R. (2003). Structural elucidation of zwitterionic carbohydrates derived from glycosphingolipids of the porcine parasitic nematode Ascaris suum. The Biochemical Journal 369, 89–102.Google Scholar
Fukushima, T., Isobe, A., Hojo, N., Shiwaku, K., Yamane, Y. and Torii, M. (1993). The metabolism of arachidonic acid to prostaglandin E2 in plerocercoids of Spirometa erinacei. Parasitology Research 79, 634–638.Google Scholar
Gamble, H. R., Purcell, J. P. and Fetterer, R. H. (1989). Purification of a 44 kilodalton protease which mediates the ecdysis of infective Haemonchus contortus larvae. Molecular and Biochemical Parasitology 33, 49–58.Google Scholar
Gems, D. and Maizels, R. M. (1996). An abundantly expressed mucin-like protein from Toxocara canis infective larvae: the precursor of the larval surface coat glycoproteins. Proceedings of the National Academy of Sciences, USA 93, 1665–1670.Google Scholar
Giacomin, P. R., Cava, M., Tumes, D. J., Gauld, A. D., Iddawela, D. R., McColl, S. R., Parsons, J. C., Gordon, D. L. and Dent, L. A. (2008). Toxocara canis larval excretory/secretory proteins impair eosinophil dependent resistance of mice to Nippostrongylus brasilensis. Parasite Immunology (epub ahead of print) (in the Press).Google Scholar
Gomez-Escobar, N., Gregory, W. F. and Maizels, R. M. (2000). Identification of tgh-2, a filarial nematode homolog of Caenorhabditis elegans daf-7 and human transforming growth factor β, expressed in microfilarial and adult stages of Brugia malayi. Infection and Immunity 68, 6402–6410.Google Scholar
Gomez-Garcia, L., Lopez-Marin, L. M., Saaverdra, R., Reyes, J. L., Rodriguez-Sosa, M. and Terrazas, L. I. (2005). Intact glycans from cestode antigens are involved in innate activation of myeloid suppressor cells. Parasite Immunology 27, 395–405.CrossRefGoogle ScholarPubMed
Gomez-Garcia, L., Rivera-Montoya, I., Rodriguez-Sosa, M. and Terrazas, L. I. (2006). Carbohydrate components of Taenia crassiceps metacestodes display TH2 adjuvant and anti-inflammatory properties when co-injected with bystander antigen. Parasitology Research 99, 440–448.CrossRefGoogle ScholarPubMed
Goodridge, H. S., Deehan, M. R., Harnett, W. and Harnett, M. M. (2005 a). Subversion of immunological signaling by a filarial nematode phosphorylcholine-containing secreted product. Cellular Signaling 17, 11–16.Google Scholar
Goodridge, H. S., Marshall, F. A., Else, K. J., Houston, K. M., Egan, C., Al-Riyami, L., Liew, F. Y., Harnett, W. and Harnett, M. M. (2005 b). Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine-containing secreted product, ES-62. Journal of Immunology 174, 284–293.Google Scholar
Goodridge, H. S., Marshall, F. A., Wilson, E. H., Houston, K. M., Liew, F. Y., Harnett, M. M. and Harnett, W. (2004). In vivo exposure of murine dendritic cell and macrophage bone marrow progenitors to the phosphorylcholine-containing filarial nematode glycoprotein ES-62 polarizes their differentiation to an anti-inflammatory phenotype. Immunology 113, 491–498.Google Scholar
Goodridge, H. S., Wilson, E. H., Harnett, W., Campbell, C. C., Harnett, M. M. and Liew, F. Y. (2001). Modulation of macrophage cytokine production by ES-62, a secreted product of the filarial nematode Acanthocheilonema vitae. Journal of Immunology 167, 940–945.Google Scholar
Gordon, S. and Taylor, P. R. (2005). Monocyte and macrophage heterogeneity. Nature Reviews in Immunology 5, 953–964.Google Scholar
Gounaris, K. (2002). Nucleotidase cascades are catalysed by secreted proteins of the parasitic nematode Trichinella spiralis. Infection and Immunity 70, 4917–4924.CrossRefGoogle Scholar
Gounaris, K., Selkirk, M. E. and Sadeghi, S. J. (2004). A nucleotidase with unique catalytic properties is secreted by Trichinella spiralis. Molecular and Biochemical Parasitology 136, 257–264.Google Scholar
Greenhalgh, C. J., Beckham, S. A. and Newton, S. E. (1999). Galectins from sheep gastrointestinal nematode parasites are highly conserved. Molecular and Biochemical Parasitology 98, 285–289.Google Scholar
Greenwel, P., Wyler, D. J., Rojkind, M. and Prakash, S. (1993). Fibroblast stimulating factor 1, a novel lymphokine produced in schistosomal egg granulomas, stimulates liver fat storing cells in vitro. Infection and Immunity 61, 3985–3987.Google Scholar
Gruden-Movsesijan, A., Petrovic, M. and Sofronic-Milosavljevic, L. (2003). Interaction of mannan-binding lectin with Trichinella spiralis glycoproteins, a possible innate immune mechanism. Parasite Immunology 25, 545–552.Google Scholar
Guillou, F., Roger, E., Mone, Y., Rognon, A., Grunau, C., Theron, A., Mitta, G., Coustau, C. and Gourbal, B. E. (2007). Excretory-secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Molecular and Biochemical Parasitology 155, 45–56.Google Scholar
Hall, A., Hewitt, G., Tuffrey, V. and de Silva, N. (2008). A review and meta-analysis of the impact of intestinal worms on child growth and nutrition. Maternal and Child Nutrition 4 (Suppl.1), 118–136.CrossRefGoogle ScholarPubMed
Harnett, W., Deehan, M. D., Houston, K. M. and Harnett, M. M. (1999). Immunomodulatory properties of a phosphorylcholine-containing secreted filarial glycoprotein. Parasite Immunology 21, 601–608.Google Scholar
Harnett, W., McInnes, I. B. and Harnett, M. H. (2004). ES-62, a filarial nematode-derived immunomodulator with anti-inflammatory potential. Immunology Letters 94, 27–33.Google Scholar
Harnett, W. and Harnett, M. M. (2008). Therapeutic immunomodulators from nematode parasites. Expert Reviews in Molecular Medicine 10, 1–13.CrossRefGoogle ScholarPubMed
Hartmann, S. and Lucius, R. (2003). Modulation of host immune responses by nematode cystatins. International Journal for Parasitology 33, 1291–1302.CrossRefGoogle ScholarPubMed
Haselmann, K. F., Budnik, B. A., Olsen, J. V., Nielsen, M. L., Reis, C. A., Clausen, H., Johnsen, A. H. and Zubarev, R. A. (2001). Advantages of external accumulation for electron capture dissociation in Fourier transform mass spectrometry. Analytical Chemistry 73, 2998–3005.Google Scholar
Haslam, S. M., Coles, G. C., Morris, H. R. and Dell, A. (2000). Structural characterization of the N-glycans of Dictyocaulus viviparus: discovery of the Lewis X structure in a nematode. Glycobiology 10, 223–229.Google Scholar
Haslam, S. M., Coles, G. C., Munn, E. A., Smith, T. S., Smith, H. F., Morris, H. R. and Dell, A. (1996). Haemonchus contortus glycoproteins contain N-linked oliogsaccharides with novel highly fucosylated core structures. Journal of Biological Chemistry 271, 30561–30570.CrossRefGoogle Scholar
Haslam, S. M., Houston, K. M., Harnett, W., Reason, A. J., Morris, H. R. 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. Journal of Biological Chemistry 274, 20953–20960.Google Scholar
Hayes, K. S., Bancroft, A. J. and Grencis, R. K. (2004). Immune-mediated regulation of chronic intestinal nematode infection. Immunological Reviews 201, 75–88.CrossRefGoogle ScholarPubMed
Hayunga, E. G., Murrell, K. D., Taylor, D. W. and Vannier, W. E. (1979). Isolation and characterization of surface antigens from Schistosoma mansoni. Evaluation of techniques for radioisotope labeling of surface proteins from adult worms. Journal of Parasitology 65, 488–496.Google Scholar
Hernandez, J. D. and Baum, L. G. (2002). Ah sweet mystery of death! Galectins and control of cell fate. Glycobiology 12, 127–136.Google Scholar
Hewitson, J. P., Harcus, Y. M., Curwen, R. S., Dowle, A. A., Atmadja, A. K., Ashton, P. D., Wilson, A. and Maizels, R. M. (2008). The secretome of the filarial parasite, Brugia malayi: proteomic profile of adult excretory-secretory products. Molecular and Biochemical Parasitology 160, 8–21.Google Scholar
Hill, D. E., Gamble, R., Rhoads, M. L., Fetterer, R. H. and Urban, J. F. Jr. (1993). Trichuris suis: a zinc metalloprotease from culture fluids of adult parasites. Experimental Parasitology 77, 170–178.Google Scholar
Holland, M. J., Harcus, Y., Balic, A. and Maizels, R. M. (2005). TH2 induction by Nippostrongylus secreted antigens in mice deficient in B cells, eosinophils or MHC Class I-related receptors. Immunology Letters 96, 93–101.CrossRefGoogle ScholarPubMed
Holland, M. J., Harcus, Y. M., Riches, P. L. and Maizels, R. M. (2000). Proteins secreted by the parasitic nematode Nippostrongylus brasilensis act as adjuvants for TH2 responses. European Journal of Immunology 30, 1977–1987.Google Scholar
Horii, Y., Owhashi, M., Ishii, A., Bandou, K. and Usui, M. (1984). Eosinophil and neutrophil chemotactic activities of adult worm extracts of Schistosoma japonicum in vivo and in vitro. Journal of Parasitology 70, 955–961.Google Scholar
Houston, K. M. and Harnett, W. (2004). Structure and synthesis of nematode phosphorylcholine-containing glycoconjugates. Parasitology 129, 655–661.Google Scholar
Houston, K. M., Sutharsan, R., Steiger, C. N., Scachter, H. and Harnett, W. (2008). Gene inactivation confirms the identity of enzymes involved in nematode phosphorylcholine-N-glycan synthesis. Molecular and Biochemical Parasitology 157, 88–91.Google Scholar
Hseih, G. C. F., Loukas, A., Wahl, A. M., Bhatia, M., Wang, Y., Williamson, A. L., Kehn, K. W., Maruyama, H., Hotez, P. J., Leitenberg, D., Bethony, J. and Constant, S. L. (2004). A secreted protein from the human hookworm Necator americanus binds selectively to NK cells and induces IFNγ production. Journal of Immunology 173, 2699–2704.Google Scholar
Huang, Y., Konse, T., Mechref, Y. and Novotny, M. V. (2002). Matrix assisted desorption ionization mass spectrometry compatible with beta-elimination of O-linked oligosaccharides. Rapid Communications in Mass Spectrometry 16, 1199–1204.CrossRefGoogle ScholarPubMed
Huberty, M. C., Vath, J. E., Yu, W. and Martin, S. A. (1993). Site specific carbohydrate identification in recombinant proteins using MALDI-TOF-MS. Analytical Chemistry 65, 2791–2800.Google Scholar
Humphreys, N. E., Xu, D., Hepworth, M. R., Liew, F. Y. and Grencis, R. K. (2008). IL-33, a potent inducer of adaptive immunity to intestinal nematodes. Journal of Immunology 180, 2443–2449.CrossRefGoogle ScholarPubMed
Hunter, M. M., Wang, A. and McKay, D. M. (2007). Helminth infection enhances disease in a murine TH2 model of colitis. Gastroenterology 132, 1320–1330.Google Scholar
Ikehara, Y., Ikehara, S. K. and Paulson, J. C. (2004). Negative regulation of T cell receptor signaling by Siglec-7 and Siglec-9. Journal of Biological Chemistry 279, 43117–43125.Google Scholar
Irwin, J. A., Morrissey, P. E. W., Ryan, J. P., Walshe, A., O'Neill, S. M., Carrington, S. D., Matthews, E., Fitzpatrick, E., Mulcahy, G., Corfield, A. P. and Dalton, J. P. (2004). Glycosidase activity in the excretory-secretory products of the liver fluke, Fasciola hepatica. Parasitology 129, 465–472.Google Scholar
Itami, D. M., Oshiro, T. M., Araujo, C. A., Perini, A., Martins, M. A., Macedo, M. S. and Macedo-Soares, M. F. (2005). Modulation of murine experimental asthma by Ascaris suum components. Clinical and Experimental Allergy 35, 873–879.Google Scholar
Jackson, S. K., Abate, W., Parton, J., Jones, S. and Harwood, J. L. (2008). Lysophospholipid metabolism facilitates Toll-like receptor 4 membrane translocation to regulate the inflammatory response. Journal of Leukocyte Biology 84, 86–92.Google Scholar
Jefferies, J. R., Turner, R. J. and Barrett, J. (1997). Effect of Fasciola hepatica excretory-secretory products on the metabolic burst of sheep and human neutrophils. International Journal for Parasitology 27, 1025–1029.Google Scholar
Jenkins, S. J., Hewitson, J. P., Ferret-Bernard, S. and Mountford, A. P. (2005). Schistosome larvae stimulate macrophage cytokine production through TLR4-dependent and independent pathways. International Immunology 17, 1409–1418.Google Scholar
Joesph, G. T., Huima, T., Lion, A. and Lustigman, S. (2000). A novel developmentally regulated galectin of Onchocerca volvulus. Molecular and Biochemical Parasitology 106, 187–195.Google Scholar
Joshi, A. D., Raymond, T., Coelho, A. L., Kunkel, S. L. and Hogaboam, C. M. (2008). A systemic granulomatous response to Schistosoma mansoni eggs alters responsiveness of bone marrow derived macrophages to Toll-like receptor agonists. Journal of Leukocyte Biology 83, 314–324.Google Scholar
Judson, D. G., Dixon, J. B. and Skerriit, G. C. (1987). Occurrence and biochemical characteristics of cestode lymphocyte mitogens. Parasitology 94, 151–160.Google Scholar
Junking, M., Wongkham, C., Sripa, B., Sawanyawisuth, K., Araki, N. and Wongkham, S. (2008). Decreased expression of galectin-3 is associated with metastatic potential of liver fluke-associated cholangiocarcinoma. European Journal of Cancer 44, 619–626.Google Scholar
Kang, S., Cummings, R. D. and McCall, J. W. (1993). Characterization of the N-linked oligosaccharides in glycoproteins synthesized by microfilariae of Dirofilaria immitis. Journal of Parasitology 79, 815–828.Google Scholar
Kanse, S. M., Liang, O., Schubert, U., Haas, H., Preissner, K. T., Doenhoff, M. J. and Dennis, R. D. (2005). Characterization and partial purification of Schistosoma mansoni egg-derived pro-angiogenic factor. Molecular and Biochemical Parasitology 144, 76–85.Google Scholar
Kasper, G., Brown, A., Eberl, M., Vallar, L., Kieffer, N., Berry, C., Girdwood, K., Eggleton, P., Quinnell, R. and Pritchard, D. I. (2001). A calreticulin-like molecule from the human hookworm Necator americanus interacts with C1q and the cytoplasmic signaling domain of some integrins. Parasite Immunology 23, 141–152.CrossRefGoogle ScholarPubMed
Kato, Y. and Komatsu, S. (1996). ASABF, a novel cysteine rich antibacterial peptide isolated from the nematode Ascaris suum: purification, primary structure and molecular cloning of cDNA. Journal of Biological Chemistry 271, 30493–30498.Google Scholar
Katz, E., Deehan, M. R., Seatter, S., Lord, C., Sturrock, R. D. and Harnett, M. M. (2001). B cell receptor stimulated mitochondrial phosphorylipase A2 activation and resultant disruption of mitochondrial membrane potential correlate with the induction of apoptosis in WEH 1–231. B cells. Journal of Immunology 166, 137–147.Google Scholar
Kean, D. E., Ohtsuka, I., Sato, K., Hada, N., Takeda, T., Lochnit, G., Geyer, R., Harnett, M. M. and Harnett, W. (2006). Dissecting Ascaris glycosphingolipids for immunomodulatory moieties – the use of synthetic structural glycosphingolipid analogues. Parasite Immunology 28, 69–76.CrossRefGoogle ScholarPubMed
Keir, P. A., Brown, D. M., Clouter-Baker, A., Harcus, Y. M. and Proudfoot, L. (2004). Inhibition of neutrophil recruitment by ES of Nippostrongylus brasilensis. Parasite Immunology 26, 137–139.Google Scholar
Kelm, S., Pelz, A., Schauer, R., Filbin, M. T., Tang, S., DeBellard, M. E., Schnaar, R. I., Mahoney, J. A., Hartnell, A., Bradfield, P. and Crocker, P. R. (1994). Sialoadhesion, MAG and CD22 define a new family of sialic acid dependent adhesion molecules of the immunoglobulin superfamily. Current Biology 4, 965–972.Google Scholar
Khan, W. I. (2008). Physiological changes in the gastrointestinal tract and host protective immunity: learning from the mouse-Trichinella spiralis model. Parasitology 135, 671–682.Google Scholar
Khoo, K. H., Sarda, S., Xu, X., Caulfield, J. P., McNeil, M. R., Homans, S. W., Morris, H. R. and Dell, A. (1995). A unique multifucosylated 3GalNAcβ1,4GlcNAcβ1,3Galα1 motif constitutes the repeating unit of the complex O-glycans derived from the cercarial glycocalyx of Schistosoma mansoni. Journal of Biological Chemistry 270, 17114–17123.Google Scholar
Kim, Y. J., Choi, M. H., Hong, S. T. and Bae, Y. M. (2008). Proliferative effects of excretory-secretory products from Clonorchis sinensis on the human epithelial cell line HEK293 via regulation of the transcription factor E2F1. Parasitology Research 102, 411–417.Google Scholar
Kina, Y., Fukumoto, S., Miura, K., Tademoto, S., Nunomura, K., Diraghayu, P. and Hirai, K. (2005). A glycoprotein from Spirometra erinaceieuropaei plerocercoids suppresses osteoclastogenesis and proinflammatory cytokine gene expression. International Journal for Parasitology 35, 1399–1406.CrossRefGoogle ScholarPubMed
King, C. H. and Dangerfield-Cha, M. (2008). The unacknowledged impoact of chronic schistosomiasis. Chronic Illness 4, 65–79.Google Scholar
Klion, A. D. and Donelson, J. E. (1994). OvGalBP, a filarial antigen with homology to vertebrate galactoside-binding proteins. Molecular and Biochemical Parasitology 65, 305–315.Google Scholar
Ko, A. I., Drager, U. C. and Harn, D. A. (1990). A Schistosoma mansoni epitope recognized by a protective monoclonal antibody is identical to the stage specific embryonic antigen 1 (SSEA-1). Proceedings of the National Academy of Sciences, USA 87, 4159–4163.CrossRefGoogle Scholar
Kooyman, F. N. J., de Vries, E., Ploegar, H. W. and van Putten, J. P. M. (2007). Antibodies elicited by the bovine lungworm, Dictyocaulus viviparus, cross-react with platelet activating factor. Infection and Immunity 75, 4456–4462.Google Scholar
Kottgen, M., Loffler, T., Jacobi, C., Nitchke, R., Pavenstadt, H., Schreiber, R., Frische, S., Nielsen, S. and Leipziger, J. (2003). P2Y6 receptor mediates colonic NaCL secretion via differential activation of cAMP-mediated transport. Journal of Clinical Investigation 111, 371–379.Google Scholar
Kradin, R. L., Badizadegan, K., Auluck, P., Korzenik, J. and Lauwers, G. Y. (2006). Iatrogenic Trichuris suis infection in a patient with Crohn's disease. Archives of Pathology and Laboratory Medicine 130, 718–720.CrossRefGoogle Scholar
Kron, M., Marquard, K., Hartlein, M., Price, S. and Leberman, R. (1995). An immunodominant antigen of Brugia malayi is an asparaginyl-tRNA synthetase. FEBS Letters 374, 122–124.Google Scholar
Kumar, S. and Pritchard, D. I. (1992). The partial characterization of proteases present in the excretory-secretory products and exsheathing fluid of the infective L3 larva of Necator americanus. International Journal for Parasitology 22, 563–572.Google Scholar
Lajaunias, F., Dayer, J. M. and Chizzolini, C. (2005). Constitutive repressor activity of CD33 on human monocytes requires sialic acid recognition and phosphoinositide 3 kinase-mediated intracellular signaling. European Journal of Immunology 35, 243–251.Google Scholar
Lee, J. C., Cho, G. S., Kwon, J. H., Shin, M. H., Lim, J. H. and Kim, W. K. (2006). Macrophageal/microglial cell activation and cerebral injury induced by excretory-secretory products secreted by Paragonimus westermani. Neuroscience Research 54, 133–139.Google Scholar
Leffler, H. and Barondes, S. H. (1986). Specificity of binding of three soluble rat lung lectins to substituted and unsubstituted mammalian beta-galactosides. Journal of Biological Chemistry 261, 10119–10126.Google Scholar
Leid, R., Suquet, C. M. and Perryman, L. E. (1984). Inhibition of antigen and lectin induced proliferation of rat spleen cells by Taenia taeniformes proteinase inhibitor. Clinical and Experimental Immunology 57, 187–194.Google Scholar
Leid, R. W., Suquet, C. M., Bouwer, H. G. A. and Hinrichs, D. J. (1986). Interleukin inhibition by a parasite proteinase inhibitor, taeniaestatin. Journal of Immunology 137, 2700–2702.Google Scholar
Liaudet, L., Mabley, J. G., Pacher, P., Virag, L., Soriano, F. G., Marton, A., Hasko, G., Deitch, E. A. and Szabo, C. (2002). Inosine exerts a broad range of anti-inflammatory effects in a murine model of acute lung injury. Annals in Surgery 235, 568–578.Google Scholar
Lima, C., Perini, A., Garcia, M. L. B., Martins, M. A., Teixeira, M. M. and Macedo, M. S. (2002). Eosinophilic inflammation and airway hyper-responsiveness are profoundly inhibited by a helminth (Ascaris suum) extract in a murine model of asthma. Clinical and Experimental Allergy 32, 1659–1666.Google Scholar
Loeffler, D. A., Lunfy, S. K., Singh, K. P., Gerard, H. C., Hudson, A. P. and Boros, D. L. (2002). Soluble egg antigens from Schistosoma mansoni induce angiogenesis-related processes by up-regulating vascular endothelial growth factor in human endothelia cells. Journal of Infectious Disease 185, 1650–1656.Google Scholar
Loukas, A., Doedens, A., Hintz, M. and Maizels, R. M. (2000 a). Identification of a new C-type lectin, TES-70, secreted by infective larvae of Toxocara canis, which binds to host ligands. Parasitology 121, 545–554.Google Scholar
Loukas, A., Hintz, M., Linder, D., Mullin, N. P., Parkinson, J., Tetteh, K. K. A. and Maizels, R. M. (2000 b). A family of secreted mucins from the parasitic nematode Toxocara canis bears diverse mucin domains but shares similar flanking six cysteine repeat motifs. Journal of Biological Chemistry 275, 39600–39607.CrossRefGoogle ScholarPubMed
Loukas, A., Mullin, N. P., Tetteh, K. K. A., Moens, L. and Maizels, R. M. (1999). A novel C-type lectin secreted by a tissue dwelling parasitic nematode. Current Biology 9, 825–828.Google Scholar
Lundy, S. K., Lerman, S. P. and Boros, D. L. (2001). Soluble egg antigen stimulated T Helper lymphocyte apoptosis and evidence for cell death mediated by FasL+ T and B cells during murine Schistosoma mansoni infection. Infection and Immunity 69, 271–280.Google Scholar
Mabley, J. G., Pacher, P., Liaudet, L., Soriano, F. G., Hasko, G., Marton, A., Szabo, C. and Salzman, A. L. (2003). Inosine reduces inflammation and improves survival in a murine model of colitis. American Journal of Physiology Gastrointestinal and Liver Physiology 284, 138–144.Google Scholar
Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D. and Allen, J. E. (2004). Helminth parasites – masters of regulation. Immunology Reviews 201, 89–116.Google Scholar
Marshall, A. J., Brunet, L. R., van Dessel, Y., Alcarez, A., Bliss, S. K., Pearce, E. J. and Denkers, E. Y. (1999). Toxoplasma gondii and Schistosoma mansoni synergize to promote hepatocyte dysfunction associated with high levels of plasma TNFα and early death in C57BL/6 mice. Journal of Immunology 163, 2089–2097.CrossRefGoogle ScholarPubMed
Marsland, B. J., Camberis, M. and Le Gros, G. (2005). Secretory products from infective forms of Nippostrongylus brasilensis induce a rapid allergic airway inflammatory response. Immunology and Cell Biology 83, 40–47.Google Scholar
McConchie, B. W., Norris, H. H., Bundoc, V. G., Trivedi, S., Boesen, A., Urban, J. F. , J. F. Jr. and Keane-Meyers, A. M. (2006). Ascaris suum-derived products suppress mucosal allergic inflammation in an interleukin 10 independent manner via interference with dendritic cell function. Infection and Immunity 74, 6632–6641.Google Scholar
McDiarmid, S. S. and Podesta, R. B. (1984). Identification of a sialic acid containing glycocalyx on the surface of Schistosoma mansoni. Molecular and Biochemical Parasitology 10, 33–43.Google Scholar
McInnes, I. B., Leung, B. P., Harnett, M., Gracie, J. A., Liew, F. Y. and Harnett, W. (2003). A novel therapeutic approach targeting articular inflammation using the filarial nematode-derived phosphorylcholine-containing glycoprotein ES-62. Journal of Immunology 171, 2127–2133.Google Scholar
McKay, D. M. (2006). The beneficial helminth parasite? Parasitology 132, 1–12.Google Scholar
McKerrow, J. H., Brindley, P., Brown, M., Gam, A. A., Staunton, C. and Neva, F. A. (1990). Strongyloides stercoralis: identification of a protease that facilitates penetration of skin by the infective larvae. Experimental Parasitology 70, 134–143.Google Scholar
Melendez, A. J., Harnett, M. M., Pushparaj, P. N., Wong, W. S., Tay, H. K., McSharry, C. P. and Harnett, W. (2007). Inhibition of Fc epsilon RI-mediated mast cell responses by ES-62, a product of parasitic filarial nematodes. Nature Medicine 13, 1375–1381.Google Scholar
Meyer, S., van Liempt, E., Imberty, A., van Kooyk, Y., Geyer, H., Geyer, R. and van Die, I. (2005). DC-SIGN mediates binding of dendritic cells to authentic pseudo-LewisY glycolipids of Schistosoma mansoni cercariae, the first parasite specific ligand of DC-SIGN. Journal of Biological Chemistry 280, 37349–37359.Google Scholar
Mikes, L. and Horak, P. (2001). A protein with lectin activity in the penetration glands of Diplostomum pseudopathaceum cercariae, International. Journal for Parasitology 31, 245–252.Google Scholar
Milos, N. and Zalik, S. E. (1983). Calcium-independent adhesion of extra-embryonic endoderm cells from the early chick blastoderm is inhibited by the blastoderm beta-D-galactoside-binding lectin and by beta-galactosidase. Cell Differentiation 12, 341–347.Google Scholar
Morelle, W. and Michaelski, J. C. (2004). The mass spectrometric analysis of glycoproteins and their glycan structures. Current Analytical Chemistry 1, 29–57.Google Scholar
Morris, H. R., Paxton, T., Panico, M., McDowell, R. and Dell, A. (1997). A novel geometry mass spectrometer, the Q-TOF, for low femtomole/attomole range biopolymer sequencing. Journal of Protein Chemistry 16, 469–479.Google Scholar
Moyle, M., Foster, D. L., McGrath, D. E., Brown, S. M., Laroche, Y., De Meutter, J., Stanssens, P., Bogowitz, C. A., Fried, V. A., Ely, J. A., Soule, H. R. and Vlasuk, G. P. (1994). A hookworm glycoprotein that inhibits neutrophil function is a ligand of the integrin CD11b/CD18. Journal of Biological Chemistry 269, 10008–10015.Google Scholar
Nagy, K., Vekey, K., Imre, T., Ludanyi, K., Barrow, M. P. and Derrick, P. J. (2004). Electrospray ionization fourier transform ion cyclotron resonance mass spectrometry of human alpha-1-acid glycoprotein. Analytical Chemistry 76, 4998–5005.Google Scholar
Nutku, E., Aizawa, H., Hudson, S. A. and Bochner, B. S. (2003). Ligation of Siglec-8: selective mechanism for induction of human eosinophil apoptosis. Blood 101, 5014–5020.Google Scholar
Nyame, K., Cummings, R. D. and Damian, R. T. (1986). Characterization of the O-linked oligosaccharides in glycoproteins synthesized by Schistosoma mansoni schistosomula. Journal of Parasitology 74, 562–572.Google Scholar
Nyame, K., Smith, D. F., Damian, R. T. and Cummings, R. D. (1989). Complex type asparagine-linked oligosaccharides in glycoproteins synthesized by Schistosoma mansoni adult males contain terminal β-linked N-acetylgalactosamine. Journal of Biological Chemistry 264, 3235–3243.Google Scholar
Oberhelman, R. A., Guerrero, E. S., Fernandez, M. L., Silio, M., Mercado, D., Comiskey, N., Ihenacho, G. and Mera, R. (1998). Correlations between intestinal parasitosis, physical growth and psychomotor development in infants and children from rural Nicaragua. American Journal of Tropical Medicine 58, 470–475.Google Scholar
O'Neill, S. M., Mills, K. H. and Dalton, J. P. (2001). Fasciola hepatica cathepsin L cysteine proteinase suppresses Bordetella pertussis-specific interferon gamma production in vivo. Parasite Immunology 23, 541–547.Google Scholar
Okano, M., Satoskar, A. R., Nishizaki, K., Abe, M. and Harn, D. A. (1999). Induction of TH2 responses and IgE is largely due to carbohydrates functioning as adjuvants on Schistosoma mansoni egg antigens. Journal of Immunology 163, 6712–6717.Google Scholar
Osborne, J. and Devaney, E. (1999). Interleukin-10 and antigen presenting cells actively suppress Th1 cells in BALB/c mice infected with the filarial parasite Brugia pahangi. Infection and Immunity 67, 1509–1605.Google Scholar
Owhashi, M. and Ishii, A. (1982). Purification and characterization of a high molecular weight eosinophil chemotactic factor from Schistosoma japonicum eggs. Journal of Immunology 129, 2226–2231.Google Scholar
Pastrana, D. V., Raghavan, N., Fitzgerald, P., Eisinger, S. W., Metz, C., Bucala, R., Schleimer, R. P., Bickel, C. and Scott, A. L. (1998). Filarial nematode parasites secrete a homologue of the human cytokine macrophage migration inhibitory factor. Infection and Immunity 66, 5955–5963.CrossRefGoogle ScholarPubMed
Perrigoue, J. G., Marshall, F. and Artis, D. (2008). On the hunt for helminths: innate immune cells in the recognition and response to helminth parasites. Cellular Microbiology 10, 1757–1764.CrossRefGoogle Scholar
Persat, F., Vincent, C., Schmitt, D. and Mojon, M. (1996). Inhibition of human peripheral blood mononuclear cell proliferative response by glycosphingolipids from metacestodes of Echinococcus multilocularis. Infection and Immunity 64, 3682–3687.Google Scholar
Persuad, R., Wang, A., Reardon, C. and McKay, D. M. (2007). Characterisation of the immuno-regulatory response to rat the tapeworm Hymenolepis diminuta in the non-permissive mouse host. International Journal for Parasitology 37, 393–403.CrossRefGoogle Scholar
Pillai, A., Ueno, S., Zhang, H., Lee, J. M. and Kato, Y. (2005). Cecropin P1 and novel cecropins: a bacteria-inducible antimicrobial peptide family in the nematode Ascaris suum. The Biochemical Journal 390, 207–214.Google Scholar
Plows, L. D., Cook, R. T., Davies, A. J. and Walker, A. J. (2005). Carbohydrates that mimic schistosome surface coat components affect ERK and PKC signaling in Lymnaea stagnalis haemocytes. International Journal for Parasitology 35, 293–302.Google Scholar
Powell, L. D. and Varki, A. (1994). The oligosaccharide binding specificities of CD22-β, a sialic acid specific lectin of B cells. Journal of Biological Chemistry 269, 10628–10636.Google Scholar
Pyz, E., Marshall, A. S. J., Gordon, S. and Brown, G. D. (2006). C-type lectin-like receptors on myleoid cells. Annals of Medicine 38, 242–251.Google Scholar
Rabinovich, G. A., Liu, F. T., Hirashima, M. and Anderson, A. (2007). An emerging role for galectins in tuning the immune response: lessons from experimental models of inflammatory disease, autoimmunity and cancer. Scandinavian Journal of Immunology 66, 143–158.Google Scholar
Rabinovich, G. A., Baum, L. G., Tinari, N., Paganelli, R., Natoli, C., Liu, F. T. and Iacobelli, S. (2002). Galectins and their ligands: amplifiers, silencers or tuners of the inflammatory response? Trends in Immunology 23, 313–320.Google Scholar
Rakha, N. K., Dixon, J. B., Carter, S. D., Craig, P. S., Jenkins, P. and Folkard, S. (1991). Echinococcus multilocularis antigens modify accessory cell function of macrophages. Immunology 74, 652–656.Google Scholar
Ramajo-Hernandez, A., Olega, A., Ramajo-Martin, V. and Perez-Sanchez, R. (2007). Carbohydrate profiling and protein identification of tegumental and excreted/secreted glycoproteins of adult Schistosoma bovis worms. Veterinary Parasitology 144, 45–60.Google Scholar
Ramirez, B. L., Zack Howard, O. M., Fang Don, H., Edamatsu, T., Hartlein, M. and Kron, M. (2006). Brugia malayi asparaginyl-transfer RNA synthetase induces chemotaxis of human leukocytes and activates G-protein-coupled receptors CXCR1 and CXCR2. Journal of Infectious Diseases 193, 1164–1171.Google Scholar
Rathore, D. K., Suchitra, S., Suini, M., Singh, B. P. and Joshi, P. (2006). Identification of a 66 kDa Haemonchus contortus excretory/secretory antigen inhibiting host monocytes. Veterinary Parasitology 138, 291–300.Google Scholar
Reese, T. A., Liang, H. E., Tager, A. M., Luster, A. D., van Rooijen, N., Voehringer, D. and Locksley, R. M. (2007). Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature Letters 447, 92–97.Google Scholar
Reyes, J. L. and Terrazas, L. I. (2007). The divergent roles of alternatively activated macrophages in helminthic infections. Parasite Immunology 29, 609–619.Google Scholar
Rigano, R., Profumo, E., Brushi, F., Carulli, G., Azzara, A., Ioppolo, S., Buttari, B., Ortona, E., Margutti, P., Teggi, A. and Siracusano, A. (2001). Modulation of human immune response by Echinococcus granulosus antigen B and its possible role in evading host defences. Infection and Immunity 69, 288–296.Google Scholar
Rigano, 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
Rikihisa, Y., Lin, Y. C. and Fukaya, T. (1985). Taenia taeniformes: inhibition of rat testosterone production by excretory-secretory product of the cultured metacestode. Experimental Parasitology 59, 390–397.Google Scholar
Rocha, F. A. C., Leite, A. K. R. M., Pompeu, M. M. L., Cunha, T. M., Verri, W. A. Jr., Soares, F. M., Castro, R. R. and Cunha, F. Q. (2008). Protective effect of an extract from Ascaris suum in experimental arthritis models. Infection and Immunity 76, 2736–2745.Google Scholar
Salatino, M., Croci, D. O., Bianco, G. A., Illarregui, G. M., Toscano, M. A. and Rabinovich, G. A. (2008). Galectin-1 as a potential therapeutic target in autoimmune disorders and cancer. Expert Opinion on Biological Therapy 8, 45–57.Google Scholar
Schallig, H. D. F. G. and van Leeuwen, M. A. W. (1996). Carbohydrate epitopes on Haemonchus contortus antigens. Parasitology Research 82, 38–42.Google Scholar
Schnoeller, C., Rausch, S., Pillai, S., Avagyan, A., Wittig, B. M., Loddenkemper, C., Hamann, A., Hamelmann, E., Lucius, R. and Hartmann, S. (2008). A helminth immunomodulator reduces allergic and inflammatory responses by induction of IL-10-producing macrophages. Journal of Immunology 180, 4265–4272.Google Scholar
Schonemeyer, A., Lucius, R., Sonnenburg, B., Brattig, N., Sabat, R., Schilling, K., Bradley, J. and Hartmann, S. (2001). Modulation of human T cell responses and macrophage functions by onchocystatin, a secreted protein of the filarial nematode Onchocerca volvulus. Journal of Immunology 167, 3207–3215.Google Scholar
Scuitto, E., Fragoso, G., Baca, M., de la Cruz, V., Lemus, L. and Lamoyi, E. (1995). Depressed T-cell proliferation associated with susceptibility to experimental Taenia crassiceps infection. Infection and Immunity 63, 2277–2281.Google Scholar
Segura, M., Su, Z., Piccirillo, C. and Stevenson, M. M. (2007). Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematode-induced immunosuppression. European Journal of Immunology 37, 1887–1904.Google Scholar
Serradell, M. C., Guasconi, L., Cervi, L., Chiapello, L. S. and Masih, D. T. (2007). Excretory-secretory products from Fasciola hepatica induce eosinophil apoptosis by a caspase-dependent mechanism. Veterinary Immunology and Immunopathology 117, 197–208.Google Scholar
Shepherd, J. C., Aitken, A. and McManus, D. P. (1991). A protein secreted in vivo by Echinococcus granulosus inhibits elastase activity and neutrophil chemotaxis. Molecular and Biochemical Parasitology 44, 81–90.Google Scholar
Smith, A. M., Dowd, A. J., Heffernan, M., Robertson, C. D. and Dalton, J. P. (1993). Fasciola hepatica: a secreted cathepsin L-like proteinase cleaves host immunoglobulin. International Journal for Parasitology 23, 977–983.Google Scholar
Souza, V. M. O., Faquin-Mauro, E. L. and Macedo, M. S. (2002). Extracts of Ascaris suum egg and adult worm share similar immunosuppressive properties. Brazilian Journal of Medical and Biological Research 35, 81–89.Google Scholar
Spolski, R. J., Corson, J., Thomas, P. G. and Kuhn, R. E. (2000). Parasite secreted products regulate the host response to larval Taenia crassiceps. Parasite Immunology 22, 297–305.Google Scholar
Spolski, R. J., Thomas, P. G., See, E. J., Mooney, K. A. and Kuhn, R. E. (2002). Larval Taenia crassiceps secretes a protein with characteristics of murine interferon-γ. Parasitology Research 88, 431–438.Google Scholar
Srivatsan, J., Smith, D. F. and Cummings, R. D. (1992). The human blood fluke Schistsoma mansoni synthesizes glycoproteins containing the LewisX antigen. Journal of Biological Chemistry 267, 20196–20203.Google Scholar
Stein, M., Keshav, S., Harris, N. and Gordon, S. (1992). Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. Journal of Experimental Medicine 176, 287–292.Google Scholar
Stepek, G., Auchie, M., Tate, R., Watson, K., Russell, D. G., Devaney, E. and Harnett, W. (2002). Expression of the filarial nematode phosphorylcholine-containing glycoprotein, ES-62, is stage specific. Parasitology Today 125, 155–164.Google Scholar
Stepek, G., Houston, K. M., Goodridge, H. S., Devaney, E. and Harnett, W. (2004). Stage specific and species specific differences in the production of the mRNA and protein for the filarial nematode secreted product ES-62. Parasitology Today 128, 91–98.Google Scholar
Suchitra, S. and Joshi, P. (2005). Characterization of Haemonchus contortus calreticulin suggests its role in feeding and immune evasion by the parasite. Biochimica et Biophysica Acta 1722, 293–303.Google Scholar
Suchitra, S., Anbu, K. A., Rathore, D. K., Mahawar, M., Singh, B. P. and Joshi, P. (2008). Haemonchus contortus calreticulin binds to C-reactive protein of its host, a novel survival strategy of the parasite. Parasite Immunology 30, 371–374.Google Scholar
Summers, R. W., Elliott, D. E., Qadir, K., Urban, J. F. Jr., Thompson, R. and Weinstock, J. V. (2003). Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. American Journal of Gastroenterology 98, 2034–2041.Google Scholar
Summers, R. W., Elliott, D. E., Urban, J. F. Jr., Thompson, R. A. and Weinstock, J. V. (2005). Trichuris suis therapy for active ulcerative colitis: a randomized control trial. Gastroenterology 128, 825–832.Google Scholar
Suquet, C. M., Green-Edwards, C. and Leid, R. W. (1984). Isolation and partial characterization of a Taenia taeniformes metacestode proteinase inhibitor. International Journal for Parasitology 14, 165–172.Google Scholar
Suttiprapa, S., Loukas, A., Laha, T., Wongkham, S., Kaewkes, S., Gaze, S., Brindley, P. J. and Sripa, B. (2008). Characterization of the anti-oxidant enzyme, thioredoxin peroxidase, from the carcinogenic human liver fluke, Opisthorchis viverrini. Molecular and Biochemical Parasitology 160, 116–122.CrossRefGoogle ScholarPubMed
Tanaka, J. and Torisu, M. (1978). Anisakis and eosinophil. Detection of a soluble factor selectively chemotactic for eosinophils in the extract from Anisakis larvae. Journal of Immunology 120, 745–749.Google Scholar
Tanaka, J., Baba, T. and Torisu, M. (1979). Ascaris and eosinophil. Isolation and characterization of eosinophil chemotactic factor and neutrophil chemotactic factor of parasite in Ascaris antigen. Journal of Immunology 122, 302–308.Google Scholar
Taylor, K. and Hoole, D. (1997). Interactions between rat C-reactive protein and adult Hymenolepis diminuta. Parasitology 115, 297–302.Google Scholar
Taylor, J. J., Mohrs, M. and Pearce, E. J. (2006). Regulatory T cells responses develop in parallel to Th responses and control the magnitude and phenotype of the Th effector population. Journal of Immunology 176, 5839–5847.Google Scholar
Terrazas, L. I., Walsh, K. L., Piskorska, D., McGuire, E. and Harn, D. A. (2001). The schistosome oligosaccharide lacto-N-neotetrose expands Gr1+ cells that secrete anti-inflammatory cytokines and inhibit proliferation of naive CD4+ cells: a potential mechanism for immune polarization in helminth infections. Journal of Immunology 167, 5294–5303.Google Scholar
Thomas, P. G., Carter, M. R., Atochina, O., Da'Dara, A. A., Piskorska, D., McGuire, E. and Harn, D. A. (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
Thomas, P. G., Carter, M. R., Da'Dara, A. A., DeSimone, T. M. and Harn, D. A. (2005). A helminth glycan induces APC maturation via alternative NFκB activation independent of IκBα degradation. Journal of Immunology 175, 2082–2090.Google Scholar
Trujillo-Vargas, C. M., Werner-Klein, M., Wohlleben, G., Polte, T., Hansen, G., Ehlers, S. and Erb, K. J. (2007). Helminth-derived products inhibit the development of allergic responses in mice. American Journal of Respiratory and Critical Care Medicine 175, 336–344.CrossRefGoogle ScholarPubMed
Truong, M. J., Gruart, V., Liu, F. T., Prin, L., Capron, A. and Capron, M. (1993). IgE-binding molecules (Mac-2εBP) expressed by human eosinophils: implication in IgE-dependent eosinophil cytotoxicity. European Journal of Immunology 23, 3230–3235.Google Scholar
Turner, D. G., Wildblood, L. A., Inglis, N. F. and Jones, D. G. (2008). Characterization of galectin like activity from the parasitic nematode, Haemonchus contortus, which modulates ovine eosinophil migration in vitro. Veterinary Immunology and Immunopathology 122, 138–145.Google Scholar
van de Vijver, K. K., Deelder, A. M., Jacobs, W., van Marck, E. A. and Hokke, C. H. (2006). LacdiNAc- and LacNAc-containing glycans induce granulomas in an in vivo model for schistosome egg-induced hepatic granuloma formation. Glycobiology 16, 237–243.Google Scholar
van den Berg, T. K., Honing, H., Franke, N., van Remoortere, A., Shiphorst, W. E. C. M., Liu, F. T., Deedler, A. M., Cummings, R. D., Hokke, C. H. and van Die, I. (2004). LacdiNAc-glycans constitute a parasite pattern for galectin-3 mediated immune recognition. Journal of Immunology 173, 1902–1907.Google Scholar
van der Kleij, D., Latz, E., Brouwers, J. F. H. M., Kruize, Y. C. M., Schmitz, M., Kurt-Jones, E. A., Espevik, T., de Jong, E. C., Kaspenberg, M. L., Golenbock, D. T., Tielens, A. G. M. and Yazdanbakhsh, M. (2002). A novel host-parasite lipid cross talk: Schistosomal lyso-phosphatidylserine activates Toll-like receptor 2 and affects immune polarization. Journal of Biological Chemistry 277, 48122–48129.Google Scholar
van Liempt, E., van Vliet, S. J., Engering, A., Vallejo, J. J. G., Bank, C. M. C., 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 Vliet, S. J., van Liempt, E., Saeland, E., Aarnoudse, C. A., Applemelk, B., Irimura, T., Geijtenbeek, T. B. H., Blixt, O., Alvarez, R., van Die, I. and van Kooyk, Y. (2005). Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor antigens by dendritic cells. International Immunology 17, 661–669.Google Scholar
Velupillai, P. and Harn, D. A. (1994). Oligosaccharide specific induction of interleukin 10 production by B220+ cells from schistosome infected mice: a mechanism for regulation of CD4+ T cell subsets. Proceedings of the National Academy of Sciences, USA 91, 18–22.Google Scholar
Velupillai, P., dos Reis, E. A., dos Reis, M. G. and Harn, D. A. (2000). Lewis X containing oligosaccharide attenuates schistosome egg antigen induced immune depression in human schistosomiasis. Human Immunology 61, 225–232.Google Scholar
von Gunten, S., Yousefi, S., Seitz, M., Jakob, S. M., Schaffner, T., Seger, R., Takala, J., Villiger, P. M. and Simon, H. U. (2005). Siglec-9 transduces apoptosis and nonapoptotic death signals into neutrophils depending on the proinflammatory cytokine environment. Blood 106, 1423–1431.Google Scholar
Wang, A. and McKay, D. M. (2005). Immune modulation by a high molecular weight fraction from the rat tapeworm, Hymenolepis diminuta. Parasitology 130, 575–585.Google Scholar
Wardlaw, A. C., Forsyth, L. M. G. and Crompton, D. W. T. (1994). Bactericidal activity in the pig roundworm Ascaris suum. Journal of Applied Bacteriology 76, 36–41.Google Scholar
Weinstock, J. V., Summers, R. W. and Elliott, D. E. (2005). Role of helminths in regulating mucosal inflammation. Springer Seminar on Immunology 27, 249–271.Google Scholar
Whelan, M., Harnett, M. M., Houston, K. M., Patel, V., Harnett, W. and Rigley, K. P. (2000). A filarial nematode secreted product signals dendritic cells to acquire a phenotype that drives the development of TH2 cells. Journal of Immunology 164, 6453–6460.Google Scholar
Wilson, E. H., Deehan, M. R., Katz, E., Brown, K. S., Houston, K. M., O'Grady, J., Harnett, M. M. and Harnett, W. (2003). Hyporesponsiveness of murine B lymphocytes exposed to the filarial nematode secreted product ES-62 in vivo. Immunology 109, 238–245.Google Scholar
Wisnewski, N., McNeil, M., Greive, R. B. and Wassom, D. L. (1993). Characterization of novel fucosylated and tyvelosyl-containing glycoconjugates from Trichinella spiralis muscle stage larvae. Molecular and Biochemical Parasitology 61, 25–35.Google Scholar
Wu, Z., Boonmars, T., Nagano, I., Nakada, T. and Takahashi, Y. (2003). Molecular expression and characterization of a homologue of host cytokine macrophage migration inhibitory factor from Trichinella spp. Journal of Parasitology 89, 507–515.Google Scholar
Wuhrer, M., Balog, C. I. A., Catalina, M. I., Jones, F. M., Schramm, G., Haas, H., Doenhoff, M. J., Dunne, D. W., Deelder, A. M. and Hokke, C. H. (2006). IPSE/alpha-1, a major secretory glycoprotein antigen from schistosome eggs, expresses the Lewis X motif on core difucosylated N-glycans. FEBS Letters 273, 2276–2293.Google Scholar
Wuhrer, M., Kantelhardt, S. R., Dennis, R. D., Doenhoff, M. J., Lochnit, G. and Geyer, R. (2002). Characterization of glycosphingolipids from Schistosoma mansoni eggs carrying Fuc(α1-3)GalNac, GalNAc(β1–4)[Fuc(α1–3)]GlcNAc and Gal(β1–4)[Fuc(α1–3)]GlcNAc (Lewis X) terminal structures. European Journal of Biochemistry 269, 481–493.Google Scholar
Wuhrer, M., Grimm, C., Dennis, R. D., Idris, M. A. and Geyer, R. (2004). The parasitic trematode Fasciola hepatica exhibits mammalian type glycolipids as well as Gal (β1,6)Gal-terminating glycolipids that account for cestode serological cross reactivity. Glycobiology 14, 115–126.Google Scholar
Yang, R. Y., Hsu, D. K. and Liu, F. T. (1996). Expression of galectin-3 modulates T cell growth and apoptosis. Proceedings of the National Academy of Sciences, USA 93, 6737–6742.Google Scholar
Zang, X., Yazdanbakhsh, M., Jiang, H., Kanost, M. R. and Maizels, R. M. (1999). A novel serpin expressed by blood borne microfilariae of the parasitic nematode Brugia malayi inhibits human neutrophil serine proteases. Blood 94, 1418–1428.Google Scholar
Zhang, J. Q., Nicoll, G., Jones, C. and Crocker, P. R. (2000). Siglec-9, a novel sialic acid binding member of the immunoglobulin superfamily expressed broadly on human blood leukocytes. Journal of Biological Chemistry 275, 22121–22126.Google Scholar