Skip to main content

Exploring the immunology of parasitism – from surface antigens to the hygiene hypothesis

  • R. M. MAIZELS (a1)

Helminth immunology is a field which has changed beyond recognition in the past 30 years, transformed not only by new technologies from cDNA cloning to flow cytometry, but also conceptually as our definition of host immune pathways has matured. The molecular revolution defined key nematode surface and secreted antigens, and identified candidate immunomodulators that are likely to underpin parasites' success in eluding immune attack. The immunological advances in defining cytokine networks, lymphocyte subsets and innate cell recognition have also made a huge impact on our understanding of helminth infections. Most recently, the ideas of regulatory immune cells, in particular the regulatory T cell, have again overturned older thinking, but also may explain immune hyporesponsiveness observed in chronic helminth diseases, as well as the link to reduced allergic reactions observed in human and animal infections. The review concludes with a forward look to where we may make future advances towards the final eradication of helminth diseases.

Corresponding author
*Tel: +44 131 650 5511. Fax: +44 131 650 5450. E-mail:
Hide All
Allen, J. E., Lawrence, R. A. and Maizels, R. M. (1996). Antigen presenting cells from mice harboring the filarial nematode, Brugia malayi, prevent cellular proliferaton but not cytokine production. International Immunology 8, 143151.
Allen, J. E. and Maizels, R. M. (1997). Th1–Th2: reliable paradigm or dangerous dogma? Immunology Today 18, 387392.
Amer, H., Hofinger, A. and Kosma, P. (2003). Synthesis of neoglycoproteins containing O-methylated trisaccharides related to excretory/secretory antigens of Toxocara larvae. Carbohydrate Research 338, 3545.
Anthony, R. M., Urban, J. F. Jr., Alem, F., Hamed, H. A., Rozo, C. T., Boucher, J. L., Van Rooijen, N. and Gause, W. C. (2006). Memory TH2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nature Medicine 12, 955960.
Badley, J. E., Grieve, R. B., Bowman, D. D. and Glickman, L. T. (1987 a). Immune-mediated adherence of eosinophils to Toxocara canis infective larvae: the role of excretory-secretory antigens. Parasite Immunology 9, 133143.
Badley, J. E., Grieve, R. B., Bowman, D. D., Glickman, L. T. and Rockey, J. H. (1987 b). Analysis of Toxocara canis larval excretory-secretory antigens: physicochemical characterization and antibody recognition. Journal of Parasitology 73, 593600.
Balic, A., Harcus, Y., Holland, M. J. and Maizels, R. M. (2004). Selective maturation of dendritic cells by Nippostrongylus brasiliensis secreted proteins drives T helper type 2 immune responses. European Journal of Immunology 34, 30473059.
Blackburn, C. C. and Selkirk, M. E. (1992). Characterisation of the secretory acetylcholinesterases from adult Nippostrongylus brasiliensis. Molecular and Biochemical Parasitology 53, 7988.
Blaxter, M. L. (1993). Cuticle surface proteins of wild type and mutant Caenorhabditis elegans. Journal of Biological Chemistry 268, 66006609.
Blaxter, M. L., Page, A. P., Rudin, W. and Maizels, R. M. (1992). Nematode surface coats: actively evading immunity. Parasitology Today 8, 243247.
Blaxter, M. L., Raghavan, N., Ghosh, I., Guiliano, D., Lu, W., Williams, S. A., Slatko, B. and Scott, A. L. (1996). Genes expressed in Brugia malayi infective third stage larvae. Molecular and Biochemical Parasitology 77, 7793.
Blumenthal, T. and Thomas, J. (1988). Cis and trans mRNA splicing in C. elegans. Trends in Genetics 4, 305308.
Bradley, J. E., Helm, R., Lahaise, M. and Maizels, R. M. (1991). cDNA clones of Onchocerca volvulus low molecular weight antigens provide immunologically specific diagnostic probes. Molecular and Biochemical Parasitology 46, 219228.
Bulgheresi, S., Schabussova, I., Chen, T., Mullin, N. P., Maizels, R. M. and Ott, J. A. (2006). A new C-type lectin similar to the human immunoreceptor DC-SIGN mediates symbiont acquisition by a marine nematode. Applied and Environmental Microbiology 72, 29502956.
Callister, D. M., Winter, A. D., Page, A. P. and Maizels, R. M. (2008). Four abundant novel transcript genes from Toxocara canis with unrelated coding sequences share untranslated region tracts implicated in the control of gene expression. Molecular and Biochemical Parasitology 162, 6070.
Cervi, L., MacDonald, A. S., Kane, C., Dzierszinski, F. and Pearce, E. J. (2004). Dendritic cells copulsed with microbial and helminth antigens undergo modified maturation, segregate the antigens to distinct intracellular compartments, and concurrently induce microbe-specific Th1 and helminth-specific Th2 responses. Journal of Immunology 172, 20162020.
Cookson, E., Blaxter, M. L. and Selkirk, M. E. (1992). Identification of the major soluble cuticular protein of lymphatic filarial nematode parasites (gp29) as a secretory homolog of glutathione peroxidase. Proceedings of the National Academy of Sciences, USA 89, 58375841.
Correale, J. and Farez, M. (2007). Association between parasite infection and immune responses in multiple sclerosis. Annals of Neurology 61, 97–108.
Day, K. P., Gregory, W. F. and Maizels, R. M. (1991 a). Age-specific acquisition of immunity to infective larvae in a Bancroftian filariasis endemic area of Papua New Guinea. Parasite Immunology 13, 277290.
Day, K. P., Grenfell, B., Spark, R., Kazura, J. W. and Alpers, M. P. (1991 b). Age specific patterns of change in the dynamics of Wuchereria bancrofti infection in Papua New Guinea. American Journal of Tropical Medicine and Hygiene 44, 518527.
de Savigny, D. H. (1975). In vitro maintenance of Toxocara canis larvae and a simple method for the production of Toxocara ES antigen for use in serodiagnosis test for visceral larva migrans. Journal of Parasitology 61, 781782.
Des Moutis, I., Ouaissi, A., Grzych, J. M., Yarzabal, L., Haque, A. and Capron, A. (1983). Onchocerca volvulus: detection of circulating antigen by monoclonal antibodies in human onchocerciasis. American Journal of Tropical Medicine and Hygiene 32, 533542.
Devaney, E. (1988). The biochemical and immunochemical characterisation of the 30 kilodalton surface antigen of Brugia pahangi. Molecular and Biochemical Parasitology 27, 183192.
Doetze, A., Satoguina, J., Burchard, G., Rau, T., Loliger, C., Fleischer, B. and Hoerauf, 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. International Immunology 12, 623630.
Elliott, D. E., Summers, R. W. and Weinstock, J. V. (2007). Helminths as governors of immune-mediated inflammation. International Journal for Parasitology 37, 457464.
Else, K. J., Finkelman, F. D., Maliszewski, C. R. and Grencis, R. K. (1994). Cytokine-mediated regulation of chronic intestinal helminth infection. Journal of Experimental Medicine 179, 347351.
Falcone, F. H., Loke, P., Zang, X., MacDonald, A. S., Maizels, R. M. and Allen, J. E. (2001). A Brugia malayi homolog of macrophage migration inhibitory factor reveals an important link between macrophages and eosinophil recruitment during nematode infection. Journal of Immunology 167, 53485354.
Fattah, D. I., Maizels, R. M., McLaren, D. J. and Spry, C. J. F. (1986). Toxocara canis: interaction of human eosinophils with infective larvae in vitro. Experimental Parasitology 61, 421433.
Fernández, C., Gregory, W. F., Loke, P. and Maizels, R. M. (2002). Full-length-enriched cDNA libraries from Echinococcus granulosus contain separate populations of oligo-capped and trans-spliced transcripts and a high level of predicted signal peptide sequences. Molecular and Biochemical Parasitology 122, 171180.
Finkelman, F. D., Shea-Donohue, T., Goldhill, J., Sullivan, C. A., Morris, S. C., Madden, K. B., Gause, W. C. and Urban, J. F. Jr. (1997). Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annual Review of Immunology 15, 505533.
Finney, C. A., Taylor, M. D., Wilson, M. S. and Maizels, R. M. (2007). Expansion and activation of CD4+CD25+ regulatory T cells in Heligmosomoides polygyrus infection. European Journal of Immunology 37, 18741886.
Forsyth, K. P., Spark, R., Kazura, J. W., Broen, G. V., Peters, P., Heywood, P., Dissanayake, S. and Mitchell, G. F. (1985). A monoclonal antibody-based immunoradiometric assay for detection of circulating antigen in Bancroftian filariasis. Journal of Immunology 134, 11721177.
Gems, D. H., Ferguson, C. J., Robertson, B. D., Page, A. P., Blaxter, M. L. and Maizels, R. M. (1995). An abundant, trans-spliced mRNA from Toxocara canis infective larvae encodes a 26 kDa protein with homology to phosphatidylethanolamine binding proteins. Journal of Biological Chemistry 270, 1851718522.
Gems, D. H. 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, 16651670.
Ghedin, E., Wang, S., Spiro, D., Caler, E., Zhao, Q., Crabtree, J., Allen, J. E., Delcher, A. L., Guiliano, D. B., Miranda-Saavedra, D., Angiuoli, S. V., Creasy, T., Amedeo, P., Haas, B., El-Sayed, N. M., Wortman, J. R., Feldblyum, T., Tallon, L., Schatz, M., Shumway, M., Koo, H., Salzberg, S. L., Schobel, S., Pertea, M., Pop, M., White, O., Barton, G. J., Carlow, C. K., Crawford, M. J., Daub, J., Dimmic, M. W., Estes, C. F., Foster, J. M., Ganatra, M., Gregory, W. F., Johnson, N. M., Jin, J., Komuniecki, R., Korf, I., Kumar, S., Laney, S., Li, B. W., Li, W., Lindblom, T. H., Lustigman, S., Ma, D., Maina, C. V., Martin, D. M., McCarter, J. P., McReynolds, L., Mitreva, M., Nutman, T. B., Parkinson, J., Peregrin-Alvarez, J. M., Poole, C., Ren, Q., Saunders, L., Sluder, A. E., Smith, K., Stanke, M., Unnasch, T. R., Ware, J., Wei, A. D., Weil, G., Williams, D. J., Zhang, Y., Williams, S. A., Fraser-Liggett, C., Slatko, B., Blaxter, M. L. and Scott, A. L. (2007). Draft genome of the filarial nematode parasite Brugia malayi. Science 317, 17561760.
Gomez-Escobar, N., Bennett, C., Prieto-Lafuente, L., Aebischer, T., Blackburn, C. C. and Maizels, R. M. (2005). Heterologous expression of the filarial nematode alt gene products reveals their potential to inhibit immune function. BMC Biology 3, 116.
Gomez-Escobar, N., Gregory, W. F. and Maizels, R. M. (2000). Identification of Bm-tgh-2, a filarial nematode homolog of C. elegans daf-7 and human TGF-β, expressed in microfilarial and adult stages of Brugia malayi. Infection and Immunity 68, 64026410.
Gomez-Escobar, N., Lewis, E. and Maizels, R. M. (1998). A novel member of the transforming growth factor-β (TGF-β) superfamily from the filarial nematodes Brugia malayi and B. pahangi. Experimental Parasitology 88, 200209.
Goodridge, H. S., McGuiness, S., Houston, K. M., Egan, C. A., Al-Riyami, L., Alcocer, M. J., Harnett, M. M. and Harnett, W. (2007). Phosphorylcholine mimics the effects of ES-62 on macrophages and dendritic cells. Parasite Immunology 29, 127137.
Gordon, S. (2003). Alternative activation of macrophages. Nature Reviews Immunology 3, 2335.
Gounaris, K., Smith, V. P. and Selkirk, M. E. (1996). Structural organization and lipid composition of the epicuticular layer of infective larvae of Trichinella spiralis. Biochimica et Biophysica Acta 1281, 91–100.
Gregory, W. F., Atmadja, A. K., Allen, J. E. and Maizels, R. M. (2000). The abundant larval transcript 1/2 genes of Brugia malayi encode stage-specific candidate vaccine antigens for filariasis. Infection and Immunity 68, 41744179.
Gregory, W. F., Blaxter, M. L. and Maizels, R. M. (1997). Differentially expressed, abundant trans-spliced cDNAs from larval Brugia malayi. Molecular and Biochemical Parasitology 87, 8595.
Gregory, W. F. and Maizels, R. M. (2008). Cystatins from filarial parasites: evolution, adaptation and function in the host-parasite relationship. International Journal of Biochemistry and Cell Biology 40, 13891398.
Grencis, R. K., Crawford, C. R., Pritchard, D. I., Behnke, J. M. and Wakelin, D. (1986). Immunization of mice with surface antigens from the muscle larvae of Trichinella spiralis. Parasite Immunology 8, 587596.
Grigg, M. E., Tang, L., Hussein, A. S. and Selkirk, M. E. (1997). Purification and properties of monomeric (G1) forms of acetylcholinesterase secreted by Nippostrongylus brasiliensis. Molecular and Biochemical Parasitology 90, 513524.
Harcus, Y. M., Parkinson, J., Fernández, C., Daub, J., Selkirk, M. E., Blaxter, M. L. and Maizels, R. M. (2004). Signal sequence analysis of expressed sequence tags from the nematode Nippostrongylus brasiliensis and the evolution of secreted proteins in parasites. Genome Biology 5, R39.
Harnett, W., Goodridge, H. S. and Harnett, M. M. (2005). Subversion of immune cell signal transduction pathways by the secreted filarial nematode product, ES-62. Parasitology 130 (Suppl.), S63S68.
Hartmann, S. and Lucius, R. (2003). Modulation of host immune responses by nematode cystatins. International Journal for Parasitology 33, 12911302.
Hawdon, J. M., Jones, B. F., Hoffman, D. R. and Hotez, P. J. (1996). Cloning and characterization of Ancylostoma-secreted protein. A novel protein associated with the transition to parasitism by infective hookworm larvae. Journal of Biological Chemistry 271, 66726678.
Healer, J., Ashall, F. and Maizels, R. M. (1991). Characterization of proteolytic enzymes from larval and adult Nippostrongylus brasiliensis. Parasitology 103, 305314.
Hewitson, J. P., Harcus, Y. M., Curwen, R. S., Dowle, A. A., Atmadja, A. K., Ashton, P. D., Wilson, R. A. and Maizels, R. M. (2008). The secretome of the filarial parasite, Brugia malayi: proteomic profile of adult excretory-secretory products. Molecular Biochemistry and Parasitology 160, 8–21.
Hintz, M., Schares, G., Taubert, A., Geyer, R., Zahner, H., Stirm, S. and Conraths, F. J. (1998). Juvenile female Litomosoides sigmodontis produce an excretory/secretory antigen (Juv-p120) highly modified with dimethylaminoethanol. Parasitology 117, 265271.
Hoerauf, A. and Brattig, N. (2002). Resistance and susceptibility in human onchocerciasis–beyond Th1 vs. Th2. Trends in Parasitology 18, 2531.
Holland, M. J., Harcus, Y. M., Riches, P. L. and Maizels, R. M. (2000). Proteins secreted by the parasitic nematode Nippostrongylus brasiliensis act as adjuvants for Th2 responses. European Journal of Immunology 30, 19771987.
Hotez, P. J., Brindley, P. J., Bethony, J. M., King, C. H., Pearce, E. J. and Jacobson, J. (2008). Helminth infections: the great neglected tropical diseases. Journal of Clinical Investigation 118, 13111321.
Hussain, R., Grögl, M. and Ottesen, E. A. (1987). IgG antibody subclasses in human filariasis. Differential subclass recognition of parasite antigens correlates with different clinical manifestations of infection. Journal of Immunology 139, 27942798.
Jones, V. E. and Ogilvie, B. M. (1972). Protective immunity to Nippostrongylus brasiliensis in the rat. III. Modulation of worm acetylcholinesterase by antibodies. Immunology 22, 119129.
Kaminsky, R., Ducray, P., Jung, M., Clover, R., Rufener, L., Bouvier, J., Weber, S. S., Wenger, A., Wieland-Berghausen, S., Goebel, T., Gauvry, N., Pautrat, F., Skripsky, T., Froelich, O., Komoin-Oka, C., Westlund, B., Sluder, A. and Maser, P. (2008). A new class of anthelmintics effective against drug-resistant nematodes. Nature, London 452, 176180.
Khoo, K.-H., Maizels, R. M., Page, A. P., Taylor, G. W., Rendell, N. and Dell, A. (1991). Characterisation of nematode glycoproteins: the major O-glycans of Toxocara excretory secretory antigens are methylated trisaccharides. Glycobiology 1, 163171.
King, C. H., Dickman, K. and Tisch, D. J. (2005). Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365, 15611569.
Kurniawan, A., Sartono, E., Partono, F., Yazdanbakhsh, M. and Maizels, R. M. (1998). Specificity of predominant IgG4 antibodies to adult and microfilarial stages of Brugia malayi. Parasite Immunology 20, 155162.
Kwan-Lim, G.-E., Forsyth, K. P. and Maizels, R. M. (1990). Filarial-specific IgG4 response correlates with active Wuchereria bancrofti infection. Journal of Immunology 145, 42984305.
Kwan-Lim, G.-E., Gregory, W. F., Selkirk, M. E., Partono, F. and Maizels, R. M. (1989). Secreted antigens of filarial nematodes: survey and characterisation of in vitro excretory/secretory (E/S) products of adult Brugia malayi filarial parasites. Parasite Immunology 11, 629654.
Lawrence, R. A., Allen, J. E., Gregory, W. F., Kopf, M. and Maizels, R. M. (1995). Infection of IL-4 deficient mice with the parasitic nematode Brugia malayi demonstrates that host resistance is not dependent on a Th2 dominated immune response. Journal of Immunology 154, 59956001.
Lawrence, R. A., Allen, J. E., Osborne, J. and Maizels, R. M. (1994). Adult and microfilarial stages of the filarial parasite Brugia malayi stimulate contrasting cytokine and immunoglobulin isotype responses in BALB/c mice. Journal of Immunology 153, 12161224.
Loke, P., Gallagher, I., Nair, M. G., Zang, X., Brombacher, F., Mohrs, M., Allison, J. P. and Allen, J. E. (2007). Alternative activation is an innate response to injury that requires CD4+ T cells to be sustained during chronic infection. Journal of Immunology 179, 39263936.
Loke, P., MacDonald, A. S., Robb, A., Maizels, R. M. and Allen, J. E. (2000). Alternatively activated macrophages induced by nematode infection inhibit proliferation via cell to cell contact. European Journal of Immunology 30, 26692678.
Loukas, A. C., 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, 545554.
Loukas, A. C., Hintz, M., Tetteh, K. K. A., Mullin, N. P. and Maizels, R. M. (2000 b). A family of secreted mucins from the parasitic nematode Toxocara canis bear diverse mucin domains but share similar flanking six-cysteine (SXC) repeat motifs. Journal of Biological Chemistry 275, 3960039607.
Loukas, A. and Maizels, R. M. (2000). Helminth C-type lectins and host-parasite interactions. Parasitology Today 16, 333339.
Loukas, A. C., 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, 825828.
MacDonald, A. S. and Maizels, R. M. (2008). Alarming dendritic cells for Th2 induction. Journal of Experimental Medicine 205, 1317.
MacDonald, A. S., Maizels, R. M., Lawrence, R. A., Dransfield, I. and Allen, J. E. (1998). Requirement for in vivo production of IL-4, but not IL-10, in the induction of proliferative suppression by filarial parasites. Journal of Immunology 160, 41244132.
Maizels, R. M. (2005). Infections and allergy – helminths, hygiene and host immune regulation. Current Opinion in Immunology 17, 656661.
Maizels, R. M., Blaxter, M. L. and Scott, A. L. (2001 a). Immunological genomics of Brugia malayi: filarial genes implicated in immune evasion and protective immunity. Parasite Immunology 23, 327344.
Maizels, R. M., Burke, J. and Denham, D. A. (1987 a). Phosphorylcholine-bearing antigens in filarial nematode parasites: analysis of somatic extracts and in vitro secretions of Brugia malayi and B. pahangi and infection sera. Parasite Immunology 9, 4966.
Maizels, R. M., Burke, J., Sutanto, I., Purnomo, and Partono, F. (1986). Secreted and surface antigens from the larval stages of Wuchereria bancrofti, the major human lymphatic filarial parasite. Molecular and Biochemical Parasitology 19, 2734.
Maizels, R. M., Clarke, J. A., Harvey, M. A., Miller, A. and Sercarz, E. E. (1980). Epitope specificity of the T cell proliferative response to lysozyme: proliferative T cells react predominantly to different determinants from those recognized by B cells. European Journal of Immunology 10, 509515.
Maizels, R. M., Denham, D. A. and Sutanto, I. (1985). Secreted and circulating antigens of the filarial parasite Brugia pahangi: Analysis of in vitro released components and detection of parasite products in vivo. Molecular and Biochemical Parasitology 17, 277278.
Maizels, R. M., de Savigny, D. and Ogilvie, B. M. (1984). Characterization of surface and excretory- secretory antigens of Toxocara canis infective larvae. Parasite Immunology 6, 2337.
Maizels, R. M., Gomez-Escobar, N., Gregory, W. F., Murray, J. and Zang, X. (2001 b). Immune evasion genes from filarial nematodes. International Journal for Parasitology 31, 889898.
Maizels, R. M., Gomez-Escobar, N., Prieto-Lafuente, L., Murray, J. and Aebischer, T. (2008). Expression of helminth genes in Leishmania: an experimental transfection system to test immunological function. Parasite Immunology 30, 195201.
Maizels, R. M., Gregory, W. F., Kwan-Lim, G.-E. and Selkirk, M. E. (1989). Filarial surface antigens: the major 29,000 mol.wt. glycoprotein and a novel 17,000–200,000 mol.wt. complex from adult Brugia malayi parasites. Molecular and Biochemical Parasitology 32, 213227.
Maizels, R. M. and Holland, M. J. (1998). Parasite immunity: pathways for expelling intestinal parasites. Current Biology 8, R711R714.
Maizels, R. M., Kennedy, M. W., Meghji, M., Robertson, B. D. and Smith, H. V. (1987 b). Shared carbohydrate epitopes on distinct surface and secreted antigens of the parasitic nematode Toxocara canis. Journal of Immunology 139, 207214.
Maizels, R. M. and Kurniawan-Atmadja, A. (2002). Variation and polymorphism in helminth parasites. Parasitology 125 (Suppl.), S25S37.
Maizels, R. M. and Lawrence, R. A. (1991). Immunological tolerance: the key feature in human filariasis? Parasitology Today 7, 271276.
Maizels, R. M., Partono, F., Oemijati, S., Denham, D. A. and Ogilvie, B. M. (1983 a). Cross-reactive surface antigens on three stages of Brugia malayi, B. pahangi and B. timori. Parasitology 87, 249263.
Maizels, R. M., Partono, F., Oemijati, S. and Ogilvie, B. M. (1983 b). Antigenic analysis of Brugia timori, a filarial nematode of man: Initial characterisation by surface radio- iodination and evaluation of diagnostic potential. Clinical and Experimental Immunology 51, 269277.
Maizels, R. M., Philipp, M. and Ogilvie, B. M. (1982). Molecules on the surface of nematodes as probes of the immune responses in infection. Immunological Reviews 61, 109136.
Maizels, R. M., Tetteh, K. K. A. and Loukas, A. C. (2000). Toxocara canis: genes expressed by the arrested infective larval stage of a parasitic nematode. International Journal of Parasitology 30, 495508.
Maizels, R. M. and Yazdanbakhsh, M. (2003). Regulation of the immune response by helminth parasites: cellular and molecular mechanisms. Nature Reviews Immunology 3, 733743.
Manoury, B., Gregory, W. F., Maizels, R. M. and Watts, C. (2001). Bm-CPI-2, a cystatin homolog secreted by the filarial parasite Brugia malayi, inhibits class II MHC-restricted antigen processing. Current Biology 11, 447451.
Mazmanian, S. K., Round, J. L. and Kasper, D. L. (2008). A microbial symbiosis factor prevents intestinal inflammatory disease. Nature, London 453, 620625.
McSorley, H. J., Harcus, Y. M., Murray, J., Taylor, M. D. and Maizels, R. M. (2008). Expansion of Foxp3+ regulatory T cells in mice infected with the filarial parasite, Brugia malayi. Journal of Immunology 181, 64566466.
Meghji, M. and Maizels, R. M. (1986). Biochemical properties of larval excretory- secretory (ES) glycoproteins of the parasitic nematode Toxocara canis. Molecular and Biochemical Parasitology 18, 155170.
Melendez, A. J., Harnett, M. M., Pushparaj, P. N., Wong, W. S. F., Tay, H. K., McSharry, C. P. and Harnett, W. (2007). Inhibition of FceRI-mediated mast cell responses by ES-62, a product of parasitic filarial nematodes. Nature Medicine 13, 13751381.
Morgan, T. M., Sutanto, I., Purnomo, , Sukartono, , Partono, F. and Maizels, R. M. (1986). Antigenic characterisation of adult Wuchereria bancrofti filarial nematodes. Parasitology 93, 559569.
Mosmann, T. R., Cherwinski, H., Bond, M. W., Giedlin, M. A. and Coffman, R. L. (1986). Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. Journal of Immunology 136, 23482357.
Murray, J., Gregory, W. F., Gomez-Escobar, N., Atmadja, A. K. and Maizels, R. M. (2001). Expression and immune recognition of Brugia malayi VAL-1, a homologue of vespid venom allergens and Ancylostoma secreted proteins. Molecular and Biochemical Parasitology 118, 8996.
Murray, J., Manoury, B., Balic, A., Watts, C. and Maizels, R. M. (2005). Bm-CPI-2, a cystatin from Brugia malayi nematode parasites, differs from C. elegans cystatins in a specific site mediating inhibition of the antigen-processing enzyme AEP. Molecular and Biochemical Parasitology 139, 197203.
Ottesen, E. A. (1984). Immunological aspects of lymphatic filariasis and onchocerciasis in man. Transactions of the Royal Society of Tropical Medicine and Hygiene, 78 (Suppl), 9–18.
Page, A. P., Hamilton, A. J. and Maizels, R. M. (1992 a). Toxocara canis: monoclonal antibodies to carbohydrate epitopes of secreted (TES) antigens localize to different secretion-related structures in infective larvae. Experimental Parasitology 75, 5671.
Page, A. P., Rudin, W., Fluri, E., Blaxter, M. L. and Maizels, R. M. (1992 b). Toxocara canis: a labile antigenic coat overlying the epicuticle of infective larvae. Experimental Parasitology 75, 7286.
Parkhouse, R. M. E., Clarke, N. W. T., Maizels, R. M. and Denham, D. A. (1985). Brugia pahangi: Labelling of secreted antigens with 35S-methionine in vitro. Parasite Immunology 7, 665668.
Parkinson, J., Mitreva, M., Whitton, C., Thomson, M., Daub, J., Martin, J., Schmid, R., Hall, N., Barrell, B., Waterston, R. H., McCarter, J. P. and Blaxter, M. L. (2004). A transcriptomic analysis of the phylum Nematoda. Nature Genetics 36, 12591267.
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, 59555963.
Péry, P., Luffau, G., Charley, J., Petit, A., Rouze, P. and Bernard, S. (1979). Phosphorylcholine antigens from Nippostrongylus brasiliensis. I. Anti-phosphorylcholine antibodies in infected rats and location of phosphorylcholine antigens. Annales d'Immunologie (Institut Pasteur) 130C, 879888.
Philipp, M., Parkhouse, R. M. E. and Ogilvie, B. M. (1980). Changing proteins on the surface of a parasitic nematode. Nature, London 287, 538540.
Philipp, M., Taylor, P. M., Parkhouse, R. M. E. and Ogilvie, B. M. (1981). Immune response to stage-specific surface antigens of the parasitic nematode Trichinella spiralis. Journal of Experimental Medicine 154, 210215.
Platts-Mills, T. A., Vaughan, J. W., Blumenthal, K., Pollart Squillace, S. and Sporik, R. B. (2001). Serum IgG and IgG4 antibodies to Fel d 1 among children exposed to 20 microg Fel d 1 at home: relevance of a nonallergic modified Th2 response. International Archives of Allergy and Immunology 124, 126129.
Prieto-Lafuente, L., Gregory, W. F., Allen, J. E. and Maizels, R. M. (2009). MIF homologues from a filarial nematode parasite synergize with IL-4 to induce alternative activation of host macrophages. Journal of Leukocyte Biology 85, 844854.
Redman, E., Packard, E., Grillo, V., Smith, J., Jackson, F. and Gilleard, J. S. (2008). Microsatellite analysis reveals marked genetic differentiation between Haemonchus contortus laboratory isolates and provides a rapid system of genetic fingerprinting. International Journal for Parasitology 38, 111122.
Sakaguchi, S. (2000). Regulatory T cells: key controllers of immunologic self-tolerance. Cell 101, 455458.
Sartono, E., Kruize, Y. C. M., Kurniawan, A., van der Meide, P. H., Partono, F., Maizels, R. M. and Yazdanbakhsh, M. (1995). Elevated cellular responses and interferon-γ release after long-term diethylcarbamazine treatment of patients with human lymphatic filariasis. Journal of Infectious Diseases 171, 16831687.
Sartono, E., Kruize, Y. C. M., Kurniawan, A., Maizels, R. M. and Yazdanbakhsh, M. (1996). In Th2 biased lymphatic filarial patients, responses to PPD remain Th1. European Journal of Immunology 26, 501504.
Sartono, E., Kruize, Y. C. M., Kurniawan-Atmadja, A., Maizels, R. M. and Yazdanbakhsh, M. (1997). Depression of antigen-specific interleukin-5 and interferon-γ responses in human lymphatic filariasis as a function of clinical status and age. Journal of Infectious Diseases 175, 12761280.
Satoguina, J. S., Weyand, E., Larbi, J. and Hoerauf, A. (2005). T regulatory-1 cells induce IgG4 production by B cells: role of IL-10. Journal of Immunology 174, 47184726.
Schabussova, I., Amer, H., van Die, I., Kosma, P. and Maizels, R. M. (2007). O-Methylated glycans from Toxocara are specific targets for antibody binding in human and animal infections. International Journal for Parasitology 37, 97–109.
Selkirk, M. E., Nielsen, L., Kelly, C., Partono, F., Sayers, G. and Maizels, R. M. (1989). Identification, synthesis and immunogenicity of cuticular collagens from the filarial nematodes Brugia malayi and B. pahangi. Molecular and Biochemical Parasitology 32, 229246.
Selkirk, M. E., Rutherford, P. J., Denham, D. A., Partono, F. and Maizels, R. M. (1987). Cloned antigen genes of Brugia filarial parasites. Biochemical Society Symposia 53, 91–102.
Selkirk, M. E., Yazdanbakhsh, M., Freedman, D., Blaxter, M. L., Cookson, E., Jenkins, R. E. and Williams, S. A. (1991). A proline-rich structural protein of the surface sheath of larval Brugia filarial nematode parasites. Journal of Biological Chemistry 266, 1100211008.
Siracusa, M. C., Reece, J. J., Urban, J. F. Jr. and Scott, A. L. (2008). Dynamics of lung macrophage activation in response to helminth infection. Journal of Leukocyte Biology 84, 14221433.
Taylor, M. D., Harris, A., Babayan, S., Bain, O., Culshaw, A., Allen, J. E. and Maizels, R. M. (2007). CTLA-4+ and CD4+CD25+ regulatory T cells inhibit protective immunity to filarial parasites in vivo. Journal of Immunology 179, 46264634.
Taylor, M., Le Goff, L., Harris, A., Malone, E., Allen, J. E. and Maizels, R. M. (2005). Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. Journal of Immunology 174, 49244933.
Taylor, M. D., van der Werf, N., Harris, A., Graham, A. L., Bain, O., Allen, J. E. and Maizels, R. M. (2009). Early recruitment of natural CD4+Foxp3+ regulatory T cells by infective larvae determines the outcome of filarial infection. European Journal of Immunology 39, 192206.
Tetteh, K. K. A., Loukas, A., Tripp, C. and Maizels, R. M. (1999). Identification of abundantly-expressed novel and conserved genes from infective stage larvae of Toxocara canis by an expressed sequence tag strategy. Infection and Immunity 67, 47714779.
Tweedie, S., Paxton, W. A., Ingram, L., Maizels, R. M., McReynolds, L. A. and Selkirk, M. E. (1993). Brugia pahangi and Brugia malayi: a surface-associated glycoprotein (gp15/400) is composed of multiple tandemly repeated units and processed from a 400-kDa precursor. Experimental Parasitology 76, 156164.
van den Biggelaar, A., van Ree, R., Roderigues, L. C., Lell, B., Deelder, A. M., Kremsner, P. G. and Yazdanbakhsh, M. (2000). Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356, 17231727.
Vermeire, J. J., Cho, Y., Lolis, E., Bucala, R. and Cappello, M. (2008). Orthologs of macrophage migration inhibitory factor from parasitic nematodes. Trends in Parasitology 24, 355363.
Weil, G. J., Lammie, P. J. and Weiss, N. (1997). The ICT filariasis test: a rapid-format antigen test for diagnosis of bancroftian filariasis. Parasitology Today 13, 401404.
Williamson, A. L., Lustigman, S., Oksov, Y., Deumic, V., Plieskatt, J., Mendez, S., Zhan, B., Bottazzi, M. E., Hotez, P. J. and Loukas, A. (2006). Ancylostoma caninum MTP-1, an astacin-like metalloprotease secreted by infective hookworm larvae, is involved in tissue migration. Infection and Immunity 74, 961967.
Wilson, M. S. and Maizels, R. M. (2004). Regulation of allergy and autoimmunity in helminth infection. Clinical Reviews in Allergy and Immunology 26, 3549.
Wilson, M. S., Taylor, M., Balic, A., Finney, C. A. M., Lamb, J. R. and Maizels, R. M. (2005). Suppression of allergic airway inflammation by helminth-induced regulatory T cells. Journal of Experimental Medicine 202, 11991212.
Wu, Y., Egerton, G., Pappins, D. J. C., Harrison, R. A., Wilkinson, M., Underwood, A. and Bianco, A. E. (2004). The secreted larval acidic proteins (SLAPs) of Onchocerca spp. are encoded by orthologues of the alt gene family of Brugia malayi and have host protective potential. Molecular and Biochemical Parasitology 134, 213224.
Yatsuda, A. P., Krijgsveld, J., Cornelissen, A. W. C. A., Heck, A. J. and De Vries, E. (2003). Comprehensive analysis of the secreted proteins of the parasite Haemonchus contortus reveals extensive sequence variation and differential immune recognition. Journal of Biological Chemistry 278, 1694116951.
Yazdanbakhsh, M., Kremsner, P. G. and van Ree, R. (2002). Allergy, parasites, and the hygiene hypothesis. Science 296, 490494.
Yazdanbakhsh, M., van den Biggelaar, A. and Maizels, R. M. (2001). Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends in Immunology 22, 372377.
Zang, X. X., Atmadja, A. K., Gray, P., Allen, J. E., Gray, C. A., Lawrence, R. A., Yazdanbakhsh, M. and Maizels, R. M. (2000). The serpin secreted by Brugia malayi microfilariae, Bm-SPN-2, elicits strong, but short-lived, immune responses in mice and humans. Journal of Immunology 165, 51615169.
Zang, X. and Maizels, R. M. (2001). Serine proteinase inhibitors from nematodes and the arms race between host and pathogen. Trends in Biochemical Sciences 26, 191197.
Zang, X. X., Taylor, P., Meyer, D., Wang, J. M., Scott, A. L., Walkinshaw, M. D. and Maizels, R. M. (2002). Homologues of human macrophage migration inhibitory factor from a parasitic nematode: gene cloning, protein activity and crystal structure. Journal of Biological Chemistry 277, 4426144267.
Zang, X. X., Yazdanbakhsh, M., Kiang, H., Kanost, M. R. and Maizels, R. M. (1999). A novel serpin expressed by the blood-borne microfilariae of the parasitic nematode Brugia malayi inhibits human neutrophil serine proteinases. Blood 94, 14181428.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 8
Total number of PDF views: 24 *
Loading metrics...

Abstract views

Total abstract views: 256 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 24th March 2018. This data will be updated every 24 hours.