Molecules released by helminth parasites involved in host colonization

• Autorzy: Dzik J. M.
• Języki publikacji: EN

Abstrakty

EN

Parasites are designed by evolution to invade the host and survive in its organism until they are ready to reproduce. Parasites release a variety of molecules that help them to penetrate the defensive barriers and avoid the immune attack of the host. In this respect, particularly interesting are enzymes and their inhibitors secreted by the parasites. Serine-, aspartic-, cysteine-, and metalloproteinases are involved in tissue invasion and extracellular protein digestion. Helminths secrete inhibitors of these enzymes (serpins, aspins, and cystatins) to inhibit proteinases, both of the host and their own. Proteinases and their inhibitors, as well as helminth homologues of cytokines and molecules containing phosphorylcholine, influence the immune response of the host biasing it towards the anti-inflammatory Th2 type. Nucleotide-metabolizing enzymes and cholinesterase are secreted by worms to reduce inflammation and expel the parasites from the gastrointestinal tract. An intracellular metazoan parasite, Trichinella spiralis, secretes, among others, protein kinases and phosphatases, endonucleases, and DNA-binding proteins, which are all thought to interfere with the host cellular signals for muscle cell differentiation. Secretion of antioxidant enzymes is believed to protect the parasite from reactive oxygen species which arise from the infection-stimulated host phagocytes. Aside from superoxide dismutase, catalase (rarely found in helminths), and glutathione peroxidase (selenium-independent, thus having a poor activity with H2O2), peroxiredoxins are probably the major H2O2-detoxifying enzymes in helminths. Secretion of antioxidant enzymes is stage-specific and there are examples of regulation of their expression by the concentration of reactive oxygen species surrounding the parasite. The majority of parasite-secreted molecules are commonly found in free-living organisms, thus parasites have only adapted them to use in their way of life.

Słowa kluczowe

EN

superoxide dismutase; phosphorylcholine; helminth; kinase; parasite; cytokine; peroxiredoxin; acetylcholinesterase; host colonization; phosphatase; proteinase; proteinase inhibitor; Th2 immune response

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 2006
• Tom: 53
• Numer: 1
• Opis fizyczny: p.33-64,fig.,ref.

Twórcy

autor

Dzik J. M.

• Polish Academy of Sciences, Warsaw, Poland

Bibliografia

• Abrahamson M (1994) Cystatins. Methods Enzymol 244: 685−700.
• Adam R, Kaltmann B, Rudin W, Friedrich T, Marti T, Lucius R (1996) Identification of chitinase as the immunodominant filarial antigen recognized by sera of vaccinated rodents. J Biol Chem 271: 1441−1447.
• Alger HM, Sayed AA, Stadecker MJ, Williams DL (2002) Molecular and enzymatic characterization of Schistosoma mansoni thioredoxin. Int J Parasitol 32: 1285−1292.
• ap-Rhys CM, Bohr VA (1996) Mammalian DNA repair responses and genomic instability. Experientia 77 (Suppl): 289−305.
• Arden SR, Smith AM, Booth MJ, Tweedi S, Gounaris K, Selkirk ME (1997) Identification of serine/threonine protein kinases secreted by Trichinella spiralis infective larvae. Mol Biochem Parasitol 90: 111−119.
• Arechavaleta F, Molinari JL, Tato P (1998) A Taenia solium metacestode factor nonspecifically inhibits cytokine production. Parasitol Res 84: 117−122.
• Auriault C, Ouaissi MA, Torpier G, Eisen H, Capron A (1981) Proteolytic cleavage of IgG bound to the Fc receptor of Schistosoma mansoni schistosomula. Parasite Immunol 3: 33−44.
• Bacher M, Metz CN, Calandra T, Mayer K, Chesney J, Lohoff M, Gemsa D, Donnelly T, Bucala R (1996) An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc Natl Acad Sci USA 93: 7849−7854.
• Bass DA, Szejda P (1979) Mechanisms of killing of newborn larvae of Trichinella spiralis by neutrophils and eosinophils. Killing by generation of hydrogen peroxide in vitro. J Clin Invest 64: 1558–1564.
• Bendjennat M, Blanchard A, Loutfi M, Montagnier L, Bahraoui E (1997) Purification and characterization of Mycoplasma penetrans Ca2+/Mg2+-dependent endonuclease. J Bacteriol 179: 2210−2220.
• Bennett K, Levine T, Ellis JS, Peanasky RJ, Samloff IM, Kay J, Chain BM (1992) Antigen processing for presentation by class II major histocompatibility complex requires cleavage by cathepsin E. Eur J Immunol 22: 1519−1524.
• Bennett CB, Snipe JR, Resnick MA (1997) A persistent double- strand break destabilizes human DNA in the yeast and can lead to G2 arrest and lethality. Cancer Res 57: 1970−1980.
• Bernal D, de la Rubia JE, Carrasco-Abad Toledo R, Mas- Coma S, Marcilla A (2004) Identification of enolase as a plasminogen-binding protein in excretory-secretory products of Fasciola hepatica. FEBS Lett 563: 203−206.
• Biaggioni I (2004) Clinical and molecular pharmacological characteristics of adenosine induced vasodilatation. Clin Pharmacol Ther 75: 137−139.
• Bitar KN, Makhlouf GM (1982) Relaxation of isolated gastric smooth muscle cells by vasoactive intestinal peptide. Science 216: 531−533.
• Boyer TD (1989) The glutathione S-transferase: an update. Hepatology 9: 486−496.
• Brigelius-Flohe R (1999) Tissue-specific functions of individual glutathione peroxidases. Free Radic Biol Med 27: 951−965.
• Brink PR, Walcott B, Roemer E, Grine E, Pastor M, Christ GJ, Cameron RH (1994) Cholinergic modulation of immunoglobulin secretion from avian plasma cells: the role of calcium. J Neuroimmunol 51: 113−121.
• Britton C, Murray L (2004) Cathepsin L protease is essential for yolk processing during embryogenesis in Caenorhabditis elegans. J Cell Sci 117: 5133−5143.
• Brown A, Burleigh JM, Billett EE, Pritchard DI (1995) An initial characterization of proteolytic enzymes secreted by the adult stage of the human hookworm Necator americanus. Parasitology 110: 555−563.
• Bucheimer RE, Linden J (2004) Purinergic regulation of epithelial transport. J Physiol 555: 311−321.
• Callahan HL, Crouch RK, James ER (1988) Helminth antioxidant enzymes: a protective mechanism against host oxidants. Parasitol Today 4: 218−225.
• Callahan HL, Crouch RK, James ER (1990) Hydrogen peroxide is the most toxic oxygen species for Onchocerca cervicalis microfilariae. Parasitology 100: 407−415.
• Capo V, Silberstein D, Despommier DD (1986) Immunocytolocalization of two protection-inducing antigens of Trichinella spiralis during its enteral phase in immune and non-immune mice. J Parasitol 72: 931−938.
• Cappello M, Vlasuk GP, Bergum PW, Huang S, Hotez PJ (1995) Ancylostoma caninum anticoagulant peptide: a hookworm derived inhibitor of human coagulation factor Xa. Proc Natl Acad Sci USA 92: 6152−6156.
• Carmona C, Dowd AJ, Smith AM, Dalton JP (1993) Cathepsin L proteinase secreted by Fasciola hepatica in vitro prevents antibody-mediated eosinophil attachment to new excysted juveniles. Mol Bioch Parasitol 62: 9−18.
• Chae HZ, Chung SJ, Rhee SG (1994a) Thioredoxin-dependent peroxide reductase from yeast. J Biol Chem 269: 27670−27678.
• Chae HZ, Robison K, Poole LB, Church G, Storz G, Rhee SG (1994b) Cloning and sequencing of thiol-specific antioxidant from mammalian brain: alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc Natl Acad Sci USA 91: 7017−7021.
• Chae HZ, Uhm TB, Rhee SG (1994c) Dimerization of thiolspecific antioxidant and the essential role of cysteine 47. Proc Natl Acad Sci USA 91: 7022−7026.
• Chandrashekar R, Tsuji N, Morales TH, Carmody AB, Ozols VO, Welton J, Tang L (2000) Removal of hydrogen peroxide by a 1-cysteine peroxiredoxin enzyme of the filarial parasite Dirofilaria immitis. Parasitol Res 86: 200−206.
• Chapman CB, Mitchell GF (1982) Proteolytic cleavage of immunoglobulin by enzymes released by Fasciola hepatica. Vet Parasitol 11: 165−178.
• Chertov O, Ueda H, Xu LL, Tani K, Murphy WJ, Wang JM, Howard OM, Sayers TJ, Oppenheim JJ (1997) Identification of human neutrophil-derived cathepsin G and azurocidin/CAP37 as chemoattractants for mononuclear cells and neutrophils. J Exp Med 186: 739−747.
• Cho SY, Chung YB, Kong Y (1992) Component proteins and proteases activities in excretory-secretory product of sparganum. Korean J Parasitol 30: 227−230.
• Coelho-Castelo AAM, Panunto-Castelo A, Moreno AN, Dias-Baruffi M, Jamur MC, Oliver C, Roque-Barreira MC, Rodrigues V (2002) Sm60, a mannose-binding protein from Schistosoma mansoni with inflammatory property Int J Parasitol 32: 1747−1754.
• Cooke HJ (1984) Influence of enteric cholinergic neurons on mucosal transport in guinea pig ileum. Am J Physiol 246: G263−G267.
• Cooke HJ, Wunderlich J, Christofi FL (2003) “The force be with you”: ATP in gut mechanosensory transduction. News Physiol Sci 18: 43−49.
• Cookson E, Blaxter ML, Selkirk ME (1992) Identification of the major soluble cuticular glycoprotein of lymphatic filarial nematode parasites (gp29) as a secretory form of glutathione peroxidase. Proc Natl Acad Sci USA 89: 5837−5841.
• Cooper ES, Whyte-Alleng CAM, Finzi-Smith JS, McDonald TT (1992) Intestinal nematode infections in children: the pathophysiological price paid. Parasitology 104: S91−S103.
• Costa M, Furness JB (1983) The originations, pathways and terminations of neurones with VIP-like immunoreactivity in the guinea pig small intestine. Neuroscience 8: 665−676.
• Criado AF, Armas SC, Gimenez CP, Casado NE, Jimenez AG, Rodriguez FC (1992) Proteolytic enzymes from Trichinella spiralis larvae. Vet Parasitol 45: 133−140.
• Cross AR, Jones OT (1991) Enzymic mechanisms of superoxide production. Biochim Biophys Acta 1057: 281−298
• Cundell DR, Gerard NP, Gerard C, Idanpaan-Heikkila I, Tuomanen EI (1995) Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature 377: 435−438.
• Dainichi T, Maekawa Y, Ishii K, Zhang T, Nashed BF, Sakai T, Takashima M, Himeno K (2001) Nippocystatin, a cysteine protease inhibitor from Nippostrongylus brasiliensis, inhibits antigen processing and modulates antigen-specific immune response. Infect Immun 69: 7380−7386.
• Dalton JP, Smith AM, Clough KA, Brindley PJ (1995) Digestion of haemoglobin by schistosomes: 35 years on. Parasitol Today 11: 299−303.
• Das L, Datta N, Bandyopadhyay S, Das PK (2001) Successful therapy of lethal murine visceral leishmaniasis with cystatin involves up-regulation of nitric oxide and a favorable T-cell response. J Immunol 166: 4020−4028.
• Daub J, Loukas A, Pritchard DI, Blaxter M (2000) A survey of genes expressed in adults of the human hookworm Necator americanus. Parasitology 120: 171−184.
• Davies SJ, Pearce EJ (1995) Surface-associated serine-threonine kinase in Schistosoma mansoni. Mol Biochem Parasitol 70: 33−44.
• Deehan MR, Goodridge HS, Blair D, Lochnit G, Dennis RD, Geyer R, Harnett MM, Harnett W (2002) Immunomodulatory properties of Ascaris suum glycosphingolipids- phosphorylcholine and non-phosphorylcholine-dependent effects. Parasite Immunol 24: 463−469.
• Delaney A, Williamson A, Brand A, Ashcom J, Varghese G, Goud GN, Hawdon JM (2005) Cloning and characterisation of an aspartyl protease inhibitor (API-1) from Ancylostoma hookworms. Int J Parasitol 35: 303−313.
• Despommier DD, Gold AM, Buck SW, Capo V, Silberstein D (1990) Trichinella spiralis secreted antigen of the infective L1 larva localizes to the cytoplasm and nucleoplasm of infected host cells. Exp Parasitol 71: 27−38.
• Devaney E, Jecock RM (1991) The expression of the Mr 30,000 antigen in the third stage larvae of Brugia pahangi. Parasite Immunol 13: 75−87.
• Di Virgilio F, Borea PA, Illes P (2001) P2 receptors meet the immune system. Trends Pharmacol Sci 22: 5−7.
• Dirgahayu P, Fukumoto S, Miura K, Hirai K (2002) Excretory/ secretory products from plerocercoids of Spirometra erinaceieuropaei suppress the TNF-α gene expression by reducing phosphorylation of ERK1/2 and p38 MAPK in macrophages. Int J Parasitol 32: 1155−1162.
• Dirgahayu P, Fukumoto S, Tademoto S, Kina Y, Hirai K (2004) Excretory/secretory products from plerocercoids of Spirometra erinaceieuropaei suppress interleukin-1β gene expression in murine macrophages. Int J Parasitol 34: 577−564.
• Don TA, Jones MK, Smyth D, O’Donoghue P, Hotez P, Loukas A (2004) A pore-forming haemolysin from the hookworm, Ancylostoma caninum. Int J Parasitol 34: 1029−1035.
• Donnelly S, O’Neill SM, Sekiya M, Mulcahy G, Dalton JP (2005) Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infect Immun 73: 166−173.
• Drake LJ, Bianco AE, Bundy DAP, Ashall F (1994) Characterization of peptidases of adult Trichuris muris. Parasitology 109: 623−630.
• Dzik JM, Gołos B, Jagielska E, Kapała A, Wałajtys-Rode E (2002a) Early response of guinea-pig lungs to Trichinella spiralis infection. Parasite Immunol 24: 369−379.
• Dzik JM, Zieliński Z, Gołos B, Jagielska E, Wranicz M, Wałajtys-Rode E (2002b) Effect of cyclosporin A on immunological response in lungs of guinea pigs infected with Trichinella spiralis. Acta Biochim Polon 49: 233–247.
• Dzik JM, Gołos B, Jagielska E, Zieliński Z, Wałajtys-Rode E (2004) A non-classical type of alveolar macrophage response to Trichinella spiralis infection. Parasite Immunol 26: 197−205.
• Dzik JM, Zieliński Z, Gołos B, Wałajtys-Rode E (2006) Trichinella spiralis infection affects p47phox protein expression in guinea pig alveolar macrophages. Exp Parasitol 112: 158–163.
• Eckelt VH, Liebau E, Walter RD, Henkle-Dürsen K (1998) Primary sequence and activity analyses of a catalase from Ascaris suum. Mol Biochem Parasitol 95: 203−214.
• Ehrlich YH, Kornecki E (1987) Extracellular protein phosphorylation systems in the regulation of cellular responsiveness. Prog Clin Biol Res 249: 193−204.
• Estes D, Teale J (1991) Biochemical and functional analysis of extracellular stress proteins Mesocestoides corti. J Immunol 147: 3926−3934.
• Esumi N, Budarf M, Ciccarelli L, Sellinger B, Kozak CA, Wistow G (1998) Conserved gene structure and genomic linkage for d-dopachrome tautomerase (DDT) and MIF. Mamm Genome 9: 753−757.
• Fetterer RH, Rhoads ML (1997a) Characterization of haemolytic activity from adult Haemonchus contortus. Int J Parasitol 27: 1037−1040.
• Fetterer RH, Rhoads ML (1997b) The in vitro uptake and incorporation of hemoglobin by adult Haemonchus-contortus. Vet Parasitol 69: 77−87.
• Fishelson Z, Amiri P, Friend DS, Marikovsky M, Petitt M, Newport G, McKerrow JH (1992) Schistosoma mansoni: cell-specific expression and secretion of a serine protease during development of cercariae. Exp Parasitol 75: 87−98.
• Foster N, Lee DL (1996) A vasoactive intestinal polypeptide- like protein excreted/secreted by Nippostrongylus brasiliensis and its effect on contraction of uninfected rat intestine. Parasitology 112: 97−104.
• Foster N, Dean EJ, Lee DL (1994) The effect of homogenates and excretory/secretory products of Nippostrongylus brasiliensis and of acetylcholinesterase on the amplitude and frequency of contractions of uninfected rat intestine in vitro. Parasitology 108: 453−459.
• Fuhrman JA (1995) Filarial chitinases. Parasitol Today 11: 259−261.
• Fukumoto S, Hirai K, Tanihata T, Ohmori Y, Stuehr DJ, Hamilton DA (1997) Excretory/secretory products from plerocercoids of Spirometra erinaceieuropaei reduce iNOS and chemokine mRNA levels in peritoneal macrophages stimulated with cytokines and/or LPS. Parasite Immunol 19: 325−332.
• Gamble HR, Mansfield LS (1996) Characterization of excretory-secretory products from larval stages of Haemonchus contortus cultured in vitro. Vet Parasitol 62: 291−305.
• Gardiner CH (1976) Habit and reproductive behavior of Trichinella spiralis. J Parasitol 62: 865−870.
• Garraud O, Nkenfou C, Bradley JE, Perler FB, Nutman TB(1995) Identification of recombinant filarial proteins capable of inducing polyclonal and antigen-specific IgE and IgG4 antibodies. J Immunol 155: 1316−1325.
• Geldhof P, Claerebout E, Knox DP, Jagneessens J, Vercruysse J (2000) Proteinases released in vitro by the parasitic stages of the bovine abomasal nematode Ostertagia ostertagi. Parasitology 121: 639−647.
• Ghendler Y, Arnon R, Fishelson Z (1994) Schistosoma mansoni: isolation and characterization of Smpi56, a novel serine protease inhibitor. Exp Parasitol 78: 121−131.
• Ghosh I, Eisinger SW, Raghavan N, Scott AL (1998) Thioredoxin peroxidases from Brugia malayi. Mol Biochem Parasitol 91: 207−220.
• Gounaris K (2002) Nucleotidase cascades are catalyzed by secreted proteins of the parasitic nematode T. spiralis. Infect Immun 70: 4917−4924.
• Gounaris K, Selkirk ME (2005) Parasite nucleotide-metabolizing enzymes and host purinergic signaling Trends Parasitol 21: 17−21.
• Gounaris K, Thomas S, Najarro P, Selkirk ME (2001) Secreted variant of nucleoside diphosphate kinase from the intracellular parasitic nematode Trichinella spiralis. Infect Immun 69: 3658−3662.
• Gounaris K, Selkirk ME, Sadeghi SJ (2004) A nucleotidase with unique catalytic properties is secreted by Trichinella spiralis. Mol Biochem Parasitol 136: 257−264.
• Grencis RK, Entwistle GM (1997) Production of an IFN-γ homologue by an intestinal nematode: functionally significant or interesting artefact? Parasitology 115: S101−S115.
• Guyer RB, Skantar AM, Deering RA (1985) Acid Dnase activity from Dictyostelium discoideum. Biochim Biophys Acta 826: 151−153.
• Haffner A, Guilavogui AZ, Tischendorf FW, Brattig NW (1998) Onchocerca volvulus: microfilariae secrete elastinolytic and males nonelastinolytic matrix-degrading serine and metalloproteases. Exp Parasitol 90: 26−33.
• Halton DW (1997) Nutritional adaptations to parasitism within platyhelminthes. Int J Parasitol 27: 693−704.
• Harcus YM, Parkinson J, Fernandez C, Daub J, Selkirk ME, Blaxter ML, Maizels RM (2004) Signal sequence analysis of expressed sequence tags from the nematode Nippostrongylus brasiliensis and the evolution of secreted proteins in parasites. Genome Biol 5: R39.
• Harnett W, Harnett MM (1999) Phosphorylcholine: friend or foe of the immune system? Immuol Today 20: 125-129.
• Harnett W, Worms MJ, Kapil A, Grainger M, Parkhouse RM (1989) Origin, kinetics of circulation and fate in vivo of the major excretory-secretory product of Acanthocheilonema viteae. Parasitology 99: 229−239.
• Harnett W, Houston KM, Tate R, Garate T, Apfel H, Adam R, Haslam SM, Panico M, Paxton T, Dell A, Morris H, Brzeski H (1999) Molecular cloning and demonstration of an aminopeptidase activity in a filarial nematode glycoprotein. Mol Biochem Parasitol 104: 11−23.
• Harnett W, Harnett MM, Byron O (2003) Structural/functional aspects of ES−62 — a secreted immunomodulatory phosphorylcholine-containing filarial nematode glycoprotein. Curr Protein Pept Sci 4: 59−71.
• Hartmann S, Lucius R (2003) Modulation of host immune responses by nematode cystatins. Int J Parasitol 33: 1291−1302.
• Hartmann S, Adam R, Marti T, Kirsten C, Seidinger S, Lucius R (1997a) A 41-kDa antigen of the rodent filaria Acanthocheilonema viteae with homologies to tropomyosin induces host-protective immune responses. Parasitol Res 83: 390−393.
• Hartmann S, Kyewski B, Sonnenburg B, Lucius R (1997b) A filarial cysteine protease inhibitor down-regulates T cell proliferation and enhances interleukin-10 production. Eur J Immunol 27: 2253−2260.
• Hasko G, Cronstein BN (2004) Adenosine an endogenous regulator of innate immunity. Trends Immunol 25: 33−39.
• Haslam SM, Houston KM, Harnett W, Reason AJ, Morris HR, Dell A (1999) Structural studies of N-glycans of filarial parasites. Conservation of phosphorylcholinesubstituted glycans among species and discovery of novel chito-oligomers. J Biol Chem 274: 20953−20960.
• Hawdon JM, Jones BJ, Perregaux MA, Hotez PJ (1995) Ancylostoma caninum: metalloprotease release coincides with activation of infective larvae in vitro. Exp Parasitol 80: 205−211.
• Henkle-Dührsen K, Kampkötter A (2001) Antioxidant enzyme families in parasitic nematodes. Mol Biochem Parasitol 114: 129−141.
• Hey AS, Theander TG, Hviid L, Hazrati SM, Kemp M, Kharazami A (1994) The major surface glycoprotein (gp63) from Leishmania major and Leishmania donovani cleaves CD4 molecules on human T cells. J Immunol 152: 4542−4548.
• Hoffmann KF, Wynn TA, Dunne DW (2002) Cytokine-mediated host responses during schistosome infections; walking the fine line between immunological control and immunopathology. Adv Parasitol 52: 265−307.
• Hotez PJ, Cerami A (1983) Secretion of an antiproteolytic coagulant by Ancylostoma hookworms. J Exp Med 157: 1594−1603.
• Jaffe JJ, Lambert RA (1986) Glutathione S-transferase in adult Dirofilaria immitis and Brugia pahangi. Mol Biochem Parasitol 20: 199−206.
• James ER (1994) Superoxide dismutase. Parasitol Today 10: 481−484.
• Jasmer DP (1993) Trichinella spiralis infected skeletal muscle cells arrest in G2/M and cease muscle gene expression. J Cell Biol 121: 785−792.
• Jasmer DP (1995) Trichinella spiralis: subversion of differentiated mammalian skeletal muscle cells. Parasitol Today 11: 185−188.
• Jolodar A, Miller DJ (1998) Identification of a novel family of non-lysosomal aspartic proteases in nematodes. Biochim Biophys Acta 1382: 13−16.
• Jolodar A, Fischer P, Bergmann S, Büttner Hammerschmidt S, Brattig NW (2003) Molecular cloning of an α-enolase from the human filarial parasite Onchocerca volvulus that binds human plasminogen. Biochim Biophys Acta 1627: 111−120.
• Jong AY, Chen SH, Stins MF, Kim KS, Tuan TL, Huang SH (2003) Binding of Candida albicans enolase to plasmin(ogen) results in enhanced invasion of human brain microvascular endothelial cells. J Med Microbiol 52: 615−622.
• Kageyama T (1998) Molecular cloning, expression and characterization of an Ascaris inhibitor for pepsin and cathepsin E. Eur J Biochem 253: 804−809.
• Kang SW, Baines IC, Rhee SG (1998) Characterization of mammalian peroxiredoxin that contains one conserved cysteine. J Biol Chem 273: 6303−6311.
• Karanu FN, Rurangirwa FR, McGuire TC, Jasmer DP (1993) Haemonchus contortus: identification of proteases with diverse characteristics in adult worm excretorysecretory products. Exp Parasitol 77: 362−371.
• Kato Y, Muto T, Tomura T, Tsumura H, Watarai H, Mikayama T, Ishizaka K, Kuroki R (1996) The crystal structure of human glycosylation-inhibiting factor is a trimeric barrel with three 6-stranded β-sheets. Proc Natl Acad Sci USA 93: 3007−3010.
• Kazura JW, Meshnick SR (1984) Scavenger enzymes and resistance to oxygen-mediated damage in Trichinella spiralis. Mol Biochem Parasitol 10: 1−10.
• Kennedy MW, Harnett W, ed (2001) Parasitic Nematodes Molecular Biology Biochemistry and Immunology, CABI Publishing.
• Kinet JP (1989) Antibody-cell interactions: Fc receptors. Cell 57: 351−354.
• King CL, Medhat A, Malhotra I, Nafeh M, Helmy A, Khaudary J, Ibrahim S, El-Sherbiny M, Zaky S, Stupi RJ, Brustoski K, Shehata M, Shata MT (1996) Cytokine control of parasite-specific anergy in human urinary schistosomiasis. IL-10 modulates lymphocyte reactivity. J Immunol 156: 4715−4721.
• Kishimoto Y, Hiraiwa M, O’Brien JS (1992) Saposins: structure, function, distribution, and molecular genetics. J Lipid Res 33: 1255−1267.
• Kleemann R, Mischke R, Kapurniotu A, Brunner H, Bernhagen J (1998) Specific reduction of insulin disulfides by macrophage migration inhibitory factor (MIF) with glutathione and dihydrolipoamide: potential role in cellular redox processes. FEBS Lett 430: 191−196.
• Knight PA, Wright SH, Lawrence CE, Paterson YYW, Miller HRP (2000) Delayed expulsion of the nematode Trichinella spiralis in mice lacking the mucosal mast cellspecific granule chymase, mouse mast cell protease-1. J Exp Med 192: 1849−1856
• Knox DP (1994) Parasite enzymes and the control of roundworm and fluke infestation in domestic animals. Br Vet J 150: 319−337.
• Kong Y, Chung YB, Cho SY, Kang SY (1994) Cleavage of immunoglobulin G by excretory-secretory cathepsin Slike protease of Spirometra mansoni plerocercoid. Parasitology 109: 611−621.
• Kotze AC, McClure SJ (2001) Haemonchus contortus utilises catalase in defence against exogenous hydrogen peroxide in vitro. Int J Parasitol 31: 1563−1571.
• Kwatia MA, Botkin DJ, Williams DL (2000) Molecular and enzymatic characterization of Schistosoma mansoni thioredoxin peroxidase. J Parasitol 86: 908−915.
• Lackey A, James ER, Sakanari JA, Resnick SD, Brown M, Bianco AE, McKerrow JH (1989) Extracellular protease of Onchocerca. Exp Parasitol 68: 176−185.
• Lähteenmäki K, Kuusela P, Korhonen TK (2001) Bacterial plasminogen activators and receptors. FEMS Microbiol Rev 25: 531−552.
• Lee DL (1996) Why do some nematode parasites of the alimentary tract secrete acetylcholinesterase? Int J Parasitol 26: 499−508.
• Lee DL, Foster N (1995) Gastrointestinal nematodes and host gut motility. Helminthologia 32: 107−110.
• Lee DL, Ko RC, Yi XY, Yeung MH (1991) Trichinella spiralis: antigenic epitopes from the stichocytes detected in the hypertrophic nuclei and cytoplasm of the parasitized muscle fibre (nurse cell) of the host. Parasitology 102: 117−123.
• Lee JY, Cho PY, Kim TY, Kang SY, Song KY, Hong SJ (2002) Hemolytic activity and developmental expression of pore-forming peptide, clonorin. Biochem Biophys Res Commun 296: 1238−1244.
• Leid RW, Suquet CM, Bouver HG, Hinrichs DJ (1986) Interleukin inhibition by a parasite proteinase inhibitor, taeniaestatin. J Immunol 137: 2700−2702.
• Liebau E, Wildenburg G, Walter RD, Henkle-Duhrsen K (1994) A novel type of glutathione S-transferase in Onchocerca volvulus. Infect Immun 62: 4762−4767.
• Lim MJ, Chae HZ, Rhee SG, Yu DY, Lee KK, Yeom YI (1998) The type II peroxiredoxin gene family of the mouse: molecular structure, expression and evolution. Gene 216: 197−205.
• Linden J (2001) Molecular approach to adenosine receptors: receptor-mediated mechanisms of tissue protection. Annu Rev Pharmacol Toxicol 41: 775−787.
• Loukas A, Maizels RA (2000) Helminth C-type lectins and host-parasite interactions. Parasitol Today 16: 333−339.
• Loukas A, Mullin NP, Tetteh KK, Moens L, Maizels RM (1999) A novel C-type lectin secreted by a tissue-dwelling parasitic nematode. Curr Biol 9: 825−828.
• Loukas A, Doedens A, Hintz M, Maizels RM (2000) 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.
• Lu W, Egerton GL, Bianco AE, Williams SA (1998) Thioredoxin peroxidase from Onchocerca volvulus: a major hydrogen peroxide detoxifying enzyme in filarial parasites. Mol Biochem Parasitol 91: 221−235.
• Lun HM, Mak CH, Ko RC (2003) Characterization and cloning of metallo-proteinase in the excretory/secretory products of the infective stage larva of Trichinella spiralis. Parasitol Res 90: 27−37.
• Lustigman S, Brotman B, Huima T, Prince AM, McKerrow JH (1992) Molecular cloning and characterization of onchocystatin, a cysteine proteinase inhibitor of Onchocerca volvulus. J Biol Chem 267: 17339−17346.
• Machado DC, Horton D, Harrop R, Peachell PT, Helm BA (1996) Potential allergens stimulate the release of mediators of the allergic response from cells of mast cell lineage in the absence of sensitization with antigenspecific IgE. Eur J Immunol 26: 2972−2980.
• Maizels RM, Gomez-Escobar N, Gregory WF, Murray J, Zang X (2001) Immune evasion genes from filarial nematodes. Int J Parasitol 31: 889−898.
• Mak CH, Ko RC (1999) Characterization of endonuclease activity from excretory/secretory products of a parasite nematode Trichinella spiralis. Eur J Biochem 260: 477−481.
• Mak CH, Ko RC (2001) DNA-binding activity in the excretory-secretory products of Trichinella pseudospiralis. Parasitology 123: 301−308.
• Mak CH, Chung YYY, Ko RC (2000) Single-stranded endonuclease activity in the excretory-secretory products of Trichinella spiralis and Trichinella pseudospiralis. Parasitology 120: 527−533.
• Makita H, Nishimura M, Miyamoto K, Nakano T, Tanino Y, Hirokawa J, Nishihira J, Kawakami Y (1998) Effect of anti-macrophage migration inhibitory factor antibody on lipopolysaccharide-induced pulmonary neutrophil accumulation. Am J Respir Crit Care Med 158: 573−579.
• Manoury B, Gregory WF, Maizels RM, Watts C (2001) Bm- CPI-2, a cystatin homolog secreted by the filarial parasite Brugia malayi, inhibits class II MHC-restricted antigen processing. Curr Biol 11: 447−451.
• Marshall CJ (1993) Evolutionary relationships among the serpins. Philos Trans R Soc Lond Biol Sci 342: 101−119.
• Martzen MR, Geise GL, Hogan BJ, Peanasky RJ (1985) Ascaris suum: localization by immunochemical and fluorescent probes of host proteases and parasite proteinase inhibitors in cross-sections. Exp Parasitol 60: 139−149.
• Martzen MR, McMullen BA, Smith NE, Fujikawa K, Peanasky RJ (1990) Primary structure of the major pepsin inhibitor from the intestinal parasitic nematode Ascaris suum. Biochemistry 29: 7366−7372.
• Maruyama H, Nawa Y (1997) Strongyloides venezuelenzis: adhesion of adult worms to culture vessels by orally secreted mucosubstances. Exp Parasitol 85: 10−15.
• McCloskey MA, Fan Y, Luther S (1999) Chemotaxis of rat mast cells toward adenine nucleotides. J Immunol 163: 970−977.
• McDermott JR, Bartram RE, Knight PA, Miller HRP, Garrod DR, Grencis RK (2003) Mast cells disrupt epithelial barrier function during enteric nematode infection. Proc Natl Acad Sci USA 100: 7761−7766.
• McGonigle S, Curley GP, Dalton JP (1997) Cloning of peroxiredoxin, a novel antioxidant enzyme, from the helminth parasite Fasciola hepatica. Parasitology 115: 101−104.
• McGonigle S, Curley GP, Dalton JP (1998) Peroxiredoxins: a new antioxidant family. Parasitol Today 14: 139−145.
• McKerrow JH (1989) Parasite proteases. Exp Parasitol 68: 111−115.
• McKerrow JH, Sun E, Rosenthal PJ, Bouvier J (1993) The proteases and pathogenicity of parasitic protozoa. Annu Rev Microbiol 47: 821−853.
• McLaren DJ, Hockley DJ (1977) Blood flukes have a double outer membrane. Nature 269: 147–149.
• Mei H, LoVerde PT (1997) Schistosoma mansoni: the developmental regulation and immunolocalization of antioxidant enzymes. Exp Parasitol 86: 69−78.
• Mitchell GF (1989) Glutathione S-transferases – potential components of anti-schistosome vaccines? Parasitol Today 5: 34−37.
• Mkoji GM, Smith JM, Prichard RK (1988) Antioxidant systems in Schistosoma mansoni: correlation between susceptibility to oxidant killing and the levels of scavengers of hydrogen peroxide and oxygen free radicals. Int J Parasitol 18: 661−666.
• Moczoń T (1994) A cysteine proteinase in the cercariae Diplostomum pseudospathaceum (Trematoda Diplostomatidae). Parasitol Res 80: 680−683.
• Moczoń T (1996) A serine proteinase in the penetration glands of the hexacanths Hymenolepis diminuta (Cestoda, Cyclophyllidea). Parasitol Res 82: 67−71.
• Moczoń T, Wranicz M (1999) Trichinella spiralis: proteinases in the larvae. Parasitol Res 85: 47−58.
• Moerman DG (1999) A metalloprotease prepares the way. Curr Biol 9: R701−R703.
• Molinari JL, Mejia H, White AC Jr, Garrido E, Borgonio-VM, Baig S, Tato P (2000) Taenia solium: a cysteine protease secreted by metacestodes depletes human CD4 lymphocytes in vitro. Exp Parasitol 94: 133−142.
• Moncada DM, Kammanadiminti SJ, Chadee K (2003) Mucin and Toll-like receptors in host defense against intestinal parasites. Trends Parasitol 19: 305−311.
• Morales FC, Furtado DR, Rumjanek FD (2004) The N-terminus moiety of the cystatin SmCys from Schistosoma mansoni regulates its inhibitory activity in vitro and in vivo. Mol Biochem Parasitol 134: 65−73.
• Mosser DM (2003) The many faces of macrophage activation. J Leukoc Biol 73: 209−212.
• Mueller JF (1963) Parasite induced weight gain in mice. Ann N Y Acad Sci 113: 217−233.
• Mueller JF (1974) The biology of Spirometra. J Parasitol 60: 3−14.
• Nakagawa TY, Rudensky AY (1999) The role of lysosomal proteinases in MHC class II-mediated antigen processing and presentation. Immunol Rev 172: 121−129.
• Newlands GF, Skuce PJ, Knox DP, Smith WD (2001) Cloning and expression of cystatin, a potent cysteine protease inhibitor from the gut of Haemonchus contortus. Parasitology 122: 371−378.
• Nicklin MJ, Barrett AJ (1984) Inhibition of cysteine proteinases and dipeptidyl peptidase I by egg-white cystatin. Biochem J 223: 245−253.
• Nor ZM, Houston KM, Devaney E, Harnett W (1997) Variation in the nature of attachment of phosphorylcholine to excretory-secretory products of adult Brugia pahangi. Parasitology 114: 257−262.
• O’Connor RA, Jenson JS, Devaney E (2000) NO contributes to proliferative suppression in a murine model of filariasis. Infect Immun 68: 6101-6107.
• Okabe T, Mori H, Ohyama T (1997) Deoxyribonuclease secreted
• from an insectivorous plant Drosera adelae. Nucleic Acids Symp Ser 37: 127−128.
• O’Neill SM, Mills KHG, Dalton JP (2001) F. hepatica cathepsin L cysteine proteinase suppresses Bordetella pertusis-specific IFN-γ production in vivo. Parasite Immunol 23: 541−547.
• Osaki Y (1990) Ultrastructural studies on the plerocercoid of Spirometra erinacei in experimental sparganosis. Parasitol Res 76: 466−472.
• Osborne J, Devaney E (1999) Interleukin-10 and antigenpresenting cells actively suppress Th1 cells in BALB/c mice infected with the filarial parasite Brugia pahangi. Infect Immun 67: 1599−1605.
• Ou X, Thomas GR, Chacon MR, Tang L, Selkirk ME (1995) Brugia malayi: differential susceptibility to and metabolism of hydrogen peroxide in adults and microfilariae. Exp Parasitol 80: 530−540.
• Page AP, Hamilton AJ, Maizels RM (1992) Toxocara canis: monoclonal antibodies to carbohydrate epitopes of secreted (TES) antigens localize to different secretionrelated
• structures in infective larvae. Exp Parasitol 75: 56−71.
• Palanivel V, Posey C, Horauf AM, Solbach W, Piessens WF, Harn DA (1996) B-cell outgrowth and ligand-specific production of IL-10 correlate with Th2 dominance in certain parasitic diseases. Exp Parasitol 84: 168−177.
• Pancholi V (2001) Multifunctional α-enolase: its role in diseases. Cell Mol Life Sci 58: 902−920.
• Panesar TS (1981) The early phase of tissue invasion by Trichuris muris (nematoda: Trichuroidea). Z Parasitenkd 66: 163−166.
• Pastrana DV, Raghavan N, FitzGerald P, Eisinger SW, Metz C, Bucala R, Schleimer RP, Bickel C, Scott AL (1998) Filarial nematode parasites secrete a homologue of the human cytokine macrophage migration inhibitory factor. Infect Immun 66: 5955−5963.
• Pennock JL, Behnke JM, Bickle QD, Devaney E, Grencis RK, Isaac RE, Joshua GW, Selkirk ME, Zhang Y, Meyer DJ (1998) Rapid purification and characterization of l-dopachrome-methyl ester tautomerase (macrophagemigration-inhibitory factor) from Trichinella spiralis, Trichuris muris and Brugia pahangi. Biochem J 335: 495−498.
• Petitfrere E, Sartelet H, Aguie-Aguie G, Martiny L, Haye B (1996) Evidence for a TSH-controlled ectophosphotyrosine phosphatase in pig thyroid cultured cells. Biochem Biophys Res Commun 220: 746−753.
• Phares K (1996) An unusual host-parasite relationship: The growth hormone like factor from plerocercoids of spirometrid tapeworms. Int J Parasitol 26: 575−588.
• Phares K, Kubik J (1996) The growth factor from plerocercoids of Spirometra mansonoides is both a growth hormone agonist and a cysteine proteinase. J Parasitol 82: 210−215.
• Piedrafita D, Spithill TW, Dalton JP, Brindley PJ, Sandeman MR, Wood PR, Parsons JC (2000) Juvenile Fasciola hepatica are resistant to killing in vitro by free radicals compared with larvae of Schistosoma mansoni. Parasite Immunol 22: 287−295.
• Plow EF, Herren T, Redlitz A, Miles LA, Hoover-Plow JL (1995) The cell biology of the plasminogen system. FASEB J 9: 939−945.
• Polzer M, Conradt U (1994a) Identification and partial characterization of the proteases from different developmental stages of Schistocephalus solidus (Cestoda: Pseudophyllidea) Int J Parasitol 24: 967−973.
• Polzer M, Overstreet RM, Taraschewski H (1994b) Proteinase activity in the plerocercoid of Proteocephalus ambloplitis (Cestoda). Parasitology 109: 209−213.
• Potempa J, Korzus E, Travis J (1994) The serpin family of proteinase inhibitors: structure, function and regulation. J Biol Chem 269: 15957−15600.
• Pritchard DI, Brow A, Toutant J-P (1994) The molecular forms of acetylcholinesterase from Necator americanus (Nematoda), a hookworm parasite of the human intestine. Eur J Biochem 219: 317−323.
• Prowse RK, Chaplin P, Clem Robinson H, Spithill TW (2002) Fasciola hepatica cathepsin L suppresses lymphocyte proliferation in vitro and modulates surface CD4 expression of human and ovine T cells. Parasite Immunol 24: 57−66.
• Rao UR, Salinas G, Mehta K, Klei TR (2000) Identification and localization of glutathione S-transferase as a potential target enzyme in Brugia species. Parasitol Res 86: 908−915.
• Redegeld FA, Caldwell CC, Sitkovsky MV (1999) Ecto-protein kinases: ecto-domain phosphorylation as a novel target for pharmacological manipulation? Trends Pharmacol Sci 20: 453−459.
• Redlitz A, Fowler BJ, Plow EF, Miles LA (1995) The role of an enolase-related molecule in plasminogen binding to cells. Eur J Biochem 227: 407−415.
• Reed MB, Strugnell RA, Panaccio M, Spithill TW (2000) A novel member of the NK-lysin protein family is developmentally regulated and secreted by Fasciola hepatica. Mol Biochem Parasitol 105: 297−303.
• Rhoads ML (1983) Trichinella spiralis: identification and purification of superoxide dismutase. Exp Parasitol 56: 41−54.
• Rhoads ML (1984) Secretory cholinesterases of nematodes: possible functions in the host-parasite relationship. Trop Veterinarian 2: 3−10.
• Rhoads ML, Fetterer RH (1995) Developmentally regulated secretion of cathepsin L-like cysteine proteases by Haemonchus contortus. J Parasitol 81: 505−512.
• Rhoads ML, Fetterer RH (1996) Extracellular matrix degradation by Haemonchus contortus. J Parasitol 82: 379−383.
• Rhoads ML, Fetterer RH, Hill DE, Urban JF Jr (2000) Trichuris suis: A secretory chymotrypsin/elastase inhibitor with potential as an immunomodulator. Exp Parasitol 95: 36−44.
• Riese RJ, Chapman HA (2000) Cathepsins and compartmentalization in antigen presentation. Curr Opin Immunol 12: 107−113.
• Rojas J, Rodriguez-Osorio M, Gomez-Garcia V (1997) Immunological characteristics and localization of the Trichinella spiralis glutathione S-transferase. J Parasitol 83: 630−635.
• Rzepczyk CM, Bishop CJ (1984) Immunological and structural aspects of the cell mediated killing of Dirofilaria immitis microfilariae. Parasite Immunol 6: 443−457.
• Sajid M, McKerrow JH (2002) Cysteine proteases of parasitic organisms. Mol Biochem Parasitol 120: 1−21.
• Satoh Y, Ishikawa K, Oomori Y, Takeda S, Ono K (1992) Bethanechol and a G-protein activator, NaF/AlCl3, induce secretory response in Paneth cells of mouse intestine. Cell Tissue Res 269: 213−220.
• Sayed AA, Williams DL (2004) Biochemical characterization of 2-Cys peroxiredoxins from Schistosoma mansoni. J Biol Chem 279: 26159−26166.
• Schierack P, Lucius R, Sonnenburg B, Schilling K, Hartmann S (2003) Parasite-specific immunomodulatory functions of filarial cystatin. Infect Immun 71: 2422−2429.
• Schonemeyer A, Lucius R, Sonnenburg B, Brattig N, Sabat R, Schilling K, Bradley J, Hartmann S (2001) Modulation of human T cell responses and macrophage functions by onchocystatin, a secreted protein of the filarial nematode Onchocerca volvulus. J Immunol 167: 3207−3215.
• Schuette CG, Pierstorff B, Huettler S, Sandhoff K (2001) Sphingolipid activator proteins: proteins with complex function in lipid degradation and skin biogenesis. Glycobiology 11: 81R−90R.
• Selkirk ME, Hussein AS, Chambers AE, Goulding D, Gares MP, Vasquez-Lopez C, Garate T, Parkhouse RM, Gounaris K (2004) Trichinella spiralis secretes a homologue of prosaposin. Mol Biochem Parasitol 135: 49−56.
• Seo MS, Kang SW, Kim K, Baines IC, Lee TH, Rhee SG (2000) Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J Biol Chem 275: 20346−20352.
• Sharp SE, Phares CK, Heidrick ML (1982) Immunological aspects associated with suppression of hormone levels in rats infected with plerocercoids of Spirometra mansonoides (Cestoda). J Parasitol 686: 993−998.
• Shaw RJ, McNeill MM, Maass DR, Hein WR, Barber TK, Wheeler M, Morris CA, Shoemaker CB (2003) Identification and characterisation of an aspartyl protease inhibitor homologue as a major allergen of Trichostrongylus colubriformis. Int J Parasitol 33: 1233−1243.
• Shenai BR, Sijvali PS, Singh A, Rosenthal PJ (2000) Characterization of native and recombinant falcipain-2, a principal trophozoite cysteine protease and essential hemoglobinase of Plasmodium falciparum. J Biol Chem 275: 29000−29010.
• Shi GP, Bryant RA, Riese R, Verhelst S, Driessen C, Li Z, Bromme D, Ploegh HL, Chapman HA (2000) Role for cathepsin F in invariant chain processing and major histocompatibility complex class II peptide loading by macrophages. J Exp Med 191: 1177−1186.
• Simpson AJ, Singer D, McCutchan TF, Sacks DL, Sher A (1983) Evidence that schistosome MHC antigens are not synthesized by the parasite but are acquired from the host as intact glycoproteins. J Immunol 131: 962−965.
• Skelly PJ, Shoemaker CB (1996) Rapid appearance and asymmetric distribution of glucose transporter SGTP4 at the apical surface of intramammalian-stage Schistosoma mansoni. Proc Natl Acad Sci USA 93: 3642−3646.
• Smith NC, Bryant C (1989) The effect of antioxidants on the rejection of Nippostrongylus brasiliensis. Parasite Immunol 11: 161−167.
• Smith VP, Selkirk ME, Gounaris K (2000) A reversible protein phosphorylation system is present at the surface of the infective larvae of the parasitic nematode Trichinella spiralis. FEBS Lett 483: 104−108.
• Soeda S, Hiraiwa M, O’Brien JS, Kishimoto Y (1993) Binding of cerebrosides and sulfatides to saposins A–D. J Biol Chem 268: 18519−18523.
• Song CY, Chappel CL (1993) Purification and partial characterization of cysteine proteinase from Spirometra mansoni plerocercoids. J Parasitol 79: 517−524.
• Specian RD, Neutra MR (1980) Mechanism of rapid mucus secretion in goblet cells stimulated by acetylcholine. J Cell Biol 85: 629−640.
• Spolski RJ, Thomas PG, See EJ, Mooney KA, Kuhn RE (2002) Larval Taenia crassiceps secretes a protein with characteristics of murine IFN-γ. Parasitol Res 88: 431−438.
• Stassens P, Bergum PW, Gansemans Y, Jespers L, Laroche Y, Huang S, Maki S, Messens J, Lauwereys M, Cappello M, Hotez PJ, Lasters I, Vlasuk GP (1996) Anticoagulant repertoire of the hookworm Ancylostoma caninum. Proc Natl Acad Sci USA 93: 2149−2154.
• Stepek G, Houston KM, Goodridge HS, Devaney E, 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 128: 91−98.
• Stewart GL (1983) Pathophysiology of the muscle phase. In Trichinella and Trichinosis (Campbell WC, ed) pp 241−264, Plenum Publishing Corporation, New York Stöcker W, Zwilling R (1995) Astacin. Methods Enzymol 248: 305−325.
• Stöcker W, Grams F, Baumann U, Reinemer P, Gomis- Ruth FX, McKay DB, Bode W (1995) The metzincinstopological and sequential relations between the tacins, adamalysins, serralysins, and matrixins (collagenases) define a superfamily of zinc-peptidases. Protein Sci 4: 823−840.
• Street NE, Mosmann TR (1991) Functional diversity of T lymphocytes due to secretion of different cytokine patterns. FASEB J 5: 171−177.
• Sugimoto H, Taniguchi M, Nakagawa A, Tanaka I, Suzuki M, Nishihira J (1999) Crystal structure of human ddopachrome tautomerase, a homologue of macrophage migration inhibitory factor, at 1.54 Å resolution. Biochemistry 38: 3268−3279.
• Swan DG, Phillips K, Tait A, Shiels BR (1999) Evidence for localisation of a Theileria parasite AT hook DNA-binding protein to the nucleus of immortalised bovine host cells. Mol Biochem Parasitol 101: 117−129.
• Takahasi Y, Homan W, Lim PL (1993) Ultrastructural localization of the phosphorylcholine-associated antigen in Trichinella spiralis. J Parasitol 79: 604−609.
• Takeya H, Nishida S, Miyata T, Kawada S, Saisaka Y, Morita T, Iwanaga S (1992) Coagulation factor X activating enzyme from Russell’s viper venom (RVV-X). A novel metalloproteinase with disintegrin (platelet aggregation inhibitor)-like and C-type lectin-like domains. J Biol Chem 267: 4109−4117.
• Tamashiro WK, Rao M, Scott AL (1987) Proteolytic cleavage of IgG and other protein substrates by Dirofilaria immitis microfilarial enzymes. J Parasitol 73: 149−154.
• Tan TH, Edgerton SA, Kumari R, McAlister MS, Roe SM, Nagl S, Pearl LH, Selkirk ME, Bianco AE, Totty NF, Engwerda C, Gray CA, Meyer DJ (2001) Macrophage migration inhibitory factor of the parasitic nematode Trichinella spiralis. Biochem J 357: 373−383.
• Tanihata T (1996) Effects of excretory and secretory products from plerocercoids of Spirometra erinaceieuropaei on tumor necrosis factor-α and interleukin-6 mRNA levels in murine peritoneal macrophages. J Yonago Med Assoc 47: 140−147.
• Tarleton RL, Kemp WM (1981) Demonstration IgG-Fc and C3 receptors on adult Schistosoma mansoni. J Immunol 125: 379−384.
• Taylor JB, Vidal A, Torpier G, Meyer DJ, Roitsch C, Balloul JM, Southan C, Sondermeyer P, Pemble S, Lecocq JP, Capron A, Ketterer B (1988) The glutathione transferase activity and tissue distribution of a cloned Mr28K protective antigen of Schistosoma mansoni. EMBO J 7: 465-472.
• Todorova VK, Stoyanow DI (2000) Partial characterization of serine proteinases secreted by adult Trichinella spiralis. Parasitol Res 86: 684−687.
• Todorova VK, Knox DP, Kennedy MV (1995) Proteinase in the excretory/secretory products (ES) of adult Trichinella spiralis. Parasitology 111: 201−208.
• Tort J, Brindley PJ, Knox D, Wolfe KH, Dalton JP (1999) Proteinase and associated genes of parasitic helminths. Adv Parasitol 43: 161−266.
• Tsuboi T, Oka K, Hirai K, Torii M (1992) Effects of proteinase inhibitors on liver cell growth stimulating activity and cytosolic calcium concentration by the infection of plerocercoids of Spirometra erinacei. Jpn J Parasitol 41: (Suppl) 64.
• Tsuji N, Kasuga-Aoki H (2001) Cloning and characterisation of a peroxiredoxin from the swine roundworm Ascaris suum. Int J Parasitol 30: 125−128.
• Tume CB, Ngu JL, McKerrow JL, Seigel J, Sun E, Barr PJ, Bathurst I, Morgan G, Nkenfou C, Asonganyi T, Lando G (1997) Characterization of a recombinant Onchocerca volvulus antigen (Ov33) produced in yeast. Am J Trop Med Hyg 57: 626−633.
• Verdot L, Lalmanach G, Vercruysse V, Hartmann S, Lucius R, Hoebeke J, Gauthier F, Vray B (1996) Cystatins up-regulate nitric oxide release from IFN-γ-activated mouse peritoneal macrophages. J Biol Chem 271: 28077−28081.
• Vray B, Hartmann S, Hoebeke J (2002) Immunomodulatory properties of cystatins. Cell Mol Life Sci 59: 1503–1512.
• Wada K, Sato H, Kinoh H, Kajita M, Yamamoto H, Seiki M (1998) Cloning of three Caenorhabditis elegans genes potentially encoding novel matrix metalloproteinases. Gene 211: 57−62.
• Walter J, Schnolzer M, Pyerin W, Kinzel V, Kubler D (1996) Induced release of cell surface protein kinase yields CK1- and CK2-like enzymes in tandem. J Biol Chem 271: 111−119.
• Wang H-R, Tanihata T, Fukumoto S, Hirai K, Phares CK (1995) Immunohistochemical localization of a 27 kDa protein in the plerocercoids of Spirometra erinacei. Jpn J Parasitol 44: 6−11.
• Weintraub H (1993) The MyoD family and myogenesis: redundancy, networks and thresholds. Cell 75: 1241−1244.
• Weis WI, Taylor ME, Drickamer K (1998) The C-type lectin superfamily in the immune system. Immunol Rev 163: 19−34.
• Wharton D (1983) The production and functional morphology of helminth egg-shells. Parasitology 786: 85−97.
• White AC Jr, Molinari JL, Pillai AV, Rege AA (1992) Detection and preliminary characterization of Taenia solium metacestode proteases. J Parasitol 78: 281−287.
• Wijffels GL, Sexton JL, Salvatore L, Pettitt JM, Humphris DC, Panaccio M, Spithill TW (1992) Primary sequence heterogeneity and tissue expression of glutathione Stransferases of Fasciola hepatica. Exp Parasitol 74: 87−99.
• Wilson RA, Barnes PE (1979) Synthesis of macromolecules by the epithelial surfaces of Schistosoma mansoni: an autoradiographic study. Parasitology 78: 295−310.
• Wright KA (1979) Trichinella spiralis: an intracellular parasite in the intestinal phase. J Parasitol 65: 441−445.
• Wu Y, Adam R, Williams SA, Bianco AE (1996) Chitinase genes expressed by infective larvae of the filarial nematodes, Acanthocheilonema viteae and Onchocerca volvulus. Mol Biochem Parasitol 75: 207−219.
• Yan L, Leontovich A, Fei K, Sarras MP Jr (2000) Hydra metalloproteinase 1: a secreted astacin metalloproteinase whose apical axis expression is differentially regulated during head regeneration. Dev Biol 219: 115−128. Yasumasu S, Yamada K, Akasaka K, Mitsunaga K, Iuchi I, Shimada H, Yamagami K (1992) Isolation of cDNAs for LCE and HCE, two constituent proteases of the hatch ing enzyme of Oryzlas latipes, and concurrent expression of their mRNAs during development. Dev Biol 153: 250−258.
• Yatsuda AP, Krijgsveld J, Cornelissen AW, Heck AJ, de Vries E (2003) Comprehensive analysis of the secreted proteins of the parasite Haemonchus contortus reveals extensive sequence variation and differential immune recognition. J Biol Chem 278: 16941−16951.
• Zaborina O, Li X, Cheng G, Kapatral V, Chakrabarty AM (1999) Secretion of ATP-utilizing enzymes, nucleoside diphosphate kinase and ATPase, by Mycobacterium bovis BCG: sequestration of ATP from macrophage P2Z receptors? Mol Microbiol 31: 1333−1343.
• Zang X, Maizels RM (2001) Serine proteinase inhibitors from nematodes and the arms race between host and pathogen Trends Biochem Sci 26: 191−197.
• Zang X, Yazdanbakhsh M, Jiang H, Kanost MR, Maizels RM (1999) A novel serpin expressed by the bloodborne microfilariae of the parasitic nematode Brugia malayi inhibits human neutrophil serine proteinases. Blood 94: 1418−1428.
• Zelck UE, Von Janowsky B (2004) Antioxidant enzymes in intramolluscan Schistosoma mansoni and ROS-induced changes in expression. Parasitology 128: 493−501.