Skip to main content
SpringerLink
Log in

The role of free oxygen radicals in the expulsion of primary infections ofNippostrongylus brasiliensis

  • Review Article
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

The many and varied pathological, immunological and physiological manifestations of infection withNippostrongylus brasiliensis may be unified by considering the role of leukocyte-generated free oxygen radicals in worm expulsion. Aside from directly damaging the adult stage ofN. brasiliensis and possibly leading to its elimination from the small intestine, free radicals may also damage intestinal cells, thereby contributing to the gut pathology characteristic of infection. γ-Interferon (and possibly tumour necrosis factor) may be involved in the initiation of free radical generation in response toN. brasiliensis and may also contribute to various side effects of infection such as hypertriglyceridaemia and cachexia. γ-Interferon may initiate free radical generation via the agency of protein kinase C, an enzyme that can induce various additional responses including lysosomal enzyme and amine secretion and arachidonic acid metabolism. The possible interactions between these mediators and free radicals are subtle and diverse and may profoundly affect the course of infection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aggarwal BB, Eassalu TE, Hass PE (1985) Characterization of receptors for human tumour necrosis factor and their regulation by γ-interferon. Nature 318:665–667

    Google Scholar 

  • Babior BM (1984) The respiratory burst of phagocytes. J Clin Invest 73:599–601

    Google Scholar 

  • Bachwich PR, Chensue SW, Larrick JW, Kunkel SL (1986) Tumour necrosis factor stimulates interleukin 1 and prostaglandin E2 production in resting macrophages. Biochem Biophys Res Commun 136:94–101

    Google Scholar 

  • Badger AM, Hutchman JS, Sung C-P, Bugelski PJ (1987) Activation of rat alveolar macrophages by gamma interferon to inhibitToxoplasma gondii in vitro. J Leukocyte Biol 42:447–454

    Google Scholar 

  • Badwey JA, Karnovsky ML (1980) Active oxygen species and the functions of phagocytic leukocytes. Annu Rev Biochem 49:695–726

    Google Scholar 

  • Bass DA, Szejda P (1979) Eosinophils versus neutrophils in host defence. Kiling of newborn larvae ofTrichinella spiralis by human granulocytes in vitro. J Clin Invest 64:1415–1422

    Google Scholar 

  • Becton DL, Adams DO, Hamilton TA (1985) Characterization of protein kinase C activity in interferon gamma treated murine peritoneal macrophages. J Cell Physiol 125:485–491

    Google Scholar 

  • Berridge MJ (1986) Intracellular signalling through inositol trisphosphate and diacylglycerol. Biol Chem Hoppe Seyler 367:447–456

    Google Scholar 

  • Berridge MJ (1987) Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu Rev Biochem 56:159–194

    Google Scholar 

  • Berridge MJ, Irvine RF (1984) Inositol trisphosphate a novel second messenger in cellular signal transduction. Nature 312:315–321

    Google Scholar 

  • Berton G, Zeni L, Cassatella MA, Rossi F (1986) Interferon-γ is able to enhance the oxidative metabolism of human neutrophils. Biochem Biophys Res Commun 138:1276–1282

    Google Scholar 

  • Beutler B, Cerami A (1986) Cachectin and tumour necrosis factor as two sides of the same biological coin. Nature 320:584–588

    Google Scholar 

  • Block KJ, Wilson RJM (1968) Homocytotropic antibody response in the rat infected with the nematode,Nippostrongylus brasiliensis: III. Characteristics of the antibody. J Immunol 100:629–636

    Google Scholar 

  • Boraschi D, Censini S, Bortalini M, Tagliabue A (1985) Regulation of arachidonic acid metabolism by immune and nonimmune interferons. J Immunol 135:502–505

    Google Scholar 

  • Boveris A, Sies H, Martino EE, Docampo R, Turrens JF, Stoppani AOM (1980) Deficient metabolic utilization of hydrogen peroxide inTrypanosoma cruzi. Biochem J 188:643–648

    Google Scholar 

  • Bronner CC, Valle A, Gies JP, Landry Y (1986) Dual effect of phorbol ester on serosal mast cell exocytosis — interactions between ionic gradients and protein kinase C. Ann Inst Pasteur/Immunol D 137:249–262

    Google Scholar 

  • Buchan JD, Armstrong DA (1978) The radiolysis of glyceralde hyde-3-phosphate dehydrogenase. Int J Radiat Biol 33:409–414

    Google Scholar 

  • Buchmüller-Rouiller Y, Mauël J (1986) correlation between enhanced oxidative metabolism and leishmanicidal activity in activated macrophages from healer and non-healer mouse strains. J Immunol 136:3884–3890

    Google Scholar 

  • Cadet J, Teoule R (1978) Comparative study of oxidation of nucleic acid components by hydroxyl radical, singlet oxygen and superoxide anion radicals. Photochem Photobiol 28:661–667

    Google Scholar 

  • Carp H, Janoff A (1980) Potential mediator of inflammation. Phagocyte-derived oxidants suppress the elastase-inhibitory capacity of alpha1-protease inhibitor in vitro. J Clin Invest 66:987–995

    Google Scholar 

  • Celada A, Schreiber RD (1986) Role of protein kinase C and intracellular calcium mobilization in the induction of macrophage tumoricidal activity by interferon-γ. J Immunol 137:2373–2379

    Google Scholar 

  • Channon JY, Blackwell JM (1985a) A study of the sensitivity ofLeishmania donovani promastigotes and amastigotes to hydrogen peroxide: I. Differences in sensitivity correlate with parasite-mediated removal of hydrogen peroxide. Parasitology 91:197–206

    Google Scholar 

  • Channon JY, Blackwell JM (1985b) A study of the sensitivity ofLeishmania donovani promastigotes and amastigotes to hydrogen peroxide: II. Possible mechanisms involved in protective H2O2 scavenging. Parasitology 91:207–217

    Google Scholar 

  • Chensue SW, Kunkel SL, Higashi GI, Ward PA, Boros DL (1983) Production of superoxide anion, prostaglandins and hydroxyeicosatetraenoic acids from macrophages from hypersensitivity-type (Schistosoma mansoni egg) and foreign-body-type granulomas. Infect Immun 42:1116–1125

    Google Scholar 

  • Chensue SW, Quinlan L, Higashi G, Kunkel SL (1984) Role of oxygen reactive species inSchistosoma mansoni egg-induced granulomatous inflammation. Biochem Biophys Res Commun 122:184–190

    Google Scholar 

  • Chensue SW, Ellul DA, Spengler M, Higashi GI, Kunkel SL (1985) Dynamics of arachidonic acid metabolism in macrophages from delayed-type hypersensitivity (Schistosoma mansoni egg) and foreign-body-type granulomas. J Leukocyte Biol 38:671–686

    Google Scholar 

  • Chio KS, Tappel AL (1969) Inactivation of ribonuclease and other enzymes by peroxidising lipids and by malonyldialdehyde. Biochemistry 8:2827–2832

    Google Scholar 

  • Clark IA, Cowden WB (1985) Antimalarials. In: Sies H (ed) Oxidative stress. Academic, London, pp 131–149

    Google Scholar 

  • Clark IA, Hunt NH (1983) Evidence for reactive oxygen intermediates causing hemolysis and parasite death in malaria. Infect Immun 39:1–6

    Google Scholar 

  • Clark IA, Hunt NH (1986) Increased production of arachidonate metabolites by peritoneal cells of mice infected withPlasmodium vinckei vinckei. Aust J Exp Biol Med Sci 64:415–418

    Google Scholar 

  • Clark IA, Cowden WB, Butcher GA (1983) Free oxygen radical generators as antimalarial drugs. Lancet I:234

    Google Scholar 

  • Clark IA, Hunt NH, Cowden WB, Maxwell LW, Mackie EJ (1984) Radical-mediated damage to parasites and erythrocytes inPlasmodium vinckei-infected mice after injection of t-butylhydroperoxide. Clin Exp Immunol 56:524–530

    Google Scholar 

  • Clark IA, Cowden WB, Hunt NH (1985) Free radical induced pathology. Med Res Rev 5:297–332

    Google Scholar 

  • Clark IA, Hunt NH, Cowden WB (1986) Oxygen-derived free radicals in the pathogenesis of parasitic disease. Adv Parasitol 25:1–44

    Google Scholar 

  • Clark IA, Chaudri G, Thumwood CM, Hunt NH, Cowden WB (1987a) Free radicals in malaria immunopathology. In: Rice-Evans C (ed) Free radicals, oxidant stress and drug action. Richelieu, London, pp 237–255

    Google Scholar 

  • Clark IA, Hunt NH, Butcher GA, Cowden WB (1987b) Inhibition of murine malaria (Plasmodium chabaudi) in vivo by recombinant interferon-γ or tumour necrosis factor and its enhancement by butylated hydroxyanisole. J Immunol 139:3493–3496

    Google Scholar 

  • Collart MA, Belin D, Vassalli J-D, deKossodo S, Vassalli P (1986) γ-Interferon enhances macrophage transcription of the tumour necrosis factor/cachectin, interleukin 1 and urokinase genes, which are controlled by short-lived repressors. J Exp Med 164:2113–2116

    Google Scholar 

  • Conn PJ, Sanderbush E (1985) Serotonin-stimulated phosphoinositide turnover — mediation by the S-2 binding site in rat cerebral cortex but not subcortical regions. J Pharmacol Exp Ther 234:195–203

    Google Scholar 

  • Cox JA, Jeng AY, Sharkey NA, Blumberg PM, Tauber AI (1985) Activation of the human neutrophil nicotinamide adenine dinucleotide phosphate (NADPH)-oxidase by protein kinase C. J Clin Invest 76:1932–1938

    Google Scholar 

  • Crowle PK (1983) Mucosal mast-cell reconstitution andNippostrongylus brasiliensis rejection by w/wv mice. J Parasitol 69:66–69

    Google Scholar 

  • Curnutte JT (1985) Activation of human neutrophil nicotinamide adenine dinucleotide phosphate, reduced (triphosphopyridine nucleotide, reduced) oxidase by arachidonic acid in a cell-free system. J Clin Invest 75:1740–1743

    Google Scholar 

  • Curnutte JT, Badwey JA, Robinson JM, Karnovsky MJ, Karnovsky ML (1984) Studies on the mechanism of superoxide release from human neutrophils stimulated with arachidonate. J Biol Chem 259:11851–11857

    Google Scholar 

  • Dale MM, Penfield A (1984) Synergism between phorbol ester and A23187 in superoxide production by neutrophils. FEBS Lett 175:170–172

    Google Scholar 

  • deChaffoy de Courcelles D, Leysen JE, deClerk F, Van Belle H, Janssen PA (1985) Evidence that phospholipid turnover is the signal transducing system coupled to serotonin S-2 receptor sites. J Biol Chem 260:7603–7608

    Google Scholar 

  • Della Bianca V, Grzeskowiak M, Cassatella MA, Zeni L, Rossi F (1986) Phorbol 12-myristate 13-acetate potentiates the respiratory burst while it inhibits phosphoinositide hydrolysis and calcium mobilization by formyl-methionyl-leucyl-phenylalanine in human neutrophils. Biochem Biophys Res Commun 135:556–565

    Google Scholar 

  • Dewald BT, Payne TG, Baggiolini M (1984) Activation of NADPH oxidase of human neutrophils. Potentiation of chemotactic peptide by a diacylglycerol. Biochem Biophys Res Commun 125:367–373

    Google Scholar 

  • Dineen JK, Kelly JD (1973) Expulsion ofNippostrongylus brasiliensis from the intestine of rats: the role of a cellular component derived from bone marrow. Int Arch Allergy Appl Immunol 45:759–766

    Google Scholar 

  • Dineen JK, Kelly JD (1976) The levels of prostaglandins in the small intestine of rats during primary and secondary infection withNippostrongylus brasiliensis. Int Arch Allergy Appl Immunol 51:429–440

    Google Scholar 

  • Dockrell HM, Playfair JHL (1983) Killing of blood-stage murine malaria parasites by hydrogen peroxide. Infect Immun 39:456–459

    Google Scholar 

  • Dockrell HM, Playfair JHL (1984) Killing ofPlasmodium yoelii by enzyme-induced products of the oxidative burst. Infect Immun 43:451–456

    Google Scholar 

  • Dockrell HM, Alavi A, Playfair JHL (1986) Changes in oxidative burst capacity during murine malaria and the effect of vaccination. Clin Exp Immunol 66:37–43

    Google Scholar 

  • Dohlstein M, Sjögren HO, Carlson R (1986) Histamine inhibits interferon-γ production via suppression of interleukin 2 synthesis. Cell Immunol 101:493–501

    Google Scholar 

  • Domingo EO, Warren KS (1967) The inhibition of granuloma formation aroundSchistosoma mansoni eggs: II. Thymectomy. Am J Pathol 51:756–767

    Google Scholar 

  • Dooley MM, Pryor WA (1982) Free radical pathology: inactivation of human α-1-proteinase inhibitor by products from reaction of nitrogen dioxide with hydrogen peroxide and the etiology of emphysema. Biochem Biophys Res Commun 106:981–987

    Google Scholar 

  • Duncombe VM, Bolin TD, Davis AE, Kelly JD (1981) Delayed expulsion of the nematodeNippostrongylus brasiliensis from rats on a low protein diet — the role of a marrow derived component. Am J Clin Nutr 34:400–403

    Google Scholar 

  • Egwang TG, Befus AD, Gauldie J (1985) Activation of alveolar macrophages following infection with the parasitic nematodeNippostrongylus brasiliensis. Immunology 54:581–588

    Google Scholar 

  • Esparza I, Mannel D, Ruppel A, Falk W, Krammer P (1987) Interferon-γ and lymphotoxin or tumour necrosis factor act synergistically to induce macrophage killing of tumour cells and schistosomula ofSchistosoma mansoni. J Exp Med 166:589–594

    Google Scholar 

  • Fantone JC, Kinnes DA (1983) Prostaglandin E1 and prostaglandin I2 modulation of superoxide production by human neutrophils. Biochem Biophys Res Commun 113:506–512

    Google Scholar 

  • Fantone JC, Ward PA (1982) Role of oxygen-derived free radicals and metabolites in leukocyte-dependent inflammatory reactions. Am J Pathol 107:397–417

    Google Scholar 

  • Fantone JC, Marasco WA, Elgas LJ, Ward PA (1984) Stimulus specificity of prostaglandin inhibition of rabbit polymorphonuclear leukocyte lysosomal enzyme release and superoxide anion production. Am J Pathol 115:9–18

    Google Scholar 

  • Fantozzi R, Brunelleschi S, Giuliattini L, Blandina P, Masini E, Cavallo G, Mannaioni PF (1985) Mast cell and neutrophil interactions: a role for superoxide anion and histamine. Agents Actions 16:260–264

    Google Scholar 

  • Feldman GM, Naples JM, Seed JL, Bueding E (1985) Effects of anethole dithiolthione and 2(3)-tert-butyl-4-hydroxyanisole on schistosome granuloma formation. Parasite Immunol 7:567–574

    Google Scholar 

  • Ferguson A, Jarrett EEE (1975) Hypersensitivity reactions in the small intestine: 1. Thymus dependence of experimental ‘partial villous atrophy’. Gut 16:114–117

    Google Scholar 

  • Fligiel SEG, Lee EC, McCoy JP, Johnson KJ, Varani J (1984) Protein degradation following treatment with hydrogen peroxide. Am J Pathol 115:418–425

    Google Scholar 

  • Flohé L, Beckmann R, Giertz H, Loschen G (1985) Oxygencentred free radicals as mediators of inflammation. In: Sies H (ed) Oxidative stress. Academic, New York, pp 403–435

    Google Scholar 

  • Freeman BA, Crapo JD (1982) Free radicals and tissue injury. Lab Invest 47:412–426

    Google Scholar 

  • Fujita I, Irita K, Minakami S (1984) Diacylglycerol, 1-oleoyl-2-acetyl-glycerol, stimulates superoxide generation from human neutrophils. Biochem Biophys Res Commun 120:318–324

    Google Scholar 

  • Fujita I, Takeshige K, Minakami S (1986) Inhibition of neutrophil superoxide formation by 1-(5-iso-quinolinesulfonyl)-2-methylpiperazine (H-7), an inhibitor of protein kinase C. Biochem Pharmacol 35:4555–4562

    Google Scholar 

  • Gerard C, McPhail LC, Marfat A, Stimler-Gerard NP, Bass DA, McCall CE (1986) Role of protein kinases in stimulation of human polymorphonuclear leukocyte oxidative metabolism by various agonists — differential effects of a novel protein kinase inhibitor. J Clin Invest 77:61–65

    Google Scholar 

  • Gerber HCh, Hörchner F, Zander B (1976) Immune mechanism of rats onNippostrongylus brasiliensis in vitro: I. The influence of humoral and secretory antibodies and of mast cells. Z Parasitenkd 50:57–66

    Google Scholar 

  • Grencis RK, Riedlinger J, Wakelin D (1987) Lymphokine production by T cells generated during infection withTrichinella spiralis. Int Arch Allergy Appl Immunol 83:92–95

    Google Scholar 

  • Gutteridge JMC (1982) Fate of oxygen free radicals in extracellular fluids. Biochem Soc Trans 10:72–73

    Google Scholar 

  • Halliwell B, Gutteridge JMC (1985) Free radicals in biology and medicine. Oxford University Press, Oxford

    Google Scholar 

  • Ham EA, Soderman DD, Zanetti ME, Dougherty HW, McCauley E, Kuehl FA Jr (1983) Inhibition by prostaglandins of leukotriene B4 release from activated neutrophils. Proc Natl Acad Sci USA 80:4349–4353

    Google Scholar 

  • Hamilton TA, Adams DO (1987) Molecular mechanisms of signal transduction in macrophages. Immunol Today 8:151–158

    Google Scholar 

  • Hamilton TA, Becton DL, Somers SD, Gray PW, Adams DO (1985a) Interferon-γ modulates protein kinase C activity in murine peritoneal macrophages. J Biol Chem 260:1378–1381

    Google Scholar 

  • Hamilton TA, Rigsbee JE, Scott WA, Adams DO (1985b) Gannma interferon enhances the secretion of arachidonic acid metabolites from murine peritoneal macrophages stimulated with phorbol diesters. J Immunol 134:2631–2636

    Google Scholar 

  • Hayakawa T, Suzuki K, Suzuki S, Andrews PC, Babior BM (1986) A possible role for protein phosphorylation in the activation of the respiratory burst in human neutrophils. Evidence from studies with cells from patients with chronic granulomatous disease. J Biol Chem 261:9109–9115

    Google Scholar 

  • Henderson WR, Chi EY, Jong EC, Klebanoff J (1986) Mast cell-mediated toxicity to schistosomula ofSchistosoma mansoni: potentiation by exogenous peroxidase. J Immunol 137:2695–2699

    Google Scholar 

  • Herrmann F, Cannistra SA, Levine H, Griffin JD (1985) Expression of interleukin 2 receptors and binding of interleukin 2 by gamma interferon-induced human leukemic and normal monocytic cells. J Exp Med 162:1111–1116

    Google Scholar 

  • Holter W, Grunow R, Stockinger H, Knapp W (1986) Recombinant interferon-gamma induces interleukin 2 receptors on human peripheral blood monocytes. J Immunol 136:2171–2178

    Google Scholar 

  • Jacobson RH, Reed ND (1974) The immune response of congenitally athymic mice to the intestinal nematode,Nippostrongylus brasiliensis. Proc Soc Exp Biol Med 147:667–670

    Google Scholar 

  • Jacobson RH, Reed ND (1976) The requirement of thymus competence for both humoral and cell-mediated steps in expulsion ofNippostrongylus brasiliensis from mice. Int Arch Allergy Appl Immunol 52:160–168

    Google Scholar 

  • Jacobson RH, Reed ND, Manning DD (1977) Expulsion ofNippostrongylus brasiliensis from mice lacking antibody production potential. Immunology 32:867–874

    Google Scholar 

  • Jain SK, Mohandas N, Clark MR, Shohet SB (1983) The effect of malonyldialdehyde, a product of lipid peroxidation, on the deformability, dehydration and51Cr-survival of erythrocytes. Br J Haematol 53:247–255

    Google Scholar 

  • Jarrett EEE, Ferguson A (1974) Effect of T cell depletion on the potentiated reagin response. Nature 250:420–422

    Google Scholar 

  • Johnson HM, Russell JK, Torres BA (1986) Second messenger role of arachidonic acid and its metabolites in interferon-γ production. J Immunol 137:3053–3056

    Google Scholar 

  • Johnston RB Jr, Kitagawa S (1985) Molecular basis for the enhanced respiratory burst of activated macrophages. Fed Proc 44:2927–2932

    Google Scholar 

  • Jones VE, Ogilvie BM (1971) Protective immunity toNippostrongylus brasiliensis: the sequence of events which expels worms from the rat intestine. Immunology 20:549–561

    Google Scholar 

  • Kaibuchi K, Takai Y, Ogawa Y, Kimura S, Nishizuka Y (1982) Inhibitory action of adenosine 3′,5′-monophosphate on phosphatidylinositol turnover: difference in tissue response. Biochem Biophys Res Commun 104:105–112

    Google Scholar 

  • Kappus H (1985) Lipid peroxidation: mechanisms, analysis, enzymology and biological relevance. In: Sies H (ed) Oxidative stress. Academic, New York, pp 273–309

    Google Scholar 

  • Kassai T (1982) Handbook ofNippostrongylus brasiliensis (Nematode). Commonwealth Agricultural Bureaux, Budapest

    Google Scholar 

  • Kassai T, Redhi P, Jéssai GY, Balla E, Harangozo E (1980) The involvement of prostaglandins and their precursors in immune rejection ofNippostrongylus brasiliensis from the rat. Int J Parasitol 10:115–120

    Google Scholar 

  • Kazura JW (1981) Host defence mechanisms against nematode parasites: destruction of newbornTrichinella spiralis larvae by human antibodies and granulocytes. J Infect Dis 143:712–718

    Google Scholar 

  • Kazura JW, Aikawa M (1980) Host defece mechanisms againstTrichinella spiralis infection in the mouse: eosinophil-mediated destruction of newborn larvae in vitro. J Immunol 124:355–361

    Google Scholar 

  • Kazura JW, Meshnick SR (1984) Scavenger enzymes and resistance to oxygen mediated damage inTrichinella spiralis. Mol Biochem Parasitol 10:1–10

    Google Scholar 

  • Kazura JW, Fanning BM, Blumer JL, Mahmoud AAF (1981) Role of cell-generated hydrogen peroxide in granulocyte-mediated killing of schistosomula ofSchistosoma mansoni in vitro. J Clin Invest 67:93–102

    Google Scholar 

  • Kazura JW, deBrito P, Rabbege J, Aikawa M (1985) Role of granulocyte oxygen products in damage ofSchistosoma mansoni eggs in vitro. J Clin Invest 75:1297–1307

    Google Scholar 

  • Keller R (1971)Nippostrongylus brasiliensis in the rat: failure to relate intestinal histamine and mast cell levels with worm expulsion. Parasitology 63:473–481

    Google Scholar 

  • Keller R, Jones VE (1971) Role of activated macrophages and antibody in inhibition and enhancement of tumour growth in rats. Lancet II:847–849

    Google Scholar 

  • Keller R, Keist R (1972) Protective immunity toNippostrongylus brasiliensis in the rat: central role of the lymphocyte in worm expulsion. Immunology 22:767–773

    Google Scholar 

  • Kelly JD (1972) Immunological suppression of parasite rejection by removal of selected lymphocyte populations: the effect of neonatal thymectomy and anti-thymocyte serum administration on the resistance of rats to infection with the nematodeNippostrongylus brasiliensis. Aust J Exp Biol Med Sci 50:477–489

    Google Scholar 

  • Kelly JD, Ogilvie BM (1972) Intestinal mast cell and eosinophil numbers during worm expulsion in nulliparous and lactating rats infected withNippostrongylus brasiliensis. Int Arch Allergy Appl Immunol 43:497–509

    Google Scholar 

  • Kelly JD, Dineen JK, Love RJ (1973) Expulsion ofNippostrongylus brasiliensis from the intestines of rats: evidence for a third component in the rejection mechanism. Int Arch Allergy Appl Immunol 45:767–779

    Google Scholar 

  • Kelly JD, Dineen JK, Goodrich BS, Smith ID (1974) Expulsion ofNippostrongylus brasiliensis from the intestines of the rat. Int Arch Allergy Appl Immunol 47:458–465

    Google Scholar 

  • Kharazmi A, Jepsen S, Anderson BJ (1987) Generation of reactive oxygen radicals by human phagocytic cells activated byPlasmodium falciparum. Scand J Immunol 25:335–342

    Google Scholar 

  • Kikkawa U, Nishizuka Y (1986) The role of protein kinase C in transmembrane signalling. Annu Rev Cell Biol 2:149–178

    Google Scholar 

  • Kikkawa U, Takai Y, Tanaka Y, Miyake R, Nishizuka Y (1983) Protein kinase C as a possible receptor protein of tumour-promoting phorbol esters. J Biol Chem 258:11442–11445

    Google Scholar 

  • Klebanoff SJ, Vadas MA, Harlan JM, Sparks LH, Gamble JR, Agosti JM, Waltersdorph AM (1986) Stimulation of neutrophils by tumour necrosis factor. J Immunol 136:4220–4225

    Google Scholar 

  • Krammer PH, Kubelka CF, Falk W, Ruppel A (1985) Priming and triggering of tumouricidal and schistosomulicidal macrophages by two sequential lymphokine signals: interferon-γ and macrophage cytotoxicity inducing factor 2. J Immunol 135:3258–3263

    Google Scholar 

  • Kunkel SL, Chensue SW, Plewa M, Higashi GI (1984) Macrophage function in theSchistosoma mansoni egg-induced pulmonary granuloma. Role of arachidonic acid metabolites in macrophage Ia antigen expression. Am J Pathol 114:240–249

    Google Scholar 

  • Kurzrock R, Rohde MF, Queseda JR, Gianturco SH, Bradley WA, Sherwin SA, Gutterman JU (1986) Recombinant γ-interferon induces hypertriglyceridemia and inhibits postheparin lipase activity in cancer patients. J Exp Med 164:1093–1101

    Google Scholar 

  • Lamontagne LR, Gauldie J, Befus AD, McAdam KPWJ, Baltz ML, Pepys MB (1984) The acute phase response in parasite infection.Nippostrongylus brasiliensis in the mouse. Immunology 52:733–741

    Google Scholar 

  • Li M, Li YJ (1987) The production of reactive oxygen species in mice infected or immunised withPlasmodium berghei. Parasite Immunol 9:293–304

    Google Scholar 

  • Lim LK, Hunt NH, Weidemann MJ (1983) Reactive oxygen production, arachidonate metabolism and cyclic AMP in macrophages. Biochem Biophys Res Commun 114:549–555

    Google Scholar 

  • Lin WS, Armstrong DA (1978) Effects of superoxide dismutase, dithiothreitol and formate ion on the inactivation of papain by hydroxyl radical and superoxide radicals in aerated solutions. Int J Radiat Biol 33:231–237

    Google Scholar 

  • Logani MK, Davies RE (1980) Lipid oxidation: biologic effects and antioxidants — a review. Lipids 15:485–495

    Google Scholar 

  • Love RJ, Ogilvie BM, McLaren DJ (1975)Nippostrongylus brasiliensis: further properties of antibody damaged worms and induction of comparable damage by maintaining worms in vitro. Parasitology 71:275–283

    Google Scholar 

  • MacKenzie CD, Jungery M, Taylor PM, Ogilvie BM (1981) The in vitro interaction of eosinophils, neutrophils, macrophages and mast cells with nematode surfaces in the presence of complement and antibodies. J Pathol 133:161–175

    Google Scholar 

  • Makimura S, Brinkman V, Mossmann H, Fischer H (1982) Chemiluminescence response of peritoneal macrophages to parasitized erythrocytes and lysed erythrocytes fromPlasmodium berghei-infected mice. Infect Immun 37:800–804

    Google Scholar 

  • Maridonneau-Parini I, Tringale SM, Tauber AI (1986) Identification of distinct activation pathways of the human neutrophil NADPH oxidase. J Immunol 137:2925–2929

    Google Scholar 

  • Matsubara T, Ziff M (1986) Increased superoxide anion release from human endothelial cells in response to cytokines. J Immunol 137:3295–3298

    Google Scholar 

  • Matthews N, Neale ML, Jackson SK, Stark JM (1987) Tumour cell killing by tumour necrosis factor — inhibition by anaerobic conditions, free radical scavengers and inhibitors of arachidonate metabolism. Immunology 62:153–155

    Google Scholar 

  • Mayberry LF, Bristol JR, Favela SH, Galindo MA (1986) Peroxidase and gamma-glutamyl transpeptidase activities duringEimeria nieschulzi (Apicomplexa) and/orNippostrongylus brasiliensis (Nematoda) infections in the rat. Experientia 42:49–50

    Google Scholar 

  • Mayrhofer G (1979) The nature of the thymus dependency of mucosal mast cells. The effect of thymectomy and of depieting recirculating lymphocytes on the response toNippostrongylus brasiliensis. Cell Immunol 47:312–322

    Google Scholar 

  • McPhail LC, Shirley PJ, Clayton CC, Snyderman R (1985) Activation of the respiratory burst enzyme from human neutrophils in a cell-free system. Evidence for a soluble cofactor. J Clin Invest 75:1735–1739

    Google Scholar 

  • Miller HRP (1971a) Immune reactions in mucous membranes: II. The differentiation of intestinal mast cells during helminth expulsion in the rat. Lab Invest 24:339–347

    Google Scholar 

  • Miller HRP (1971b) Immune reactions in mucous membranes: III. The discharge of intestinal mast cells during helminth expulsion in the rat. Lab Invest 24:348–354

    Google Scholar 

  • Miller HRP, Jarrett WFH (1971) Immune reactions in mucous membranes: I. Intestinal mast cell response during helminth expulsion in the rat. Immunology 20:277–288

    Google Scholar 

  • Mitchell LA, Wescott RB, Perryman LA (1983) Kinetics of expulsion of the nematodeNippostrongylus brasiliensis in mast cell-deficient w/wv mice. Parasite Immunol 5:1–12

    Google Scholar 

  • Mobley A, Tai H-H (1985) Synergistic stimulation of thromboxane biosynthesis by calcium ionophore and phorbol ester or thromboxin in human platelets. Biochem Biophys Res Commun 130:717–723

    Google Scholar 

  • Moqbel R, King SJ, MacDonald AJ, Miller HRP, Cromwell O, Shaw RJ, Kay AB (1986) Enteral and systemic release of leukotrienes during anaphylaxis ofNippostrongylus brasiliensis-primed rats. J Immunol 137:296–301

    Google Scholar 

  • Moqbel R, Wakelin D, MacDonald AJ, King SJ, Grencis RK, Kay AB (1987) Release of leukotrienes during rapid expulsion ofTrichinella spiralis from immune rats. Immunology 60:425–430

    Google Scholar 

  • Murray HW (1981) Susceptibility ofLeishmania to oxygen intermediates and killing by normal macrophages. J Exp Med 153:1302–1315

    Google Scholar 

  • Murray HW (1982a) Pretreatment with phorbol myristate acetate inhibits macrophage activity against intracellular protozoa. J Reticuloendothel Soc 31:479–487

    Google Scholar 

  • Murray HW (1982b) Cell-mediated immune response in experimental visceral leishmaniansis: II. Oxygen-dependent killing of intracellularLeishmania donovani amastigotes. J Immunol 129:351–357

    Google Scholar 

  • Murray HW, Cohn ZA (1980) Macrophage oxygen-dependent antimicrobial activity: III. Enhanced oxidative metabolism as an expression of macrophage activation. J Exp Med 152:1596–1609

    Google Scholar 

  • Murray HW, Juangbhanich CW, Nathan CF, Cohn ZA (1979) Macrophage oxygen-dependent antimicrobial activity: II. The role of oxygen intermediates. J Exp Med 150:950–964

    Google Scholar 

  • Murray HW, Nathan CF, Cohn ZA (1980) Macrophage oxygen-dependent antimicrobial activity: IV. Role of endogenous scavengers of oxygen intermediates. J Exp Med 152:1610–1624

    Google Scholar 

  • Murray HW, Spitalny GL, Nathan CF (1985) Activation of mouse peritoneal macrophages in vitro and in vivo by interferon gamma. J Immunol 134:1619–1627

    Google Scholar 

  • Murray M, Miller HRP, Sanford J, Jarrett WFH (1971a) 5-Hydroxytryptamine in intestinal immunological reactions. Its relationship to mast cell activity and worm expulsion in rats infected withNippostrongylus brasiliensis. Int Arch Allergy Appl Immunol 40:236–247

    Google Scholar 

  • Murray M, Smith WD, Waddell AH, Jarrett WFH (1971b)Nippostrongylus brasiliensis: histamine and 5-hydroxytryptamine inhibition and worm expulsion. Exp Parasitol 30:58–63

    Google Scholar 

  • Naray-Fejes-Toth A, Guyre PM (1984) Recombinant human immune interferon induces increased IgE receptor expression on the human monocyte line U-937. J Immunol 133:1914–1919

    Google Scholar 

  • Nathan CF, Nogueira N, Juangbhanich C, Ellis J, Cohn ZA (1979) Activation of macrophages in vivo and in vitro. Correlation between hydrogen peroxide release and killing ofTrypanosoma cruzi. J Exp Med 149:1056–1068

    Google Scholar 

  • Nathan CF, Murray HW, Wiebe ME, Rubin BY (1983) Identification of interferon-γ as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J Exp Med 158:670–689

    Google Scholar 

  • Nawa Y, Miller HRP (1978) Adoptive transfer of the intestinal mast cell response in rats infected withNippostrongylus brasiliensis. Cell Immunol 42:225–239

    Google Scholar 

  • Nawa Y, Parish CR, Miller HRP (1978) The protective capacities of fractionated immune thoracic duct lymphocytes againstNippostrongylus brasiliensis. Cell Immunol 37:41–50

    Google Scholar 

  • Nedwin GE, Svedersky LP, Bringman TS, Palladino MA Jr, Goeddel DV (1985) Effect of interleukin 2, interferon-γ and mitogens on the production of tumour necrosis factors α and β. J Immunol 135:2492–2497

    Google Scholar 

  • Nishizuka Y (1984) Turnover of inositol phospholipids and signal transduction. Science 225:1365–1370

    Google Scholar 

  • Ockenhouse CF, Shear HL (1984) Oxidative killing of the intraerythrocytic malaria parasitePlasmodium yoelii by activated macrophages. J Immunol 132:424–429

    Google Scholar 

  • Ockenhouse CF, Schulman S, Shear HL (1984) Induction of crisis forms in the human malaria parasitePlasmodium falciparum by γ-interferon-activated monocyte-derived macrophages. J Immunol 133:1601–1608

    Google Scholar 

  • Ogilvie BM (1964) Reagin-like antibodies in animals immune to helminth parasites. Nature 204:91–92

    Google Scholar 

  • Ogilvie BM (1967) Reagin-like antibodies in rats infected with the nematode parasiteNippostrongylus brasiliensis. Immunology 12:113–131

    Google Scholar 

  • Ogilvie BM, Jones VE (1971)Nippostrongylus brasiliensis in the rat. A review of immunity and the host/parasite relationship. Exp Parasitol 29:138–177

    Google Scholar 

  • Ogilvie BM, Love RJ (1974) The role of cells in immunity to developing larvae and static adult worm populations ofNippostrongylus brasiliensis. Proceedings of the 3rd International Congress of Parasitology, vol. 3. FACTA, Vienna, pp 1194–1195

    Google Scholar 

  • Ogilvie BM, Love RJ, Jarra W, Brown KN (1977)Nippostrongylus brasiliensis in rats: the cellular requirement for worm expulsion. Immunology 32:521–528

    Google Scholar 

  • Ogilvie BM, Hesketh PM, Rose ME (1978)Nippostrongylus brasiliensis: peripheral blood leukocyte response of rats with special reference to basophils. Exp Parasitol 46:20–30

    Google Scholar 

  • Ohuchi K, Watanabe M, Takahashi C, Hayashi Y, Hirasawa N, Tsurufuji S, Fujika H, Sugimura T (1987) Analysis of tumour-promotor-induced inflammation in rats: participation of histamine and prostaglandin E2. Biochim Biophys Acta 925:156–163

    Google Scholar 

  • Ovington KS (1985) Dose-dependent relationships betweenNippostrongylus brasiliensis populations and rat food intake. Parasitology 91:157–168

    Google Scholar 

  • Ovington KS (1987)Nippostrongylus brasiliensis: physiological and metabolic responses of rats to primary infection. Exp Parasitol 63:10–20

    Google Scholar 

  • Papini E, Grzeskowiak M, Bellavite P, Rossi F (1985) Protein kinase C phosphorylates, a component of NADPH oxidase of neutrophils. FEBS Lett 190:204–208

    Google Scholar 

  • Penfield A, Dale MM (1984) Synergism between A23187 and 1-oleoyl-2-acetyl-glycerol in superoxide production by human neutrophils. Biochem Biophys Res Commun 125:332–336

    Google Scholar 

  • Penfield A, Dale MM (1985) Prostaglandins E1 and E2 enhance the stimulation of superoxide release by 1-oleoyl-2-acetyl glycerol from human neutrophils. FEBS Lett 181:335–338

    Google Scholar 

  • Perussia B, Dayton ET, Lazarus R, Fanning V, Trinchieri G (1983) Immune interferon induces the receptor for monomeric IgG1 on human monocyte and myeloid cells. J Exp Med 158:1092–1113

    Google Scholar 

  • Pfafferott G, Meiselman HJ, Hochstein P (1982) The effect of malonyldialdehyde on erythrocyte deformability. Blood 59:12–15

    Google Scholar 

  • Pfannkuche H-J, Kaever V, Resch K (1986) A possible role of protein kinase C in regulating prostaglandin synthesis of mouse peritoneal macrophages. Biochem Biophys Res Commun 139:604–611

    Google Scholar 

  • Philip R, Epstein LB (1986) Tumour necrosis factor as immuno-modulator and mediator of monocyte toxicity induced by itself, γ-interferon and interleukin 1. Nature 323:86–89

    Google Scholar 

  • Pryor WA (1976) The role of free radical reactions in biological systems. In: Pryor WA (ed) Free radicals in biology, vol 1. Academic, New York, pp 1–49

    Google Scholar 

  • Qureshi F, Kennedy MW, Gibson S, Ye PZ, Miller HRP (1987) Resistance of nematode secretory products to cleavage by mast cell proteinases. Mol Biochem Parasitol 24:137–145

    Google Scholar 

  • Rankin JA, Hitchcock M, Merrill W, Bach MK, Brashler JR, Askenase PW (1982) IgE-dependent release of leukotriene C4 from alveolar macrophages. Nature 297:329–331

    Google Scholar 

  • Remick DG, Kunkel RG, Larrick JW, Kunkel SL (1987) Acute in vivo effects of human recombinant tumour necrosis factor. Lab Invest 56:583–590

    Google Scholar 

  • Robinson JM, Badwey JA, Karnovsky ML, Karnovsky MJ (1984) Superoxide release by neutrophils: synergistic effects of a phorbol ester and a calcium ionophore. Biochem Biophys Res Commun 122:734–739

    Google Scholar 

  • Robinson JM, Badwey JA, Karnovsky ML, Karnovsky MJ (1985) Release of superoxide and change in morphology by neutrophils in response to phorbol esters: antagonism by inhibitors of calcium-binding proteins. J Cell Biol 101:1052–1058

    Google Scholar 

  • Rossi F (1986) The O2 −-forming NADPH oxidase of the phagocytes: nature, mechanisms of activation and function. Biochim Biophys Acta 853:65–89

    Google Scholar 

  • Roux-Lombard P, Cruchaud A, Dayer J-M (1986) Effect of interferon-γ and 1α,25 dihydroxyvitamin D3 on superoxide anion, prostaglandin E2 and mononuclear cell factor production by U937 cells. Cell Immunol 97:286–296

    Google Scholar 

  • Rouzer CA, Cerami A (1980) Hypertriglyceridaemia associated withTrypanosoma brucei brucei infections in rabbits: role of defective triglyceride removal. Mol Biochem Parasitol 2:31–38

    Google Scholar 

  • Ronzer CA, Scott WA, Hamil AL, Liu F-T, Katz DH, Cohn ZA (1982) Secretion of leukotriene C4 and other arachidonic acid metabolites by macrophages challenged with immunoglobulin E immune complexes. J Exp Med 156:1077–1086

    Google Scholar 

  • Russell JK, Torres BA, Johnson HM (1987) Phospholipase A2 treatment of lymphocytes provides helper signal for interferon-γ induction: evidence for second messenger role of endogenous arachidonic acid. J Immunol 139:3442–3446

    Google Scholar 

  • Rzepczyk CM, Bishop CJ (1984) Immunological and ultrastructural aspects of the cell-mediated killing ofDirofilaria immitis microfilariae. Parasite Immunol 6:443–449

    Google Scholar 

  • Rzepczyk CM, Bishop CJ, Cheung K, Atwell R, Ferrante A (1986) Stimulation of neutrophil respiratory burst and iodination reaction by opsonized microfilariae ofDirofilaria immitis. Aust J Exp Biol Med Sci 64:43–52

    Google Scholar 

  • Sakata A, Ida E, Tominaga M, Onoue K (1987) Arachidonic acid acts as an intracellular activator of NADPH oxidase in Fc receptor-mediated superoxide generation in macrophages. J Immunol 138:4353–4359

    Google Scholar 

  • Salmon D, Vilde JL, Andrieu B, Simonovic R, Lebras J (1986) Role of immune serum and complement in stimulation of the metabolic burst of human neutrophils byPlasmodium falciparum. Infect Immun 51:801–809

    Google Scholar 

  • Schmitz B, Possart-Schmitz P, Gehrung M, Stauffer U, Mossmann H, Fischer H (1982) Cellular response and resistance to the primary infection of rats and mice withNematospiroides dubius. Z Parasitenkd 68:339–347

    Google Scholar 

  • Sedgwick JB, Berube ML, Zurier RB (1985) Stimulus-dependent inhibition of superoxide generation by prostaglandins. Clin Immunol Immunopathol 34:205–215

    Google Scholar 

  • Shalaby MR, Palladino MA Jr, Hirabayashi SE, Eessulu TE, Lewis GD, Shepard HM, Aggarwal BB (1987) Receptor binding and activation of polymorphonuclear neutrophils by tumor necrosis factor-alpha. J Leukocyte Biol 41:196–204

    Google Scholar 

  • Sinski E, Holmes PH (1977)Nippostrongylus brasiliensis: systemic and local IgA and IgG immunoglobulin response in parasitized rats. Exp Parasitol 43:382–389

    Google Scholar 

  • Smith JW, Castro GA (1978) Relation of peroxidase activity in gut mucosa to inflammation. Am J Physiol 234:R72-R79

    Google Scholar 

  • Smith NC, Bryant C (1986) The role of host generated free radicals in helminth infections:Nippostrongylus brasiliensis andNematospiroides dubius compared. Int J Parasitol 16:617–622

    Google Scholar 

  • Smith NC, Bryant C (1989a) Free radical generation during primary infections withNippostrongylus brasiliensis. Parasite Immunol (in press)

  • Smith NC, Bryant C (1989b) The effect of antioxidants on the rejection ofNippostrongylus brasiliensis. Parasite Immunol (in press)

  • Snyderman R, Smith CD, Verghese MW (1986) Model for leukocyte regulation by chemoattractant receptors: roles of a guanine nucleotide regulatory protein and polyphosphoinositide metabolism. J Leukocyte Biol 40:785–800

    Google Scholar 

  • Somers SD, Weiel JE, Hamilton TA, Adams DO (1986) Phorbol esters and calcium ionophore can prime murine peritoneal macrophages for tumour cell destruction. J Immunol 136:4199–4205

    Google Scholar 

  • Speer CP, Pabst MJ, Hedegaard HB, Rest RF, Johnston RB (1984) Enhanced release of oxygen metabolites by monocyte-derived macrophages exposed to proteolytic enzymes: activity of neutrophil elastase and cathepsin G. J Immunol 133:2151–2156

    Google Scholar 

  • Stocker R, Hunt NH, Clark IA, Weidemann MJ (1984) Production of luminol-reactive oxygen radicals duringPlasmodium vinckei infection. Infect Immun 45:708–712

    Google Scholar 

  • Takenawa T, Ishitoya J, Homma Y, Kato M, Nagai Y (1985) Role of enhanced inositol phospholipid metabolism in neutrophil activation. Biochem Pharmacol 34:1931–1935

    Google Scholar 

  • Taliaferro WH, Sarles MP (1939) The cellular reactions in the skin, lungs and intestine of normal and immune rats after infection withNippostrongylus brasiliensis. J Infect Dis 64:157–192

    Google Scholar 

  • Tanaka Y, Kiyotaki C, Tanowitz H, Bloom BR (1982) Reconstitution of a variant macrophage cell line defective in oxygen metabolism with a H2O2-generating system. Proc Natl Acad Sci USA 79:2584–2588

    Google Scholar 

  • Taverne J, Tavernier J, Fiers W, Playfair JHL (1987) Recombinant tumour necrosis factor inhibits malaria parasites in vivo but not in vitro. Clin Exp Immunol 67:1–4

    Google Scholar 

  • Torti FM, Dieckmann B, Beutler B, Cerami A, Ringold GM (1985) A macrophage factor inhibits adipocyte gene expressions: an in vitro model of cachexia. Science 229:867–869

    Google Scholar 

  • Tou J-S, Maier C (1976) Phospholipid metabolism and lysosomal enzyme secretion by leukocytes. Effects of dibutyrul cyclic adenosine 3′,5′-monophosphate and ATP. Biochim Biophys Acta 451:353–362

    Google Scholar 

  • Tracey KJ, Beutler B, Lowry SF, Merryweather J, Wolpe S, Milsark IW, Hariri RJ, Fahey TJ, Zentella A, Albert JD, Shires GT, Cerami A (1986) Shock and tissue injury induced by recombinant human cachectin. Science 234:470–476

    Google Scholar 

  • Tsujimoto M, Yip YK, Vilcek J (1986) Interferon-γ enhances expression of cellular receptors for tumor necrosis factor. J Immunol 136:2441–2444

    Google Scholar 

  • Tsunawaki S, Nathan CF (1986) Release of arachidonate and reduction of oxygen. Independent metabolic bursts of the mouse peritoneal macrophage. J Biol Chem 261:11563–11570

    Google Scholar 

  • Veldhuis JD, Demers LM (1987) Activation of protein kinase C is coupled to prostaglandin E2 synthesis in swine granulosa cells. Prostaglandins 33:819–830

    Google Scholar 

  • Verghese MW, Smith CD, Snyderman R (1986) Role of guanine nucleotide regulatory protein in polyphosphoinositide degradation and activation of phagocytic leukocytes by chemoattractants. J Cell Biochem 32:59–69

    Google Scholar 

  • Wedrychowicz H, MacLean JM, Holmes PH (1983) The detection and measurement of coproantibodies toNippostrongylus brasiliensis in rats following a primary infection. Parasite Immunol 5:277–287

    Google Scholar 

  • Weiss SJ, LoBuglio AF (1982) Phagocyte-generated oxygen metabolites and cellular injury. Lab Invest 47:5–18

    Google Scholar 

  • Weiss SJ, Peppin G, Ortix X, Ragsdale C, Test ST (1985) Oxidative autoxidation of latent collagenase by human neutrophils. Science 227:747–749

    Google Scholar 

  • Wells PD (1962) Mast cell, eosinophil and histamine levels inNippostrongylus brasiliensis infected rats. Exp Parasitol 12:82–101

    Google Scholar 

  • Wey HE, Baxter CS (1986) Phorbol diester synergistically stimulates agonist-induced lipoxygenase product formation in murine neutrophils. Biochem Biophys Res Commun 140:861–867

    Google Scholar 

  • Wilson CB, Tsai V, Remington JS (1980) Failure to trigger the oxidative metabolic burst by normal macrophages: possible mechanism for survival of intracellular pathogens. J Exp Med 151:328–346

    Google Scholar 

  • Woodbury RG, Miller HRP, Huntley JF, Newlands GFJ, Palliser AC, Wakelin D (1984) Mucosal mast cells are functionally active during spontaneous expulsion of intestinal nematode infections in rat. Nature 312:450–452

    Google Scholar 

  • Wozencraft AO, Dockrell HM, Taverne J, Targett GAT, Playfair JHL (1984) Killing of human malaria parasites by macrophage secretory products. Infect Immun 43:664–671

    Google Scholar 

  • Wright B, Zeidman I, Greig R, Poste G (1985) Inhibition of macrophage activation by calcium channel blockers and calmodulin antagonists. Cell Immunol 95:46–53

    Google Scholar 

  • Yamanishi J, Takai Y, Kaibuchi K, Sano K, Costagna M, Nishizuka Y (1983) Synergistic functions of phorbol ester and calcium in serotonin release from human platelets. Biochem Biophys Res Commun 112:778–786

    Google Scholar 

  • Yap WH, Teo TS, Tan YH (1986) An early event in the interferon-induced transmembrane signalling process. Science 234:355–358

    Google Scholar 

  • Zander B, Hörchner F (1976) Influence of macrophages and lymphocytes of rats onNippostrongylus brasiliensis in vitro. In: Soulsby EJL (ed) Pathophysiology of parasitic infection. Academic, New York, pp 241–246

    Google Scholar 

  • Zavoico GB, Feinstein MB (1984) Cytoplasmic Ca2+ in platelets is controlled by cyclic AMP: antagonism between stimulators and inhibitors of adenylate cyclase. Biochem Biophys Res Commun 120:579–585

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, Australian National University, GPO Box 4, 2601, Canberra, A.C.T., Australia

    N. C. Smith

Authors
  1. N. C. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smith, N.C. The role of free oxygen radicals in the expulsion of primary infections ofNippostrongylus brasiliensis . Parasitol Res 75, 423–438 (1989). https://doi.org/10.1007/BF00930968

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00930968

Keywords

Search

Navigation