Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Immunologic Research
Published in: Immunologic Research 2-3/2011

01-12-2011 | Current Immunology Research at Jefferson

Innate and adaptive immunity to the nematode Strongyloides stercoralis in a mouse model

Authors: Sandra Bonne-Année, Jessica A. Hess, David Abraham

Published in: Immunologic Research | Issue 2-3/2011

Login to get access

Abstract

Mice have been used to the study the mechanisms of protective innate and adaptive immunity to larval Strongyloides stercoralis. During primary infection, neutrophils and eosinophils are attracted by parasite components and kill the larvae by release of granule products. Eosinophils also function as antigen-presenting cells for the induction of a Th2 response. B cells produce both IgM and IgG that collaborate with neutrophils to kill worms in the adaptive immune response. Vaccine studies have identified a recombinant diagnostic antigen that induced high levels of immunity to infection with S. stercoralis in mice. These studies demonstrate that there are redundancies in the mechanisms used by the immune response to kill the parasite and that a vaccine with a single antigen may be suitable as a prophylactic vaccine to prevent human strongyloidiasis.
Literature
1.
Olsen A, van Lieshout L, Marti H, Polderman T, Polman K, Steinmann P, Stothard R, Thybo S, Verweij JJ, Magnussen P. Strongyloidiasis—the most neglected of the neglected tropical diseases? Trans R Soc Trop Med Hyg. 2009;103:967–72.PubMedCrossRef
2.
Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367:1521–32.PubMedCrossRef
3.
Croker C, Reporter R, Redelings M, Mascola L. Strongyloidiasis-related deaths in the United States, 1991–2006. Am J Trop Med Hyg. 2010;83:422–6.PubMedCrossRef
4.
Krolewiecki AJ, Ramanathan R, Fink V, McAuliffe I, Cajal SP, Won K, Juarez M, Di Paolo A, Tapia L, Acosta N, Lee R, Lammie P, Abraham D, Nutman TB. Improved diagnosis of Strongyloides stercoralis using recombinant antigen-based serologies in a community-wide study in northern Argentina. Clin Vaccine Immunol. 2010;17:1624–30.PubMedCrossRef
5.
Montes M, Sawhney C, Barros N. Strongyloides stercoralis: there but not seen. Curr Opin Infect Dis. 2010;23:500–4.PubMedCrossRef
6.
Keiser PB, Nutman TB. Strongyloides stercoralis in the immunocompromised population. Clin Microbiol Rev. 2004;17:208–17.PubMedCrossRef
7.
Marcos LA, Terashima A, Dupont HL, Gotuzzo E. Strongyloides hyperinfection syndrome: an emerging global infectious disease. Trans R Soc Trop Med Hyg. 2008;102:314–8.PubMedCrossRef
8.
Montes M, Sanchez C, Verdonck K, Lake JE, Gonzalez E, Lopez G, Terashima A, Nolan T, Lewis DE, Gotuzzo E, White AC Jr. Regulatory T cell expansion in HTLV-1 and strongyloidiasis co-infection is associated with reduced IL-5 responses to Strongyloides stercoralis antigen. PLoS Negl Trop Dis. 2009;3:e456.PubMedCrossRef
9.
Ramanathan R, Nutman T. Strongyloides stercoralis infection in the immunocompromised host. Curr Infect Dis Rep. 2008;10:105–10.PubMedCrossRef
10.
Horton J. Albendazole: a review of anthelmintic efficacy and safety in humans. Parasitology. 2000;121(Suppl):S113–32.PubMedCrossRef
11.
Ikeda T. Pharmacological effects of ivermectin, an antiparasitic agent for intestinal strongyloidiasis: its mode of action and clinical efficacy. Nihon Yakurigaku Zasshi. 2003;122:527–38.PubMedCrossRef
12.
Brigandi RA, Rotman HL, Leon O, Nolan TJ, Schad GA, Abraham D. Strongyloides stercoralis host-adapted third-stage larvae are the target of eosinophil-associated immune-mediated killing in mice. J Parasitol. 1998;84:440–5.PubMedCrossRef
13.
Brigandi RA, Rotman HL, Nolan TJ, Schad GA, Abraham D. Chronicity in Strongyloides stercoralis infections: dichotomy of the protective immune response to infective and autoinfective larvae in a mouse model. Am J Trop Med Hyg. 1997;56:640–6.PubMed
14.
Maruyama H, Nishimaki A, Takuma Y, Kurimoto M, Suzuki T, Sakatoku Y, Ishikawa M, Ohta N. Successive changes in tissue migration capacity of developing larvae of an intestinal nematode, Strongyloides venezuelensis. Parasitology. 2006;132:411–8.PubMedCrossRef
15.
Machado ER, Carlos D, Sorgi CA, Ramos SG, Souza DI, Soares EG, Costa-Cruz JM, Ueta MT, Aronoff DM, Faccioli LH. Dexamethasone effects in the Strongyloides venezuelensis infection in a murine model. Am J Trop Med Hyg. 2011;84:957–66.PubMedCrossRef
16.
Viney M. How do host immune responses affect nematode infections? Trends Parasitol. 2002;18:63–6.PubMedCrossRef
17.
18.
Yoshida A, Nagayasu E, Nishimaki A, Sawaguchi A, Yanagawa S, Maruyama H. Transcripts analysis of infective larvae of an intestinal nematode, Strongyloides venezuelensis. Parasitol Int. 2011;60:75–83.PubMedCrossRef
19.
Dawkins HJ, Grove DI. Attempts to establish infections with Strongyloides stercoralis in mice and other laboratory animals. J Helminthol. 1982;56:23–6.PubMedCrossRef
20.
Rotman HL, Yutanawiboonchai W, Brigandi RA, Leon O, Nolan TJ, Schad GA, Abraham D. Strongyloides stercoralis: complete life cycle in SCID mice. Exp Parasitol. 1995;81:136–9.PubMedCrossRef
21.
Machado ER, Carlos D, Lourenco EV, Souza GE, Sorgi CA, Silva EV, Ueta MT, Ramos SG, Aronoff DM, Faccioli LH. Cyclooxygenase-derived mediators regulate the immunological control of Strongyloides venezuelensis infection. FEMS Immunol Med Microbiol. 2010;59:18–32.PubMedCrossRef
22.
Abraham D, Rotman HL, Haberstroh HF, Yutanawiboonchai W, Brigandi RA, Leon O, Nolan TJ, Schad GA. Strongyloides stercoralis: protective immunity to third-stage larvae inBALB/cByJ mice. Exp Parasitol. 1995;80:297–307.PubMedCrossRef
23.
O’Connell AE, Hess JA, Santiago GA, Nolan TJ, Lok JB, Lee JJ, Abraham D. Major basic protein from eosinophils and myeloperoxidase from neutrophils are required for protective immunity to Strongyloides stercoralis in mice. Infect Immun. 2011;79:2770–8.PubMedCrossRef
24.
Dawkins HJ, Muir GM, Grove DI. Histopathological appearances in primary and secondary infections with Strongyloides ratti in mice. Int J Parasitol. 1981;11:97–103.PubMedCrossRef
25.
McHugh TD, Jenkins T, McLaren DJ. Strongyloides ratti: studies of cutaneous reactions elicited in naive and sensitized rats and of changes in surface antigenicity of skin-penetrating larvae. Parasitology. 1989;98(Pt 1):95–103.PubMedCrossRef
26.
Watanabe K, Noda K, Hamano S, Koga M, Kishihara K, Nomoto K, Tada I. The crucial role of granulocytes in the early host defense against Strongyloides ratti infection in mice. Parasitol Res. 2000;86:188–93.PubMedCrossRef
27.
Galioto AM, Hess JA, Nolan TJ, Schad GA, Lee JJ, Abraham D. Role of eosinophils and neutrophils in innate and adaptive protective immunity to larval Strongyloides stercoralis in mice. Infect Immun. 2006;74:5730–8.PubMedCrossRef
28.
Padigel UM, Stein L, Redding K, Lee JJ, Nolan TJ, Schad GA, Birnbaumer L, Abraham D. Signaling through Galphai2 protein is required for recruitment of neutrophils for antibody-mediated elimination of larval Strongyloides stercoralis in mice. J Leukoc Biol. 2007;81:1120–6.PubMedCrossRef
29.
O’Connell AE, Redding KM, Hess JA, Lok JB, Nolan TJ, Abraham D. Soluble extract from the nematode Strongyloides stercoralis induces CXCR2 dependent/IL-17 independent neutrophil recruitment. Microbes Infect. 2011;13:536–44.PubMedCrossRef
30.
Lalani T, Simmons RK, Ahmed AR. Biology of IL-5 in health and disease. Ann Allergy Asthma Immunol. 1999;82:317–32, 332–3.PubMedCrossRef
31.
Roboz GJ, Rafii S. Interleukin-5 and the regulation of eosinophil production. Curr Opin Hematol. 1999;6:164–8.PubMedCrossRef
32.
Watanabe K, Sasaki O, Hamano S, Kishihara K, Nomoto K, Tada I, Aoki Y. Strongyloides ratti: the role of interleukin-5 in protection against tissue migrating larvae and intestinal adult worms. J Helminthol. 2003;77:355–61.PubMedCrossRef
33.
Herbert DR, Lee JJ, Lee NA, Nolan TJ, Schad GA, Abraham D. Role of IL-5 in innate and adaptive immunity to larval Strongyloides stercoralis in mice. J Immunol. 2000;165:4544–51.PubMed
34.
Rotman HL, Yutanawiboonchai W, Brigandi RA, Leon O, Gleich GJ, Nolan TJ, Schad GA, Abraham D. Strongyloides stercoralis: eosinophil-dependent immune-mediated killing of third stage larvae in BALB/cByJ mice. Exp Parasitol. 1996;82:267–78.PubMedCrossRef
35.
Jong EC, Mahmoud AA, Klebanoff SJ. Peroxidase-mediated toxicity to schistosomula of Schistosoma mansoni. J Immunol. 1981;126:468–71.PubMed
36.
Brennan ML, Wu W, Fu X, Shen Z, Song W, Frost H, Vadseth C, Narine L, Lenkiewicz E, Borchers MT, Lusis AJ, Lee JJ, Lee NA, Abu-Soud HM, Ischiropoulos H, Hazen SL. A tale of two controversies: defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species. J Biol Chem. 2002;277:17415–27.PubMedCrossRef
37.
Spalteholz H, Panasenko OM, Arnhold J. Formation of reactive halide species by myeloperoxidase and eosinophil peroxidase. Arch Biochem Biophys. 2006;445:225–34.PubMedCrossRef
38.
Borelli V, Vita F, Shankar S, Soranzo MR, Banfi E, Scialino G, Brochetta C, Zabucchi G. Human eosinophil peroxidase induces surface alteration, killing, and lysis of Mycobacterium tuberculosis. Infect Immun. 2003;71:605–13.PubMedCrossRef
39.
Stein LH, Redding KM, Lee JJ, Nolan TJ, Schad GA, Lok JB, Abraham D. Eosinophils utilize multiple chemokine receptors for chemotaxis to the parasitic nematode Strongyloides stercoralis. J Innate Immun. 2009;1:618–30.PubMedCrossRef
40.
Fabre V, Beiting DP, Bliss SK, Gebreselassie NG, Gagliardo LF, Lee NA, Lee JJ, Appleton JA. Eosinophil deficiency compromises parasite survival in chronic nematode infection. J Immunol. 2009;182:1577–83.PubMed
41.
Brigandi RA, Rotman HL, Yutanawiboonchai W, Leon O, Nolan TJ, Schad GA, Abraham D. Strongyloides stercoralis: role of antibody and complement in immunity to the third stage of larvae in BALB/cByJ mice. Exp Parasitol. 1996;82:279–89.PubMedCrossRef
42.
Kerepesi LA, Hess JA, Nolan TJ, Schad GA, Abraham D. Complement component C3 is required for protective innate and adaptive immunity to larval Strongyloides stercoralis in mice. J Immunol. 2006;176:4315–22.PubMed
43.
de Messias IJ, Genta RM, Mohren WD. Adherence of monocytes and polymorphonuclear cells to infective larvae of Strongyloides stercoralis after complement activation. J Parasitol. 1994;80:267–74.PubMedCrossRef
44.
Grove DI, Northern C, Dawkins HJ. Interactions of Strongyloides ratti free-living and skin-penetrated infective larvae and parasitic adults with serum and cells in vitro. Aust J Exp Biol Med Sci. 1985;63(Pt 5):521–9.PubMed
45.
Padigel UM, Hess JA, Lee JJ, Lok JB, Nolan TJ, Schad GA, Abraham D. Eosinophils act as antigen-presenting cells to induce immunity to Strongyloides stercoralis in mice. J Infect Dis. 2007;196:1844–51.PubMedCrossRef
46.
Padigel UM, Lee JJ, Nolan TJ, Schad GA, Abraham D. Eosinophils can function as antigen-presenting cells to induce primary and secondary immune responses to Strongyloides stercoralis. Infect Immun. 2006;74:3232–8.PubMedCrossRef
47.
MacKenzie JR, Mattes J, Dent LA, Foster PS. Eosinophils promote allergic disease of the lung by regulating CD4(+) Th2 lymphocyte function. J Immunol. 2001;167:3146–55.PubMed
48.
49.
Xie ZF, Shi HZ, Qin XJ, Kang LF, Huang CP, Chen YQ. Effects of antigen presentation of eosinophils on lung Th1/Th2 imbalance. Chin Med J (Engl). 2005;118:6–11.
50.
Neva FA, Filho JO, Gam AA, Thompson R, Freitas V, Melo A, Carvalho EM. Interferon-gamma and interleukin-4 responses in relation to serum IgE levels in persons infected with human T lymphotropic virus type I and Strongyloides stercoralis. J Infect Dis. 1998;178:1856–9.PubMedCrossRef
51.
Porto AF, Neva FA, Bittencourt H, Lisboa W, Thompson R, Alcantara L, Carvalho EM. HTLV-1 decreases Th2 type of immune response in patients with strongyloidiasis. Parasite Immunol. 2001;23:503–7.PubMedCrossRef
52.
Lange AM, Yutanawiboonchai W, Scott P, Abraham D. IL-4- and IL-5-dependent protective immunity to Onchocerca volvulus infective larvae in BALB/cBYJ mice. J Immunol. 1994;153:205–11.PubMed
53.
Urban JF Jr, Katona IM, Paul WE, Finkelman FD. Interleukin 4 is important in protective immunity to a gastrointestinal nematode infection in mice. Proc Natl Acad Sci USA. 1991;88:5513–7.PubMedCrossRef
54.
Else KJ, Grencis RK. Cellular immune responses to the murine nematode parasite Trichuris muris. I. Differential cytokine production during acute or chronic infection. Immunology. 1991;72:508–13.PubMed
55.
Sasaki O, Sugaya H, Ishida K, Yoshimura K. Ablation of eosinophils with anti-IL-5 antibody enhances the survival of intracranial worms of Angiostrongylus cantonensis in the mouse. Parasite Immunol. 1993;15:349–54.PubMedCrossRef
56.
Rotman HL, Schnyder-Candrian S, Scott P, Nolan TJ, Schad GA, Abraham D. IL-12 eliminates the Th-2 dependent protective immune response of mice to larval Strongyloides stercoralis. Parasite Immunol. 1997;19:29–39.PubMedCrossRef
57.
Fernandes A, Pereira AT, Eschenazi PD, Schilter HC, Sousa AL, Teixeira MM, Negrao-Correa D. Evaluation of the immune response against Strongyloides venezuelensis in antigen-immunized or previously infected mice. Parasite Immunol. 2008;30:139–49.PubMedCrossRef
58.
Bleay C, Wilkes CP, Paterson S, Viney ME. Density-dependent immune responses against the gastrointestinal nematode Strongyloides ratti. Int J Parasitol. 2007;37:1501–9.PubMedCrossRef
59.
Chiuso-Minicucci F, Marra NM, Zorzella-Pezavento SF, Franca TG, Ishikawa LL, Amarante MR, Amarante AF, Sartori A. Recovery from Strongyloides venezuelensis infection in Lewis rats is associated with a strong Th2 response. Parasite Immunol. 2010;32:74–8.PubMedCrossRef
60.
Machado ER, Carlos D, Lourenco EV, Sorgi CA, Silva EV, Ramos SG, Ueta MT, Aronoff DM, Faccioli LH. Counterregulation of Th2 immunity by interleukin 12 reduces host defenses against Strongyloides venezuelensis infection. Microbes Infect. 2009;11:571–8.PubMedCrossRef
61.
Wilkes CP, Bleay C, Paterson S, Viney ME. The immune response during a Strongyloides ratti infection of rats. Parasite Immunol. 2007;29:339–46.PubMedCrossRef
62.
Eschbach ML, Klemm U, Kolbaum J, Blankenhaus B, Brattig N, Breloer M. Strongyloides ratti infection induces transient nematode-specific Th2 response and reciprocal suppression of IFN-gamma production in mice. Parasite Immunol. 2010;32:370–83.PubMedCrossRef
63.
Paterson S, Wilkes C, Bleay C, Viney ME. Immunological responses elicited by different infection regimes with Strongyloides ratti. PLoS One. 2008;3:e2509.PubMedCrossRef
64.
Genta RM, Gomes MC. Pathology. In: Grove DI, editor. Strongyloidiasis a major roundworm infection of man. Philadelphia, PA, USA: Taylor & Francis Inc.; 1989. p. 105–132.
65.
Haque AK, Schnadig V, Rubin SA, Smith JH. Pathogenesis of human strongyloidiasis: autopsy and quantitative parasitological analysis. Mod Pathol. 1994;7:276–88.PubMed
66.
Wang HB, Weller PF. Pivotal advance: eosinophils mediate early alum adjuvant-elicited B cell priming and IgM production. J Leukoc Biol. 2008;83:817–21.PubMedCrossRef
67.
Hayashi Y, Nakagaki K, Nogami S, Hammerberg B, Tanaka H. Protective immunity against Brugia malayi infective larvae in mice. I. Parameters of active and passive immunity. Am J Trop Med Hyg. 1989;41:650–6.PubMed
68.
Kerepesi LA, Leon O, Lustigman S, Abraham D. Protective immunity to the larval stages of Onchocerca volvulus is dependent on Toll-like receptor 4. Infect Immun. 2005;73:8291–7.PubMedCrossRef
69.
Helmby H, Grencis RK. Essential role for TLR4 and MyD88 in the development of chronic intestinal nematode infection. Eur J Immunol. 2003;33:2974–9.PubMedCrossRef
70.
Stewart PW, Chapes SK. Role of major histocompatibility complex class II in resistance of mice to naturally acquired infection with Syphacia obvelata. Comp Med. 2003;53:70–4.PubMed
71.
Fan J, Malik AB. Toll-like receptor-4 (TLR4) signaling augments chemokine-induced neutrophil migration by modulating cell surface expression of chemokine receptors. Nat Med. 2003;9:315–21.PubMedCrossRef
72.
Kirimanjeswara GS, Mann PB, Pilione M, Kennett MJ, Harvill ET. The complex mechanism of antibody-mediated clearance of Bordetella from the lungs requires TLR4. J Immunol. 2005;175:7504–11.PubMed
73.
Kerepesi LA, Hess JA, Leon O, Nolan TJ, Schad GA, Abraham D. Toll-like receptor 4 (TLR4) is required for protective immunity to larval Strongyloides stercoralis in mice. Microbes Infect. 2007;9:28–34.PubMedCrossRef
74.
Herbert DR, Nolan TJ, Schad GA, Abraham D. The role of B cells in immunity against larval Strongyloides stercoralis in mice. Parasite Immunol. 2002;24:95–101.PubMedCrossRef
75.
Ligas JA, Kerepesi LA, Galioto AM, Lustigman S, Nolan TJ, Schad GA, Abraham D. Specificity and mechanism of immunoglobulin M (IgM)- and IgG-dependent protective immunity to larval Strongyloides stercoralis in mice. Infect Immun. 2003;71:6835–43.PubMedCrossRef
76.
Nolan TJ, Rotman HL, Bhopale VM, Schad GA, Abraham D. Immunity to a challenge infection of Strongyloides stercoralis third-stage larvae in the jird. Parasite Immunol. 1995;17:599–604.PubMedCrossRef
77.
Murrell KD. Protective role of immunoglobulin G in immunity to Strongyloides ratti. J Parasitol. 1981;67:167–73.PubMedCrossRef
78.
Dawkins HJ, Grove DI. Transfer by serum and cells of resistance to infection with Strongyloides ratti in mice. Immunology. 1981;43:317–22.PubMed
79.
Uchikawa R, Ichiki H, Komaki E. Antibody responses and protective immunity in rats receiving repeated inoculations of Strongyloides ratti. J Parasitol. 1991;77:737–41.PubMedCrossRef
80.
Kerepesi LA, Keiser PB, Nolan TJ, Schad GA, Abraham D, Nutman TB. DNA immunization with Na+–K+ ATPase (Sseat-6) induces protective immunity to larval Strongyloides stercoralis in mice. Infect Immun. 2005;73:2298–305.PubMedCrossRef
81.
Abraham D, Hess JA, Mejia R, Nolan TJ, Lok JB, Lustigman S, Nutman TB. Immunization with the recombinant antigen Ss-IR induces protective immunity to infection with Strongyloides stercoralis in mice. Vaccine. 2011;29:8134–40.PubMedCrossRef
82.
Kerepesi LA, Nolan TJ, Schad GA, Lustigman S, Herbert DR, Keiser PB, Nutman TB, Krolewiecki AJ, Abraham D. Human immunoglobulin G mediates protective immunity and identifies protective antigens against larval Strongyloides stercoralis in mice. J Infect Dis. 2004;189:1282–90.PubMedCrossRef
83.
Brewer JM, Conacher M, Hunter CA, Mohrs M, Brombacher F, Alexander J. Aluminium hydroxide adjuvant initiates strong antigen-specific Th2 responses in the absence of IL-4- or IL-13-mediated signaling. J Immunol. 1999;163:6448–54.PubMed
Metadata
Title
Innate and adaptive immunity to the nematode Strongyloides stercoralis in a mouse model
Authors
Sandra Bonne-Année
Jessica A. Hess
David Abraham
Publication date
01-12-2011
Publisher
Humana Press Inc
Published in
Immunologic Research / Issue 2-3/2011
Print ISSN: 0257-277X
Electronic ISSN: 1559-0755
DOI
https://doi.org/10.1007/s12026-011-8258-2

Other articles of this Issue 2-3/2011

Immunologic Research 2-3/2011 Go to the issue

Current Immunology Research at Jefferson

Human immune system mice: current potential and limitations for translational research on human antibody responses

Current Immunology Research at Jefferson

Beyond the classical: Influenza virus and the elucidation of alternative MHC class II-restricted antigen processing pathways

Current Immunology Research at Jefferson

Mechanisms controlling granule-mediated cytolytic activity of cytotoxic T lymphocytes

Current Immunology Research at Jefferson

The impact of bacterial infection on mast cell degranulation

Current Immunology Research at Jefferson

Buffered memory: a hypothesis for the maintenance of functional, virus-specific CD8+ T cells during cytomegalovirus infection

Current Immunology Research at Jefferson

B1b lymphocyte-derived antibodies control Borrelia hermsii independent of Fcα/μ receptor and in the absence of host cell contact