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

Immunologic Research

Volumn 51, Issue 2-3, 2011, Pages 205-214

  Bonne Année, Sandra ^a   Hess, Jessica A ^a   Abraham, David ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Adaptive immunity; Antigen presenting cell; B cells; Complement; Eosinophils; IgG; IgM; Innate immunity; Neutrophils; Recombinant vaccine; Ss IR; Strongyloides stercoralis; Th2 cells

Indexed keywords

ANTIBODY; COMPLEMENT; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; RECOMBINANT ANTIGEN; RECOMBINANT PURIFIED PROTEIN ANTIGEN; TROPOMYOSIN; UNCLASSIFIED DRUG; VACCINE;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; EOSINOPHIL; EXPERIMENTAL MODEL; IMMUNE RESPONSE; INNATE IMMUNITY; LARVA; NEUTROPHIL; NONHUMAN; PARASITE; PRIMARY INFECTION; PRIORITY JOURNAL; STRONGYLOIDES STERCORALIS; STRONGYLOIDIASIS; TH2 CELL; WORM;

EID: 84856510695     PISSN: 0257277X     EISSN: 15590755     Source Type: Journal    
DOI: 10.1007/s12026-011-8258-2     Document Type: Article

References (83)

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.
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.
3. Croker C, Reporter R, Redelings M, Mascola L. Strongyloidiasisrelated deaths in the United States, 1991-2006. Am J Trop Med Hyg. 2010;83:422-6.
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.
5. Montes M, Sawhney C, Barros N. Strongyloides stercoralis: There but not seen. Curr Opin Infect Dis. 2010;23:500-4.
6. Keiser PB, Nutman TB. Strongyloides stercoralis in the immunocompromised population. Clin Microbiol Rev. 2004;17:208-17. (Pubitemid 38120934)
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.
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 coinfection is associated with reduced IL-5 responses to Strongyloides stercoralis antigen. PLoS Negl Trop Dis. 2009;3:e456.
9. Ramanathan R, Nutman T. Strongyloides stercoralis infection in the immunocompromised host. Curr Infect Dis Rep. 2008;10: 105-10.
10. Horton J. Albendazole: A review of anthelmintic efficacy and safety in humans. Parasitology. 2000;121(Suppl):S113-32. (Pubitemid 32499891)
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. (Pubitemid 38019945)
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. (Pubitemid 28217427)
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. (Pubitemid 27318587)
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. (Pubitemid 43376229)
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.
16. Viney M. How do host immune responses affect nematode infections? Trends Parasitol. 2002;18:63-6.
17. Viney ME. The biology and genomics of Strongyloides. Med Microbiol Immunol. 2006;195:49-54. (Pubitemid 43742467)
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.
19. Dawkins HJ, Grove DI. Attempts to establish infections with Strongyloides stercoralis in mice and other laboratory animals. J Helminthol. 1982;56:23-6.
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.
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.
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.
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.
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. (Pubitemid 11149394)
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. (Pubitemid 19111314)
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.
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. (Pubitemid 44484558)
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. (Pubitemid 46495661)
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.
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.
31. Roboz GJ, Rafii S. Interleukin-5 and the regulation of eosinophil production. Curr Opin Hematol. 1999;6:164-8. (Pubitemid 29467540)
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. (Pubitemid 37463214)
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.
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. (Pubitemid 26161942)
35. Jong EC, Mahmoud AA, Klebanoff SJ. Peroxidase-mediated toxicity to schistosomula of Schistosoma mansoni. J Immunol. 1981;126:468-71. (Pubitemid 11136695)
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. (Pubitemid 34967541)
37. Spalteholz H, Panasenko OM, Arnhold J. Formation of reactive halide species by myeloperoxidase and eosinophil peroxidase. Arch Biochem Biophys. 2006;445:225-34. (Pubitemid 43082215)
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. (Pubitemid 36150751)
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.
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.
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. (Pubitemid 26161943)
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. (Pubitemid 44264410)
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. (Pubitemid 24129712)
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. (Pubitemid 16175274)
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. (Pubitemid 351411946)
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. (Pubitemid 43794511)
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. (Pubitemid 32852553)
48. Shi HZ. Eosinophils function as antigen-presenting cells. J Leukoc Biol. 2004;76:520-7.
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. (Pubitemid 28558171)
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. (Pubitemid 34205735)
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. (Pubitemid 24186533)
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. (Pubitemid 21914775)
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.
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. (Pubitemid 23202087)
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. (Pubitemid 27046945)
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. (Pubitemid 351171236)
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. (Pubitemid 47417976)
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.
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.
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. (Pubitemid 46944444)
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 IFNgamma production in mice. Parasite Immunol. 2010;32:370-83.
63. Paterson S, Wilkes C, Bleay C, Viney ME. Immunological responses elicited by different infection regimes with Strongyloides ratti. PLoS One. 2008;3:e2509.
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.
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. (Pubitemid 351959860)
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. (Pubitemid 20022739)
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. (Pubitemid 41740319)
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. (Pubitemid 37428329)
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. (Pubitemid 36323516)
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. (Pubitemid 36362787)
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. (Pubitemid 41713448)
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. (Pubitemid 46149414)
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. (Pubitemid 34225278)
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. (Pubitemid 37475312)
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. (Pubitemid 26005621)
77. Murrell KD. Protective role of immunoglobulin G in immunity to Strongyloides ratti. J Parasitol. 1981;67:167-73. (Pubitemid 11000413)
78. Dawkins HJ, Grove DI. Transfer by serum and cells of resistance to infection with Strongyloides ratti in mice. Immunology. 1981;43:317-22. (Pubitemid 11031810)
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.
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. (Pubitemid 40470831)
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.
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. (Pubitemid 38457254)
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.