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Published in: Immunologic Research 1-2/2012

01-04-2012 | Immunology in Serbia

Trichinella spiralis: shaping the immune response

Authors: Natasa Ilic, Alisa Gruden-Movsesijan, Ljiljana Sofronic-Milosavljevic

Published in: Immunologic Research | Issue 1-2/2012

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Abstract

The co-evolution of a wide range of helminth parasites and vertebrates represented a constant pressure on the host’s immune system and a selective force for shaping the immune response. Modulation of the immune system by parasites is accomplished partly by dendritic cells. When exposed to helminth parasites or their products, dendritic cells do not become classically mature and are potent inducers of Th2 and regulatory responses. Treating animals with helminths (eggs, larvae, extracts) causes dampening or in some cases prevention of allergic or autoimmune diseases. Trichinella spiralis (T. spiralis) possess a capacity to retune the immune cell repertoire, acting as a moderator of the host response not only to itself but also to third party antigens. In this review, we will focus on the ability of T. spiralis-stimulated dendritic cells to polarize the immune response toward Th2 and regulatory mode in vitro and in vivo and also on the capacity of this parasite to modulate autoimmune disease—such as experimental autoimmune encephalomyelitis.
Literature
1.
go back to reference Allen JE, Maizels RM. Diversity and dialogue in immunity to helminths. Nat Rev Immunol. 2011;11:375–88.PubMedCrossRef Allen JE, Maizels RM. Diversity and dialogue in immunity to helminths. Nat Rev Immunol. 2011;11:375–88.PubMedCrossRef
2.
go back to reference Matisz CE, McDougall JJ, Sharkey KA, McKay DM. Helminth parasite and the modulation of joint inflammation. J Parasitol Res. 2011;2022:942616. Matisz CE, McDougall JJ, Sharkey KA, McKay DM. Helminth parasite and the modulation of joint inflammation. J Parasitol Res. 2011;2022:942616.
3.
go back to reference Fleming JO. Helminths and multiple sclerosis: will old friend give us new treatment for MS? J Neuroimmunol. 2011;233:3–5.PubMedCrossRef Fleming JO. Helminths and multiple sclerosis: will old friend give us new treatment for MS? J Neuroimmunol. 2011;233:3–5.PubMedCrossRef
4.
go back to reference Fleming JO, Issak A, Lee JE, Luzzio CC, Carrithers MD, Cook TD, Field AS, Boland J, Fabry Z. Probiotic helminth administration in relapsing-remiting multiple sclerosis: a phase 1 study. Mult Scler. 2011;17:743–54.PubMedCrossRef Fleming JO, Issak A, Lee JE, Luzzio CC, Carrithers MD, Cook TD, Field AS, Boland J, Fabry Z. Probiotic helminth administration in relapsing-remiting multiple sclerosis: a phase 1 study. Mult Scler. 2011;17:743–54.PubMedCrossRef
5.
go back to reference He Y, Li Y, Zhuang W, Lin Y, Chen C, Li J, Chi F, Bai Y, Chen XP. The inhibitory effect against collagen-induced arthritis by Schistosoma japonicum infection is infection stage dependent. BMC Immunol. 2010;11:28–37.PubMedCrossRef He Y, Li Y, Zhuang W, Lin Y, Chen C, Li J, Chi F, Bai Y, Chen XP. The inhibitory effect against collagen-induced arthritis by Schistosoma japonicum infection is infection stage dependent. BMC Immunol. 2010;11:28–37.PubMedCrossRef
7.
go back to reference Reis e Sousa C, Hieny S, Scharton-Kersten T, Jankovic D, Charest H, Germain R, Sher A. In vivo microbial stimulation induces rapid CD40L-independent production of IL-12 by dendritic cells and their re-distribution to T-cell areas. J Exp Med. 1997;186:1819–29.PubMedCrossRef Reis e Sousa C, Hieny S, Scharton-Kersten T, Jankovic D, Charest H, Germain R, Sher A. In vivo microbial stimulation induces rapid CD40L-independent production of IL-12 by dendritic cells and their re-distribution to T-cell areas. J Exp Med. 1997;186:1819–29.PubMedCrossRef
8.
go back to reference Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE. Helminth parasites—masters of regulation. Immunol Rev. 2004;201:89–116.PubMedCrossRef Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE. Helminth parasites—masters of regulation. Immunol Rev. 2004;201:89–116.PubMedCrossRef
9.
go back to reference van Riet E, Everts B, Retra K, Phylipsen M, van Hellemond JJ, Tielens AGM, van der Kleij D, Hartgerts FC, Yazdanbakhsh M. Combined TLR-2 and TLR-4 ligation in the context of bacterial or helminth extracts in human monocyte derived dendritic cells: molecular correlation for Th1/Th2 polarization. BMC Immunol. 2009;10:9–20.PubMedCrossRef van Riet E, Everts B, Retra K, Phylipsen M, van Hellemond JJ, Tielens AGM, van der Kleij D, Hartgerts FC, Yazdanbakhsh M. Combined TLR-2 and TLR-4 ligation in the context of bacterial or helminth extracts in human monocyte derived dendritic cells: molecular correlation for Th1/Th2 polarization. BMC Immunol. 2009;10:9–20.PubMedCrossRef
10.
go back to reference Cervi L, MacDonald A, Kane C, Dzierszinski F, Pearce EJ. Cutting edge: dendritic cells copulsed with microbial and helminh antigens undergo modified maturation, segregate the antigens to distinct intracellular compartments, and concurrently induce microbe-specific Th1 and helminth-specific Th2 responses. J Immunol. 2004;172:2016–20.PubMed Cervi L, MacDonald A, Kane C, Dzierszinski F, Pearce EJ. Cutting edge: dendritic cells copulsed with microbial and helminh antigens undergo modified maturation, segregate the antigens to distinct intracellular compartments, and concurrently induce microbe-specific Th1 and helminth-specific Th2 responses. J Immunol. 2004;172:2016–20.PubMed
11.
go back to reference Whelan M, Harnett MM, Houston KM, Patel V, Harnett W, Rigley KP. Filaral nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J Immunol. 2000;164:6453–60.PubMed Whelan M, Harnett MM, Houston KM, Patel V, Harnett W, Rigley KP. Filaral nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J Immunol. 2000;164:6453–60.PubMed
12.
go back to reference Balic A, Harcus Y, Holland MJ, Maizels RM. Selective maturation of dendritic cells by Nippostongylus brasiliensis-secreted proteins drives Th2 immune responses. Eur J Immunol. 2004;34:3047–59.PubMedCrossRef Balic A, Harcus Y, Holland MJ, Maizels RM. Selective maturation of dendritic cells by Nippostongylus brasiliensis-secreted proteins drives Th2 immune responses. Eur J Immunol. 2004;34:3047–59.PubMedCrossRef
13.
go back to reference Grainger JR, Smith KA, Hewitson JP, McSorley HJ, Harcus Y, Filbey KJ, Finney CA, Greenwood EJ, Knox DP, Wilson MS, Belkaid Y, Rudensky AY, Maizels RM. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-b pathway. J Exp Med. 2010;207:2331–41.PubMedCrossRef Grainger JR, Smith KA, Hewitson JP, McSorley HJ, Harcus Y, Filbey KJ, Finney CA, Greenwood EJ, Knox DP, Wilson MS, Belkaid Y, Rudensky AY, Maizels RM. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-b pathway. J Exp Med. 2010;207:2331–41.PubMedCrossRef
14.
go back to reference Beiting DP, Gagliardo LF, Hesse M, Bliss SK, Meskill D, Appleton JA. Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T Cells, and TGF-b. J Immunol. 2007;178:1039–47.PubMed Beiting DP, Gagliardo LF, Hesse M, Bliss SK, Meskill D, Appleton JA. Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T Cells, and TGF-b. J Immunol. 2007;178:1039–47.PubMed
15.
go back to reference Wu Z, Sofronic-Milosavljevic Lj, Nagano, Takahashi Y. Trichinella spiralis: nurse cell formation with emphasis on analogy to muscle cell repair. Parasit Vectors. 2008;1:27.PubMedCrossRef Wu Z, Sofronic-Milosavljevic Lj, Nagano, Takahashi Y. Trichinella spiralis: nurse cell formation with emphasis on analogy to muscle cell repair. Parasit Vectors. 2008;1:27.PubMedCrossRef
16.
go back to reference Nagano I, Wu Y, Takahashi Y. Functional genes and proteins of Trichinella spp. Parasitol Res. 2009;104:197–207.PubMedCrossRef Nagano I, Wu Y, Takahashi Y. Functional genes and proteins of Trichinella spp. Parasitol Res. 2009;104:197–207.PubMedCrossRef
17.
go back to reference Else KJ. Have gastrointestinal nematode outwitted the immune system? Parasite Immunol. 2005;27:407–15.PubMedCrossRef Else KJ. Have gastrointestinal nematode outwitted the immune system? Parasite Immunol. 2005;27:407–15.PubMedCrossRef
18.
go back to reference Mosmann TR. Cytokine secretion patterns and cross-regulation of T cell subsets. Immunol Res. 1991;10:183–8.PubMedCrossRef Mosmann TR. Cytokine secretion patterns and cross-regulation of T cell subsets. Immunol Res. 1991;10:183–8.PubMedCrossRef
19.
go back to reference Ishikawa N, Goyal PK, Mahida YR, Li FP, Wakelin D. Early cytokine responses during intestinal parasitic infections. Immunology. 1998;93:257–63.PubMedCrossRef Ishikawa N, Goyal PK, Mahida YR, Li FP, Wakelin D. Early cytokine responses during intestinal parasitic infections. Immunology. 1998;93:257–63.PubMedCrossRef
20.
go back to reference Finney CAM, Taylor MD, Wilson MS, Maizels RM. Expansion and activation of CD4+CD25+ regulatory T cells in Heligmosomoides polygyrus infection. Eur J Immunol. 2007;37:1874–86.PubMedCrossRef Finney CAM, Taylor MD, Wilson MS, Maizels RM. Expansion and activation of CD4+CD25+ regulatory T cells in Heligmosomoides polygyrus infection. Eur J Immunol. 2007;37:1874–86.PubMedCrossRef
21.
go back to reference Taylor JJ, Mohrs M, Pearce EJ. Regulatory T cell responses develop in parallel to Th responses, and control the magnitude and phenotype of the Th effector population. J Immunol. 2006;176:5839–47.PubMed Taylor JJ, Mohrs M, Pearce EJ. Regulatory T cell responses develop in parallel to Th responses, and control the magnitude and phenotype of the Th effector population. J Immunol. 2006;176:5839–47.PubMed
22.
go back to reference Sher A, Pearce E, Kaye P. Shaping the immune response to parasites: role of dendritic cells. Curr Opin Immunol. 2003;15:421–9.PubMedCrossRef Sher A, Pearce E, Kaye P. Shaping the immune response to parasites: role of dendritic cells. Curr Opin Immunol. 2003;15:421–9.PubMedCrossRef
23.
go back to reference Kane CM, Cervi L, Sun J, McKee AS, Masek KS, Shapira S, Hunter CA, Pearce EJ. Helminth antigens modulate TLR-initiated dendritic cell activation. J Immunol. 2004;173:7454–61.PubMed Kane CM, Cervi L, Sun J, McKee AS, Masek KS, Shapira S, Hunter CA, Pearce EJ. Helminth antigens modulate TLR-initiated dendritic cell activation. J Immunol. 2004;173:7454–61.PubMed
24.
go back to reference Segura M, Su Z, Piccirillo C, Stevenson MM. Impairment of dendritic cell function by excretory-secretory products: a potentiaol mechanism for nematode-induced immunosuppression. Eur J Immunol. 2007;37:1887–904.PubMedCrossRef Segura M, Su Z, Piccirillo C, Stevenson MM. Impairment of dendritic cell function by excretory-secretory products: a potentiaol mechanism for nematode-induced immunosuppression. Eur J Immunol. 2007;37:1887–904.PubMedCrossRef
25.
go back to reference van Riet E, Hartgers FC, Yazdanbakhsh M. Chronic helminth infections induce immuno-modulation: consequences and mechanisms. Immunobiology. 2007;212:475–90.PubMedCrossRef van Riet E, Hartgers FC, Yazdanbakhsh M. Chronic helminth infections induce immuno-modulation: consequences and mechanisms. Immunobiology. 2007;212:475–90.PubMedCrossRef
26.
27.
go back to reference Ilic N, Colic M, Gruden-Movsesijan A, Majstorovic I, Vasilev S, Sofronic-Milosavljevic Lj. Characterization of rat bone marrow dendritic cells initially primed by Trichinella spiralis antigens. Parasite Immunol. 2008;30:491–5.PubMedCrossRef Ilic N, Colic M, Gruden-Movsesijan A, Majstorovic I, Vasilev S, Sofronic-Milosavljevic Lj. Characterization of rat bone marrow dendritic cells initially primed by Trichinella spiralis antigens. Parasite Immunol. 2008;30:491–5.PubMedCrossRef
28.
go back to reference Ilic N, Worthington JJ, Gruden-Movsesijan A, Travis MA, Sofronic-Milosavljevic Lj, Grencis RK. Trichinella spiralis antigens prime mixed Th1/Th2 response but do not induce de novo generation of Foxp3+ T cells in vitro. Parasite Immunol. 2011;33:572–82.PubMedCrossRef Ilic N, Worthington JJ, Gruden-Movsesijan A, Travis MA, Sofronic-Milosavljevic Lj, Grencis RK. Trichinella spiralis antigens prime mixed Th1/Th2 response but do not induce de novo generation of Foxp3+ T cells in vitro. Parasite Immunol. 2011;33:572–82.PubMedCrossRef
29.
go back to reference Leech MD, Grencis RK. Induction of enhanced immunity to intestinal nematodes using IL-9-producing dendritic cells. J Immunol. 2006;176:2505–11.PubMed Leech MD, Grencis RK. Induction of enhanced immunity to intestinal nematodes using IL-9-producing dendritic cells. J Immunol. 2006;176:2505–11.PubMed
30.
go back to reference Langelaar M, Aranzamendi C, Franssen F, van der Giessen J, Rutten V, van der Ley P, Pinelli E. Suppresion of dendritic cells matiuration by Trichinella spiralis excretory/secretory products. Parasite Immunol. 2009;31:641–5.PubMedCrossRef Langelaar M, Aranzamendi C, Franssen F, van der Giessen J, Rutten V, van der Ley P, Pinelli E. Suppresion of dendritic cells matiuration by Trichinella spiralis excretory/secretory products. Parasite Immunol. 2009;31:641–5.PubMedCrossRef
31.
go back to reference Thomas PG, Carter MR, Atochina O, Da’Dara AA, Piskorska D, McGuire E, Harn DA. Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J Immunol. 2003;171:5837–41.PubMed Thomas PG, Carter MR, Atochina O, Da’Dara AA, Piskorska D, McGuire E, Harn DA. Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J Immunol. 2003;171:5837–41.PubMed
32.
go back to reference Jenkins SJ, Mountford AP. Dendritic cells activated with product released by Shistosome larvae drive Th2 type immune response which can be inhibited by manipulation of CD40 costimulation. Infect Immun. 2005;73:395–402.PubMedCrossRef Jenkins SJ, Mountford AP. Dendritic cells activated with product released by Shistosome larvae drive Th2 type immune response which can be inhibited by manipulation of CD40 costimulation. Infect Immun. 2005;73:395–402.PubMedCrossRef
33.
go back to reference Marshall FA, Pearce EJ. Uncoupling of induced protein processing from maturation in dendritic cells exposed to a highly antigenic preparation from a helminth parasite. J Immunol. 2008;181:7562–70.PubMed Marshall FA, Pearce EJ. Uncoupling of induced protein processing from maturation in dendritic cells exposed to a highly antigenic preparation from a helminth parasite. J Immunol. 2008;181:7562–70.PubMed
34.
go back to reference Poncini CV, Soto CDA, Batalla E, Solana ME, Gonzalez Cappa SM. Trypanosoma cruzi induces regulatory dendritic cells in vitro≯. Infect Immun. 2008;76:2633–41.PubMedCrossRef Poncini CV, Soto CDA, Batalla E, Solana ME, Gonzalez Cappa SM. Trypanosoma cruzi induces regulatory dendritic cells in vitro≯. Infect Immun. 2008;76:2633–41.PubMedCrossRef
35.
go back to reference Bousheri S, Cao H. New insight into the role of dendritic cells in malaria immune pathogenesis. Trends Parasitol. 2008;24:199–200.PubMedCrossRef Bousheri S, Cao H. New insight into the role of dendritic cells in malaria immune pathogenesis. Trends Parasitol. 2008;24:199–200.PubMedCrossRef
36.
go back to reference Revest M, Donaghy L, Cabilic F, Guiguen C, Gangneux JP. Comparison of the immunomodulatory effects of L. donovani and L. major excreted–secreted antigens, particulate and soluble extracts and viable parasites on human dendritic cells. Vaccine. 2008;26:6119–23.PubMedCrossRef Revest M, Donaghy L, Cabilic F, Guiguen C, Gangneux JP. Comparison of the immunomodulatory effects of L. donovani and L. major excreted–secreted antigens, particulate and soluble extracts and viable parasites on human dendritic cells. Vaccine. 2008;26:6119–23.PubMedCrossRef
37.
go back to reference Wiethe C, Debus A, Mohrs M, Steinkasserer A, Lutz M, Gessner A. Dendritic cell differentiation state and their interaction with NKT cells determine Th1/Th2 differentiation in the murine model of Leishmania major infection1. J Immunol. 2008;180:4371–81.PubMed Wiethe C, Debus A, Mohrs M, Steinkasserer A, Lutz M, Gessner A. Dendritic cell differentiation state and their interaction with NKT cells determine Th1/Th2 differentiation in the murine model of Leishmania major infection1. J Immunol. 2008;180:4371–81.PubMed
38.
go back to reference Manickasingham SP, Edwards AD, Schulz O, Reis e Sousa C. The ability of murine dendritic cell subsets to direct T helper cell differentiation is dependent on microbial signals. Eur J Immunol. 2003;33:101–7.PubMedCrossRef Manickasingham SP, Edwards AD, Schulz O, Reis e Sousa C. The ability of murine dendritic cell subsets to direct T helper cell differentiation is dependent on microbial signals. Eur J Immunol. 2003;33:101–7.PubMedCrossRef
39.
go back to reference Chang JH, Kunkel SL, Chang CH. Negative regulation of MyD88-dependent signaling by IL-10 in dendritic cells. PNAS. 2009;106:18327–32.PubMedCrossRef Chang JH, Kunkel SL, Chang CH. Negative regulation of MyD88-dependent signaling by IL-10 in dendritic cells. PNAS. 2009;106:18327–32.PubMedCrossRef
40.
go back to reference Xio CQ, Kao KJ. Suppression of interleukin-12 production through endogenously secreted interleukin-10 in activated dendritic cells: involvement of activation of extracellular signal-regulated protein kinase. Scand J Immunol. 2003;58:23–32.CrossRef Xio CQ, Kao KJ. Suppression of interleukin-12 production through endogenously secreted interleukin-10 in activated dendritic cells: involvement of activation of extracellular signal-regulated protein kinase. Scand J Immunol. 2003;58:23–32.CrossRef
41.
go back to reference Muthana M, Fairburn B, Mirza S, Slack LK, Hopkinson K, Pockley AG. Identification of a rat bone marrow-derived dendritic cell population which secretes both IL-10 and IL-12: evidence against a reciprocal relationship between IL-10 and IL-12 secretion. Immunobiology. 2006;211:391–402.PubMedCrossRef Muthana M, Fairburn B, Mirza S, Slack LK, Hopkinson K, Pockley AG. Identification of a rat bone marrow-derived dendritic cell population which secretes both IL-10 and IL-12: evidence against a reciprocal relationship between IL-10 and IL-12 secretion. Immunobiology. 2006;211:391–402.PubMedCrossRef
42.
go back to reference Sallusto F, Lanzavecchia A. The instructive role of dendritic cells on T-cell responses. Arthritis Res. 2002;4(suppl3):S127–32.PubMedCrossRef Sallusto F, Lanzavecchia A. The instructive role of dendritic cells on T-cell responses. Arthritis Res. 2002;4(suppl3):S127–32.PubMedCrossRef
43.
go back to reference Carvalho LP, Pearce EJ, Scott P. Functional dichotomy of dendritic cells following interaction with Leishmania braziliensis: infected cells produce high levels of TNF-α, whereas bystander dendritic cells are activated to promote T cell responses. J Immunol. 2008;181:6473–80.PubMed Carvalho LP, Pearce EJ, Scott P. Functional dichotomy of dendritic cells following interaction with Leishmania braziliensis: infected cells produce high levels of TNF-α, whereas bystander dendritic cells are activated to promote T cell responses. J Immunol. 2008;181:6473–80.PubMed
44.
go back to reference Vasquez RE, Xin L, Soong L. Effects of CXCL10 on dendritic cell and CD4+ T-Cell functions during Leishmania amazonensis infection. Infect Immun. 2008;76:161–9.PubMedCrossRef Vasquez RE, Xin L, Soong L. Effects of CXCL10 on dendritic cell and CD4+ T-Cell functions during Leishmania amazonensis infection. Infect Immun. 2008;76:161–9.PubMedCrossRef
45.
go back to reference Shaw J, Grund V, Durling L, Crane D, Caldwell HD. Dendritic cells pulsed with recombinant Chlamydial major outer membrane protein antigen elicit a CD4+ type 2 rather than type 1 immune response that is not protective. Infect Immun. 2002;70:1097–105.PubMedCrossRef Shaw J, Grund V, Durling L, Crane D, Caldwell HD. Dendritic cells pulsed with recombinant Chlamydial major outer membrane protein antigen elicit a CD4+ type 2 rather than type 1 immune response that is not protective. Infect Immun. 2002;70:1097–105.PubMedCrossRef
46.
go back to reference Koyasu S, Moro K, Tanabe M, Takeuchi T. Natural helper cells: a new player in the innate immune response against helminth infection. Adv Immunol. 2010;108:21–44.PubMedCrossRef Koyasu S, Moro K, Tanabe M, Takeuchi T. Natural helper cells: a new player in the innate immune response against helminth infection. Adv Immunol. 2010;108:21–44.PubMedCrossRef
47.
go back to reference Saenz SA, Noti M, Artis D. Innate immune cell populations function as initiators and effectors in Th2 cytokine responses. Trends Immunol. 2010;31:407–13.PubMedCrossRef Saenz SA, Noti M, Artis D. Innate immune cell populations function as initiators and effectors in Th2 cytokine responses. Trends Immunol. 2010;31:407–13.PubMedCrossRef
48.
go back to reference MacDonald AS, Arujo AI, Pearce EJ. Immunology of parasitic helminth infections. Infect Immun. 2002;70:427–33.PubMedCrossRef MacDonald AS, Arujo AI, Pearce EJ. Immunology of parasitic helminth infections. Infect Immun. 2002;70:427–33.PubMedCrossRef
49.
go back to reference Gruden-Movsesijan A, Ilic N, Colic M, Majstorovic I, Radovic I, Sofronic-Milosavljevic Lj. The impact of Trichinella spiralis excretory-secretory products on dendritic cells. Comp Immunol Microbiol Infect Dis. 2011;34:429–39.PubMedCrossRef Gruden-Movsesijan A, Ilic N, Colic M, Majstorovic I, Radovic I, Sofronic-Milosavljevic Lj. The impact of Trichinella spiralis excretory-secretory products on dendritic cells. Comp Immunol Microbiol Infect Dis. 2011;34:429–39.PubMedCrossRef
50.
go back to reference Gruden-Movsesijan A, Ilic N, Mostarica-Stojkovic M, Stosic-Grujicic S, Milic M, Sofronic-Milosavljevic Lj. Mechanisms of modulation of experimental autoimmune encephalomyelitis by Trichinella spiralis infection in Dark Agouti rats. Parasite Immunol. 2010;32:450–9.PubMedCrossRef Gruden-Movsesijan A, Ilic N, Mostarica-Stojkovic M, Stosic-Grujicic S, Milic M, Sofronic-Milosavljevic Lj. Mechanisms of modulation of experimental autoimmune encephalomyelitis by Trichinella spiralis infection in Dark Agouti rats. Parasite Immunol. 2010;32:450–9.PubMedCrossRef
51.
go back to reference Maldonado RA, von Andrian UH. How tolerogenic dendritic cells induce regulatory T cells. Adv Immunol. 2010;108:111–65.PubMedCrossRef Maldonado RA, von Andrian UH. How tolerogenic dendritic cells induce regulatory T cells. Adv Immunol. 2010;108:111–65.PubMedCrossRef
52.
go back to reference Babu S, Blauvelt CP, Kumaraswami V, Nutman TB. Regulatory networks induced by live parasites impair both Th1 and Th2 pathways in patent lymphatic filariasis: implications for parasite persistence. J Immunol. 2006;176:3248–56.PubMed Babu S, Blauvelt CP, Kumaraswami V, Nutman TB. Regulatory networks induced by live parasites impair both Th1 and Th2 pathways in patent lymphatic filariasis: implications for parasite persistence. J Immunol. 2006;176:3248–56.PubMed
53.
go back to reference Sakagushi S, Ono M, Setoguchi R, Yagi H, Hori S, Fehervari Z, Shimizu J, Takahashi T, Nomura T. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev. 2006;212:8–27.CrossRef Sakagushi S, Ono M, Setoguchi R, Yagi H, Hori S, Fehervari Z, Shimizu J, Takahashi T, Nomura T. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev. 2006;212:8–27.CrossRef
54.
go back to reference Okada H, Kuhn C, Feillet H, Bach JF. The “hygiene hypothesis” for autoimmune and allergic diseases: an update. Clin Exp Immunol. 2010;160:1–9.PubMedCrossRef Okada H, Kuhn C, Feillet H, Bach JF. The “hygiene hypothesis” for autoimmune and allergic diseases: an update. Clin Exp Immunol. 2010;160:1–9.PubMedCrossRef
55.
go back to reference Rook GAW. 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: Darwinian medicine and the ‘hygiene’ or ‘old friends’ hypothesis. Clin Exp Immunol. 2010;160:70–9.PubMedCrossRef Rook GAW. 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: Darwinian medicine and the ‘hygiene’ or ‘old friends’ hypothesis. Clin Exp Immunol. 2010;160:70–9.PubMedCrossRef
57.
go back to reference Zaccone P, Fehervari Z, Jones FM, Sidobre S, Kronenberg M, Dunne DW, Cooke A. Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes. Eur J Immunol. 2003;33:1439–49.PubMedCrossRef Zaccone P, Fehervari Z, Jones FM, Sidobre S, Kronenberg M, Dunne DW, Cooke A. Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes. Eur J Immunol. 2003;33:1439–49.PubMedCrossRef
58.
go back to reference Correale J, Farez M. Association between parasite infection and immune responses in multiple sclerosis. Ann Neurol. 2007;61:97–108.PubMedCrossRef Correale J, Farez M. Association between parasite infection and immune responses in multiple sclerosis. Ann Neurol. 2007;61:97–108.PubMedCrossRef
59.
go back to reference Zaccone P, Burton OT, Cooke A. Interplay of parasite-driven immune responses and autoimmunity. Trends Parasitol. 2008;24:35–42.PubMedCrossRef Zaccone P, Burton OT, Cooke A. Interplay of parasite-driven immune responses and autoimmunity. Trends Parasitol. 2008;24:35–42.PubMedCrossRef
60.
go back to reference Maizels RM. Infections and allergy—helminths, hygiene and host immune regulation. Curr Opin Immunol. 2005;17:656–61.PubMedCrossRef Maizels RM. Infections and allergy—helminths, hygiene and host immune regulation. Curr Opin Immunol. 2005;17:656–61.PubMedCrossRef
61.
go back to reference Smits HH, Yazdanbakhsh M. Chronic helminth infections modulate allergen-specific immune responses: protection against development of allergic disorders? Ann Med. 2007;39:428–39.PubMedCrossRef Smits HH, Yazdanbakhsh M. Chronic helminth infections modulate allergen-specific immune responses: protection against development of allergic disorders? Ann Med. 2007;39:428–39.PubMedCrossRef
62.
go back to reference Maizels RM, Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol. 2003;3:733–44.PubMedCrossRef Maizels RM, Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol. 2003;3:733–44.PubMedCrossRef
63.
go back to reference Cooke A, Tonks P, Jones FM, O’Shea H, Hutchings P, Fulford AJ, Dunne DW. Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol. 1999;21:169–76.PubMedCrossRef Cooke A, Tonks P, Jones FM, O’Shea H, Hutchings P, Fulford AJ, Dunne DW. Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol. 1999;21:169–76.PubMedCrossRef
64.
go back to reference La Flamme AC, Ruddenklau U, Backstrom BT. Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infect Immun. 2003;71:4996–5004.PubMedCrossRef La Flamme AC, Ruddenklau U, Backstrom BT. Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infect Immun. 2003;71:4996–5004.PubMedCrossRef
65.
go back to reference Sewell D, Qing Z, Reinke E, Elliott D, Weinstock J, Sandor M, Fabry Z. Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int Immunol. 2003;15:59–69.PubMedCrossRef Sewell D, Qing Z, Reinke E, Elliott D, Weinstock J, Sandor M, Fabry Z. Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int Immunol. 2003;15:59–69.PubMedCrossRef
66.
go back to reference Elliott DE, Li J, Blum A, Metwali A, Qadir K, Urban JF Jr, Weinstock JV. Exposure to schistosomiasis eggs protects mice from TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol. 2003;284:385–91. Elliott DE, Li J, Blum A, Metwali A, Qadir K, Urban JF Jr, Weinstock JV. Exposure to schistosomiasis eggs protects mice from TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol. 2003;284:385–91.
67.
go back to reference Reardon C, Sanchez A, Hogaboam CM, McKay DM. Tapeworm infection reduces epithelial ion transport abnormalities in murine dextran sulfate sodium-induced colitis. Infect Immun. 2001;69:4417–23.PubMedCrossRef Reardon C, Sanchez A, Hogaboam CM, McKay DM. Tapeworm infection reduces epithelial ion transport abnormalities in murine dextran sulfate sodium-induced colitis. Infect Immun. 2001;69:4417–23.PubMedCrossRef
68.
go back to reference McInnes IB, Leung BP, Harnett M, Gracie JA, Liew FI, Harnett W. A novel therapeutic approach targeting articular inflammation using the filarial nematode-derived phosphorylcholine-containing glycoprotein ES-62. J Immunol. 2003;171:2127–33.PubMed McInnes IB, Leung BP, Harnett M, Gracie JA, Liew FI, Harnett W. A novel therapeutic approach targeting articular inflammation using the filarial nematode-derived phosphorylcholine-containing glycoprotein ES-62. J Immunol. 2003;171:2127–33.PubMed
69.
go back to reference Summers RW, Elliott DE, Qadir K, Urban JF Jr, Thomson R, Weinstock JV. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am J Gastroenterol. 2003;98:2034–41.PubMedCrossRef Summers RW, Elliott DE, Qadir K, Urban JF Jr, Thomson R, Weinstock JV. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am J Gastroenterol. 2003;98:2034–41.PubMedCrossRef
70.
go back to reference Summers RW, Elliott DE, Urban JF Jr, Thomson R, Weinstock JV. Trichuris suis therapy in Crohn’s disease. Gut. 2005;54:87–90.PubMedCrossRef Summers RW, Elliott DE, Urban JF Jr, Thomson R, Weinstock JV. Trichuris suis therapy in Crohn’s disease. Gut. 2005;54:87–90.PubMedCrossRef
71.
go back to reference Elliot DE, Satiawan T, Metwali A, Blum A, Urban JF Jr, Weinstock JV. Heligmosomoides polygurus inhibits established colitis in IL10-deficient mice. Eur J Immunol. 2004;34:2690–8.CrossRef Elliot DE, Satiawan T, Metwali A, Blum A, Urban JF Jr, Weinstock JV. Heligmosomoides polygurus inhibits established colitis in IL10-deficient mice. Eur J Immunol. 2004;34:2690–8.CrossRef
72.
go back to reference Khan WI, Blennerhasset PA, Varqhese AK, Chowdhury CK, Omsted P, Deng Y, Collins SM. Intestinal nematode infection ameliorates experimental colitis in mice. Infect Immun. 2002;70:5931–7.PubMedCrossRef Khan WI, Blennerhasset PA, Varqhese AK, Chowdhury CK, Omsted P, Deng Y, Collins SM. Intestinal nematode infection ameliorates experimental colitis in mice. Infect Immun. 2002;70:5931–7.PubMedCrossRef
73.
go back to reference Motomura Y, Wang H, Deng Y, El-Sharkawy RT, Verdu EF, Khan WI. Helminth antigen-based strategy to ameliorate inflammation in an experimental model of colitis. Clin Exp Immunol. 2009;155:88–95.PubMedCrossRef Motomura Y, Wang H, Deng Y, El-Sharkawy RT, Verdu EF, Khan WI. Helminth antigen-based strategy to ameliorate inflammation in an experimental model of colitis. Clin Exp Immunol. 2009;155:88–95.PubMedCrossRef
74.
go back to reference Saunders KA, Raine T, Cooke A, Lawrence CE. Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection. Infect Immun. 2007;75:397–407.PubMedCrossRef Saunders KA, Raine T, Cooke A, Lawrence CE. Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection. Infect Immun. 2007;75:397–407.PubMedCrossRef
75.
go back to reference Gruden-Movsesijan A, Ilic N, Mostarica-Stojkovic M, Stosic-Grujicic S, Milic M, Sofronic-Milosavljevic Lj. Trichinella spiralis: modulation of experimental autoimmune encephalomyelitis in DA rats. Exp Parasitol. 2008;188:641–7.CrossRef Gruden-Movsesijan A, Ilic N, Mostarica-Stojkovic M, Stosic-Grujicic S, Milic M, Sofronic-Milosavljevic Lj. Trichinella spiralis: modulation of experimental autoimmune encephalomyelitis in DA rats. Exp Parasitol. 2008;188:641–7.CrossRef
76.
go back to reference Bettelli E, Nicholson LB, Kuchroo VK. IL-10, a key effector regulatory cytokine in experimental autoimmune encephalomyelitis. J Autoimmun. 2003;20:265–7.PubMedCrossRef Bettelli E, Nicholson LB, Kuchroo VK. IL-10, a key effector regulatory cytokine in experimental autoimmune encephalomyelitis. J Autoimmun. 2003;20:265–7.PubMedCrossRef
77.
go back to reference Mangan NE, Fallon RE, Smith P, van Rooijen N, McKenzie AN, Fallon PG. Helminth infection protects mice from anaphylaxis via IL-10-producing B cells. J Immunol. 2004;173:6346–56.PubMed Mangan NE, Fallon RE, Smith P, van Rooijen N, McKenzie AN, Fallon PG. Helminth infection protects mice from anaphylaxis via IL-10-producing B cells. J Immunol. 2004;173:6346–56.PubMed
78.
go back to reference Tang Q, Bluestone JA. The Foxp3+ regulatory T cell: a jack of all trades, master of regulation. Nat Immunol. 2008;9:239–44.PubMedCrossRef Tang Q, Bluestone JA. The Foxp3+ regulatory T cell: a jack of all trades, master of regulation. Nat Immunol. 2008;9:239–44.PubMedCrossRef
79.
go back to reference Anderton SM, Liblau RS. Regulatory T cells in the control of inflammatory demyelinating diseases of the central nervous system. Curr Opin Neurol. 2008;21:248–54.PubMedCrossRef Anderton SM, Liblau RS. Regulatory T cells in the control of inflammatory demyelinating diseases of the central nervous system. Curr Opin Neurol. 2008;21:248–54.PubMedCrossRef
80.
go back to reference Hewitson JP, Grainger JR, Maizels RM. Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol. 2009;167:1–11.PubMedCrossRef Hewitson JP, Grainger JR, Maizels RM. Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol. 2009;167:1–11.PubMedCrossRef
81.
go back to reference Gruden-Movsesijan A, Sofronic-Milosavljevic Lj. The involvement of macrophage mannose receptor in the innate immune response to infection with parasite Trichinella spiralis. Vet Immunol Immunoparasitol. 2006;109:57–67.CrossRef Gruden-Movsesijan A, Sofronic-Milosavljevic Lj. The involvement of macrophage mannose receptor in the innate immune response to infection with parasite Trichinella spiralis. Vet Immunol Immunoparasitol. 2006;109:57–67.CrossRef
Metadata
Title
Trichinella spiralis: shaping the immune response
Authors
Natasa Ilic
Alisa Gruden-Movsesijan
Ljiljana Sofronic-Milosavljevic
Publication date
01-04-2012
Publisher
Springer-Verlag
Published in
Immunologic Research / Issue 1-2/2012
Print ISSN: 0257-277X
Electronic ISSN: 1559-0755
DOI
https://doi.org/10.1007/s12026-012-8287-5

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