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Published in: Medical Microbiology and Immunology 3/2014

01-06-2014 | Original Investigation

Distinctive cytokine, chemokine, and antibody responses in Echinococcus multilocularis-infected patients with cured, stable, or progressive disease

Authors: Xiangsheng Huang, Beate Grüner, Christian J. Lechner, Peter Kern, Peter T. Soboslay

Published in: Medical Microbiology and Immunology | Issue 3/2014

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Abstract

Metacestode larvae of the tapeworm Echinococcus multilocularis can cause alveolar echinococcosis (AE), a severe parasitic disease in man, which, if it remains untreated, may cause organ failure and death. Spontaneous and parasite antigen-induced cellular responses were studied in patients with cured, stable, and progressive AE to differentiate the response profiles between the distinct states of infection. Antibody reactivity was evaluated in AE patients with cured, stable, and progressive disease. The spontaneous cellular release of pro-inflammatory IL-31 and IL-33 was clearly depressed in all AE patients, while regulatory IL-27, anti-inflammatory SDF-1/CXCL12, and eosinophil granulocyte attracting Eotaxin-1, Eotaxin-2, and Eotaxin-3 (CCL11, CCL24, CCL26) were enhanced with disease progression. Such distinctive response profiles could be applied for monitoring of AE disease progression or regression. E. multilocularis metacestode (Em) antigens (entire metacestode EmAg as well as EmVesicles) stimulated in vitro IL-31, IL-33, Eotaxin-1, Eotaxin-3, and CXCL12 cytokine and chemokine responses, which were similarly present in all AE patient groups, while regulatory IL-27 was suppressed and pro-inflammatory Eotaxin-2 was enhanced. E. multilocularis metacestode-specific IgG1, IgG3, and IgE responses progressively diminished with regression from active to stable and cured AE. IgG2 and IgG4 reactivity remained similarly high in stable and progressive cases, and lessened only with cured AE. Antibody reactivity against E. multilocularis vesicle antigen distinctively separated between cured, stable, or progressive AE, with the exception of IgG4. In sum, the combined and longitudinal study of several cytokines and chemokines, together with the evaluation of E. multilocularis vesicle-specific antibody responses, should provide a better understanding of the immune response during progression and regression of AE, and may help to improve the staging of AE patients.
Literature
1.
go back to reference Gottstein B, Saucy F, Deplazes P, Reichen J, Demierre G, Busato A, Zuercher C, Pugin P (2001) Is high prevalence of Echinococcus multilocularis in wild and domestic animals associated with disease incidence in humans? Emerg Infect Dis 7(3):408–412PubMedCentralPubMedCrossRef Gottstein B, Saucy F, Deplazes P, Reichen J, Demierre G, Busato A, Zuercher C, Pugin P (2001) Is high prevalence of Echinococcus multilocularis in wild and domestic animals associated with disease incidence in humans? Emerg Infect Dis 7(3):408–412PubMedCentralPubMedCrossRef
2.
go back to reference Bresson-Hadni S, Laplante JJ, Lenys D, Rohmer P, Gottstein B, Jacquier P, Mercet P, Meyer JP, Miguet JP, Vuitton DA (1994) Seroepidemiologic screening of Echinococcus multilocularis infection in a European area endemic for alveolar echinococcosis. Am J Trop Med Hyg 51(6):837–846PubMed Bresson-Hadni S, Laplante JJ, Lenys D, Rohmer P, Gottstein B, Jacquier P, Mercet P, Meyer JP, Miguet JP, Vuitton DA (1994) Seroepidemiologic screening of Echinococcus multilocularis infection in a European area endemic for alveolar echinococcosis. Am J Trop Med Hyg 51(6):837–846PubMed
3.
go back to reference Rausch RL, Wilson JF, Schantz PM, McMahon BJ (1987) Spontaneous death of Echinococcus multilocularis: cases diagnosed serologically (by Em2 ELISA) and clinical significance. Am J Trop Med Hyg 36(3):576–585PubMed Rausch RL, Wilson JF, Schantz PM, McMahon BJ (1987) Spontaneous death of Echinococcus multilocularis: cases diagnosed serologically (by Em2 ELISA) and clinical significance. Am J Trop Med Hyg 36(3):576–585PubMed
4.
5.
go back to reference Maizels RM, Sartono E, Kurniawan A, Partono F, Selkirk ME, Yazdanbakhsh M (1995) T-cell activation and the balance of antibody isotypes in human lymphatic filariasis. Parasitol Today 11(2):50–56PubMedCrossRef Maizels RM, Sartono E, Kurniawan A, Partono F, Selkirk ME, Yazdanbakhsh M (1995) T-cell activation and the balance of antibody isotypes in human lymphatic filariasis. Parasitol Today 11(2):50–56PubMedCrossRef
6.
go back to reference Hagan P, Blumenthal UJ, Dunn D, Simpson AJ, Wilkins HA (1991) Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349(6306):243–245PubMedCrossRef Hagan P, Blumenthal UJ, Dunn D, Simpson AJ, Wilkins HA (1991) Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349(6306):243–245PubMedCrossRef
7.
go back to reference Mosmann TR, Sad S (1996) The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 17(3):138–146PubMedCrossRef Mosmann TR, Sad S (1996) The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 17(3):138–146PubMedCrossRef
8.
go back to reference Dreweck CM, Luder CG, Soboslay PT, Kern P (1997) Subclass-specific serological reactivity and IgG4-specific antigen recognition in human echinococcosis. Trop Med Int Health 2(8):779–787PubMedCrossRef Dreweck CM, Luder CG, Soboslay PT, Kern P (1997) Subclass-specific serological reactivity and IgG4-specific antigen recognition in human echinococcosis. Trop Med Int Health 2(8):779–787PubMedCrossRef
9.
go back to reference Wen H, Craig PS, Ito A, Vuitton DA, Bresson-Hadni S, Allan JC, Rogan MT, Paollilo E, Shambesh M (1995) Immunoblot evaluation of IgG and IgG-subclass antibody responses for immunodiagnosis of human alveolar echinococcosis. Ann Trop Med Parasitol 89(5):485–495PubMed Wen H, Craig PS, Ito A, Vuitton DA, Bresson-Hadni S, Allan JC, Rogan MT, Paollilo E, Shambesh M (1995) Immunoblot evaluation of IgG and IgG-subclass antibody responses for immunodiagnosis of human alveolar echinococcosis. Ann Trop Med Parasitol 89(5):485–495PubMed
10.
go back to reference Tappe D, Gruner B, Kern P, Frosch M (2008) Evaluation of a commercial Echinococcus Western Blot assay for serological follow-up of patients with alveolar echinococcosis. Clin Vaccine Immunol 15(11):1633–1637PubMedCentralPubMedCrossRef Tappe D, Gruner B, Kern P, Frosch M (2008) Evaluation of a commercial Echinococcus Western Blot assay for serological follow-up of patients with alveolar echinococcosis. Clin Vaccine Immunol 15(11):1633–1637PubMedCentralPubMedCrossRef
11.
go back to reference Vuitton DA (2003) The ambiguous role of immunity in echinococcosis: protection of the host or of the parasite? Acta Trop 85(2):119–132PubMedCrossRef Vuitton DA (2003) The ambiguous role of immunity in echinococcosis: protection of the host or of the parasite? Acta Trop 85(2):119–132PubMedCrossRef
12.
go back to reference Sturm D, Menzel J, Gottstein B, Kern P (1995) Interleukin-5 is the predominant cytokine produced by peripheral blood mononuclear cells in alveolar echinococcosis. Infect Immun 63(5):1688–1697PubMedCentralPubMed Sturm D, Menzel J, Gottstein B, Kern P (1995) Interleukin-5 is the predominant cytokine produced by peripheral blood mononuclear cells in alveolar echinococcosis. Infect Immun 63(5):1688–1697PubMedCentralPubMed
13.
go back to reference Godot V, Harraga S, Beurton I, Deschaseaux M, Sarciron E, Gottstein B, Vuitton DA (2000) Resistance/susceptibility to Echinococcus multilocularis infection and cytokine profile in humans. I. Comparison of patients with progressive and abortive lesions. Clin Exp Immunol 121(3):484–490PubMedCentralPubMedCrossRef Godot V, Harraga S, Beurton I, Deschaseaux M, Sarciron E, Gottstein B, Vuitton DA (2000) Resistance/susceptibility to Echinococcus multilocularis infection and cytokine profile in humans. I. Comparison of patients with progressive and abortive lesions. Clin Exp Immunol 121(3):484–490PubMedCentralPubMedCrossRef
14.
go back to reference Hubner MP, Manfras BJ, Margos MC, Eiffler D, Hoffmann WH, Schulz-Key H, Kern P, Soboslay PT (2006) Echinococcus multilocularis metacestodes modulate cellular cytokine and chemokine release by peripheral blood mononuclear cells in alveolar echinococcosis patients. Clin Exp Immunol 145(2):243–251PubMedCentralPubMedCrossRef Hubner MP, Manfras BJ, Margos MC, Eiffler D, Hoffmann WH, Schulz-Key H, Kern P, Soboslay PT (2006) Echinococcus multilocularis metacestodes modulate cellular cytokine and chemokine release by peripheral blood mononuclear cells in alveolar echinococcosis patients. Clin Exp Immunol 145(2):243–251PubMedCentralPubMedCrossRef
15.
go back to reference Lechner CJ, Gruner B, Huang X, Hoffmann WH, Kern P, Soboslay PT (2012) Parasite-specific IL-17-type cytokine responses and soluble IL-17 receptor levels in alveolar echinococcosis patients. Clin Dev Immunol 2012:735342PubMedCentralPubMedCrossRef Lechner CJ, Gruner B, Huang X, Hoffmann WH, Kern P, Soboslay PT (2012) Parasite-specific IL-17-type cytokine responses and soluble IL-17 receptor levels in alveolar echinococcosis patients. Clin Dev Immunol 2012:735342PubMedCentralPubMedCrossRef
16.
go back to reference Shin HD, Kim LH, Park BL, Jung JH, Kim JY, Chung IY, Kim JS, Lee JH, Chung SH, Kim YH, Park HS, Choi JH, Lee YM, Park SW, Choi BW, Hong SJ, Park CS (2003) Association of Eotaxin gene family with asthma and serum total IgE. Hum Mol Genet 12(11):1279–1285PubMedCrossRef Shin HD, Kim LH, Park BL, Jung JH, Kim JY, Chung IY, Kim JS, Lee JH, Chung SH, Kim YH, Park HS, Choi JH, Lee YM, Park SW, Choi BW, Hong SJ, Park CS (2003) Association of Eotaxin gene family with asthma and serum total IgE. Hum Mol Genet 12(11):1279–1285PubMedCrossRef
17.
go back to reference Sousa-Pereira SR, Teixeira AL, Silva LC, Souza AL, Antunes CM, Teixeira MM, Lambertucci JR (2006) Serum and cerebral spinal fluid levels of chemokines and Th2 cytokines in Schistosoma mansoni myeloradiculopathy. Parasite Immunol 28(9):473–478PubMedCrossRef Sousa-Pereira SR, Teixeira AL, Silva LC, Souza AL, Antunes CM, Teixeira MM, Lambertucci JR (2006) Serum and cerebral spinal fluid levels of chemokines and Th2 cytokines in Schistosoma mansoni myeloradiculopathy. Parasite Immunol 28(9):473–478PubMedCrossRef
18.
go back to reference Charlot-Rabiega P, Bardel E, Dietrich C, Kastelein R, Devergne O (2011) Signaling events involved in interleukin 27 (IL-27)-induced proliferation of human naive CD4+ T cells and B cells. J Biol Chem 286(31):27350–27362PubMedCentralPubMedCrossRef Charlot-Rabiega P, Bardel E, Dietrich C, Kastelein R, Devergne O (2011) Signaling events involved in interleukin 27 (IL-27)-induced proliferation of human naive CD4+ T cells and B cells. J Biol Chem 286(31):27350–27362PubMedCentralPubMedCrossRef
19.
go back to reference Schneider R, Yaneva T, Beauseigle D, El-Khoury L, Arbour N (2011) IL-27 increases the proliferation and effector functions of human naive CD8+ T lymphocytes and promotes their development into Tc1 cells. Eur J Immunol 41(1):47–59PubMedCrossRef Schneider R, Yaneva T, Beauseigle D, El-Khoury L, Arbour N (2011) IL-27 increases the proliferation and effector functions of human naive CD8+ T lymphocytes and promotes their development into Tc1 cells. Eur J Immunol 41(1):47–59PubMedCrossRef
20.
go back to reference Guzzo C, Che Mat NF, Gee K (2010) Interleukin-27 induces a STAT1/3- and NF-kappaB-dependent proinflammatory cytokine profile in human monocytes. J Biol Chem 285(32):24404–24411PubMedCentralPubMedCrossRef Guzzo C, Che Mat NF, Gee K (2010) Interleukin-27 induces a STAT1/3- and NF-kappaB-dependent proinflammatory cytokine profile in human monocytes. J Biol Chem 285(32):24404–24411PubMedCentralPubMedCrossRef
21.
go back to reference Ezzat MH, Hasan ZE, Shaheen KY (2011) Serum measurement of interleukin-31 (IL-31) in paediatric atopic dermatitis: elevated levels correlate with severity scoring. J Eur Acad Dermatol Venereol 25(3):334–339PubMedCrossRef Ezzat MH, Hasan ZE, Shaheen KY (2011) Serum measurement of interleukin-31 (IL-31) in paediatric atopic dermatitis: elevated levels correlate with severity scoring. J Eur Acad Dermatol Venereol 25(3):334–339PubMedCrossRef
22.
go back to reference Dillon SR, Sprecher C, Hammond A, Bilsborough J, Rosenfeld-Franklin M, Presnell SR, Haugen HS, Maurer M, Harder B, Johnston J, Bort S, Mudri S, Kuijper JL, Bukowski T, Shea P, Dong DL, Dasovich M, Grant FJ, Lockwood L, Levin SD, LeCiel C, Waggie K, Day H, Topouzis S, Kramer J, Kuestner R, Chen Z, Foster D, Parrish-Novak J, Gross JA (2004) Interleukin 31, a cytokine produced by activated T cells, induces dermatitis in mice. Nat Immunol 5(7):752–760PubMedCrossRef Dillon SR, Sprecher C, Hammond A, Bilsborough J, Rosenfeld-Franklin M, Presnell SR, Haugen HS, Maurer M, Harder B, Johnston J, Bort S, Mudri S, Kuijper JL, Bukowski T, Shea P, Dong DL, Dasovich M, Grant FJ, Lockwood L, Levin SD, LeCiel C, Waggie K, Day H, Topouzis S, Kramer J, Kuestner R, Chen Z, Foster D, Parrish-Novak J, Gross JA (2004) Interleukin 31, a cytokine produced by activated T cells, induces dermatitis in mice. Nat Immunol 5(7):752–760PubMedCrossRef
23.
go back to reference Suzukawa M, Koketsu R, Iikura M, Nakae S, Matsumoto K, Nagase H, Saito H, Matsushima K, Ohta K, Yamamoto K, Yamaguchi M (2008) Interleukin-33 enhances adhesion, CD11b expression and survival in human eosinophils. Lab Invest 88(11):1245–1253PubMedCrossRef Suzukawa M, Koketsu R, Iikura M, Nakae S, Matsumoto K, Nagase H, Saito H, Matsushima K, Ohta K, Yamamoto K, Yamaguchi M (2008) Interleukin-33 enhances adhesion, CD11b expression and survival in human eosinophils. Lab Invest 88(11):1245–1253PubMedCrossRef
24.
go back to reference Yasuoka S, Kawanokuchi J, Parajuli B, Jin S, Doi Y, Noda M, Sonobe Y, Takeuchi H, Mizuno T, Suzumura A (2011) Production and functions of IL-33 in the central nervous system. Brain Res 1385:8–17PubMedCrossRef Yasuoka S, Kawanokuchi J, Parajuli B, Jin S, Doi Y, Noda M, Sonobe Y, Takeuchi H, Mizuno T, Suzumura A (2011) Production and functions of IL-33 in the central nervous system. Brain Res 1385:8–17PubMedCrossRef
26.
go back to reference Kern P, Wen H, Sato N, Vuitton DA, Gruener B, Shao Y, Delabrousse E, Kratzer W, Bresson-Hadni S (2006) WHO classification of alveolar echinococcosis: principles and application. Parasitol Int 55(Suppl):S283–S287PubMedCrossRef Kern P, Wen H, Sato N, Vuitton DA, Gruener B, Shao Y, Delabrousse E, Kratzer W, Bresson-Hadni S (2006) WHO classification of alveolar echinococcosis: principles and application. Parasitol Int 55(Suppl):S283–S287PubMedCrossRef
27.
go back to reference Dreweck CM, Soboslay PT, Schulz-Key H, Gottstein B, Kern P (1999) Cytokine and chemokine secretion by human peripheral blood cells in response to viable Echinococcus multilocularis metacestode vesicles. Parasite Immunol 21(8):433–438PubMedCrossRef Dreweck CM, Soboslay PT, Schulz-Key H, Gottstein B, Kern P (1999) Cytokine and chemokine secretion by human peripheral blood cells in response to viable Echinococcus multilocularis metacestode vesicles. Parasite Immunol 21(8):433–438PubMedCrossRef
28.
go back to reference Hemphill A, Stettler M, Walker M, Siles-Lucas M, Fink R, Gottstein B (2003) In vitro culture of Echinococcus multilocularis and Echinococcus vogeli metacestodes: studies on the host–parasite interface. Acta Trop 85(2):145–155PubMedCrossRef Hemphill A, Stettler M, Walker M, Siles-Lucas M, Fink R, Gottstein B (2003) In vitro culture of Echinococcus multilocularis and Echinococcus vogeli metacestodes: studies on the host–parasite interface. Acta Trop 85(2):145–155PubMedCrossRef
29.
go back to reference Soboslay PT, Luder CG, Hoffmann WH, Michaelis I, Helling G, Heuschkel C, Dreweck CM, Blanke CH, Pritze S, Banla M et al (1994) Ivermectin-facilitated immunity in onchocerciasis; activation of parasite-specific Th1-type responses with subclinical Onchocerca volvulus infection. Clin Exp Immunol 96(2):238–244PubMedCentralPubMedCrossRef Soboslay PT, Luder CG, Hoffmann WH, Michaelis I, Helling G, Heuschkel C, Dreweck CM, Blanke CH, Pritze S, Banla M et al (1994) Ivermectin-facilitated immunity in onchocerciasis; activation of parasite-specific Th1-type responses with subclinical Onchocerca volvulus infection. Clin Exp Immunol 96(2):238–244PubMedCentralPubMedCrossRef
30.
go back to reference Kocherscheidt L, Flakowski AK, Gruner B, Hamm DM, Dietz K, Kern P, Soboslay PT (2008) Echinococcus multilocularis: inflammatory and regulatory chemokine responses in patients with progressive, stable and cured alveolar echinococcosis. Exp Parasitol 119(4):467–474PubMedCrossRef Kocherscheidt L, Flakowski AK, Gruner B, Hamm DM, Dietz K, Kern P, Soboslay PT (2008) Echinococcus multilocularis: inflammatory and regulatory chemokine responses in patients with progressive, stable and cured alveolar echinococcosis. Exp Parasitol 119(4):467–474PubMedCrossRef
31.
go back to reference Eger A, Kirch A, Manfras B, Kern P, Schulz-Key H, Soboslay PT (2003) Pro-inflammatory (IL-1beta, IL-18) cytokines and IL-8 chemokine release by PBMC in response to Echinococcus multilocularis metacestode vesicles. Parasite Immunol 25(2):103–105PubMedCrossRef Eger A, Kirch A, Manfras B, Kern P, Schulz-Key H, Soboslay PT (2003) Pro-inflammatory (IL-1beta, IL-18) cytokines and IL-8 chemokine release by PBMC in response to Echinococcus multilocularis metacestode vesicles. Parasite Immunol 25(2):103–105PubMedCrossRef
32.
go back to reference Luster AD (2002) The role of chemokines in linking innate and adaptive immunity. Curr Opin Immunol 14(1):129–135PubMedCrossRef Luster AD (2002) The role of chemokines in linking innate and adaptive immunity. Curr Opin Immunol 14(1):129–135PubMedCrossRef
33.
go back to reference Anderson CF, Stumhofer JS, Hunter CA, Sacks D (2009) IL-27 regulates IL-10 and IL-17 from CD4+ cells in nonhealing Leishmania major infection. J Immunol 183(7):4619–4627PubMedCentralPubMedCrossRef Anderson CF, Stumhofer JS, Hunter CA, Sacks D (2009) IL-27 regulates IL-10 and IL-17 from CD4+ cells in nonhealing Leishmania major infection. J Immunol 183(7):4619–4627PubMedCentralPubMedCrossRef
34.
go back to reference Cornelissen C, Luscher-Firzlaff J, Baron JM, Luscher B (2012) Signaling by IL-31 and functional consequences. Eur J Cell Biol 91(6–7):552–566PubMedCrossRef Cornelissen C, Luscher-Firzlaff J, Baron JM, Luscher B (2012) Signaling by IL-31 and functional consequences. Eur J Cell Biol 91(6–7):552–566PubMedCrossRef
35.
go back to reference Kasraie S, Niebuhr M, Werfel T (2010) Interleukin (IL)-31 induces pro-inflammatory cytokines in human monocytes and macrophages following stimulation with staphylococcal exotoxins. Allergy 65(6):712–721PubMedCrossRef Kasraie S, Niebuhr M, Werfel T (2010) Interleukin (IL)-31 induces pro-inflammatory cytokines in human monocytes and macrophages following stimulation with staphylococcal exotoxins. Allergy 65(6):712–721PubMedCrossRef
36.
go back to reference Nile CJ, Barksby E, Jitprasertwong P, Preshaw PM, Taylor JJ (2010) Expression and regulation of interleukin-33 in human monocytes. Immunology 130(2):172–180PubMedCentralPubMedCrossRef Nile CJ, Barksby E, Jitprasertwong P, Preshaw PM, Taylor JJ (2010) Expression and regulation of interleukin-33 in human monocytes. Immunology 130(2):172–180PubMedCentralPubMedCrossRef
37.
go back to reference Rostan O, Gangneux JP, Piquet-Pellorce C, Manuel C, McKenzie AN, Guiguen C, Samson M, Robert-Gangneux F (2013) The IL-33/ST2 axis is associated with human visceral leishmaniasis and suppresses Th1 responses in the livers of BALB/c mice infected with Leishmania donovani. MBio 4(5):e00383–e00413PubMedCentralPubMedCrossRef Rostan O, Gangneux JP, Piquet-Pellorce C, Manuel C, McKenzie AN, Guiguen C, Samson M, Robert-Gangneux F (2013) The IL-33/ST2 axis is associated with human visceral leishmaniasis and suppresses Th1 responses in the livers of BALB/c mice infected with Leishmania donovani. MBio 4(5):e00383–e00413PubMedCentralPubMedCrossRef
38.
go back to reference Jones LA, Roberts F, Nickdel MB, Brombacher F, McKenzie AN, Henriquez FL, Alexander J, Roberts CW (2010) IL-33 receptor (T1/ST2) signalling is necessary to prevent the development of encephalitis in mice infected with Toxoplasma gondii. Eur J Immunol 40(2):426–436PubMedCrossRef Jones LA, Roberts F, Nickdel MB, Brombacher F, McKenzie AN, Henriquez FL, Alexander J, Roberts CW (2010) IL-33 receptor (T1/ST2) signalling is necessary to prevent the development of encephalitis in mice infected with Toxoplasma gondii. Eur J Immunol 40(2):426–436PubMedCrossRef
39.
go back to reference Ayimba E, Hegewald J, Segbena AY, Gantin RG, Lechner CJ, Agosssou A, Banla M, Soboslay PT (2011) Proinflammatory and regulatory cytokines and chemokines in infants with uncomplicated and severe Plasmodium falciparum malaria. Clin Exp Immunol 166(2):218–226PubMedCentralPubMedCrossRef Ayimba E, Hegewald J, Segbena AY, Gantin RG, Lechner CJ, Agosssou A, Banla M, Soboslay PT (2011) Proinflammatory and regulatory cytokines and chemokines in infants with uncomplicated and severe Plasmodium falciparum malaria. Clin Exp Immunol 166(2):218–226PubMedCentralPubMedCrossRef
40.
go back to reference Rakha NK, Dixon JB, Carter SD, Craig PS, Jenkins P, Folkard S (1991) Echinococcus multilocularis antigens modify accessory cell function of macrophages. Immunology 74(4):652–656PubMedCentralPubMed Rakha NK, Dixon JB, Carter SD, Craig PS, Jenkins P, Folkard S (1991) Echinococcus multilocularis antigens modify accessory cell function of macrophages. Immunology 74(4):652–656PubMedCentralPubMed
41.
go back to reference Kizaki T, Ishige M, Bingyan W, Kumagai M, Day NK, Good RA, Onoe K (1993) Interleukin-1-dependent mitogenic responses induced by protoscoleces of Echinococcus multilocularis in murine lymphocytes. J Leukoc Biol 53(3):233–239PubMed Kizaki T, Ishige M, Bingyan W, Kumagai M, Day NK, Good RA, Onoe K (1993) Interleukin-1-dependent mitogenic responses induced by protoscoleces of Echinococcus multilocularis in murine lymphocytes. J Leukoc Biol 53(3):233–239PubMed
42.
go back to reference Kizaki T, Kobayashi S, Ogasawara K, Day NK, Good RA, Onoe K (1991) Immune suppression induced by protoscoleces of Echinococcus multilocularis in mice. Evidence for the presence of CD8dull suppressor cells in spleens of mice intraperitoneally infected with E. multilocularis. J Immunol 147(5):1659–1666PubMed Kizaki T, Kobayashi S, Ogasawara K, Day NK, Good RA, Onoe K (1991) Immune suppression induced by protoscoleces of Echinococcus multilocularis in mice. Evidence for the presence of CD8dull suppressor cells in spleens of mice intraperitoneally infected with E. multilocularis. J Immunol 147(5):1659–1666PubMed
43.
go back to reference Gottstein B, Haag K, Walker M, Matsumoto J, Mejri N, Hemphill A (2006) Molecular survival strategies of Echinococcus multilocularis in the murine host. Parasitol Int 55(Suppl):S45–S49PubMedCrossRef Gottstein B, Haag K, Walker M, Matsumoto J, Mejri N, Hemphill A (2006) Molecular survival strategies of Echinococcus multilocularis in the murine host. Parasitol Int 55(Suppl):S45–S49PubMedCrossRef
44.
go back to reference Emery I, Liance M, Leclerc C (1997) Secondary Echinococcus multilocularis infection in A/J mice: delayed metacestode development is associated with Th1 cytokine production. Parasite Immunol 19(11):493–503PubMedCrossRef Emery I, Liance M, Leclerc C (1997) Secondary Echinococcus multilocularis infection in A/J mice: delayed metacestode development is associated with Th1 cytokine production. Parasite Immunol 19(11):493–503PubMedCrossRef
45.
go back to reference Zhang W, You H, Li J, Zhang Z, Turson G, Aili H, Wang J, McManus DP (2003) Immunoglobulin profiles in a murine intermediate host model of resistance for Echinococcus granulosus infection. Parasite Immunol 25(3):161–168PubMedCrossRef Zhang W, You H, Li J, Zhang Z, Turson G, Aili H, Wang J, McManus DP (2003) Immunoglobulin profiles in a murine intermediate host model of resistance for Echinococcus granulosus infection. Parasite Immunol 25(3):161–168PubMedCrossRef
46.
go back to reference Al-Qaoud KM, Abdel-Hafez SK (2005) Humoral and cytokine response during protection of mice against secondary hydatidosis caused by Echinococcus granulosus. Parasitol Res 98(1):54–60PubMedCrossRef Al-Qaoud KM, Abdel-Hafez SK (2005) Humoral and cytokine response during protection of mice against secondary hydatidosis caused by Echinococcus granulosus. Parasitol Res 98(1):54–60PubMedCrossRef
47.
go back to reference Jenne L, Kilwinski J, Scheffold W, Kern P (1997) IL-5 expressed by CD4+ lymphocytes from Echinococcus multilocularis-infected patients. Clin Exp Immunol 109(1):90–97PubMedCentralPubMedCrossRef Jenne L, Kilwinski J, Scheffold W, Kern P (1997) IL-5 expressed by CD4+ lymphocytes from Echinococcus multilocularis-infected patients. Clin Exp Immunol 109(1):90–97PubMedCentralPubMedCrossRef
48.
go back to reference Evans CA, Garcia HH, Hartnell A, Gilman RH, Jose PJ, Martinez M, Remick DG, Williams TJ, Friedland JS (1998) Elevated concentrations of eotaxin and interleukin-5 in human neurocysticercosis. Infect Immun 66(9):4522–4525PubMedCentralPubMed Evans CA, Garcia HH, Hartnell A, Gilman RH, Jose PJ, Martinez M, Remick DG, Williams TJ, Friedland JS (1998) Elevated concentrations of eotaxin and interleukin-5 in human neurocysticercosis. Infect Immun 66(9):4522–4525PubMedCentralPubMed
49.
go back to reference Intapan PM, Niwattayakul K, Sawanyawisuth K, Chotmongkol V, Maleewong W (2007) Cerebrospinal fluid eotaxin and eotaxin-2 levels in human eosinophilic meningitis associated with angiostrongyliasis. Cytokine 39(2):138–141PubMedCrossRef Intapan PM, Niwattayakul K, Sawanyawisuth K, Chotmongkol V, Maleewong W (2007) Cerebrospinal fluid eotaxin and eotaxin-2 levels in human eosinophilic meningitis associated with angiostrongyliasis. Cytokine 39(2):138–141PubMedCrossRef
50.
go back to reference del Pozo V, Arrieta I, Tunon T, Cortegano I, Gomez B, Cardaba B, Gallardo S, Rojo M, Renedo G, Palomino P, Tabar AI, Lahoz C (1999) Immunopathogenesis of human gastrointestinal infection by Anisakis simplex. J Allergy Clin Immunol 104(3 Pt 1):637–643PubMedCrossRef del Pozo V, Arrieta I, Tunon T, Cortegano I, Gomez B, Cardaba B, Gallardo S, Rojo M, Renedo G, Palomino P, Tabar AI, Lahoz C (1999) Immunopathogenesis of human gastrointestinal infection by Anisakis simplex. J Allergy Clin Immunol 104(3 Pt 1):637–643PubMedCrossRef
51.
go back to reference Petering H, Kluthe C, Dulkys Y, Kiehl P, Ponath PD, Kapp A, Elsner J (2001) Characterization of the CC chemokine receptor 3 on human keratinocytes. J Invest Dermatol 116(4):549–555PubMedCrossRef Petering H, Kluthe C, Dulkys Y, Kiehl P, Ponath PD, Kapp A, Elsner J (2001) Characterization of the CC chemokine receptor 3 on human keratinocytes. J Invest Dermatol 116(4):549–555PubMedCrossRef
52.
go back to reference Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verastegui E, Zlotnik A (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410(6824):50–56PubMedCrossRef Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verastegui E, Zlotnik A (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410(6824):50–56PubMedCrossRef
53.
go back to reference Berahovich RD, Zabel BA, Lewen S, Walters MJ, Ebsworth K, Wang Y, Jaen JC, Schall TJ (2014) Endothelial expression of CXCR7 and the regulation of systemic CXCL12 levels. Immunology 141(1):111–122PubMedCrossRef Berahovich RD, Zabel BA, Lewen S, Walters MJ, Ebsworth K, Wang Y, Jaen JC, Schall TJ (2014) Endothelial expression of CXCR7 and the regulation of systemic CXCL12 levels. Immunology 141(1):111–122PubMedCrossRef
54.
go back to reference Balabanian K, Couderc J, Bouchet-Delbos L, Amara A, Berrebi D, Foussat A, Baleux F, Portier A, Durand-Gasselin I, Coffman RL, Galanaud P, Peuchmaur M, Emilie D (2003) Role of the chemokine stromal cell-derived factor 1 in autoantibody production and nephritis in murine lupus. J Immunol 170(6):3392–3400PubMedCrossRef Balabanian K, Couderc J, Bouchet-Delbos L, Amara A, Berrebi D, Foussat A, Baleux F, Portier A, Durand-Gasselin I, Coffman RL, Galanaud P, Peuchmaur M, Emilie D (2003) Role of the chemokine stromal cell-derived factor 1 in autoantibody production and nephritis in murine lupus. J Immunol 170(6):3392–3400PubMedCrossRef
55.
go back to reference Karin N (2010) The multiple faces of CXCL12 (SDF-1alpha) in the regulation of immunity during health and disease. J Leukoc Biol 88(3):463–473PubMedCrossRef Karin N (2010) The multiple faces of CXCL12 (SDF-1alpha) in the regulation of immunity during health and disease. J Leukoc Biol 88(3):463–473PubMedCrossRef
56.
go back to reference Negrete-Garcia MC, Velazquez JR, Popoca-Coyotl A, Montes-Vizuet AR, Juarez-Carvajal E, Teran LM (2010) Chemokine (C-X-C motif) ligand 12/stromal cell-derived factor-1 is associated with leukocyte recruitment in asthma. Chest 138(1):100–106PubMed Negrete-Garcia MC, Velazquez JR, Popoca-Coyotl A, Montes-Vizuet AR, Juarez-Carvajal E, Teran LM (2010) Chemokine (C-X-C motif) ligand 12/stromal cell-derived factor-1 is associated with leukocyte recruitment in asthma. Chest 138(1):100–106PubMed
57.
go back to reference Hussain R, Grogl M, Ottesen EA (1987) IgG antibody subclasses in human filariasis. Differential subclass recognition of parasite antigens correlates with different clinical manifestations of infection. J Immunol 139(8):2794–2798PubMed Hussain R, Grogl M, Ottesen EA (1987) IgG antibody subclasses in human filariasis. Differential subclass recognition of parasite antigens correlates with different clinical manifestations of infection. J Immunol 139(8):2794–2798PubMed
58.
go back to reference Daeki AO, Craig PS, Shambesh MK (2000) IgG-subclass antibody responses and the natural history of hepatic cystic echinococcosis in asymptomatic patients. Ann Trop Med Parasitol 94(4):319–328PubMed Daeki AO, Craig PS, Shambesh MK (2000) IgG-subclass antibody responses and the natural history of hepatic cystic echinococcosis in asymptomatic patients. Ann Trop Med Parasitol 94(4):319–328PubMed
59.
go back to reference Wen H, Craig PS (1994) Immunoglobulin G subclass responses in human cystic and alveolar echinococcosis. Am J Trop Med Hyg 51(6):741–748PubMed Wen H, Craig PS (1994) Immunoglobulin G subclass responses in human cystic and alveolar echinococcosis. Am J Trop Med Hyg 51(6):741–748PubMed
60.
go back to reference Rigano R, Profumo E, Ioppolo S, Notargiacomo S, Ortona E, Teggi A, Siracusano A (1995) Immunological markers indicating the effectiveness of pharmacological treatment in human hydatid disease. Clin Exp Immunol 102(2):281–285PubMedCentralPubMedCrossRef Rigano R, Profumo E, Ioppolo S, Notargiacomo S, Ortona E, Teggi A, Siracusano A (1995) Immunological markers indicating the effectiveness of pharmacological treatment in human hydatid disease. Clin Exp Immunol 102(2):281–285PubMedCentralPubMedCrossRef
61.
go back to reference Gottstein B, Eckert J, Woodtli W (1984) Determination of parasite-specific immunoglobulins using the ELISA in patients with echinococcosis treated with mebendazole. Z Parasitenkd 70(3):385–389PubMedCrossRef Gottstein B, Eckert J, Woodtli W (1984) Determination of parasite-specific immunoglobulins using the ELISA in patients with echinococcosis treated with mebendazole. Z Parasitenkd 70(3):385–389PubMedCrossRef
62.
go back to reference Wellinghausen N, Jochle W, Reuter S, Flegel WA, Grunert A, Kern P (1999) Zinc status in patients with alveolar echinococcosis is related to disease progression. Parasite Immunol 21(5):237–241PubMedCrossRef Wellinghausen N, Jochle W, Reuter S, Flegel WA, Grunert A, Kern P (1999) Zinc status in patients with alveolar echinococcosis is related to disease progression. Parasite Immunol 21(5):237–241PubMedCrossRef
63.
Metadata
Title
Distinctive cytokine, chemokine, and antibody responses in Echinococcus multilocularis-infected patients with cured, stable, or progressive disease
Authors
Xiangsheng Huang
Beate Grüner
Christian J. Lechner
Peter Kern
Peter T. Soboslay
Publication date
01-06-2014
Publisher
Springer Berlin Heidelberg
Published in
Medical Microbiology and Immunology / Issue 3/2014
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI
https://doi.org/10.1007/s00430-014-0331-8

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