Enhanced pro-inflammatory cytokine responses following toll-like-receptor ligation in Schistosoma haematobium-infected schoolchildren from rural Gabon

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Meurs, Lynn ^a   Labuda, Lucja ^b,c,d   Amoah, Abena Serwaa ^e   Mbow, Moustapha ^f   Ngoa, Ulysse Ateba ^c,d   Boakye, Daniel Adjei ^e   Mboup, Souleymane ^f   Dièye, Tandakha Ndiaye ^f   Mountford, Adrian P ^g   Turner, Joseph D ^g   Kremsner, Peter Gottfried ^c,d   Polman, Katja ^a   Yazdanbakhsh, Maria ^b   Adegnika, Ayola Akim ^b,c,d  

^a INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ALBERT SCHWEITZER HOSPITAL   (Gabon)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e University of Ghana   (Ghana)

^f Centre Hospitalier Universitaire Dakar   (Senegal)

^g UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; FOLLISTATIN; FOLLISTATIN LIKE 1 PROTEIN; INTERLEUKIN 10; PARASITE ANTIGEN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; AUTACOID; LIGAND;

ADAPTIVE IMMUNITY; ADOLESCENT; ARTICLE; CHILD; CHILD HEALTH; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; FEMALE; GABON; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOREACTIVITY; INCUBATION TIME; INFECTION RATE; INNATE IMMUNITY; LIGAND BINDING; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; RURAL AREA; SCHISTOSOMIASIS HAEMATOBIA; SCHOOL CHILD; WORM EGG; ANIMAL; BIOSYNTHESIS; BLOOD; CELL CULTURE; IMMUNOLOGY; METABOLISM; MONONUCLEAR CELL; PARASITOLOGY; RURAL POPULATION; SCHISTOSOMA HEMATOBIUM; SCHOOL;

SCHISTOSOMA; SCHISTOSOMA HAEMATOBIUM;

ADOLESCENT; ANIMALS; CELLS, CULTURED; CHILD; CYTOKINES; FEMALE; HUMANS; INFLAMMATION MEDIATORS; LEUKOCYTES, MONONUCLEAR; LIGANDS; MALE; RURAL POPULATION; SCHISTOSOMA HAEMATOBIUM; SCHISTOSOMIASIS HAEMATOBIA; SCHOOLS; TOLL-LIKE RECEPTORS;

EID: 80052549970     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024393     Document Type: Article

References (55)

1. Chitsulo L, Engels D, Montresor A, Savioli L, (2000) The global status of schistosomiasis and its control. Acta Trop 77: 41-51.
2. WHO website. Available: www.who.int/mediacentre/factsheets/fs115/en/index.html. Accessed 2011 Aug 11.
3. Burke ML, Jones MK, Gobert GN, Li YS, Ellis MK, et al. (2009) Immunopathogenesis of human schistosomiasis. Parasite Immunol 31: 163-176.
4. Diaz A, Allen JE, (2007) Mapping immune response profiles: the emerging scenario from helminth immunology. Eur J Immunol 37: 3319-3326.
5. Maizels RM, Yazdanbakhsh M, (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 3: 733-744.
6. King CH, Dangerfield-Cha M, (2008) The unacknowledged impact of chronic schistosomiasis. Chronic Illn 4: 65-79.
7. Gryseels B, Polman K, Clerinx J, Kestens L, (2006) Human schistosomiasis. Lancet 368: 1106-1118.
8. Grogan JL, Kremsner PG, Deelder AM, Yazdanbakhsh M, (1998) Antigen-specific proliferation and interferon-gamma and interleukin-5 production are down-regulated during Schistosoma haematobium infection. J Infect Dis 177: 1433-1437.
9. Rocklin RE, Brown AP, Warren KS, Pelley RP, Houba V, et al. (1980) Factors that modify the cellular-immune response in patients infected by Schistosoma mansoni. J Immunol 125: 1916-1923.
10. King CL, Medhat A, Malhotra I, Nafeh M, Helmy A, et al. (1996) Cytokine control of parasite-specific anergy in human urinary schistosomiasis. IL-10 modulates lymphocyte reactivity. J Immunol 156: 4715-4721.
11. Wamachi AN, Mayadev JS, Mungai PL, Magak PL, Ouma JH, et al. (2004) Increased ratio of tumor necrosis factor-alpha to interleukin-10 production is associated with Schistosoma haematobium-induced urinary-tract morbidity. J Infect Dis 190: 2020-2030.
12. Booth M, Mwatha JK, Joseph S, Jones FM, Kadzo H, et al. (2004) Periportal fibrosis in human Schistosoma mansoni infection is associated with low IL-10, low IFN-gamma, high TNF-alpha, or low RANTES, depending on age and gender. J Immunol 172: 1295-1303.
13. Montenegro SM, Miranda P, Mahanty S, Abath FG, Teixeira KM, et al. (1999) Cytokine production in acute versus chronic human Schistosomiasis mansoni: the cross-regulatory role of interferon-gamma and interleukin-10 in the responses of peripheral blood mononuclear cells and splenocytes to parasite antigens. J Infect Dis 179: 1502-1514.
14. Mwatha JK, Kimani G, Kamau T, Mbugua GG, Ouma JH, et al. (1998) High levels of TNF, soluble TNF receptors, soluble ICAM-1, and IFN-gamma, but low levels of IL-5, are associated with hepatosplenic disease in human schistosomiasis mansoni. J Immunol 160: 1992-1999.
15. van den Biggelaar AH, van Ree R, Rodrigues LC, Lell B, Deelder AM, et al. (2000) Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356: 1723-1727.
16. Nookala S, Srinivasan S, Kaliraj P, Narayanan RB, Nutman TB, (2004) Impairment of tetanus-specific cellular and humoral responses following tetanus vaccination in human lymphatic filariasis. Infect Immun 72: 2598-2604.
17. Cooper PJ, Espinel I, Paredes W, Guderian RH, Nutman TB, (1998) Impaired tetanus-specific cellular and humoral responses following tetanus vaccination in human onchocerciasis: a possible role for interleukin-10. J Infect Dis 178: 1133-1138.
18. Sabin EA, Araujo MI, Carvalho EM, Pearce EJ, (1996) Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni. J Infect Dis 173: 269-272.
19. Smits HH, Hammad H, van Nimwegen M, Soullie T, Willart MA, et al. (2007) Protective effect of Schistosoma mansoni infection on allergic airway inflammation depends on the intensity and chronicity of infection. J Allergy Clin Immunol 120: 932-940.
20. Iwasaki A, Medzhitov R, (2004) Toll-like receptor control of the adaptive immune responses. Nat Immunol 5: 987-995.
21. Lee MS, Kim YJ, (2007) Signaling pathways downstream of pattern-recognition receptors and their cross talk. Annu Rev Biochem 76: 447-480.
22. Geijtenbeek TB, Gringhuis SI, (2009) Signalling through C-type lectin receptors: shaping immune responses. Nat Rev Immunol 9: 465-479.
23. Chang ZL, (2010) Important aspects of Toll-like receptors, ligands and their signaling pathways. Inflamm Res 59: 791-808.
24. van der Kleij D, van den Biggelaar AH, Kruize YC, Retra K, Fillie Y, et al. (2004) Responses to Toll-like receptor ligands in children living in areas where schistosome infections are endemic. J Infect Dis 189: 1044-1051.
25. Retra K, van Riet E, Adegnika AA, Everts B, van Geest S, et al. (2008) Immunologic activity of schistosomal and bacterial TLR2 ligands in Gabonese children. Parasite Immunol 30: 39-46.
26. Katz N, Chaves A, Pellegrino J, (1972) A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14: 397-400.
27. Reiss D, Harrison LM, Bungiro R, Cappello M, (2007) Short report: an agar plate method for culturing hookworm larvae: analysis of growth kinetics and infectivity compared with standard coproculture techniques. Am J Trop Med Hyg 77: 1087-1090.
28. Krepel HP, Baeta S, Polderman AM, (1992) Human Oesophagostomum infection in northern Togo and Ghana: epidemiological aspects. Ann Trop Med Parasitol 86: 289-300.
29. Polderman AM, Krepel HP, Baeta S, Blotkamp J, Gigase P, (1991) Oesophagostomiasis, a common infection of man in northern Togo and Ghana. Am J Trop Med Hyg 44: 336-344.
30. Planche T, Krishna S, Kombila M, Engel K, Faucher JF, et al. (2001) Comparison of methods for the rapid laboratory assessment of children with malaria. Am J Trop Med Hyg 65: 599-602.
31. Abraham E, Anzueto A, Gutierrez G, Tessler S, San Pedro G, et al. (1998) Double-blind randomised controlled trial of monoclonal antibody to human tumour necrosis factor in treatment of septic shock. NORASEPT II Study Group. Lancet 351: 929-933.
32. Martich GD, Boujoukos AJ, Suffredini AF, (1993) Response of man to endotoxin. Immunobiology 187: 403-416.
33. Feldmann M, Brennan FM, Maini RN, (1996) Role of cytokines in rheumatoid arthritis. Annu Rev Immunol 14: 397-440.
34. Spits H, de Waal MR, (1992) Functional characterization of human IL-10. Int Arch Allergy Immunol 99: 8-15.
35. de Vries JE, (1995) Immunosuppressive and anti-inflammatory properties of interleukin 10. Ann Med 27: 537-541.
36. Papadakis KA, Targan SR, (2000) Role of cytokines in the pathogenesis of inflammatory bowel disease. Annu Rev Med 51: 289-298.
37. Grant AV, Araujo MI, Ponte EV, Oliveira RR, Cruz AA, et al. (2011) Polymorphisms in IL10 are associated with total Immunoglobulin E levels and Schistosoma mansoni infection intensity in a Brazilian population. Genes Immun 12: 46-50.
38. Montresor A, Crompton DWT, Hall A, Bundy DAP, Savioli L, (1998) Guidelines for the evaluation of soil-transmitted heminthiasis and schistosomiasis at community level.
39. Wildling E, Winkler S, Kremsner PG, Brandts C, Jenne L, et al. (1995) Malaria epidemiology in the province of Moyen Ogoov, Gabon. Trop Med Parasitol 46: 77-82.
40. Ritter M, Gross O, Kays S, Ruland J, Nimmerjahn F, et al. (2010) Schistosoma mansoni triggers Dectin-2, which activates the Nlrp3 inflammasome and alters adaptive immune responses. Proc Natl Acad Sci U S A 107: 20459-20464.
41. Caldas IR, Campi-Azevedo AC, Oliveira LF, Silveira AM, Oliveira RC, et al. (2008) Human schistosomiasis mansoni: immune responses during acute and chronic phases of the infection. Acta Trop 108: 109-117.
42. Thomas PG, (2003) Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J Immunol 171: 5837-5841.
43. van der Kleij D, Latz E, Brouwers JF, Kruize YC, Schmitz M, et al. (2002) A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J Biol Chem 277: 48122-48129.
44. van Die I, (2003) The dendritic cell-specific C-type lectin DC-SIGN is a receptor for Schistosoma mansoni egg antigens and recognizes the glycan antigen Lewis x. Glycobiology 13: 471-478.
45. van Liempt E, van Vliet SJ, Engering A, Garcia Vallejo JJ, Bank CM, et al. (2007) Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation. Mol Immunol 44: 2605-2615.
46. van Vliet SJ, (2005) Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor antigens by dendritic cells. Int Immunol 17: 661-669.
47. Aksoy E, Zouain CS, Vanhoutte F, Fontaine J, Pavelka N, et al. (2005) Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells. J Biol Chem 280: 277-283.
48. Montenegro SM, Abath FG, Domingues AL, Melo WG, Morais CN, et al. (2002) Enhanced interleukin-12 and CD40 ligand activities but reduced Staphylococcus aureus Cowan 1-induced responses suggest a generalized and progressively impaired type 1 cytokine pattern for human schistosomiasis. Infect Immun 70: 5903-5912.
49. Joshi AD, Raymond T, Coelho AL, Kunkel SL, Hogaboam CM, (2008) A systemic granulomatous response to Schistosoma mansoni eggs alters responsiveness of bone-marrow-derived macrophages to Toll-like receptor agonists. J Leukoc Biol 83: 314-324.
50. Babu S, Blauvelt CP, Kumaraswami V, Nutman TB, (2005) Diminished expression and function of TLR in lymphatic filariasis: a novel mechanism of immune dysregulation. J Immunol 175: 1170-1176.
51. Babu S, Blauvelt CP, Kumaraswami V, Nutman TB, (2006) Cutting edge: diminished T cell TLR expression and function modulates the immune response in human filarial infection. J Immunol 176: 3885-3889.
52. Babu S, Bhat SQ, Kumar NP, Anuradha R, Kumaran P, et al. (2009) Attenuation of toll-like receptor expression and function in latent tuberculosis by coexistent filarial infection with restoration following antifilarial chemotherapy. PLoS Negl Trop Dis 3: e489.
53. Jackson JA, Turner JD, Kamal M, Wright V, Bickle Q, et al. (2006) Gastrointestinal nematode infection is associated with variation in innate immune responsiveness. Microbes Infect 8: 487-492.
54. Hartgers FC, Yazdanbakhsh M, (2006) Co-infection of helminths and malaria: modulation of the immune responses to malaria. Parasite Immunol 28: 497-506.
55. Carvalho L, Sun J, Kane C, Marshall F, Krawczyk C, et al. (2009) Review series on helminths, immune modulation and the hygiene hypothesis: mechanisms underlying helminth modulation of dendritic cell function. Immunology 126: 28-34.