Chronic helminth infections induce immunomodulation: Consequences and mechanisms

Immunobiology

Volumn 212, Issue 6, 2007, Pages 475-490

  van Riet, Elly ^a   Hartgers, Franca C ^a   Yazdanbakhsh, Maria ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Allergy; Helminth; T helper 2 cells; TLR signaling; Vaccination

Indexed keywords

ALBENDAZOLE; ALLERGEN; ANTHELMINTIC AGENT; ANTIRETROVIRUS AGENT; BACTERIAL VACCINE; BCG VACCINE; CHOLERA VACCINE; FREUND ADJUVANT; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; MALARIA VACCINE; MEBENDAZOLE; OXAMNIQUINE; PARASITE ANTIGEN; POLIOMYELITIS VACCINE; PRAZIQUANTEL; PROTEIN PAS 1; ROTAVIRUS VACCINE; TETANUS TOXOID; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; WORM EXTRACT;

ALLERGIC DISEASE; ALLERGY; ARTICLE; ASCARIS LUMBRICOIDES; AUTOIMMUNE DISEASE; BACTERIAL INFECTION; CELL MATURATION; CELL STIMULATION; CELLULAR IMMUNITY; CHRONIC DISEASE; DENDRITIC CELL; DRUG EFFICACY; HELIGMOSOMOIDES POLYGYRUS; HELMINTHIASIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; INFECTION; INFLAMMATORY DISEASE; MALARIA; MIXED INFECTION; MORBIDITY; MORTALITY; MULTIPLE CYCLE TREATMENT; NEMATODIASIS; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; ONCHOCERCA VOLVULUS; PARASITE PREVALENCE; PARASITE SURVIVAL; PARASITOSIS; PRIORITY JOURNAL; SCHISTOSOMA MANSONI; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; TETANUS; TH2 CELL; TRICHINELLA SPIRALIS; TRICHURIS; TUBERCULOSIS; VIRUS INFECTION; WORM INFECTION; WUCHERERIA BANCROFTI;

EID: 34249660624     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2007.03.009     Document Type: Article

References (109)

1. Agrawal S., Agrawal A., Doughty B., Gerwitz A., Blenis J., Van Dyke T., and Pulendran B. Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos. J. Immunol. 171 (2003) 4984-4989
2. Agrawal A., Dillon S., Denning T.L., and Pulendran B. ERK1-/- mice exhibit Th1 cell polarization and increased susceptibility to experimental autoimmune encephalomyelitis. J. Immunol. 176 (2006) 5788-5796
3. Akira S., Takeda K., and Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2 (2001) 675-680
4. Akira S., Uematsu S., and Takeuchi O. Pathogen recognition and innate immunity. Cell 124 (2006) 783-801
5. Aksoy E., Zouain C.S., Vanhoutte F., Fontaine J., Pavelka N., Thieblemont N., Willems F., Ricciardi-Castagnoli P., Goldman M., Capron M., Ryffel B., and Trottein F. Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells. J. Biol. Chem. 280 (2005) 277-283
6. Araujo M.I., Lopes A.A., Medeiros M., Cruz A.A., Sousa-Atta L., Sole D., and Carvalho E.M. Inverse association between skin response to aeroallergens and Schistosoma mansoni infection. Int. Arch. Allergy Immunol. 123 (2000) 145-148
7. Araujo M.I., Hoppe B., Medeiros Jr. M., Alcantara L., Almeida M.C., Schriefer A., Oliveira R.R., Kruschewsky R., Figueiredo J.P., Cruz A.A., and Carvalho E.M. Impaired T helper 2 response to aeroallergen in helminth-infected patients with asthma. J. Infect. Dis. 190 (2004) 1797-1803
8. Atochina O., Daly-Engel T., Piskorska D., McGuire E., and Harn D.A. A schistosome-expressed immunomodulatory glycoconjugate expands peritoneal Gr1+ macrophages that suppress naive CD4+ T cell proliferation via an IFN-{gamma} and nitric oxide-dependent mechanism. J. Immunol. 167 (2001) 4293-4302
9. Auriault C., Ouaissi M.A., Torpier G., Eisen H., and Capron A. Proteolytic cleavage of IgG bound to the Fc receptor of Schistosoma mansoni schistosomula. Parasite Immunol. 3 (1981) 33-44
10. Ayash-Rashkovsky M., Weisman Z., Diveley J., Moss R.B., Bentwich Z., and Borkow G. Generation of Th1 immune responses to inactivated, gp120-depleted HIV-1 in mice with a dominant Th2 biased immune profile via immunostimulatory oligonucleotides-relevance to AIDS vaccines in developing countries. Vaccine 20 (2002) 2684-2692
11. Balic A., Harcus Y., Holland M.J., and Maizels R.M. Selective maturation of dendritic cells by Nippostrongylus brasiliensis-secreted proteins drives Th2 immune responses. Eur. J. Immunol. 34 (2004) 3047-3059
12. Bashir M.E., Andersen P., Fuss I.J., Shi H.N., and Nagler-Anderson C. An enteric helminth infection protects against an allergic response to dietary antigen. J. Immunol. 169 (2002) 3284-3292
13. Blander J.M., and Medzhitov R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 440 (2006) 808-812
14. Brenchley J.M., Price D.A., and Douek D.C. HIV disease: fallout from a mucosal catastrophe?. Nat. Immunol. 7 (2006) 235-239
15. Brown M., Kizza M., Watera C., Quigley M.A., Rowland S., Hughes P., Whitworth J.A., and Elliott A.M. Helminth infection is not associated with faster progression of HIV disease in coinfected adults in Uganda. J. Infect. Dis. 190 (2004) 1869-1879
16. Brown M., Mawa P.A., Joseph S., Bukusuba J., Watera C., Whitworth J.A., Dunne D.W., and Elliott A.M. Treatment of Schistosoma mansoni infection increases helminth-specific type 2 cytokine responses and HIV-1 loads in coinfected Ugandan adults. J. Infect. Dis. 191 (2005) 1648-1657
17. Buijs J., Borsboom G., Renting M., Hilgersom W.J., van Wieringen J.C., Jansen G., and Neijens J. Relationship between allergic manifestations and Toxocara seropositivity: a cross-sectional study among elementary school children. Eur. Respir. J. 10 (1997) 1467-1475
18. Caparros E., Munoz P., Sierra-Filardi E., Serrano-Gomez D., Puig-Kroger A., Rodriguez-Fernandez J.L., Mellado M., Sancho J., Zubiaur M., and Corbi A.L. DC-SIGN ligation on dendritic cells results in ERK and PI3 K activation and modulates cytokine production. Blood 107 (2006) 3950-3958
19. Cervi L., MacDonald A.S., Kane C., Dzierszinski F., and Pearce E.J. Cutting edge: dendritic cells copulsed with microbial and helminth antigens undergo modified maturation, segregate the antigens to distinct intracellular compartments, and concurrently induce microbe-specific Th1 and helminth-specific Th2 responses. J. Immunol. 172 (2004) 2016-2020
20. Cooke A., Tonks P., Jones F.M., O'Shea H., Hutchings P., Fulford A.J., and Dunne D.W. Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol. 21 (1999) 169-176
21. Cooper P.J. Intestinal worms and human allergy. Parasite Immunol. 26 (2004) 455-467
22. Cooper P.J., Espinel I., Paredes W., Guderian R.H., and Nutman T.B. Impaired tetanus-specific cellular and humoral responses following tetanus vaccination in human onchocerciasis: a possible role for interleukin-10. J. Infect. Dis. 178 (1998) 1133-1138
23. Cooper P.J., Espinel I., Wieseman M., Paredes W., Espinel M., Guderian R.H., and Nutman T.B. Human onchocerciasis and tetanus vaccination: impact on the postvaccination antitetanus antibody response. Infect. Immun. 67 (1999) 5951-5957
24. Cooper P.J., Chico M.E., Losonsky G., Sandoval C., Espinel I., Sridhara R., Aguilar M., Guevara A., Guderian R.H., Levine M.M., Griffin G.E., and Nutman T.B. Albendazole treatment of children with ascariasis enhances the vibriocidal antibody response to the live attenuated oral cholera vaccine CVD 103-HgR. J. Infect. Dis. 182 (2000) 1199-1206
25. Cooper P.J., Chico M., Sandoval C., Espinel I., Guevara A., Levine M.M., Griffin G.E., and Nutman T.B. Human infection with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with the live oral cholera vaccine CVD 103-HgR. Infect. Immun. 69 (2001) 1574-1580
26. Cooper P.J., Chico M.E., Rodrigues L.C., Ordonez M., Strachan D., Griffin G.E., and Nutman T.B. Reduced risk of atopy among school-age children infected with geohelminth parasites in a rural area of the tropics. J. Allergy Clin. Immunol. 111 (2003) 995-1000
27. Cooper P.J., Chico M.E., Bland M., Griffin G.E., and Nutman T.B. Allergic symptoms, atopy, and geohelminth infections in a rural area of Ecuador. Am. J. Respir. Crit. Care Med. 168 (2003) 313-317
28. Cooper P.J., Chico M.E., Vaca M.G., Moncayo A.L., Bland J.M., Mafla E., Sanchez F., Rodrigues L.C., Strachan D.P., and Griffin G.E. Effect of albendazole treatments on the prevalence of atopy in children living in communities endemic for geohelminth parasites: a cluster-randomised trial. Lancet 367 (2006) 1598-1603
29. Dagoye D., Bekele Z., Woldemichael K., Nida H., Yimam M., Hall A., Venn A.J., Britton J.R., Hubbard R., and Lewis S.A. Wheezing, allergy, and parasite infection in children in urban and rural Ethiopia. Am. J. Respir. Crit. Care Med. 167 (2003) 1369-1373
30. Davey G., Venn A., Belete H., Berhane Y., and Britton J. Wheeze, allergic sensitization and geohelminth infection in Butajira, Ethiopia. Clin. Exp. Allergy 35 (2005) 301-307
31. Dillon S., Agrawal S., Banerjee K., Letterio J., Denning T.L., Oswald-Richter K., Kasprowicz D.J., Kellar K., Pare J., van Dyke T., Ziegler S., Unutmaz D., and Pulendran B. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J. Clin. Invest. 116 (2006) 916-928
32. Druilhe P., Tall A., and Sokhna C. Worms can worsen malaria: towards a new means to roll back malaria?. Trends Parasitol. 21 (2005) 359-362
33. Dunne D.W., and Cooke A. A worm's eye view of the immune system: consequences for evolution of human autoimmune disease. Nat. Rev. Immunol. 5 (2005) 420-426
34. El Wakil H.S., Aboushousha T.S., El Haddad O., Gamil N.B., Mansour T., and El Said H. Effect of Schistosoma mansoni egg deposition on multiple low doses streptozotocin induced insulin dependent diabetes. J. Egypt. Soc. Parasitol. 32 (2002) 987-1002
35. Elias D., Wolday D., Akuffo H., Petros B., Bronner U., and Britton S. Effect of deworming on human T cell responses to mycobacterial antigens in helminth-exposed individuals before and after bacille Calmette-Guerin (BCG) vaccination. Clin. Exp. Immunol. 123 (2001) 219-225
36. Elias D., Akuffo H., Pawlowski A., Haile M., Schon T., and Britton S. Schistosoma mansoni infection reduces the protective efficacy of BCG vaccination against virulent Mycobacterium tuberculosis. Vaccine 23 (2005) 1326-1334
37. Elliott D.E., Li J., Blum A., Metwali A., Qadir K., Urban Jr. J.F., and Weinstock J.V. Exposure to schistosome eggs protects mice from TNBS-induced colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 284 (2003) G385-G391
38. Elliott D.E., Setiawan T., Metwali A., Blum A., Urban Jr. J.F., and Weinstock J.V. Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice. Eur. J. Immunol. 34 (2004) 2690-2698
39. Elliott A.M., Mpairwe H., Quigley M.A., Nampijja M., Muhangi L., Oweka-Onyee J., Muwanga M., Ndibazza J., and Whitworth J.A. Helminth infection during pregnancy and development of infantile eczema. JAMA 294 (2005) 2032-2034
40. Finkelman F.D., Shea-Donohue T., Morris S.C., Gildea L., Strait R., Madden K.B., Schopf L., and Urban J.F. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 201 (2004) 139-155
41. Goodridge H.S., Marshall F.A., Wilson E.H., Houston K.M., Liew F.Y., Harnett M.M., and Harnett W. In vivo exposure of murine dendritic cell and macrophage bone marrow progenitors to the phosphorylcholine-containing filarial nematode glycoprotein ES-62 polarizes their differentiation to an anti-inflammatory phenotype. Immunology 113 (2004) 491-498
42. Goodridge H.S., Marshall F.A., Else K.J., Houston K.M., Egan C., Al Riyami L., Liew F.Y., Harnett W., and Harnett M.M. Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine-containing secreted product, ES-62. J. Immunol. 174 (2005) 284-293
43. Hagel I., Lynch N.R., Di Prisco M.C., Rojas E., Perez M., and Alvarez N. Ascaris reinfection of slum children: relation with the IgE response. Clin. Exp. Immunol. 94 (1993) 80-83
44. Hartgers F.C., and Yazdanbakhsh M. Co-infection of helminths and malaria: modulation of the immune responses to malaria. Parasite Immunol. 28 (2006) 497-506
45. Imai S., Tezuka H., and Fujita K. A factor of inducing IgE from a filarial parasite prevents insulin-dependent diabetes mellitus in nonobese diabetic mice. Biochem. Biophys. Res. Commun. 286 (2001) 1051-1058
46. Itami D.M., Oshiro T.M., Araujo C.A., Perini A., Martins M.A., Macedo M.S., and Macedo-Soares M.F. Modulation of murine experimental asthma by Ascaris suum components. Clin. Exp. Allergy 35 (2005) 873-879
47. Jenkins S.J., and Mountford A.P. Dendritic cells activated with products released by schistosome larvae drive Th2-type immune responses, which can be inhibited by manipulation of CD40 costimulation. Infect. Immun. 73 (2005) 395-402
48. Kane C.M., Cervi L., Sun J., McKee A.S., Masek K.S., Shapira S., Hunter C.A., and Pearce E.J. Helminth antigens modulate TLR-initiated dendritic cell activation. J. Immunol. 173 (2004) 7454-7461
49. Kapsenberg M.L. Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 3 (2003) 984-993
50. Khan W.I., and Collins S.M. Immune-mediated alteration in gut physiology and its role in host defence in nematode infection. Parasite Immunol. 26 (2004) 319-326
51. Khan W.I., Blennerhasset P.A., Varghese A.K., Chowdhury S.K., Omsted P., Deng Y., and Collins S.M. Intestinal nematode infection ameliorates experimental colitis in mice. Infect. Immun. 70 (2002) 5931-5937
52. La Flamme A.C., Ruddenklau K., and Backstrom B.T. Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infect. Immun. 71 (2003) 4996-5004
53. Lau S., and Matricardi P.M. Worms, asthma, and the hygiene hypothesis. Lancet 367 (2006) 1556-1558
54. Le Hesran J.Y., Akiana J., Ndiaye E.H.M., Dia M., Senghor P., and Konate L. Severe malaria attack is associated with high prevalence of Ascaris lumbricoides infection among children in rural Senegal. Trans. R. Soc. Trop. Med. Hyg. 98 (2004) 397-399
55. Lima C., Perini A., Garcia M.L., Martins M.A., Teixeira M.M., and Macedo M.S. Eosinophilic inflammation and airway hyper-responsiveness are profoundly inhibited by a helminth (Ascaris suum) extract in a murine model of asthma. Clin. Exp. Allergy 32 (2002) 1659-1666
56. Lwin M., Last C., Targett G.A., and Doenhoff M.J. Infection of mice concurrently with Schistosoma mansoni and rodent malarias: contrasting effects of patent S. mansoni infections on Plasmodium chabaudi, P. yoelii and P. berghei. Ann. Trop. Med. Parasitol. 76 (1982) 265-273
57. Lyke K.E., Dicko A., Dabo A., Sangare L., Kone A., Coulibaly D., Guindo A., Traore K., Daou M., Diarra I., Sztein M.B., Plowe C.V., and Doumbo O.K. Association of Schistosoma haematobium infection with protection against acute Plasmodium falciparum malaria in Malian children. Am. J. Trop. Med. Hyg. 73 (2005) 1124-1130
58. Lynch N.R., Palenque M., Hagel I., and DiPrisco M.C. Clinical improvement of asthma after anthelminthic treatment in a tropical situation. Am. J. Respir. Crit Care Med. 156 (1997) 50-54
59. Mahanty S., Mollis S.N., Ravichandran M., Abrams J.S., Kumaraswami V., Jayaraman K., Ottesen E.A., and Nutman T.B. High levels of spontaneous and parasite antigen-driven interleukin-10 production are associated with antigen-specific hyporesponsiveness in human lymphatic filariasis. J. Infect. Dis. 173 (1996) 769-773
60. Mahnke K., Qian Y., Knop J., and Enk A.H. Induction of CD4+/CD25+ regulatory T cells by targeting of antigens to immature dendritic cells. Blood 101 (2003) 4862-4869
61. Maizels R.M., and Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol. 3 (2003) 733-744
62. Maizels R.M., Bundy D.A., Selkirk M.E., Smith D.F., and Anderson R.M. Immunological modulation and evasion by helminth parasites in human populations. Nature 365 (1993) 797-805
63. Maizels R.M., Balic A., Gomez-Escobar N., Nair M., Taylor M.D., and Allen J.E. Helminth parasites-masters of regulation. Immunol. Rev. 201 (2004) 89-116
64. Malhotra I., Mungai P., Wamachi A., Kioko J., Ouma J.H., Kazura J.W., and King C.L. Helminth- and Bacillus Calmette-Guerin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. J. Immunol. 162 (1999) 6843-6848
65. Mangan N.E., Fallon R.E., Smith P., van Rooijen N., McKenzie A.N., and Fallon P.G. Helminth infection protects mice from anaphylaxis via IL-10-producing B cells. J. Immunol. 173 (2004) 6346-6356
66. Martinon F., and Tschopp J. NLRs join TLRs as innate sensors of pathogens. Trends Immunol. 26 (2005) 447-454
67. McInnes I.B., Leung B.P., Harnett M., Gracie J.A., Liew F.Y., and Harnett W. A novel therapeutic approach targeting articular inflammation using the filarial nematode-derived phosphorylcholine-containing glycoprotein ES-62. J. Immunol. 171 (2003) 2127-2133
68. Medeiros J., Figueiredo J.P., Almeida M.C., Matos M.A., Araujo M.I., Cruz A.A., Atta A.M., Rego M.A., and de Jesus A.R. Schistosoma mansoni infection is associated with a reduced course of asthma. J. Allergy Clin. Immunol. 111 (2003) 947-951
69. Modjarrad K., Zulu I., Redden D.T., Njobvu L., Lane H.C., Bentwich Z., and Vermund S.H. Treatment of intestinal helminths does not reduce plasma concentrations of HIV-1 RNA in coinfected Zambian adults. J. Infect. Dis. 192 (2005) 1277-1283
70. Moreels T.G., Nieuwendijk R.J., De Man J.G., De Winter B.Y., Herman A.G., Van Marck E.A., and Pelckmans P.A. Concurrent infection with Schistosoma mansoni attenuates inflammation induced changes in colonic morphology, cytokine levels, and smooth muscle contractility of trinitrobenzene sulphonic acid induced colitis in rats. Gut 53 (2004) 99-107
71. Nacher M., Gay F., Singhasivanon P., Krudsood S., Treeprasertsuk S., Mazier D., Vouldoukis I., and Looareesuwan S. Ascaris lumbricoides infection is associated with protection from cerebral malaria. Parasite Immunol. 22 (2000) 107-113
72. Nacher M., Singhasivanon P., Silachamroon U., Treeprasertsuk S., Vannaphan S., Traore B., Gay F., and Looareesuwan S. Helminth infections are associated with protection from malaria-related acute renal failure and jaundice in Thailand. Am. J. Trop. Med. Hyg. 65 (2001) 834-836
73. Nacher M., Singhasivanon P., Yimsamran S., Manibunyong W., Thanyavanich N., Wuthisen R., and Looareesuwan S. Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum malaria in Thailand. J. Parasitol. 88 (2002) 55-58
74. Nagayama Y., Watanabe K., Niwa M., McLachlan S.M., and Rapoport B. Schistosoma mansoni and {alpha}-galactosylceramide: prophylactic effect of Th1 immune suppression in a mouse model of Graves' hyperthyroidism. J. Immunol. 173 (2004) 2167-2173
75. Nielsen N.O., Simonsen P.E., Magnussen P., Magesa S., and Friis H. Cross-sectional relationship between HIV, lymphatic filariasis and other parasitic infections in adults in coastal northeastern Tanzania. Trans. R. Soc. Trop. Med. Hyg. 100 (2006) 543-550
76. Nookala S., Srinivasan S., Kaliraj P., Narayanan R.B., and Nutman T.B. Impairment of tetanus-specific cellular and humoral responses following tetanus vaccination in human lymphatic filariasis. Infect. Immun. 72 (2004) 2598-2604
77. Nyan O.A., Walraven G.E.L., Banya W.A.S., Milligan P., Van Der Sande M., Ceesay S.M., Del Prete G., and McAdam K.P.W.J. Atopy, intestinal helminth infection and total serum IgE in rural and urban adult Gambian communities. Clin. Exp. Allergy 31 (2001) 1672-1678
78. Obihara C.C., Beyers N., Gie R.P., Hoekstra M.O., Fincham J.E., Marais B.J., Lombard C.J., Dini L.A., and Kimpen J.L.L. Respiratory atopic disease, Ascaris-immunoglobulin E and tuberculin testing in urban South African children. Clin. Exp. Allergy 36 (2006) 640-648
79. Ouaissi M.A., Auriault C., Santoro F., and Capron A. Interaction between Schistosoma mansoni and the complement system: role of IgG Fc peptides in the activation of the classical pathway by schistosomula. J. Immunol. 127 (1981) 1556-1559
80. Palmer L.J., Celedon J.C., Weiss S.T., Wang B., Fang Z., and Xu X. Ascaris lumbricoides infection is associated with increased risk of childhood asthma and atopy in rural China. Am. J. Respir. Crit. Care Med. 165 (2002) 1489-1493
81. Prost A., Nebout M., and Rougemont A. Lepromatous leprosy and onchocerciasis. Br. Med. J. 1 (1979) 589-590
82. Prost A., Schlumberger M., and Fayet M.T. Response to tetanus immunization in onchocerciasis patients. Ann. Trop. Med. Parasitol. 77 (1983) 83-85
83. Reardon C., Sanchez A., Hogaboam C.M., and McKay D.M. Tapeworm infection reduces epithelial ion transport abnormalities in murine dextran sulfate sodium-induced colitis. Infect. Immun. 69 (2001) 4417-4423
84. Sabin E.A., Araujo M.I., Carvalho E.M., and Pearce E.J. Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni. J. Infect. Dis. 173 (1996) 269-272
85. Sacco R.E., Hagen M., Sandor M., Weinstock J.V., and Lynch R.G. Established TH1 granulomatous responses induced by active Mycobacterium avium infection switch to TH2 following challenge with Schistosoma mansoni. Clin. Immunol. 104 (2002) 274-281
86. Scrivener S., Yemaneberhan H., Zebenigus M., Tilahun D., Girma S., Ali S., McElroy P., Custovic A., Woodcock A., Pritchard D., Venn A., and Britton J. Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia: a nested case-control study. Lancet 358 (2001) 1493-1499
87. Sewell D., Qing Z., Reinke E., Elliot D., Weinstock J., Sandor M., and Fabry Z. Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int. Immunol. 15 (2003) 59-69
88. Shortman K., and Liu Y.J. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2 (2002) 151-161
89. Smith P., Fallon R.E., Mangan N.E., Walsh C.M., Saraiva M., Sayers J.R., McKenzie A.N.J., Alcami A., and Fallon P.G. Schistosoma mansoni secretes a chemokine binding protein with antiinflammatory activity. J. Exp. Med. 202 (2005) 1319-1325
90. Spiegel A., Tall A., Raphenon G., Trape J.F., and Druilhe P. Increased frequency of malaria attacks in subjects co-infected by intestinal worms and Plasmodium falciparum malaria. Trans. R. Soc. Trop. Med. Hyg. 97 (2003) 198-199
91. Steel C., and Nutman T.B. CTLA-4 in filarial infections: implications for a role in diminished T cell reactivity. J. Immunol. 170 (2003) 1930-1938
92. Stewart G.R., Boussinesq M., Coulson T., Elson L., Nutman T., and Bradley J.E. Onchocerciasis modulates the immune response to mycobacterial antigens. Clin. Exp. Immunol. 117 (1999) 517-523
93. Su Z., Segura M., Morgan K., Loredo-Osti J.C., and Stevenson M.M. Impairment of protective immunity to blood-stage malaria by concurrent nematode infection. Infect. Immun. 73 (2005) 3531-3539
94. Summers R.W., Elliott D.E., Qadir K., Urban J.F., Thompson R., and Weinstock J.V. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am. J. Gastroenterol. 98 (2003) 2034-2041
95. Summers R.W., Elliott D.E., Urban Jr. J.F., Thompson R., and Weinstock J.V. Trichuris suis therapy in Crohn's disease. Gut 54 (2005) 87-90
96. Summers R.W., Elliott D.E., Urban Jr. J.F., Thompson R.A., and Weinstock J.V. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128 (2005) 825-832
97. Talaat K.R., Bonawitz R.E., Domenech P., and Nutman T.B. Preexposure to live Brugia malayi microfilariae alters the innate response of human dendritic cells to Mycobacterium tuberculosis. J. Infect. Dis. 193 (2006) 196-204
98. Taylor M.D., LeGoff L., Harris A., Malone E., Allen J.E., and Maizels R.M. Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J. Immunol. 174 (2005) 4924-4933
99. Thomas P.G., Carter M.R., Atochina O., Da'Dara A.A., Piskorska D., McGuire E., and Harn D.A. Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J. Immunol. 171 (2003) 5837-5841
100. van den Biggelaar A.H., van Ree R., Rodrigues L.C., Lell B., Deelder A.M., Kremsner P.G., and Yazdanbakhsh M. Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356 (2000) 1723-1727
101. van den Biggelaar A.H., Lopuhaa C., van Ree R., van der Zee J.S., Jans J., Hoek A., Migombet B., Borrmann S., Luckner D., Kremsner P.G., and Yazdanbakhsh M. The prevalence of parasite infestation and house dust mite sensitization in Gabonese schoolchildren. Int. Arch. Allergy Immunol. 126 (2001) 231-238
102. van den Biggelaar A.H., Rodrigues L.C., van Ree R., van der Zee J.S., Hoeksma-Kruize Y.C., Souverijn J.H., Missinou M.A., Borrmann S., Kremsner P.G., and Yazdanbakhsh M. Long-term treatment of intestinal helminths increases mite skin-test reactivity in Gabonese schoolchildren. J. Infect. Dis. 189 (2004) 892-900
103. van der Kleij D., Latz E., Brouwers J.F., Kruize Y.C., Schmitz M., Kurt-Jones E.A., Espevik T., de Jong E.C., Kapsenberg M.L., Golenbock D.T., Tielens A.G.M., and Yazdanbakhsh M. A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine acivates Toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 277 (2002) 48122-48129
104. Whelan M., Harnett M.M., Houston K.M., Patel V., Harnett W., and Rigley K.P. A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J. Immunol. 164 (2000) 6453-6460
105. Wilson M.S., Taylor M.D., Balic A., Finney C.A.M., Lamb J.R., and Maizels R.M. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J. Exp. Med. 202 (2005) 1199-1212
106. Wolday D., Mayaan S., Mariam Z.G., Berhe N., Seboxa T., Britton S., Galai N., Landay A., and Bentwich Z. Treatment of intestinal worms is associated with decreased HIV plasma viral load. J. AIDS 31 (2002) 56-62
107. Yazdanbakhsh M., van den Biggelaar A., and Maizels R.M. Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol. 22 (2001) 372-377
108. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., and Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5 (2004) 730-737
109. Zaccone P., Fehervari Z., Jones F.M., Sidobre S., Kronenberg M., Dunne D.W., and Cooke A. Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes. Eur. J. Immunol. 33 (2003) 1439-1449