Th2 immune response against Schistosoma mansoni infection

Microbes and Infection

Volumn 12, Issue 12-13, 2010, Pages 881-888

  Schramm, Gabriele ^a   Haas, Helmut ^a  

^a RESEARCH CENTER BORSTEL   (Germany)

Author keywords

Excretory secretory products; IPSE alpha 1; Omega 1; Schistosoma mansoni; Schistosome egg; Th2 response

Indexed keywords

IMMUNOGLOBULIN E;

BASOPHIL; DENDRITIC CELL; HUMAN; IMMUNE RESPONSE; NONHUMAN; PRIORITY JOURNAL; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SHORT SURVEY; TH2 CELL;

ANIMALS; ANTIGENS, HELMINTH; HELMINTH PROTEINS; HUMANS; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; TH2 CELLS;

SCHISTOSOMA; SCHISTOSOMA MANSONI;

EID: 77958088338     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2010.06.001     Document Type: Short Survey

References (71)

1. Hotez P.J., Brindley P.J., Bethony J.M., King C.H., Pearce E.J., Jacobson J. Helminth infections: the great neglected tropical diseases. J. Clin. Invest. 2008, 118:1311-1321.
2. Pearce E.J., Kane C.M., Sun J., Taylor J.J., McKee A.S., Cervi L. Th2 response polarization during infection with the helminth parasite Schistosoma mansoni. Immunol. Rev. 2004, 201:117-126.
3. Foundations of Parasitology 2000, McGrawHill Book Companies Inc., New York. sixth ed. G.D. Schmidt, L.S. Roberts (Eds.).
4. Pearce E.J., MacDonald A.S. The immunobiology of schistosomiasis. Nat. Rev. Immunol. 2002, 2:499-511.
5. Doenhoff M.J. A role for granulomatous inflammation in the transmission of infectious disease: schistosomiasis and tuberculosis. Parasitology 1997, 115(Suppl.):S113-S125.
6. Dunne D.W., Doenhoff M.J. Schistosoma mansoni egg antigens and hepatocyte damage in infected T cell-deprived mice. Contrib. Microbiol. Immunol. 1983, 7:22-29.
7. Sabin E.A., Araujo M.I., Carvalho E.M., Pearce E.J. Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni. J. Infect. Dis. 1996, 173:269-272.
8. Jenkins S.J., Hewitson J.P., Jenkins G.R., Mountford A.P. Modulation of the host's immune response by schistosome larvae. Parasite Immunol. 2005, 27:385-393.
9. de Oliveira Fraga L.A., Torrero M.N., Tocheva A.S., Mitre E., Davies S.J. Induction of type 2 responses by schistosome worms during prepatent infection. J. Infect. Dis. 2010, 201:464-472.
10. Cass C.L., Johnson J.R., Califf L.L., Xu T., Hernandez H.J., Stadecker M.J., Yates J.R., Williams D.L. Proteomic analysis of Schistosoma mansoni egg secretions. Mol. Biochem. Parasitol. 2007, 155:84-93.
11. Mathieson W., Wilson R.A. A comparative proteomic study of the undeveloped and developed Schistosoma mansoni egg and its contents: the miracidium, hatch fluid and secretions. Int. J. Parasitol. 2010, 40:617-628.
12. Colonna M., Pulendran B., Iwasaki A. Dendritic cells at the host-pathogen interface. Nat. Immunol. 2006, 7:117-120.
13. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
14. Kapsenberg M.L. Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 2003, 3:984-993.
15. O'Garra A. Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 1998, 8:275-283.
16. Haas H., Falcone F.H., Holland M.J., Schramm G., Haisch K., Gibbs B.F., Bufe A., Schlaak M. Early interleukin-4: its role in the switch towards a Th2 response and IgE-mediated allergy. Int. Arch. Allergy Immunol. 1999, 119:86-94.
17. + T cells from T cell receptor transgenic mice. J. Exp. Med. 1992, 176:1091-1098.
18. Hsieh C.S., Heimberger A.B., Gold J.S., O'Garra A., Murphy K.M. Differential regulation of T helper phenotype development by interleukins 4 and 10 in an alpha beta T-cell-receptor transgenic system. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:6065-6069.
19. Corthay A. A three-cell model for activation of naive T helper cells. Scand. J. Immunol. 2006, 64:93-96.
20. + lymphocytes with a Th2 cytokine profile. J. Immunol. 2000, 164:3047-3055.
21. van Panhuys N., Tang S.C., Prout M., Camberis M., Scarlett D., Roberts J., Hu-Li J., Paul W.E., Le Gros G. In vivo studies fail to reveal a role for IL-4 or STAT6 signaling in Th2 lymphocyte differentiation. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:12423-12428.
22. de Jong E.C., Vieira P.L., Kalinski P., Schuitemaker J.H., Tanaka Y., Wierenga E.A., Yazdanbakhsh M., Kapsenberg M.L. Microbial compounds selectively induce Th1 cell-promoting or Th2 cell-promoting dendritic cells in vitro with diverse Th cell-polarizing signals. J. Immunol. 2002, 168:1704-1709.
23. van Liempt E., van Vliet S.J., Engering A., Garcia Vallejo J.J., Bank C.M., Sanchez-Hernandez M., Van Kooyk Y., van Die I. 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. 2007, 44:2605-2615.
24. Everts B., Perona-Wright G., Smits H.H., Hokke C.H., van der Ham A.J., Fitzsimmons C.M., Doenhoff M.J., van der B.J., Mohrs K., Haas H., Mohrs M., Yazdanbakhsh M., Schramm G. Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J. Exp. Med. 2009, 206:1673-1680.
25. Steinfelder S., Andersen J.F., Cannons J.L., Feng C.G., Joshi M., Dwyer D., Caspar P., Schwartzberg P.L., Sher A., Jankovic D. The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J. Exp. Med. 2009, 206:1681-1690.
26. Jankovic D., Kullberg M.C., Caspar P., Sher A. Parasite-induced Th2 polarization is associated with down-regulated dendritic cell responsiveness to Th1 stimuli and a transient delay in T lymphocyte cycling. J. Immunol. 2004, 173:2419-2427.
27. + T cells. J. Exp. Med. 1995, 182:1591-1596.
28. MacDonald A.S., Straw A.D., Dalton N.M., Pearce E.J. Cutting edge: Th2 response induction by dendritic cells: a role for CD40. J. Immunol. 2002, 168:537-540.
29. Thomas P.G., Carter M.R., Atochina O., Da'Dara A.A., Piskorska D., McGuire E., Harn D.A. Maturation of dendritic cell 2 phenotype by a helminth glycan uses a toll-like receptor 4-dependent mechanism. J. Immunol. 2003, 171:5837-5841.
30. Agrawal S., Agrawal A., Doughty B., Gerwitz A., Blenis J., Van D.T., 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. 2003, 171:4984-4989.
31. Kane C.M., Jung E., Pearce E.J. Schistosoma mansoni egg antigen-mediated modulation of Toll-like receptor (TLR)-induced activation occurs independently of TLR2, TLR4, and MyD88. Infect. Immun. 2008, 76:5754-5759.
32. Geijtenbeek T.B., Gringhuis S.I. Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 2009, 9:465-479.
33. Gringhuis S.I., den.Dunnen J., Litjens M., van der Vlist M., Geijtenbeek T.B. Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat. Immunol. 2009, 10:1081-1088.
34. Fitzsimmons C.M., Schramm G., Jones F.M., Chalmers I.W., Hoffmann K.F., Grevelding C.G., Wuhrer M., Hokke C.H., Haas H., Doenhoff M.J., Dunne D.W. Molecular characterization of omega-1: a hepatotoxic ribonuclease from Schistosoma mansoni eggs. Mol. Biochem. Parasitol. 2005, 144:123-127.
35. Yang D., Chen Q., Su S.B., Zhang P., Kurosaka K., Caspi R.R., Michalek S.M., Rosenberg H.F., Zhang N., Oppenheim J.J. Eosinophil-derived neurotoxin acts as an alarmin to activate the TLR2-MyD88 signal pathway in dendritic cells and enhances Th2 immune responses. J. Exp. Med. 2008, 205:79-90.
36. Meevissen M.H., Wuhrer M., Doenhoff M.J., Schramm G., Haas H., Deelder A.M., Hokke C.H. Structural characterization of glycans on omega-1, a major Schistosoma mansoni egg glycoprotein that drives Th2 responses. J. Proteome Res. 2010, 9:2630-2642.
37. Schroeder J.T. Basophils beyond effector cells of allergic inflammation. Adv. Immunol. 2009, 101:123-161.
38. Haas H., Falcone F.H., Schramm G., Haisch K., Gibbs B.F., Klaucke J., Pöppelmann M., Becker W.-M., Gabius H.-J., Schlaak M. Dietary lectins can induce in vitro release of IL-4 and IL-13 from human basophils. Eur. J. Immunol. 1999, 29:918-927.
39. Marone G., Florio G., Petraroli A., Triggiani M., de Paulis A. Role of human FcepsilonRI+ cells in HIV-1 infection. Immunol. Rev. 2001, 179:128-138.
40. Oh K., Shen T., Le Gros G., Min B. Induction of Th2 type immunity in a mouse system reveals a novel immunoregulatory role of basophils. Blood 2007, 109:2921-2927.
41. Sokol C.L., Barton G.M., Farr A.G., Medzhitov R. A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat. Immunol. 2008, 9:310-318.
42. Sokol C.L., Chu N.Q., Yu S., Nish S.A., Laufer T.M., Medzhitov R. Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat. Immunol. 2009, 10:713-720.
43. + T cell interactions promote T(H)2 cytokine-dependent immunity. Nat. Immunol. 2009, 10:697-705.
44. + T cells. Nat. Immunol. 2009, 10:706-712.
45. Falcone F.H., Dahinden C.A., Gibbs B.F., Noll T., Amon U., Hebestreit H., Abrahamson O., Klaucke J., Schlaak M., Haas H. Human basophils release interleukin-4 after stimulation with Schistosoma mansoni egg antigen. Eur. J. Immunol. 1996, 26:1147-1155.
46. Schramm G., Falcone F.H., Gronow A., Haisch K., Mamat U., Doenhoff M.J., Oliveira G., Galle J., Dahinden C.A., Haas H. Molecular characterization of an interleukin-4-inducing factor from Schistosoma mansoni eggs. J. Biol. Chem. 2003, 278:18384-18392.
47. Schramm G., Gronow A., Knobloch J., Wippersteg V., Grevelding C.G., Galle J., Fuller H., Stanley R.G., Chiodini P.L., Haas H., Doenhoff M.J. IPSE/alpha-1: a major immunogenic component secreted from Schistosoma mansoni eggs. Mol. Biochem. Parasitol. 2006, 147:9-19.
48. Schramm G., Mohrs K., Wodrich M., Doenhoff M.J., Pearce E.J., Haas H., Mohrs M. Cutting edge: IPSE/alpha-1, a glycoprotein from Schistosoma mansoni eggs, induces IgE-dependent, antigen-independent IL-4 production by murine basophils in vivo. J. Immunol. 2007, 178:6023-6027.
49. Kim S., Prout M., Ramshaw H., Lopez A.F., LeGros G., Min B. Cutting edge: basophils are transiently recruited into the draining lymph nodes during helminth infection via IL-3, but infection-induced Th2 immunity can develop without basophil lymph node recruitment or IL-3. J. Immunol. 2010, 184:1143-1147.
50. Dunne D.W., Butterworth A.E., Fulford A.J., Kariuki H.C., Langley J.G., Ouma J.H., Capron A., Pierce R.J., Sturrock R.F. Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. Eur. J. Immunol. 1992, 22:1483-1494.
51. Butterworth A.E., Curry A.J., Dunne D.W., Fulford A.J., Kimani G., Kariuki H.C., Klumpp R., Koech D., Mbugua G., Ouma J.H. Immunity and morbidity in human schistosomiasis mansoni. Trop. Geogr. Med. 1994, 46:197-208.
52. Fitzsimmons C.M., McBeath R., Joseph S., Jones F.M., Walter K., Hoffmann K.F., Kariuki H.C., Mwatha J.K., Kimani G., Kabatereine N.B., Vennervald B.J., Ouma J.H., Dunne D.W. Factors affecting human IgE and IgG responses to allergen-like Schistosoma mansoni antigens: molecular structure and patterns of in vivo exposure. Int. Arch. Allergy Immunol. 2007, 142:40-50.
53. Akdis C.A., Blaser K., Akdis M. Mechanisms of allergen-specific immunotherapy. Chem. Immunol. Allergy 2006, 91:195-203.
54. Schramm G., Hamilton J.V., Balog C.I., Wuhrer M., Gronow A., Beckmann S., Wippersteg V., Grevelding C.G., Goldmann T., Weber E., Brattig N.W., Deelder A.M., Dunne D.W., Hokke C.H., Haas H., Doenhoff M.J. Molecular characterisation of kappa-5, a major antigenic glycoprotein from Schistosoma mansoni eggs. Mol. Biochem. Parasitol. 2009, 166:4-14.
55. Tawill S., Le G.L., Ali F., Blaxter M., Allen J.E. Both free-living and parasitic nematodes induce a characteristic Th2 response that is dependent on the presence of intact glycans. Infect. Immun. 2004, 72:398-407.
56. Maizels R.M., Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Natl. Rev. 2003, 3:733-744.
57. Brunet L.R., Finkelman F.D., Cheever A.W., Kopf M.A., Pearce E.J. IL-4 protects against TNF-alpha-mediated cachexia and death during acute schistosomiasis. J. Immunol. 1997, 159:777-785.
58. Herbert D.R., Orekov T., Perkins C., Rothenberg M.E., Finkelman F.D. IL-4R alpha expression by bone marrow-derived cells is necessary and sufficient for host protection against acute schistosomiasis. J. Immunol. 2008, 180:4948-4955.
59. Chiaramonte M.G., Donaldson D.D., Cheever A.W., Wynn T.A. An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J. Clin. Invest. 1999, 104:777-785.
60. Smits H.H., Hammad H., van Nimwegen M., Soullie T., Willart M.A., Lievers E., Kadouch J., Kool M., Kos-van Oosterhoud J., Deelder A.M., Lambrecht B.N., Yazdanbakhsh M. Protective effect of Schistosoma mansoni infection on allergic airway inflammation depends on the intensity and chronicity of infection. J. Allergy Clin. Immunol. 2007, 120:932-940.
61. Jeannin P., Lecoanet S., Delneste Y., Gauchat J.F., Bonnefoy J.Y. IgE versus IgG4 production can be differentially regulated by IL-10. J. Immunol. 1998, 160:3555-3561.
62. King C.L., Nutman T.B. IgE and IgG subclass regulation by IL-4 and IFN-gamma in human helminth infections. Assessment by B cell precursor frequencies. J. Immunol. 1993, 151:458-465.
63. van der Neut K.M., Schuurman J., Losen M., Bleeker W.K., Martinez-Martinez P., Vermeulen E., den Bleker T.H., Wiegman L., Vink T., Aarden L.A., de Baets M.H., van de Winkel J.G., Aalberse R.C., Parren P.W. Anti-inflammatory activity of human IgG4 antibodies by dynamic Fab arm exchange. Science 2007, 317:1554-1557.
64. Hoffmann K.F., Cheever A.W., Wynn T.A. IL-10 and the danger of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. J. Immunol. 2000, 164:6404-6416.
65. Hesse M., Piccirillo C.A., Belkaid Y., Prufer J., Mentink-Kane M., Leusink M., Cheever A.W., Shevach E.M., Wynn T.A. The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. J. Immunol. 2004, 172:3157-3166.
66. Van der Kleij D., Latz E., Brouwers J.F.H.M., Kruize Y.C.M., Schmitz M., Kurt-Jones E.A., Espevik T., de Jong E.C., Kapsenberg M.L., Golenbock D.T., Tielens A.G.M., Yazdanbakhsh M. A novel host-parasite lipid cross-talk. J. Biol. Chem. 2002, 277:48122-48129.
67. + T cells. Nat. Immunol. 2007, 8:1353-1362.
68. Baumgart M., Tompkins F., Leng J., Hesse M. Naturally occurring CD4+Foxp3+ regulatory T cells are an essential, IL-10-independent part of the immunoregulatory network in Schistosoma mansoni egg-induced inflammation. J. Immunol. 2006, 176:5374-5387.
69. + Th cells in granulomas: a novel effector mechanism involved in the control of egg-induced immunopathology in murine schistosomiasis. J. Immunol. 2003, 171:1859-1867.
70. Pesce J.T., Ramalingam T.R., Mentink-Kane M.M., Wilson M.S., El Kasmi K.C., Smith A.M., Thompson R.W., Cheever A.W., Murray P.J., Wynn T.A. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog. 2009, 5:e1000371.
71. Martinez F.O., Helming L., Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 2009, 27:451-483.