Chronic schistosome infection leads to modulation of granuloma formation and systemic immune suppression

Frontiers in Immunology

Volumn 4, Issue FRB, 2013, Pages

  Lundy, Steven K ^a   Lukacs, Nicholas W ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Hygiene hypothesis; Immune regulation; Sialyl Lewisx glycans; Soluble egg antigen; T helper lymphocytes

Indexed keywords

FAS LIGAND; GAMMA INTERFERON; GLYCAN; GLYCOPROTEIN; GLYCOPROTEIN OMEGA 1; IMMUNOMODULATING AGENT; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 4; LACTO N GLYCAN FUCOPENTAOSE III; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ASTHMA; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CELL DEATH; EGG; GRANULOMA; HUMAN; HYGIENE; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOMODULATION; INFLAMMATORY BOWEL DISEASE; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE MODEL; NONHUMAN; REVIEW; SCHISTOSOMA HEMATOBIUM; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; TH1 CELL; TH2 CELL; VACCINATION;

EID: 84883704513     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00039     Document Type: Review

References (225)

1. Abdulla, M. H., Lim, K. C., Mckerrow, J. H., and Caffrey, C. R. (2011). Proteomic identification of IPSE/alpha-1 as a major hepatotoxin secreted by Schistosoma mansoni eggs. PLoS Negl. Trop. Dis. 5:e1368. doi: 10.1371/journal.pntd.0001368
2. Airaghi, L., and Tedeschi, A. (2004). Results of the US Third National Health and Nutrition Examination Survey support the hygiene hypothesis. J. Allergy Clin. Immunol. 113, 179-180. author reply: 180.
3. Amsden, A. F., Boros, D. L., and Hood, A. T. (1980). Etiology of the liver granulomatous response in Schistosoma mansoni-infected athymic nude mice. Infect. Immun. 27, 75-80.
4. Amu, S., Saunders, S. P., Kronenberg, M., Mangan, N. E., Atzberger, A., and Fallon, P. G. (2010). Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J. Allergy Clin. Immunol. 125, 1114.e8-1124.e8.
5. Angelico, M., Renganathan, E., Gandin, C., Fathy, M., Profili, M. C., Refai, W., et al. (1997). Chronic liver disease in the Alexandria governorate, Egypt: contribution of schistosomiasis and hepatitis virus infections. J. Hepatol. 26, 236-243.
6. Anthony, R. M., Nimmerjahn, F., Ashline, D. J., Reinhold, V. N., Paulson, J. C., and Ravetch, J. V. (2008). Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science 320, 373-376.
7. Anthony, R. M., Wermeling, F., and Ravetch, J. V. (2012). Novel roles for the IgG Fc glycan. Ann. N.Y. Acad. Sci. 1253, 170-180.
8. Araujo, M. I., and De Carvalho, E. M. (2006). Human schistosomiasis decreases immune responses to allergens and clinical manifestations of asthma. Chem. Immunol. Allergy 90, 29-44.
9. Araujo, M. I., Hoppe, B. S., Medeiros, M. Jr., and Carvalho, E. M. (2004). Schistosoma mansoni infection modulates the immune response against allergic and auto-immune diseases. Mem. Inst. Oswaldo Cruz 99, 27-32.
10. Atochina, O., and Harn, D. (2005). LNFPIII/LeX-stimulated macrophages activate natural killer cells via CD40-CD40L interaction. Clin. Diagn. Lab. Immunol. 12, 1041-1049.
11. Atochina, O., and Harn, D. (2006). Prevention of psoriasis-like lesions development in fsn/fsn mice by helminth glycans. Exp. Dermatol. 15, 461-468.
12. Baumgart, M., Tompkins, F., Leng, J., and Hesse, M. (2006). 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. 176, 5374-5387.
13. Blair, P. A., Norena, L. Y., Flores-Borja, F., Rawlings, D. J., Isenberg, D. A., Ehrenstein, M. R., et al. (2010). CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 32, 129-140.
14. Borkow, G., and Bentwich, Z. (2000). Eradication of helminthic infections may be essential for successful vaccination against HIV and tuberculosis. Bull. World Health Organ. 78, 1368-1369.
15. Boros, D. L. (1989). Immunopathology of Schistosoma mansoni infection. Clin. Microbiol. Rev. 2, 250-269.
16. Boros, D. L. (1994). The role of cytokines in the formation of the schistosome egg granuloma. Immunobiology 191, 441-450.
17. Boros, D. L. (1999). T helper cell populations, cytokine dynamics, and pathology of the schistosome egg granuloma. Microbes Infect. 1, 511-516.
18. Boros, D. L., Amsden, A. F., and Hood, A. T. (1982). Modulation of granulomatous hypersensitivity. IV. Immunoglobulin and antibody production by vigorous and immunomodulated liver granulomas of Schistosoma mansoni-infected mice. J. Immunol. 128, 1050-1053.
19. Boros, D. L., and Lande, M. A. (1983). Induction of collagen synthesis in cultured human fibroblasts by live Schistosoma mansoni eggs and soluble egg antigens (SEA). Am. J. Trop. Med. Hyg. 32, 78-82.
20. Boros, D. L., Pelley, R. P., and Warren, K. S. (1975). Spontaneous modulation of granulomatous hypersensitivity in Schistosomiasis mansoni. J. Immunol. 114, 1437-1441.
21. Boros, D. L., and Warren, K. S. (1970). Delayed hypersensitivity-type granuloma formation and dermal reaction induced and elicited by a soluble factor isolated from Schistosoma mansoni eggs. J. Exp. Med. 132, 488-507.
22. Boros, D. L., and Warren, K. S. (1971a). Effect of antimacrophage serum on hypersensitivity (Schistosoma mansoni egg) and foreign body (divinyl-benzene copolymer bead) granulomas. J. Immunol. 107, 534-539.
23. Boros, D. L., and Warren, K. S. (1971b). Specific granulomatous hypersensitivity elicited by bentonite particles coated with soluble antigens from schistosome eggs and turcle bacilli. Nature 229, 200-201.
24. Boros, D. L., and Whitfield, J. R. (1998). Endogenous IL-10 regulates IFN-gamma and IL-5 cytokine production and the granulomatous response in Schistosomiasis mansoni-infected mice. Immunology 94, 481-487.
25. Brockhaus, M., Magnani, J. L., Herlyn, M., Blaszczyk, M., Steplewski, Z., Koprowski, H., et al. (1982). Monoclonal antibodies directed against the sugar sequence of lacto-N-fucopentaose III are obtained from mice immunized with human tumors. Arch. Biochem. Biophys. 217, 647-651.
26. Brown, M., Miiro, G., Nkurunziza, P., Watera, C., Quigley, M. A., Dunne, D. W., et al. (2006). Schistosoma mansoni, nematode infections, and progression to active tuberculosis among HIV-1-infected Ugandans. Am. J. Trop. Med. Hyg. 74, 819-825.
27. Brunet, L. R., Sabin, E. A., Cheever, A. W., Kopf, M. A., and Pearce, E. J. (1999). Interleukin 5 (IL-5) is not required for expression of a Th2 response or host resistance mechanisms during murine Schistosomiasis mansoni but does play a role in development of IL-4-producing non-T, non-B cells. Infect. Immun. 67, 3014-3018.
28. Burke, M. L., McManus, D. P., Ramm, G. A., Duke, M., Li, Y., Jones, M. K., et al. (2010). Temporal expression of chemokines dictates the hepatic inflammatory infiltrate in a murine model of schistosomiasis. PLoS Negl. Trop. Dis. 4:e598. doi: 10.1371/journal.pntd.0000598
29. Cai, Y., Langley, J. G., Smith, D. I., and Boros, D. L. (1996). A cloned major Schistosoma mansoni egg antigen with homologies to small heat shock proteins elicits Th1 responsiveness. Infect. Immun. 64, 1750-1755.
30. Cardoso, L. S., Oliveira, S. C., Goes, A. M., Oliveira, R. R., Pacifico, L. G., Marinho, F. V., et al. (2010). Schistosoma mansoni antigens modulate the allergic response in a murine model of ovalbumin-induced airway inflammation. Clin. Exp. Immunol. 160, 266-274.
31. Cardoso, L. S., Oliveira, S. C., Pacifico, L. G., Goes, A. M., Oliveira, R. R., Fonseca, C. T., et al. (2006). Schistosoma mansoni antigen-driven interleukin-10 production in infected asthmatic individuals. Mem. Inst. Oswaldo Cruz 101(Suppl. 1), 339-343.
32. Carneiro-Santos, P., Martins-Filho, O., Alves-Oliveira, L. F., Silveira, A. M., Coura-Filho, P., Viana, I. R., et al. (2000). Apoptosis: a mechanism of immunoregulation during human Schistosomiasis mansoni. Parasite Immunol. 22, 267-277.
33. Cheever, A. W., Byram, J. E., Hieny, S., Von Lichtenberg, F., Lunde, M. N., and Sher, A. (1985). Immunopathology of Schistosoma japonicum and S. mansoni infection in B cell depleted mice. Parasite Immunol. 7, 399-413.
34. Cheever, A. W., Williams, M. E., Wynn, T. A., Finkelman, F. D., Seder, R. A., Cox, T. M., et al. (1994). Anti-IL-4 treatment of Schistosoma mansoni-infected mice inhibits development of T cells and non-B, non-T cells expressing Th2 cytokines while decreasing egg-induced hepatic fibrosis. J. Immunol. 153, 753-759.
35. Chen, Y., and Boros, D. L. (1998). Identification of the immunodominant T cell epitope of p38, a major egg antigen, and characterization of the epitope-specific Th responsiveness during murine Schistosomiasis mansoni. J. Immunol. 160, 5420-5427.
36. Chen, Y., and Boros, D. L. (2001). The Schistosoma mansoni egg-derived r38 peptide-induced Th1 response affects the synchronous pulmonary but not the asynchronous hepatic granuloma growth. Parasite Immunol. 23, 43-50.
37. Chen, Y., Khanna, S., Goodyear, C. S., Park, Y. B., Raz, E., Thiel, S., et al. (2009). Regulation of dendritic cells and macrophages by an anti-apoptotic cell natural antibody that suppresses TLR responses and inhibits inflammatory arthritis. J. Immunol. 183, 1346-1359.
38. Chensue, S. W., and Boros, D. L. (1979). Modulation of granulomatous hypersensitivity. I. Characterization of T lymphocytes involved in the adoptive suppression of granuloma formation in Schistosoma mansoni-infected mice. J. Immunol. 123, 1409-1414.
39. Chensue, S. W., Wellhausen, S. R., and Boros, D. L. (1981). Modulation of granulomatous hypersensitivity. II. Participation of Ly 1+ and Ly 2+ T lymphocytes in the suppression of granuloma formation and lymphokine production in Schistosoma mansoni-infected mice. J. Immunol. 127, 363-367.
40. Chiaramonte, M. G., Donaldson, D. D., Cheever, A. W., and Wynn, T. A. (1999a). An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J. Clin. Invest. 104, 777-785.
41. Chiaramonte, M. G., Schopf, L. R., Neben, T. Y., Cheever, A. W., Donaldson, D. D., and Wynn, T. A. (1999b). IL-13 is a key regulatory cytokine for Th2 cell-mediated pulmonary granuloma formation and IgE responses induced by Schistosoma mansoni eggs. J. Immunol. 162, 920-930.
42. Colley, D. G. (1975). Immune responses to a soluble schistosomal egg antigen preparation during chronic primary infection with Schistosoma mansoni. J. Immunol. 115, 150-156.
43. Colley, D. G. (1976). Adoptive suppression of granuloma formation. J. Exp. Med. 143, 696-700.
44. Combs, S. G., Marder, R. J., Minna, J. D., Mulshine, J. L., Polovina, M. R., and Rosen, S. T. (1984). Immunohistochemical localization of the immunodominant differentiation antigen lacto-N-fucopentaose III in normal adult and fetal tissues. J. Histochem. Cytochem. 32, 982-988.
45. Cooke, A., Tonks, P., Jones, F. M., O'Shea, H., Hutchings, P., Fulford, A. J., et al. (1999). Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol. 21, 169-176.
46. Correale, J., and Farez, M. (2007). Association between parasite infection and immune responses in multiple sclerosis. Ann. Neurol. 61, 97-108.
47. Correale, J., and Farez, M. (2009). Helminth antigens modulate immune responses in cells from multiple sclerosis patients through TLR2-dependent mechanisms. J. Immunol. 183, 5999-6012.
48. Correale, J., Farez, M., and Razzitte, G. (2008). Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann. Neurol. 64, 187-199.
49. Dewals, B. G., Marillier, R. G., Hoving, J. C., Leeto, M., Schwegmann, A., and Brombacher, F. (2010). IL-4Ralpha-independent expression of mannose receptor and Ym1 by macrophages depends on their IL-10 responsiveness. PLoS Negl. Trop. Dis. 4:e689. doi: 10.1371/journal.pntd.0000689
50. Doenhoff, M. J. (1997). A role for granulomatous inflammation in the transmission of infectious disease: schistosomiasis and tuberculosis. Parasitology 115(Suppl.), S113-S125.
51. Domingo, E. O., and Warren, K. S. (1968). The inhibition of granuloma formation around Schistosoma mansoni eggs. 3. Heterologous antilymphocyte serum. Am. J. Pathol. 52, 613-631.
52. Dunne, D. W., Jones, F. M., and Doenhoff, M. J. (1991). The purification, characterization, serological activity and hepatotoxic properties of two cationic glycoproteins (alpha 1 and omega 1) from Schistosoma mansoni eggs. Parasitology 103(Pt 2), 225-236.
53. Dutta, P., Hullett, D. A., Roenneburg, D. A., Torrealba, J. R., Sollinger, H. W., Harn, D. A., et al. (2010). Lacto-N-fucopentaose III, a pentasaccharide, prolongs heart transplant survival. Transplantation 90, 1071-1078.
54. Edwards, M. J., Buchatska, O., Ashton, M., Montoya, M., Bickle, Q. D., and Borrow, P. (2005). Reciprocal immunomodulation in a schistosome and hepatotropic virus coinfection model. J. Immunol. 175, 6275-6285.
55. El-Cheikh, M. C., Bonomo, A. C., Rossi, M. I., Pinho Mde, F., and Borojevic, R. (1998). Experimental murine Schistosomiasis mansoni: modulation of the B-1 lymphocyte distribution and phenotype expression. Immunobiology 199, 51-62.
56. Elias, D., Akuffo, H., Thors, C., Pawlowski, A., and Britton, S. (2005). Low dose chronic Schistosoma mansoni infection increases susceptibility to Mycobacterium bovis BCG infection in mice. Clin. Exp. Immunol. 139, 398-404.
57. El-Kady, I. M., Lotfy, M., Badra, G., El-Masry, S., and Waked, I. (2005). Interleukin (IL)-4, IL-10, IL-18 and IFN-gamma cytokines pattern in patients with combined hepatitis C virus and Schistosoma mansoni infections. Scand. J. Immunol. 61, 87-91.
58. Elliott, D. E., and Boros, D. L. (1984). Schistosome egg antigen(s) presentation and regulatory activity by macrophages isolated from vigorous or immunomodulated liver granulomas of Schistosoma mansoni-infected mice. J. Immunol. 132, 1506-1510.
59. Elliott, D. E., Li, J., Blum, A., Metwali, A., Qadir, K., Urban, J. F., et al. (2003). Exposure to schistosome eggs protects mice from TNBS-induced colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 284, G385-G391.
60. Elliott, D. E., Ragheb, S., Wellhausen, S. R., and Boros, D. L. (1990). Interactions between adherent mononuclear cells and lymphocytes from granulomas of mice with Schistosomiasis mansoni. Infect. Immun. 58, 1577-1583.
61. Elliott, D. E., Righthand, V. F., and Boros, D. L. (1987). Characterization of regulatory (interferon-alpha/beta) and accessory (LAF/IL 1) monokine activities from liver granuloma macrophages of Schistosoma mansoni-infected mice. J. Immunol. 138, 2653-2662.
62. Elliott, D. E., Urban, J. J., Argo, C. K., and Weinstock, J. V. (2000). Does the failure to acquire helminthic parasites predispose to Crohn's disease?. FASEB J. 14, 1848-1855.
63. Elliott, D. E., and Weinstock, J. V. (2012). Helminth-host immunological interactions: prevention and control of immune-mediated diseases. Ann. N.Y. Acad. Sci. 1247, 83-96.
64. Estaquier, J., Marguerite, M., Sahuc, F., Bessis, N., Auriault, C., and Ameisen, J. C. (1997). Interleukin-10-mediated T cell apoptosis during the T helper type 2 cytokine response in murine Schistosoma mansoni parasite infection. Eur. Cytokine Netw. 8, 153-160.
65. Evans, J. G., Chavez-Rueda, K. A., Eddaoudi, A., Meyer-Bahlburg, A., Rawlings, D. J., Ehrenstein, M. R., et al. (2007). Novel suppressive function of transitional 2 B cells in experimental arthritis. J. Immunol. 178, 7868-7878.
66. Everts, B., Hussaarts, L., Driessen, N. N., Meevissen, M. H., Schramm, G., van der Ham, A. J., et al. (2012). Schistosome-derived omega-1 drives Th2 polarization by suppressing protein synthesis following internalization by the mannose receptor. J. Exp. Med. 209, 1753-1767.
67. Everts, B., Perona-Wright, G., Smits, H. H., Hokke, C. H., van der Ham, A. J., Fitzsimmons, C. M., et al. (2009). Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J. Exp. Med. 206, 1673-1680.
68. Falcone, F. H., Dahinden, C. A., Gibbs, B. F., Noll, T., Amon, U., Hebestreit, H., et al. (1996). Human basophils release interleukin-4 after stimulation with Schistosoma mansoni egg antigen. Eur. J. Immunol. 26, 1147-1155.
69. Fallon, P. G., and Dunne, D. W. (1999). Tolerization of mice to Schistosoma mansoni egg antigens causes elevated type 1 and diminished type 2 cytokine responses and increased mortality in acute infection. J. Immunol. 162, 4122-4132.
70. Fallon, P. G., Richardson, E. J., McKenzie, G. J., and McKenzie, A. N. (2000a). Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J. Immunol. 164, 2585-2591.
71. Fallon, P. G., Richardson, E. J., Smith, P., and Dunne, D. W. (2000b). Elevated type 1, diminished type 2 cytokines and impaired antibody response are associated with hepatotoxicity and mortalities during Schistosoma mansoni infection of CD4-depleted mice. Eur. J. Immunol. 30, 470-480.
72. Fallon, P. G., Smith, P., and Dunne, D. W. (1998). Type 1 and type 2 cytokine-producing mouse CD4+ and CD8+ T cells in acute Schistosoma mansoni infection. Eur. J. Immunol. 28, 1408-1416.
73. Farghaly, A. G., and Barakat, R. M. (1993). The effect of praziquantel administration on the course of hepatitis B among cases with concomitant schistosome infection. J. Egypt. Public Health Assoc. 68, 81-100.
74. Faveeuw, C., Angeli, V., Fontaine, J., Maliszewski, C., Capron, A., Van Kaer, L., et al. (2002). Antigen presentation by CD1d contributes to the amplification of Th2 responses to Schistosoma mansoni glycoconjugates in mice. J. Immunol. 169, 906-912.
75. Ferru, I., Roye, O., Delacre, M., Auriault, C., and Wolowczuk, I. (1998). Infection of B-cell-deficient mice by the parasite Schistosoma mansoni: demonstration of the participation of B cells in granuloma modulation. Scand. J. Immunol. 48, 233-240.
76. Fidel, P. L. Jr., and Boros, D. L. (1990). Regulation of granulomatous inflammation in murine schistosomiasis. IV. Antigen-induced suppressor T cells down-regulate proliferation and IL-2 production. J. Immunol. 145, 1257-1264.
77. Fischer, E., Camus, D., Santoro, F., and Capron, A. (1981). Schistosoma mansoni: autoantibodies and polyclonal B cell activation in infected mice. Clin. Exp. Immunol. 46, 89-97.
78. Flores Villanueva, P. O., Chikunguwo, S. M., Harris, T. S., and Stadecker, M. J. (1993). Role of IL-10 on antigen-presenting cell function for schistosomal egg-specific monoclonal T helper cell responses in vitro and in vivo. J. Immunol. 151, 3192-3198.
79. Flores-Villanueva, P. O., Zheng, X. X., Strom, T. B., and Stadecker, M. J. (1996). Recombinant IL-10 and IL-10/Fc treatment down-regulate egg antigen-specific delayed hypersensitivity reactions and egg granuloma formation in schistosomiasis. J. Immunol. 156, 3315-3320.
80. Frantz, F. G., Rosada, R. S., Peres-Buzalaf, C., Perusso, F. R., Rodrigues, V., Ramos, S. G., et al. (2010). Helminth coinfection does not affect therapeutic effect of a DNA vaccine in mice harboring tuberculosis. PLoS Negl. Trop. Dis. 4:e700. doi: 10.1371/journal.pntd.0000700
81. Gale, E. A. (2002). A missing link in the hygiene hypothesis?. Diabetologia 45, 588-594.
82. Gaubert, S., Viana da Costa, A., Maurage, C. A., Lima, E. C., Fontaine, J., Lafitte, S., et al. (1999). X-linked immunodeficiency affects the outcome of Schistosoma mansoni infection in the murine model. Parasite Immunol. 21, 89-101.
83. Glocker, E. O., Kotlarz, D., Boztug, K., Gertz, E. M., Schaffer, A. A., Noyan, F., et al. (2009). Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N. Engl. J. Med. 361, 2033-2045.
84. Goes, A. M., Gazzinelli, G., Rocha, R., Katz, N., and Doughty, B. L. (1991). Granulomatous hypersensitivity to Schistosoma mansoni egg antigens in human schistosomiasis. III. In vitro granuloma modulation induced by immune complexes. Am. J. Trop. Med. Hyg. 44, 434-443.
85. Harnett, W., and Harnett, M. M. (2006). Molecular basis of worm-induced immunomodulation. Parasite Immunol. 28, 535-543.
86. Harnett, W., and Harnett, M. M. (2010). Helminth-derived immunomodulators: can understanding the worm produce the pill?. Nat. Rev. Immunol. 10, 278-284.
87. Haseeb, M. A., and Craig, J. P. (1997). Suppression of the immune response to diphtheria toxoid in murine schistosomiasis. Vaccine 15, 45-50.
88. Helal, T. E., Danial, M. F., and Ahmed, H. F. (1998). The relationship between hepatitis C virus and schistosomiasis: histopathologic evaluation of liver biopsy specimens. Hum. Pathol. 29, 743-749.
89. Helmby, H., and Bickle, Q. (2006). Immune modulation by helminth infections. Parasite Immunol. 28, 479-481.
90. Helmby, H., Kullberg, M., and Troye-Blomberg, M. (1998). Altered immune responses in mice with concomitant Schistosoma mansoni and Plasmodium chabaudi infections. Infect. Immun. 66, 5167-5174.
91. Hernandez, H. J., Wang, Y., and Stadecker, M. J. (1997). In infection with Schistosoma mansoni, B cells are required for T helper type 2 cell responses but not for granuloma formation. J. Immunol. 158, 4832-4837.
92. Hoffmann, K. F., Cheever, A. W., and Wynn, T. A. (2000). IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. J. Immunol. 164, 6406-6416.
93. Hood, A. T., and Boros, D. L. (1980). The effect of splenectomy on the pathophysiology and egg-specific immune response of Schistosoma mansoni-infected mice. Am. J. Trop. Med. Hyg. 29, 586-591.
94. Hori, S., Nomura, T., and Sakaguchi, S. (2003). Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057-1061.
95. Iwata, Y., Matsushita, T., Horikawa, M., Dilillo, D. J., Yanaba, K., Venturi, G. M., et al. (2011). Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 117, 530-541.
96. Jankovic, D., Cheever, A. W., Kullberg, M. C., Wynn, T. A., Yap, G., Caspar, P., et al. (1998). CD4+ T cell-mediated granulomatous pathology in schistosomiasis is downregulated by a B cell-dependent mechanism requiring Fc receptor signaling. J. Exp. Med. 187, 619-629.
97. Jankovic, D., Kullberg, M. C., Dombrowicz, D., Barbieri, S., Caspar, P., Wynn, T. A., et al. (1997). Fc epsilonRI-deficient mice infected with Schistosoma mansoni mount normal Th2-type responses while displaying enhanced liver pathology. J. Immunol. 159, 1868-1875.
98. Jankovic, D., Kullberg, M. C., Noben-Trauth, N., Caspar, P., Ward, J. M., Cheever, A. W., et al. (1999). Schistosome-infected IL-4 receptor knockout (KO) mice, in contrast to IL-4 KO mice, fail to develop granulomatous pathology while maintaining the same lymphokine expression profile. J. Immunol. 163, 337-342.
99. Joseph, A. L., and Boros, D. L. (1993). Tumor necrosis factor plays a role in Schistosoma mansoni egg-induced granulomatous inflammation. J. Immunol. 151, 5461-5471.
100. Kalinkovich, A., Weisman, Z., and Bentwich, Z. (1999). Chemokines and chemokine receptors: role in HIV infection. Immunol. Lett. 68, 281-287.
101. Kallestrup, P., Zinyama, R., Gomo, E., Butterworth, A. E., Mudenge, B., van Dam, G. J., et al. (2005). Schistosomiasis and HIV-1 infection in rural Zimbabwe: effect of treatment of schistosomiasis on CD4 cell count and plasma HIV-1 RNA load. J. Infect. Dis. 192, 1956-1961.
102. Kamal, S. M., Bianchi, L., Al Tawil, A., Koziel, M., El Sayed Khalifa, K., Peter, T., et al. (2001). Specific cellular immune response and cytokine patterns in patients coinfected with hepatitis C virus and Schistosoma mansoni. J. Infect. Dis. 184, 972-982.
103. Kamal, S. M., and El Sayed Khalifa, K. (2006). Immune modulation by helminthic infections: worms and viral infections. Parasite Immunol. 28, 483-496.
104. Kamal, S. M., Graham, C. S., He, Q., Bianchi, L., Tawil, A. A., Rasenack, J. W., et al. (2004). Kinetics of intrahepatic hepatitis C virus (HCV)-specific CD4+ T cell responses in HCV and Schistosoma mansoni coinfection: relation to progression of liver fibrosis. J. Infect. Dis. 189, 1140-1150.
105. Kaplan, M. H., Whitfield, J. R., Boros, D. L., and Grusby, M. J. (1998). Th2 cells are required for the Schistosoma mansoni egg-induced granulomatous response. J. Immunol. 160, 1850-1856.
106. Klinker, M. W., and Lundy, S. K. (2012). Multiple mechanisms of immune suppression by B lymphocytes. Mol. Med. 18, 123-137.
107. Kullberg, M. C., Berzofsky, J. A., Jankovic, D. L., Barbieri, S., Williams, M. E., Perlmann, P., et al. (1996). T cell-derived IL-3 induces the production of IL-4 by non-B, non-T cells to amplify the Th2-cytokine response to a non-parasite antigen in Schistosoma mansoni-infected mice. J. Immunol. 156, 1482-1489.
108. La Flamme, A. C., Ruddenklau, K., and Backstrom, B. T. (2003). Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infect. Immun. 71, 4996-5004.
109. Larouze, B., Dazza, M. C., Gaudebout, C., Habib, M., Elamy, M., and Cline, B. (1987). Absence of relationship between Schistosoma mansoni and hepatitis B virus infection in the Qalyub Governate, Egypt. Ann. Trop. Med. Parasitol. 81, 373-375.
110. Lawn, S. D., Karanja, D. M., Mwinzia, P., Andove, J., Colley, D. G., Folks, T. M., et al. (2000). The effect of treatment of schistosomiasis on blood plasma HIV-1 RNA concentration in coinfected individuals. AIDS 14, 2437-2443.
111. Layland, L. E., Mages, J., Loddenkemper, C., Hoerauf, A., Wagner, H., Lang, R., et al. (2010). Pronounced phenotype in activated regulatory T cells during a chronic helminth infection. J. Immunol. 184, 713-724.
112. Lindell, D. M., Berlin, A. A., Schaller, M. A., and Lukacs, N. W. (2008). B cell antigen presentation promotes Th2 responses and immunopathology during chronic allergic lung disease. PLoS ONE 3:e3129. doi: 10.1371/journal.pone.0003129
113. Liu J. Y., Li, L. Y., Yang, X. Z., Li, J., Zhong, G., Wang, J., et al. (2011). Adoptive transfer of dendritic cells isolated from helminth-infected mice enhanced T regulatory cell responses in airway allergic inflammation. Parasite Immunol. 33, 525-534.
114. Lopes, L. M., Pereira, M. A., Gerken, S. E., and Vaz, N. (1990). Polyclonal activation of B lymphocytes during experimental infection with Schistosoma mansoni. Parasitology 100(Pt 1), 83-91.
115. Lucas, S., Musallam, R., Bain, J., Hassounah, O., Bickle, Q., and Doenhoff, M. (1980). The pathological effects of immunosuppression of Schistosoma mansoni-infected mice, with particular reference to survival and hepatotoxicity after thymectomy and treatment with antithymocyte serum, and treatment with hydrocortisone acetate. Trans. R. Soc. Trop. Med. Hyg. 74, 633-643.
116. Lukacs, N. W., and Boros, D. L. (1991). Identification of larval cross-reactive and egg-specific antigens involved in granuloma formation in murine Schistosomiasis mansoni. Infect. Immun. 59, 3237-3242.
117. Lukacs, N. W., and Boros, D. L. (1992). Utilization of fractionated soluble egg antigens reveals selectively modulated granulomatous and lymphokine responses during murine Schistosomiasis mansoni. Infect. Immun. 60, 3209-3216.
118. Lukacs, N. W., and Boros, D. L. (1993). Lymphokine regulation of granuloma formation in murine Schistosomiasis mansoni. Clin. Immunol. Immunopathol. 68, 57-63.
119. Lukacs, N. W., Kunkel, S. L., Strieter, R. M., Warmington, K., and Chensue, S. W. (1993). The role of macrophage inflammatory protein 1 alpha in Schistosoma mansoni egg-induced granulomatous inflammation. J. Exp. Med. 177, 1551-1559.
120. Lundy, S. K. (2009). Killer B lymphocytes: the evidence and the potential. Inflamm. Res. 58, 345-357.
121. Lundy, S. K., and Boros, D. L. (2002). Fas ligand-expressing B-1a lymphocytes mediate CD4(+)-T-cell apoptosis during schistosomal infection: induction by interleukin 4 (IL-4) and IL-10. Infect. Immun. 70, 812-819.
122. Lundy, S. K., Berlin, A. A., Martens, T. F., and Lukacs, N. W. (2005). Deficiency of regulatory B cells increases allergic airway inflammation. Inflamm. Res. 54, 514-521.
123. Lundy, S. K., and Fox, D. A. (2009). Reduced Fas ligand-expressing splenic CD5+ B lymphocytes in severe collagen-induced arthritis. Arthritis Res. Ther. 11:R128. doi: 10.1186/ar2795
124. Lundy, S. K., Lerman, S. P., and Boros, D. L. (2001). Soluble egg antigen-stimulated T helper lymphocyte apoptosis and evidence for cell death mediated by FasL(+) T and B cells during murine Schistosoma mansoni infection. Infect. Immun. 69, 271-280.
125. Maizels, R. M. (2009). Exploring the immunology of parasitism-from surface antigens to the hygiene hypothesis. Parasitology 136, 1549-1564.
126. Mathew, R. C., and Boros, D. L. (1986). Anti-L3T4 antibody treatment suppresses hepatic granuloma formation and abrogates antigen-induced interleukin-2 production in Schistosoma mansoni infection. Infect. Immun. 54, 820-826.
127. Maynard, C. L., and Weaver, C. T. (2009). Intestinal effector T cells in health and disease. Immunity 31, 389-400.
128. McElroy, M. D., Elrefaei, M., Jones, N., Ssali, F., Mugyenyi, P., Barugahare, B., et al. (2005). Coinfection with Schistosoma mansoni is associated with decreased HIV-specific cytolysis and increased IL-10 production. J. Immunol. 174, 5119-5123.
129. McKenzie, G. J., Fallon, P. G., Emson, C. L., Grencis, R. K., and McKenzie, A. N. (1999). Simultaneous disruption of interleukin (IL)-4 and IL-13 defines individual roles in T helper cell type 2-mediated responses. J. Exp. Med. 189, 1565-1572.
130. Meevissen, M. H., Wuhrer, M., Doenhoff, M. J., Schramm, G., Haas, H., Deelder, A. M., et al. (2010). Structural characterization of glycans on omega-1, a major Schistosoma mansoni egg glycoprotein that drives Th2 responses. J. Proteome Res. 9, 2630-2642.
131. Metwali, A., Elliott, D., Blum, A. M., Li, J., Sandor, M., Lynch, R., et al. (1996). The granulomatous response in murine Schistosomiasis mansoni does not switch to Th1 in IL-4-deficient C57BL/6 mice. J. Immunol. 157, 4546-4553.
132. Milner, T., Reilly, L., Nausch, N., Midzi, N., Mduluza, T., Maizels, R., et al. (2010). Circulating cytokine levels and antibody responses to human Schistosoma haematobium: IL-5 and IL-10 levels depend upon age and infection status. Parasite Immunol. 32, 710-721.
133. Mohamed, A., Elsheikh, A., Ghandour, Z., and Al Karawi, M. (1998). Impact of hepatitis C virus infection on schistosomal liver disease. Hepatogastroenterology 45, 1492-1496.
134. Mwatha, J. K., Kimani, G., Kamau, T., Mbugua, G. G., Ouma, J. H., Mumo, J., 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.
135. Nacher, M., Singhasivanon, P., Traore, B., Vannaphan, S., Gay, F., Chindanond, D., et al. (2002a). Helminth infections are associated with protection from cerebral malaria and increased nitrogen derivatives concentrations in Thailand. Am. J. Trop. Med. Hyg. 66, 304-309.
136. Nacher, M., Singhasivanon, P., Yimsamran, S., Manibunyong, W., Thanyavanich, N., Wuthisen, R., et al. (2002b). Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum malaria in Thailand. J. Parasitol. 88, 55-58.
137. Nagayama, Y., McLachlan, S. M., Rapoport, B., and Oishi, K. (2004). Graves' hyperthyroidism and the hygiene hypothesis in a mouse model. Endocrinology 145, 5075-5079.
138. Okano, M., Satoskar, A. R., Nishizaki, K., and Harn, D. A. Jr. (2001). Lacto-N-fucopentaose III found on Schistosoma mansoni egg antigens functions as adjuvant for proteins by inducing Th2-type response. J. Immunol. 167, 442-450.
139. Osada, Y., Shimizu, S., Kumagai, T., Yamada, S., and Kanazawa, T. (2009). Schistosoma mansoni infection reduces severity of collagen-induced arthritis via down-regulation of pro-inflammatory mediators. Int. J. Parasitol. 39, 457-464.
140. Oswald, I. P., Gazzinelli, R. T., Sher, A., and James, S. L. (1992a). IL-10 synergizes with IL-4 and transforming growth factor-beta to inhibit macrophage cytotoxic activity. J. Immunol. 148, 3578-3582.
141. Oswald, I. P., Wynn, T. A., Sher, A., and James, S. L. (1992b). Interleukin 10 inhibits macrophage microbicidal activity by blocking the endogenous production of tumor necrosis factor alpha required as a costimulatory factor for interferon gamma-induced activation. Proc. Natl. Acad. Sci. U.S.A. 89, 8676-8680.
142. Pacifico, L. G., Marinho, F. A., Fonseca, C. T., Barsante, M. M., Pinho, V., Sales-Junior, P. A., et al. (2009). Schistosoma mansoni antigens modulate experimental allergic asthma in a murine model: a major role for CD4+ CD25+ Foxp3+ T cells independent of interleukin-10. Infect. Immun. 77, 98-107.
143. Pereira, L. M., Melo, M. C., Lacerda, C., Spinelli, V., Domingues, A. L., Massarolo, P., et al. (1994). Hepatitis B virus infection in Schistosomiasis mansoni. J. Med. Virol. 42, 203-206.
144. Perrigoue, J. G., Saenz, S. A., Siracusa, M. C., Allenspach, E. J., Taylor, B. C., Giacomin, P. R., et al. (2009). MHC class II-dependent basophil-CD4+ T cell interactions promote T(H)2 cytokine-dependent immunity. Nat. Immunol. 10, 697-705.
145. Phillips, S. M., Diconza, J. J., Gold, J. A., and Reid, W. A. (1977). Schistosomiasis in the congenitally athymic (nude) mouse. I. Thymic dependency of eosinophilia, granuloma formation, and host morbidity. J. Immunol. 118, 594-599.
146. Qadir, K., Metwali, A., Blum, A. M., Li, J., Elliott, D. E., and Weinstock, J. V. (2001). TGF-beta and IL-10 regulation of IFN-gamma produced in Th2-type schistosome granulomas requires IL-12. Am. J. Physiol. Gastrointest. Liver Physiol. 281, G940-G946.
147. Quinn, T. C., Wawer, M. J., Sewankambo, N., Serwadda, D., Li, C., Wabwire-Mangen, F., et al. (2000). Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N. Engl. J. Med. 342, 921-929.
148. Ragheb, S., and Boros, D. L. (1989). Characterization of granuloma T lymphocyte function from Schistosoma mansoni-infected mice. J. Immunol. 142, 3239-3246.
149. Rakasz, E., Blum, A. M., Metwali, A., Elliott, D. E., Li, J., Ballas, Z. K., et al. (1998). Localization and regulation of IFN-gamma production within the granulomas of murine schistosomiasis in IL-4-deficient and control mice. J. Immunol. 160, 4994-4999.
150. Reis, E. A., Mauadi Carmo, T. A., Athanazio, R., Reis, M. G., and Harn, D. A. Jr. (2008). Schistosoma mansoni triose phosphate isomerase peptide MAP4 is able to trigger naive donor immune response towards a type-1 cytokine profile. Scand. J. Immunol. 68, 169-176.
151. Rezende, S. A., Gollob, K. J., Correa-Oliveira, R., and Goes, A. M. (1998). Down modulation of MHC surface molecules on B cells by suppressive immune complexes obtained from chronic intestinal schistosomiasis patients. Immunol. Lett. 62, 67-73.
152. Rook, G. A. (2012). Hygiene hypothesis and autoimmune diseases. Clin. Rev. Allergy Immunol. 42, 5-15.
153. Rubtsov, Y. P., Rasmussen, J. P., Chi, E. Y., Fontenot, J., Castelli, L., Ye, X., et al. (2008). Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28, 546-558.
154. Rumbley, C. A., Sugaya, H., Zekavat, S. A., El Refaei, M., Perrin, P. J., and Phillips, S. M. (1999). Activated eosinophils are the major source of Th2-associated cytokines in the schistosome granuloma. J. Immunol. 162, 1003-1009.
155. Rutitzky, L. I., Bazzone, L., Shainheit, M. G., Joyce-Shaikh, B., Cua, D. J., and Stadecker, M. J. (2008). IL-23 is required for the development of severe egg-induced immunopathology in schistosomiasis and for lesional expression of IL-17. J. Immunol. 180, 2486-2495.
156. Rutitzky, L. I., Lopes da Rosa, J. R., and Stadecker, M. J. (2005). Severe CD4 T cell-mediated immunopathology in murine schistosomiasis is dependent on IL-12p40 and correlates with high levels of IL-17. J. Immunol. 175, 3920-3926.
157. Rutitzky, L. I., Smith, P. M., and Stadecker, M. J. (2009). T-bet protects against exacerbation of schistosome egg-induced immunopathology by regulating Th17-mediated inflammation. Eur. J. Immunol. 39, 2470-2481.
158. Rutitzky, L. I., and Stadecker, M. J. (2011). Exacerbated egg-induced immunopathology in murine Schistosoma mansoni infection is primarily mediated by IL-17 and restrained by IFN-gamma. Eur. J. Immunol. 41, 2677-2687.
159. Ruyssers, N. E., De Winter, B. Y., De Man, J. G., Loukas, A., Pearson, M. S., Weinstock, J. V., et al. (2009). Therapeutic potential of helminth soluble proteins in TNBS-induced colitis in mice. Inflamm. Bowel Dis. 15, 491-500.
160. Sabin, E. A., Araujo, M. I., Carvalho, E. M., and Pearce, E. J. (1996a). Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni. J. Infect. Dis. 173, 269-272.
161. Sabin, E. A., Kopf, M. A., and Pearce, E. J. (1996b). Schistosoma mansoni egg-induced early IL-4 production is dependent upon IL-5 and eosinophils. J. Exp. Med. 184, 1871-1878.
162. Sabin, E. A., and Pearce, E. J. (1995). Early IL-4 production by non-CD4+ cells at the site of antigen deposition predicts the development of a T helper 2 cell response to Schistosoma mansoni eggs. J. Immunol. 155, 4844-4853.
163. Sacco, R., Hagen, M., Sandor, M., Weinstock, J. V., and Lynch, R. G. (2002). Established T(H1) granulomatous responses induced by active Mycobacterium avium infection switch to T(H2) following challenge with Schistosoma mansoni. Clin. Immunol. 104, 274-281.
164. Schramm, G., Mohrs, K., Wodrich, M., Doenhoff, M. J., Pearce, E. J., Haas, H., et al. (2007). 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. 178, 6023-6027.
165. Scott, P., Pearce, E., Cheever, A. W., Coffman, R. L., and Sher, A. (1989). Role of cytokines and CD4+ T-cell subsets in the regulation of parasite immunity and disease. Immunol. Rev. 112, 161-182.
166. Secor, W. E., Karanja, D. M., and Colley, D. G. (2004). Interactions between schistosomiasis and human immunodeficiency virus in Western Kenya. Mem. Inst. Oswaldo Cruz 99, 93-95.
167. Secor, W. E., Shah, A., Mwinzi, P. M., Ndenga, B. A., Watta, C. O., and Karanja, D. M. (2003). Increased density of human immunodeficiency virus type 1 coreceptors CCR5 and CXCR4 on the surfaces of CD4(+) T cells and monocytes of patients with Schistosoma mansoni infection. Infect. Immun. 71, 6668-6671.
168. Sewell, D., Qing, Z., Reinke, E., Elliot, D., Weinstock, J., Sandor, M., et al. (2003). Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int. Immunol. 15, 59-69.
169. Shainheit, M. G., Smith, P. M., Bazzone, L. E., Wang, A. C., Rutitzky, L. I., and Stadecker, M. J. (2008). Dendritic cell IL-23 and IL-1 production in response to schistosome eggs induces Th17 cells in a mouse strain prone to severe immunopathology. J. Immunol. 181, 8559-8567.
170. Shapira-Nahor, O., Kalinkovich, A., Weisman, Z., Greenberg, Z., Nahmias, J., Shapiro, M., et al. (1998). Increased susceptibility to HIV-1 infection of peripheral blood mononuclear cells from chronically immune-activated individuals. AIDS 12, 1731-1733.
171. Sher, A., Coffman, R. L., Hieny, S., Scott, P., and Cheever, A. W. (1990). Interleukin 5 is required for the blood and tissue eosinophilia but not granuloma formation induced by infection with Schistosoma mansoni. Proc. Natl. Acad. Sci. U.S.A. 87, 61-65.
172. Sher, A., Fiorentino, D., Caspar, P., Pearce, E., and Mosmann, T. (1991). Production of IL-10 by CD4+ T lymphocytes correlates with down-regulation of Th1 cytokine synthesis in helminth infection. J. Immunol. 147, 2713-2716.
173. Singh, K. P., Gerard, H. C., Hudson, A. P., Reddy, T. R., and Boros, D. L. (2005). Retroviral Foxp3 gene transfer ameliorates liver granuloma pathology in Schistosoma mansoni infected mice. Immunology 114, 410-417.
174. Singh, S. K., Stephani, J., Schaefer, M., Kalay, H., Garcia-Vallejo, J. J., Den Haan, J., et al. (2009). Targeting glycan modified OVA to murine DC-SIGN transgenic dendritic cells enhances MHC class I and II presentation. Mol. Immunol. 47, 164-174.
175. Smith, P., Mangan, N. E., Walsh, C. M., Fallon, R. E., McKenzie, A. N., van Rooijen, N., et al. (2007). Infection with a helminth parasite prevents experimental colitis via a macrophage-mediated mechanism. J. Immunol. 178, 4557-4566.
176. Sokhna, C., Le Hesran, J. Y., Mbaye, P. A., Akiana, J., Camara, P., Diop, M., et al. (2004). Increase of malaria attacks among children presenting concomitant infection by Schistosoma mansoni in Senegal. Malar. J. 3:43. doi: 10.1186/1475-2875-3-43
177. Sokol, C. L., Chu, N. Q., Yu, S., Nish, S. A., Laufer, T. M., and Medzhitov, R. (2009). Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat. Immunol. 10, 713-720.
178. Song, X., Shen, J., Wen, H., Zhong, Z., Luo, Q., Chu, D., et al. (2011). Impact of Schistosoma japonicum infection on collagen-induced arthritis in DBA/1 mice: a murine model of human rheumatoid arthritis. PLoS ONE 6:e23453. doi: 10.1371/journal.pone.0023453
179. Steinfelder, S., Andersen, J. F., Cannons, J. L., Feng, C. G., Joshi, M., Dwyer, D., et al. (2009). The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J. Exp. Med. 206, 1681-1690.
180. Stene, L. C., and Nafstad, P. (2001). Relation between occurrence of type 1 diabetes and asthma. Lancet 357, 607-608.
181. Stockinger, B., Botzenhardt, U., and Lemmel, E. M. (1979). On the feedback regulation of humoral immune response. I. Evidence for 'B suppressor cells'. Immunology 36, 87-94.
182. Summers, R. W., Elliott, D. E., Qadir, K., Urban, J. F. Jr., Thompson, R., and Weinstock, J. V. (2003). Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am. J. Gastroenterol. 98, 2034-2041.
183. Summers, R. W., Elliott, D. E., Urban, J. F. Jr., Thompson, R. A., and Weinstock, J. V. (2005). Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128, 825-832.
184. Taylor, J. J., Mohrs, M., and Pearce, E. J. (2006). Regulatory T cell responses develop in parallel to Th responses and control the magnitude and phenotype of the Th effector population. J. Immunol. 176, 5839-5847.
185. Terrazas, L. I., Walsh, K. L., Piskorska, D., McGuire, E., and Harn, D. A. Jr. (2001). The schistosome oligosaccharide lacto-N-neotetraose expands Gr1(+) cells that secrete anti-inflammatory cytokines and inhibit proliferation of naive CD4(+) cells: a potential mechanism for immune polarization in helminth infections. J. Immunol. 167, 5294-5303.
186. Thomas, P. G., Carter, M. R., Da'dara, A. A., Desimone, T. M., and Harn, D. A. (2005). A helminth glycan induces APC maturation via alternative NF-kappa B activation independent of I kappa B alpha degradation. J. Immunol. 175, 2082-2090.
187. Todt, J. C., Whitfield, J. R., Ivard, S. R., and Boros, D. L. (2000). Down-regulation of interleukin-12, interleukin-12R expression/activity mediates the switch from Th1 to Th2 granuloma response during murine Schistosomiasis mansoni. Scand. J. Immunol. 52, 385-392.
188. Van Der Vlugt, L. E., Labuda, L. A., Ozir-Fazalalikhan, A., Lievers, E., Gloudemans, A. K., Liu, K. Y., et al. (2012). Schistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells. PLoS ONE 7:e30883. doi: 10.1371/journal.pone.0030883
189. Van Liempt, E., Imberty, A., Bank, C. M., Van Vliet, S. J., Van Kooyk, Y., Geijtenbeek, T. B., et al. (2004). Molecular basis of the differences in binding properties of the highly related C-type lectins DC-SIGN and L-SIGN to Lewis X trisaccharide and Schistosoma mansoni egg antigens. J. Biol. Chem. 279, 33161-33167.
190. Van Liempt, E., Van Vliet, S. J., Engering, A., Garcia Vallejo, J. J., Bank, C. M., Sanchez-Hernandez, M., 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.
191. Vas, J., Gronwall, C., Marshak-Rothstein, A., and Silverman, G. J. (2012). Natural antibody to apoptotic cell membranes inhibits the proinflammatory properties of lupus autoantibody immune complexes. Arthritis Rheum. 64, 3388-3398.
192. Velupillai, P., and Harn, D. A. (1994). Oligosaccharide-specific induction of interleukin 10 production by B220+ cells from schistosome-infected mice: a mechanism for regulation of CD4+ T-cell subsets. Proc. Natl. Acad. Sci. U.S.A. 91, 18-22.
193. Velupillai, P., Posey, C., Horauf, A. M., Solbach, W., Piessens, W. F., and Harn, D. A. (1996a). B-cell outgrowth and ligand-specific production of IL-10 correlate with Th2 dominance in certain parasitic diseases. Exp. Parasitol. 84, 168-177.
194. Velupillai, P., Sypek, J., and Harn, D. A. (1996b). Interleukin-12 and -10 and gamma interferon regulate polyclonal and ligand-specific expansion of murine B-1 cells. Infect. Immun. 64, 4557-4560.
195. Velupillai, P., Secor, W. E., Horauf, A. M., and Harn, D. A. (1997). B-1 cell (CD5+B220+) outgrowth in murine schistosomiasis is genetically restricted and is largely due to activation by polylactosamine sugars. J. Immunol. 158, 338-344.
196. Wahl, S. M., Frazier-Jessen, M., Jin, W. W., Kopp, J. B., Sher, A., and Cheever, A. W. (1997). Cytokine regulation of schistosome-induced granuloma and fibrosis. Kidney Int. 51, 1370-1375.
197. Waknine-Grinberg, J. H., Gold, D., Ohayon, A., Flescher, E., Heyfets, A., Doenhoff, M. J., et al. (2010). Schistosoma mansoni infection reduces the incidence of murine cerebral malaria. Malar. J. 9:5. doi: 10.1186/1475-2875-9-5
198. Wang, Y., Da'dara, A. A., Thomas, P. G., and Harn, D. A. (2010). Dendritic cells activated by an anti-inflammatory agent induce CD4(+) T helper type 2 responses without impairing CD8(+) memory and effector cytotoxic T-lymphocyte responses. Immunology 129, 406-417.
199. Weinstock, J. V., and Boros, D. L. (1983). Modulation of granulomatous hypersensitivity. VI. T lymphocyte subsets influence mast cell density in liver granulomas of Schistosoma mansoni-infected mice. J. Immunol. 131, 959-961.
200. Weinstock, J. V., and Elliott, D. E. (2009). Helminths and the IBD hygiene hypothesis. Inflamm. Bowel Dis. 15, 128-133.
201. Weinstock, J. V., Summers, R. W., Elliott, D. E., Qadir, K., Urban, J. F. Jr., and Thompson, R. (2002). The possible link between de-worming and the emergence of immunological disease. J. Lab. Clin. Med. 139, 334-338.
202. Weng, M., Huntley, D., Huang, I. F., Foye-Jackson, O., Wang, L., Sarkissian, A., et al. (2007). Alternatively activated macrophages in intestinal helminth infection: effects on concurrent bacterial colitis. J. Immunol. 179, 4721-4731.
203. Williams, M. E., Kullberg, M. C., Barbieri, S., Caspar, P., Berzofsky, J. A., Seder, R. A., et al. (1993). Fc epsilon receptor-positive cells are a major source of antigen-induced interleukin-4 in spleens of mice infected with Schistosoma mansoni. Eur. J. Immunol. 23, 1910-1916.
204. Wilson, M. S., Taylor, M. D., O'Gorman, M. T., Balic, A., Barr, T. A., Filbey, K., et al. (2010). Helminth-induced CD19+CD23hi B cells modulate experimental allergic and autoimmune inflammation. Eur. J. Immunol. 40, 1682-1696.
205. Wolday, D., Mayaan, S., Mariam, Z. G., Berhe, N., Seboxa, T., Britton, S., et al. (2002). Treatment of intestinal worms is associated with decreased HIV plasma viral load. J. Acquir. Immune Defic. Syndr. 31, 56-62.
206. Wynn, T. A., Cheever, A. W., Williams, M. E., Hieny, S., Caspar, P., Kuhn, R., et al. (1998). IL-10 regulates liver pathology in acute murine Schistosomiasis mansoni but is not required for immune down-modulation of chronic disease. J. Immunol. 160, 4473-4480.
207. Wynn, T. A., Eltoum, I., Cheever, A. W., Lewis, F. A., Gause, W. C., and Sher, A. (1993). Analysis of cytokine mRNA expression during primary granuloma formation induced by eggs of Schistosoma mansoni. J. Immunol. 151, 1430-1440.
208. Wynn, T. A., Eltoum, I., Oswald, I. P., Cheever, A. W., and Sher, A. (1994). Endogenous interleukin 12 (IL-12) regulates granuloma formation induced by eggs of Schistosoma mansoni and exogenous IL-12 both inhibits and prophylactically immunizes against egg pathology. J. Exp. Med. 179, 1551-1561.
209. Wynn, T. A., and Hoffmann, K. F. (2000). Defining a schistosomiasis vaccination strategy - is it really Th1 versus Th2? Parasitol. Today 16, 497-501.
210. Wynn, T. A., Jankovic, D., Hieny, S., Zioncheck, K., Jardieu, P., Cheever, A. W., et al. (1995). IL-12 exacerbates rather than suppresses T helper 2-dependent pathology in the absence of endogenous IFN-gamma. J. Immunol. 154, 3999-4009.
211. Wynn, T. A., Morawetz, R., Scharton-Kersten, T., Hieny, S., Morse, H. C. 3rd., Kuhn, R., et al. (1997). Analysis of granuloma formation in double cytokine-deficient mice reveals a central role for IL-10 in polarizing both T helper cell 1- and T helper cell 2-type cytokine responses in vivo. J. Immunol. 159, 5014-5023.
212. Yamashita, T., and Boros, D. L. (1992). IL-4 influences IL-2 production and granulomatous inflammation in murine Schistosomiasis mansoni. J. Immunol. 149, 3659-3664.
213. Yanaba, K., Bouaziz, J. D., Haas, K. M., Poe, J. C., Fujimoto, M., and Tedder, T. F. (2008). A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 28, 639-650.
214. Yang, J., Zhao, J., Yang, Y., Zhang, L., Yang, X., Zhu, X., et al. (2007). Schistosoma japonicum egg antigens stimulate CD4 CD25 T cells and modulate airway inflammation in a murine model of asthma. Immunology 120, 8-18.
215. Yap, G., Cheever, A., Caspar, P., Jankovic, D., and Sher, A. (1997). Unimpaired down-modulation of the hepatic granulomatous response in CD8 T-cell- and gamma interferon-deficient mice chronically infected with Schistosoma mansoni. Infect. Immun. 65, 2583-2586.
216. Yazdanbakhsh, M., Van den Biggelaar, A., and Maizels, R. M. (2001). Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol. 22, 372-377.
217. Yoshimoto, T., Yasuda, K., Tanaka, H., Nakahira, M., Imai, Y., Fujimori, Y., et al. (2009). Basophils contribute to T(H)2-IgE responses in vivo via IL-4 production and presentation of peptide-MHC class II complexes to CD4+ T cells. Nat. Immunol. 10, 706-712.
218. Zaccone, P., Burton, O., Miller, N., Jones, F. M., Dunne, D. W., and Cooke, A. (2009). Schistosoma mansoni egg antigens induce Treg that participate in diabetes prevention in NOD mice. Eur. J. Immunol. 39, 1098-1107.
219. Zaccone, P., Burton, O. T., and Cooke, A. (2008). Interplay of parasite-driven immune responses and autoimmunity. Trends Parasitol. 24, 35-42.
220. Zaccone, P., Burton, O. T., Gibbs, S. E., Miller, N., Jones, F. M., Schramm, G., et al. (2011). The, S. mansoni glycoprotein omega-1 induces Foxp3 expression in NOD mouse CD4(+) T cells. Eur. J. Immunol. 41, 2709-2718.
221. Zaccone, P., Fehervari, Z., Jones, F. M., Sidobre, S., Kronenberg, M., Dunne, D. W., et al. (2003). Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes. Eur. J. Immunol. 33, 1439-1449.
222. Zaccone, P., Fehervari, Z., Phillips, J. M., Dunne, D. W., and Cooke, A. (2006). Parasitic worms and inflammatory diseases. Parasite Immunol. 28, 515-523.
223. Zheng, X., Hu, X., Zhou, G., Lu, Z., Qiu, W., Bao, J., et al. (2008). Soluble egg antigen from Schistosoma japonicum modulates the progression of chronic progressive experimental autoimmune encephalomyelitis via Th2-shift response. J. Neuroimmunol. 194, 107-114.
224. Zhu, B., Trikudanathan, S., Zozulya, A. L., Sandoval-Garcia, C., Kennedy, J. K., Atochina, O., et al. (2012). Immune modulation by Lacto-N-fucopentaose III in experimental autoimmune encephalomyelitis. Clin. Immunol. 142, 351-361.
225. Zubler, R. H., Cantor, H., Benacerraf, B., and Germain, R. N. (1980). Feedback suppression of the immune response in vitro. I. Activity of antigen-stimulated B cells. J. Exp. Med. 151, 667-680.