Coinfection with the intestinal nematode Heligmosomoides polygyrus markedly reduces hepatic egg-induced immunopathology and proinflammatory cytokines in mouse models of severe schistosomiasis

Infection and Immunity

Volumn 76, Issue 11, 2008, Pages 5164-5172

  Bazzone, Lindsey E ^a   Smith, Patrick M ^a   Rutitzky, Laura I ^a   Shainheit, Mara G ^a   Urban, Joseph F ^c   Setiawan, Tommy ^b   Blum, Arthur M ^b   Weinstock, Joel V ^b   Stadecker, Miguel J ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TUFTS MEDICAL CENTER   (United States)

^c BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; FREUND ADJUVANT; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; PARASITE ANTIGEN; SECRETORY PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; YM1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; EXPERIMENTAL MODEL; FEMALE; HELIGMOSOMOIDES POLYGYRUS; LIVER GRANULOMA; LYMPH NODE CELL; MACROPHAGE ACTIVATION; MESENTERY LYMPH NODE; MIXED INFECTION; MOUSE; NEMATODIASIS; NONHUMAN; PARASITE IDENTIFICATION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; TH1 CELL; TH2 CELL;

ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; LIVER; LIVER DISEASES, PARASITIC; MACROPHAGES; MICE; NEMATOSPIROIDES DUBIUS; OVUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SCHISTOSOMIASIS MANSONI; STRONGYLIDA INFECTIONS; T-LYMPHOCYTES, REGULATORY;

EID: 55849095063     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00673-08     Document Type: Article

References (78)

1. Adewusi, O. I., N. A. Nix, X. Lu, D. G. Colley, and W. E. Secor. 1996. Schistosoma mansoni: relationship of tumor necrosis factor-alpha to morbidity and collagen deposition in chronic experimental infection. Exp. Parasitol. 84:115-123.
2. Aggarwal, S., N. Ghilardi, M. H. Xie, F. J. de Sauvage, and A. L. Gurney. 2003. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278:1910-1914.
3. + T cells regulate the expansion of peripheral CD4 T cells through the production of IL-10. J. Immunol. 166:3008-3018.
4. Anthony, R. M., L. I. Rutitzky, J. F. Urban, Jr., M. J. Stadecker, and W. C. Gause. 2007. Protective immune mechanisms in helminth infection. Nat. Rev. Immunol. 7:975-987.
5. Araujo, M. I., S. K. Bliss, Y. Suzuki, A. Alcaraz, E. Y. Denkers, and E. J. Pearce. 2001. Interleukin-12 promotes pathologic liver changes and death in mice coinfected with Schistosoma mansoni and Toxoplasma gondii. Infect. Immun. 69:1454-1462.
6. Araujo, M. I., A. R. de Jesus, O. Bacellar, E. Sabin, E. Pearce, and E. M. Carvalho. 1996. Evidence of a T helper type 2 activation in human schistosomiasis. Eur. J. Immunol. 26:1399-1403.
7. Attallah, A. M., A. T. Abbas, M. I. Dessouky, H. M. El-Emshaty, and H. M. Elsheikha. 2006. Susceptibility of neonate mice born to Schistosoma mansoni-infected and noninfected mothers to subsequent S. mansoni infection. Parasitol. Res. 99:137-145.
8. + 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.
9. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441:235-238.
10. Bica, I., D. H. Hamer, and M. J. Stadecker. 2000. Hepatic schistosomiasis. Infect. Dis. Clin. N. Am. 14:583-604, viii.
11. Boros, D. L., and K. S. Warren. 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.
12. Capron, A., D. Dombrowicz, and M. Capron. 2004. Helminth infections and allergic diseases: from the Th2 paradigm to regulatory networks. Clin. Rev. Allergy Immunol. 26:25-34.
13. Cheever, A. W., R. H. Duvall, T. A. Hallack, Jr., R. G. Minker, J. D. Malley, and K. G. Malley. 1987. Variation of hepatic fibrosis and granuloma size among mouse strains infected with Schistosoma mansoni. Am. J. Trop. Med. Hyg. 37:85-97.
14. Chen, Y., C. L. Langrish, B. McKenzie, B. Joyce-Shaikh, J. S. Stumhofer, T. McClanahan, W. Blumenschein, T. Churakovsa, J. Low, L. Presta, C. A. Hunter, R. A. Kastelein, and D. J. Cua. 2006. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J. Clin. Investig. 116:1317-1326.
15. Chiaramonte, M. G., D. D. Donaldson, A. W. Cheever, and T. A. Wynn. 1999. An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J. Clin. Investig. 104:777-785.
16. Colley, D. G., M. A. Montesano, G. L. Freeman, and W. E. Secor. 1999. Infection-stimulated or perinatally initiated idiotypic interactions can direct differential morbidity and mortality in schistosomiasis. Microbes Infect. 1:517-524.
17. Cooke, A., P. Tonks, F. M. Jones, H. O'Shea, P. Hutchings, A. J. Fulford, and D. W. Dunne. 1999. Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol. 21:169-176.
18. de Jesus, A. R., A. Silva, L. B. Santana, A. Magalhaes, A. A. de Jesus, R. P. de Almeida, M. A. Rego, M. N. Burattini, E. J. Pearce, and E. M. Carvalho. 2002. Clinical and immunologic evaluation of 31 patients with acute schistosomiasis mansoni. J. Infect. Dis. 185:98-105.
19. Dunne, D. W., and A. Cooke. 2005. A worm's eye view of the immune system: consequences for evolution of human autoimmune disease. Nat. Rev. Immunol. 5:420-426.
20. Dunne, D. W., and E. M. Riley. 2004. Immunity, morbidity and immunoepidemiology in parasite infections. Parasite Immunol. 26:425-428.
21. Elias, D., S. Britton, A. Kassu, and H. Akuffo. 2007. Chronic helminth infections may negatively influence immunity against tuberculosis and other diseases of public health importance. Expert Rev. Anti-Infect. Ther. 5:475-484.
22. Elliott, D. E., T. Setiawan, A. Metwali, A. Blum, J. F. Urban, Jr., and J. V. Weinstock. 2004. Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice. Eur. J. Immunol. 34:2690-2698.
23. Fallon, P. G., E. J. Richardson, G. J. McKenzie, and A. N. McKenzie. 2000. 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.
24. + regulatory T cells. Nat. Immunol. 4:330-336.
25. Gause, W. C., J. F. Urban, Jr., and M. J. Stadecker. 2003. The immune response to parasitic helminths: insights from murine models. Trends Immunol. 24:269-277.
26. Goerdt, S., and C. E. Orfanos. 1999. Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 10:137-142.
27. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3:23-35.
28. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6:1123-1132.
29. Helmby, H., M. Kullberg, and M. Troye-Blomberg. 1998. Altered immune responses in mice with concomitant Schistosoma mansoni and Plasmodium chabaudi infections. Infect. Immun. 66:5167-5174.
30. Herbert, D. R., C. Holscher, M. Mohrs, B. Arendse, A. Schwegmann, M. Radwanska, M. Leeto, R. Kirsch, P. Hall, H. Mossmann, B. Claussen, I. Forster, and F. Brombacher. 2004. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20:623-635.
31. Hesse, M., C. A. Piccirillo, Y. Belkaid, J. Prufer, M. Mentink-Kane, M. Leusink, A. W. Cheever, E. M. Shevach, and T. A. Wynn. 2004. The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. J. Immunol. 172:3157-3166.
32. Kastelein, R. A., C. A. Hunter, and D. J. Cua. 2007. Discovery and biology of IL-23 and IL-27: related but functionally distinct regulators of inflammation. Annu. Rev. Immunol. 25:221-242.
33. + T-cell immunity against Toxoplasma gondii. Infect. Immun. 76:1305-1313.
34. Kitagaki, K., T. R. Businga, D. Racila, D. E. Elliott, J. V. Weinstock, and J. N. Kline. 2006. Intestinal helminths protect in a murine model of asthma. J. Immunol. 177:1628-1635.
35. Kolls, J. K., and A. Linden. 2004. Interleukin-17 family members and inflammation. Immunity 21:467-476.
36. Korn, T., E. Bettelli, W. Gao, A. Awasthi, A. Jager, T. B. Strom, M. Oukka, and V. K. Kuchroo. 2007. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448:484-487.
37. La Flamme, A. C., K. Canagasabey, M. Harvie, and B. T. Backstrom. 2004. Schistosomiasis protects against multiple sclerosis. Mem. Inst. Oswaldo Cruz 99:33-36.
38. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201:233-240.
39. Legesse, M., B. Erko, and F. Balcha. 2004. Increased parasitaemia and delayed parasite clearance in Schistosoma mansoni and Plasmodium berghei co-infected mice. Acta Trop. 91:161-166.
40. Loke, P., M. G. Nair, J. Parkinson, D. Guiliano, M. Blaxter, and J. E. Allen. 2002. IL-4 dependent alternatively-activated macrophages have a distinctive in vivo gene expression phenotype. BMC Immunol. 3:7.
41. Maizels, R. M. 2005. Infections and allergy - helminths, hygiene and host immune regulation. Curr. Opin. Immunol. 17:656-661.
42. Maizels, R. M., A. Balic, N. Gomez-Escobar, M. Nair, M. D. Taylor, and J. E. Allen. 2004. Helminth parasites - masters of regulation. Immunol. Rev. 201:89-116.
43. + T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197:111-119.
44. Mantovani, A., A. Sica, and M. Locati. 2005. Macrophage polarization comes of age. Immunity 23:344-346.
45. Marquet, S., L. Abel, D. Hillaire, H. Dessein, J. Kalil, J. Feingold, J. Weissenbach, and A. J. Dessein. 1996. Genetic localization of a locus controlling the intensity of infection by Schistosoma mansoni on chromosome 5q31-q33. Nat. Genet. 14:181-184.
46. + cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development. J. Immunol. 173:1224-1231.
47. Montenegro, S. M., P. Miranda, S. Mahanty, F. G. Abath, K. M. Teixeira, E. M. Coutinho, J. Brinkman, I. Goncalves, L. A. Domingues, A. L. Domingues, A. Sher, and T. A. Wynn. 1999. Cytokine production in acute versus chronic human Schistosomiasis mansoni: the cross-regulatory role of interferon-gamma and interleukin-10 in the responses of peripheral blood mononuclear cells and splenocytes to parasite antigens. J. Infect. Dis. 179:1502-1514.
48. Montesano, M. A., D. G. Colley, M. T. Willard, G. L. Freeman, Jr., and W. E. Secor. 2002. Idiotypes expressed early in experimental Schistosoma mansoni infections predict clinical outcomes of chronic disease. J. Exp. Med. 195:1223-1228.
49. Mwatha, J. K., G. Kimani, T. Kamau, G. G. Mbugua, J. H. Ouma, J. Mumo, A. J. Fulford, F. M. Jones, A. E. Butterworth, M. B. Roberts, and D. W. Dunne. 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.
50. Nacher, M., P. Singhasivanon, S. Yimsamran, W. Manibunyong, N. Thanyavanich, R. Wuthisen, and S. Looareesuwan. 2002. Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum malaria in Thailand. J. Parasitol. 88:55-58.
51. Nagayama, Y., K. Watanabe, M. Niwa, S. M. McLachlan, and B. Rapoport. 2004. Schistosoma mansoni and alpha-galactosylceramide: prophylactic effect of Th1 immune suppression in a mouse model of Graves' hyperthyroidism. J. Immunol. 173:2167-2173.
52. Noland, G. S., J. F. Urban, Jr., B. Fried, and N. Kumar. 2008. Counter-regulatory anti-parasite cytokine responses during concurrent Plasmodium yoelli and intestinal helminth infections in mice. Exp. Parasitol. 119:272-278.
53. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6:1133-1141.
54. Rutitzky, L. I., L. Bazzone, M. G. Shainheit, B. Joyce-Shaikh, D. J. Cua, and M. J. Stadecker. 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.
55. Rutitzky, L. I., H. J. Hernandez, and M. J. Stadecker. 2001. Th1-polarizing immunization with egg antigens correlates with severe exacerbation of immunopathology and death in schistosome infection. Proc. Natl. Acad. Sci. USA 98:13243-13248.
56. Rutitzky, L. I., H. J. Hernandez, Y. S. Yim, D. E. Ricklan, E. Finger, C. Mohan, I. Peter, E. K. Wakeland, and M. J. Stadecker. 2005. Enhanced egg-induced immunopathology correlates with high IFN-gamma in murine schistosomiasis: identification of two epistatic genetic intervals. J. Immunol. 174:435-440.
57. Rutitzky, L. I., J. R. Lopes da Rosa, and M. J. Stadecker. 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.
58. Saunders, K. A., T. Raine, A. Cooke, and C. E. Lawrence. 2007. Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection. Infect. Immun. 75:397-407.
59. Sewell, D., Z. Qing, E. Reinke, D. Elliot, J. Weinstock, M. Sandor, and Z. Fabry. 2003. Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int. Immunol. 15:59-69.
60. Silveira, A. M., G. Gazzinelli, L. F. Alves-Oliveira, J. Bethony, A. Gazzinelli, C. Carvalho-Queiroz, M. C. Alvarez, F. C. Lima-Silva, A. Prata, P. T. LoVerde, and R. Correa-Oliveira. 2004. Human schistosomiasis mansoni: intensity of infection differentially affects the production of interleukin-10, interferon-gamma and interleukin-13 by soluble egg antigen or adult worm antigen stimulated cultures. Trans. R. Soc. Trop. Med. Hyg. 98:514-519.
61. Stockinger, B., M. Veldhoen, and B. Martin. 2007. Th17 T cells: linking innate and adaptive immunity. Semin. Immunol. 19:353-361.
62. Su, Z., M. Segura, K. Morgan, J. C. Loredo-Osti, and M. M. Stevenson. 2005. Impairment of protective immunity to blood-stage malaria by concurrent nematode infection. Infect. Immun. 73:3531-3539.
63. Summers, R. W., D. E. Elliott, J. F. Urban, Jr., R. Thompson, and J. V. Weinstock. 2005. Trichuris suis therapy in Crohn's disease. Gut 54:87-90.
64. Sutton, C., C. Brereton, B. Keogh, K. H. Mills, and E. C. Lavelle. 2006. A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J. Exp. Med. 203:1685-1691.
65. Svetic, A., K. B. Madden, X. D. Zhou, P. Lu, I. M. Katona, F. D. Finkelman, J. F. Urban, Jr., and W. C. Gause. 1993. A primary intestinal helminthic infection rapidly induces a gut-associated elevation of Th2-associated cytokines and IL-3. J. Immunol. 150:3434-3441.
66. Talaat, K. R., R. E. Bonawitz, P. Domenech, and T. B. Nutman. 2006. Preexposure to live Brugia malayi microfilariae alters the innate response of human dendritic cells to Mycobacterium tuberculosis. J. Infect. Dis. 193:196-204.
67. Taylor, J. J., M. Mohrs, and E. J. Pearce. 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.
68. Tristao-Sa, R., R. Ribeiro-Rodrigues, L. T. Johnson, F. E. Pereira, and R. Dietze. 2002. Intestinal nematodes and pulmonary tuberculosis. Rev. Soc. Bras. Med. Trop. 35:533-535.
69. Urban, J. F., Jr., I. M. Katona, W. E. Paul, and F. D. Finkelman. 1991. Interleukin 4 is important in protective immunity to a gastrointestinal nematode infection in mice. Proc. Natl. Acad. Sci. USA 88:5513-5517.
70. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24:179-189.
71. Vignali, D. A., L. W. Collison, and C. J. Workman. 2008. How regulatory T cells work. Nat. Rev. Immunol. 8:523-532.
72. Welch, J. S., L. Escoubet-Lozach, D. B. Sykes, K. Liddiard, D. R. Greaves, and C. K. Glass. 2002. TH2 cytokines and allergic challenge induce Ym1 expression in macrophages by a STAT6-dependent mechanism. J. Biol. Chem. 277:42821-42829.
73. Weng, M., D. Huntley, I. F. Huang, O. Foye-Jackson, L. Wang, A. Sarkissian, Q. Zhou, W. A. Walker, B. J. Cherayil, and H. N. Shi. 2007. Alternatively activated macrophages in intestinal helminth infection: effects on concurrent bacterial colitis. J. Immunol. 179:4721-4731.
74. Yazdanbakhsh, M., P. G. Kremsner, and R. van Ree. 2002. Allergy, parasites, and the hygiene hypothesis. Science 296:490-494.
75. Yazdanbakhsh, M., and P. M. Matricardi. 2004. Parasites and the hygiene hypothesis: regulating the immune system? Clin. Rev. Allergy Immunol. 26:15-24.
76. Zaccone, P., Z. Fehervari, F. M. Jones, S. Sidobre, M. Kronenberg, D. W. Dunne, and A. Cooke. 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.
77. Zaccone, P., Z. Fehervari, J. M. Phillips, D. W. Dunne, and A. Cooke. 2006. Parasitic worms and inflammatory diseases. Parasite Immunol. 28:515-523.
78. Zinn-Justin, A., S. Marquet, D. Hillaire, A. Dessein, and L. Abel. 2001. Genome search for additional human loci controlling infection levels by Schistosoma mansoni. Am. J. Trop. Med. Hyg. 65:754-758.