Functional analysis of effector and regulatory T cells in a parasitic nematode infection

Infection and Immunity

Volumn 76, Issue 5, 2008, Pages 1908-1919

  Rausch, Sebastian ^a   Huehn, Jochen ^b   Kirchhoff, Dennis ^c   Rzepecka, Justyna ^a   Schnoeller, Corinna ^a   Pillai, Smitha ^a   Loddenkemper, Christoph ^b   Scheffold, Alexander ^c   Hamann, Alf ^b   Lucius, Richard ^a   Hartmann, Susanne ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CD103 ANTIGEN; CD40 LIGAND; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; TRANSCRIPTION FACTOR FOXP3; ALPHA E INTEGRINS; ALPHA INTEGRIN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; LEUKOCYTE ANTIGEN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CD4+ T LYMPHOCYTE; CELL CULTURE; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; EFFECTOR CELL; ENZYME ACTIVITY; FLOW CYTOMETRY; HELIGMOSOMOIDES POLYGYRUS; HISTOLOGY; IMMUNE RESPONSE; IMMUNOHISTOLOGY; IN VITRO STUDY; LYMPHATIC DRAINAGE; LYMPHOCYTE COUNT; MOUSE; NEMATODIASIS; NONHUMAN; PARASITOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN TRANSPORT; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN; STATISTICAL SIGNIFICANCE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CHEMISTRY; HELPER CELL; IMMUNOLOGY; ISOLATION AND PURIFICATION; LYMPH NODE; METABOLISM; NEMATOSPIROIDES DUBIUS; PARASITOLOGY;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD; CD40 LIGAND; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; INTEGRIN ALPHA CHAINS; INTERLEUKIN-10; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; INTERLEUKIN-4; LYMPH NODES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEMATOSPIROIDES DUBIUS; SPLEEN; STRONGYLIDA INFECTIONS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY;

EID: 42949155819     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01233-07     Document Type: Article

References (70)

1. Akiho, H., Y. Deng, P. Blennerhassett, H. Kanbayashi, and S. M. Collins. 2005. Mechanisms underlying the maintenance of muscle hypercontractility in a model of postinfective gut dysfunction. Gastroenterology 129:131-141.
2. Al-Qaoud, K. M., B. Fleischer, and A. Hoerauf. 1998. The Xid defect imparts susceptibility to experimental murine filariosis - association with a lack of antibody and IL-10 production by B cells in response to phosphorylcholine. Int. Immunol. 10:17-25.
3. - Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204:285-297.
4. H2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat. Med. 12:955-960.
5. H2 pathways in patent lymphatic filariasis: implications for parasite persistence. J. Immunol. 176:3248-3256.
6. + 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.
7. Behnke, J. M., A. Lowe, S. Clifford, and D. Wakelin. 2003. Cellular and serological responses in resistant and susceptible mice exposed to repeated infection with Heligmosomoides polygyrus bakeri. Parasite Immunol. 25:333-340.
8. Beiting, D. P., L. F. Gagliardo, M. Hesse, S. K. Bliss, D. Meskill, and J. A. Appleton. 2007. Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T cells, and TGF-beta. J. Immunol. 178:1039-1047.
9. + regulatory T cells control Leishmania major persistence and immunity. Nature 420:502-507.
10. Doligalska, M., K. Donskow-Schmelter, J. Rzepecka, and N. Drela. 2007. Reduced apoptosis in BALB/c mice infected with Heligmosomoides polygyrus. Parasite Immunol. 29:283-291.
11. Fallon, P. G., H. E. Jolin, P. Smith, C. L. Emson, M. J. Townsend, R. Fallon, P. Smith, and A. N. McKenzie. 2002. IL-4 induces characteristic Th2 responses even in the combined absence of IL-5, IL-9, and IL-13. Immunity 17:7-17.
12. Finkelman, F. D., T. Shea-Donohue, J. Goldhill, C. A. Sullivan, S. C. Morris, K. B. Madden, W. C. Gause, and J. F. Urban, Jr. 1997. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 15:505-533.
13. Finkelman, F. D., T. Shea-Donohue, S. C. Morris, L. Gildea, R. Strait, K. B. Madden, L. Schopf, and J. F. Urban, Jr. 2004. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 201:139-155.
14. + regulatory T cells in Heligmosomoides polygyrus infection. Eur. J. Immunol. 37:1874-1886.
15. + T cells specific for defined antigens according to CD154 expression. Nat. Med. 11:1118-1124.
16. Gessner, A., K. Mohrs, and M. Mohrs. 2005. Mast cells, basophils, and eosinophils acquire constitutive IL-4 and IL-13 transcripts during lineage differentiation that are sufficient for rapid cytokine production. J. Immunol. 174:1063-1072.
17. Gillan, V., R. A. Lawrence, and E. Devaney. 2005. B cells play a regulatory role in mice infected with the L3 of Brugia pahangi. Int. Immunol. 17:373-382.
18. Grencis, R. K., and A. J. Bancroft. 2004. Interleukin-13: a key mediator in resistance to gastrointestinal-dwelling nematode parasites. Clin. Rev. Allergy Immunol. 26:51-60.
19. Harnett, W., and M. M. Harnett. 2006. What causes lymphocyte hyporesponsiveness during filarial nematode infection? Trends Parasitol. 22:105-110.
20. 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.
21. + regulatory T cells. Nat. Med. 10:29-30.
22. Huehn, J., and A. Hamann. 2005. Homing to suppress: address codes for Treg migration. Trends. Immunol. 26:632-636.
23. + regulatory T cells. J. Exp. Med. 199:303-313.
24. Jackson, J. A., J. D. Turner, L. Rentoul, H. Faulkner, J. M. Behnke, M. Hoyle, R. K. Grencis, K. L. Else, J. Kamgno, M. Boussinesq, and J. E. Bradley. 2004. T helper cell type 2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. J. Infect. Dis. 190:1804-1811.
25. - Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 204:273-283.
26. Kirchhoff, D., M. Frentsch, P. Leclerk, D. Bumann, S. Rausch, S. Hartmann, A. Thiel, and A. Scheffold. 2007. Identification and isolation of murine antigen-reactive T cells according to CD154 expression. Eur. J. Immunol. 37:2370-2377.
27. 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.
28. Kursar, M., M. Koch, H. W. Mittrucker, G. Nouailles, K. Bonhagen, T. Kamradt, and S. H. Kaufmann. 2007. Regulatory T cells prevent efficient clearance of Mycobacterium tuberculosis. J. Immunol. 178:2661- 2665.
29. Layland, L. E., R. Rad, H. Wagner, and C. U. da Costa. 2007. Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2. Eur. J. Immunol. 37:2174-2184.
30. - regulatory T cells. Proc. Natl. Acad. Sci. USA 99:13031-13036.
31. -ΔΔCT method. Methods 25:402-408.
32. + regulatory T cells at the single-cell level. Eur. J. Immunol. 36:245.
33. + regulatory T cells in human colorectal cancer. J. Transl. Med. 4:52.
34. Maizels, R. M., and M. Yazdanbakhsh. 2003. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol. 3:733-744.
35. 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.
36. + T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197:111-119.
37. + cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development. J. Immunol. 173:1224-1231.
38. + regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity. J. Exp. Med. 200:201-210.
39. + regulatory T cells in the intestine by Heligmosomoides polygyrus infection. Am. J. Physiol. Gastrointest. Liver 291:253-259.
40. Miyara, M., and S. Sakaguchi. 2007. Natural regulatory T cells: mechanisms of suppression. Trends. Mol. Med. 13:108-116.
41. Mohrs, K., A. E. Wakil, N. Killeen, R. M. Locksley, and M. Mohrs. 2005. A two-step process for cytokine production revealed by IL-4 dual-reporter mice. Immunity 23:419-429.
42. Monroy, F. G., and F. J. Enriquez. 1992. Heligmosomoides polygyrus: a model for chronic gastrointestinal helminthiasis. Parasitol. Today 8:49-54.
43. Morimoto, M., M. Morimoto, J. Whitmire, S. Xiao, R. M. Anthony, H. Mirakami, R. A. Star, J. F. Urban, Jr., and W. C. Gause. 2004. Peripheral CD4 T cells rapidly accumulate at the host:parasite interface during an inflammatory Th2 memory response. J. Immunol. 172:2424-2430.
44. + T-cell function and inhibit the development of Plasmodium berghei-specific TH1 responses involved in cerebral malaria pathogenesis. Infect. Immun. 75:2275-2282.
45. O'Garra, A., R. Chang, N. Go, R. Hastings, C. Haughton, and M. Howard. 1992. Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur. J. Immunol. 22:711-717.
46. Palanivel, V., C. Posey, A. M. Horauf, W. Solbach, W. F. Pressens, and D. A. Harn. 1996. B-cell outgrowth and ligand-specific production of IL-10 correlate with Th2 dominance in certain parasitic diseases. Exp. Parasitol. 84:168-177.
47. Pritchard, D. I., C. E. Lawrence, P. Appleby, I. A. Gibb, and K. Glover. 1994. Immunosuppressive proteins secreted by the gastrointestinal nematode parasite Heligmosomoides polygyrus. Int. J. Parasitol. 24:495-500.
48. + suppressor T cells regulate pathogen induced inflammation and disease. FEMS Immunol. Med. Microbiol. 44:121-127.
49. Rzepecka, J., R. Lucius, M. Doligalska, S. Beck, S. Rausch, and S. Hartmann. 2006. Screening for immunomodulatory proteins of the intestinal parasitic nematode Heligmosomoides polygyrus. Parasite Immunol. 28:463-472.
50. Sakaguchi, S., and F. Powrie. 2007. Emerging challenges in regulatory T cell function and biology. Science 317:627-629.
51. Satoguina, J., M. Mempel, J. Larbi, M. Badusche, C. Loliger, O. Adjei, G. Gachelin, B. Fleischer, and A. Hoerauf. 2002. Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). Microbes Infect. 4:1291-1300.
52. Segura, M., Z. Su, C. Piccirillo, and M. M. Stevenson. 2007. Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematode-induced immunosuppression. Eur. J. Immunol. 37:1887-1904.
53. Shea-Donohue, T., C. Sullivan, F. D. Finkelman, K. B. Madden, S. C. Morris, J. Goldhill, V. Pineiro-Carrero, and J. F. Urban, Jr. 2001. The role of IL-4 in Heligmosomoides polygyrus-induced alterations in murine intestinal epithelial cell function. J. Immunol. 167:2234-2239.
54. Siegmund, K., M. Feuerer, C. Siewert, S. Ghani, U. Haubold, A. Dankof, V. Krenn, M. P. Schon, A. Scheffold, J. B. Lowe, A. Hamann, U. Syrbe, and J. Huehn. 2005. Migration matters: regulatory T-cell compartmentalization determines suppressive activity in vivo. Blood 106:3097-3104.
55. Solbach, W., and R. Lucius. 2005. Parasite evasion, p. 675-691. In S. Kaufmann and M. Steward (ed.), Topley and Wilson microbiology and microbial infections, 10th ed. Hodder Arnold, London, United Kingdom.
56. 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.
57. + Treg and control of Leishmania major infection. J. Immunol. 174:5444-5455.
58. Taylor, J. D., 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.
59. Taylor, M. D., L. LeGoff, A. Harris, E. Malone, J. E. Allen, and R. M. Maizels. 2005. Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J. Immunol. 174:4924-4933.
60. + T cell hyporesponsiveness at sites peripheral to filarial infection. J. Immunol. 176:6918-6927.
61. Trinchieri, G. 2007. Interleukin-10 production by effector T cells: Th1 cells show self control. J. Exp. Med. 204:239-243.
62. Turner, J. D., H. Faulkner, J. Kamgno, F. Cormont, J. van Snick, K. J. Else, R. K. Grencis, J. M. Behnke, M. Boussinesq, and J. E. Bradley. 2003. Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. J. Infect. Dis. 188:1768-1775.
63. 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.
64. Urban, J. F., Jr., C. R. Maliszewski, K. B. Madden, I. M. Katona, and F. D. Finkelman. 1995. IL4 treatment can cure established gastrointestinal nematode infections in immunocompetent and immunodeficient mice. J. Immunol. 154:4675-4684.
65. Urban, J. F., Jr., N. Noben-Trauth, D. D. Donaldson, K. B. Madden, S. C. Morris, M. Collins, and F. D. Finkelman. 1998. IL-13, IL4Rα, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 8:255-264.
66. Uzonna, J. E., G. Wei, D. Yurkowski, and P. Bretscher. 2001. Immune elimination of Leishmania major in mice: implications for immune memory, vaccination, and reactivation disease. J. Immunol. 167:6967-6974.
67. + regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 23:287-296.
68. Wilson, M. S., M. D. Taylor, A. Balic, C. A. Finney, J. R. Lamb, and R. M. Maizels. 2005. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J. Exp. Med. 202:1199-1212.
69. + T cells following infection with a gastrointestinal helminth. J. Immunol. 177:511-518.
70. Zhao, A., J. McDermott, J. F. Urban, Jr., W. Gause, K. B. Madden, K. A. Yeung, S. C. Morris, F. D. Finkelman, and T. Shea-Donohue. 2003. Dependence of IL-4, IL-13, and nematode-induced alterations in murine small intestinal smooth muscle contractility on Stat6 and enteric nerves. J. Immunol. 171:948-954.