Concurrent bacterial stimulation alters the function of Helminth-activated dendritic cells, resulting in IL-17 induction

Journal of Immunology

Volumn 188, Issue 5, 2012, Pages 2350-2358

  Perona Wright, Georgia ^a,c   Lundie, Rachel J ^a   Jenkins, Stephen J ^a   Webb, Lauren M ^a   Grencis, Richard K ^b   MacDonald, Andrew S ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 17; PARASITE ANTIGEN; SCHISTOSOME ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIUM; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE SEVERITY; FEMALE; HOST; IMMUNIZATION; IMMUNOREGULATION; IMMUNOSTIMULATION; LEUKOCYTE FUNCTION; MALE; NONHUMAN; PRIORITY JOURNAL; SCHISTOSOMIASIS; WILD TYPE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, HELMINTH; CELLS, CULTURED; DENDRITIC CELLS; INTERLEUKIN-10; INTERLEUKIN-17; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROPIONIBACTERIUM ACNES; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS;

EID: 84857497002     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101642     Document Type: Article

References (86)

1. Hotez, P. J., P. J. Brindley, J. M. Bethony, C. H. King, E. J. Pearce, and J. Jacobson. 2008. Helminth infections: the great neglected tropical diseases. J. Clin. Invest. 118: 1311-1321. (Pubitemid 351500423)
2. van der Werf, M. J., S. J. de Vlas, S. Brooker, C. W. Looman, N. J. Nagelkerke, J. D. Habbema, and D. Engels. 2003. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop. 86: 125-139. (Pubitemid 36561364)
3. Cheever, A. W., J. G. Macedonia, J. E. Mosimann, and E. A. Cheever. 1994. Kinetics of egg production and egg excretion by Schistosoma mansoni and S. japonicum in mice infected with a single pair of worms. Am. J. Trop. Med. Hyg. 50: 281-295.
4. Pearce, E. J., and A. S. MacDonald. 2002. The immunobiology of schistosomiasis. Nat. Rev. Immunol. 2: 499-511. (Pubitemid 37328741)
5. Cheever, A. W., and G. S. Yap. 1997. Immunologic basis of disease and disease regulation in schistosomiasis. Chem. Immunol. 66: 159-176. (Pubitemid 27139774)
6. Bica, I., D. H. Hamer, and M. J. Stadecker. 2000. Hepatic schistosomiasis. Infect. Dis. Clin. North Am. 14: 583-604, viii.
7. 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. (Pubitemid 17155348)
8. Pearce, E. J., P. Caspar, J. M. Grzych, F. A. Lewis, and A. Sher. 1991. Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J. Exp. Med. 173: 159-166.
9. 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. Invest. 104: 777-785. (Pubitemid 29536363)
10. 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. (Pubitemid 30115489)
11. Brunet, L. R., F. D. Finkelman, A. W. Cheever, M. A. Kopf, and E. J. Pearce. 1997. IL-4 protects against TNF-alpha-mediated cachexia and death during acute schistosomiasis. J. Immunol. 159: 777-785. (Pubitemid 127484229)
12. Herbert, D. R., C. Hölscher, M. Mohrs, B. Arendse, A. Schwegmann, M. Radwanska, M. Leeto, R. Kirsch, P. Hall, H. Mossmann, et al. 2004. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20: 623-635. (Pubitemid 38659504)
13. Hernandez, H. J., C. M. Edson, D. A. Harn, C. J. Ianelli, and M. J. Stadecker. 1998. Schistosoma mansoni: genetic restriction and cytokine profile of the CD4 + T helper cell response to dominant epitope peptide of major egg antigen Sm-p40. Exp. Parasitol. 90: 122-130. (Pubitemid 28406694)
14. 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. (Pubitemid 41292052)
15. 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.
16. Sadler, C. H., L. I. Rutitzky, M. J. Stadecker, and R. A. Wilson. 2003. IL-10 is crucial for the transition from acute to chronic disease state during infection of mice with Schistosoma mansoni. Eur. J. Immunol. 33: 880-888. (Pubitemid 36546675)
17. Wynn, T. A., A. W. Cheever, M. E. Williams, S. Hieny, P. Caspar, R. Kühn, W. Müller, and A. Sher. 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. (Pubitemid 28217306)
18. Cua, D. J., J. Sherlock, Y. Chen, C. A. Murphy, B. Joyce, B. Seymour, L. Lucian, W. To, S. Kwan, T. Churakova, et al. 2003. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421: 744-748. (Pubitemid 36227625)
19. 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. (Pubitemid 41541791)
20. Nakae, S., A. Nambu, K. Sudo, and Y. Iwakura. 2003. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J. Immunol. 171: 6173-6177. (Pubitemid 37467240)
21. Huang, W., L. Na, P. L. Fidel, and P. Schwarzenberger. 2004. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis. 190: 624-631. (Pubitemid 38982105)
22. Puel, A., S. Cypowyj, J. Bustamante, J. F. Wright, L. Liu, H. K. Lim, M. Migaud, L. Israel, M. Chrabieh, M. Audry, et al. 2011. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332: 65-68.
23. Luzza, F., T. Parrello, G. Monteleone, L. Sebkova, M. Romano, R. Zarrilli, M. Imeneo, and F. Pallone. 2000. Up-regulation of IL-17 is associated with bioactive IL-8 expression in Helicobacter pylori-infected human gastric mucosa. J. Immunol. 165: 5332-5337.
24. Burchill, M. A., D. T. Nardelli, D. M. England, D. J. DeCoster, J. A. Christopherson, S. M. Callister, and R. F. Schell. 2003. Inhibition of interleukin-17 prevents the development of arthritis in vaccinated mice challenged with Borrelia burgdorferi. Infect. Immun. 71: 3437-3442. (Pubitemid 36637572)
25. 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.
26. Mangan, P. R., L. E. Harrington, D. B. O'Quinn, W. S. Helms, D. C. Bullard, C. O. Elson, R. D. Hatton, S. M. Wahl, T. R. Schoeb, and C. T. Weaver. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441: 231-234.
27. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24: 179-189. (Pubitemid 43214587)
28. Stritesky, G. L., N. Yeh, and M. H. Kaplan. 2008. IL-23 promotes maintenance but not commitment to the Th17 lineage. J. Immunol. 181: 5948-5955.
29. 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. (Pubitemid 44036274)
30. Chung, Y., S. H. Chang, G. J. Martinez, X. O. Yang, R. Nurieva, H. S. Kang, L. Ma, S. S. Watowich, A. M. Jetten, Q. Tian, and C. Dong. 2009. Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 30: 576-587.
31. Nurieva, R., X. O. Yang, G. Martinez, Y. Zhang, A. D. Panopoulos, L. Ma, K. Schluns, Q. Tian, S. S. Watowich, A. M. Jetten, and C. Dong. 2007. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448: 480-483. (Pubitemid 47123514)
32. Korn, T., E. Bettelli, W. Gao, A. Awasthi, A. Jäger, 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. (Pubitemid 47123515)
33. Perona-Wright, G., S. J. Jenkins, R. A. O'Connor, D. Zienkiewicz, H. J. McSorley, R. M. Maizels, S. M. Anderton, and A. S. MacDonald. 2009. A pivotal role for CD40-mediated IL-6 production by dendritic cells during IL-17 induction in vivo. J. Immunol. 182: 2808-2815.
34. Phythian-Adams, A. T., P. C. Cook, R. J. Lundie, L. H. Jones, K. A. Smith, T. A. Barr, K. Hochweller, S. M. Anderton, G. J. Hämmerling, R. M. Maizels, and A. S. MacDonald. 2010. CD11c depletion severely disrupts Th2 induction and development in vivo. J. Exp. Med. 207: 2089-2096.
35. Shainheit, M. G., P. M. Smith, L. E. Bazzone, A. C. Wang, L. I. Rutitzky, and M. J. Stadecker. 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.
36. MacDonald, A. S., A. D. Straw, B. Bauman, and E. J. Pearce. 2001. CD8- dendritic cell activation status plays an integral role in influencing Th2 response development. J. Immunol. 167: 1982-1988. (Pubitemid 32747504)
37. MacDonald, A. S., and E. J. Pearce. 2002. Cutting edge: polarized Th cell response induction by transferred antigen-pulsed dendritic cells is dependent on IL-4 or IL-12 production by recipient cells. J. Immunol. 168: 3127-3130. (Pubitemid 34250368)
38. Lutz, M. B., N. Kukutsch, A. L. Ogilvie, S. Rössner, F. Koch, N. Romani, and G. Schuler. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223: 77-92. (Pubitemid 29096240)
39. Perona-Wright, G., S. J. Jenkins, A. Crawford, D. Gray, E. J. Pearce, and A. S. MacDonald. 2006. Distinct sources and targets of IL-10 during dendritic cell-driven Th1 and Th2 responses in vivo. Eur. J. Immunol. 36: 2367-2375. (Pubitemid 44420593)
40. Worsley, A. G., S. LeibundGut-Landmann, E. Slack, L. K. Phng, H. Gerhardt, C. Reis e Sousa, and A. S. MacDonald. 2008. Dendritic cell expression of the Notch ligand jagged2 is not essential for Th2 response induction in vivo. Eur. J. Immunol. 38: 1043-1049.
41. Perona-Wright, G., S. M. Anderton, S. E. Howie, and D. Gray. 2007. IL-10 permits transient activation of dendritic cells to tolerize T cells and protect from central nervous system autoimmune disease. Int. Immunol. 19: 1123-1134. (Pubitemid 47434245)
42. Jenkins, S. J., G. Perona-Wright, A. G. Worsley, N. Ishii, and A. S. MacDonald. 2007. Dendritic cell expression of OX40 ligand acts as a costimulatory, not polarizing, signal for optimal Th2 priming and memory induction in vivo. J. Immunol. 179: 3515-3523.
43. Perona-Wright, G., S. J. Jenkins, and A. S. MacDonald. 2006. Dendritic cell activation and function in response to Schistosoma mansoni. Int. J. Parasitol. 36: 711-721. (Pubitemid 43786222)
44. Oppmann, B., R. Lesley, B. Blom, J. C. Timans, Y. Xu, B. Hunte, F. Vega, N. Yu, J. Wang, K. Singh, et al. 2000. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13: 715-725.
45. 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. (Pubitemid 38263706)
46. McKee, A. S., and E. J. Pearce. 2004. CD25+CD4+ cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development. J. Immunol. 173: 1224-1231. (Pubitemid 38924300)
47. Kane, C. M., L. Cervi, J. Sun, A. S. McKee, K. S. Masek, S. Shapira, C. A. Hunter, and E. J. Pearce. 2004. Helminth antigens modulate TLR-initiated dendritic cell activation. J. Immunol. 173: 7454-7461. (Pubitemid 39628185)
48. Cervi, L., A. S. MacDonald, C. Kane, F. Dzierszinski, and E. J. Pearce. 2004. Cutting edge: dendritic cells copulsed with microbial and helminth antigens undergo modified maturation, segregate the antigens to distinct intracellular compartments, and concurrently induce microbe-specific Th1 and helminth-specific Th2 responses. J. Immunol. 172: 2016-2020. (Pubitemid 38182346)
49. Kelsall, B. L., C. A. Biron, O. Sharma, and P. M. Kaye. 2002. Dendritic cells at the host-pathogen interface. Nat. Immunol. 3: 699-702.
50. Balic, A., Y. Harcus, M. J. Holland, and R. M. Maizels. 2004. Selective maturation of dendritic cells by Nippostrongylus brasiliensis-secreted proteins drives Th2 immune responses. Eur. J. Immunol. 34: 3047-3059. (Pubitemid 39549384)
51. Jenkins, S. J., G. Perona-Wright, and A. S. MacDonald. 2008. Full development of Th2 immunity requires both innate and adaptive sources of CD154. J. Immunol. 180: 8083-8092.
52. Pulendran, B., H. Tang, and S. Manicassamy. 2010. Programming dendritic cells to induce T(H)2 and tolerogenic responses. Nat. Immunol. 11: 647-655.
53. Harrington, L. E., R. D. Hatton, P. R. Mangan, H. Turner, T. L. Murphy, K. M. Murphy, and C. T. Weaver. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132. (Pubitemid 41541790)
54. Passos, S. T., J. S. Silver, A. C. O'Hara, D. Sehy, J. S. Stumhofer, and C. A. Hunter. 2010. IL-6 promotes NK cell production of IL-17 during toxoplasmosis. J. Immunol. 184: 1776-1783.
55. Doisne, J. M., C. Becourt, L. Amniai, N. Duarte, J. B. Le Luduec, G. Eberl, and K. Benlagha. 2009. Skin and peripheral lymph node invariant NKT cells are mainly retinoic acid receptor-related orphan receptor (gamma)t+ and respond preferentially under inflammatory conditions. J. Immunol. 183: 2142-2149.
56. Lochner, M., L. Peduto, M. Cherrier, S. Sawa, F. Langa, R. Varona, D. Riethmacher, M. Si-Tahar, J. P. Di Santo, and G. Eberl. 2008. In vivo equilibrium of proinflammatory IL-17+ and regulatory IL-10+ Foxp3+ RORgamma t+ T cells. J. Exp. Med. 205: 1381-1393. (Pubitemid 351831494)
57. Sutton, C. E., S. J. Lalor, C. M. Sweeney, C. F. Brereton, E. C. Lavelle, and K. H. Mills. 2009. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 31: 331-341.
58. Moore, K. W., R. de Waal Malefyt, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765. (Pubitemid 32368050)
59. Couper, K. N., D. G. Blount, and E. M. Riley. 2008. IL-10: the master regulator of immunity to infection. J. Immunol. 180: 5771-5777.
60. Grimbaldeston, M. A., S. Nakae, J. Kalesnikoff, M. Tsai, and S. J. Galli. 2007. Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nat. Immunol. 8: 1095-1104. (Pubitemid 47423757)
61. Zhang, X., L. Majlessi, E. Deriaud, C. Leclerc, and R. Lo-Man. 2009. Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity 31: 761-771.
62. Maroof, A., L. Beattie, S. Zubairi, M. Svensson, S. Stager, and P. M. Kaye. 2008. Posttranscriptional regulation of II10 gene expression allows natural killer cells to express immunoregulatory function. Immunity 29: 295-305.
63. Perona-Wright, G., K. Mohrs, F. M. Szaba, L. W. Kummer, R. Madan, C. L. Karp, L. L. Johnson, S. T. Smiley, and M. Mohrs. 2009. Systemic but not local infections elicit immunosuppressive IL-10 production by natural killer cells. Cell Host Microbe 6: 503-512.
64. Neill, D. R., S. H. Wong, A. Bellosi, R. J. Flynn, M. Daly, T. K. Langford, C. Bucks, C. M. Kane, P. G. Fallon, R. Pannell, et al. 2010. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464: 1367-1370.
65. Saenz, S. A., M. C. Siracusa, J. G. Perrigoue, S. P. Spencer, J. F. Urban, Jr., J. E. Tocker, A. L. Budelsky, M. A. Kleinschek, R. A. Kastelein, T. Kambayashi, et al. 2010. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature 464: 1362-1366.
66. Moro, K., T. Yamada, M. Tanabe, T. Takeuchi, T. Ikawa, H. Kawamoto, J. Furusawa, M. Ohtani, H. Fujii, and S. Koyasu. 2010. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 463: 540-544.
67. Huber, S., N. Gagliani, E. Esplugues, W. O'Connor, Jr., F. J. Huber, A. Chaudhry, M. Kamanaka, Y. Kobayashi, C. J. Booth, A. Y. Rudensky, et al. 2011. Th17 cells express interleukin-10 receptor and are controlled by Foxp3- and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 34: 554-565.
68. Chaudhry, A., R. M. Samstein, P. Treuting, Y. Liang, M. C. Pils, J. M. Heinrich, R. S. Jack, F. T. Wunderlich, J. C. Brüning, W. Müller, and A. Y. Rudensky. 2011. Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation. Immunity 34: 566-578.
69. Hoffmann, K. F., A. W. Cheever, and T. A. Wynn. 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. (Pubitemid 30408823)
70. Redford, P. S., A. Boonstra, S. Read, J. Pitt, C. Graham, E. Stavropoulos, G. J. Bancroft, and A. O'Garra. 2010. Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung. Eur. J. Immunol. 40: 2200-2210.
71. McKinstry, K. K., T. M. Strutt, A. Buck, J. D. Curtis, J. P. Dibble, G. Huston, M. Tighe, H. Hamada, S. Sell, R. W. Dutton, and S. L. Swain. 2009. IL-10 deficiency unleashes an influenza-specific Th17 response and enhances survival against high-dose challenge. J. Immunol. 182: 7353-7363.
72. McGeachy, M. J., K. S. Bak-Jensen, Y. Chen, C. M. Tato, W. Blumenschein, T. McClanahan, and D. J. Cua. 2007. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat. Immunol. 8: 1390-1397. (Pubitemid 350138974)
73. Jarchum, I., and E. G. Pamer. 2011. Regulation of innate and adaptive immunity by the commensal microbiota. Curr. Opin. Immunol. 213: 353-360.
74. Wardwell, L. H., C. Huttenhower, and W. S. Garrett. 2011. Current concepts of the intestinal microbiota and the pathogenesis of infection. Curr. Infect. Dis. Rep. 13: 28-34.
75. Benson, A., R. Pifer, C. L. Behrendt, L. V. Hooper, and F. Yarovinsky. 2009. Gut commensal bacteria direct a protective immune response against Toxoplasma gondii. Cell Host Microbe 6: 187-196.
76. Hayes, K. S., A. J. Bancroft, M. Goldrick, C. Portsmouth, I. S. Roberts, and R. K. Grencis. 2010. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science 328: 1391-1394.
77. Ivanov, I. I., Rde. L. Frutos, N. Manel, K. Yoshinaga, D. B. Rifkin, R. B. Sartor, B. B. Finlay, and D. R. Littman. 2008. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4: 337-349.
78. Ivanov, I. I., K. Atarashi, N. Manel, E. L. Brodie, T. Shima, U. Karaoz, D. Wei, K. C. Goldfarb, C. A. Santee, S. V. Lynch, et al. 2009. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139: 485-498.
79. Ochoa-Repáraz, J., D. W. Mielcarz, L. E. Ditrio, A. R. Burroughs, D. M. Foureau, S. Haque-Begum, and L. H. Kasper. 2009. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J. Immunol. 183: 6041-6050.
80. Huse, M., B. F. Lillemeier, M. S. Kuhns, D. S. Chen, and M. M. Davis. 2006. T cells use two directionally distinct pathways for cytokine secretion. Nat. Immunol. 7: 247-255.
81. Perona-Wright, G., K. Mohrs, and M. Mohrs. 2010. Sustained signaling by canonical helper T cell cytokines throughout the reactive lymph node. Nat. Immunol. 11: 520-526.
82. Zhou, L., I. I. Ivanov, R. Spolski, R. Min, K. Shenderov, T. Egawa, D. E. Levy, W. J. Leonard, and D. R. Littman. 2007. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat. Immunol. 8: 967-974. (Pubitemid 47300011)
83. La Flamme, A. C., A. S. MacDonald, and E. J. Pearce. 2000. Role of IL-6 in directing the initial immune response to schistosome eggs. J. Immunol. 164: 2419-2426. (Pubitemid 30115470)
84. Kurreeman, F. A., J. J. Schonkeren, B. T. Heijmans, R. E. Toes, and T. W. Huizinga. 2004. Transcription of the IL10 gene reveals allele-specific regulation at the mRNA level. Hum. Mol. Genet. 13: 1755-1762. (Pubitemid 39173444)
85. Shainheit, M. G., K. W. Lasocki, E. Finger, B. M. Larkin, P. M. Smith, A. H. Sharpe, C. A. Dinarello, L. I. Rutitzky, and M. J. Stadecker. 2011. The pathogenic Th17 cell response to major schistosome egg antigen is sequentially dependent on IL-23 and IL-1b. J. Immunol. 187: 5328-5335.
86. 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. (Pubitemid 350166058)