Parasitology Research

, Volume 97, Issue 3, pp 186–190

Dendritic cell expansion occurs in mesenteric lymph nodes of B10.BR mice infected with the murine nematode parasite Trichuris muris

Original Paper

Abstract

Dendritic cells (DCs) are a crucial element in the immune system and bridge innate and adaptive immunity. CD11c+ B220 DCs residing in Peyer’s patches (PPs) have the ability to produce interleukin 10 (IL-10) and induce T helper (Th2) development. Evidence suggests that CD11c+ B220 DCs maintain the gut environment by suppressing Th1 responses with IL-10, resulting in a Th2-dominat gut environment. Th2 effectors are required for protection against the murine nematode parasite Trichuris muris, and thus CD11c+ B220 DCs may be involved in the induction of Th2 cells in T. muris infection. In the present study, the kinetics of CD11c+ B220 DCs were analyzed in mesenteric lymph nodes of B10.BR mice infected with the E-J isolate of T. muris, and the cellular expansion of CD11c+ B220 DCs was also observed. As well, the DC expansion was consistent with the occurrence of worm expulsion augmented by IL-4 and IL-13. The evidence here suggests the involvement of CD11c+ B220 DCs in protective Th2 responses to T. muris infection.

References

  1. Ardavín C (2003) Origin, precursor and differentiation of mouse dendritic cells. Nat Rev Immunol 3:1–9Google Scholar
  2. Balic A, Harcus Y, Holland MJ, Maizels RM (2004) Selective maturation of dendritic cells by Nippostrongylus brasiliensis-secreted proteins drives Th2 immune responses. Eur J Immunol 34:3047–3059CrossRefPubMedGoogle Scholar
  3. Bancroft AJ, Else KJ, Sypek JP, Grencis RK (1997) Interleukin-12 promotes a chronic intestinal nematode infection. Eur J Immunol 27:866–870Google Scholar
  4. Bancroft AJ, McKenzie ANJ, Grencis RK (1998) A critical role for IL-13 in resistance to intestinal nematode infection. J Immunol 160:3453–3461PubMedGoogle Scholar
  5. Bellaby T, Robinson K, Wakelin D, Behnke JM (1995) Isolates of Trichuris muris vary in their ability to elicit protective immune responses to infection in mice. Parasitology 111:353–357PubMedGoogle Scholar
  6. Chambers SJ, Bertelli E, Winterbone MS, Regoli M, Man AL, Nicoletti C (2004) Adoptive transfer of dendritic cells from allergic mice induces specific immunoglobulin E antibody in naïve recipients in absence of antigen challenge without altering the T helper 1/T helper 2 balance. Immunology 112:72–79CrossRefPubMedGoogle Scholar
  7. Colonna M, Trichieri G, Liu YJ (2004) Plasmacytoid dendritic cells in immunity. Nat Immunol 5:1219–1226CrossRefPubMedGoogle Scholar
  8. Else KJ, Finkelman FD, Maliszewski CR, Grencis RK (1994) Cytokine-mediated regulation of chronic intestinal helminth infection. J Exp Med 179:347–351CrossRefPubMedGoogle Scholar
  9. Filippe C, Hugues S, Cazareth J, Cazareth J, Julia V, Glaichenhaus N, Ugolini S (2003) CD4+ T cell polarization in mice is modulated by strain-specific major histocompatibility complex-independent differences within dendritic cells. J Exp Med 198:201–209CrossRefPubMedGoogle Scholar
  10. Frucht DM, Fukao T, Bogadan C, Schindler H, O’Shea JJ, Koyasu S (2001) IFN-γ production by antigen-presenting cells: mechanisms emerge. Trends Immunol 22:556–560CrossRefPubMedGoogle Scholar
  11. Gause WC, Urban JF Jr, Stadecker MJ (2003) The immune response to parasitic helminthes: insights from murine models. Trends Immunol 24:269–277Google Scholar
  12. Goodridge HS, Marshall FA, Wilson EH, Houston KM, Liew FY, Harnett MM, Harnett W (2004) In vivo exposure of murine dendritic cell and macrophage bone marrow progenitors to the phosphorylcholine-containing filarial nematode glycoprotein ES-62 polarizes their differentiation to an anti-inflammatory phenotype. Immunology 113:491–498CrossRefPubMedGoogle Scholar
  13. Helmby H, Takeda K, Akira S, Grencis RK (2001) Interleukin (IL)-18 promotes the development of chronic gastorointestinal helminth infection by downregulating IL-13. J Exp Med 194:355–364Google Scholar
  14. Hoebe K, Janssen E, Beutler B (2004) The interface between innate and adaptive immunity. Nat Immnonol 5:971–974CrossRefGoogle Scholar
  15. Ito Y (1991) The absence of resistance in congenitally athymic nude mice toward infection with the intestinal nematode, Trichuris muris: resistance restored by lymphoid cell transfer. Int J Parasitol 21:65–69CrossRefPubMedGoogle Scholar
  16. Iwasaki A (2003) The role of dendritic cells in immune responses against vaginal infection by herpes simplex virus type 2. Microbes Infect 5:1221–1230CrossRefPubMedGoogle Scholar
  17. Iwasaki A, Kelsall BL (1999) Freshly isolated Peyer’s patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells. J Exp Med 190:229–239CrossRefPubMedGoogle Scholar
  18. Iwasaki A, Medzhitov R (2004) Toll-like receptor control of the adaptive immune responses. Nat Immunol 5:987–995CrossRefPubMedGoogle Scholar
  19. Kapsenber M (2003) Dendritic-cell control of pahogen-driven T-cell polarization. Nat Rev Immunol 3:984–993Google Scholar
  20. Kelsall BL, Rescigno M (2004) Mucosal dendritic cells in immunity and inflammation. Nat Immunol 5:1091–1095CrossRefPubMedGoogle Scholar
  21. van Kooyk Y, Geijtenbeek TBH. (2003) DC-ISAN: escape mechanism for pathogens. Nat Rev Immunol 3:697–709Google Scholar
  22. Koyama K, Ito Y (1996) Comparative studies on immune responses to infection in susceptible B10.BR mice infected with different strains of the murine nematode parasite Trichuris muris. Parasite Immunol 18:257–263CrossRefPubMedGoogle Scholar
  23. Koyama K, Tamauchi H, Tomita M, Kitajima T, Ito Y (1999) B-cell activation in the mesenteric lymph nodes of resistant BALB/c mice infected with the murine nematode parasite Trichuris muris. Parasitol Res 85:194–199CrossRefPubMedGoogle Scholar
  24. MacDonald AS, Straw AD, Bauman B, Pearce E (2001) CD8 dendritic cell activation status plays an integral role in influencing Th2 response development. J Immunol 167:1982–1988PubMedGoogle Scholar
  25. Mellman I, Steinman RM (2001) Dendritic cells: specialized and regulated antigen processing machines. Cell 106:255–258CrossRefPubMedGoogle Scholar
  26. Morgner COM, Mota MM, Rodriguez A (2003) Malaria Blood stage suppression of liver stage immunity by dendritic cells. J Exp Med 197:143–151CrossRefPubMedGoogle Scholar
  27. O’Garra A, Trinchieri G (2004) Are dendritic cells afraid of commitment? Nat Immunol 5:1206–1208CrossRefPubMedGoogle Scholar
  28. Sharpe AH, Freeman GJ (2002) The B7-CD28 superfamily. Nat Rev Immunol 2:116–126PubMedGoogle Scholar
  29. Shortman K, Liu YJ (2002) Mouse and dendritic cell subtypes. Nat Rev Immunol 2:151–161Google Scholar
  30. Stagg AJ, Hart AL, Knight SC, Kamm MA (2003) The dendritic cell: its role in intestinal inflammation and relation ship with gut bacteria. Gut 52:1522–1529CrossRefPubMedGoogle Scholar
  31. von Stebut E, Ehrchen JM, Belkaid Y, Kostka SL, Mölle K, Knop J, Sunderkötter C, Udey MC (2003) Interleuikin 1α promotes Th1 differentiation and inhibits disease progression in Leishmania major-susceptible BALB/c mice. J Exp Med 198:191–199CrossRefPubMedGoogle Scholar
  32. Thomas PG, Carter MR, Atochina O, Da’Dara AA, Piskorska D, McGuire E, Harn DA (2003) Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J Immunol 171:5837–5841PubMedGoogle Scholar
  33. Urban J, Fang H, Liu Q, Ekkens MJ, Chen S-J, Nguyen D, Mitro V, Donaldson DD, Byrd C, Peach R, Morris SC, Finkelman FD, Schopf L, Gause WC (2000) IL-13-mediated worm expulsion is B7 independent and IFN-γsensitive. J Immunol 164:4250–4256PubMedGoogle Scholar
  34. Whelan M, Harnett MM, Houston KM, Patel V, Harnett W, Rigley KP (2000) A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J Immunol 164:6453–6460PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of ParasitologyKitasato University School of MedicineSagamiharaJapan

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