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. 1995 Feb;84(2):233–240.

Role of epidermal Langerhans' cells in the induction of protective immunity to Schistosoma mansoni in guinea-pigs.

H Sato 1, H Kamiya 1
PMCID: PMC1415112  PMID: 7750999

Abstract

Percutaneous exposure of guinea-pigs to attenuated or normal larvae of Schistosoma mansoni induced proliferative T-cell responses in the skin-draining lymph nodes (SLN). The responses elicited by attenuated larvae were stronger and more prolonged [2-12 days post-infection (p.i.)] than those by normal larvae (3-8 days p.i.). The former were coincident with greater and more sustained increases in numbers of SLN dendritic cells. During this event, epidermal Langerhans' cells (LC) showed marked changes in their distribution and morphology. Resident LC were similarly exhausted by either attenuated or normal larvae between 12 hr and 1 day p.i., but thereafter more blood-borne LC were recruited around the former, since reaggregation of LC around these persisted larvae was more frequent and intensive, and enhanced replenishment of epidermal LC was achieved by 8 days p.i. When the skin depleted of epidermal LC by short-wavelength ultraviolet (UVC) irradiation was exposed to attenuated larvae, consequent T-cell responses were delayed. Excision of the whole exposed skin on day 4 p.i. also reduced T-cell responses to marginal levels. These results indicate that during the afferent phase of immunity to S. mansoni, efficient T-cell responses in the SLN need an active involvement of not only resident LC but also blood-borne LC as immunostimulatory cells.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bieber T. Fc epsilon RI on human Langerhans cells: a receptor in search of new functions. Immunol Today. 1994 Feb;15(2):52–53. doi: 10.1016/0167-5699(94)90132-5. [DOI] [PubMed] [Google Scholar]
  2. Coulson P. S., Mountford A. P. Fate of attenuated schistosomula administered to mice by different routes, relative to the immunity induced against Schistosoma mansoni. Parasitology. 1989 Aug;99(Pt 1):39–45. doi: 10.1017/s003118200006100x. [DOI] [PubMed] [Google Scholar]
  3. Dean D. A. Schistosoma and related genera: acquired resistance in mice. Exp Parasitol. 1983 Feb;55(1):1–104. doi: 10.1016/0014-4894(83)90002-4. [DOI] [PubMed] [Google Scholar]
  4. Gschnait F., Brenner W. Kinetics of epidermal Langerhans cells. J Invest Dermatol. 1979 Dec;73(6):566–569. doi: 10.1111/1523-1747.ep12541607. [DOI] [PubMed] [Google Scholar]
  5. Inaba K., Steinman R. M. Accessory cell-T lymphocyte interactions. Antigen-dependent and -independent clustering. J Exp Med. 1986 Feb 1;163(2):247–261. doi: 10.1084/jem.163.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Inaba K., Steinman R. M. Resting and sensitized T lymphocytes exhibit distinct stimulatory (antigen-presenting cell) requirements for growth and lymphokine release. J Exp Med. 1984 Dec 1;160(6):1717–1735. doi: 10.1084/jem.160.6.1717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kamiya H., Ozaki T., Nakayama H., Inaba T. Immunizing potential of ultraviolet-attenuated cercariae of Schistosoma mansoni in rodent hosts. Parasitol Res. 1993;79(4):293–296. doi: 10.1007/BF00932184. [DOI] [PubMed] [Google Scholar]
  8. Kaplan G., Nusrat A., Witmer M. D., Nath I., Cohn Z. A. Distribution and turnover of Langerhans cells during delayed immune responses in human skin. J Exp Med. 1987 Mar 1;165(3):763–776. doi: 10.1084/jem.165.3.763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kelly E. A., Colley D. G. In vivo effects of monoclonal anti-L3T4 antibody on immune responsiveness of mice infected with Schistosoma mansoni. Reduction of irradiated cercariae-induced resistance. J Immunol. 1988 Apr 15;140(8):2737–2745. [PubMed] [Google Scholar]
  10. Kupiec-Weglinski J. W., Austyn J. M., Morris P. J. Migration patterns of dendritic cells in the mouse. Traffic from the blood, and T cell-dependent and -independent entry to lymphoid tissues. J Exp Med. 1988 Feb 1;167(2):632–645. doi: 10.1084/jem.167.2.632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lessard R. J., Wolff K., Winkelmann R. K. The disappearance and regeneration of Langerhans cells following epidermal injury. J Invest Dermatol. 1968 Feb;50(2):171–179. doi: 10.1038/jid.1968.20. [DOI] [PubMed] [Google Scholar]
  12. Macatonia S. E., Edwards A. J., Knight S. C. Dendritic cells and the initiation of contact sensitivity to fluorescein isothiocyanate. Immunology. 1986 Dec;59(4):509–514. [PMC free article] [PubMed] [Google Scholar]
  13. Macatonia S. E., Knight S. C., Edwards A. J., Griffiths S., Fryer P. Localization of antigen on lymph node dendritic cells after exposure to the contact sensitizer fluorescein isothiocyanate. Functional and morphological studies. J Exp Med. 1987 Dec 1;166(6):1654–1667. doi: 10.1084/jem.166.6.1654. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Metlay J. P., Puré E., Steinman R. M. Control of the immune response at the level of antigen-presenting cells: a comparison of the function of dendritic cells and B lymphocytes. Adv Immunol. 1989;47:45–116. doi: 10.1016/s0065-2776(08)60662-8. [DOI] [PubMed] [Google Scholar]
  15. Moll H. Epidermal Langerhans cells are critical for immunoregulation of cutaneous leishmaniasis. Immunol Today. 1993 Aug;14(8):383–387. doi: 10.1016/0167-5699(93)90138-B. [DOI] [PubMed] [Google Scholar]
  16. Mountford A. P., Coulson P. S., Pemberton R. M., Smythies L. E., Wilson R. A. The generation of interferon-gamma-producing T lymphocytes in skin-draining lymph nodes, and their recruitment to the lungs, is associated with protective immunity to Schistosoma mansoni. Immunology. 1992 Feb;75(2):250–256. [PMC free article] [PubMed] [Google Scholar]
  17. Mountford A. P., Coulson P. S., Saunders N., Wilson R. A. Characteristics of protective immunity in mice induced by drug-attenuated larvae of Schistosoma mansoni. Antigen localization and antibody responses. J Immunol. 1989 Aug 1;143(3):989–995. [PubMed] [Google Scholar]
  18. Mountford A. P., Coulson P. S., Wilson R. A. Antigen localization and the induction of resistance in mice vaccinated with irradiated cercariae of Schistosoma mansoni. Parasitology. 1988 Aug;97(Pt 1):11–25. doi: 10.1017/s0031182000066701. [DOI] [PubMed] [Google Scholar]
  19. Mountford A. P., Wilson R. A. Schistosoma mansoni: the effect of regional lymphadenectomy on the level of protection induced in mice by radiation-attenuated cercariae. Exp Parasitol. 1990 Nov;71(4):463–469. doi: 10.1016/0014-4894(90)90072-k. [DOI] [PubMed] [Google Scholar]
  20. Pearce E. J., McLaren D. J. Schistosoma mansoni: in vivo and in vitro studies of immunity using the guinea-pig model. Parasitology. 1983 Dec;87(Pt 3):465–479. doi: 10.1017/s0031182000082998. [DOI] [PubMed] [Google Scholar]
  21. Pemberton R. M., Smythies L. E., Mountford A. P., Wilson R. A. Patterns of cytokine production and proliferation by T lymphocytes differ in mice vaccinated or infected with Schistosoma mansoni. Immunology. 1991 Jul;73(3):327–333. [PMC free article] [PubMed] [Google Scholar]
  22. Puré E., Inaba K., Crowley M. T., Tardelli L., Witmer-Pack M. D., Ruberti G., Fathman G., Steinman R. M. Antigen processing by epidermal Langerhans cells correlates with the level of biosynthesis of major histocompatibility complex class II molecules and expression of invariant chain. J Exp Med. 1990 Nov 1;172(5):1459–1469. doi: 10.1084/jem.172.5.1459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Romani N., Koide S., Crowley M., Witmer-Pack M., Livingstone A. M., Fathman C. G., Inaba K., Steinman R. M. Presentation of exogenous protein antigens by dendritic cells to T cell clones. Intact protein is presented best by immature, epidermal Langerhans cells. J Exp Med. 1989 Mar 1;169(3):1169–1178. doi: 10.1084/jem.169.3.1169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ron Y., Sprent J. T cell priming in vivo: a major role for B cells in presenting antigen to T cells in lymph nodes. J Immunol. 1987 May 1;138(9):2848–2856. [PubMed] [Google Scholar]
  25. Rowden G., Boudreau S., Higley H. Langerhans cells and extra-epidermal dendritic cells. An investigation in laboratory animals and man with immunomorphological methods. Scand J Immunol. 1985 May;21(5):471–478. doi: 10.1111/j.1365-3083.1985.tb01834.x. [DOI] [PubMed] [Google Scholar]
  26. Schuler G., Steinman R. M. Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J Exp Med. 1985 Mar 1;161(3):526–546. doi: 10.1084/jem.161.3.526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Scott P., Pearce E., Cheever A. W., Coffman R. L., Sher A. Role of cytokines and CD4+ T-cell subsets in the regulation of parasite immunity and disease. Immunol Rev. 1989 Dec;112:161–182. doi: 10.1111/j.1600-065x.1989.tb00557.x. [DOI] [PubMed] [Google Scholar]
  28. Silberberg-Sinakin I., Gigli I., Baer R. L., Thorbecke G. J. Langerhans cells: role in contact hypersensitivity and relationship to lymphoid dendritic cells and to macrophages. Immunol Rev. 1980;53:203–232. doi: 10.1111/j.1600-065x.1980.tb01045.x. [DOI] [PubMed] [Google Scholar]
  29. Steinman R. M. The dendritic cell system and its role in immunogenicity. Annu Rev Immunol. 1991;9:271–296. doi: 10.1146/annurev.iy.09.040191.001415. [DOI] [PubMed] [Google Scholar]
  30. Streilein J. W., Grammer S. F. In vitro evidence that Langerhans cells can adopt two functionally distinct forms capable of antigen presentation to T lymphocytes. J Immunol. 1989 Dec 15;143(12):3925–3933. [PubMed] [Google Scholar]
  31. Streilein J. W., Grammer S. F., Yoshikawa T., Demidem A., Vermeer M. Functional dichotomy between Langerhans cells that present antigen to naive and to memory/effector T lymphocytes. Immunol Rev. 1990 Oct;117:159–183. doi: 10.1111/j.1600-065x.1990.tb00572.x. [DOI] [PubMed] [Google Scholar]
  32. Streilein J. W., Lonsberry L. W., Bergstresser P. R. Depletion of epidermal langerhans cells and Ia immunogenicity from tape-stripped mouse skin. J Exp Med. 1982 Mar 1;155(3):863–871. doi: 10.1084/jem.155.3.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vignali D. A., Crocker P., Bickle Q. D., Cobbold S., Waldmann H., Taylor M. G. A role for CD4+ but not CD8+ T cells in immunity to Schistosoma mansoni induced by 20 krad-irradiated and Ro 11-3128-terminated infections. Immunology. 1989 Aug;67(4):466–472. [PMC free article] [PubMed] [Google Scholar]
  34. Wales A., Kusel J. R., Jones J. T. Inhibition of protein synthesis in irradiated larvae of Schistosoma mansoni. Parasite Immunol. 1992 Sep;14(5):513–530. doi: 10.1111/j.1365-3024.1992.tb00025.x. [DOI] [PubMed] [Google Scholar]
  35. Wheater P. R., Wilson R. A. Schistosoma mansoni: a histological study of migration in the laboratory mouse. Parasitology. 1979 Aug;79(1):49–62. doi: 10.1017/s0031182000051970. [DOI] [PubMed] [Google Scholar]

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