Skip to main content
NCBI home page
Immunology logoLink to Immunology
. 1997 May;91(1):35–44. doi: 10.1046/j.1365-2567.1997.00229.x

Interleukin-7 in the skin of Schistosoma mansoni-infected mice is associated with a decrease in interferon-gamma production and leads to an aggravation of the disease.

I Wolowczuk 1, M Delacre 1, O Roye 1, S L Giannini 1, C Auriault 1
PMCID: PMC1364032  PMID: 9203963

Abstract

The effect of recombinant interleukin-7 (rIL-7) on the course of murine schistosomiasis and the development of the accompanying immune response were investigated. We demonstrated that IL-7 expression could be detected in the skin of infected mice from 1 to 21 days following infection. We here report that intradermal injection of exogenous human IL-7, prior to the penetration of the parasite into the skin, leads to a more severe liver pathology and an increased number of surviving adult parasites. In addition, injection of rIL-7 alters parasite migration (estimation of burdens of young larvae in lungs and liver). Administration of rIL-7 led to a decrease of IL-12 and interferon-gamma-(IFN-gamma) specific messengers RNA in skin and, more markedly, in skin-draining lymph nodes. The number of B220 expressing cells was increased, and T-cell number was reduced, in IL-7-treated infected mice. In addition, levels of IFN-gamma and IL-4 in sera were significantly reduced, whereas there was a shift from a Th1 to a Th2 type associated humoral response towards the egg antigens. Our experimental observation illustrate that the exogenous administration of rIL-7 affects both the development of the host's immune response and the behaviour of the parasite within the infected host. The early and specific production of IL-7 in the host skin, following infection with Schistosoma mansoni, raises fascinating questions concerning the relationships between the parasite and its host at the very beginning of their interaction.

Full text

PDF
35

Images in this article

38Figure 1
on p.38
38Figure 2
on p.38

Selected References

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

  1. Afonso L. C., Scharton T. M., Vieira L. Q., Wysocka M., Trinchieri G., Scott P. The adjuvant effect of interleukin-12 in a vaccine against Leishmania major. Science. 1994 Jan 14;263(5144):235–237. doi: 10.1126/science.7904381. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Cumberbatch M., Kimber I. Dermal tumour necrosis factor-alpha induces dendritic cell migration to draining lymph nodes, and possibly provides one stimulus for Langerhans' cell migration. Immunology. 1992 Feb;75(2):257–263. [PMC free article] [PubMed] [Google Scholar]
  4. Enk A. H., Katz S. I. Early molecular events in the induction phase of contact sensitivity. Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1398–1402. doi: 10.1073/pnas.89.4.1398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Gajewski T. F., Pinnas M., Wong T., Fitch F. W. Murine Th1 and Th2 clones proliferate optimally in response to distinct antigen-presenting cell populations. J Immunol. 1991 Mar 15;146(6):1750–1758. [PubMed] [Google Scholar]
  6. Georgi J. R. Schistosoma mansoni: quantification of skin penetration and early migration by differential external radioassay and autoradiography. Parasitology. 1982 Apr;84(Pt 2):263–281. doi: 10.1017/s0031182000044826. [DOI] [PubMed] [Google Scholar]
  7. Gessner A., Vieth M., Will A., Schröppel K., Röllinghoff M. Interleukin-7 enhances antimicrobial activity against Leishmania major in murine macrophages. Infect Immun. 1993 Sep;61(9):4008–4012. doi: 10.1128/iai.61.9.4008-4012.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gessner A., Will A., Vieth M., Schröppel K., Röllinghoff M. Stimulation of B-cell lymphopoiesis by interleukin-7 leads to aggravation of murine leishmaniasis. Immunology. 1995 Mar;84(3):416–422. [PMC free article] [PubMed] [Google Scholar]
  9. Goodwin R. G., Lupton S., Schmierer A., Hjerrild K. J., Jerzy R., Clevenger W., Gillis S., Cosman D., Namen A. E. Human interleukin 7: molecular cloning and growth factor activity on human and murine B-lineage cells. Proc Natl Acad Sci U S A. 1989 Jan;86(1):302–306. doi: 10.1073/pnas.86.1.302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Grabstein K. H., Waldschmidt T. J., Finkelman F. D., Hess B. W., Alpert A. R., Boiani N. E., Namen A. E., Morrissey P. J. Inhibition of murine B and T lymphopoiesis in vivo by an anti-interleukin 7 monoclonal antibody. J Exp Med. 1993 Jul 1;178(1):257–264. doi: 10.1084/jem.178.1.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hauser C., Saurat J. H., Schmitt A., Jaunin F., Dayer J. M. Interleukin 1 is present in normal human epidermis. J Immunol. 1986 May 1;136(9):3317–3323. [PubMed] [Google Scholar]
  12. Heufler C., Topar G., Grasseger A., Stanzl U., Koch F., Romani N., Namen A. E., Schuler G. Interleukin 7 is produced by murine and human keratinocytes. J Exp Med. 1993 Sep 1;178(3):1109–1114. doi: 10.1084/jem.178.3.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hoerauf A., Solbach W., Röllinghoff M., Gessner A. Effect of IL-7 treatment on Leishmania major-infected BALB.Xid mice: enhanced lymphopoiesis with sustained lack of B1 cells and clinical aggravation of disease. Int Immunol. 1995 Nov;7(11):1879–1884. [PubMed] [Google Scholar]
  14. Jicha D. L., Mulé J. J., Rosenberg S. A. Interleukin 7 generates antitumor cytotoxic T lymphocytes against murine sarcomas with efficacy in cellular adoptive immunotherapy. J Exp Med. 1991 Dec 1;174(6):1511–1515. doi: 10.1084/jem.174.6.1511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Kasper L. H., Matsuura T., Khan I. A. IL-7 stimulates protective immunity in mice against the intracellular pathogen, Toxoplasma gondii. J Immunol. 1995 Nov 15;155(10):4798–4804. [PubMed] [Google Scholar]
  17. Kirnbauer R., Köck A., Schwarz T., Urbanski A., Krutmann J., Borth W., Damm D., Shipley G., Ansel J. C., Luger T. A. IFN-beta 2, B cell differentiation factor 2, or hybridoma growth factor (IL-6) is expressed and released by human epidermal cells and epidermoid carcinoma cell lines. J Immunol. 1989 Mar 15;142(6):1922–1928. [PubMed] [Google Scholar]
  18. Kullberg M. C., Pearce E. J., Hieny S. E., Sher A., Berzofsky J. A. Infection with Schistosoma mansoni alters Th1/Th2 cytokine responses to a non-parasite antigen. J Immunol. 1992 May 15;148(10):3264–3270. [PubMed] [Google Scholar]
  19. López-De León A., Rojkind M. A simple micromethod for collagen and total protein determination in formalin-fixed paraffin-embedded sections. J Histochem Cytochem. 1985 Aug;33(8):737–743. doi: 10.1177/33.8.2410480. [DOI] [PubMed] [Google Scholar]
  20. Matsue H., Bergstresser P. R., Takashima A. Keratinocyte-derived IL-7 serves as a growth factor for dendritic epidermal T cells in mice. J Immunol. 1993 Dec 1;151(11):6012–6019. [PubMed] [Google Scholar]
  21. 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]
  22. Morikawa Y., Tohya K., Ishida H., Matsuura N., Kakudo K. Different migration patterns of antigen-presenting cells correlate with Th1/Th2-type responses in mice. Immunology. 1995 Aug;85(4):575–581. [PMC free article] [PubMed] [Google Scholar]
  23. Morrissey P. J., Goodwin R. G., Nordan R. P., Anderson D., Grabstein K. H., Cosman D., Sims J., Lupton S., Acres B., Reed S. G. Recombinant interleukin 7, pre-B cell growth factor, has costimulatory activity on purified mature T cells. J Exp Med. 1989 Mar 1;169(3):707–716. doi: 10.1084/jem.169.3.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Murray R., Suda T., Wrighton N., Lee F., Zlotnik A. IL-7 is a growth and maintenance factor for mature and immature thymocyte subsets. Int Immunol. 1989;1(5):526–531. doi: 10.1093/intimm/1.5.526. [DOI] [PubMed] [Google Scholar]
  26. Namen A. E., Lupton S., Hjerrild K., Wignall J., Mochizuki D. Y., Schmierer A., Mosley B., March C. J., Urdal D., Gillis S. Stimulation of B-cell progenitors by cloned murine interleukin-7. Nature. 1988 Jun 9;333(6173):571–573. doi: 10.1038/333571a0. [DOI] [PubMed] [Google Scholar]
  27. Noble A., Kemeny D. M. Interleukin-4 enhances interferon-gamma synthesis but inhibits development of interferon-gamma-producing cells. Immunology. 1995 Jul;85(3):357–363. [PMC free article] [PubMed] [Google Scholar]
  28. Pearce E. J., Caspar P., Grzych J. M., Lewis F. A., Sher A. Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med. 1991 Jan 1;173(1):159–166. doi: 10.1084/jem.173.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pearce E. J., Caspar P., Grzych J. M., Lewis F. A., Sher A. Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med. 1991 Jan 1;173(1):159–166. doi: 10.1084/jem.173.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sato H., Kamiya H. Role of epidermal Langerhans' cells in the induction of protective immunity to Schistosoma mansoni in guinea-pigs. Immunology. 1995 Feb;84(2):233–240. [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Smithers S. R., Terry R. J. Immunity in schistosomiasis. Ann N Y Acad Sci. 1969 Oct 6;160(2):826–840. doi: 10.1111/j.1749-6632.1969.tb15904.x. [DOI] [PubMed] [Google Scholar]
  33. Smythies L. E., Coulson P. S., Wilson R. A. Monoclonal antibody to IFN-gamma modifies pulmonary inflammatory responses and abrogates immunity to Schistosoma mansoni in mice vaccinated with attenuated cercariae. J Immunol. 1992 Dec 1;149(11):3654–3658. [PubMed] [Google Scholar]
  34. Smythies L. E., Pemberton R. M., Coulson P. S., Mountford A. P., Wilson R. A. T cell-derived cytokines associated with pulmonary immune mechanisms in mice vaccinated with irradiated cercariae of Schistosoma mansoni. J Immunol. 1992 Mar 1;148(5):1512–1518. [PubMed] [Google Scholar]
  35. Standiford T. J., Strieter R. M., Allen R. M., Burdick M. D., Kunkel S. L. IL-7 up-regulates the expression of IL-8 from resting and stimulated human blood monocytes. J Immunol. 1992 Sep 15;149(6):2035–2039. [PubMed] [Google Scholar]
  36. Stirewalt M. A. Schistosoma mansoni: cercaria to schistosomule. Adv Parasitol. 1974;12:115–182. doi: 10.1016/s0065-308x(08)60388-7. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Wiles M. V., Ruiz P., Imhof B. A. Interleukin-7 expression during mouse thymus development. Eur J Immunol. 1992 Apr;22(4):1037–1042. doi: 10.1002/eji.1830220424. [DOI] [PubMed] [Google Scholar]
  39. Wilson R. A., Coulson P. S., Dixon B. Migration of the schistosomula of Schistosoma mansoni in mice vaccinated with radiation-attenuated cercariae, and normal mice: an attempt to identify the timing and site of parasite death. Parasitology. 1986 Feb;92(Pt 1):101–116. doi: 10.1017/s0031182000063484. [DOI] [PubMed] [Google Scholar]
  40. von Freeden-Jeffry U., Vieira P., Lucian L. A., McNeil T., Burdach S. E., Murray R. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J Exp Med. 1995 Apr 1;181(4):1519–1526. doi: 10.1084/jem.181.4.1519. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Immunology are provided here courtesy of British Society for Immunology

RESOURCES