Skip to main content
PMC home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1979 Dec 1;150(6):1456–1471. doi: 10.1084/jem.150.6.1456

Interactions between human eosinophils and schistosomula of schistosoma mansoni. II. The mechanism of irreversible eosinophil adherence

AE Butterworth, MA Vadas, DL Wassom, A Dessein, M Hogan, B Sherry, GJ Gleich, David JR
PMCID: PMC2185735  PMID: 390086

Abstract

Previous work (1)(1) has shown that normal human eosinophils show a preferential capacity, in comparison with neutrophils, to bind to antibody- coated schistosomula of Schistosoma mansoni. This effect is attributable to a temperature-dependent function of the eosinophil which renders its binding stable and irreversible by aggregated gamma globulin or Staphylococcus aureus protein A. In contrast, the binding of neutrophils is readily reversible by these agents. It has now been shown that the differences observed between eosinophils and neutrophils is a property of their interaction with living schistosomula. When dead or artificially damaged schistosomula were tested, neutrophils showed a markedly enhanced capacity to adhere, in both the presence and absence of anti-chistosomular serum. Subsequent experiments were designed to test the hypothesis that the strong, stable binding of eosinophils was attributable to degranulation, with release of granule contents which would then serve as ligands to bind the cell to the organism. First, an enhanced adherence both of eosinophils and of neutrophils could be demonstrated in the presence of eosinophil major basic protein (MBP) or of protamine, a high molecular weight cation. Second, the binding of eosinophils induced by concanavalin A (Con A) was found to differ markedly from that induced by antischistosomular serum. Con A-mediated binding of eosinophils was fully reversible by alpha-methyl-mannoside, was not associated with damage to the organism, and did not lead to degranulation of the cell, as estimated by measuring the release of MBP into the culture supernate. However, induction of degranulation of concanavalin A-bound eosinophils, but not of neutrophils, with the calcium ionophore A23187 converted the reaction into one which was no longer reversible by alpha- methylmannoside and in which damage to the organism now did occur. These findings support the hypothesis that the stable binding of eosinophils is associated with degranulation, a process which may contribute to the preferential capacity of this cell to mediate antibody-dependent damage to schistosomula.

Full Text

The Full Text of this article is available as a PDF (970.3 KB).

Selected References

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

  1. Anwar A. R., Kay A. B. Membrane receptors for IgG and complement (C4, C3b and C3d) on human eosinophils and neutrophils and their relation to eosinophilia. J Immunol. 1977 Sep;119(3):976–982. [PubMed] [Google Scholar]
  2. Anwar A. R., Smithers S. R., Kay A. B. Killing of schistosomula of Schistosoma mansoni coated with antibody and/or complement by human leukocytes in vitro: requirement for complement in preferential killing by eosinophils. J Immunol. 1979 Feb;122(2):628–637. [PubMed] [Google Scholar]
  3. Brink L. H., McLaren D. J., Smithers S. R. Schistosoma mansoni: a comparative study of artificially transformed schistosomula and schistosomula recovered after cercarial penetration of isolated skin. Parasitology. 1977 Feb;74(1):73–86. doi: 10.1017/s0031182000047545. [DOI] [PubMed] [Google Scholar]
  4. Butterworth A. E., Wassom D. L., Gleich G. J., Loegering D. A., David J. R. Damage to schistosomula of Schistosoma mansoni induced directly by eosinophil major basic protein. J Immunol. 1979 Jan;122(1):221–229. [PubMed] [Google Scholar]
  5. Clegg J. A., Smithers S. R. The effects of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. Int J Parasitol. 1972 Mar;2(1):79–98. doi: 10.1016/0020-7519(72)90036-7. [DOI] [PubMed] [Google Scholar]
  6. Foreman J. C., Hallett M. B., Mongar J. L. The relationship between histamine secretion and 45calcium uptake by mast cells. J Physiol. 1977 Sep;271(1):193–214. doi: 10.1113/jphysiol.1977.sp011996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Glauert A. M., Butterworth A. E. Morphological evidence for the ability of eosinophils to damage antibody-coated schistosomula. Trans R Soc Trop Med Hyg. 1977;71(5):392–395. doi: 10.1016/0035-9203(77)90036-0. [DOI] [PubMed] [Google Scholar]
  8. Glauert A. M., Butterworth A. E., Sturrock R. F., Houba V. The mechansim of antibody-dependent, eosinophil-mediated damage to schistosomula of Schistosoma mansoni in vitro: a study by phase-contrast and electron microscopy. J Cell Sci. 1978 Dec;34:173–192. doi: 10.1242/jcs.34.1.173. [DOI] [PubMed] [Google Scholar]
  9. Gleich G. J., Loegering D. A., Kueppers F., Bajaj S. P., Mann K. G. Physiochemical and biological properties of the major basic protein from guinea pig eosinophil granules. J Exp Med. 1974 Aug 1;140(2):313–332. doi: 10.1084/jem.140.2.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gleich G. J., Loegering D. A., Maldonado J. E. Identification of a major basic protein in guinea pig eosinophil granules. J Exp Med. 1973 Jun 1;137(6):1459–1471. doi: 10.1084/jem.137.6.1459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gleich G. J., Loegering D. A., Mann K. G., Maldonado J. E. Comparative properties of the Charcot-Leyden crystal protein and the major basic protein from human eosinophils. J Clin Invest. 1976 Mar;57(3):633–640. doi: 10.1172/JCI108319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gupta S., Ross G. D., Good R. A., Siegal F. P. Surface markers of human eosinophils. Blood. 1976 Nov;48(5):755–763. [PubMed] [Google Scholar]
  13. McLaren D. J., Mackenzie C. D., Ramalho-Pinto F. J. Ultrastructural observations on the in vitro interaction between rat eosinophils and some parasitic helminths (Schistosoma mansoni, Trichinella spiralis and Nippostrongylus brasiliensis). Clin Exp Immunol. 1977 Oct;30(1):105–118. [PMC free article] [PubMed] [Google Scholar]
  14. McLaren D. J., Ramalho-Pinto F. J., Smithers S. R. Ultrastructural evidence for complement and antibody-dependent damage to schistosomula of Schistosoma mansoni by rat eosinophils in vitro. Parasitology. 1978 Dec;77(3):313–324. doi: 10.1017/s0031182000050277. [DOI] [PubMed] [Google Scholar]
  15. Naccache P. H., Showell H. J., Becker E. L., Sha'afi R. I. Changes in ionic movements across rabbit polymorphonuclear leukocyte membranes during lysosomal enzyme release. Possible ionic basis for lysosomal enzyme release. J Cell Biol. 1977 Dec;75(3):635–649. doi: 10.1083/jcb.75.3.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ottesen E. A., Stanley A. M., Gelfand J. A., Gadek J. E., Frank M. M., Nash T. E., Cheever A. W. Immunoglobulin and complement receptors on human eosinophils and their role in cellular adherence to schistosomules. Am J Trop Med Hyg. 1977 Nov;26(6 Pt 2):134–141. doi: 10.4269/ajtmh.1977.26.134. [DOI] [PubMed] [Google Scholar]
  17. Ramalho-Pinto F. J., McLaren D. J., Smithers S. R. Complement-mediated killing of schistosomula of Schistosoma mansoni by rat eosinophils in vitro. J Exp Med. 1978 Jan 1;147(1):147–156. doi: 10.1084/jem.147.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Stirewalt M. A., Minnick D. R., Fregeau W. A. Definition and collection in quantity of schistosomules of Schistosoma mansoni. Trans R Soc Trop Med Hyg. 1966;60(3):352–360. doi: 10.1016/0035-9203(66)90299-9. [DOI] [PubMed] [Google Scholar]
  19. Tai P. C., Spry C. J. Studies on blood eosinophils. I. Patients with a transient eosinophilia. Clin Exp Immunol. 1976 Jun;24(3):415–422. [PMC free article] [PubMed] [Google Scholar]
  20. Vadas M. A., David J. R., Butterworth A., Pisani N. T., Siongok T. A. A new method for the purification of human eosinophils and neutrophils, and a comparison of the ability of these cells to damage schistosomula of Schistosoma mansoni. J Immunol. 1979 Apr;122(4):1228–1236. [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES