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. 1982 Aug 1;94(2):370–378. doi: 10.1083/jcb.94.2.370

Human neutrophils endocytose multivalent ligands from the surface of schistosomula of Schistosoma mansoni before membrane fusion

PMCID: PMC2112873  PMID: 7107703

Abstract

Human buffy coat cells adhering to schistosomula of Schistosoma mansoni that were preincubated in fluorochrome-conjugated concanavalin A (Con A), wheat germ agglutinin, lentil lectin, or purified IgG from a hyperimmunized rabbit, were examined by fluorescence and transmission electron microscopy and by freeze-fracture. All four fluorochrome- conjugated multivalent ligands were homogeneously distributed on the parasite surface after preincubation. Within 1-3 h after the addition of cells, large areas of nonfluorescence, 10-20 micrometer in diameter, were seen on the parasite surface. In addition, the fluorochromes were observed in granules within the cells. Electron microscope autoradiography of worms preincubated with 125I-Con A showed silver grains evenly distributed over the tegumental membrane. After the addition of cells, grains were seen over phagolysosomes in the cytoplasm of neutrophils adhering to the parasites. In addition, no grains were present over large areas of the tegumental membrane, which still retained its normal architecture, or over fusions between the neutrophil plasma membrane and the outer tegumental membrane. Rabbit IgG formed an electron-dense layer on the tegumental membrane which was endocytosed by neutrophils. Both neutrophils and eosinophils fused with the parasite in areas containing no electron-dense material on the surface. It is concluded that human neutrophils will endocytose a variety of multivalent ligands from the surface of schistosomula, which probably accounts for the failure of neutrophils to kill the parasite and acts to clear the parasite surface of both antigen and antibody. Presumably, the components of the parasite surface which have originally bound the ligands are also endocytosed since surface components labeled by galactose oxidase and NaB3H4 are taken into cells when examined by light microscope autoradiography. Finally, membrane fusion occurs in areas devoid of multivalent glands, which suggests that these ligands serve to bring the cells and parasites close together, but the actual fusigens probably reside in the lipids in the outer tegumental membrane.

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Selected References

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  1. Butterworth A. E., Vadas M. A., Wassom D. L., Dessein A., Hogan M., Sherry B., Gleich G. J., David J. R. Interactions between human eosinophils and schistosomula of Schistosoma mansoni. II. The mechanism of irreversible eosinophil adherence. J Exp Med. 1979 Dec 1;150(6):1456–1471. doi: 10.1084/jem.150.6.1456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Caulfield J. P., Korman G., Butterworth A. E., Hogan M., David J. R. Partial and complete detachment of neutrophils and eosinophils from schistosomula: evidence for the establishment of continuity between a fused and normal parasite membrane. J Cell Biol. 1980 Jul;86(1):64–76. doi: 10.1083/jcb.86.1.64. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Caulfield J. P., Korman G., Butterworth A. E., Hogan M., David J. R. The adherence of human neutrophils and eosinophils to schistosomula: evidence for membrane fusion between cells and parasites. J Cell Biol. 1980 Jul;86(1):46–63. doi: 10.1083/jcb.86.1.46. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chandler D. E., Heuser J. E. Arrest of membrane fusion events in mast cells by quick-freezing. J Cell Biol. 1980 Aug;86(2):666–674. doi: 10.1083/jcb.86.2.666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dean D. A., Sell K. W. Surface antigens on Schistosoma mansoni. II. Adsorption of a Forssman-like host antigen by schistosomula. Clin Exp Immunol. 1972 Dec;12(4):525–540. [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Glauert A. M., Oliver R. C., Thorne K. J. The interaction of human eosinophils and neutrophils with non-phagocytosable surfaces: a model for studying cell-mediated immunity in schistosomiasis. Parasitology. 1980 Jun;80(3):525–537. doi: 10.1017/s0031182000000986. [DOI] [PubMed] [Google Scholar]
  9. Goldring O. L., Clegg J. A., Smithers S. R., Terry R. J. Acquisition of human blood group antigens by Schistosoma mansoni. Clin Exp Immunol. 1976 Oct;26(1):181–187. [PMC free article] [PubMed] [Google Scholar]
  10. Hockley D. J., McLaren D. J. Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. Int J Parasitol. 1973 Jan;3(1):13–25. doi: 10.1016/0020-7519(73)90004-0. [DOI] [PubMed] [Google Scholar]
  11. Hockley D. J. Schistosoma mansoni: the development of the cercarial tegument. Parasitology. 1972 Apr;64(2):245–252. doi: 10.1017/s003118200002967x. [DOI] [PubMed] [Google Scholar]
  12. Jong E. C., Mahmoud A. A., Klebanoff S. J. Peroxidase-mediated toxicity to schistosomula of Schistosoma mansoni. J Immunol. 1981 Feb;126(2):468–471. [PubMed] [Google Scholar]
  13. Kemp W. M., Damian R. T., Greene N. D. Schistosoma mansoni: immunohistochemical localization of the CHR reaction in glycocalyx of cercaria. Exp Parasitol. 1973 Feb;33(1):27–33. doi: 10.1016/0014-4894(73)90006-4. [DOI] [PubMed] [Google Scholar]
  14. Kemp W. M. Ultrastructure of the Cercarienhüllen Reaktion of Schistosoma mansoni. J Parasitol. 1970 Aug;56(4):713–723. [PubMed] [Google Scholar]
  15. Lawson D., Raff M. C., Gomperts B., Fewtrell C., Gilula N. B. Molecular events during membrane fusion. A study of exocytosis in rat peritoneal mast cells. J Cell Biol. 1977 Feb;72(2):242–259. doi: 10.1083/jcb.72.2.242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Samuelson J. C., Caulfield J. P., David J. R. Schistosomula of Schistosoma mansoni clear concanavalin A from their surface by sloughing. J Cell Biol. 1982 Aug;94(2):355–362. doi: 10.1083/jcb.94.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Samuelson J. C., Caulfield J. P. Loss of covalently labeled glycoproteins and glycolipids from the surface of newly transformed schistosomula of Schistosoma mansoni. J Cell Biol. 1982 Aug;94(2):363–369. doi: 10.1083/jcb.94.2.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Shands J. W. Localization of somatic antigen on gram-negative bacteria using ferritin antibody conjugates. Ann N Y Acad Sci. 1966 Jun 30;133(2):292–298. doi: 10.1111/j.1749-6632.1966.tb52372.x. [DOI] [PubMed] [Google Scholar]
  20. Sher A., Hall B. F., Vadas M. A. Acquisition of murine major histocompatibility complex gene products by schistosomula of Schistosoma mansoni. J Exp Med. 1978 Jul 1;148(1):46–57. doi: 10.1084/jem.148.1.46. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sher A., Hein A., Moser G., Caulfield J. P. Complement receptors promote the phagocytosis of bacteria by rat peritoneal mast cells. Lab Invest. 1979 Dec;41(6):490–499. [PubMed] [Google Scholar]
  22. Silverman D. J., Wisseman C. L., Jr, Waddell A. D., Jones M. External layers of Rickettsia prowazekii and Rickettsia rickettsii: occurrence of a slime layer. Infect Immun. 1978 Oct;22(1):233–246. doi: 10.1128/iai.22.1.233-246.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Specian R. D., Neutra M. R. Mechanism of rapid mucus secretion in goblet cells stimulated by acetylcholine. J Cell Biol. 1980 Jun;85(3):626–640. doi: 10.1083/jcb.85.3.626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Torpier G., Capron M., Capron A. Structural changes of the tegumental membrane complex in relation to developmental stages of Schistosoma mansoni (Platyhelminthes: Trematoda). J Ultrastruct Res. 1977 Dec;61(3):309–324. doi: 10.1016/s0022-5320(77)80056-7. [DOI] [PubMed] [Google Scholar]
  25. Vadas M. A., Butterworth A. E., Sherry B., Dessein A., Hogan M., Bout D., David J. R. Interactions between human eosinophils and schistosomula of Schistosoma mansoni. I. Stable and irreversible antibody-dependent adherence. J Immunol. 1980 Mar;124(3):1441–1448. [PubMed] [Google Scholar]
  26. 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]

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