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. 1985 May 1;100(5):1423–1434. doi: 10.1083/jcb.100.5.1423

The cercarial glycocalyx of Schistosoma mansoni

PMCID: PMC2113874  PMID: 2985622

Abstract

Cercariae, the freshwater stage of Schistosoma mansoni infectious to man, are covered by a single unit membrane and an immunogenic glycocalyx. When cercariae penetrate the host skin, they transform to schistosomula by shedding tails, secreting mucous and enzymes, and forming microvilli over their surface. Here the loss of the glycocalyx from cercariae transforming in vitro was studied morphologically and biochemically. By scanning electron microscopy, the glycocalyx was a dense mesh composed of 15-30 nm fibrils that obscured spines on the cercarial surface. The glycocalyx was absent on organisms fixed without osmium and was partially lost when parasites aggregated in their own secretions before fixation. By transmission electron microscopy, a 1-2 microns thick mesh of 8-15-nm fibrils was seen on parasites incubated with anti-schistosomal antibodies or fixed in aldehydes containing tannic acid or ruthenium red. Cercariae transformed to schistosomula when tails were removed mechanically and parasites were incubated in saline. Within 5 min of transformation, organisms synchronously formed microvilli which elongated to 3-5 microns by 20 min and then were shed. However, considerable fibrillar material remained adherent to the double unit membrane surface of schistosomula. For biochemical labeling, parasites were treated with eserine sulfate, which blocked cercarial swimming, secretion, infectivity, and transformation to schistosomula. Material labeled by periodate oxidation and NaB3H4 was on the surface as shown by autoradiography and had an apparent molecular weight of greater than 10(6) by chromatography. Periodate- NaB3H4 glycocalyx had an isoelectric point of 5.0 +/- 0.4 and was precipitable with anti-schistosomal antibodies. More than 60% of the radiolabeled glycocalyx was released into the medium by transforming parasites in 3 h and was recovered as high molecular weight material. Parasites labeled with periodate and fluorescein-thiosemicarbazide and then transformed had a corona of fluorescence containing microvilli, much of which was shed onto the slide. Material on cercariae labeled by lodogen-catalyzed iodination was also of high molecular weight and was antigenic. In conclusion, the cercarial glycocalyx appears to be composed of acidic high molecular weight fibrils which are antigenic and incompletely cleared during transformation.

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Selected References

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  1. Barker L. R., Bueding E., Timms A. R. The possible role of acetylcholine in Schistosoma mansoni. Br J Pharmacol Chemother. 1966 Mar;26(3):656–665. doi: 10.1111/j.1476-5381.1966.tb01845.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Butterworth A. E. The eosinophil and its role in immunity to helminth infection. Curr Top Microbiol Immunol. 1977;77:127–168. doi: 10.1007/978-3-642-66740-4_5. [DOI] [PubMed] [Google Scholar]
  4. Caulfield J. P., Korman G., Samuelson J. C. Human neutrophils endocytose multivalent ligands from the surface of schistosomula of Schistosoma mansoni before membrane fusion. J Cell Biol. 1982 Aug;94(2):370–378. doi: 10.1083/jcb.94.2.370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Colley D. G., Wikel S. K. Schistosoma mansoni: simplified method for the production of schistosomules. Exp Parasitol. 1974 Feb;35(1):44–51. doi: 10.1016/0014-4894(74)90005-8. [DOI] [PubMed] [Google Scholar]
  6. Crabtree J. E., Wilson R. A. Schistosoma mansoni: a scanning electron microscope study of the developing schistosomulum. Parasitology. 1980 Dec;81(Pt 3):553–564. doi: 10.1017/s003118200006193x. [DOI] [PubMed] [Google Scholar]
  7. Dean D. A. Decreased binding of cytotoxic antibody by developing Schistosoma mansoni. Evidence for a surface change independent of host antigen adsorption and membrane turnover. J Parasitol. 1977 Jun;63(3):418–426. [PubMed] [Google Scholar]
  8. Dessein A., Samuelson J. C., Butterworth A. E., Hogan M., Sherry B. A., Vadas M. A., David J. R. Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules. Parasitology. 1981 Jun;82(Pt 3):357–374. doi: 10.1017/s0031182000066890. [DOI] [PubMed] [Google Scholar]
  9. Dias Da Silva W., Kasatchkine M. D. Schistosoma mansoni: activation of the alternative pathway of human complement by schistosomula. Exp Parasitol. 1980 Oct;50(2):278–286. doi: 10.1016/0014-4894(80)90029-6. [DOI] [PubMed] [Google Scholar]
  10. Dissous C., Dissous C., Capron A. Isolation and characterization of surface antigens from Schistosoma mansoni schistosomula. Mol Biochem Parasitol. 1981 Aug;3(4):215–225. doi: 10.1016/0166-6851(81)90053-0. [DOI] [PubMed] [Google Scholar]
  11. Dissous C., Grzych J. M., Capron A. Schistosoma mansoni surface antigen defined by a rat monoclonal IgG2a. J Immunol. 1982 Nov;129(5):2232–2234. [PubMed] [Google Scholar]
  12. GORDON R. M., GRIFFITHS R. B. Observations on the means by which the cercariae of Schistosoma mansoni penetrate mammalian skin, together with an account of certain morphological changes observed in the newly penetrated larvae. Ann Trop Med Parasitol. 1951 Dec;45(3-4):227–243. doi: 10.1080/00034983.1951.11685493. [DOI] [PubMed] [Google Scholar]
  13. Gahmberg C. G., Andersson L. C. Selective radioactive labeling of cell surface sialoglycoproteins by periodate-tritiated borohydride. J Biol Chem. 1977 Aug 25;252(16):5888–5894. [PubMed] [Google Scholar]
  14. Harn D. A., Mitsuyama M., David J. R. Schistosoma mansoni. Anti-egg monoclonal antibodies protect against cercarial challenge in vivo. J Exp Med. 1984 May 1;159(5):1371–1387. doi: 10.1084/jem.159.5.1371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hasty D. L., Hay E. D. Freeze-fracture studies of the developing cell surface. II. Particle-free membrane blisters on glutaraldehyde-fixed corneal fibroblasts are artefacts. J Cell Biol. 1978 Sep;78(3):756–768. doi: 10.1083/jcb.78.3.756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Hubbard A. L., Cohn Z. A. Externally disposed plasma membrane proteins. I. Enzymatic iodination of mouse L cells. J Cell Biol. 1975 Feb;64(2):438–460. doi: 10.1083/jcb.64.2.438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kassim O., Gibertson D. E. Hatching of Schistosoma mansoni eggs and observations on motility of miracidia. J Parasitol. 1976 Oct;62(5):715–720. [PubMed] [Google Scholar]
  19. 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]
  20. Kemp W. M. Serology of the Cercarienhüllen Reaktion of Schistosoma mansoni. J Parasitol. 1972 Aug;58(4):686–692. [PubMed] [Google Scholar]
  21. Kemp W. M. Ultrastructure of the Cercarienhüllen Reaktion of Schistosoma mansoni. J Parasitol. 1970 Aug;56(4):713–723. [PubMed] [Google Scholar]
  22. Kessler S. W. Rapid isolation of antigens from cells with a staphylococcal protein A-antibody adsorbent: parameters of the interaction of antibody-antigen complexes with protein A. J Immunol. 1975 Dec;115(6):1617–1624. [PubMed] [Google Scholar]
  23. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  24. Luft J. H. Ruthenium red and violet. I. Chemistry, purification, methods of use for electron microscopy and mechanism of action. Anat Rec. 1971 Nov;171(3):347–368. doi: 10.1002/ar.1091710302. [DOI] [PubMed] [Google Scholar]
  25. Markwell M. A., Fox C. F. Surface-specific iodination of membrane proteins of viruses and eucaryotic cells using 1,3,4,6-tetrachloro-3alpha,6alpha-diphenylglycoluril. Biochemistry. 1978 Oct 31;17(22):4807–4817. doi: 10.1021/bi00615a031. [DOI] [PubMed] [Google Scholar]
  26. Maupin P., Pollard T. D. Improved preservation and staining of HeLa cell actin filaments, clathrin-coated membranes, and other cytoplasmic structures by tannic acid-glutaraldehyde-saponin fixation. J Cell Biol. 1983 Jan;96(1):51–62. doi: 10.1083/jcb.96.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McLaren D. J., Clegg J. A., Smithers S. R. Acquisition of host antigens by young Schistosoma mansoni in mice: correlation with failure to bind antibody in vitro. Parasitology. 1975 Feb;70(1):67–75. doi: 10.1017/s0031182000048873. [DOI] [PubMed] [Google Scholar]
  28. McLaren D. J., Hockley D. J. Schistosoma mansoni: the occurrence of microvilli on the surface of the tegument during transformation from cercaria to schistosomulum. Parasitology. 1976 Oct;73(2):169–187. doi: 10.1017/s0031182000046850. [DOI] [PubMed] [Google Scholar]
  29. Phillips S. M., Colley D. G. Immunologic aspects of host responses to schistosomiasis: resistance, immunopathology, and eosinophil involvement. Prog Allergy. 1978;24:49–182. [PubMed] [Google Scholar]
  30. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Radola B. J. Isoelectric focusing in layers of granulated gels. I. Thin-layer isoelectric focusing of proteins. Biochim Biophys Acta. 1973 Feb 21;295(2):412–428. doi: 10.1016/0005-2795(73)90037-8. [DOI] [PubMed] [Google Scholar]
  32. Ramalho-Pinto F. J., Gazzinelli G., Howells R. E., Mota-Santos T. A., Figueiredo E. A., Pellegrino J. Schistosoma mansoni: defined system for stepwise transformation of cercaria to schistosomule in vitro. Exp Parasitol. 1974 Dec;36(3):360–372. doi: 10.1016/0014-4894(74)90076-9. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Rando R. R., Bangerter F. W. On the labelling of oxidized cell surface membranes by acyl hydrazides. Biochim Biophys Acta. 1979 Nov 2;557(2):354–362. doi: 10.1016/0005-2736(79)90333-x. [DOI] [PubMed] [Google Scholar]
  35. Robson R. T., Erasmus D. A. The ultrastructure, based on stereoscan observations, of the oral sucker of the cercaria of Schistosoma mansoni with special reference to penetration. Z Parasitenkd. 1970;35(1):76–86. doi: 10.1007/BF00259532. [DOI] [PubMed] [Google Scholar]
  36. STIREWALT M. A., EVANS A. S. Serologic reactions in Schistosoma mansoni infections. I. Cercaricidal, precipitation, agglutination, and CHR phenomena. Exp Parasitol. 1955 Mar;4(2):123–142. doi: 10.1016/0014-4894(55)90006-0. [DOI] [PubMed] [Google Scholar]
  37. Samuelson J. C., Caulfield J. P., David J. R. Schistosoma mansoni: post-transformational surface changes in schistosomula grown in vitro and in mice. Exp Parasitol. 1980 Dec;50(3):369–383. doi: 10.1016/0014-4894(80)90040-5. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. Samuelson J. C., Sher A., Caulfield J. P. Newly transformed schistosomula spontaneously lose surface antigens and C3 acceptor sites during culture. J Immunol. 1980 Apr;124(4):2055–2057. [PubMed] [Google Scholar]
  41. Sher A., Benno D. Decreasing immunogenicity of developing schistosome larvae. Parasite Immunol. 1982 Mar;4(2):101–107. doi: 10.1111/j.1365-3024.1982.tb00423.x. [DOI] [PubMed] [Google Scholar]
  42. Smith J. H., Reynolds E. S., Von Lichtenberg F. The integument of Schistosoma mansoni. Am J Trop Med Hyg. 1969 Jan;18(1):28–49. [PubMed] [Google Scholar]
  43. Snary D., Smith M. A., Clegg J. A. Surface proteins of Schistosoma mansoni and their expression during morphogenesis. Eur J Immunol. 1980 Jul;10(7):573–575. doi: 10.1002/eji.1830100716. [DOI] [PubMed] [Google Scholar]
  44. Stein P. C., Lumsden R. D. Schistosoma mansoni: topochemical features of cercariae, schistosomula, and adults. Exp Parasitol. 1973 Jun;33(3):499–514. doi: 10.1016/0014-4894(73)90118-5. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. 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]
  47. Taylor D. W., Hayunga E. G., Vannier W. E. Surface antigens of Schistosoma mansoni. Mol Biochem Parasitol. 1981 Jul;3(3):157–168. doi: 10.1016/0166-6851(81)90046-3. [DOI] [PubMed] [Google Scholar]
  48. Van der Linden P. W., Koerten H. K., Deelder A. M. Scanning electron microscopical observations on antigen-antibody coat formation on mechanically transformed Schistosoma mansoni schistosomula. Z Parasitenkd. 1982;68(1):73–80. doi: 10.1007/BF00926659. [DOI] [PubMed] [Google Scholar]
  49. Weber K., Osborn M. The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J Biol Chem. 1969 Aug 25;244(16):4406–4412. [PubMed] [Google Scholar]
  50. Wilson R. A., Barnes P. E. The tegument of Schistosoma mansoni: observations on the formation, structure and composition of cytoplasmic inclusions in relation to tegument function. Parasitology. 1974 Apr;68(2):239–258. [PubMed] [Google Scholar]

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