Glycocalyx of bodies versus tails of Schistosoma mansoni cercariae: Lectin-binding, size, charge, and electron microscopic characterization

Jayasri Nanduri, James E. Dennis, Terrone L. Rosenberry, Adel A F Mahmoud, Alan M. Tartakoff

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Abstract

Infection with Schistosoma mansoni is initiated by penetration of the intact skin of the mammalian host with the head but not the tail of the parasite cercariae. The surface of cercariae is covered by a 1-2-micron thick carbohydrate-rich glycocalyx (gx). Furthermore, the transformation of cercariae to schistosomula (the next parasitic stage in the mammalian host) is associated with loss of gx from the bodies. To understand the role of gx in the host-parasite relationship, we have characterized the gx of both bodies and tails of S. mansoni cercariae. A fluorescent fucose-specific lectin-stained bodies and not tails of the organism. Moreover, when an enriched preparation of gx obtained by extraction with 40% aqueous phenol and exclusion from Sepharose CL-6B was subjected to affinity chromatography on insolubilized Lotus lectin, which binds fucose-containing glycans, only body gx was retained. Body gx is smaller and less negatively charged than tail gx. Electron microscopy showed that gx from bodies and tails is composed of 25-40-nm particles and fibrillar material. Carbohydrate composition of gx of bodies and tails indicate that fucose and glucose are major components, respectively. β-Elimination experiments indicate that the linkage sugar is N-acetylgalactosamine in both cases. Upon treatment with alkaline borohydride, nearly 90% of gx of both bodies and tails was recovered as two glycan chains: I and II (Mr ∼10,500 and 5,600, respectively). Glycan I was in both cases more negatively charged than glycan II. Fucose is the predominant sugar in glycan I of the bodies while glycan I of tails is mainly composed of glucose. The gx was resistant to several proteases. This resistance and the abundance of carbohydrate in gx may be of biological importance for survival of cercariae. The substantial differences observed between the gx of bodies and tails may provide the basis for understanding the mechanism of selective release of body gx during transformation.

Original languageEnglish (US)
Pages (from-to)1341-1347
Number of pages7
JournalJournal of Biological Chemistry
Volume266
Issue number2
StatePublished - Jan 15 1991
Externally publishedYes

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Glycocalyx
Cercaria
Schistosoma mansoni
Lectins
Polysaccharides
Tail
Electrons
Fucose
Carbohydrates
Sugars
Affinity chromatography
Acetylgalactosamine
Glucose
Borohydrides
Phenol
Electron microscopy
Skin
Peptide Hydrolases
Host-Parasite Interactions
Schistosomiasis mansoni

ASJC Scopus subject areas

  • Biochemistry

Cite this

Nanduri, J., Dennis, J. E., Rosenberry, T. L., Mahmoud, A. A. F., & Tartakoff, A. M. (1991). Glycocalyx of bodies versus tails of Schistosoma mansoni cercariae: Lectin-binding, size, charge, and electron microscopic characterization. Journal of Biological Chemistry, 266(2), 1341-1347.

Glycocalyx of bodies versus tails of Schistosoma mansoni cercariae : Lectin-binding, size, charge, and electron microscopic characterization. / Nanduri, Jayasri; Dennis, James E.; Rosenberry, Terrone L.; Mahmoud, Adel A F; Tartakoff, Alan M.

In: Journal of Biological Chemistry, Vol. 266, No. 2, 15.01.1991, p. 1341-1347.

Research output: Contribution to journalArticle

Nanduri, Jayasri ; Dennis, James E. ; Rosenberry, Terrone L. ; Mahmoud, Adel A F ; Tartakoff, Alan M. / Glycocalyx of bodies versus tails of Schistosoma mansoni cercariae : Lectin-binding, size, charge, and electron microscopic characterization. In: Journal of Biological Chemistry. 1991 ; Vol. 266, No. 2. pp. 1341-1347.
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abstract = "Infection with Schistosoma mansoni is initiated by penetration of the intact skin of the mammalian host with the head but not the tail of the parasite cercariae. The surface of cercariae is covered by a 1-2-micron thick carbohydrate-rich glycocalyx (gx). Furthermore, the transformation of cercariae to schistosomula (the next parasitic stage in the mammalian host) is associated with loss of gx from the bodies. To understand the role of gx in the host-parasite relationship, we have characterized the gx of both bodies and tails of S. mansoni cercariae. A fluorescent fucose-specific lectin-stained bodies and not tails of the organism. Moreover, when an enriched preparation of gx obtained by extraction with 40{\%} aqueous phenol and exclusion from Sepharose CL-6B was subjected to affinity chromatography on insolubilized Lotus lectin, which binds fucose-containing glycans, only body gx was retained. Body gx is smaller and less negatively charged than tail gx. Electron microscopy showed that gx from bodies and tails is composed of 25-40-nm particles and fibrillar material. Carbohydrate composition of gx of bodies and tails indicate that fucose and glucose are major components, respectively. β-Elimination experiments indicate that the linkage sugar is N-acetylgalactosamine in both cases. Upon treatment with alkaline borohydride, nearly 90{\%} of gx of both bodies and tails was recovered as two glycan chains: I and II (Mr ∼10,500 and 5,600, respectively). Glycan I was in both cases more negatively charged than glycan II. Fucose is the predominant sugar in glycan I of the bodies while glycan I of tails is mainly composed of glucose. The gx was resistant to several proteases. This resistance and the abundance of carbohydrate in gx may be of biological importance for survival of cercariae. The substantial differences observed between the gx of bodies and tails may provide the basis for understanding the mechanism of selective release of body gx during transformation.",
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