Skip to main content
SpringerLink
Log in

Two lectins on the surface of Helix pomatia haemocytes: a Ca2+-dependent, GalNac-specific lectin and a Ca2+-independent, mannose 6-phosphate-specific lectin which recognises activated homologous opsonins

  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Summary

Haemocytes of the gastropod mollusc, Helix pomatia, possess on their surface a membrane-integrated GalNac-specific lectin which binds to and stimulates phagocytosis of GalNac-bearing target cells (human A erythrocytes) only in the presence of extracellular calcium ions. Target cells without GalNac moieties on their surface (human B and bovine erythrocytes) are not recognised. Helix haemocytes also possess a Ca2+-independent mannose-6-phosphate-specific lectin on their surface which, in the absence of extracellular calcium ions, enables recognition and phagocytosis of A rbc opsonised with agglutinins isolated from either the snail's albumin gland or serum. These opsonins, however, bind to host haemocytes only after binding to GalNac moieties on the surface of test particles. Our results indicate that such a ligand-specific opsonin/target cell interaction apparently induces a conformational change in the opsonin, resulting in exposure of mannose 6-phosphate moieties that are recognised by the Ca2+-independent lectin on the surface of the haemocytes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

BSA :

bovine serum albumin

bv :

bovine

DAB :

3-3-diamino-benzidine tetrahydrochloride

ELISA :

enzyme-linked immunosorbent assay

GalNac :

N-Acetyl-D-galactosamine

G6-P :

glucose 6-phosphate

HE :

haemocyte extract

HPA :

Helix pomatia albumin gland agglutinin

HPA :

PO peroxidase-labelled HPA

M6-P :

mannose 6-phosphate

ML :

monolayer

MLS :

monolayer supernatant

OPD :

orthophenylene diamine

PBS :

phosphate buffered saline

PMSF :

phenylmethylsulphonyl fluoride

PO :

peroxidase

rbc :

red blood cells

RT :

room temperature

SA :

Helix pomatia serum agglutinin

TBS :

Tris buffered saline

References

  • Anderson RS, Holmes B, Good RA (1973) In vitro bactericidal capacity of Blaberus craniifer hemocytes. J Invertebr Pathol 22:127–135

    Google Scholar 

  • Ashwell G, Harford J (1982) Carbohydrate-specific receptors of the liver. Ann Rev Biochem 51:531–554

    Google Scholar 

  • Baker DA, Sugii S, Kabat E, Ratcliffe RM, Hermentin P (1983) Immunochemical studies on the combining sites of Forssman hapten reactive hemagglutinins from Dolichos biflorus and Helix pomatia, and Wisteria floribunda. Biochem 22:2741–2750

    Google Scholar 

  • Ballou CE, Raschke W (1974) Polymorphism of the somatic antigen of yeast. Science 184:127–134

    Google Scholar 

  • Bayne CJ (1983) Molluscan immunology. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca Vol V. Academic Press, New York pp 407–486

    Google Scholar 

  • Cheng TC (1975) Functional morphology and biochemistry of molluscan phagocytes. Ann NY Acad Sci 266:343–379

    Google Scholar 

  • Cheng TC (1983) The role of lysosomes in molluscan inflammation. Amer Zool 3:129–144

    Google Scholar 

  • Coombe DR, Rider CC (1989) Lymphocyte homing receptors cloned — a role for anionic polysaccharides in lymphocyte adhesion. Immunol Today 10:289–291

    Google Scholar 

  • Coombe DR, Ey L, Jenkin CR (1984) Particle recognition by haemocytes from the ascidian Botrylloides leachii: evidence that the B. leachii HA-2 agglutinin is opsonic. J Comp Physiol B 154:509–521

    Google Scholar 

  • Creek KE, Sly WS (1982) Adsorptive pinocytosis of phosphorylated oligosaccharides by human fibroblasts. J Biol Chem 257:9931–9937

    Google Scholar 

  • Di Virgilio F, Meyer BC, Greenberg S, Silverstein S (1986) Fc receptor-mediated phagocytosis occurs in macrophages at exceedingly low cytosolic Ca2+ levels. J Cell Biol 106:657–666

    Google Scholar 

  • Forbes JF, Brethauer AK, Oeltmann TN (1981) Mannose-6-, fructose-1-, and fructose-6-phosphates inhibit human natural killer cell-mediated cytotoxicity. Proc Natl Acad Sci USA 78:5797–5801

    Google Scholar 

  • Fryer SE, Bayne CJ (1989) Opsonisation of yeast by the plasma of Biomphalaria glabrata (Gastropoda): a strain-specific, time-dependent process. Parasit Immunol 11:269–278

    Google Scholar 

  • Fryer SE, Bull CJ, Bayne CJ (1989) Phagocytosis of yeast by Biomphalaria glabrata: carbohydrate specificity of hemocyte receptors and a plasma opsonin. Dev Comp Immunol 13:9–16

    Google Scholar 

  • Gallatin WM, Weissman IL, Butcher EC (1983) A cell surface molecule involved in organ-specific homing of lymphocytes. Nature 304:30–34

    Google Scholar 

  • Hammarström S, Kabat E (1969) Purification and characterization of a blood group A reactive hemagglutinin from the snail Helix pomatia and a study of its combining site. Biochemistry 8:2696–2705

    Google Scholar 

  • Hammarström S, Westöö A, Björk I (1972) Subunit structure of Helix pomatia A hemagglutinin. Scand J Immunol 1:295–309

    Google Scholar 

  • Harm H, Renwrantz L (1980) The inhibition of serum opsonins by a carbohydrate and the opsonizing effect of purified agglutinin on the clearance of nonself particles from the circulation of Helix pomatia. J Invertebr Pathol 36:64–70

    Google Scholar 

  • Herberman RB (1988) Lymphocytes: cytotoxic activities. In: Gallin JI, Goldstein IM, Snyderman R (eds) Inflammation: basic principles and clinical correlates. Raven Press Ltd. New York; pp 613–629

    Google Scholar 

  • Hoflack B, Fujimoto K, Kornfeld S (1987) The interaction of phosphorylated oligosaccharides and lysosomal enzymes with bovine liver cation-dependent mannose-6-phosphate receptor. J Biol Chem 262:123–129

    Google Scholar 

  • Kolb-Bachofen V, Schlepper-Schäfer J, Roos P, Hülsmann D, Kolb H (1984) GalNac/Gal-specific rat liver lectins: their role in cellular recognition. Biol Cell 51:219–226

    Google Scholar 

  • Koopman Jr. WR, Jackson RC (1990) Clacium and guanine-nucleotide-dependent exocytosis in permeabilized rat mast cells. Biochem J 265:365–373

    Google Scholar 

  • Korchak HM, Rutherfold LE, Weissmann G (1984) Stimulus response coupling in the human neutrophil. I. Kinetic analysis of changes in calcium permeability. J Biochem 259:4070–4075

    Google Scholar 

  • Kühnemund O, Köhler W (1969) Untersuchungen über die Reinigung des Protektins Anti-Ahel (Anti-AHP) aus Helix pomatia. Experientia 25:1137–1138

    Google Scholar 

  • Leippe M, Renwrantz L (1988) Release of cytotoxic and agglutinating molecules by Mytilus haemocytes. Dev Comp Immunol 12:297–308

    Google Scholar 

  • Lew DP (1989) Receptor signalling and intracellular calcium in neutrophil activation. Eur J Clin Invest 19:338–346

    Google Scholar 

  • Lew PD, Andersson T, Hed J, Di Virgilio F, Pozzan T, Stendhal O (1985) Ca2+-dependent and Ca2+-independent phagocytosis in human neutrophils. Nature 315:509–511

    Google Scholar 

  • Lew PD, Monod A, Waldvogel FA, Dewald B, Baggiolini M, Pozzan T (1986) Quantitative analysis of the cytosolic free calcium dependency of exocytosis from three subcellular compartments in intact human neutrophils. J Cell Biol 102:2197–2204

    Google Scholar 

  • Lev B, Ward H, Keusch GT, Pereira EA (1986) Lectin activation in Giardia lamblia by host protease: A novel host-parasite interaction. Science 232:71–73

    Google Scholar 

  • McNeil PL, Swanson JA, Wright SD, Silverstein SC, Taylor DL (1986) Fc-receptor mediated phagocytosis occurs in macrophages without an increase in average [Ca2+]i. J Cell Biol 102:1586–1592

    Google Scholar 

  • Mullainadhan P, Renwrantz L (1986) Lectin-dependent recognition of foreign cells by hemocytes of the mussel, Mytilus edulis. Immunobiology 171:263–273

    Google Scholar 

  • Mullainadhan P, Renwrantz L (1989) Comparative analysis of agglutinins from hemolymph and albumin gland of Helix pomatia. J Comp Physiol 159:443–452

    Google Scholar 

  • Naccache PH, Showell HJ, Becker EL, Sha'afi RI (1977) Changes in ionic movements across rabbit polymorphonuclear leucocyte membranes during lysosomal enzyme release. Possible ionic basis for lysosomal enzyme release. J Cell Biol 75:635–649

    Google Scholar 

  • Ortaldo JR (1988) Human natural killer cytotoxic factor (NKCF). Relevance, mode of action, and relationship to other cytotoxic factors. In: Ransom JH, Ortaldo JR (eds) Leucolysins and cancer. The Humana Press, Inc., pp 137–147

  • Parod RJ, Brain JD (1983) Uptake of latex particles by pulmonary macrophages: role of calcium. Am J Physiol 245:227–234

    Google Scholar 

  • Pendland JC, Heath MA, Boucias DG (1988) Function of a galactose-binding lectin from Spodoptera exigua larval hemolymph: opsonisation of blastospores from entomogeneous hyphomycetes. J Insect Physiol 34:533–540

    Google Scholar 

  • Pospíšil M, Kubrycht J (1988) Lymphocyte membrane lectins functionally important in NK cytotoxicity. In: Lectin — biology, biochemistry, clinical biochemistry. Vol. 6. Signma Chemical Company, St Louis, Missouri USA

    Google Scholar 

  • Renwrantz L (1979) Eine Untersuchung molekularer und zellulärer Bestandteile der Hämolymphe von Helix pomatia unter besonderer Berücksichtigung immunobiologisch aktiver Komponenten. Zool Jb Physiol 83:283–333

    Google Scholar 

  • Renwrantz L (1986) Lectins in molluscs and arthropods: their occurrence, origin and roles in immunity. In: Lackie AM (ed) Immune mechanisms in invertebrate vectors. Oxford, Oxford Scientific Publications, pp 81–93

    Google Scholar 

  • Renwrantz L, Mohr W (1978) Opsonising effects of serum and albumin gland extracts on the elimination of human erythrocytes from the circulation of Helix pomatia. J Invertebr Pathol 31:164–170

    Google Scholar 

  • Renwrantz L, Stahmer A (1983) Opsonising properties of an isolated serum agglutinin and demonstration of lectin-like recognition molecules at the surface of hemocytes from Mytilus edulis. J Comp Physiol 149:535–546

    Google Scholar 

  • Renwrantz L, Yoshino T, Cheng TC (1979) Size determination of hemocytes from the American oyster, Crassostrea virginica, and the description of a phagocytosis mechanism. Zool Jb Physiol 83:1–12

    Google Scholar 

  • Renwrantz L, Schänke W, Harm H, Erl H, Liebsch H, Gerken J (1981) Discriminative ability and function of the immunobiological recognition system of the snail, Helix pomatia. J Comp Physiol 141:477–488

    Google Scholar 

  • Rosen SD, Singer MS, Yednock TA (1985) Involvement of sialic acid on endothelial cells in organ-specific lymphocyte recirculation. Science 228:1005–1007

    Google Scholar 

  • Rowley AF, Ratcliffe NA (1980) Insect erythrocyte agglutinins. In vitro opsonisation experiments with Clitumnus extradentatus and Periplaneta americana. Immunology 40:483–491

    Google Scholar 

  • Rowley AF, Ratcliffe NA (1981) (eds) Invertebrate blood cells. I. Academic Press, New York

    Google Scholar 

  • Roos D, Bot AAM, van Shaik MLJ, De Boer M, Daha M (1980) Interaction between human neutrophils and zymosan particles: The role of opsonins and divalent cations. J Immunol 126:433–440

    Google Scholar 

  • Sahagian GG, Distler J, Jourdian GW (1981) Characterisation of a membrane-associated receptor from bovine liver that binds phosphomannosyl residues of bovine testicular B-galactosidase. Proc Natl Acad Sci USA 78:4289–4293

    Google Scholar 

  • Sarin A, Saxena RK (1989) Natural killer cells. Ind J Exp Biol 27:583–592

    Google Scholar 

  • Schlesinger PH, Rodman JS, Doebber TW, Stahl PD, Lee YC, Stowell CP, Kuhlenschmidt TB (1980) The role of extra-hepatic tissues in receptor-mediated plasma clearance of glycoproteins terminated by mannose or N-acetylglucosamine. Biochem J 192:597–606

    Google Scholar 

  • Scott MT (1971) Recognition of foreignness in invertebrates. II. In vitro studies of cockroach phagocytic hemocytes. Immunol 21:817–828

    Google Scholar 

  • Sharon N (1975) Complex carbohydrates. Their chemistry, biosynthesis, and functions. A set of lecture notes. Addison-Wesely, Reading, MA

    Google Scholar 

  • Shepherd VL, Freeze HH, Miller AL, Stahl PD (1984) Identification of mannose-6-phosphate receptors in rabbit alveolar macrophages. J Biol Chem 259:2257–2261

    Google Scholar 

  • Sminia T, van der Knaap WPW, Edelenbosch P (1979) The role of serum factors in phagocytosis of foreign particles by blood cells of the freshwater snail, Lymnaea stagnalis. Dev Comp Immunol 3:37–44

    Google Scholar 

  • Smolen JE, Korchak HM, Weissmann G (1981) The roles of extracellular and intracellular calcium in lysosomal enzyme release and superoxide anion generation by human neutrophils. Biochim Biophys Acta 677:512–520

    Google Scholar 

  • Stein-Streilein J, Guffee J (1989) A common trigger molecule (TrgS) for secretion of lytic factor is expressed on cells that participate in non-MHC restricted cellular cytotoxicity. Transplantation Proc 21:105–107

    Google Scholar 

  • Stockert RJ, Haimes HB, Morrel G, Novikov PM, Novikov AB, Quintana N, Sternlieb I (1980) Endocytosis of asialoglycoprotein-enzyme conjugates by hepatocytes. Lab Invest 43:556–563

    Google Scholar 

  • Stoolman LM (1989) Adhesion molecules controlling lymphocyte migration. Cell 56:907–910

    Google Scholar 

  • Takayama H, Sitkovsky M (1987) Antigen receptor-regulated exocytosis in cytotoxic T lymphocytes. J Exp Med 166:725–743

    Google Scholar 

  • Townsend R, Stahl P (1981) Isolation and characterisation of a mannose/N-acetylglucosamine/fucose-binding protein from rat liver. Biochem J 194:209–214

    Google Scholar 

  • Tuan T-L, Yoshino TP (1987) Role of divalent cations in plasma opsonin-dependent and-independent erythrophagocytosis by hemocytes of the Asian clam, Corbicula fluminea. J Invertebr Pathol 50:310–319

    Google Scholar 

  • Uhlenbruck G, Sprenger I, Pardoe GI (1970) Über Lectine mit einem breiten Agglutinationsspektrum. VIII. Serologische Eigenschaften der Blutgruppensubstanz A aus Pepton. Z Immun Forsch 140:496–504

    Google Scholar 

  • Ullrich K, Mersmann G, Weber E, von Figura K (1978) Evidence for lysosomal enzyme recognition by human fibroblasts via a phosphorylated carbohydrate moiety. Biochem J 170:643–650 Physiol Chem 359:1591–1598

    Google Scholar 

  • van der Knaap WPW, Boerrigter-Barendsen LH, van der Hoven DSP, Sminia T (1981) Immunocytochemical demonstration of a humoral defence factor in blood cells (amoebocytes) of the pond snail, Lymnaea stagnalis. Cell Tissue Res 219:291–296

    Google Scholar 

  • Vasta GR, Cheng TC, Marchalonis JJ (1984) A lectin on the hemocyte membrane of the oyster (Crassostrea virginica). Cell Immunol 8:475–488

    Google Scholar 

  • Von Figura K, Hasilik A (1986) Lysosomal enzymes and their receptors. Ann Rev Biochem 55:167–193

    Google Scholar 

  • Warr GA (1980) A macrophage receptor for (mannose/glucosamine)-glycoproteins of potential importance in phagocytic activity. Biochem Biophys Res Commun 93:737–745

    Google Scholar 

  • Yagita M, Nakajima M, Saksela E (1989) Suppression of human natural killer cell activity by amino sugars. Cell Immunol 122:83–95

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zoologisches Institut und Zoologisches Museum der Universität Hamburg, Martin-Luther-King-Platz 3, W-2000, Hamburg 13, Federal Republic of Germany

    Elaine H. Richards & Lothar R. Renwrantz

Authors
  1. Elaine H. Richards
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lothar R. Renwrantz
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Richards, E.H., Renwrantz, L.R. Two lectins on the surface of Helix pomatia haemocytes: a Ca2+-dependent, GalNac-specific lectin and a Ca2+-independent, mannose 6-phosphate-specific lectin which recognises activated homologous opsonins. J Comp Physiol B 161, 43–54 (1991). https://doi.org/10.1007/BF00258745

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00258745

Key words

Search

Navigation