Abstract
Human erythrocyte glycophorin, a putative receptor to Plasmodium falciparum malaria parasites, was studied in terms of its structural domains involved in mediating invasion. These domains were isolated from purified glycophorin A and from supernatants and membranes obtained from protease-treated erythrocytes. They were tested for invasion blocking capacity by using an in vitro assay system. The role of carbohydrate-rich domains was assessed with the following compounds: (i) sialoglycopeptides released by proteases either from whole cells or isolated glycophorin A; (ii) the sialoglycoproteins fetuin and alpha 1 acid glycoprotein and the N-acetylglucosamine-rich ovomucoid; and (iii) the saccharides N-acetylneuraminlactose, N-acetylglucosamine, and free sialic acid. With the exception of N-acetylglucosamine, all of the compounds failed to block invasion. The role of carbohydrate-poor domains of glycophorin was assessed with peptides isolated from membranes of proteolyzed cells and with the hydrophobic fragment of glycophorin A. Glycophorin and the derived hydrophobic peptides formed high-molecular-weight aggregates in physiological solutions. They all inhibited invasion to a comparable extent. The inhibitory potency of glycophorin A increased by sixfold after reconstitution into egg lecithin vesicles. The observations reported here underscore the role played by the hydrophobic domain in the glycophorin-mediated blockage of invasion. They also suggest that in the interactions between P. falciparum merozoites and the erythrocyte membrane, the exposed glycosylated domains of glycophorins provide the initial but rather weak binding sites, whereas the internal domains of the molecules provide the more stable attachment sites for merozoites.
MeSH Terms
Acetylglucosamine/pharmacology
Binding Sites
Chemical Phenomena
Chemistry, Physical
Erythrocyte Membrane/parasitology
Erythrocytes/parasitology
Glycophorins/analysis,physiology
Humans
Lactose/analogs & derivatives,pharmacology
Orosomucoid/pharmacology
Ovomucin/pharmacology
Plasmodium falciparum/physiology
Sialic Acids/pharmacology
Sialoglycoproteins/pharmacology,physiology
alpha-Fetoproteins/pharmacology
Chemicals
Glycophorins
Orosomucoid
Sialic Acids
Sialoglycoproteins
alpha-Fetoproteins
Ovomucin
N-acetylneuraminoyllactose
Lactose
Acetylglucosamine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Breuer W V
Kahane I
Baruch D
Ginsburg H
Cabantchik Z I
References (30)
30 references, click to expand
-
Studies on glycopeptides released by trypsin from intact human erythrocytes.
Biochemistry. 1967 Jul;6(7):2195-202
PMID: 6049454
-
The relationship of the influenza virus inhibitory activity of glycoproteins to their molecular size and sialic acid content.
Proc Natl Acad Sci U S A. 1969 Oct;64(2):634-41
PMID: 5261039
-
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature. 1970 Aug 15;227(5259):680-5
PMID: 5432063
-
Solubilization of human erythrocyte membrane glycoproteins and separation of the MN glycoprotein from a glycoprotein with I, S, and A activity.
Biochim Biophys Acta. 1972 Sep 29;278(2):271-80
PMID: 4673526
-
Major glycoprotein of the human erythrocyte membrane: evidence for an amphipathic molecular structure.
Arch Biochem Biophys. 1973 Mar;155(1):167-83
PMID: 4712445
-
Membrane proteins related to anion permeability of human red blood cells. II. Effects of proteolytic enzymes on disulfonic stilbene sites of surface proteins.
J Membr Biol. 1974;15(3):227-48
PMID: 4838038
-
Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants.
Science. 1975 Aug 15;189(4202):561-3
PMID: 1145213
-
Isolation of membrane glycoproteins by affinity chromatography in the presence of detergents.
Biochim Biophys Acta. 1976 Mar 19;426(3):464-76
PMID: 1268207
-
Human malaria parasites in continuous culture.
Science. 1976 Aug 20;193(4254):673-5
PMID: 781840
-
Comparative aspects of glycoprotein structure.
Annu Rev Biochem. 1976;45:217-37
PMID: 786150
-
Vertical displacement of membrane proteins mediated by changes in microviscosity.
Proc Natl Acad Sci U S A. 1976 Dec;73(12):4526-30
PMID: 1070002
-
Evidence for differences in erythrocyte surface receptors for the malarial parasites, Plasmodium falciparum and Plasmodium knowlesi.
J Exp Med. 1977 Jul 1;146(1):277-81
PMID: 327014
-
The Duffy blood group determinants: their role in the susceptibility of human and animal erythrocytes to Plasmodium knowlesi malaria.
Br J Haematol. 1977 Jul;36(3):327-35
PMID: 70210
-
Hypothesis on the mechanism of erythrocyte invasion by malaria merozoites.
Bull World Health Organ. 1977;55(2-3):157-62
PMID: 412599
-
Structural comparison of glycophorins and immunochemical analysis of genetic variants.
Nature. 1978 Feb 9;271(5645):519-24
PMID: 622188
-
The intramembranous segment of human erythrocyte glycophorin A.
Arch Biochem Biophys. 1978 Jan 15;185(1):21-9
PMID: 623483
-
Glycophorins A, B, and C: a family of sialoglycoproteins. Isolation and preliminary characterization of trypsin derived peptides.
J Supramol Struct. 1978;9(1):79-95
PMID: 732312
-
Synchronization of Plasmodium falciparum erythrocytic stages in culture.
J Parasitol. 1979 Jun;65(3):418-20
PMID: 383936
-
Biochemistry of Plasmodium (malarial parasites).
Microbiol Rev. 1979 Dec;43(4):453-95
PMID: 94424
-
Plasmodium falciparum: assay in vitro for inhibitors of merozoite penetration of erythrocytes.
Exp Parasitol. 1981 Jun;51(3):400-7
PMID: 7014239
-
Isolation of binding sites to glycophorin from Mycoplasma pneumoniae membranes.
Infect Immun. 1980 Dec;30(3):628-34
PMID: 6785229
-
Inhibitory effects of erythrocyte membrane proteins on the in vitro invasion of the human malarial parasite (Plasmodium falciparum) into its host cell.
J Cell Biol. 1981 Sep;90(3):563-7
PMID: 7026577
-
Competitive inhibition by soluble erythrocyte glycoproteins of penetration by Plasmodium falciparum.
Am J Trop Med Hyg. 1981 Nov;30(6):1164-7
PMID: 7034559
-
Erythrocytes deficiency in glycophorin resist invasion by the malarial parasite Plasmodium falciparum.
Nature. 1982 May 6;297(5861):64-6
PMID: 7040988
-
The interaction of malaria parasites with red blood cells.
Br Med Bull. 1982 May;38(2):133-40
PMID: 7052193
-
Glycophorin as a possible receptor for Plasmodium falciparum.
Lancet. 1982 Oct 30;2(8305):947-50
PMID: 6127459
-
Studies on the role of red blood cell glycoproteins as receptors for invasion by Plasmodium falciparum merozoites.
Mol Biochem Parasitol. 1982 Nov;6(5):303-15
PMID: 6757749
-
New approaches for the reconstitution and functional assay of membrane transport proteins. Application to the anion transporter of human erythrocytes.
Biochim Biophys Acta. 1983 Jan 5;727(1):77-88
PMID: 6824657
-
Protein measurement with the Folin phenol reagent.
J Biol Chem. 1951 Nov;193(1):265-75
PMID: 14907713
-
The thiobarbituric acid assay of sialic acids.
J Biol Chem. 1959 Aug;234(8):1971-5
PMID: 13672998