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Adherence of Erythrocytes during Exflagellation of Plasmodium falciparum Microgametes Is Dependent on Erythrocyte Surface Sialic Acid and Glycophorins

By Thomas J. Templeton, David B. Keister, Olga Muratova, Jo Lynn Procter and David C. Kaslow


Malaria male gametocytes within a newly ingested infected blood meal in the mosquito midgut emerge from erythrocytes and extrude approximately eight flagellar microgametes in a process termed exflagellation. In culture, and in blood removed from infected patients, emerging microgametes avidly adhere to neighboring uninfected and infected erythrocytes, as well as to emerged female macrogametes, creating “exflagellation centers”. The mechanism of erythrocyte adherence is not known nor has it been determined for what purpose microgametes may bind to erythrocytes. The proposition of a function underlying erythrocyte adherence is supported by the observation of species-specificity in adhesion: microgametes of the human malaria Plasmodium falciparum can bind human erythrocytes but not chicken erythrocytes, whereas avian host Plasmodium gallinaceum microgametes bind chicken but not human erythrocytes. In this study we developed a binding assay in which normal, enzyme-treated, variant or null erythrocytes are identified by a cell surface fluorescent label and assayed for adherence to exflagellating microgametes. Neuraminidase, trypsin or ficin treatment of human erythrocytes eliminated their ability to adhere to Plasmodium falciparum microgametes, suggesting a role of sialic acid and one or more glycophorins in the binding to a putative gamete receptor. Using nulls lacking glycophorin A [En(a−)], glycophorin B (S−s−U−) or a combination of glycophorin A and B (Mk/Mk) we showed that erythrocytes lacking glycophorin B retain the ability to bind but a lack of glycophorin A reduced adherence by exflagellating microgametes. We propose that either the sialic acid moiety of glycophorins, predominantly glycophorin A, or a more complex interaction involving the glycophorin peptide backbone, is the erythrocyte receptor for adhesion to microgametes

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    1. (1993). A revised structure for fucoidan may explain some of its biological activities.
    2. (1956). A study of the factors affecting the emergence of the gametocytes of Plasmodium gallinaceum from the erythrocytes and the exflagellation of the male gametocytes.
    3. (1976). Absence of the major sialoglycoprotein in the membrane of human En(a2) erythrocytes and increased glycosylation of Band 3.
    4. (1979). Antibodies that define NANA-independent MN-system antigens.
    5. (1992). Binding of Plasmodium falciparum 175-kilodalton erythrocyte binding antigen and invasion of murine erythrocytes requires N-acetylneuraminic but not its O-acetylated form.
    6. (1991). Blocking of the receptor-mediated invasion of erythrocytes by Plasmodium knowlesi malaria with sulfated polysaccharides and glycosaminoglycans.
    7. (1984). Characterization of antigens on mosquito midgut stages of Plasmodium gallinaceum. II.1608 Adherence of Erythrocytes during Malaria Exflagellation Comparison of surface antigens of male and female gametes and zygotes.
    8. (1987). Characterization of the Ss sialoglycoprotein and its antigens in Rhnull erythrocytes.
    9. (1995). Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes.
    10. (1981). Complete in vitro maturation of P. falciparum gametocytes.
    11. (1977). Control of gamete formation (exflagellation) in malaria parasites.
    12. (1994). Defining the Rh blood group antigens. Blood Rev.
    13. (1986). DNA synthesis in Plasmodium berghei during asexual and sexual development.
    14. (1992). Effect of enzymes on and chemical modifications of high-frequency red cell antigens.
    15. (1982). Erythrocytes deficient in glycophorin resist invasion by the malarial parasite Plasmodium falciparum.
    16. (1977). Evidence for differences in erythrocyte surface receptors for the malarial parasites, Plasmodium falciparum and Plasmodium knowlesi.
    17. (1946). Experiments upon the feeding of Aedes aegypti through animal membranes with a view to applying this method to the chemotherapy of malaria.
    18. (1993). Factors affecting exflagellation of in vitro–cultivated Plasmodium falciparum gametocytes.
    19. (1954). Factors determining the true reservoir of infection of Plasmodium falciparum and Wuchereria bancrofti in a west African village.
    20. (1987). Falciparum malaria parasites invade erythrocytes that lack Glycophorin A and
    21. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1.
    22. (1978). Gamete development in malaria parasites. Bicarbonate-dependent stimulation by pH in vitro.
    23. (1984). Gametocyte-forming and non-gametocyte-forming clones of Plasmodium falciparum.
    24. (1985). Gametogenesis in Plasmodium; the inhibitory effects of anticytoskeletal agents.
    25. (1987). Genetic analysis of the human malaria parasite Plasmodium falciparum.
    26. (1994). Glycophorin B as an EBA175 independent Plasmodium falciparum receptor of human erythrocytes.
    27. (1975). Human blood-group MN and precursor specificities: structural and biological aspects.
    28. (1992). Human erythrocyte glycophorins: protein and gene structure analyses.
    29. (1984). Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from the same isolate.
    30. (1981). Inhibitory effects of erythrocyte membrane proteins on the in vitro invasion of the human malarial parasite (Plasmodium falciparum) into its host cell.
    31. (1986). Invasion of erythrocytes by malaria parasites: a cellular and molecular overview.
    32. (1975). Invasion of erythrocytes by Plasmodium falciparum in vitro.
    33. (1987). Invasion of mouse erythrocytes by the human malaria parasite Plasmodium falciparum.
    34. (1997). Isolation of a substance from the mosquito that activates Plasmodium fertilization.
    35. Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates.
    36. (1993). Null red blood cell phenotypes: associated biological changes.
    37. On some peculiar pigmented cells found in two mosquitoes fed on malarial blood.
    38. On the flagellated form of the malarial parasite.
    39. On the haematozoan infections of birds.
    40. Plasmodium gallinaceum: erythrocyte factor essential for zygote infection of Aedes aegypti.
    41. (1977). Plasmodium gallinaceum: exflagellation stimulated by a mosquito factor.
    42. Plasmodium gallinaceum: induction of male gametocyte exflagellation by phosphodiesterase inhibitors.
    43. (1990). Possible roles of Ca21 and cGMP as mediators of the exflagellation of Plasmodium berghei and Plasmodium falciparum.
    44. (1986). Rapid repeated DNA replication during microgametogenesis and DNA synthesis in young zygotes of Plasmodium berghei.
    45. (1994). Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum.
    46. (1905). Researches on malaria.
    47. (1994). Structural and functional properties of Trypa-1609 Templeton et al. nosoma trans-sialidase.
    48. (1996). Sulfated polyanions inhibit invasion of erythrocytes by Plasmodial merozoites and cytoadherence of endothelial cells to parasitized erythrocytes.
    49. (1983). Susceptibility to invasion by Plasmodium falciparum of some human erythrocytes carrying rare blood group antigens.
    50. (1987). The 230-kDa gamete surface protein of Plasmodium falciparum is also a target for transmissionblocking antibodies.
    51. (1981). The blood group MNSs-active sialoglycoproteins.
    52. The large diverse gene family var encodes proteins involved in cytoadherence an antigenic variation of Plasmodium falciparum–infected erythrocytes.
    53. (1957). The malarial infectivity of an African village population to mosquitoes (Anopheles gambiae). A random xenodiagnostic survey.
    54. (1993). The origin of the parasitophorous vacuole membrane lipids in malariainfected erythrocytes.
    55. (1992). The reservoir of Plasmodium falciparum malaria in a holoendemic area of western Kenya.
    56. (1997). The roles of temperature, pH and mosquito factors as triggers of male and female gametogenesis of Plasmodium berghei in vitro.
    57. (1993). The surface trans-sialidase family of Trypanosoma cruzi.
    58. (1993). Thrombospondin related anonymous protein (TRAP) of Plasmodium falciparum binds specifically to sulfated glycoconjugates and to HepG2 hepatoma cells suggesting a role for this molecule in sporozoite invasion of hepatocytes.

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