Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1987 Jan;55(1):187–192. doi: 10.1128/iai.55.1.187-192.1987

Glycoprotein recognition mediates attachment of Plasmodium chabaudi to mouse erythrocytes.

M H Rodriguez, M Jungery
PMCID: PMC260299  PMID: 3539801

Abstract

The interaction between Plasmodium falciparum merozoites and human erythrocytes is mediated by specific parasite proteins and sialoglycoproteins (SGPs) on the surface of the host cell. To investigate whether a similar mechanism functions in rodent malaria, a series of experiments was performed to identify the proteins involved in the interaction of Plasmodium chabaudi parasites and mouse erythrocytes. Labeled parasite proteins incubated with purified mouse SGP bound specifically to glycoprotein 2.1. Two parasite proteins (72 and 126 kilodaltons [kDa]) were coprecipitated with antibody directed to mouse erythrocyte membrane proteins. The lower band (72 kDa) as well as a band of 105 kDa were also observed to bind to N-acetyl-D-galactosamine affinity columns, suggesting a carbohydrate component in the binding of these parasites to erythrocytes. These experiments indicate that P. chabaudi possesses specific proteins which recognized SGP on the surface of murine erythrocytes in a manner similar to that of the merozoites of P. falciparum. Thus P. chabaudi in mice may provide an in vivo model of the human parasite for testing ways to inhibit merozoite recognition and invasion of host cells.

Full text

PDF
187

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aikawa M., Miller L. H., Johnson J., Rabbege J. Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. J Cell Biol. 1978 Apr;77(1):72–82. doi: 10.1083/jcb.77.1.72. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aikawa M., Miller L. H., Rabbege J. R., Epstein N. Freeze-fracture study on the erythrocyte membrane during malarial parasite invasion. J Cell Biol. 1981 Oct;91(1):55–62. doi: 10.1083/jcb.91.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anstee D. J., Tanner M. J. The distribution of blood-group antigens on butanol extraction of human erythrocyte 'ghosts'. Biochem J. 1974 Mar;138(3):381–386. doi: 10.1042/bj1380381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baggaley V. C., Atkinson E. M. Use of CF 12 columns for preparations of DNA from rodent malarias. Trans R Soc Trop Med Hyg. 1972;66(1):4–5. doi: 10.1016/0035-9203(72)90005-3. [DOI] [PubMed] [Google Scholar]
  5. Breuer W. V., Ginsburg H., Cabantchik Z. I. An assay of malaria parasite invasion into human erythrocytes. The effects of chemical and enzymatic modification of erythrocyte membrane components. Biochim Biophys Acta. 1983 Jan 25;755(2):263–271. doi: 10.1016/0304-4165(83)90213-1. [DOI] [PubMed] [Google Scholar]
  6. Breuer W. V., Kahane I., Baruch D., Ginsburg H., Cabantchik Z. I. Role of internal domains of glycophorin in Plasmodium falciparum invasion of human erythrocytes. Infect Immun. 1983 Oct;42(1):133–140. doi: 10.1128/iai.42.1.133-140.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cohen S., Butcher G. A. Properties of protective malarial antibody. Nature. 1970 Feb 21;225(5234):732–734. doi: 10.1038/225732a0. [DOI] [PubMed] [Google Scholar]
  8. Deas J. E., Lee L. T. Competitive inhibition by soluble erythrocyte glycoproteins of penetration by Plasmodium falciparum. Am J Trop Med Hyg. 1981 Nov;30(6):1164–1167. doi: 10.4269/ajtmh.1981.30.1164. [DOI] [PubMed] [Google Scholar]
  9. Dvorak J. A., Miller L. H., Whitehouse W. C., Shiroishi T. Invasion of erythrocytes by malaria merozoites. Science. 1975 Feb 28;187(4178):748–750. doi: 10.1126/science.803712. [DOI] [PubMed] [Google Scholar]
  10. Facer C. A. Erythrocyte sialoglycoproteins and Plasmodium falciparum invasion. Trans R Soc Trop Med Hyg. 1983;77(4):524–530. doi: 10.1016/0035-9203(83)90130-x. [DOI] [PubMed] [Google Scholar]
  11. Franco da Silveira J., Falanga P. B., Pereira da Silva L. Identification of surface membrane proteins and surface membrane antigens of plasmodium chabaudi merozoites. Mol Biochem Parasitol. 1984 Jan;10(1):11–23. doi: 10.1016/0166-6851(84)90014-8. [DOI] [PubMed] [Google Scholar]
  12. Gabriel J. A., Holmquist G., Perlmann H., Berzins K., Wigzell H., Perlmann P. Identification of a Plasmodium chabaudi antigen present in the membrane of ring stage infected erythrocytes. Mol Biochem Parasitol. 1986 Jul;20(1):67–75. doi: 10.1016/0166-6851(86)90143-x. [DOI] [PubMed] [Google Scholar]
  13. Howard R. J., Haynes J. D., McGinniss M. H., Miller L. H. Studies on the role of red blood cell glycoproteins as receptors for invasion by Plasmodium falciparum merozoites. Mol Biochem Parasitol. 1982 Nov;6(5):303–315. doi: 10.1016/0166-6851(82)90063-9. [DOI] [PubMed] [Google Scholar]
  14. Jungery M., Pasvol G., Newbold C. I., Weatherall D. J. A lectin-like receptor is involved in invasion of erythrocytes by Plasmodium falciparum. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1018–1022. doi: 10.1073/pnas.80.4.1018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jungery M. Studies on the biochemical basis of the interaction of the merozoites of Plasmodium falciparum and the human red cell. Trans R Soc Trop Med Hyg. 1985;79(5):591–597. doi: 10.1016/0035-9203(85)90164-6. [DOI] [PubMed] [Google Scholar]
  16. Miller L. H., Haynes J. D., McAuliffe F. M., Shiroishi T., Durocher J. R., McGinniss M. H. Evidence for differences in erythrocyte surface receptors for the malarial parasites, Plasmodium falciparum and Plasmodium knowlesi. J Exp Med. 1977 Jul 1;146(1):277–281. doi: 10.1084/jem.146.1.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Miller L. H., Powers K. G., Shiroishi T. Plasmodium knowlesi: functional immunity and antimerozoite antibodies in rhesus monkeys after repeated infection. Exp Parasitol. 1977 Feb;41(1):105–111. doi: 10.1016/0014-4894(77)90135-7. [DOI] [PubMed] [Google Scholar]
  18. Mitchell G. H., Hadley T. J., McGinniss M. H., Klotz F. W., Miller L. H. Invasion of erythrocytes by Plasmodium falciparum malaria parasites: evidence for receptor heterogeneity and two receptors. Blood. 1986 May;67(5):1519–1521. [PubMed] [Google Scholar]
  19. Moore S., Woodrow C. F., McClelland D. B. Isolation of membrane components associated with human red cell antigens Rh(D), (c), (E) and Fy. Nature. 1982 Feb 11;295(5849):529–531. doi: 10.1038/295529a0. [DOI] [PubMed] [Google Scholar]
  20. Newbold C. I., Boyle D. B., Smith C. C., Brown K. N. Identification of a schizont- and species-specific surface glycoprotein on erythrocytes infected with rodent malarias. Mol Biochem Parasitol. 1982 Jan;5(1):45–54. doi: 10.1016/0166-6851(82)90005-6. [DOI] [PubMed] [Google Scholar]
  21. Pasvol G., Anstee D., Tanner M. J. Glycophorin C and the invasion of red cells by Plasmodium falciparum. Lancet. 1984 Apr 21;1(8382):907–908. doi: 10.1016/s0140-6736(84)91366-7. [DOI] [PubMed] [Google Scholar]
  22. Pasvol G., Jungery M. Glycophorins and red cell invasion by Plasmodium falciparum. Ciba Found Symp. 1983;94:174–195. doi: 10.1002/9780470715444.ch11. [DOI] [PubMed] [Google Scholar]
  23. Pasvol G., Jungery M., Weatherall D. J., Parsons S. F., Anstee D. J., Tanner M. J. Glycophorin as a possible receptor for Plasmodium falciparum. Lancet. 1982 Oct 30;2(8305):947–950. doi: 10.1016/s0140-6736(82)90157-x. [DOI] [PubMed] [Google Scholar]
  24. Pasvol G., Wainscoat J. S., Weatherall D. J. Erythrocytes deficiency in glycophorin resist invasion by the malarial parasite Plasmodium falciparum. Nature. 1982 May 6;297(5861):64–66. doi: 10.1038/297064a0. [DOI] [PubMed] [Google Scholar]
  25. Perkins M. E. Binding of glycophorins to Plasmodium falciparum merozoites. Mol Biochem Parasitol. 1984 Jan;10(1):67–78. doi: 10.1016/0166-6851(84)90019-7. [DOI] [PubMed] [Google Scholar]
  26. Perkins M. E. Surface proteins of Plasmodium falciparum merozoites binding to the erythrocyte receptor, glycophorin. J Exp Med. 1984 Sep 1;160(3):788–798. doi: 10.1084/jem.160.3.788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Perkins M. 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):563–567. doi: 10.1083/jcb.90.3.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Perlmann H., Berzins K., Wahlgren M., Carlsson J., Björkman A., Patarroyo M. E., Perlmann P. Antibodies in malarial sera to parasite antigens in the membrane of erythrocytes infected with early asexual stages of Plasmodium falciparum. J Exp Med. 1984 Jun 1;159(6):1686–1704. doi: 10.1084/jem.159.6.1686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Perrin L. H., Dayal R. Immunity to asexual erythrocytic stages of Plasmodium falciparum: role of defined antigens in the humoral response. Immunol Rev. 1982;61:245–269. doi: 10.1111/j.1600-065x.1982.tb00379.x. [DOI] [PubMed] [Google Scholar]
  30. Phillips R. S., Trigg P. I., Scott-Finnigan T. J., Bartholomew R. K. Culture of Plasmodium falciparum in vitro: a subculture technique used for demonstrating antiplasmodial activity in serum from some Gambians, resident in an endemic malarious area. Parasitology. 1972 Dec;65(3):525–535. doi: 10.1017/s0031182000044139. [DOI] [PubMed] [Google Scholar]
  31. Sarris A. H., Palade G. E. Isolation and partial characterization of the sialoglycoprotein fraction of murine erythrocyte ghosts. J Cell Biol. 1982 Jun;93(3):583–590. doi: 10.1083/jcb.93.3.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sarris A. H., Palade G. E. The sialoglycoproteins of murine erythrocyte ghosts. A modified periodic acid-Schiff stain procedure staining nonsubstituted and O-acetylated sialyl residues on glycopeptides. J Biol Chem. 1979 Jul 25;254(14):6724–6731. [PubMed] [Google Scholar]
  33. Schrevel J., Philippe M., Bernard F., Monsigny M. Surface Plasmodium sugar-binding components evidenced by fluorescent neoglycoproteins. Biol Cell. 1986;56(1):49–55. doi: 10.1111/j.1768-322x.1986.tb00442.x. [DOI] [PubMed] [Google Scholar]
  34. Schulman S., Oppenheim J. D., Vanderberg J. P. Assay of erythrocyte components as inhibitors of Plasmodium falciparum merozoite invasion of erythrocytes. Am J Trop Med Hyg. 1983 Jul;32(4):666–670. doi: 10.4269/ajtmh.1983.32.666. [DOI] [PubMed] [Google Scholar]
  35. Tanner M. J., Anstee D. J. A method for the direct demonstration of the lectin-binding components of the human erythrocyte membrane. Biochem J. 1976 Feb 1;153(2):265–270. doi: 10.1042/bj1530265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Vanderberg J. P., Gupta S. K., Schulman S., Oppenheim J. D., Furthmayr H. Role of the carbohydrate domains of glycophorins as erythrocyte receptors for invasion by Plasmodium falciparum merozoites. Infect Immun. 1985 Jan;47(1):201–210. doi: 10.1128/iai.47.1.201-210.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Weiss M. M., Oppenheim J. D., Vanderberg J. P. Plasmodium falciparum: assay in vitro for inhibitors of merozoite penetration of erythrocytes. Exp Parasitol. 1981 Jun;51(3):400–407. doi: 10.1016/0014-4894(81)90127-2. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES