Skip to main content
PMC home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1987 Oct;80(4):1190–1193. doi: 10.1172/JCI113178

Falciparum malaria parasites invade erythrocytes that lack glycophorin A and B (MkMk). Strain differences indicate receptor heterogeneity and two pathways for invasion.

T J Hadley 1, F W Klotz 1, G Pasvol 1, J D Haynes 1, M H McGinniss 1, Y Okubo 1, L H Miller 1
PMCID: PMC442364  PMID: 3308959

Abstract

To determine the ligands on erythrocytes for invasion by Plasmodium falciparum, we tested invasion into MkMk erythrocytes that lack glycophorins A and B and enzyme-treated erythrocytes by parasites that differ in their requirement for erythrocyte sialic acid. The 7G8 strain invaded MkMk erythrocytes and neuraminidase-treated normal erythrocytes with greater than 50% the efficiency of normal erythrocytes. In contrast, the Camp strain invaded MkMk erythrocytes at 20% of control and neuraminidase-treated normal erythrocytes at only 1.8% of control. Invasion of MkMk erythrocytes by 7G8 parasites was unaffected by treatment with neuraminidase but was markedly reduced by treatment with trypsin. In contrast, invasion of MkMk cells by Camp parasites was markedly reduced by neuraminidase but was unaffected by trypsin. We conclude that the 7G8 and Camp strains differ in ligand requirements for invasion and that 7G8 requires a trypsin sensitive ligand distinct from glycophorins A and B.

Full text

PDF
1193

Images in this article

1191Image
on p.1191

Selected References

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

  1. Anstee D. J. The blood group MNSs-active sialoglycoproteins. Semin Hematol. 1981 Jan;18(1):13–31. [PubMed] [Google Scholar]
  2. 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]
  3. Burkot T. R., Williams J. L., Schneider I. Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from the same isolate. Trans R Soc Trop Med Hyg. 1984;78(3):339–341. doi: 10.1016/0035-9203(84)90114-7. [DOI] [PubMed] [Google Scholar]
  4. Camus D., Hadley T. J. A Plasmodium falciparum antigen that binds to host erythrocytes and merozoites. Science. 1985 Nov 1;230(4725):553–556. doi: 10.1126/science.3901257. [DOI] [PubMed] [Google Scholar]
  5. Chulay J. D., Haynes J. D., Diggs C. L. Serotypes of Plasmodium falciparum defined by immune serum inhibition of in vitro growth. Bull World Health Organ. 1985;63(2):317–323. [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Friedman M. J., Blankenberg T., Sensabaugh G., Tenforde T. S. Recognition and invasion of human erythrocytes by malarial parasites: contribution of sialoglycoproteins to attachment and host specificity. J Cell Biol. 1984 May;98(5):1672–1677. doi: 10.1083/jcb.98.5.1672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gahmberg C. G., Andersson L. C. Selective radioactive labeling of cell surface sialoglycoproteins by periodate-tritiated borohydride. J Biol Chem. 1977 Aug 25;252(16):5888–5894. [PubMed] [Google Scholar]
  9. Hadley T. J., Erkmen Z., Kaufman B. M., Futrovsky S., McGuinnis M. H., Graves P., Sadoff J. C., Miller L. H. Factors influencing invasion of erythrocytes by Plasmodium falciparum parasites: the effects of an N-acetyl glucosamine neoglycoprotein and an anti-glycophorin A antibody. Am J Trop Med Hyg. 1986 Sep;35(5):898–905. doi: 10.4269/ajtmh.1986.35.898. [DOI] [PubMed] [Google Scholar]
  10. Hadley T. J. Invasion of erythrocytes by malaria parasites: a cellular and molecular overview. Annu Rev Microbiol. 1986;40:451–477. doi: 10.1146/annurev.mi.40.100186.002315. [DOI] [PubMed] [Google Scholar]
  11. Jungery M., Boyle D., Patel T., Pasvol G., Weatherall D. J. Lectin-like polypeptides of P. falciparum bind to red cell sialoglycoproteins. Nature. 1983 Feb 24;301(5902):704–705. doi: 10.1038/301704a0. [DOI] [PubMed] [Google Scholar]
  12. McGinniss M. H., Wasniowska K., Zopf D. A., Straus S. E., Reichert C. M. An erythrocyte Pr auto-antibody with sialoglycoprotein specificity in a patient with purine nucleoside phosphorylase deficiency. Transfusion. 1985 Mar-Apr;25(2):131–136. doi: 10.1046/j.1537-2995.1985.25285169204.x. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. 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]
  16. 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]
  17. 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]
  18. 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]
  19. 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]
  20. Rosario V. Cloning of naturally occurring mixed infections of malaria parasites. Science. 1981 May 29;212(4498):1037–1038. doi: 10.1126/science.7015505. [DOI] [PubMed] [Google Scholar]
  21. Tokunaga E., Sasakawa S., Tamaka K., Kawamata H., Giles C. M., Ikin E. W., Poole J., Anstee D. J., Mawby W., Tanner M. J. Two apparently healthy Japanese individuals of type MkMk have erythrocytes which lack both the blood group MN and Ss-active sialoglycoproteins. J Immunogenet. 1979 Dec;6(6):383–390. doi: 10.1111/j.1744-313x.1979.tb00693.x. [DOI] [PubMed] [Google Scholar]
  22. Trager W., Jensen J. B. Human malaria parasites in continuous culture. Science. 1976 Aug 20;193(4254):673–675. doi: 10.1126/science.781840. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES