Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1998 Sep 15;334(Pt 3):525–530. doi: 10.1042/bj3340525

Increased choline transport in erythrocytes from mice infected with the malaria parasite Plasmodium vinckei vinckei.

H M Staines 1, K Kirk 1
PMCID: PMC1219718  PMID: 9729457

Abstract

Parasitized erythrocytes from mice infected with the murine malaria parasite Plasmodium vinckei vinckei showed a marked increase in the rate of influx of choline compared with erythrocytes from uninfected mice. In contrast, uninfected erythrocytes from P. vinckei-infected animals transported choline at the same rate as those from uninfected mice. The increased influx of choline into parasitized cells was via two discrete routes. One was a saturable pathway with a Km similar to that of the choline carrier of normal erythrocytes but a Vmax approx. 20-fold higher than that observed in uninfected cells. The other was a non-saturable pathway inhibited by furosemide. At choline concentrations within the normal physiological plasma concentration range, the former pathway contributed approx. two-thirds and the latter approx. one-third of the influx of choline into parasitized cells. The characteristics of the furosemide-sensitive pathway were similar to those of a broad-specificity pathway that is induced in human erythrocytes infected in vitro with Plasmodium falciparum. The results of this study rule out the possibility that the induced transport pathway of P. falciparum-infected erythrocytes is an artifact arising in vitro from the long-term culture of parasitized cells and provide evidence that this pathway makes a significant contribution to the uptake of choline into the parasitized cells of malaria-infected animals.

Full Text

The Full Text of this article is available as a PDF (310.0 KB).

Selected References

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

  1. Ancelin M. L., Parant M., Thuet M. J., Philippot J. R., Vial H. J. Increased permeability to choline in simian erythrocytes after Plasmodium knowlesi infection. Biochem J. 1991 Feb 1;273(Pt 3):701–709. doi: 10.1042/bj2730701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ancelin M. L., Vial H. J. Regulation of phosphatidylcholine biosynthesis in Plasmodium-infected erythrocytes. Biochim Biophys Acta. 1989 Jan 23;1001(1):82–89. doi: 10.1016/0005-2760(89)90310-x. [DOI] [PubMed] [Google Scholar]
  3. Ancelin M. L., Vial H. J. Saturable and non-saturable components of choline transport in Plasmodium-infected mammalian erythrocytes: possible role of experimental conditions. Biochem J. 1992 Apr 15;283(Pt 2):619–621. doi: 10.1042/bj2830619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cabantchik Z. I. Properties of permeation pathways induced in the human red cell membrane by malaria parasites. Blood Cells. 1990;16(2-3):421–432. [PubMed] [Google Scholar]
  5. Crandall I., Sherman I. W. Plasmodium falciparum (human malaria)-induced modifications in human erythrocyte band 3 protein. Parasitology. 1991 Jun;102(Pt 3):335–340. doi: 10.1017/s0031182000064271. [DOI] [PubMed] [Google Scholar]
  6. Das I., de Belleroche J., Moore C. J., Rose F. C. Determination of free choline in plasma and erythrocyte samples and choline derived from membrane phosphatidylcholine by a chemiluminescence method. Anal Biochem. 1986 Jan;152(1):178–182. doi: 10.1016/0003-2697(86)90138-7. [DOI] [PubMed] [Google Scholar]
  7. Elford B. C., Cowan G. M., Ferguson D. J. Parasite-regulated membrane transport processes and metabolic control in malaria-infected erythrocytes. Biochem J. 1995 Jun 1;308(Pt 2):361–374. doi: 10.1042/bj3080361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ellory J. C., Kirk K., Culliford S. J., Nash G. B., Stuart J. Nitrendipine is a potent inhibitor of the Ca(2+)-activated K+ channel of human erythrocytes. FEBS Lett. 1992 Jan 20;296(2):219–221. doi: 10.1016/0014-5793(92)80383-r. [DOI] [PubMed] [Google Scholar]
  9. Gati W. P., Lin A. N., Wang T. I., Young J. D., Paterson A. R. Parasite-induced processes for adenosine permeation in mouse erythrocytes infected with the malarial parasite Plasmodium yoelii. Biochem J. 1990 Nov 15;272(1):277–280. doi: 10.1042/bj2720277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ginsburg H. Transport pathways in the malaria-infected erythrocyte. Their characterization and their use as potential targets for chemotherapy. Biochem Pharmacol. 1994 Nov 16;48(10):1847–1856. doi: 10.1016/0006-2952(94)90582-7. [DOI] [PubMed] [Google Scholar]
  11. Holz G. G., Jr Lipids and the malarial parasite. Bull World Health Organ. 1977;55(2-3):237–248. [PMC free article] [PubMed] [Google Scholar]
  12. Homewood C. A., Neame K. D. Malaria and the permeability of the host erythrocyte. Nature. 1974 Dec 20;252(5485):718–719. doi: 10.1038/252718a0. [DOI] [PubMed] [Google Scholar]
  13. Kirk K., Horner H. A., Elford B. C., Ellory J. C., Newbold C. I. Transport of diverse substrates into malaria-infected erythrocytes via a pathway showing functional characteristics of a chloride channel. J Biol Chem. 1994 Feb 4;269(5):3339–3347. [PubMed] [Google Scholar]
  14. Kirk K., Horner H. A. In search of a selective inhibitor of the induced transport of small solutes in Plasmodium falciparum-infected erythrocytes: effects of arylaminobenzoates. Biochem J. 1995 Nov 1;311(Pt 3):761–768. doi: 10.1042/bj3110761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kirk K., Horner H. A., Kirk J. Glucose uptake in Plasmodium falciparum-infected erythrocytes is an equilibrative not an active process. Mol Biochem Parasitol. 1996 Nov 25;82(2):195–205. doi: 10.1016/0166-6851(96)02734-x. [DOI] [PubMed] [Google Scholar]
  16. Kirk K., Horner H. A. Novel anion dependence of induced cation transport in malaria-infected erythrocytes. J Biol Chem. 1995 Oct 13;270(41):24270–24275. doi: 10.1074/jbc.270.41.24270. [DOI] [PubMed] [Google Scholar]
  17. Kirk K., Poli de Figueiredo C. E., Elford B. C., Ellory J. C. Effect of cell age on erythrocyte choline transport: implications for the increased choline permeability of malaria-infected erythrocytes. Biochem J. 1992 Apr 15;283(Pt 2):617–619. doi: 10.1042/bj2830617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kirk K., Wong H. Y., Elford B. C., Newbold C. I., Ellory J. C. Enhanced choline and Rb+ transport in human erythrocytes infected with the malaria parasite Plasmodium falciparum. Biochem J. 1991 Sep 1;278(Pt 2):521–525. doi: 10.1042/bj2780521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Maguire P. A., Prudhomme J., Sherman I. W. Alterations in erythrocyte membrane phospholipid organization due to the intracellular growth of the human malaria parasite, Plasmodium falciparum. Parasitology. 1991 Apr;102(Pt 2):179–186. doi: 10.1017/s0031182000062466. [DOI] [PubMed] [Google Scholar]
  20. Saliba K. J., Horner H. A., Kirk K. Transport and metabolism of the essential vitamin pantothenic acid in human erythrocytes infected with the malaria parasite Plasmodium falciparum. J Biol Chem. 1998 Apr 24;273(17):10190–10195. doi: 10.1074/jbc.273.17.10190. [DOI] [PubMed] [Google Scholar]
  21. Singh S., Puri S. K., Singh S. K., Srivastava R., Gupta R. C., Pandey V. C. Characterization of simian malarial parasite (Plasmodium knowlesi)-induced putrescine transport in rhesus monkey erythrocytes. A novel putrescine conjugate arrests in vitro growth of simian malarial parasite (Plasmodium knowlesi) and cures multidrug resistant murine malaria (Plasmodium yoelii) infection in vivo. J Biol Chem. 1997 May 23;272(21):13506–13511. doi: 10.1074/jbc.272.21.13506. [DOI] [PubMed] [Google Scholar]
  22. Upston J. M., Gero A. M. Parasite-induced permeation of nucleosides in Plasmodium falciparum malaria. Biochim Biophys Acta. 1995 Jun 14;1236(2):249–258. doi: 10.1016/0005-2736(95)00055-8. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES