Resistance of glucose-6-phosphate dehydrogenase deficiency to malaria: Effects of fava bean hydroxypyrimidine glucosides on Plasmodium falciparum growth in culture and on the phagocytosis of infected cells

Parasitology

Volumn 113, Issue 1, 1996, Pages 7-18

  Ginsburg, H ^a   Atamna, H ^a   Shalmiev, G ^a   Kanaani, J ^a   Krugliak, M ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Convicine; Glucose 6 phosphate dehydrogenase deficiency; Hexose monophosphate; Phagocytosis; Plasmodium falciparum; Shunt activity; Vicine

Indexed keywords

GLUCOSE 6 PHOSPHATASE; GLUCOSIDE;

ANIMAL EXPERIMENT; ARTICLE; BEAN; CONTROLLED STUDY; ENZYME DEFICIENCY; ERYTHROCYTE; FEEDING BEHAVIOR; GENETIC POLYMORPHISM; GROWTH INHIBITION; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; NONHUMAN; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

ANIMALIA; FAVA; PHASEOLUS (ANGIOSPERM); PLASMODIUM FALCIPARUM; VICIA FABA;

EID: 0029899980     PISSN: 00311820     EISSN: None     Source Type: Journal    
DOI: 10.1017/s0031182000066221     Document Type: Article

References (54)

1. ALLRED, D. R. (1495). Immune evasion by Babesia bovis and Plasmodium falciparum: Cliff-dwellers of the parasite world. Parasitology Today 11, 100 5.
2. ARBID, M. S. S. & MARQUARDT, R. R. (1986). Effects of intraperitoneally injected vicine and convicine on the rat: induction of favism-like signs. Journal of Science Food and Agriculture 37, 539-47.
3. ARESE, P. (1982). Favism a natural model for the study of hemolytic mechanisms. Reviews in Pure and Applied Pharmacological Sciences 3, 123-83.
4. ARESE, P., BOSIA, A. & NAITANA, A. (1981). Effect of divicine and isouramil on red cell metabolism in normal and G6PD-deficient (Mediterranean variant) subjects. In The Red Cell, Fifth Ann Arbor Conference (ed. Brewer, G.), pp. 725 744. New York: Alan Liss.
5. ARESE, P. & DE FLORA, A. (1990). Pathophysiology of hemolysis in glucose-6-phosphate dehydrogenase deficiency. Seminars in Hematology 27, 1-40.
6. ATAMNA, H. & GINSBURG, H. (1994). The redox status of malaria-infected erythrocytes: An overview with an emphasis on unresolved problems. Parasite 1, 5 13.
7. ATAMNA, H., PASCARMONA, G. & GINSBURG, H. (1994). Hexose-monophosphate shunt activity in intact Plasmodium falciparum infected erythrocytes and in free parasites. Molecular and Biochemical Parasitology 67, 79-89.
8. BENATTI, U., GUIDA, L., GRASSO, M., TONETTI, M., DE FLORA, A. & WINTERBOURN, C. C. (1985). Hexose monophosphate shunt-stimulated reduction of methemoglobin by divicine. Archives of Biochemistry and Biophysics 242, 549-56.
9. BEUITLER, E. (1994). G6PD deficiency. Blood 84, 3613-36.
10. BOSMAN, B. (1971). Red cell hydrolases: glycosidase activities in human erythrocyte plasma membrane. Journal of Membrane Biology 4, 113-23.
11. CHEVION, M., NAVOK, T., GLASER, G. & MAGER, J. (1982). The chemistry of favism-inducing compounds. The properties of isouramil and divicine and their reaction with glutathione. European Journal of Biochemistry 127, 405-9.
12. CLARK, I. A. & COWDEN, W. B. (1985). Antimalarials. In Oxidative Stress (ed. Sies, H.), pp. 131-149. London: Academic Press.
13. CLARK, I. A., COWDEN, W. B., HUNT, N. H., MAXWELL, L. & MACKIE, E. (1984). Activity of divicine in Plasmodium vinckei-infected mice has implications for treatment of favism and epidemiology of G-6-PD deficiency. British Journal of Haematology 57, 479-87.
14. D'AQUINO, M., GAETANI, s. & SPADONI, M. (1983). Effect of factors of Favism on the protein and lipid components of rat erythrocyte membrane. Biochimica et Biophysica Acta 731, 161-7.
15. DAVIDSON, W. D. & TANAKA, K. R. (1972). Factors affecting pentose pathway activity in human red cells. British Journal of Haematology 23, 371.
16. DESJARDINS, R. S., CANFIELD, C. J., HAYNES, J. D. & CHULAY, J. D. (1979). Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrobial Agents and Chemotherapy 16, 710-18.
17. ECKMAN, J. R. & EATON, J. W. (1979). Dependence of plasmodial glutathione metabolism on the host cell. Nature, London 278, 754-6.
18. FRIEDMAN, M. J. (1979). Oxidant damage mediates variant red cell resistance to malaria. Nature, London 280, 245-7.
19. GINSBURG, H. (1994). Transport pathways in the malaria-infected erythrocyte - their characterization and their use as potential targets for chemotherapy. Biochemical Pharmacology 48, 1847-56.
20. GINSBURG, H., KUTNER, S., ZANGVILL, M. & CABANTCHIK, Z. I. (1986). Selectivity properties of pores induced in host erythrocyte membranes by Plasmodium falciparum: Effect of parasite maturation. Biochimica et Biophysica Acta 861, 194-6.
21. GOLENSER, J., MILLER, J., SPIRA, D., NAVOK, T. & CHEVION, M. (1983). Inhibitor effect of fava bean component on the in vitro development of Plasmodium falciparum in normal and glucose-6-phosphate dehydrogenase deficient erythrocytes. Biochemistry 61, 507-10.
22. GOLENSER, J., MILLER, J., SPIRA, D., KOSOWER, N., VANDE, WAA, J. & JENSEN, J. (1988). Inhibition of the intraerythrocytic development of Plasmodium falciparum in glucose-6-phosphate dehydrogenase deficient erythrocytes is enhanced by oxidants and crisis form factor. Tropical Medicine and Parasitology 39, 273-6.
23. GREENE, L. S. (1993). G6PD deficiency as protection against falciparum malaria: an epidemiologic critique of population and experimental studies. Yearbook of Physical Anthropology 36, 153-78.
24. HEGAZY, M. & MARQUARDT, R. (1984). Metabolism of vicine and convicine in rat tissues: Absorption and excretion patterns and sites of hydrolysis. Journal of Science Food and Agriculture 35, 139-46.
25. HUHEEY, J. E. & MARTIN, D. L. (1975). Malaria, favism and glucose-6-phosphate dehydrogenase deficiency. Experientia 31, 1145-7.
26. HUNT, N. H. & STOCKER, R. (1990). Oxidative stress and the redox status of malaria-infected erythrocytes. Blood Cells 16, 499-526.
27. JENSEN, J. B. (1978). Concentration from continuous culture of erythrocytes infected with trophozoites and schizonts of Plasmodium falciparum. American Journal of Tropical Medicine and Hygiene 27, 1274-6.
28. KAMCHONWONGPAISAN, S., BUNYARATVEJ, A., WANACHIWANAWIN, W. & YUTHAVONG, T. (1989). Susceptibility to hydrogen peroxide of Plasmodium falciparum infecting glucose-6-phosphate dehydrogenase-deficient erythrocytes. Parasitology 99, 171-4.
29. KANAANI, J. & GINSBURG, H. (1989). Metabolic interconnection between the human malarial parasite Plasmodium falciparum and its host erythrocyte: Regulation of ATP levels by means of an adenylate translocator and adenylate kinase. Journal of Biological Chemistry 264, 3194-9.
30. KRUATRACHUE, M., KLONGKUMNUANHARA, K. & HARINASUTA, C. (1966). Infection rates of malarial parasites in red blood cells with normal and deficient glucose-6-phosphate dehydrogenase. Lancet 1(434), 404-6.
31. KURDI-HAIDAR, B. & LUZZATTO, L. (1990). Expression and characterization of glucose-6-phosphate dehydrogenase of Plasmodium falciparum. Molecular and Biochemical Parasitology 41, 83-92.
32. KUTNER, S., BREUER, W. V., GINSBURG, H., ALEY, S. B. & CABANTCHIK, Z. I. (1995). Characterization of permeation pathways in the plasma membrane of human erythrocytes infected with early stages of Plasmodium falciparum: Association with parasite development. Journal of Cell Physiology 125, 521-7.
33. KWIATKOWSKI, D. & NOWAK, M. (1991). Periodic and chaotic host parasite interactions in human malaria. Proceedings of the National Academy of Sciences, USA 88, 5111-13.
34. LAMBROS, C. & VANDERBERG, J. P. (1979). Synchronization of Plasmodium falciparum erythrocytic stages in culture. Journal of Parasitology 65, 418-20.
35. LOMBARDO, A., CAIMI, L., MARCHESINI, S., GOI, G. C. & TETTAMANTI, G. (1980). Enzymes of lysosomal origin in human plasma and serum: Assay conditions and parameters influencing the assay. Clinica Chimica Acta 108, 337-46.
36. LUZZATTO, L., USANGA, E. & REDDY, S. (1969). Glucose-6-phosphate dehydrogenase deficient red cells: Resistance to infection by malarial parasites. Science 164, 839-41.
37. LUZZATTO, L., SODEINDE, O. & MARTINI, G. (1983). Genetic variation in the host and adaptive phenomena in Plasmodion falciparum infection. In Malaria and the Red Cell, (ed. Evered, D. & Whelan, J.) pp. 159-173. London: Ciba Foundation Symposium No. 94, Pitman.
38. LUZZATTO, L. & BATTISTUZZI, G. (1985). Glucosc-6-phosphate dehydrogenase. Advances in Medical Genetics 14, 217-329.
39. LUZZATTO, L. & MEHTA, A. (1989). Glucose-6-phosphate deficiency. In The Metabolic Basis of Inherited Diseases (ed. Scriver, C. R., Baudet, A. L., Sly, W. S. & Valle, D.), pp. 2237 2265. New York: McGraw-Hill.
40. MAGER, J., GLASER, G., RAZIN, A., IZAK, G., BIEN, S. & NOAM, M. (1965). Metabolic effects of pyrimidines derived from fava bean glycosides on human erythrocytes deficient in glucose-6-phosphate dehydrogenase. Biochemical and Biophysical Research Communications 20, 235-4.
41. MARQUARDT, R. R. & FROHLICH, A. A. (1981). Rapid reversed-phase high-performance liquid chromatographic method for the quantitation of vicine, convicine and related compounds. Journal of Chromatography 208, 373 9.
42. MAVELLI, I., CIRIOLO, M., ROSSI, L., MELONI, T., FORTELEONI, G., DE FLORA, A., BENATTI, U., MORELLI, A. & ROTILIO, G. (1984). Favism: a hemolytic disease associated with increased superoxide dismutase and decreased glutathione peroxidase activities in red blood cells. EMBO Journal 139, 13 18.
43. MILLER, J., GOLENSER, J., SPIHA, D. & KOSOWER, N. (1984). Plasmodium falciparum. Thiol status and growth in normal and glucose-6-phosphate dehydrogenase deficient human erythrocytes. Experimental Parasitology 57, 239-47.
44. OCKENHOUSE, C., SCHULMAN, S. & SHEAR, H. (1984). Induction of crisis forms in the human malaria parasite Plasmodium falciparum by gamma-interferon-activated, monocyte-derived macrophages, Journal of Immunology 133, 1601 8.
45. OSGOOD, E. E. & BROOKE, J. H. (1955). Continuous tissue culture of leukocytes from human leukemic blood by application of "gradient" principle. Blood 51, 1010 22.
46. PESCARMONA, G., BOSIA, A., ARESE, P., SARTORI, M. & GHIGO, D. (1982). A simplified method for the pentose phosphate pathway assay in red cells. International Journal of Biochemistry 14, 243 5.
47. ROTH, E. F., RAVENTOS, S., RINALDI, A. & NAGEL, R. L. (1983). Glucose-6-phosphate dehydrogenase deficiency inhibits in vitro growth of Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 80, 298 302.
48. ROTH, E. F. & SCHULMAN, S. (1988). The adaptation of Plasmodium falciparum to oxidative stress in G6PD deficient human erythrocytes. British Journal of Haematology 70, 363 7.
49. THORBURN, D. R. & KUCHEL, P. W. (1985). Regulation of the human erythrocyte hexose-monophosphate shunt under conditions of oxidative stress. A study using NMR spectroscopy, a kinetic isotope effect, a reconstituted system and computer simulation. European Journal of Biochemistry 150, 371 86.
50. TURRINI, F., GINSBURG, H., BUSSOLINO, F., PESCARMONA, G. P., SERRA, M. V. & ARESE, P. (1992). Phagocytosis of Plasmodium falciparum -infected human red blood cells by human monocytes involvement of immune and nonimmune determinants and dependence on parasite development stage. Blood 80, 801 8.
51. USANGA, E. & LUZZATTO, L. (1985). Adaptation of Plasmodium falciparum to glucose-6-phosphate dehydrogenase-deficient host red cells by production of parasite encoded enzyme, Nature, London 313, 793 5.
52. VENNERSTROM, J. L. & EATON, J. W. (1988). Oxidants, oxidant drugs, and malaria. Journal of Medicinal Chemistry 31, 1269 77.
53. WINTERBOURN, C. C., BENATTI, U. & DE FLORA, A. (1986). Contributions of superoxide, hydrogen peroxide, and transition metal ions to auto-oxidation of the favism-inducing pyrimidme aglycone, divicine, and its reactions with haemoglobin. Biochemical Pharmacology 35, 2009 15.
54. WINTERBOURN, C. C., COWDEN, W. B. & SUTTON, H. (1989). Auto-oxidation of dialuric acid, divicine and isouramil. Superoxide dependent and independent mechanisms. Biochemical Pharmacology 38, 611 18.