Inherited glutathione reductase deficiency and Plasmodium falciparum malaria - A case study

PLoS ONE

Volumn 4, Issue 10, 2009, Pages

  Gallo, Valentina ^a   Schwarzer, Evelin ^a   Rahlfs, Stefan ^b   Schirmer, R Heiner ^c   van Zwieten, Rob ^d   Roos, Dirk ^d   Arese, Paolo ^a   Becker, Katja ^b  

^a UNIVERSITY OF TURIN   (Italy)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

APOPROTEIN; ARTEMISININ; CHLOROQUINE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTATHIONE REDUCTASE; IMMUNOGLOBULIN G; METHYLENE BLUE; NITROPRUSSIDE SODIUM; PARAQUAT; PENTOSE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; COMPLEMENT COMPONENT C3; GLUTATHIONE;

ADULT; ANTIOXIDANT ACTIVITY; ARTICLE; CELL GROWTH; CELL INVASION; CONTROLLED STUDY; DRUG SENSITIVITY; GENE MUTATION; HOMOZYGOSITY; HUMAN; INHERITANCE; MALARIA; NONHUMAN; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM; PROTEIN DEFICIENCY; VIRUS CELL INTERACTION; CASE CONTROL STUDY; CASE REPORT; DRUG EFFECT; DRUG RESISTANCE; ENZYMOLOGY; FEMALE; GENETIC PREDISPOSITION; GENETICS; HOMOZYGOTE; IC 50; MALARIA FALCIPARUM; METABOLISM; MIDDLE AGED;

PLASMODIUM FALCIPARUM;

CASE-CONTROL STUDIES; COMPLEMENT C3; DRUG RESISTANCE; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GLUTATHIONE; GLUTATHIONE REDUCTASE; HOMOZYGOTE; HUMANS; IMMUNOGLOBULIN G; INHIBITORY CONCENTRATION 50; MALARIA, FALCIPARUM; MIDDLE AGED; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM;

EID: 70350234635     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007303     Document Type: Article

References (67)

1. Beutler E (2001a) Composition of the erythrocyte. In: Beutler E, Lichtman MA, Coller BS, Kipps TJ, Seligsohn U, eds. Williams Hematology, 6th edition. New York: McGraw-Hill. pp 289-293.
2. Beutler E (2001b) Energy metabolism and maintenance of erythrocytes. In: Beutler E, Lichtman MA, Coller BS, Kipps TJ, Seligsohn U, eds. Williams Hematology, 6th edition. New York: McGraw-Hill. pp 319-332.
3. Becker K, Rahlfs S, Nickel C, Schirmer RH (2003) Glutathione-functions and metabolism in the malarial parasite Plasmodium falciparum. Biol Chem 384: 551-566.
4. Becker K, Tilley L, Vennerstrom J, Roberts F, Rogerson S, Ginsburg H (2004) Oxidative stress in malaria parasite-infected erythrocytes: host-parasite interactions. Int J Parasitol 34: 163-189.
5. Becker K, Koncarevic S, Hunt NH (2005) Oxidative stress and antioxidant defense in malarial parasites. In: Sherman IW, ed. Molecular Approaches to Malaria. Herndon: American Society of Microbiology Press. pp 365-383.
6. Atamna H, Ginsburg H (1995) Heme degradation in the presence of glutathione. A proposed mechanism to account for the high levels of non-heme iron found in the membranes of hemoglobinopathic red blood cells. J Biol Chem 270: 24876-24883.
7. Akoachere M, Iozef R, Rahlfs S, Deponte M, Mannervik B, et al. (2005) Characterization of the glyoxalases of the malarial parasite Plasmodium falciparum and comparison with their human counterparts. Biol Chem 386: 41-45.
8. Hiller N, Fritz-Wolf K, Deponte M, Wende W, Zimmermann H, et al. (2006) Plasmodium falciparum glutathione S-transferase-structural and mechanistic studies on ligand binding and enzyme inhibition. Protein Sci 15: 281-289.
9. Krauth-Siegel R, Bauer H, Schirmer RH (2005) Dithiol proteins as guardians of the intracellular redox milieu in parasites: old and new drug targets in trypanosomes and malaria-causing plasmodia. Angew Chem Int Ed Engl 44: 690-715.
10. Buchholz K, Mwongela Mailu B, Heiner Schirmer R, Becker K (2007) Structure-Based Drug Development Against Malaria. Frontiers in Drug Design & Discovery 3: 225-255.
11. Rahlfs S, Becker K (2006) Interference with redox-active enzymes as a basis for the design of antimalarial drugs. Mini Rev Med Chem 6: 163-76.
12. Beutler E (2001c) Glucose-6-phosphate dehydrogenase deficiency and other red cell enzyme abnormalities. In: Beutler E, Lichtman MA, Coller BS, Kipps TJ, Seligsohn U, eds. Williams Hematology, 6th edition. New York: McGraw-Hill. pp 527-545.
13. Luzzatto L, Mehta A, Vulliamy T (2001) Glucose-6-phosphate dehydrogenase deficiency. In: Scriver CR, Beaudet RAL, Sly WS, Vallet D, eds. The Metabolic and Molecular Bases of Inherited Disease. New York: McGraw-Hill. pp 4517-4553.
14. Greene L (1993) G6PD deficiency as protection against falciparum malaria: an epidemiologic critique of population and experimental studies. Yearb Phys Anthropol 36: 26.
15. Nkhoma ET, Poole C, Vannappagari V, Hall SA, Beutler E (2009) The global prevalence of glucose-6-phosphate dehydrogenase deficiency: A systematic review and meta-analysis. Blood Cells Mol Dis, pub ahead of print, Feb. 2009.
16. Beutler E (1996) G6PD: population genetics and clinical manifestations. Blood Rev 10: 45-52.
17. Loos H, Roos D, Weening R, Houwerzijl J (1976) Familial deficiency of glutathione reductase in human blood cells. Blood 48: 53-62.
18. Kamerbeek N, van Zwieten R, de Boer M, Morren G, Vuil H, et al. (2007) Molecular basis of glutathione reductase deficiency in human blood cells. Blood 109: 3560-3566.
19. Ruwende C, Hill A (1998) Glucose-6-phosphate dehydrogenase deficiency and malaria. J Mol Med 76: 581-588.
20. Cappadoro MG, Giribaldi E, O'Brien F, Turrini F, Mannu D, et al. (1998) Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood 92: 2527-2534.
21. Arese P, Turrini F, Schwarzer E (2005) Band 3/complement-mediated recognition and removal of normally senescent and pathological human erythrocytes. Cell Physiol Biochem 16: 133-146.
22. Ayi K, Turrini F, Piga A, Arese P (2004) Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood 104: 3364-3371.
23. Ayi K, Min-Oo G, Serghides L, Crockett M, Kirby-Allen M, et al. (2008) Pyruvate kinase deficiency and malaria. N Engl J Med 358: 1805-1810.
24. Williams T (2006) Human red blood cell polymorphisms and malaria. Curr Opin Microbiol 9: 388-394.
25. Roberts DJ, Harris T, Williams T (2004) The influence of inherited traits on malaria infection. In: Bellamy R, ed. Susceptibility to Infectious Diseases: the Importance of Host Genetics. Cambridge: Cambridge University Press. pp 139-184.
26. Min-Oo G, Gros P (2005) Erythrocyte variants and the nature of their malaria protective effect. Cell Microbiol 7: 753-763.
27. Arie T, Fairhurst R, Brittain N, Wellems T, Dvorak J (2005) Hemoglobin C modulates the surface topography of Plasmodium falciparum-infected erythrocytes. J Struct Biol 150: 163-169.
28. Tokumasu F, Fairhurst R, Ostera G, Brittain N, Hwang J, et al. (2005) Band 3 modifications in Plasmodium falciparum-infected AA and CC erythrocytes assayed by autocorrelation analysis using quantum dots. J Cell Sci 118: 1091-1098.
29. Chotivanich K, Udomsangpetch R, Pattanapanyasat K, Chierakul W, Simpson J, et al. (2002) Hemoglobin E: a balanced polymorphism protective against high parasitemias and thus severe P. falciparum malaria. Blood 100: 1172-1176.
30. Turrini F, Ginsburg H, Bussolino F, Pescarmona GP, Serra MV, 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 developmental stage. Blood 80: 801-808).
31. Schwarzer E, Turrini F, Ulliers D, Giribaldi G, Ginsburg H, et al. (1992) Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. J Exp Med 176: 1033-1041.
32. Hänscheid T, Egan T, Grobusch M (2007) Haemozoin: from melatonin pigment to drug target, diagnostic tool, and immune modulator. Lancet Infect Dis 7: 675-685.
33. Fiori P, Rappelli P, Mirkarimi S, Ginsburg H, Cappuccinelli P, et al. (1993) Reduced microbicidal and anti-tumour activities of human monocytes after ingestion of Plasmodium falciparum-infected red blood cells. Parasite Immunol 15: 647-655.
34. Schwarzer E, Alessio M, Ulliers D, Arese P (1998) Phagocytosis of the malarial pigment, hemozoin, impairs expression of major histocompatibility complex class II antigen, CD54, and CD11c in human monocytes. Infect Immun 66: 1601-1606.
35. Scorza T, Magez S, Brys L, De Baetselier P (1999) Hemozoin is a key factor in the induction of malaria-associated immunosuppression. Parasite Immunol 21: 545-554.
36. Skorokhod O, Alessio M, Mordmuller B, Arese P, Schwarzer E (2004) Hemozoin (malarial pigment) inhibits differentiation and maturation of human monocyte-derived dendritic cells: a peroxisome proliferator-activated receptorgamma mediated effect. J Immunol 173: 4066-4074.
37. Chakravorty S, Hughes K, Craig A (2008) Host response to cytoadherence in Plasmodium falciparum. Biochem Soc Trans 36: 221-228.
38. Cholera R, Brittain N, Gillrie M, Lopera-Mesa T, Diakité S, et al. (2008) Impaired cytoadherence of Plasmodium falciparum-infected erythrocytes containing sickle hemoglobin. Proc Natl Acad Sci USA 105: 991-996.
39. Fairhurst R, Wellems T (2006) Modulation of malaria virulence by determinants of Plasmodium falciparum erythrocyte membrane protein-1 display. Curr Opin Hematol 13: 124-130.
40. Fairhurst R, Baruch D, Brittain N, Ostera G, Wallach J, et al. (2005) Abnormal display of PfEMP-1 on erythrocytes carrying haemoglobin C may protect against malaria. Nature 435: 1117-1121.
41. Arese P, De Flora A (1990) Pathophysiology of hemolysis in glucose-6-phosphate dehydrogenase deficiency. Semin Hematol 27: 1-40.
42. Komaki-Yasuda K, Kawazu S, Kano S (2003) Disruption of the Plasmodium falciparum 2-Cys peroxiredoxin gene renders parasites hypersensitive to reactive oxygen and nitrogen species. FEBS Lett 547: 140-144.
43. Schulz G, Schirmer RH, Pai E (1982) FAD-binding site of glutathione reductase. J Mol Biol 160: 287-308.
44. Ahmed F, Khan M, Banu C, Qazi M, Akhtaruzzaman M (2008) The coexistence of other micronutrient deficiencies in anaemic adolescent schoolgirls in rural Bangladesh. Eur J Clin Nutr 62: 365-372.
45. Rohner F, Zimmermann M, Wegmueller R, Tschannen A, Hurrell R (2007) Mild riboflavin deficiency is highly prevalent in school-age children but does not increase risk for anaemia in Côte d'Ivoire. Br J Nutr 97: 970-976.
46. Das B, Das D, Satpathy R, Patnaik J, Bose T (1988) Riboflavin deficiency and severity of malaria. Eur J Clin Nutr 42: 277-283.
47. Kaikai P, Thurnham D (1983) The influence of riboflavin deficiency on Plasmodium berghei infection in rats. Trans R Soc Trop Med Hyg 77: 680-686.
48. Anderson B, Giubert M, Perry G, Salsini G, Casadio I, et al. (1993) Low red blood cell glutathione reductase and pyridoxine phosphate oxidase activities not related to dietary riboflavin: selection by malaria? Am J Clin Nutr 57: 666-672.
49. Anderson B, Scattoni M, Perry G, Galvan P, Giuberti M, et al. (1994) Is the flavin-deficient red blood cell common in Maremma, Italy, an important defense against malaria in this area? Am J Hum Genet 55: 975-980.
50. Anderson B, Corda L, Perry G, Pilato D, Giuberti M, et al. (1995) Deficiency of two red-cell flavin enzymes in a population in Sardinia: was glutathione reductase deficiency specifically selected for by malaria? Am J Hum Genet 57: 674-681.
51. Siniscalco M, Bernini L, Filippi G, Latte B, Meera-Khan P, et al. (1966) Population genetics of haemoglobin variants, thalassaemia and glucose-6-phosphate dehydrogenase deficiency, with particular reference to the malaria hypothesis. Bull World Health Organ 34: 379-393.
52. El-Hazmi M, Warsy A (1985) Glutathione reductase deficiency in association with sickle cell and thalassaemia genes in Saudi populations. Hum Hered 35: 326-332.
53. Anderson B, Perry G, Clements J, Studds C, Fashola R, et al. (1989) Genetic and other influences on red-cell flavin enzymes, pyridoxine phosphate oxidase and glutathione reductase in families with beta-thalassaemia. Eur J Haematol 42: 354-360.
54. Clements J, Anderson B, Perry G (1981) Low red cell activity of pyridoxine (pyridoxamine) phosphate oxidase and glutathione reductase associated with thalassaemia. Biomedicine 34: 119-123.
55. Varma R, Mankad V, Phelps D, Jenkins L, Suskind R (1983) Depressed erythrocyte glutathione reductase activity in sickle cell disease. Am J Clin Nutr 38: 884-887.
56. Zhang YA, König I, Schirmer RH (1988) Glutathione reductase-deficient erythrocytes as host cells of malarial parasites. Biochem Pharmacol 37: 861-865.
57. Frischer H, Ahmad T (1977) Severe generalized glutathione reductase deficiency after antitumor chemotherapy with BCNU [1,3-bis(chloroethyl)-1-nitrosourea]. J Lab Clin Med 89: 1080-1091.
58. Trager W, Jensen J (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
59. Lambros C, Vanderberg J (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65: 418-420.
60. Becker K, Gui M, Traxler A, Kirsten C, Schirmer RH (1994) Redox processes in malaria and other parasitic diseases. Determination of intracellular glutathione. Histochemistry 102: 389-395.
61. Nordhoff A, Bucheler U, Werner D, Schirmer RH (1993) Folding of the four domains and dimerization are impaired by the Gly446->Glu exchange in human glutathione reductase. Implications for the design of antiparasitic drugs. Biochemistry 32: 4060-4066.
62. Desjardins R, Canfield C, Haynes J, Chulay J (1979) Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob Agents Chemother 16: 710-718.
63. Fivelman Q, Adagu I, Warhurst D (2004) Modified fixed-ratio isobologram method for studying in vitro interactions between atovaquone and proguanil or dihydroartemisinin against drug-resistant strains of Plasmodium falciparum. Antimicrob Agents Chemother 48: 4097-4102.
64. Steck T, Weinstein R, Straus J, Wallach D (1970) Inside-out red cell membrane vesicles: preparation and purification. Science 168: 255-257.
65. Schwarzer E, Turrini F, Arese P (1994) A luminescence method for the quantitative determination of phagocytosis of erythrocytes, of malaria-parasitized erythrocytes and of malarial pigment. Br J Haematol 88: 740-745.
66. Lutz HU (2004) Innate immune and non-immune mediators of erythrocyte clearance. Cell Mol Biol 50: 107-116.
67. Skorokhod O, Schwarzer E, Ceretto M, Arese P (2007) Malarial pigment haemozoin, IFN-gamma, TNF-alpha, IL-1beta and LPS do not stimulate expression of inducible nitric oxide synthase and production of nitric oxide in immuno-purified human monocytes. Malar J 6: 73.