Glutathione export from human erythrocytes and Plasmodium falciparum malaria parasites

Biochemical Journal

Volumn 448, Issue 3, 2012, Pages 389-400

  Barrand, Margery A ^a   Winterberg, Markus ^b   Ng, Frances ^a   Nguyen, Mai ^a   Kirk, Kiaran ^b   Hladky, Stephen B ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Erythrocyte membrane; Glutathione export; Malaria parasite; Multidrug resistance protein (MRP); New permeability pathway (NPP); Reduced and oxidized glutathione

Indexed keywords

FUROSEMIDE; GLUTATHIONE; GLUTATHIONE DISULFIDE; MULTIDRUG RESISTANCE PROTEIN; VERLUKAST;

ARTICLE; CELL TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DERIVATIZATION; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; NONHUMAN; OXIDATION; PARASITE ISOLATION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CELLS, CULTURED; ERYTHROCYTES; GLUTATHIONE; HUMANS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; OXIDATION-REDUCTION; PLASMODIUM FALCIPARUM; PROPIONATES; QUINOLINES;

MAMMALIA; PLASMODIUM FALCIPARUM;

EID: 84870003252     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121050     Document Type: Article

References (63)

1. Meister, A. and Anderson, M. E. (1983) Glutathione. Annu. Rev. Biochem. 52, 711-760 (Pubitemid 13030692)
2. Meister, A. (1989) A brief history of glutathione and a survey of its metabolism and functions. In Glutathione: Chemical, Biochemical, and Medical Aspects (Dolphin, D., Avramovic, O. and Poulson, R., eds), pp. 1-48, John Wiley & Sons, New York
3. Ballatori, N., Krance, S. M., Notenboom, S., Shi, S. J., Tieu, K. and Hammond, C. L. (2009) Glutathione dysregulation and the etiology and progression of human diseases. Biol. Chem. 390, 191-214
4. Ballatori, N., Krance, S. M., Marchan, R. and Hammond, C. L. (2009) Plasma membrane glutathione transporters and their roles in cell physiology and pathophysiology. Mol. Aspects Med. 30, 13-28
5. van Haaften, R. I. M., Haenen, G., Evelo, C. T. A. and Bast, A. (2003) Effect of vitamin E on glutathione-dependent enzymes. Drug Metab. Rev. 35, 215-253 (Pubitemid 37048296)
6. Ogasawara, Y., Komiyama, M., Funakoshi, M. and Ishii, K. (2010) Disruption of glutathione homeostasis causes accumulation of S-glutathionyl proteins in response to exposure to reactive oxygen species in human erythrocytes. Biol. Pharm. Bull. 33, 1925-1931
7. Vennerstrom, J. L. and Eaton, J. W. (1988) Oxidants, oxidant drugs, and malaria. J. Med. Chem. 31, 1269-1277
8. Ginsburg, H. and Atamna, H. (1994) The redox status of malaria-infected erythrocytes: an overview with an emphasis on unresolved problems. Parasite 1, 5-13
9. Becker, K., Tilley, L., Vennerstrom, J. L., Roberts, D., Rogerson, S. and Ginsburg, H. (2004) Oxidative stress in malaria parasite-infected erythrocytes: host-parasite interactions. Int. J. Parasitol. 34, 163-189 (Pubitemid 38229822)
10. Fu, Y., Tilley, L., Kenny, S. and Klonis, N. (2010) Dual labeling with a far red probe permits analysis of growth and oxidative stress in P. falciparum-infected erythrocytes. Cytometry, Part A 77A, 253-263
11. Atamna, H. and Ginsburg, H. (1997) The malaria parasite supplies glutathione to its host cell: investigation of glutathione transport and metabolism in human erythrocytes infected with Plasmodium falciparum. Eur. J. Biochem. 250, 670-679 (Pubitemid 28022483)
12. Raftos, J. E., Dwarte, T. M., Luty, A. and Willcock, C. J. (2006) Direct measurement of the rate of glutathione synthesis in 1-chloro-2,4-dinitrobenzene treated human erythrocytes. Redox Rep. 11, 9-14 (Pubitemid 44111118)
13. Srivastava, S. K. and Beutler, E. (1969) The transport of oxidized glutathione from human erythrocytes. J. Biol. Chem. 244, 9-16
14. Lunn, G., Dale, G. L. and Beutler, E. (1979) Transport accounts for glutathione turnover in human erythrocytes. Blood 54, 238-244 (Pubitemid 9228103)
15. Prchal, J., Srivastava, S. K. and Beutler, E. (1975) Active transport of GSSG from reconstituted erythrocyte ghosts. Blood 46, 111-117
16. Kondo, T., Dale, G. L. and Beutler, E. (1980) Glutathione transport by inside-out vesicles from human erythrocytes. Proc. Natl. Acad. Sci. U.S.A. 77, 6359-6362 (Pubitemid 11219144)
17. Kondo, T., Dale, G. L. and Beutler, E. (1995) Thiol transport from human red blood cells. Methods Enzymol. 252, 72-82
18. Leier, I., Jedlitschky, G., Buchholz, U., Center, M., Cole, S. P. C., Deeley, R. G. and Keppler, D. (1996) ATP-dependent glutathione disulphide transport mediated by the MRP gene-encoded conjugate export pump. Biochem. J. 314, 433-437 (Pubitemid 26075650)
19. Pulaski, L., Jedlitschky, G., Leier, I., Buchholz, U. and Keppler, D. (1996) Identification of the multidrug-resistance protein (MRP) as the glutathione-S-conjugate export pump of erythrocytes. Eur. J. Biochem. 241, 644-648 (Pubitemid 26356857)
20. Klokouzas, A., Barrand, M. A. and Hladky, S. B. (2001) Effects of clotrimazole on transport mediated by multidrug resistance associated protein 1 (MRP1) in human erythrocytes and tumour cells. Eur. J. Biochem. 268, 6569-6577 (Pubitemid 34014764)
21. Klokouzas, A., Wu, C. P., Van Veen, H. W., Barrand, M. A. and Hladky, S. B. (2003) cGMP and glutathione-conjugate transport in human erythrocytes: the roles of the multidrug resistance-associated proteins, MRP1, MRP4 and MRP5. Eur. J. Biochem. 270, 3696-3708 (Pubitemid 37123241)
22. Wu, C. P., Klokouzas, A., Hladky, S. B., Ambudkar, S. V. and Barrand, M. A. (2005) Interactions of mefloquine with ABC proteins, MRP1 (ABCC1) and MRP4 (ABCC4) that are present in human red cell membranes. Biochem. Pharmacol. 70, 500-510 (Pubitemid 40978539)
23. Ellison, I. and Richie, Jr, J. P. (2012) Mechanisms of glutathione disulfide efflux from erythrocytes. Biochem. Pharmacol. 83, 164-169
24. Giustarini, D., Milzani, A., Dalle-Donne, I. and Rossi, R. (2008) Red blood cells as a physiological source of glutathione for extracellular fluids. Blood Cells Mol. Dis. 40, 174-179 (Pubitemid 351221382)
25. Ayi, K., Cappadoro, M., Branca, M., Turrini, F. and Arese, P. (1998) Plasmodium falciparum glutathione metabolism and growth are independent of glutathione system of host erythrocyte. FEBS Lett. 424, 257-261 (Pubitemid 28135325)
26. Lüersen, K., Walter, R. D. and Muller, S. (2000) Plasmodium falciparum-infected red blood cells depend on a functional glutathione de novo synthesis attributable to an enhanced loss of glutathione. Biochem. J. 346, 545-552 (Pubitemid 30148144)
27. Meierjohann, S., Walter, R. D. and Muller, S. (2002) Regulation of intracellular glutathione levels in erythrocytes infected with chloroquine-sensitive and chloroquine-resistant Plasmodium falciparum. Biochem. J. 368, 761-768 (Pubitemid 36042677)
28. Patzewitz, E. M., Wong, E. H. and Muller, S. (2012) Dissecting the role of glutathione biosynthesis in Plasmodium falciparum. Mol. Microbiol. 83, 304-318
29. Tietze, F. (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 27, 502-522
30. Whillier, S., Raftos, J. E., Sparrow, R. L. and Kuchel, P. W. (2011) The effects of long-term storage of human red blood cells on the glutathione synthesis rate and steady-state concentration. Transfusion 51, 1450-1459
31. Allen, R. J. W. and Kirk, K. (2010) Plasmodium falciparum culture: the benefits of shaking. Mol. Biochem. Parasitol. 169, 63-65
32. Cobbold, S. A., Martin, R. E. and Kirk, K. (2011) Methionine transport in the malaria parasite Plasmodium falciparum. Int. J. Parasitol. 41, 125-135
33. Ansorge, I., Benting, J., Bhakdi, S. and Lingelbach, K. (1996) Protein sorting in Plasmodium falciparum-infected red blood cells permeabilized with the pore-forming protein streptolysin O. Biochem. J. 315, 307-314 (Pubitemid 26113567)
34. +-ATPase. J. Biol. Chem. 274, 33213-33219
35. Spillman, N. J., Allen, R. J. W. and Kirk, K. (2008) Acid extrusion from the intraerythrocytic malaria parasite is not via a Na+ /H+ exchanger. Mol. Biochem. Parasitol. 162, 96-99
36. Shaik, I. H. and Mehvar, R. (2006) Rapid determination of reduced and oxidized glutathione levels using a new thiol-masking reagent and the enzymatic recycling method: application to the rat liver and bile samples. Anal. Bioanal. Chem. 385, 105-113
37. +-ATPase localized in plasma membranes of malaria parasite cells, Plasmodium falciparum, is involved in regional acidification of parasitized erythrocytes. J. Biol. Chem. 275, 34353-34358
38. Ellman, G. L. (1959) Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82, 70-77
39. Russell, J., McKeown, J. A., Hensman, C., Smith, W. E. and Reglinski, J. (1997) HPLC determination of biologically active thiols using pre-column derivatisation with 5,5′-dithio-(bis-2-nitrobenzoic acid). J. Pharm. Biomed. Anal. 15, 1757-1763 (Pubitemid 27308687)
40. Dringen, R., Kussmaul, L. and Hamprecht, B. (1998) Detoxification of exogenous hydrogen peroxide and organic hydroperoxides by cultured astroglial cells assessed by microtiter plate assay. Brain Res. Protoc. 2, 223-228 (Pubitemid 28277484)
41. Hirrlinger, J., Konig, J., Keppler, D., Lindenau, J., Schulz, J. B. and Dringen, R. (2001) The multidrug resistance protein MRP1 mediates the release of glutathione disulfide from rat astrocytes during oxidative stress. J. Neurochem. 76, 627-636 (Pubitemid 32097039)
42. Kirk, K., Horner, H. A. and Kirk, J. (1996) Glucose uptake in Plasmodium falciparum-infected erythrocytes is an equilibrative not an active process. Mol. Biochem. Parasitol. 82, 195-205 (Pubitemid 26375825)
43. Plagemann, P. G. W., Wohlhueter, R. M. and Kraupp, M. (1985) Adenine nucleotide metabolism and nucleoside transport in human erythrocytes under ATP depletion conditions. Biochim. Biophys. Acta 817, 51-60 (Pubitemid 15011678)
44. Srivastava, S. K. and Beutler, E. (1968) Accurate measurement of oxidized glutathione content of human, rabbit, and rat red blood cells and tissues. Anal. Biochem. 25, 70-76
45. Rossi, R., Dalle-Donne, I., Milzani, A. and Giustarini, D. (2006) Oxidized forms of glutathione in peripheral blood as biomarkers of oxidative stress. Clin. Chem. 52, 1406-1414 (Pubitemid 43956034)
46. Saliba, K. J., Horner, H. A. and Kirk, K. (1998) Transport and metabolism of the essential vitamin pantothenic acid in human erythrocytes infected with the malaria parasite Plasmodium falciparum. J. Biol. Chem. 273, 10190-10195 (Pubitemid 28227619)
47. Waterman, C. S., Atkinson, Jr, E. E., Wilkins, Jr, B., Fischer, C. L. and Kimzey, S. L. (1975) Improved measurement of erythrocyte volume distribution by aperture-counter signal analysis. Clin. Chem. 21, 1201-1211
48. Richie, Jr, J. P., Skowronski, L., Abraham, P. and Leutzinger, Y. (1996) Blood glutathione concentrations in a large-scale human study. Clin. Chem. 42, 64-70 (Pubitemid 26030383)
49. Rossi, R., Giustarini, D., Milzani, A. and Dalle-Donne, I. (2006) Membrane skeletal protein S-glutathionylation and hemolysis in human red blood cells. Blood Cells Mol. Dis. 37, 180-187 (Pubitemid 44716720)
50. Kondo, T. and Beutler, E. (1979) Depletion of red cell ATP by incubation with 2-deoxyglucose. J. Lab. Clin. Med. 94, 617-623 (Pubitemid 10210892)
51. 1H NMR spectroscopy. NMR Biomed. 22, 292-302
52. Wu, C. P., Woodcock, H., Hladky, S. B. and Barrand, M. A. (2005) cGMP (guanosine 3′,5′-cyclic monophosphate) transport across human erythrocyte membranes. Biochem. Pharmacol. 69, 1257-1262 (Pubitemid 40417498)
53. Cole, S. P. C. and Deeley, R. G. (2006) Transport of glutathione and glutathione conjugates by MRP1. Trends Pharmacol. Sci. 27, 438-446 (Pubitemid 44051570)
54. Leslie, E. M., Deeley, R. G. and Cole, S. P. C. (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol. 204, 216-237 (Pubitemid 40552845)
55. Klokouzas, A., Shahi, S., Hladky, S. B., Barrand, M. A. and van Veen, H. W. (2003) ABC transporters and drug resistance in parasitic protozoa. Int. J. Antimicrob. Agents. 22, 301-317 (Pubitemid 37107459)
56. Klokouzas, A., Tiffert, T., van Schalkwyk, D., Wu, C. P., van Veen, H. W., Barrand, M. A. and Hladky, S. B. (2004) Plasmodium falciparum expresses a multidrug resistance associated protein. Biochem. Biophys. Res. Commun. 321, 197-201 (Pubitemid 39055624)
57. Raj, D. K., Mu, J. B., Jiang, H. Y., Kabat, J., Singh, S., Sullivan, M., Fay, M. P., McCutchan, T. F. and Su, X. Z. (2009) Disruption of a Plasmodium falciparum multidrug resistance-associated protein (PfMRP) alters its fitness and transport of antimalarial drugs and glutathione. J. Biol. Chem. 284, 7687-7696
58. Kavishe, R. A., van den Heuvel, J. M. W., van de Vegte-Bolmer, M., Luty, A. J. F., Russel, F. G. M. and Koenderink, J. B. (2009) Localization of the ATP-binding cassette (ABC) transport proteins PfMRP1, PfMRP2, and PfMDR5 at the Plasmodium falciparum plasma membrane. Malar. J. 8, 205
59. Deeley, R. G. and Cole, S. P. C. (2006) Substrate recognition and transport by multidrug resistance protein 1 (ABCC1). FEBS Lett. 580, 1103-1111 (Pubitemid 43185290)
60. Fischer, S., Loncar, J., Zaja, R., Schnell, S., Schirmer, K., Smital, T. and Luckenbach, T. (2011) Constitutive mRNA expression and protein activity levels of nine ABC efflux transporters in seven permanent cell lines derived from different tissues of rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 101, 438-446
61. Luckenbach, T. and Epel, D. (2008) ABCB- and ABCC-type transporters confer multixenobiotic resistance and form an environment-tissue barrier in bivalve gills. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1919-R1929
62. Gould, N. S., Min, E., Martin, R. J. and Day, B. J. (2012) CFTR is the primary known apical glutathione transporter involved in cigarette smoke-induced adaptive responses in the lung. Free Radical Biol. Med. 52, 1201-1206
63. Frade, J., Pope, S., Schmidt, M., Dringen, R., Barbosa, R., Pocock, J., Laranjinha, J. and Heales, S. (2008) Glutamate induces release of glutathione from cultured rat astrocytes: a possible neuroprotective mechanism? J. Neurochem. 105, 1144-1152 (Pubitemid 351590782)