Chemical activation of a high-affinity glutamate transporter in human erythrocytes and its implications for malaria-parasite-induced glutamate uptake

Blood

Volumn 119, Issue 15, 2012, Pages 3604-3612

  Winterberg, Markus ^a,b   Rajendran, Esther ^b   Baumeister, Stefan ^a   Bietz, Sven ^a   Kirk, Kiaran ^b   Lingelbach, Klaus ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC TRIOXIDE; DEXTRO ASPARTIC ACID; DEXTRO GLUTAMIC ACID; EXCITATORY AMINO ACID TRANSPORTER 3; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; SODIUM CHANNEL;

ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; EXTRACELLULAR MATRIX; HOST CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; RECEPTOR AFFINITY; WESTERN BLOTTING;

EID: 84859850955     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-10-386003     Document Type: Article

References (52)

1. Elford BC, Haynes JD, Chulay JD, Wilson RJ. Selective stage-specific changes in the permeability to small hydrophilic solutes of human erythrocytes infected with Plasmodium falciparum. Mol Biochem Parasitol. 1985;16(1):43-60. (Pubitemid 15059381)
2. Ginsburg H, Kutner S, Krugliak M, Cabantchik ZI. Characterization of permeation pathways appearing in the host membrane of Plasmodium falciparum infected red blood cells. Mol Biochem Parasitol. 1985;14(3):313-322. (Pubitemid 15140562)
3. Kirk K, Horner HA, Elford BC, Ellory JC, Newbold CI. Transport of diverse substrates into malaria-infected erythrocytes via a pathway showing functional characteristics of a chloride channel. J Biol Chem. 1994; 269(5):3339-3347. (Pubitemid 24237649)
4. Staines HM, Ellory JC, Kirk K. Perturbation of the pump-leak balance for Na(+) and K(+) in malaria-infected erythrocytes. Am J Physiol Cell Physiol. 2001;280(6):C1576-1587.
5. Upston JM, Gero AM. Parasite-induced permeation of nucleosides in Plasmodium falciparum malaria. Biochim Biophys Acta. 1995;1236(2): 249-258.
6. Cobbold SA, Martin RE, Kirk K. Methionine transport in the malaria parasite Plasmodium falciparum. Int J Parasitol. 2011;41(1):125-135.
7. Martin RE, Kirk K. Transport of the essential nutrient isoleucine in human erythrocytes infected with the malaria parasite Plasmodium falciparum. Blood. 2007;109(5):2217-2224. (Pubitemid 46348226)
8. Saliba KJ, Kirk K. Uptake of an antiplasmodial protease inhibitor into Plasmodium falciparum-infected human erythrocytes via a parasite-induced pathway. Mol Biochem Parasitol. 1998; 94(2):297-301. (Pubitemid 28377296)
9. Baumeister S, Wiesner J, Reichenberg A, et al. Fosmidomycin uptake into Plasmodium and babesia-infected erythrocytes is facilitated by parasite-induced new permeability pathways. PLoS One. 2011;6(5):e19334.
10. Lisk G, Pain M, Gluzman IY, et al. Changes in the plasmodial surface anion channel reduce leupeptin uptake and can confer drug resistance in Plasmodium falciparum-infected erythrocytes. Antimicrob Agents Chemother. 2008;52(7):2346-2354. (Pubitemid 351915661)
11. Lisk G, Pain M, Sellers M, et al. Altered plasmodial surface anion channel activity and in vitro resistance to permeating antimalarial compounds. Biochim Biophys Acta. 2010;1798(9):1679-1688.
12. Stead AM, Bray PG, Edwards IG, et al. Diamidine compounds: selective uptake and targeting in Plasmodium falciparum. Mol Pharmacol. 2001; 59(5):1298-1306. (Pubitemid 32381609)
13. Poole RC, Halestrap AP. Transport of lactate and other monocarboxylates across mammalian plasma membranes. Am J Physiol. 1993;264(4 pt 1):C761-C782. (Pubitemid 23118095)
14. Mauritz JM, Seear R, Esposito A, et al. X-ray microanalysis investigation of the changes in Na, K, and hemoglobin concentration in Plasmodium falciparum-infected red blood cells. Biophys J. 2011;100(6):1438-1445.
15. Huber SM, Duranton C, Lang F. Patch-clamp analysis of the "new permeability pathways" in malaria-infected erythrocytes. Int Rev Cytol. 2005;246:59-134. (Pubitemid 41829516)
16. Huber SM, Uhlemann AC, Gamper NL, Duranton C, Kremsner PG, Lang F. Plasmodium falciparum activates endogenous Cl(-) channels of human erythrocytes by membrane oxidation. EMBO J. 2002;21(1-2):22-30. (Pubitemid 34087071)
17. Egée, Lapaix F, Decherf G, et al. A stretch-activated anion channel is up-regulated by the malaria parasite Plasmodium falciparum. J Physiol. 2002;542(pt 3):795-801.
18. Merckx A, Bouyer G, Thomas SL, Langsley G, Egee S. Anion channels in Plasmodium-falciparum-infected erythrocytes and protein kinase A. Trends Parasitol. 2009;25(3):139-144.
19. Merckx A, Nivez MP, Bouyer G, et al. Plasmodium falciparum regulatory subunit of cAMP-dependent PKA and anion channel conductance. PLoS Pathog. 2008;4(2):e19.
20. Bouyer G, Cueff A, Egee S, et al. Erythrocyte peripheral type benzodiazepine receptor/voltagedependent anion channels are up-regulated by Plasmodium falciparum. Blood. 2011;118(8): 2305-2312.
21. Alkhalil A, Cohn JV, Wagner MA, Cabrera JS, Rajapandi T, Desai SA. Plasmodium falciparum likely encodes the principal anion channel on infected human erythrocytes. Blood. 2004;104(13): 4279-4286. (Pubitemid 39620183)
22. Alkhalil A, Pillai AD, Bokhari AA, Vaidya AB, Desai SA. Complex inheritance of the plasmodial surface anion channel in a Plasmodium falciparum genetic cross. Mol Microbiol. 2009;72(2): 459-469.
23. Hill DA, Pillai AD, Nawaz F, et al. A blasticidin S-resistant Plasmodium falciparum mutant with a defective plasmodial surface anion channel. Proc Natl Acad Sci U S A. 2007;104(3):1063-1068. (Pubitemid 46154736)
24. Nguitragool W, Bokhari AA, Pillai AD, et al. Malaria parasite clag3 genes determine channelmediated nutrient uptake by infected red blood cells. Cell. 2011;145(5):665-677.
25. Ventura-Lima J, Bogo MR, Monserrat JM. Arsenic toxicity in mammals and aquatic animals: a comparative biochemical approach. Ecotoxicol Environ Saf. 2011;74(3):211-218.
26. Flatman PW, Creanor J. Stimulation of Na+-K+-2Cl- cotransport by arsenite in ferret erythrocytes. J Physiol. 1999;519(pt 1):143-152. (Pubitemid 29417809)
27. Kirk K, Staines HM, Martin RE, Saliba KJ. Transport properties of the host cell membrane. Novartis Found Symp. 1999;226:55-66; discussion 66-73.
28. Lauer SA, Rathod PK, Ghori N, Haldar K. A membrane network for nutrient import in red cells infected with the malaria parasite. Science. 1997; 276(5315):1122-1125. (Pubitemid 27218122)
29. Beart PM, O'Shea RD. Transporters for L-glutamate: an update on their molecular pharmacology and pathological involvement. Br J Pharmacol. 2007;150(1):5-17. (Pubitemid 46094664)
30. Kanai Y, Hediger MA. The glutamate/neutral amino acid transporter family SLC1: molecular, physiological and pharmacological aspects. Pflugers Arch. 2004;447(5):469-479. (Pubitemid 38241433)
31. Allen RJ, Kirk K. Plasmodium falciparum culture: the benefits of shaking. Mol Biochem Parasitol. 2010;169(1):63-65.
32. Lambros C, Vanderberg JP. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol. 1979;65(3):418-420. (Pubitemid 10222999)
33. Baumeister S, Winterberg M, Duranton C, et al. Evidence for the involvement of Plasmodium falciparum proteins in the formation of new permeability pathways in the erythrocyte membrane. Mol Microbiol. 2006;60(2):493-504.
34. Liu X, Pohl CA. Comparison of reversed-phase/cation-exchange/anion- exchange trimodal stationary phases and their use in active pharmaceutical ingredient and counterion determinations. J Chromatogr A. 2012;1232:190-195.
35. Tonkin CJ, van Dooren GG, Spurck TP, et al. Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol. 2004;137(1):13-21. (Pubitemid 38987938)
36. Ellory JC, Preston RL, Osotimehin B, Young JD. Transport of amino acids for glutathione biosynthesis in human and dog red cells. Biomed Biochim Acta. 1983;42(11-12):S48-52. (Pubitemid 14128724)
37. Shashidharan P, Huntley GW, Murray JM, et al. Immunohistochemical localization of the neuron-specific glutamate transporter EAAC1 (EAAT3) in rat brain and spinal cord revealed by a novel monoclonal antibody. Brain Res. 1997;773(1-2): 139-148. (Pubitemid 27521118)
38. Danbolt NC. Glutamate uptake. Prog Neurobiol. 2001;65(1):1-105. (Pubitemid 32479155)
39. Ryu J, Cheong IY, Do SH, Zuo Z. Alphaxalone, a neurosteroid anaesthetic, increases the activity of the glutamate transporter type 3 expressed in Xenopus oocytes. Eur J Pharmacol. 2009;602(1): 23-27.
40. Griffiths R, Dunlop J, GormanA, Senior J, Grieve A. L-trans-pyrrolidine- 2,4-dicarboxylate and cis-1-aminocyclobutane-1,3-dicarboxylate behave as transportable, competitive inhibitors of the high-affinity glutamate transporters. Biochem Pharmacol. 1994; 47(2):267-274.
41. Sato K, Inaba M, Maede Y. Characterization of Na(+)-dependent L-glutamate transport in canine erythrocytes. Biochim Biophys Acta. 1994; 1195(2):211-217. (Pubitemid 24331640)
42. Novak D, Beveridge M, Verlander-Reed J. Rat erythrocytes express the anionic amino acid transport protein EAAC1. Blood Cells Mol Dis. 2002;29(3):261-266. (Pubitemid 36054941)
43. Ruiz-Ramos R, Lopez-Carrillo L, Rios-Perez AD, De Vizcaya-Ruiz A, Cebrian ME. Sodium arsenite induces ROS generation, DNA oxidative damage, HO-1 and c-Myc proteins, NF-kappaB activation and cell proliferation in human breast cancer MCF-7 cells. Mutat Res. 2009;674(1-2):109-115.
44. Desai SA, Bezrukov SM, Zimmerberg J. A voltage-dependent channel involved in nutrient uptake by red blood cells infected with the malaria parasite. Nature. 2000;406(6799):1001-1005.
45. Staines HM, Alkhalil A, Allen RJ, et al. Electrophysiological studies of malaria parasite-infected erythrocytes: current status. Int J Parasitol. 2007; 37(5):475-482. (Pubitemid 46399711)
46. Kirk K, Howitt SM, Broer S, Saliba KJ, Downie MJ. Purine uptake in Plasmodium: transport versus metabolism. Trends Parasitol. 2009;25(6):246-249.
47. Divo AA, Geary TG, Davis NL, Jensen JB. Nutritional requirements of Plasmodium falciparum in culture. I. Exogenously supplied dialyzable components necessary for continuous growth. J Protozool. 1985;32(1):59-64. (Pubitemid 15107964)
48. Liu J, Istvan ES, Gluzman IY, Gross J, Goldberg DE. Plasmodium falciparum ensures its amino acid supply with multiple acquisition pathways and redundant proteolytic enzyme systems. Proc Natl Acad Sci USA. 2006;103(23):8840-8845. (Pubitemid 43878106)
49. Ginsburg H, Handeli S, Friedman S, Gorodetsky R, Krugliak M. Effects of red blood cell potassium and hypertonicity on the growth of Plasmodium falciparum in culture. Z Parasitenkd. 1986;72(2):185-199. (Pubitemid 16154383)
50. Lee P, Ye Z, Van Dyke K, Kirk RG. X-ray microanalysis of Plasmodium falciparum and infected red blood cells: effects of qinghaosu and chloroquine on potassium, sodium, and phosphorus composition. Am J Trop Med Hyg. 1988;39(2): 157-165.
51. Lew VL, Tiffert T, Ginsburg H. Excess hemoglobin digestion and the osmotic stability of Plasmodium falciparum-infected red blood cells. Blood. 2003; 101(10):4189-4194. (Pubitemid 36857903)
52. Mauritz JM, Esposito A, Ginsburg H, Kaminski CF, Tiffert T, Lew VL. The homeostasis of Plasmodium falciparum-infected red blood cells. PLoS Comput Biol. 2009;5(4):e1000339.