The Plasmodium falciparum-induced anion channel of human erythrocytes is an ATP-release pathway

Pflugers Archiv European Journal of Physiology

Volumn 457, Issue 5, 2009, Pages 1035-1047

  Akkaya, Canan ^a   Shumilina, Ekaterina ^a   Bobballa, Diwakar ^a   Brand, Verena B ^a   Mahmud, Hasan ^a   Lang, Florian ^a   Huber, Stephan M ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

New permeability pathways; Organic osmolyte and anion channels; Patch clamp; Plasmodium falciparum; Red blood cells

Indexed keywords

5 NITRO 2(3 PHENYLPROPYLAMINO) BENZOIC ACID; ADENOSINE TRIPHOSPHATE; ANION CHANNEL; BENZOIC ACID DERIVATIVE; SERUM ALBUMIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; HUMAN; HUMAN CELL; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANIONS; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; HUMANS; ION CHANNELS; NITROBENZOATES; PLASMODIUM FALCIPARUM;

EID: 59849123764     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-008-0572-8     Document Type: Article

References (56)

1. PH Barry JW Lynch 1991 Liquid junction potentials and small cell effects in patch-clamp analysis J Membr Biol 121 101 117
2. DC Bencic TJ Yates RL Ingermann 1997 Ecto-ATPase activity of vertebrate blood cells Physiol Zool 70 621 630
3. GR Bergfeld T Forrester 1992 Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia Cardiovasc Res 26 40 47
4. G Bouyer S Egee SL Thomas 2006 Three types of spontaneously active anionic channels in malaria-infected human red blood cells Blood Cells Mol Dis 36 248 254
5. G Bouyer S Egee SL Thomas 2007 Toward a unifying model of malaria-induced channel activity Proc Natl Acad Sci USA 104 11044 11049
6. GM Braunstein RM Roman JP Clancy BA Kudlow AL Taylor VG Shylonsky B Jovov K Peter T Jilling Ismailov II DJ Benos LM Schwiebert JG Fitz EM Schwiebert 2001 Cystic fibrosis transmembrane conductance regulator facilitates ATP release by stimulating a separate ATP release channel for autocrine control of cell volume regulation J Biol Chem 276 6621 6630
7. G Decherf G Bouyer S Egee SL Thomas 2007 Chloride channels in normal and cystic fibrosis human erythrocyte membrane Blood Cells Mol Dis 39 24 34
8. G Decherf S Egee HM Staines JC Ellory SL Thomas 2004 Anionic channels in malaria-infected human red blood cells Blood Cells Mol Dis 32 366 371
9. SA Desai SM Bezrukov J Zimmerberg 2000 A voltage-dependent channel involved in nutrient uptake by red blood cells infected with the malaria parasite Nature 406 1001 1005
10. HH Dietrich ML Ellsworth RS Sprague RG Dacey Jr 2000 Red blood cell regulation of microvascular tone through adenosine triphosphate Am J Physiol 278 H1294 H1298
11. C Duranton S Huber V Tanneur K Lang V Brand C Sandu F Lang 2003 Electrophysiological properties of the Plasmodium falciparum-induced cation conductance of human erythrocytes Cell Physiol Biochem 13 189 198
12. --dependent cation conductance in human red blood cells J Physiol 539 847 855
13. C Duranton SM Huber V Tanneur VB Brand C Akkaya EV Shumilina CD Sandu F Lang 2004 Organic osmolyte permeabilities of the malaria-induced anion conductances in human erythrocytes J Gen Physiol 123 417 426
14. C Duranton V Tanneur V Brand CD Sandu C Akkaya SM Huber F Lang 2005 Permselectivity and pH-dependence of Plasmodium falciparum-induced anion currents in human erythrocytes Pflugers Arch 450 335 344
15. Duranton C, Tanneur V, Lang C, Brand VB, Koka S, Kasinathan RS, Dorsch M, Hedrich HJ, Baumeister S, Lingelbach K, Lang F, Huber SM (2008) A high specificity and affinity interaction with serum albumin stimulates an anion conductance in malaria-infected erythrocytes. Cell Physiol Biochem 22 (in press)
16. J Edwards R Sprung R Sprague D Spence 2001 Chemiluminescence detection of ATP release from red blood cells upon passage through microbore tubing Analyst 126 1257 1260
17. S Egee F Lapaix G Decherf HM Staines JC Ellory C Doerig SLY Thomas 2002 A stretch-activated anion channel is up-regulated by the malaria parasite Plasmodium falciparum J Physiol 542 795 801
18. M Farias 3rd MW Gorman MV Savage EO Feigl 2005 Plasma ATP during exercise: possible role in regulation of coronary blood flow Am J Physiol 288 H1586 H1590
19. H Ginsburg M Krugliak O Eidelman ZI Cabantchik 1983 New permeability pathways induced in membranes of Plasmodium falciparum infected erythrocytes Mol Biochem Parasitol 8 177 190
20. R Grygorczyk JW Hanrahan 1997 CFTR-independent ATP release from epithelial cells triggered by mechanical stimuli Am J Physiol 272 C1058 C1066
21. R Grygorczyk JA Tabcharani JW Hanrahan 1996 CFTR channels expressed in CHO cells do not have detectable ATP conductance J Membr Biol 151 139 148
22. SM Huber C Duranton G Henke C Van De Sand V Heussler E Shumilina CD Sandu V Tanneur V Brand RS Kasinathan KS Lang PG Kremsner CA Hubner MB Rust K Dedek TJ Jentsch F Lang 2004 Plasmodium induces swelling-activated ClC-2 anion channels in the host erythrocyte J Biol Chem 279 41444 41452
23. - channels of human erythrocytes by membrane oxidation Embo J 21 22 30
24. K Kirk 2001 Membrane transport in the malaria-infected erythrocyte Physiol Rev 81 495 537
25. K Kirk HA Horner 1995 In search of a selective inhibitor of the induced transport of small solutes in Plasmodium falciparum-infected erythrocytes: effects of arylaminobenzoates Biochem J 311 761 768
26. K Kirk HA Horner BC Elford JC Ellory CI Newbold 1994 Transport of diverse substrates into malaria-infected erythrocytes via a pathway showing functional characteristics of a chloride channel J Biol Chem 269 3339 3347
27. R Knofler G Weissbach E Kuhlisch 1997 Release of adenosine triphosphate by adenosine diphosphate in whole blood and in erythrocyte suspensions Am J Hematol 56 259 265
28. S Kutner H Ginsburg ZI Cabantchik 1983 Permselectivity changes in malaria (Plasmodium falciparum) infected human red blood cell membranes J Cell Physiol 114 245 251
29. G Laing AH Stephenson AJ Lonigro RS Sprague 2005 Erythrocytes of humans with cystic fibrosis fail to stimulate nitric oxide synthesis in isolated rabbit lungs Am J Physiol 288 H1580 H1585
30. VL Lew L Macdonald H Ginsburg M Krugliak T Tiffert 2004 Excess haemoglobin digestion by malaria parasites: a strategy to prevent premature host cell lysis Blood Cells Mol Dis 32 353 359
31. DB Light PK Dahlstrom RT Gronau NL Baumann 2001 Extracellular ATP activates a P2 receptor in necturus erythrocytes during hypotonic swelling J Membr Biol 182 193 202
32. S Locovei L Bao G Dahl 2006 Pannexin 1 in erythrocytes: function without a gap Proc Natl Acad Sci USA 103 7655 7659
33. CH Mitchell DA Carre AM McGlinn RA Stone MM Civan 1998 A release mechanism for stored ATP in ocular ciliary epithelial cells Proc Natl Acad Sci USA 95 7174 7178
34. JJ Olearczyk ML Ellsworth AH Stephenson AJ Lonigro RS Sprague 2004 Nitric oxide inhibits ATP release from erythrocytes J Pharmacol Exp Ther 309 1079 1084
35. JJ Olearczyk AH Stephenson AJ Lonigro RS Sprague 2001 Receptor-mediated activation of the heterotrimeric G-protein Gs results in ATP release from erythrocytes Med Sci Monit 7 669 674
36. JJ Olearczyk AH Stephenson AJ Lonigro RS Sprague 2004 NO inhibits signal transduction pathway for ATP release from erythrocytes via its action on heterotrimeric G protein Gi Am J Physiol 287 H748 H754
37. EM Schwiebert ME Egan TH Hwang SB Fulmer SS Allen GR Cutting WB Guggino 1995 CFTR regulates outwardly rectifying chloride channels through an autocrine mechanism involving ATP Cell 81 1063 1073
38. R Sprague E Bowles M Stumpf G Ricketts A Freidman WH Hou A Stephenson A Lonigro 2005 Rabbit erythrocytes possess adenylyl cyclase type II that is activated by the heterotrimeric G proteins Gs and Gi Pharmacol Rep 57 Suppl 222 228
39. RS Sprague ML Ellsworth AH Stephenson ME Kleinhenz AJ Lonigro 1998 Deformation-induced ATP release from red blood cells requires CFTR activity Am J Physiol 275 H1726 H1732
40. RS Sprague ML Ellsworth AH Stephenson AJ Lonigro 1996 ATP: the red blood cell link to NO and local control of the pulmonary circulation Am J Physiol 271 H2717 H2722
41. RS Sprague ML Ellsworth AH Stephenson AJ Lonigro 2001 Participation of cAMP in a signal-transduction pathway relating erythrocyte deformation to ATP release Am J Physiol 281 C1158 C1164
42. RS Sprague JJ Olearczyk DM Spence AH Stephenson RW Sprung AJ Lonigro 2003 Extracellular ATP signaling in the rabbit lung: erythrocytes as determinants of vascular resistance Am J Physiol 285 H693 H700
43. RS Sprague AH Stephenson RA Dimmitt NL Weintraub CA Branch L McMurdo AJ Lonigro 1995 Effect of L-NAME on pressure-flow relationships in isolated rabbit lungs: role of red blood cells Am J Physiol 269 H1941 H1948
44. RS Sprague AH Stephenson ML Ellsworth C Keller AJ Lonigro 2001 Impaired release of ATP from red blood cells of humans with primary pulmonary hypertension Exp Biol Med (Maywood) 226 434 439
45. R Sprung R Sprague D Spence 2002 Determination of ATP release from erythrocytes using microbore tubing as a model of resistance vessels in vivo Anal Chem 74 2274 2278
46. HM Staines A Alkhalil RJ Allen HR De Jonge E Derbyshire S Egee H Ginsburg DA Hill SM Huber K Kirk F Lang G Lisk E Oteng AD Pillai K Rayavara S Rouhani KJ Saliba C Shen T Solomon SL Thomas P Verloo SA Desai 2007 Electrophysiological studies of malaria parasite-infected erythrocytes: current status Int J Parasitol 37 475 482
47. HM Staines S Ashmore H Felgate J Moore T Powell JC Ellory 2006 Solute transport via the new permeability pathways in Plasmodium falciparum-infected human red blood cells is not consistent with a simple single channel model Blood 108 3187 3194
48. HM Staines T Powell JC Ellory S Egee F Lapaix G Decherf SL Thomas C Duranton F Lang SM Huber 2003 Modulation of whole-cell currents in Plasmodium falciparum-infected human red blood cells by holding potential and serum J Physiol 552 177 183
49. HM Staines C Rae K Kirk 2000 Increased permeability of the malaria-infected erythrocyte to organic cations Biochim Biophys Acta 1463 88 98
50. - channel and CFTR-associated ATP channel: distinct pores regulated by common gates Embo J 17 898 908
51. V Tanneur C Duranton VB Brand CD Sandu C Akkaya RS Kasinathan C Gachet R Sluyter JA Barden JS Wiley F Lang SM Huber 2006 Purinoceptors are involved in the induction of an osmolyte permeability in malaria-infected and oxidized human erythrocytes Faseb J 20 133 135
52. RJ Thompson N Zhou BA MacVicar 2006 Ischemia opens neuronal gap junction hemichannels Science 312 924 927
53. W Trager JB Jensen 1976 Human malaria parasites in continuous culture Science 193 673 675
54. EG Trams 1980 A proposal for the role of ecto-enzymes and adenylates in traumatic shock J Theor Biol 87 609 621
55. P Verloo CH Kocken A Van der Wel BC Tilly BM Hogema M Sinaasappel AW Thomas HR De Jonge 2004 Plasmodium falciparum-activated chloride channels are defective in erythrocytes from cystic fibrosis patients J Biol Chem 279 10316 10322
56. L Wang G Olivecrona M Gotberg ML Olsson MS Winzell D Erlinge 2005 ADP acting on P2Y13 receptors is a negative feedback pathway for ATP release from human red blood cells Circ Res 96 189 196