Skip to main content
Log in

Channel-induced apoptosis of infected host cells—the case of malaria

  • Invited Review
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

Infection of erythrocytes by the malaria pathogen Plasmodium falciparum leads to activation of several distinct anion channels and a non-selective, Ca2+-permeable cation channel. All channel types are presumably activated by the oxidative stress generated by the pathogen. Similar or identical channels are activated by oxidation of non-infected erythrocytes. Activation of the non-selective cation channel allows entry of Ca2+ and Na+, both of which are required for intracellular growth of the pathogen. The entry of Ca2+ stimulates an intraerythrocytic scramblase that facilitates bi-directional phospholipid migration across the bilayer, resulting in breakdown of the phosphatidylserine asymmetry of the cell membrane. The exposure of phosphatidylserine at the outer surface of the cell membrane is presumably followed by binding to phosphatidylserine receptors on macrophages and subsequent phagocytosis of the affected erythrocyte. The lysosomal degradation may eventually eliminate the pathogen. The channel may thus play a dual role in pathogen survival. Absence of the channels is not compatible with pathogen growth, enhanced channel activity accelerates erythrocyte “apoptosis” that may represent a host defence mechanism serving to eliminate infected erythrocytes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1A–C
Fig. 2

Similar content being viewed by others

References

  1. Atamna H, Ginsburg H (1993) Origin of reactive oxygen species in erythrocytes infected with Plasmodium falciparum. Mol Biochem Parasitol 61:231–241

    CAS  PubMed  Google Scholar 

  2. Atamna H, 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

    CAS  PubMed  Google Scholar 

  3. Atamna H, Pascarmona G, Ginsburg H (1994) Hexose-monophosphate shunt activity in intact Plasmodium falciparum-infected erythrocytes and in free parasites. Mol Biochem Parasitol 67:79–89

    Article  CAS  PubMed  Google Scholar 

  4. 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

    CAS  PubMed  Google Scholar 

  5. Bennekou P (1993) The voltage-gated non-selective cation channel from human red cells is sensitive to acetylcholine. Biochim Biophys Acta 1147:165–167

    Article  CAS  PubMed  Google Scholar 

  6. Berg CP, Engels IH, Rothbart A, Lauber K, Renz A, Schlosser SF, Schulze-Osthoff K, Wesselborg S (2001) Human mature red blood cells express caspase-3 and caspase-8, but are devoid of mitochondrial regulators of apoptosis. Cell Death Differ 8:1197–1206

    Article  PubMed  Google Scholar 

  7. Bernhardt I, Hall AC, Ellory JC (1991) Effects of low ionic strength media on passive human red cell monovalent cation transport. J Physiol (Lond) 434:489–506

    Google Scholar 

  8. Boas FE, Forman L, Beutler E (1998) Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia. Proc Natl Acad Sci USA 95:3077–3081

    Article  CAS  PubMed  Google Scholar 

  9. Bookchin RM, Ortiz OE, Lew VL (1987) Activation of calcium-dependent potassium channels in deoxygenated sickled red cells. Prog Clin Biol Res 240:193–200

    CAS  PubMed  Google Scholar 

  10. Bortner CD, Cidlowski JA (1999) Caspase independent/dependent regulation of K+, cell shrinkage, and mitochondrial membrane potential during lymphocyte apoptosis. J Biol Chem 274:21953–21962

    CAS  PubMed  Google Scholar 

  11. Bortner CD, Cidlowski JA (2004) The role of apoptotic volume decrease and ionic homeostasis in the activation and repression of apoptosis. Pflugers Arch (In press)

  12. Bortner CD, Hughes FM Jr, Cidlowski JA (1997) A primary role for K+ and Na+ efflux in the activation of apoptosis. J Biol Chem 272:32436–32442

    CAS  PubMed  Google Scholar 

  13. Brand VB, Sandu CD, Duranton C, Tanneur V, Lang KS, Huber SM, Lang F (2003) Dependence of Plasmodium falciparum in vitro growth on the cation permeability of the human host erythrocyte. Cell Physiol Biochem 13:347–356

    Article  CAS  PubMed  Google Scholar 

  14. Bratosin D, Estaquier J, Petit F, Arnoult D, Quatannens B, Tissier JP, Slomianny C, Sartiaux C, Alonso C, Huart JJ, Montreuil J, Ameisen JC (2001) Programmed cell death in mature erythrocytes: a model for investigating death effector pathways operating in the absence of mitochondria. Cell Death Differ 8:1143–1156

    Article  PubMed  Google Scholar 

  15. Breuer WV, Kutner S, Sylphen J, Ginsburg H, Cabantchik ZI (1987) Covalent modification of the permeability pathways induced in the human erythrocyte membrane by the malarial parasite Plasmodium falciparum. J Cell Physiol 133:55–63

    CAS  PubMed  Google Scholar 

  16. Brugnara C, de Franceschi L, Alper SL (1993) Ca2+-activated K+ transport in erythrocytes. Comparison of binding and transport inhibition by scorpion toxins. J Biol Chem 268:8760–8768

    CAS  PubMed  Google Scholar 

  17. Christophersen P, Bennekou P (1991) Evidence for a voltage-gated, non-selective cation channel in the human red cell membrane. Biochim Biophys Acta 1065:103–106

    Article  CAS  PubMed  Google Scholar 

  18. Closse C, Dachary-Prigent J, Boisseau MR (1999) Phosphatidylserine-related adhesion of human erythrocytes to vascular endothelium. Br J Haematol 107:300–302

    Article  CAS  PubMed  Google Scholar 

  19. Culliford SJ, Bernhardt I, Ellory JC (1995) Activation of a novel organic solute transporter in mammalian red blood cells. J Physiol (Lond) 489:755–765

    Google Scholar 

  20. Daugas E, Cande C, Kroemer G (2001) Erythrocytes: death of a mummy. Cell Death Differ 8:1131–1133

    Article  PubMed  Google Scholar 

  21. Desai SA, McCleskey EW, Schlesinger PH, Krogstad DJ (1996) A novel pathway for Ca++ entry into Plasmodium falciparum-infected blood cells. Am J Trop Med Hyg 54:464–470

    CAS  PubMed  Google Scholar 

  22. Desai SA, Bezrukov SM, Zimmerberg J (2000) A voltage-dependent channel involved in nutrient uptake by red blood cells infected with the malaria parasite. Nature 406:1001–1005

    Article  CAS  PubMed  Google Scholar 

  23. Duranton C, Huber SM, Lang F (2002) Oxidation induces a Cl-dependent cation conductance in human red blood cells. J Physiol (Lond) 539:847–855

    Google Scholar 

  24. Duranton C, Huber S, Tanneur V, Lang K, Brand V, Sandu C, Lang F (2003) Electrophysiological properties of the Plasmodium falciparum-induced cation conductance of human erythrocytes. Cell Physiol Biochem 13:189–198

    Article  CAS  PubMed  Google Scholar 

  25. Eda S, Sherman IW (2002) Cytoadherence of malaria-infected red blood cells involves exposure of phosphatidylserine. Cell Physiol Biochem 12:373–384

    PubMed  Google Scholar 

  26. Egee S, Lapaix F, Decherf G, Staines HM, Ellory JC, Doerig C, Thomas SL (2002) A stretch-activated anion channel is up-regulated by the malaria parasite Plasmodium falciparum. J Physiol (Lond) 542:795–801

    Google Scholar 

  27. Fadok VA, Bratton DL, Rose DM, Pearson A, Ezekewitz RA, Henson PM (2000) A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405:85–90

    Article  CAS  PubMed  Google Scholar 

  28. Gazarini ML, Thomas AP, Pozzan T, Garcia CR (2003) Calcium signaling in a low calcium environment: how the intracellular malaria parasite solves the problem. J Cell Biol 161:103–110

    Article  CAS  PubMed  Google Scholar 

  29. Gerold P, Schwarz RT (2001) Biosynthesis of glycosphingolipids de-novo by the human malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 112:29–37

    Article  CAS  PubMed  Google Scholar 

  30. Ginsburg H (1994) Transport pathways in the malaria-infected erythrocyte. Their characterization and their use as potential targets for chemotherapy. Biochem Pharmacol 48:1847–1856

    Article  CAS  PubMed  Google Scholar 

  31. Ginsburg H, Atamna H (1994) The redox status of malaria-infected erythrocytes: an overview with an emphasis on unresolved problems. Parasite 1:5–13

    CAS  PubMed  Google Scholar 

  32. Ginsburg H, Kirk K (1998) Membrane transport in malaria-infected erythrocyte. In Sherman IW (Ed) American Society for Microbiology, Washington DC, pp 219–232

  33. Grassme H, Kirschnek S, Riethmueller J, Riehle A, von Kurthy G, Lang F, Weller M, Gulbins E (2000) CD95/CD95 ligand interactions on epithelial cells in host defense to Pseudomonas aeruginosa. Science 290:527–530

    Article  PubMed  Google Scholar 

  34. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312

    CAS  PubMed  Google Scholar 

  35. Gulbins E, Lang F (2001) Pathogens, host-cell invasion and disease. Am Scientist 89:406–413

    Article  Google Scholar 

  36. Gulbins E, Szabo I, Baltzer K, Lang F (1997) Ceramide-induced inhibition of T lymphocyte voltage-gated potassium channel is mediated by tyrosine kinases. Proc Natl Acad Sci USA 94:7661–7666

    CAS  PubMed  Google Scholar 

  37. Gulbins E, Jekle A, Ferlinz K, Grassme H, Lang F (2000) Physiology of apoptosis. Am J Physiol 279:F605–F615

    PubMed  Google Scholar 

  38. Haldar K, Uyetake L, Ghori N, Elmendorf HG, Li WL (1991) The accumulation and metabolism of a fluorescent ceramide derivative in Plasmodium falciparum-infected erythrocytes. Mol Biochem Parasitol 49:143–156

    Article  CAS  PubMed  Google Scholar 

  39. Hanada K, Mitamura T, Fukasawa M, Magistrado PA, Horii T, Nishijima M (2000) Neutral sphingomyelinase activity dependent on Mg2+ and anionic phospholipids in the intraerythrocytic malaria parasite Plasmodium falciparum. Biochem J 346:671–677

    Article  CAS  PubMed  Google Scholar 

  40. Henson PM, Bratton DL, Fadok VA (2001) The phosphatidylserine receptor: a crucial molecular switch? Nat Rev Mol Cell Biol 2:627–633

    Article  CAS  PubMed  Google Scholar 

  41. Hoffman JF, Joiner W, Nehrke K, Potapova O, Foye K, Wickrema A (2003) The hSK4 (KCNN4) isoform is the Ca2+-activated K+ channel (Gardos channel) in human red blood cells. Proc Natl Acad Sci USA 100:7366–7371

    Article  CAS  PubMed  Google Scholar 

  42. Huber SM, Gamper N, Lang F (2001) Chloride conductance and volume-regulatory non-selective cation conductance in human red blood cell ghosts. Pflugers Arch 441:551–558

    Article  CAS  PubMed  Google Scholar 

  43. Huber SM, Uhlemann AC, Gamper NL, Duranton C, Kremsner PG, Lang F (2002) Plasmodium falciparum activates endogenous Cl channels of human erythrocytes by membrane oxidation. EMBO J 21:22–30

    Article  CAS  PubMed  Google Scholar 

  44. Joiner CH (1993) Cation transport and volume regulation in sickle red blood cells. Am J Physiol 264:C251–C270

    PubMed  Google Scholar 

  45. Jones GS, Knauf PA (1985) Mechanism of the increase in cation permeability of human erythrocytes in low-chloride media. Involvement of the anion transport protein capnophorin. J Gen Physiol 86:721–738

    CAS  PubMed  Google Scholar 

  46. Joshi P, Dutta GP, Gupta CM (1987) An intracellular simian malarial parasite (Plasmodium knowlesi) induces stage-dependent alterations in membrane phospholipid organization of its host erythrocyte. Biochem J 246:103–108

    CAS  PubMed  Google Scholar 

  47. Kaestner L, Bollensdorff C, Bernhardt I (1999) Non-selective voltage-activated cation channel in the human red blood cell membrane. Biochim Biophys Acta 1417:9–15

    Article  CAS  PubMed  Google Scholar 

  48. Kaestner L, Christophersen P, Bernhardt I, Bennekou P (2000) The non-selective voltage-activated cation channel in the human red blood cell membrane: reconciliation between two conflicting reports and further characterisation. Bioelectrochemistry 52:117–125

    Article  CAS  PubMed  Google Scholar 

  49. Kirk K (2001) Membrane transport in the malaria-infected erythrocyte. Physiol Rev 81:495–537

    CAS  PubMed  Google Scholar 

  50. Kirk K, Horner HA (1995) Novel anion dependence of induced cation transport in malaria-infected erythrocytes. J Biol Chem 270:24270–24275

    Article  CAS  PubMed  Google Scholar 

  51. Kirk K, Strange K (1998) Functional properties and physiological roles of organic solute channels. Annu Rev Physiol 60:719–739

    CAS  PubMed  Google Scholar 

  52. Kirk K, Horner HA, Spillett DJ, Elford BC (1993) Glibenclamide and meglitinide block the transport of low molecular weight solutes into malaria-infected erythrocytes. FEBS Lett 323:123–128

    Article  CAS  PubMed  Google Scholar 

  53. Kirk K, Horner HA, Elford BC, Ellory JC, Newbold CI (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

    CAS  PubMed  Google Scholar 

  54. Kutner S, Breuer WV, Ginsburg H, Cabantchik ZI (1987) On the mode of action of phlorizin as an antimalarial agent in in vitro cultures of Plasmodium falciparum. Biochem Pharmacol 36:123–129

    Article  CAS  PubMed  Google Scholar 

  55. Lang F, Busch GL, Ritter M, Völkl H, Waldegger S, Gulbins E, Häussinger D (1998) Functional significance of cell volume regulatory mechanisms. Physiol Rev 78:247–306

    PubMed  Google Scholar 

  56. Lang F, Madlung J, Uhlemann AC, Risler T, Gulbins E (1998) Cellular taurine release triggered by stimulation of the Fas(CD95) receptor in Jurkat lymphocytes. Pflugers Arch 436:377–383

    Article  CAS  PubMed  Google Scholar 

  57. Lang F, Madlung J, Siemen D, Ellory C, Lepple-Wienhues A, Gulbins E (2000) The involvement of caspases in the CD95(Fas/Apo-1)- but not swelling-induced cellular taurine release from Jurkat T-lymphocytes. Pflugers Arch 440:93–99

    Article  CAS  PubMed  Google Scholar 

  58. Lang KS, Roll B, Myssina S, Schittenhelm M, Scheel-Walter HG, Kanz L, Fritz J, Lang F, Huber SM, Wieder T (2002) Enhanced erythrocyte apoptosis in sickle cell anemia, thalassemia and glucose-6-phosphate dehydrogenase deficiency. Cell Physiol Biochem 12:365–372

    PubMed  Google Scholar 

  59. Lang KS, Duranton C, Poehlmann H, Myssina S, Bauer C, Lang F, Wieder T, Huber SM (2003) Cation channels trigger apoptotic death of erythrocytes. Cell Death Differ 10:249–256

    Article  CAS  PubMed  Google Scholar 

  60. Lang KS, Myssina S, Tanneur V, Wieder T, Huber SM, Lang F, Duranton C (2003) Inhibition of erythrocyte cation channels and apoptosis by ethylisopropylamiloride. Naunyn Schmiedeberg’s Arch Pharmacol 367:391–396

    Google Scholar 

  61. Lang KS, Weigert C, Braedel S, Fillon S, Palmada M, Schleicher E, Rammensee HG, Lang F (2003) Inhibition of interferon-gamma expression by osmotic shrinkage of peripheral blood lymphocytes. Am J Physiol 284:C200–C208

    CAS  Google Scholar 

  62. Lang KS, Myssina S, Brand V, Sandu C, Lang PA, Berchtold S, Huber SM, Lang F, Wieder T (2004) Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes. Cell Death Differ 11:231–243

    Article  CAS  PubMed  Google Scholar 

  63. Lang PA, Kaiser S, Myssina S, Wieder T, Lang F, Huber SM (2003) Role of Ca2+-activated K+ channels in human erythrocyte apoptosis. Am J Physiol 285:C1553–C1560

    CAS  Google Scholar 

  64. Lang PA, Warskulat U, Heller-Stilb B, Huang DY, Grenz A, Myssina S, Duszenko M, Lang F, Haussinger D, Vallon V, Wieder T (2003) Blunted apoptosis of erythrocytes from taurine transporter deficient mice. Cell Physiol Biochem 13:337–346

    Article  CAS  PubMed  Google Scholar 

  65. Lauer SA, Ghori N, Haldar K (1995) Sphingolipid synthesis as a target for chemotherapy against malaria parasites. Proc Natl Acad Sci USA 92:9181–9185

    CAS  PubMed  Google Scholar 

  66. Lepple-Wienhues A, Belka C, Laun T, Jekle A, Walter B, Wieland U, Welz M, Heil L, Kun J, Busch G, Weller M, Bamberg M, Gulbins E, Lang F (1999) Stimulation of CD95 (Fas) blocks T lymphocyte calcium channels through sphingomyelinase and sphingolipids. Proc Natl Acad Sci USA 96:13795–13800

    CAS  PubMed  Google Scholar 

  67. Lew VL, Bookchin RM (1991) Osmotic effects of protein polymerization: analysis of volume changes in sickle cell anemia red cells following deoxy-hemoglobin S polymerization. J Membr Biol 122:55–67

    CAS  PubMed  Google Scholar 

  68. Lew VL, Tiffert T, Ginsburg H (2003) Excess hemoglobin digestion and the osmotic stability of Plasmodium falciparum-infected red blood cells. Blood 101:4189–4194

    Article  CAS  PubMed  Google Scholar 

  69. Maeno E, Ishizaki Y, Kanaseki T, Hazama A, Okada Y (2000) Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc Natl Acad Sci USA 97:9487–9492

    PubMed  Google Scholar 

  70. Maguire PA, Prudhomme J, Sherman IW (1991) Alterations in erythrocyte membrane phospholipid organization due to the intracellular growth of the human malaria parasite, Plasmodium falciparum. Parasitology 102:179–186

    PubMed  Google Scholar 

  71. Miller LH, Carter R (1976) A review. Innate resistance in malaria. Exp Parasitol 40:132–146

    CAS  PubMed  Google Scholar 

  72. Moll GN, Vial HJ, Bevers EM, Ancelin ML, Roelofsen B, Comfurius P, Slotboom AJ, Zwaal RF, Op den Kamp JA, van Deenen LL (1990) Phospholipid asymmetry in the plasma membrane of malaria infected erythrocytes. Biochem Cell Biol 68:579–585

    CAS  PubMed  Google Scholar 

  73. Moran J, Hernandez-Pech X, Merchant-Larios H, Pasantes-Morales H (2000) Release of taurine in apoptotic cerebellar granule neurons in culture. Pflugers Arch 439:271–277

    Article  PubMed  Google Scholar 

  74. Okada Y, Maeno E, Shimizu T, Manabe K, Mori S, Nabekura T (2004) Double-edged roles of plasmalemmal chloride channels in induction of cell death. Pflugers Arch (In press)

  75. Pankova-Kholmyansky I, Dagan A, Gold D, Zaslavsky Z, Skutelsky E, Gatt S, Flescher E (2003) Ceramide mediates growth inhibition of the Plasmodium falciparum parasite. Cell Mol Life Sci 60:577–587

    Article  CAS  PubMed  Google Scholar 

  76. Patel AJ, Lazdunski M (2004) The 2P domain K+ channels: role in apoptosis and tumorigenesis. Pflugers Arch (In press)

  77. Poole RC, Halestrap AP (1993) Transport of lactate and other monocarboxylates across mammalian plasma membranes. Am J Physiol 264:C761–C782

    CAS  PubMed  Google Scholar 

  78. Sherman IW, Prudhomme J, Tait JF (1997) Altered membrane phospholipid asymmetry in Plasmodium falciparum-infected erythrocytes. Parasitol Today 13:242–243

    Article  Google Scholar 

  79. Sherman IW, Eda S, Winograd E (2003) Cytoadherence and sequestration in Plasmodium falciparum: defining the ties that bind. Microbes Infect 5:897–909

    Article  CAS  PubMed  Google Scholar 

  80. Staines HM, Chang W, Ellory JC, Tiffert T, Kirk K, Lew VL (1999) Passive Ca2+ transport and Ca2+-dependent K+ transport in Plasmodium falciparum-infected red cells. J Membr Biol 172:13–24

    Article  CAS  PubMed  Google Scholar 

  81. Staines HM, Rae C, Kirk K (2000) Increased permeability of the malaria-infected erythrocyte to organic cations. Biochim Biophys Acta 1463:88–98

    Article  CAS  PubMed  Google Scholar 

  82. Staines HM, Ellory JC, Kirk K (2001) Perturbation of the pump-leak balance for Na+ and K+ in malaria-infected erythrocytes. Am J Physiol 280:C1576–C1587

    CAS  Google Scholar 

  83. Staines HM, Powell T, Ellory JC, Egee S, Lapaix F, Decherf G, Thomas SL, Duranton C, Lang F, Huber SM (2003) Modulation of whole-cell currents in Plasmodium falciparum-infected human red blood cells by holding potential and serum. J Physiol (Lond) 552:177–183

    Google Scholar 

  84. Szabo I, Adams C, Gulbins E (2004) Ion channels and membrane rafts in apoptosis. Pflugers Arch (In press)

  85. Szabo I, Gulbins E, Apfel H, Zhang X, Barth P, Busch AE, Schlottmann K, Pongs O, Lang F (1996) Tyrosine phosphorylation-dependent suppression of a voltage-gated K+ channel in T lymphocytes upon Fas stimulation. J Biol Chem 271:20465–20469

    CAS  PubMed  Google Scholar 

  86. Szabo I, Gulbins E, Lang F (1997) Regulation of Kv1.3 during Fas-induced apoptosis. Cell Physiol Biochem 7:148–158

    CAS  Google Scholar 

  87. Szabo I, Lepple-Wienhues A, Kaba KN, Zoratti M, Gulbins E, Lang F (1998) Tyrosine kinase-dependent activation of a chloride channel in CD95-induced apoptosis in T lymphocytes. Proc Natl Acad Sci USA 95:6169–6174

    CAS  PubMed  Google Scholar 

  88. Thomas SL, Egee S, Lapaix F, Kaestner L, Staines HM, Ellory JC (2001) Malaria parasite Plasmodium gallinaceum up-regulates host red blood cell channels. FEBS Lett 500:45–51

    Article  CAS  PubMed  Google Scholar 

  89. Tiffert T, Staines HM, Ellory JC, Lew VL (2000) Functional state of the plasma membrane Ca2+ pump in Plasmodium falciparum-infected human red blood cells. J Physiol (Lond) 525:125–134

    Google Scholar 

  90. Wang Z (2004) K+ Channels in tumor cells and their role in regulating tumor cell proliferation and apoptosis. Pflugers Arch (In press)

  91. Wasserman M (1990) The role of calcium ions in the invasion of Plasmodium falciparum. Blood Cells 16:450–451

    CAS  PubMed  Google Scholar 

  92. Wasserman M, Alarcon C, Mendoza PM (1982) Effects of Ca++ depletion on the asexual cell cycle of Plasmodium falciparum. Am J Trop Med Hyg 31:711–717

    CAS  PubMed  Google Scholar 

  93. Wei L, Xiao AY, Jin C, Yang A, Lu ZY, Yu SP (2004) Distinct effects of chloride and potassium channel blockers on apoptotic cell shrinkage and apoptosis in cortical neurons. Pflugers Arch (In press)

Download references

Acknowledgements

The authors acknowledge the technical assistance of E. Faber and the meticulous preparation of the manuscript by Lejla Subasic. The work of the authors is supported by the Deutsche Forschungsgemeinschaft, Nr. La 315/4-3, La 315/6-1, DFG Schwerpunkt “Intrazelluläre Lebensformen” La 315/11-1, by the Landesschwerpunkt Baden-Württemberg “Dynamik und Modulation zellulärer Infektionsprozesse” and by the Bundesministerium für Bildung, Wissenschaft, Forschung und Technologie (Centre for Interdisciplinary Clinical Research) 01 KS 9602.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Florian Lang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lang, F., Lang, P.A., Lang, K.S. et al. Channel-induced apoptosis of infected host cells—the case of malaria. Pflugers Arch - Eur J Physiol 448, 319–324 (2004). https://doi.org/10.1007/s00424-004-1254-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-004-1254-9

Keywords

Navigation