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Permeabilization of Host Cell Membrane

  • Living reference work entry
  • First Online:
Encyclopedia of Malaria

  • 343 Accesses

Synonyms

Host membrane permeability; Ion channel; New permeation pathways

Definition

By replicating within red blood cells, malaria parasites are largely hidden from immune recognition, but parasites enter an unusual closed environment where some nutrients are limited and where accumulation of hazardous metabolic end products can rapidly become deleterious. Therefore, to survive within erythrocytes, parasites circumvent the relative low permeability of the host plasma membrane by altering the permeability of the host plasma membrane either by upregulating existing carriers or by creating new permeation pathways (NPPs). Recent electrophysiological studies of Plasmodium-infected erythrocytes have demonstrated that these changes reflect transmembrane transports through ion channels or pores in the infected erythrocyte.

Introduction

The intraerythrocytic stage of malaria parasite’s life cycle allows Plasmodiumgenus to escape host immune system threatening and recognition. However, by...

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References

  • Baumeister S, Winterberg M, Duranton C, Huber SM, Lang F, Kirk K, Lingelbach K. 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.

    Article  CAS  PubMed  Google Scholar 

  • Bernhardt I, Ellory JC. Red cell membrane transport in Health and disease. Berlin/Heidelberg: Springer; 2003.

    Book  Google Scholar 

  • Bouyer G, Egee S, Thomas SL. Three types of spontaneously active anionic channels in malaria-infected human red blood cells. Blood Cells Mol Dis. 2006;36(2):248–54.

    Article  CAS  PubMed  Google Scholar 

  • Bouyer G, Egee S, Thomas SL. Toward a unifying model of malaria-induced channel activity. Proc Natl Acad Sci U S A. 2007;104(26):11044–9.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bouyer G, Thomas SLY, Egee S. Protein kinase-regulated inwardly rectifying anion and organic osmolyte channels in malaria-infected erythrocytes. Open Biol J. 2011;4:10–7.

    Article  CAS  Google Scholar 

  • Bouyer G, Thomas S, Egée S (2012) Patch-clamp analysis of membrane transport in erythrocytes, In: Kaneez FS, editor. Patch clamp technique, ISBN: 978-953-51-0406-3, InTech, Available from: http://www.intechopen.com/books/patch-clamp-technique/patch-clamp-analysis-of-membrane-transport-in-erythrocytes

  • Cobbold SA, Martin RE, Kirk K. Methionine transport in the malaria parasite Plasmodium falciparum. Int J Parasitol. 2011;41(1):125–35.

    Article  CAS  PubMed  Google Scholar 

  • Cohn JV, Alkhalil A, Wagner MA, Rajapandi T, Desai SA. Extracellular lysines on the plasmodial surface anion channel involved in Na + exclusion. Mol Biochem Parasitol. 2003;132(1):27–34.

    Article  CAS  PubMed  Google Scholar 

  • Desai SA. Why do malaria parasites increase host erythrocyte permeability? Trends Parasitol. 2014;30(3):151–9.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Desai SA, McCleskey EW, Schlesinger PH, Krogstad DJ. A novel pathway for Ca++ entry into Plasmodium falciparum-infected blood cells. Am J Trop Med Hyg. 1996;54(5):464–70.

    CAS  PubMed  Google Scholar 

  • 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):1001–5.

    Article  CAS  PubMed  Google Scholar 

  • Duranton C, Huber S, Tanneur V, Lang K, Brand V, Sandu C, Lang F. Electrophysiological properties of the Plasmodium falciparum-induced cation conductance of human erythrocytes. Cell Physiol Biochem. 2003;13(4):189–98.

    Article  CAS  PubMed  Google Scholar 

  • Egee S, Lapaix F, Decherf G, Staines HM, Ellory JC, Doerig C, Thomas SL. A stretch-activated anion channel is up-regulated by the malaria parasite Plasmodium falciparum. J Physiol. 2002;542(Pt 3):795–801.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ekland EH, Akabas MH, Fidock DA. Taking charge: feeding malaria via anion channels. Cell. 2011;145(5):645–7.

    Article  CAS  PubMed  Google Scholar 

  • Esposito A, Tiffert T, Mauritz JM, Schlachter S, Bannister LH, Kaminski CF, Lew VL. FRET imaging of hemoglobin concentration in Plasmodium falciparum-infected red cells. PLoS One. 2008;3(11):e3780.

    Article  PubMed Central  PubMed  Google Scholar 

  • Fishbein WN, Davis JI, Foellmer JW, Casey MR. Clinical assay of the human erythrocyte lactate transporter. II. Analysis and display of normal human data. Biochem Med Metab Biol. 1988;39(3):351–9.

    Article  CAS  PubMed  Google Scholar 

  • Ginsburg H, Stein WD. The new permeability pathways induced by the malaria parasite in the membrane of the infected erythrocyte: comparison of results using different experimental techniques. J Membr Biol. 2004;197(2):113–34.

    Article  CAS  PubMed  Google Scholar 

  • Ginsburg H, Stein WD. How many functional transport pathways does Plasmodium falciparum induce in the membrane of its host erythrocyte? Trends Parasitol. 2005;21(3):118–21.

    Article  CAS  PubMed  Google Scholar 

  • Ginsburg H, Krugliak M, Eidelman O, Cabantchik ZI. New permeability pathways induced in membranes of Plasmodium falciparum infected erythrocytes. Mol Biochem Parasitol. 1983;8(2):177–90.

    Article  CAS  PubMed  Google Scholar 

  • Glogowska E, Dyrda A, Cueff A, Bouyer G, Egee S, Bennekou P, Thomas SL. Anion conductance of the human red cell is carried by a maxi-anion channel. Blood Cells Mol Dis. 2010;44(4):243–51.

    Article  CAS  PubMed  Google Scholar 

  • Halestrap AP. Monocarboxylate and other organic anion transport. In: Bernhardt I, Ellory JC, editors. Red cell membrane transport in health and disease. Berlin/Heidelberg: Springer; 2003.

    Google Scholar 

  • Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981;391(2):85–100.

    Article  CAS  PubMed  Google Scholar 

  • Hoffman JF, Joiner W, Nehrke K, Potapova O, Foye K, Wickrema A. The hSK4 (KCNN4) isoform is the Ca2 + -activated K+ channel (Gardos channel) in human red blood cells. Proc Natl Acad Sci U S A. 2003;100(12):7366–71.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Kaestner L, Christophersen P, Bernhardt I, Bennekou P. The non-selective voltage-activated cation channel in the human red blood cell membrane: reconciliation between two conflicting reports and further characterisation. Bioelectrochemistry. 2000;52(2):117–25.

    Article  CAS  PubMed  Google Scholar 

  • Kanaani J, Ginsburg H. Transport of lactate in Plasmodium falciparum-infected human erythrocytes. J Cell Physiol. 1991;149(3):469–76.

    Article  CAS  PubMed  Google Scholar 

  • Kirk K. Membrane transport in the malaria-infected erythrocyte. Physiol Rev. 2001;81(2):495–537.

    CAS  PubMed  Google Scholar 

  • Krugliak M, Ginsburg H. The evolution of the new permeability pathways in Plasmodium falciparum–infected erythrocytes–a kinetic analysis. Exp Parasitol. 2006;114(4):253–8.

    Article  CAS  PubMed  Google Scholar 

  • Krugliak M, Zhang J, Ginsburg H. Intraerythrocytic Plasmodium falciparum utilizes only a fraction of the amino acids derived from the digestion of host cell cytosol for the biosynthesis of its proteins. Mol Biochem Parasitol. 2002;119(2):249–56.

    Article  CAS  PubMed  Google Scholar 

  • Lew VL, Tiffert T, Ginsburg H. Excess hemoglobin digestion and the osmotic stability of Plasmodium falciparum-infected red blood cells. Blood. 2003;101(10):4189–94.

    Article  CAS  PubMed  Google Scholar 

  • Lew VL, Macdonald L, Ginsburg H, Krugliak M, Tiffert T. Excess haemoglobin digestion by malaria parasites: a strategy to prevent premature host cell lysis. Blood Cells Mol Dis. 2004;32(3):353–9.

    Article  CAS  PubMed  Google Scholar 

  • Martin RE, Kirk K. Transport of the essential nutrient isoleucine in human erythrocytes infected with the malaria parasite Plasmodium falciparum. Blood. 2007;109(5):2217–24.

    Article  CAS  PubMed  Google Scholar 

  • Martin RE, Henry RI, Abbey JL, Clements JD, Kirk K. The ‘permeome’ of the malaria parasite: an overview of the membrane transport proteins of Plasmodium falciparum. Genome Biol. 2005;6(3):R26.

    Article  PubMed Central  PubMed  Google Scholar 

  • Martin RE, Ginsburg H, Kirk K. Membrane transport proteins of the malaria parasite. Mol Microbiol. 2009;74(3):519–28.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • Nguitragool W, Bokhari AA, Pillai AD, Rayavara K, Sharma P, Turpin B, Aravind L, Desai SA. Malaria parasite clag3 genes determine channel-mediated nutrient uptake by infected red blood cells. Cell. 2011;145(5):665–77.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nguitragool W, Rayavara K, Desai SA. Proteolysis at a specific extracellular residue implicates integral membrane CLAG3 in malaria parasite nutrient channels. PLoS One. 2014;9(4):e93759.

    Article  PubMed Central  PubMed  Google Scholar 

  • Saliba KJ, Kirk K. Nutrient acquisition by intracellular apicomplexan parasites: staying in for dinner. Int J Parasitol. 2001;31(12):1321–30.

    Article  CAS  PubMed  Google Scholar 

  • Saliba KJ, Martin RE, Broer A, Henry RI, McCarthy CS, Downie MJ, Allen RJ, Mullin KA, McFadden GI, Broer S, et al. Sodium-dependent uptake of inorganic phosphate by the intracellular malaria parasite. Nature. 2006;443(7111):582–5.

    CAS  PubMed  Google Scholar 

  • 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):C1576–87.

    CAS  PubMed  Google Scholar 

  • Staines HM, Powell T, Ellory JC, Egee S, Lapaix F, Decherf G, Thomas SL, Duranton C, Lang F, Huber SM. Modulation of whole-cell currents in Plasmodium falciparum-infected human red blood cells by holding potential and serum. J Physiol. 2003;552(Pt 1):177–83.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Staines HM, Ashmore S, Felgate H, Moore J, Powell T, Ellory JC. 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. 2006;108(9):3187–94.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Staines HM, Alkhalil A, Allen RJ, De Jonge HR, Derbyshire E, Egee S, Ginsburg H, Hill DA, Huber SM, Kirk K, et al. Electrophysiological studies of malaria parasite-infected erythrocytes: current status. Int J Parasitol. 2007;37(5):475–82.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vander Jagt DL, Hunsaker LA, Campos NM, Baack BR. D-lactate production in erythrocytes infected with Plasmodium falciparum. Mol Biochem Parasitol. 1990;42(2):277–84.

    Article  CAS  PubMed  Google Scholar 

  • Zarchin S, Krugliak M, Ginsburg H. Digestion of the host erythrocyte by malaria parasites is the primary target for quinoline-containing antimalarials. Biochem Pharmacol. 1986;35(14):2435–42.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The labex GR-Ex, reference ANR-11-LABX-0051 is funded by the program “Investissements d’avenir” of the French National Research Agency, reference ANR-11-IDEX-0005-02.

Author information

Authors and Affiliations

  1. Integrative Biology of Marine Models, Comparative Physiology of Erythrocytes, Station Biologique de Roscoff, Sorbonne Universités, UPMC Univ. Paris 06, UMR 8227, Roscoff, France

    Stéphane Egée, Guillaume Bouyer & Serge L. Y. Thomas

  2. Integrative Biology of Marine Models, Comparative Physiology of Erythrocytes, Station Biologique de Roscoff, CNRS, UMR 8227, Roscoff, France

    Stéphane Egée, Guillaume Bouyer & Serge L. Y. Thomas

  3. Laboratory of Excellence GR-Ex, Paris, France

    Stéphane Egée, Guillaume Bouyer & Serge L. Y. Thomas

Authors
  1. Stéphane Egée
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  2. Guillaume Bouyer
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  3. Serge L. Y. Thomas
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Corresponding author

Correspondence to Stéphane Egée .

Editor information

Editors and Affiliations

  1. Heswall, United Kingdom

    Marcel Hommel

  2. Institut für Tropenmedizin, Universität Tübingen, Tübingen, Germany

    Peter G. Kremsner

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Egée, S., Bouyer, G., Thomas, S.L.Y. (2015). Permeabilization of Host Cell Membrane. In: Hommel, M., Kremsner, P. (eds) Encyclopedia of Malaria. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8757-9_38-1

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  • DOI: https://doi.org/10.1007/978-1-4614-8757-9_38-1

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  • Online ISBN: 978-1-4614-8757-9

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