Purinoceptor signaling in malaria-infected erythrocytes

Microbes and Infection

Volumn 14, Issue 10, 2012, Pages 779-786

  Huber, Stephan M ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

ATP release; Malaria; New permeability pathways; Patch clamp recording; Plasmodium falciparum; Purinergic signaling

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL TOXIN; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y1 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PURINERGIC P2Y4 RECEPTOR; PURINERGIC P2Y6 RECEPTOR; PURINERGIC RECEPTOR;

ARTICLE; AUTOCRINE EFFECT; BLOOD PARASITE; BLOOD VESSEL TONE; CELL ACTIVATION; CELL DEATH; CELL MEMBRANE PERMEABILITY; CELL TYPE; ERYTHROCYTE; ESCHERICHIA COLI; HEMOLYSIS; HOST; HUMAN; HYPERCAPNIA; HYPOXIA; MALARIA; NONHUMAN; PRIORITY JOURNAL; SEPTICEMIA; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; CELL MEMBRANE PERMEABILITY; ERYTHROCYTES; HUMANS; MALARIA; PLASMODIUM; RECEPTORS, PURINERGIC; SIGNAL TRANSDUCTION;

PLASMODIUM FALCIPARUM;

EID: 84863852840     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2012.04.009     Document Type: Article

References (95)

1. Sluyter R., Shemon A.N., Barden J.A., Wiley J.S. Extracellular ATP increases cation fluxes in human erythrocytes by activation of the P2X7 receptor. J. Biol. Chem. 2004, 279:44749-44755.
2. Y. Zhang, Y. Xia, Adenosine signaling in normal and sickle erythrocytes and beyond, Microbes Infect. (this issue).
3. Sprague R.S., Bowles E.A., Achilleus D., Ellsworth M.L. Erythrocytes as controllers of perfusion distribution in the microvasculature of skeletal muscle. Acta Physiol. (Oxf.) 2011, 202:285-292.
4. Bouyer G., Thomas S.L., Egée S. Protein kinase-regulated Inwardly rectifying anion and organic osmolyte channels in malaria-infected erythrocytes. Open Biol. J. 2011, 4:10-17.
5. Lang F., Birka C., Myssina S., Lang K.S., Lang P.A., Tanneur V., Duranton C., Wieder T., Huber S.M. Erythrocyte ion channels in regulation of apoptosis. Adv. Exp. Med. Biol. 2004, 559:211-217.
6. Bouyer G., Cueff A., Egee S., Kmiecik J., Maksimova Y., Glogowska E., Gallagher P.G., Thomas S.L. Erythrocyte peripheral type benzodiazepine receptor/voltage-dependent anion channels are upregulated by Plasmodium falciparum. Blood 2011, 118:2305-2312.
7. Thomas S.L., Bouyer G., Cueff A., Egee S., Glogowska E., Ollivaux C. Ion channels in human red blood cell membrane: actors or relics?. Blood Cells Mol. Dis. 2011, 46:261-265.
8. Merckx A., Bouyer G., Thomas S.L., Langsley G., Egee S. Anion channels in Plasmodium-falciparum-infected erythrocytes and protein kinase A. Trends Parasitol. 2009, 25:139-144.
9. Bouyer G., Egee S., Thomas S.L. Toward a unifying model of malaria-induced channel activity. Proc. Natl. Acad. Sci. U.S.A 2007, 104:11044-11049.
10. Bouyer G., Egee S., Thomas S.L. Three types of spontaneously active anionic channels in malaria-infected human red blood cells. Blood Cells Mol. Dis. 2006, 36:248-254.
11. Thomas S.L., Egee S., Lapaix F., Kaestner L., Staines H.M., Ellory J.C. Malaria parasite Plasmodium gallinaceum up-regulates host red blood cell channels. FEBS Lett. 2001, 500:45-51.
12. Decherf G., Egee S., Staines H.M., Ellory J.C., Thomas S.L. Anionic channels in malaria-infected human red blood cells. Blood Cells Mol. Dis. 2004, 32:366-371.
13. Egee S., Lapaix F., Decherf G., Staines H.M., Ellory J.C., Doerig C., Thomas S.L. A stretch-activated anion channel is up-regulated by the malaria parasite Plasmodium falciparum. J. Physiol. 2002, 542:795-801.
14. Huber S.M., Uhlemann A.C., Gamper N.L., Duranton C., Kremsner P.G., Lang F. Plasmodium falciparum activates endogenous Cl(-) channels of human erythrocytes by membrane oxidation. EMBO J. 2002, 21:22-30.
15. 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, 13:189-198.
16. Huber S.M., Duranton C., Henke G., Van De Sand C., Heussler V., Shumilina E., Sandu C.D., Tanneur V., Brand V., Kasinathan R.S., Lang K.S., Kremsner P.G., Hubner C.A., Rust M.B., Dedek K., Jentsch T.J., Lang F. Plasmodium induces swelling-activated ClC-2 anion channels in the host erythrocyte. J. Biol. Chem. 2004, 279:41444-41452.
17. Tanneur V., Duranton C., Brand V.B., Sandu C.D., Akkaya C., Kasinathan R.S., Gachet C., Sluyter R., Barden J.A., Wiley J.S., Lang F., Huber S.M. Purinoceptors are involved in the induction of an osmolyte permeability in malaria-infected and oxidized human erythrocytes. FASEB J. 2006, 20:133-135.
18. Foller M., Bobbala D., Koka S., Boini K.M., Mahmud H., Kasinathan R.S., Shumilina E., Amann K., Beranek G., Sausbier U., Ruth P., Sausbier M., Lang F., Huber S.M. Functional significance of the intermediate conductance Ca2+-activated K+ channel for the short-term survival of injured erythrocytes. Pflugers Arch. 2010, 460:1029-1044.
19. Ginsburg H., Krugliak M., Eidelman O., Cabantchik Z.I. New permeability pathways induced in membranes of Plasmodium falciparum infected erythrocytes. Mol. Biochem. Parasitol. 1983, 8:177-190.
20. Kirk K. Membrane transport in the malaria-infected erythrocyte. Physiol. Rev. 2001, 81:495-537.
21. Lew V.L., 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, 32:353-359.
22. Huber S.M., Duranton C., Lang F. Patch-clamp analysis of the "new permeability pathways" in malaria-infected erythrocytes. Int. Rev. Cytol. 2005, 246:59-134.
23. Staines H.M., Alkhalil A., Allen R.J., De Jonge H.R., Derbyshire E., Egee S., Ginsburg H., Hill D.A., Huber S.M., Kirk K., Lang F., Lisk G., Oteng E., Pillai A.D., Rayavara K., Rouhani S., Saliba K.J., Shen C., Solomon T., Thomas S.L., Verloo P., Desai S.A. Electrophysiological studies of malaria parasite-infected erythrocytes: current status. Int. J. Parasitol. 2007, 37:475-482.
24. Shumilina E., Huber S.M. Clc-2 channels in erythrocytes. Open Biol. J. 2011, 4:18-26.
25. Nguitragool W., Bokhari A.A., Pillai A.D., Rayavara K., Sharma P., Turpin B., Aravind L., Desai S.A. Malaria parasite clag3 genes determine channel-mediated nutrient uptake by infected red blood cells. Cell 2011, 145:665-677.
26. A.A. Holder, M.A.M. Ridzuan, J.L. Green, Calcium dependent protein kinase 1 and calcium fluxes in the malaria parasite, Microbes Infect. (this issue).
27. S. Singh, C.E. Chitnis, Signaling mechanisms involved in apical organelle discharge during invasion of apicomplexan parasites, Microbes Infect. (this issue).
28. A. Touré, G. Langsley, S. Egée, "Spermatozoa and Plasmodium zoites: the same way to invade oocyte and host cells?" Microbes Infect. (this issue).
29. R.M. Fairhurst, C.D. Bess, M.A. Krause, Abnormal PfEMP1/knob display on Plasmodium falciparum-infected erythrocytes containing hemoglobin variants: fresh insights into malaria pathogenesis and protection, Microbes Infect. (this issue).
30. Atamna H., Ginsburg H. Origin of reactive oxygen species in erythrocytes infected with Plasmodium falciparum. Mol. Biochem. Parasitol. 1993, 61:231-241.
31. Duranton C., Huber S.M., Tanneur V., Brand V.B., Akkaya C., Shumilina E.V., Sandu C.D., Lang F. Organic osmolyte permeabilities of the malaria-induced anion conductances in human erythrocytes. J. Gen. Physiol. 2004, 123:417-426.
32. Lang P.A., Kasinathan R.S., Brand V.B., Duranton C., Lang C., Koka S., Shumilina E., Kempe D.S., Tanneur V., Akel A., Lang K.S., Foller M., Kun J.F., Kremsner P.G., Wesselborg S., Laufer S., Clemen C.S., Herr C., Noegel A.A., Wieder T., Gulbins E., Lang F., Huber S.M. Accelerated clearance of Plasmodium-infected erythrocytes in sickle cell trait and annexin-A7 deficiency. Cell. Physiol. Biochem. 2009, 24:415-428.
33. A. Budu, C.R.S. Garcia, Generation of second messengers in Plasmodium, Microbes Infect. (this issue).
34. C.S. Hopp, P.W. Bowyer, D.A. Baker, The role of cGMP signalling in regulating life cycle progression of Plasmodium, Microbes Infect. (this issue).
35. E. Lasonder, M. Treeck, M. Alam, A.B. Tobin, Insights in to the P. falciparum schizont phospho-proteome, Microbes Infect. (this issue).
36. N.M. Haste, H. Talabani, A. Doo, A. Merckx, G. Langsley, S.S. Taylor, Exploring the Plasmodium falciparum cyclic-adenosine monophosphate (cAMP)-dependent Protein kinase (PfPKA) as a therapeutic target, Microbes Infect. (this issue).
37. D. Miranda-Saavedra, T. Gabaldón, G.J. Barton, G. Langsley, C. Doerig, The kinomes of apicomplexan parasites, Microbes Infect. (this issue).
38. Bergfeld G.R., Forrester T. Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia. Cardiovasc. Res. 1992, 26:40-47.
39. Sprague R.S., Ellsworth M.L., Stephenson A.H., Kleinhenz M.E., Lonigro A.J. Deformation-induced ATP release from red blood cells requires CFTR activity. Am. J. Physiol. 1998, 275:H1726-H1732.
40. Edwards J., Sprung R., Sprague R., Spence D. Chemiluminescence detection of ATP release from red blood cells upon passage through microbore tubing. Analyst 2001, 126:1257-1260.
41. Sprung R., Sprague R., Spence D. Determination of ATP release from erythrocytes using microbore tubing as a model of resistance vessels in vivo. Anal. Chem. 2002, 74:2274-2278.
42. Ellsworth M.L., Forrester T., Ellis C.G., Dietrich H.H. The erythrocyte as a regulator of vascular tone. Am. J. Physiol. Heart Circ. Physiol. 1995, 269:H2155-H2161.
43. Locovei S., Bao L., Dahl G. Pannexin 1 in erythrocytes: function without a gap. Proc. Natl. Acad. Sci. U.S.A 2006, 103:7655-7659.
44. Sprague R.S., Bowles E.A., Hanson M.S., DuFaux E.A., Sridharan M., Adderley S., Ellsworth M.L., Stephenson A.H. Prostacyclin analogs stimulate receptor-mediated cAMP synthesis and ATP release from rabbit and human erythrocytes. Microcirculation 2008, 15:461-471.
45. Sprague R., Bowles E., Stumpf M., Ricketts G., Freidman A., Hou W.H., Stephenson A., Lonigro A. Rabbit erythrocytes possess adenylyl cyclase type II that is activated by the heterotrimeric G proteins Gs and Gi. Pharmacol. Rep. 2005, 57(Suppl):222-228.
46. Adderley S.P., Sridharan M., Bowles E.A., Stephenson A.H., Sprague R.S., Ellsworth M.L. Inhibition of ATP release from erythrocytes: a role for EPACs and PKC. Microcirculation 2011, 18:128-135.
47. Knofler R., Weissbach G., Kuhlisch E. Release of adenosine triphosphate by adenosine diphosphate in whole blood and in erythrocyte suspensions. Am. J. Hematol. 1997, 56:259-265.
48. Olearczyk J.J., Stephenson A.H., Lonigro A.J., Sprague R.S. Receptor-mediated activation of the heterotrimeric G-protein Gs results in ATP release from erythrocytes. Med. Sci. Monit. 2001, 7:669-674.
49. Sprague R.S., Bowles E.A., Olearczyk J.J., Stephenson A.H., Lonigro A.J. The role of G protein beta subunits in the release of ATP from human erythrocytes. J. Physiol. Pharmacol. 2002, 53:667-674.
50. Olearczyk J.J., Stephenson A.H., Lonigro A.J., Sprague R.S. NO inhibits signal transduction pathway for ATP release from erythrocytes via its action on heterotrimeric G protein Gi. Am. J. Physiol. Heart Circ. Physiol. Circ. Physiol. 2004, 287:H748-H754.
51. Sprague R.S., Ellsworth M.L., Stephenson A.H., Lonigro A.J. Participation of cAMP in a signal-transduction pathway relating erythrocyte deformation to ATP release. Am. J. Physiol. Cell. Physiol. 2001, 281:C1158-C1164.
52. Adderley S.P., Sridharan M., Bowles E.A., Stephenson A.H., Ellsworth M.L., Sprague R.S. Protein kinases A and C regulate receptor-mediated increases in cAMP in rabbit erythrocytes. Am. J. Physiol. Heart Circ. Physiol. 2010, 298:H587-H593.
53. Laing G., Stephenson A.H., Lonigro A.J., Sprague R.S. Erythrocytes of humans with cystic fibrosis fail to stimulate nitric oxide synthesis in isolated rabbit lungs. Am. J. Physiol. Heart Circ. Physiol. 2004, 288:H1580-H1585.
54. Adderley S.P., Thuet K.M., Sridharan M., Bowles E.A., Stephenson A.H., Ellsworth M.L., Sprague R.S. Identification of cytosolic phosphodiesterases in the erythrocyte: a possible role for PDE5. Med. Sci. Monit. 2011, 17:CR241-247.
55. Hanson M.S., Stephenson A.H., Bowles E.A., Sprague R.S. Insulin inhibits human erythrocyte cAMP accumulation and ATP release: role of phosphodiesterase 3 and phosphoinositide 3-kinase. Exp. Biol. Med. (Maywood) 2010, 235:256-262.
56. Sprague R.S., Ellsworth M.L., Stephenson A.H., Lonigro A.J. ATP: the red blood cell link to NO and local control of the pulmonary circulation. Am. J. Physiol. Heart Circ. Physiol. 1996, 271:H2717-H2722.
57. Sprague R.S., Olearczyk J.J., Spence D.M., Stephenson A.H., Sprung R.W., Lonigro A.J. Extracellular ATP signaling in the rabbit lung: erythrocytes as determinants of vascular resistance. Am. J. Physiol. Heart Circ. Physiol. 2003, 285:H693-H700.
58. Sprague R.S., Stephenson A.H., Dimmitt R.A., Weintraub N.L., Branch C.A., McMurdo L., Lonigro A.J. Effect of L-NAME on pressure-flow relationships in isolated rabbit lungs: role of red blood cells. Am. J. Physiol. Heart Circ. Physiol. 1995, 269:H1941-H1948.
59. Olearczyk J.J., Ellsworth M.L., Stephenson A.H., Lonigro A.J., Sprague R.S. Nitric oxide inhibits ATP release from erythrocytes. J. Pharmacol. Exp. Ther. 2004, 309:1079-1084.
60. Dietrich H.H., Ellsworth M.L., Sprague R.S., Dacey R.G. Red blood cell regulation of microvascular tone through adenosine triphosphate. Am. J. Physiol. Heart Circ. Physiol. 2000, 278:H1294-H1298.
61. Sprague R.S., Stephenson A.H., Ellsworth M.L., Keller C., Lonigro A.J. Impaired release of ATP from red blood cells of humans with primary pulmonary hypertension. Exp. Biol. Med. (Maywood) 2001, 226:434-439.
62. Sprague R.S., Stephenson A.H., Bowles E.A., Stumpf M.S., Lonigro A.J. Reduced expression of G(i) in erythrocytes of humans with type 2 diabetes is associated with impairment of both cAMP generation and ATP release. Diabetes 2006, 55:3588-3593.
63. Hanson M.S., Ellsworth M.L., Achilleus D., Stephenson A.H., Bowles E.A., Sridharan M., Adderley S., Sprague R.S. Insulin inhibits low oxygen-induced ATP release from human erythrocytes: implication for vascular control. Microcirculation 2009, 16:424-433.
64. Sridharan M., Adderley S.P., Bowles E.A., Egan T.M., Stephenson A.H., Ellsworth M.L., Sprague R.S. Pannexin 1 is the conduit for low oxygen tension-induced ATP release from human erythrocytes. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:H1146-H1152.
65. Qiu F., Wang J., Spray D.C., Scemes E., Dahl G. Two non-vesicular ATP release pathways in the mouse erythrocyte membrane. FEBS Lett. 2011, 585:3430-3435.
66. Sridharan M., Bowles E.A., Richards J.P., Krantic M., Davis K.L., Dietrich K.A., Stephenson A.H., Ellsworth M.L., Sprague R.S. Prostacyclin receptor-mediated ATP release from erythrocytes requires the voltage-dependent anion channel (VDAC). Am. J. Physiol. Heart Circ. Physiol. 2011.
67. Hoffman J.F., Dodson A., Wickrema A., Dib-Hajj S.D. Tetrodotoxin-sensitive Na+ channels and muscarinic and purinergic receptors identified in human erythroid progenitor cells and red blood cell ghosts. Proc. Natl. Acad. Sci. U.S.A 2004, 101:12370-12374.
68. Sluyter R., Shemon A.N., Wiley J.S. P2X(7) receptor activation causes phosphatidylserine exposure in human erythrocytes. Biochem. Biophys. Res. Commun. 2007, 355:169-173.
69. Skals M., Jorgensen N.R., Leipziger J., Praetorius H.A. Alpha-hemolysin from Escherichia coli uses endogenous amplification through P2X receptor activation to induce hemolysis. Proc. Natl. Acad. Sci. U.S.A 2009, 106:4030-4035.
70. Wang L., Olivecrona G., Gotberg M., Olsson M.L., Winzell M.S., Erlinge D. ADP acting on P2Y13 receptors is a negative feedback pathway for ATP release from human red blood cells. Circ. Res. 2005, 96:189-196.
71. Skals M., Leipziger J., Praetorius H.A. Haemolysis induced by alpha-toxin from Staphylococcus aureus requires P2X receptor activation. Pflugers Arch. 2011, 462:669-679.
72. Skals M., Jensen U.B., Ousingsawat J., Kunzelmann K., Leipziger J., Praetorius H.A. Escherichia coli alpha-hemolysin triggers shrinkage of erythrocytes via K(Ca)3.1 and TMEM16A channels with subsequent phosphatidylserine exposure. J. Biol. Chem. 2010, 285:15557-15565.
73. Schwiebert E.M., Egan M.E., Hwang T.H., Fulmer S.B., Allen S.S., Cutting G.R., Guggino W.B. CFTR regulates outwardly rectifying chloride channels through an autocrine mechanism involving ATP. Cell 1995, 81:1063-1073.
74. Braunstein G.M., Roman R.M., Clancy J.P., Kudlow B.A., Taylor A.L., Shylonsky V.G., Jovov B., Peter K., Jilling T., Ismailov, Benos D.J., Schwiebert L.M., Fitz J.G., Schwiebert E.M. 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. 2001, 276:6621-6630.
75. Barriere H., Belfodil R., Rubera I., Tauc M., Poujeol C., Bidet M., Poujeol P. CFTR null mutation altered cAMP-sensitive and swelling-activated Cl- currents in primary cultures of mouse nephron. Am. J. Physiol. Ren. Physiol. 2003, 284:F796-F811.
76. Ollivier H., Pichavant-Rafini K., Puill-Stephan E., Calves P., Nonnotte L., Nonnotte G. Effects of hypo-osmotic stress on ATP release in isolated turbot (Scophthalmus maximus) hepatocytes. Biol. Cell 2006, 98:427-437.
77. Hazama A., Shimizu T., Ando-Akatsuka Y., Hayashi S., Tanaka S., Maeno E., Okada Y. Swelling-induced, CFTR-independent ATP release from a human epithelial cell line: lack of correlation with volume-sensitive cl(-) channels. J. Gen. Physiol. 1999, 114:525-533.
78. Okada S.F., Nicholas R.A., Kreda S.M., Lazarowski E.R., Boucher R.C. Physiological regulation of ATP release at the apical surface of human airway epithelia. J. Biol. Chem. 2006, 281:22992-23002.
79. Sabirov R.Z., Dutta A.K., Okada Y. Volume-dependent ATP-conductive large-conductance anion channel as a pathway for swelling-induced ATP release. J. Gen. Physiol. 2001, 118:251-266.
80. Bell P.D., Lapointe J.Y., Peti-Peterdi J. Macula densa cell signaling. Annu. Rev. Physiol. 2003, 65:481-500.
81. Bell P.D., Lapointe J.Y., Sabirov R., Hayashi S., Peti-Peterdi J., Manabe K., Kovacs G., Okada Y. Macula densa cell signaling involves ATP release through a maxi anion channel. Proc. Natl. Acad. Sci. U.S.A 2003, 100:4322-4327.
82. Dutta A.K., Sabirov R.Z., Uramoto H., Okada Y. Role of ATP-conductive anion channel in ATP release from neonatal rat cardiomyocytes in ischaemic or hypoxic conditions. J. Physiol. 2004, 559:799-812.
83. Light D.B., Dahlstrom P.K., Gronau R.T., Baumann N.L. Extracellular ATP activates a P2 receptor in necturus erythrocytes during hypotonic swelling. J. Membr. Biol. 2001, 182:193-202.
84. Akkaya C., Shumilina E., Bobballa D., Brand V.B., Mahmud H., Lang F., Huber S.M. The Plasmodium falciparum-induced anion channel of human erythrocytes is an ATP-release pathway. Pflugers Arch. 2009, 457:1035-1047.
85. Duranton C., Tanneur V., Lang C., Brand V.B., Koka S., Kasinathan R.S., Dorsch M., Hedrich H.J., Baumeister S., Lingelbach K., Lang F., Huber S.M. A high specificity and affinity interaction with serum albumin stimulates an anion conductance in malaria-infected erythrocytes. Cell. Physiol. Biochem. 2008, 22:395-404.
86. Staines H.M., Powell T., Ellory J.C., Egee S., Lapaix F., Decherf G., Thomas S.L., Duranton C., Lang F., Huber S.M. Modulation of whole-cell currents in Plasmodium falciparum-infected human red blood cells by holding potential and serum. J. Physiol. 2003, 552:177-183.
87. Huber S.M., Lang C., Lang F., Duranton C. Organic osmolyte channels in malaria-infected erythrocytes. Biochem. Biophys. Res. Commun. 2008, 376:514-518.
88. Glogowska E., Dyrda A., Cueff A., Bouyer G., Egee S., Bennekou P., Thomas S.L. Anion conductance of the human red cell is carried by a maxi-anion channel. Blood Cells Mol. Dis. 2010, 44:243-251.
89. Sabirov R.Z., Okada Y. Wide nanoscopic pore of maxi-anion channel suits its function as an ATP-conductive pathway. Biophys. J. 2004, 87:1672-1685.
90. Sabirov R.Z., Okada Y. ATP release via anion channels. Purinergic Signal. 2005, 1:311-328.
91. Olson J.M., Ciliax B.J., Mancini W.R., Young A.B. Presence of peripheral-type benzodiazepine binding sites on human erythrocyte membranes. Eur. J. Pharmacol. 1988, 152:47-53.
92. Thinnes F.P., Gotz H., Kayser H., Benz R., Schmidt W.E., Kratzin H.D., Hilschmann N. Identification of human porins. I. Purification of a porin from human B-lymphocytes (Porin 31HL) and the topochemical proof of its expression on the plasmalemma of the progenitor cell. Biol. Chem. Hoppe Seyler 1989, 370:1253-1264.
93. Veenman L., Gavish M. The peripheral-type benzodiazepine receptor and the cardiovascular system. Implications for drug development. Pharmacol. Ther. 2006, 110:503-524.
94. Sabirov R.Z., Merzlyak P.G. Plasmalemmal VDAC controversies and maxi-anionchannel puzzle. Biochim. Biophys. Acta. 2012, 1818:1570-1580.
95. Levano-Garcia J., Dluzewski A.R., Markus R.P., Garcia C.R. Purinergic signalling is involved in the malaria parasite Plasmodium falciparum invasion to red blood cells. Purinergic Signal. 2010, 6:365-372.