Leal Denis, M.F.; Incicco, J.J.; Espelt, M.V.; Verstraeten, S.V.; Pignataro, O.P.; Lazarowski, E.R.; Schwarzbaum, P.J. "Kinetics of extracellular ATP in mastoparan 7-activated human erythrocytes" (2013) Biochimica et Biophysica Acta - General Subjects. 1830(10):4692-4707
El editor solo permite decargar el artículo en su versión post-print desde el repositorio. Por favor, si usted posee dicha versión, enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor


Background The peptide mastoparan 7 (MST7) stimulated ATP release in human erythrocytes. We explored intra- and extracellular processes governing the time-dependent accumulation of extracellular ATP (i.e., ATPe kinetics). Methods Human erythrocytes were treated with MST7 in the presence or absence of two blockers of pannexin 1. ATPe concentration was monitored by luciferin-luciferase based real-time luminometry. Results Exposure of human erythrocytes to MST7 led to an acute increase in [ATPe], followed by a slower increase phase. ATPe kinetics reflected a strong activation of ATP efflux and a low rate of ATPe hydrolysis by ectoATPase activity. Enhancement of [ATPe] by MST7 required adhesion of erythrocytes to poly-D-lysin-coated coverslips, and correlated with a 31% increase of cAMP and 10% cell swelling. However, when MST7 was dissolved in a hyperosmotic medium to block cell swelling, ATPe accumulation was inhibited by 49%. Erythrocytes pre-exposure to 10 μM of either carbenoxolone or probenecid, two blockers of pannexin 1, exhibited a partial reduction of ATP efflux. Erythrocytes from pannexin 1 knockout mice exhibited similar ATPe kinetics as those of wild type mice erythrocytes exposed to pannexin 1 blockers. Conclusions MST7 induced release of ATP required either cell adhesion or strong activation of cAMP synthesis. Part of this release required cell swelling. Kinetic analysis and a data driven model suggested that ATP efflux is mediated by two ATP conduits displaying different kinetics, with one conduit being fully blocked by pannexin 1 blockers. General significance Kinetic analysis of extracellular ATP accumulation from human erythrocytes and potential effects on microcirculation. © 2013 Elsevier B.V.


Documento: Artículo
Título:Kinetics of extracellular ATP in mastoparan 7-activated human erythrocytes
Autor:Leal Denis, M.F.; Incicco, J.J.; Espelt, M.V.; Verstraeten, S.V.; Pignataro, O.P.; Lazarowski, E.R.; Schwarzbaum, P.J.
Filiación:Department of Biological Chemistry, School of Pharmacy and Biochemistry, University of Buenos Aires, Buenos Aires, Argentina
Laboratory of Molecular Endocrinology and Signal Transduction, Institute of Biology and Experimental Medicine-CONICET, Vuelta de Obligado 2490, CP 1428 Buenos Aires, Argentina
Department of Biological Chemistry, School of Sciences, University of Buenos Aires, Buenos Aires, Argentina
Cystic Fibrosis/Pulmonary Research and Treatment Center, University of North Carolina at Chapel Hill, 4029A Thurston Bowles Building, Chapel Hill, NC 27599-7248, United States
Palabras clave:ATP; ATPases; Erythrocyte; Extracellular; Pannexin 1; adenosine triphosphatase; adenosine triphosphate; carbenoxolone; cell protein; mastoparan; mastoparan 7; pannexin 1; poly dextro lysine; probenecid; unclassified drug; animal cell; article; cell activation; cell swelling; chemical reaction kinetics; concentration (parameters); controlled study; enzyme activity; erythrocyte; erythrocyte adhesiveness; erythrocyte volume; experimental dog; hematocrit; human; human cell; hydrolysis; inhibition kinetics; intracellular signaling; long term exposure; mouse; nonhuman; nucleotide transport; priority journal; reduction kinetics; wild type; 3V; a cAMP activating cocktail containing isoproterenol, forskolin and papaverine; ATPases; ATPe; ATPi; carbenoxolone; CBX; cilostazol; CTZ; Erythrocyte; extracellular ATP; Extracellular ATP; flux of ATP release; flux of ATPe hydrolysis; GEFs; guanine exchange factors; intracellular ATP; J(R); J(V); mastoparan; MST; pannexin 1; Pannexin 1; pannexin 1 heterozygous mice; pannexin 1 knockout mice, PTX, pertussis toxin; pannexin 1 wild type mice; PBC; pnx; pnx(+/+); pnx(+/-); pnx(-/-); probenecid; rbcs; red blood cells; relative cell volume; Vr; Adenosine Triphosphate; Animals; Dogs; Erythrocytes; Humans; Hydrolysis; Kinetics; Mice; Mice, Knockout; Peptides; Signal Transduction; Mus
Página de inicio:4692
Página de fin:4707
Título revista:Biochimica et Biophysica Acta - General Subjects
Título revista abreviado:Biochim. Biophys. Acta Gen. Subj.
CAS:adenosine triphosphatase, 37289-25-1, 9000-83-3; adenosine triphosphate, 15237-44-2, 56-65-5, 987-65-5; carbenoxolone, 5697-56-3, 7421-40-1; mastoparan, 72093-21-1; probenecid, 57-66-9; Adenosine Triphosphate, 56-65-5; Mas7 protein, synthetic; Peptides


  • Gorman, M.W., Feigl, E.O., Buffington, C.W., Human plasma ATP concentration (2007) Clinical Chemistry, 53 (2), pp. 318-325. , DOI 10.1373/clinchem.2006.076364
  • Lazarowski, E.R., Boucher, R.C., Harden, T.K., Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules (2003) Molecular Pharmacology, 64 (4), pp. 785-795. , DOI 10.1124/mol.64.4.785
  • Montalbetti, N., Leal Denis, M.F., Pignataro, O.P., Kobatake, E., Lazarowski, E.R., Schwarzbaum, P.J., Homeostasis of extracellular ATP in human erythrocytes (2011) J. Biol. Chem., 286, pp. 38397-38407
  • Sprague, R.S., Stephenson, A.H., Ellsworth, M.L., Red not dead: Signaling in and from erythrocytes (2007) Trends in Endocrinology and Metabolism, 18 (9), pp. 350-355. , DOI 10.1016/j.tem.2007.08.008, PII S1043276007001543
  • Gonzalez-Alonso, J., Olsen, D.B., Saltin, B., Erythrocyte and the regulation of human skeletal muscle blood flow and oxygen delivery: Role of circulating ATP (2002) Circulation Research, 91 (11), pp. 1046-1055. , DOI 10.1161/01.RES.0000044939.73286.E2
  • Sprague, R.S., Bowles, E.A., Achilleus, D., Ellsworth, M.L., Erythrocytes as controllers of perfusion distribution in the microvasculature of skeletal muscle (2011) Acta Physiol., 202, pp. 285-292
  • Ellsworth, M.L., Sprague, R.S., Regulation of blood flow distribution in skeletal muscle: Role of erythrocyte-released ATP (2012) J. Physiol., 590, pp. 4985-4991
  • Hellsten, Y., Nyberg, M., Mortensen, S.P., Contribution of intravascular versus interstitial purines and nitric oxide in the regulation of exercise hyperaemia in humans (2012) J. Physiol., 590, pp. 5015-5023
  • Bergfeld, G.R., Forrester, T., Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia (1992) Cardiovasc. Res., 26, pp. 40-47
  • 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 (2001) Am. J. Physiol. Cell Physiol., 281, pp. 1158-C1164
  • Olearczyk, J.J., Stephenson, A.H., Lonigro, A.J., Sprague, R.S., Heterotrimeric G protein Gi is involved in a signal transduction pathway for ATP release from erythrocytes (2004) Am. J. Physiol. Heart Circ. Physiol., 286, pp. 940-H945
  • Sridharan, M., Adderley, S.P., Bowles, E.A., Egan, T.M., Stephenson, A.H., Ellsworth, M.L., Sprague, R.S., (2010) Am. J. Physiol. Heart Circ. Physiol., 299, pp. 1146-H1152
  • Zimmerberg, J., Parsegian, V.A., Polymer inaccessible volume changes during opening and closing of a voltage-dependent ionic channel (1986) Nature, 323, pp. 36-39
  • Higashijima, T., Burnier, J., Ross, E.M., Regulation of Gi and G0 by mastoparan, related amphiphilic peptides, and hydrophobic amines (1990) J. Biol. Chem., 265, pp. 14176-14186
  • Park, H.S., Lee, S.Y., Kim, Y.H., Kim, J.Y., Lee, S.J., Choi, M.-U., Membrane perturbation by mastoparan 7 elicits a broad alteration in lipid composition of L1210 cells (2000) Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids, 1484 (2-3), pp. 151-162. , DOI 10.1016/S1388-1981(00)00002-0, PII S1388198100000020
  • Sprague, R.S., Stephenson, A.H., Bowles, E.A., Stumpf, M.S., Lonigro, A.J., Reduced expression of Gi in erythrocytes of humans with type 2 diabetes is associated with impairment of both cAMP generation and ATP release (2006) Diabetes, 55 (12), pp. 3588-3593. ,, DOI 10.2337/db06-0555
  • Sprague, R.S., 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 (2005) Pharm. Reports, 57, pp. 222-228
  • Sprague, R.S., Bowles, E.A., Olearczyk, J.J., Stephenson, A.H., Lonigro, A.J., The role of G protein B subunits in the release of ATP from human erythrocytes (2002) Journal of Physiology and Pharmacology, 53 (I4), pp. 667-674
  • 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 (2010) Exp. Biol. Med., 235, pp. 256-262
  • 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 (1998) Am. J. Physiol. Heart Circ. Physiol., 275, pp. 1726-H1732
  • Sugita, M., Yue, Y., Foskett, J.K., CFTR Cl-- channel and CFTR-associated ATP channel: Distinct pores regulated by common gates (1998) EMBO J., 17, pp. 898-908
  • Dupré, D.J., Robitaille, M., Rebois, R.B., H'Ebert, T.E., The role of Gβγ subunits in the organization, assembly, and function of GPCR signaling complexes (2009) Annu. Rev. Pharmacol. Toxicol., 49, pp. 31-56
  • 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 (2005) Circulation Research, 96 (2), pp. 189-196. , DOI 10.1161/01.RES.0000153670.07559.E4
  • Pafundo, D.E., Alvarez, C.L., Krumschnabel, G., Schwarzbaum, P.J., A volume regulatory response can be triggered by nucleosides in human erythrocytes, a perfect osmometer no longer (2010) J. Biol. Chem., 285, pp. 6134-6144
  • Erlinge, D., Burnstock, G., P2 receptors in cardiovascular regulation and disease (2008) Purinergic Signal, 4, pp. 1-20
  • Kunapuli, S.P., Daniel, J.L., P2 receptor subtypes in the cardiovascular system (1998) Biochem. J., 336, pp. 513-523
  • Burnstock, G., Dual control of vascular tone and remodelling by ATP released from nerves and endothelial cells (2008) Pharmacological Reports, 60 (1), pp. 12-20. ,
  • Ellsworth, M.L., Ellis, C.G., Goldman, D., Stephenson, A.H., Dietrich, H.H., Sprague, R.S., Erythrocytes: Oxygen sensors and modulators of vascular tone (2009) Physiology, 24, pp. 107-116
  • Crecelius, A.R., Kirby, B.S., Luckasen, G.J., Larson, D.G., Dinenno, F.A., ATP-mediated vasodilatation occurs via activation of inwardly-rectifying potassium channels in humans (2012) J. Physiol., 590, pp. 5349-5359
  • Sevigny, J., Sundberg, C., Braun, N., Guckelberger, O., Csizmadia, E., Qawi, I., Imai, M., Robson, S.C., Differential catalytic properties and vascular topography of murine nucleoside triphosphate diphosphohydrolase 1 (NTPDase1) and NTPDase2 have implications for thromboregulation (2002) Blood, 99 (8), pp. 2801-2809. , DOI 10.1182/blood.V99.8.2801
  • Kukulski, F., Levesque, S.A., Lavoie, E.G., Lecka, J., Bigonnesse, F., Knowles, A.F., Robson, S.C., Sevigny, J., Comparative hydrolysis of P2 receptor agonists by NTPDases 1, 2, 3 and 8 (2005) Purinergic Signalling, 1 (2), pp. 193-204. , DOI 10.1007/s11302-005-6217-x
  • Locovei, S., Bao, L., Dahl, G., Pannexin 1 in erythrocytes: Function without a gap (2006) Proc. Natl. Acad. Sci. U. S. A., 103, pp. 7655-7659
  • Qiu, F., Dahl, G., A permeant regulating its permeation pore: Inhibition of pannexin 1 channels by ATP (2009) Am. J. Physiol. Cell Physiol., 296, pp. 250-C255
  • Ransford, G.A., Fregien, N., Qiu, F., Dahl, G., Conner, G.E., Salathe, M., Pannexin 1 contributes to ATP release in airway epithelia (2009) Am. J. Respir. Cell Mol. Biol., 41, pp. 525-534
  • Grygorczyk, R., Tabcharani, J.A., Hanrahan, J.W., CFTR channels expressed in CHO cells do not have detectable ATP conductance (1996) Journal of Membrane Biology, 151 (2), pp. 139-148. , DOI 10.1007/s002329900065
  • Grygorczyk, R., Hanrahan, J.W., CFTR-independent ATP release from epithelial cells triggered by mechanical stimuli (1997) Am. J. Physiol. Cell Physiol., 272, pp. 1058-C1066
  • Silverman, W., Locovei, S., Dahl, G., Probenecid, a gout remedy, inhibits pannexin 1 channels (2008) Am. J. Physiol. Cell Physiol., 295, pp. 761-C767
  • Sridharan, M., Sprague, R.S., Adderley, S.P., Bowles, E.A., Ellsworth, M.L., Stephenson, A.H., Diamide decreases deformability of rabbit erythrocytes and attenuates low oxygen tension-induced ATP release (2010) Exp. Biol. Med., 235, pp. 1142-1148
  • Sprague, R.S., Bowles, E.A., Achilleus, D., Stephenson, A.H., Ellis, C.G., Ellsworth, M.L., A selective phosphodiesterase 3 inhibitor rescues low PO 2-induced ATP release from erythrocytes of humans with type 2 diabetes: Implication for vascular control (2011) Am. J. Physiol. Heart, 301, pp. 2466-H2472
  • Thuet, K.M., Bowles, E.A., Ellsworth, M.L., Sprague, R.S., Stephenson, A.H., The Rho kinase inhibitor Y-27632 increases erythrocyte deformability and low oxygen tension-induced ATP release (2011) Am. J. Physiol. Heart, 301, pp. 1891-H1896
  • Seminario-Vidal, L., Okada, S.F., Sesma, J.I., Kreda, S.M., Van Heusden, C.A., Zhu, Y., Jones, L.C., Lazarowski, E.R., Rho signaling regulates Pannexin 1-mediated ATP release from airway epithelia (2011) J. Biol. Chem., 286, pp. 26277-26286
  • Strehler, B.L., Bioluminescence assay: Principles and practice (1968) Methods Biochem. Anal., 16, pp. 99-181
  • Brown, A.M., ATP and ATPase determination in red blood cells (1982) Red Cell Membranes - A Methodological Approach, pp. 223-238. , J.C. Ellory, J.D. Young, Academic Press London
  • Pafundo, D.E., Chara, O., Faillace, M.P., Krumschnabel, G., Schwarzbaum, P.J., Kinetics of ATP and cell volume regulation of hyposmotically challenged goldfish hepatocytes (2008) Am. J. Physiol. Regul. Integr. Comp. Physiol., 294, pp. 220-R233
  • Gorman, M.W., Marble, D.R., Ogimoto, K., Feigl, E.O., Measurements of adenine nucleotides in plasma (2003) Luminescence, 18, pp. 173-181
  • Kwant, W.O., Seeman, P., The erythrocyte ghost is a perfect osmometer (1970) J. Gen. Physiol., 55, pp. 208-219
  • Grynkiewicz, G., Poenie, M., Tsien, R.Y., A new generation of Ca2+ indicators with greatly improved fluorescence properties (1985) Journal of Biological Chemistry, 260 (6), pp. 3440-3450
  • Steiner, A.L., Kipnis, D.M., Utiger, R., Parker, C., Radioimmunoassay for the measurement of adenosine 3′ 5′- cyclic monophosphate (1969) Proc. Natl. Acad. Sci. U. S. A., 64, pp. 367-373
  • Mondillo, C., Patrignani, Z., Reche, C., Rivera, E., Pignataro, O., Dual role of histamine in modulation of Leydig cell steroidogenesis via HRH1 and HRH2 receptor subtypes (2005) Biology of Reproduction, 73 (5), pp. 899-907. , DOI 10.1095/biolreprod.105.041285
  • Del Punta, K., Charreau, E.H., Pignataro, O.P., Nitric oxide inhibits leydig cell steroidogenesis (1996) Endocrinology, 137 (12), pp. 5337-5343. , DOI 10.1210/en.137.12.5337
  • Schwarzbaum, P.J., Kaufman, S.B., Rossi, R.C., Garrahan, P.J., An unexpected effect of ATP on the ratio between activity and phosphoenzyme level of Na+/K+-ATPase in steady state (1995) Biochim. Biophys. Acta, 1233, pp. 33-40
  • Vázquez, A., Tudela, J., Varón, R., García-Cánovas, F., Determination of hemoglobin through its peroxidase activity on chlorpromazine (1991) J. Biochem. Biophys. Methods, 23, pp. 45-52
  • Bencic, D.C., Yates, T.J., Ingermann, R.L., Ecto-ATPase activity of vertebrate blood cells (1997) Physiol. Zool., 70, pp. 621-630
  • Freshney, R.I., (2005) Culture of Animal Cells: A Manual of Basic Technique, , fifth ed. Wiley and sons New York
  • Hategan, A., Sengupta, K., Kahn, S., Sackmann, E., Discher, D.E., Topographical pattern dynamics in passive adhesion of cell membranes (2004) Biophysical Journal, 87 (5), pp. 3547-3560. , DOI 10.1529/biophysj.104.041475
  • Forsyth, A.M., Wan, J., Owrutsky, P.D., Abkarian, M., Stone, A.H., Multiscale approach to link red blood cell dynamics, shear viscosity, and ATP release (2011) Proc. Natl. Acad. Sci. U. S. A., 108, pp. 10986-10991
  • Jagger, J.E., Bateman, R.M., Ellsworth, M.L., Ellis, C.G., Role of erythrocyte in regulating local O2 delivery mediated by hemoglobin oxygenation (2001) Am. J. Physiol. Heart Circ. Physiol., 280, pp. 2833-H2839
  • Ellsworth, M.L., Red Blood Cell-Derived ATP as a Regulator of Skeletal Muscle Perfusion (2004) Medicine and Science in Sports and Exercise, 36 (1), pp. 35-41
  • Sprague, R.S., Hanson, M.S., Achilleus, D., Bowles, E.A., Stephenson, A.H., Sridharan, M., Adderley, S., Ellsworth, M.L., Rabbit erythrocytes release ATP and dilate skeletal muscle arterioles in the presence of reduced oxygen tension (2009) Pharmacol. Rep., 61, pp. 183-190
  • Dubyak, G.R., Both sides now: Multiple interactions of ATP with pannexin-1 hemichannels. Focus on "a permeant regulating its permeation pore: Inhibition of pannexin 1 channels by ATP" (2009) Am. J. Physiol. Cell Physiol., 296, pp. 235-C241
  • Boassa, D., Ambrosi, C., Qiu, F., Dahl, G., Gaietta, G., Sosinsky, G., Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane (2007) Journal of Biological Chemistry, 282 (43), pp. 31733-31743. ,, DOI 10.1074/jbc.M702422200
  • Bao, L., Locovei, S., Dahl, G., Pannexin membrane channels are mechanosensitive conduits for ATP (2004) FEBS Letters, 572 (1-3), pp. 65-68. , DOI 10.1016/j.febslet.2004.07.009, PII S001457930400866X
  • Dahl, G., Keane, R.W., Pannexin: From discovery to bedside in 11 ± 4 years? (2012) Brain Res., 1487, pp. 150-159
  • Bruzzone, R., Barbe, M.T., Jakob, N.J., Monyer, H., Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes (2005) Journal of Neurochemistry, 92 (5), pp. 1033-1043. , DOI 10.1111/j.1471-4159.2004.02947.x
  • Qiu, F., Wang, J., Spray, D.C., Scemes, E., Dahl, G., Two non-vesicular ATP release pathways in the mouse erythrocyte membrane (2011) FEBS Lett., 585, pp. 3430-3435
  • Islam, R., Uramoto, H., Okada, T., Sabirov, R.Z., Okada, Y., Maxi-anion channel and pannexin 1 hemichannel constitute separate pathways for swelling-induced ATP release in murine L929 fibrosarcoma cells (2012) Am. J. Physiol. Cell Physiol., 303, pp. 924-C935
  • Sridharan, M., Bowles, E.A., Richards, J.P., Krantic, M., Davis, K.L., Dietrich, K.A., Stephenson, A.H., Sprague, R.S., Prostacyclin receptor-mediated ATP release from erythrocytes requires the voltage-dependent anion channel (2012) Am. J. Physiol. Heart Circ. Physiol., 302, pp. 553-H559
  • Taruno, A., Vingtdeux, V., Ohmoto, M., Ma, Z., Dvoryanchikov, G., Li, A., Adrien, L., Foskett, J.K., CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes (2013) Nature, 495, pp. 223-226
  • Silverman, W.R., De Rivero Vaccari, J.P., Locovei, S., Qiu, F., Carlsson, S.K., Scemes, E., Keane, R.W., Dahl, G., The pannexin 1 channel activates the inflammasome in neurons and astrocytes (2009) J. Biol. Chem., 284, pp. 18143-18151
  • Ma, W., Hui, H., Pelegrin, P., Surprenant, A., Pharmacological characterization of pannexin-1 currents expressed in mammalian cells (2009) J. Pharmacol. Exp. Ther., 328, pp. 409-418
  • Mortensen, S.P., Thaning, P., Nyberg, M., Saltin, B., Hellsten, Y., Local release of ATP into the arterial inflow and venous drainage of human skeletal muscle: Insight from ATP determination with the intravascular microdialysis technique (2011) J. Physiol., 589, pp. 1847-1857
  • Farias III, M., Gorman, M.W., Savage, M.V., Feigl, E.O., Plasma ATP during exercise: Possible role in regulation of coronary blood flow (2005) Am. J. Physiol. Heart Circ. Physiol., 288, pp. 1586-H1590
  • Oldenborg, P.-A., Zheleznyak, A., Fang, Y.-F., Lagenaur, C.F., Gresham, H.D., Lindberg, F.P., Role of CD47 as a marker of self on red blood cells (2000) Science, 288 (5473), pp. 2051-2054. , DOI 10.1126/science.288.5473.2051
  • Zhu, H., Zennadi, R., Xu, B.X., Eu, J.P., Torok, J.A., Telen, M.J., McMahon, T.J., Impaired adenosine-5′-triphosphate release from red blood cells promotes their adhesion to endothelial cells: A mechanism of hypoxemia after transfusion (2011) Crit. Care Med., 39, pp. 2478-2486
  • Sabirov, R.Z., Okada, Y., ATP release via anion channels (2005) Purinergic Signalling, 1 (4), pp. 311-328. , DOI 10.1007/s11302-005-1557-0
  • Kaji, D.M., Effect of membrane potential on K-Cl transport in human erythrocytes (1993) Am. J. Physiol. Cell Physiol., 264, pp. 376-C382
  • Akaike, H., Data analysis by statistical models (1992) No to Hattatsu, 24, pp. 127-133
  • Hoops, S., Gauges, R., Lee, C., Pahle, J., Simus, N., Singhal, M., Xu, L., Kummer, U., COPASI - A COmplex PAthway SImulator (2006) Bioinformatics, 22 (24), pp. 3067-3074. , DOI 10.1093/bioinformatics/btl485


---------- APA ----------
Leal Denis, M.F., Incicco, J.J., Espelt, M.V., Verstraeten, S.V., Pignataro, O.P., Lazarowski, E.R. & Schwarzbaum, P.J. (2013) . Kinetics of extracellular ATP in mastoparan 7-activated human erythrocytes. Biochimica et Biophysica Acta - General Subjects, 1830(10), 4692-4707.
---------- CHICAGO ----------
Leal Denis, M.F., Incicco, J.J., Espelt, M.V., Verstraeten, S.V., Pignataro, O.P., Lazarowski, E.R., et al. "Kinetics of extracellular ATP in mastoparan 7-activated human erythrocytes" . Biochimica et Biophysica Acta - General Subjects 1830, no. 10 (2013) : 4692-4707.
---------- MLA ----------
Leal Denis, M.F., Incicco, J.J., Espelt, M.V., Verstraeten, S.V., Pignataro, O.P., Lazarowski, E.R., et al. "Kinetics of extracellular ATP in mastoparan 7-activated human erythrocytes" . Biochimica et Biophysica Acta - General Subjects, vol. 1830, no. 10, 2013, pp. 4692-4707.
---------- VANCOUVER ----------
Leal Denis, M.F., Incicco, J.J., Espelt, M.V., Verstraeten, S.V., Pignataro, O.P., Lazarowski, E.R., et al. Kinetics of extracellular ATP in mastoparan 7-activated human erythrocytes. Biochim. Biophys. Acta Gen. Subj. 2013;1830(10):4692-4707.