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Plasma membrane ion channels in suicidal cell death
ABB Archives of Biochemistry and Biophysics 462 (2007) 189–194 www.elsevier.com/locate/yabbi
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Plasma membrane ion channels in suicidal cell death Florian Lang a
a,*
, Stephan M. Huber a, Ildiko Szabo b, Erich Gulbins
c
Department of Physiology, University of Tu¨bingen, Gmelinstrasse 5, D72076 Tuebingen, Germany b Department of Biology, University of Padova, Italy c Department of Molecular Medicine, University Duisburg-Essen, Germany Received 5 December 2006, and in revised form 21 December 2006 Available online 22 January 2007
Abstract The machinery leading to apoptosis includes altered activity of ion channels. The channels contribute to apoptotic cell shrinkage and modify intracellular ion composition. Cl channels allow the exit of Cl , osmolytes and HCO3 leading to cell shrinkage and cytosolic acidification. K+ exit through K+ channels contributes to cell shrinkage and decreases intracellular K+ concentration, which in turn favours apoptotic cell death. K+ channel activity further determines the cell membrane potential, a driving force for Ca2+ entry through Ca2+ channels. Ca2+ may enter through unselective cation channels. An increase of cytosolic Ca2+ may stimulate several enzymes executing apoptosis. Specific ion channel blockers may either promote or counteract suicidal cell death. The present brief review addresses the role of ion channels in the regulation of suicidal cell death with special emphasis on the role of channels in CD95 induced apoptosis of lymphocytes and suicidal death of erythrocytes or eryptosis. Ó 2007 Elsevier Inc. All rights reserved. Keywords: CD95; Scramblase; PGE2; Cell volume; Lymphocytes; Erythrocytes; Eryptosis
Apoptosis or programmed cell death eliminates abundant and potentially harmful cells. Apoptosis may be triggered by a wide variety of factors including stimulation of death receptors such as CD95 [1–4], somatostatin receptor [5] or TNFa receptor [6], by thyroid hormones [7], increased cell density [8], adhesion [9,10] or growth factor withdrawal [11], or by exposure to stressors such as oxidants [12], radiation [12], inhibition of glutaminase [13], chemotherapeutics [14,15], energy depletion [16], choline deficiency [17] or osmotic shock [3,12,18–21]. Hallmarks of apoptosis include mitochondrial depolarization, DNA fragmentation, nuclear condensation, cell shrinkage, cell membrane blebbing and scrambling of cell membrane lipids with breakdown of phosphatidylserine asymmetry of the plasma membrane [22]. The cell membrane scrambling results from the activity of a scramblase [23], which is stimulated by increase of cytosolic Ca2+ activity [24,25]. Macrophages are equipped with receptors *
Corresponding author. Fax: +49 7071 29 5618. E-mail address: fl[email protected] (F. Lang).
0003-9861/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.abb.2006.12.028
specific for phosphatidylserine [26,27] and thus engulf cells or cellular fragments exposing phosphatidylserine at their surface [28]. The engulfment is facilitated by the shrinkage of apoptotic cells [28]. Suicidal death may not only affect nucleated cells but similarly erythrocytes [29,30]. Suicidal death of mature erythrocytes or ‘‘eryptosis’’ [31] is characterized by cell shrinkage, cell membrane blebbing and breakdown of phosphatidylserine asymmetry, features mimicking respective events of nucleated cell apoptosis [32–34]. The machinery of apoptosis involves altered regulation of Cl channels, K+ channels and Ca2+ permeable channels, which play an active role in the machinery leading to suicidal cell death. Accordingly, apoptosis and eryptosis are modified by respective channel inhibitors. Anion channels, osmolyte transport and pH regulation Activation of Cl channels during apoptosis has first been observed following stimulation of CD95 in Jurkat
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cells [35]. Subsequently, Cl channel activation has been described in TNFa or staurosporine induced apoptosis of various cell types [20,36]. In Jurkat cells the same channels serve regulatory cell volume decrease following osmotic cell swelling [37]. Activation of those Cl channels by cell swelling [37] or stimulation of CD95 [35] requires the Src-like kinase Lck56. The kinase is activated by ceramide [38], which is formed by activation of a sphingomyelinase following stimulation of CD95. In lymphocytes from patients with cystic fibrosis the Cl channels cannot be activated by protein kinase A but by cell swelling, by ceramide or by active Lck56[39]. Cl channel activation plays a pivotal role in the apoptotic machinery. Accordingly, Cl channel inhibitors abrogate CD95 induced Jurkat cell apoptosis [35], TNFa or staurosporine induced apoptosis of various cell types [20,36], apoptotic death of cortical neurons [40], GABA-induced enhancement of excitotoxic cell death of rat cerebral neurons [41], cardiomyocyte apoptosis [42], antimycin A induced death of proximal renal tubules [43] and suicidal death of erythrocytes [44]. As Lck56 does activate CFTR sensitive outwardly rectifying Cl channels in lymphocytes of cystic fibrosis patients, CD95 induced lymphocyte death is not affected in those patients [39]. Activation of Cl channels leads to exit of Cl , which tends to depolarize the cell membrane. Thus, the driving force for K+ exit is enhanced and, dependent on the activity of K+ channels, the cells release KCl. The loss of osmotically active KCl is paralleled by loss of osmotically obliged water and thus by cell shrinkage, one of the hallmarks of apoptosis [3]. Even though the underlying mechanisms are still ill-defined, it is believed that the loss of cell volume contributes to the machinery leading to apoptotic cell death [18,45]. It should be pointed out, though, that the Cl channels are activated within a few minutes following CD95 triggering of Jurkat cells, but that apoptotic cell shrinkage occurs only some 90 min later. As outlined below, the lack of early cell shrinkage is presumably a result of early K+ channel inhibition. Cl channels do not only contribute to apoptotic cell shrinkage. Several anion channels are permeable to organic osmolytes such as taurine. Activation of those anion channels leads to cellular loss of organic osmolytes [3,46,47], which is again accompanied by osmotically obliged water and thus contributes to apoptotic cell shrinkage [3]. It should be pointed out, however, that at least following CD95 induced death of Jurkat lymphocytes, the taurine release mechanism is not the outwardly rectifying Cl channel. Whereas CD95 induced activation of the outwardly rectifying Cl channel requires Lck56 [35], the taurine release is abrogated by the caspase inhibitor zVAD [46]. Moreover, inhibition of the outwardly rectifying Cl channel is an early event after CD95 triggering [35], whereas taurine release is a late event immediately preceding DNA fragmentation [3]. As organic osmolytes stabilize cellular proteins (for review see [3]), their exit could lead to protein destabilization and thus contribute to the triggering
of cell death. Along the same lines, inhibition of inositol uptake has been shown to trigger renal failure presumably due to suicidal death of renal tubular cells [48]. On the other hand, erythrocytes from mice lacking the taurine transporter are rather less sensitive to osmotically induced cell death [33]. Interestingly, the stimulation of taurine release and apoptotic DNA fragmentation following CD95 stimulation of Jurkat cells are both highly sensitive to ambient temperature [3]. Similarly, CD95 mediated stimulation of epithelial cell death by exposure to Pseudomonas is highly temperature sensitive [1]. CD95 mediated Pseudomonas induced host cell death is critically important for the host defence [49] and it is tempting to speculate that the increased body temperature of fever may help to stimulate apoptosis and thus removal of infected cells [1]. Several Cl channels allow the passage of HCO3 . Their activation leads to HCO3 exit and thus to cytosolic acidification, a typical feature of apoptotic cells [6,35,50–61]. As DNase type II has its pH optimum in the acidic range, cytosolic acidification favours DNA fragmentation (for review see [62]). Moreover, intracellular acidification may facilitate caspase activation. While the pH optimum of most caspases is pH 7.0 [63], a low cytosolic pH (6.4) has been shown to enhance cytochrome c/dATP-mediated caspase activation [64], indicating that assembly of the apoptosome might be controlled by the intracellular pH. Particularly, cellular acidification has previously been shown to foster autocatalytic maturation of procaspase-3 and to increase proteolytic cleavage by caspase-9 [65]. It should be pointed out that the acidification during apoptosis is not only due to activation of HCO3 permeable Cl channels but in addition due to inhibition of the Na+/ H+ exchanger [66], which is at least partially due to caspase dependent degradation of the carrier protein NHE1 [67]. NHE1 degradation and inhibition is not an early but a late event in the apoptotic machinery [67]. Staurosporine-induced intracellular acidification was not prevented by the caspase inhibitor zVAD-fmk but completely abrogated by Bcl-2 overexpression, pointing to a role of mitochondria in the triggering of cytosolic acidification [67]. Thus, Cl channels contribute to but do not fully account for cytosolic acidification. K+ channels In several cell types, apoptosis is stimulated by activation of K+ channels [40,68] and inhibited by K+ channel blockers [69,70] or increase of extracellular K+ concentration [70–72]. Activation of K+ channels leads to hyperpolarization of the cell membrane, which increases the electrical driving force for Cl exit into the extracellular space. Thus, as indicated above, enhanced activity of K+ channels and Cl channels leads to cellular loss of KCl with osmotically obliged water and hence to cell shrinkage. Beyond that cellular loss of K+ may favour apoptosis in a wide variety of cells [19,20,45,73–82].
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Cellular loss of K+ may not only be due to activation of K channels but may as well involve impaired activity of the Na+/K+ ATPase [83]. Inhibition of the Na+/K+ ATPase, however, does not usually shrink cells, as it leads to an increase of intracellular Na+ concentration usually outcasting the decrease of intracellular K+ concentration. In some cells, inhibition rather than activation of K+ channels may parallel apoptosis. Conversely, inhibition of K+ channels may cause apoptosis [84–89] and activation of K+ channels may inhibit [90,91] apoptosis. Along those lines, mice with mutated G-protein coupled inward rectifier K+ channels (Weaver mice) suffer from extensive neuronal cell death [92–96]. CD95 stimulation leads to early inhibition of Kv1.3 K+ channels [35,97,98], the cell volume regulatory K+ channels of Jurkat lymphocytes [99]. The inhibition of the Kv1.3 channels is paralleled by tyrosine phosphorylation of the channel protein upon CD95 stimulation [38,97]. Kv1.3 channels are sensitive to tyrosine phosphorylation [100] and inhibition of Kv1.3 channels by CD95 is abrogated by tyrosine kinase inhibitors and genetic knockout of Lck56 [38,97]. Similar to stimulation of CD95, ceramide inhibits Kv1.3 and induces apoptosis [38]. Conversely, Kv1.3 is stimulated by the serum and glucocorticoid inducible kinase SGK1 [101], which has been shown to inhibit apoptosis [102]. Upon CD95 triggering, the early inhibition of Kv1.3 channels prevents premature cell shrinkage, which would interfere with apoptosis signaling [3]. Moderate osmotic cell shrinkage prior to CD95 stimulation blunted the CD95 induced activation of reactive oxygen species and subsequent apoptosis, indicating that cell shrinkage indeed disrupts the apoptotic signaling cascade [38] without interfering with some of the upstream signaling. Thus, while excessive osmotic cell shrinkage or osmotic shock by itself induces apoptosis [3,12,18–21], at least in Jurkat lymphocytes moderate decrease of cell volume confers some resistance to receptor mediated cell death. The early inhibition of Kv1.3 is followed by late activation of Kv1.3 [103], which supports the apoptotic cell shrinkage during the execution phase of apoptosis [103]. In suicidal erythrocytes increased cytosolic Ca2+ activity stimulates Ca2+ sensitive K+ channels (Gardos channels) [104–111]. Activation of those channels leads to hyperpolarization and, due to high erythrocyte Cl permeability, to parallel exit of K+ and Cl . The exit of KCl and osmotically obliged water leads not only to cell shrinkage but enhances the scrambling of the cell membrane [70], a typical feature of suicidal erythrocyte death or eryptosis [31]. Conversely, pharmacological inhibition of the Gardos channels or increase of extracellular K+ concentration does not only abrogate eryptotic cell shrinkage but leads to a moderate blunting of the phosphatidylserine exposure following treatment of erythrocytes with the Ca2+ ionophore ionomycin [70]. Cell shrinkage leads to formation of platelet activating factor PAF, which in turn activates a sphingomyelinase leading to formation of ceramide [112]. +
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Ceramide then contributes to the triggering of cell membrane scrambling [112,113]. Presently, it is not clear, whether increased extracellular K+ concentration exerts its antieryptotic effect by interference with eryptotic cell shrinkage or by prevention of eryptotic K+ loss. Ca2+ and unselective cation channels Jurkat lymphocyte apoptosis following CD95 triggering is paralleled by inhibition of ICRAC [114,115], a channel involved in the activation and proliferation of a wide variety of cells [116–120]. Thus, in the early phase of CD95 triggering, cytosolic Ca2+ activity rather decreases in Jurkat T lymphocytes [115]. On the other hand, sustained increase of cytosolic Ca2+ activity may trigger apoptosis of a variety of nucleated cells [22,116,117,121,122] and suicidal death or eryptosis of erythrocytes [32,123–126]. In erythrocytes, the increase of cytosolic Ca2+ activity may result from activation of Ca2+ permeable cation channels, which are activated by exposure of erythrocytes to osmotic shock [127], oxidative stress [128], energy depletion [32] and infection with the malaria pathogen Plasmodium falciparum [129–131]. The eryptosis following energy depletion may partially be due to impaired replenishment of GSH and weakening of the antioxidative defence [132,133]. The cation channels are activated by prostaglandin E2 (PGE2)1, which is released upon osmotic shock [134]. The cation channels are further activated by removal of intracellular and extracellular Cl [127,128] or by incubation in low ionic strength [135–137]. Nonselective cation channels are further activated by depolarization [138–140]. Enhanced cytosolic Ca2+ concentrations lead to phospholipid scrambling [23] with breakdown of the phosphatidylserine asymmetry of the erythrocyte cell membrane [25]. Moreover, Ca2+ may activate calpain [141], which in turn leads to cell membrane blebbing, another hallmark of eryptosis [123,124]. A wide variety of further substances or conditions trigger eryptosis [31], such as paclitaxel [142], chlorpromazine [143], cyclosporine [144], mercury [145], lead [146], hemolysin [147], phosphate depletion [148], iron deficiency [149], Hemolytic Uremic Syndrome [150] and several inherited erythrocyte disorders [126]. Eryptosis is inhibited by erythropoietin [151], urea [152], catecholamines [153], by lowering of extracellular Ca2+ activity [32] and by inhibitors of cation channels [32]. Mechanisms underlying eryptosis may further contribute to erythrocyte senescence [29,31,154,155] or neocytolysis [30]. Cell shrinkage activates cation channels in a wide variety of nucleated cells including airway epithelia cells [156], colon carcinoma cells [157], cortical collecting duct cells [158], hepatocytes [159,160], mast cells [161], macrophages [162], vascular smooth muscle [157] and neuroblastoma cells [157]. Cl removal activates cation channels in salivary and 1
Abbreviation used: (PGE2), prostaglandin E2.
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lung epithelial cells [163–165] and influences the channels via a pertussis toxin sensitive G-protein [163]. Whether or not those channels participate in Ca2+ entry and apoptosis, has not been explored. Most recent experiments disclosed, however that, similar to what has been observed in erythrocytes, osmotic cell shrinkage leads to formation of PGE2 in K562 cells, which in turn activate Ca2+ permeable cation channels and leads to apoptotic cell death [166]. In those cells, silencing of the cation channel TRPC7 blunts the cell death following osmotic shock. Thus, in those cells TRPC7 contributes to the triggering of apoptosis. Conclusions Ion channels in the plasma membrane play a decisive role in the machinery eventually leading to suicidal cell death. They influence the apoptotic signalling by modifying intracellular ion concentrations and cell volume. The role of individual channels depends on the cell type, the physiological condition, the time course and the intensity of channel activation. Much has to be learned prior to a full understanding of the complex interplay between channel activity and apoptosis signalling. Acknowledgments The authors acknowledge the meticulous preparation of the manuscript by Lejla Subasic. The work of the authors was supported by the Deutsche Forschungsgemeinschaft, Nr. La 315/4-3, La 315/6-1, Le 792/3-3, DFG Schwerpunkt Intrazellula¨re Lebensformen La 315/11-1, and Bundesministerium fu¨r Bildung, Wissenschaft, Forschung und Technologie (Center for Interdisciplinary Clinical Research) 01 KS 9602. References [1] S. Fillon, K. Klingel, S. Warntges, M. Sauter, S. Gabrysch, S. Pestel, V. Tanneur, S. Waldegger, A. Zipfel, R. Viebahn, D. Haussinger, S. Broer, R. Kandolf, F. Lang, Cell Physiol. Biochem. 12 (2002) 47–54. [2] E. Gulbins, A. Jekle, K. Ferlinz, H. Grassme, F. Lang, Am. J. Physiol. Renal Physiol. 279 (2000) F605–F615. [3] F. Lang, G.L. Busch, M. Ritter, H. Volkl, S. Waldegger, E. Gulbins, D. Haussinger, Physiol. Rev. 78 (1998) 247–306. [4] F. Lang, I. Szabo, A. Lepple-Wienhues, D. Siemen, E. Gulbins, News Physiol. Sci. 14 (1999) 194–200. [5] R. Teijeiro, R. Rios, J.A. Costoya, R. Castro, J.L. Bello, J. Devesa, V.M. Arce, Cell Physiol. Biochem. 12 (2002) 31–38. [6] K.S. Lang, S. Fillon, D. Schneider, H.G. Rammensee, F. Lang, Pflugers Arch. 443 (2002) 798–803. [7] A. Alisi, I. Demori, S. Spagnuolo, E. Pierantozzi, E. Fugassa, S. Leoni, Cell Physiol. Biochem. 15 (2005) 69–76. [8] H. Long, H. Han, B. Yang, Z. Wang, Cell Physiol. Biochem. 13 (2003) 401–414. [9] A.M. Davies, EMBO J. 22 (2003) 2537–2545. [10] M.F. Walsh, V. Thamilselvan, R. Grotelueschen, L. Farhana, M. Basson, Cell Physiol. Biochem. 13 (2003) 135–146. [11] J.W. Sturm, H. Zhang, R. Magdeburg, T. Hasenberg, R. Bonninghoff, J. Oulmi, M. Keese, R. McCuskey, Cell Physiol. Biochem. 14 (2004) 249–260. [12] C. Rosette, M. Karin, Science 274 (1996) 1194–1197.
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Minireview
Plasma membrane ion channels in suicidal cell death Florian Lang a
a,*
, Stephan M. Huber a, Ildiko Szabo b, Erich Gulbins
c
Department of Physiology, University of Tu¨bingen, Gmelinstrasse 5, D72076 Tuebingen, Germany b Department of Biology, University of Padova, Italy c Department of Molecular Medicine, University Duisburg-Essen, Germany Received 5 December 2006, and in revised form 21 December 2006 Available online 22 January 2007
Abstract The machinery leading to apoptosis includes altered activity of ion channels. The channels contribute to apoptotic cell shrinkage and modify intracellular ion composition. Cl channels allow the exit of Cl , osmolytes and HCO3 leading to cell shrinkage and cytosolic acidification. K+ exit through K+ channels contributes to cell shrinkage and decreases intracellular K+ concentration, which in turn favours apoptotic cell death. K+ channel activity further determines the cell membrane potential, a driving force for Ca2+ entry through Ca2+ channels. Ca2+ may enter through unselective cation channels. An increase of cytosolic Ca2+ may stimulate several enzymes executing apoptosis. Specific ion channel blockers may either promote or counteract suicidal cell death. The present brief review addresses the role of ion channels in the regulation of suicidal cell death with special emphasis on the role of channels in CD95 induced apoptosis of lymphocytes and suicidal death of erythrocytes or eryptosis. Ó 2007 Elsevier Inc. All rights reserved. Keywords: CD95; Scramblase; PGE2; Cell volume; Lymphocytes; Erythrocytes; Eryptosis
Apoptosis or programmed cell death eliminates abundant and potentially harmful cells. Apoptosis may be triggered by a wide variety of factors including stimulation of death receptors such as CD95 [1–4], somatostatin receptor [5] or TNFa receptor [6], by thyroid hormones [7], increased cell density [8], adhesion [9,10] or growth factor withdrawal [11], or by exposure to stressors such as oxidants [12], radiation [12], inhibition of glutaminase [13], chemotherapeutics [14,15], energy depletion [16], choline deficiency [17] or osmotic shock [3,12,18–21]. Hallmarks of apoptosis include mitochondrial depolarization, DNA fragmentation, nuclear condensation, cell shrinkage, cell membrane blebbing and scrambling of cell membrane lipids with breakdown of phosphatidylserine asymmetry of the plasma membrane [22]. The cell membrane scrambling results from the activity of a scramblase [23], which is stimulated by increase of cytosolic Ca2+ activity [24,25]. Macrophages are equipped with receptors *
Corresponding author. Fax: +49 7071 29 5618. E-mail address: fl[email protected] (F. Lang).
0003-9861/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.abb.2006.12.028
specific for phosphatidylserine [26,27] and thus engulf cells or cellular fragments exposing phosphatidylserine at their surface [28]. The engulfment is facilitated by the shrinkage of apoptotic cells [28]. Suicidal death may not only affect nucleated cells but similarly erythrocytes [29,30]. Suicidal death of mature erythrocytes or ‘‘eryptosis’’ [31] is characterized by cell shrinkage, cell membrane blebbing and breakdown of phosphatidylserine asymmetry, features mimicking respective events of nucleated cell apoptosis [32–34]. The machinery of apoptosis involves altered regulation of Cl channels, K+ channels and Ca2+ permeable channels, which play an active role in the machinery leading to suicidal cell death. Accordingly, apoptosis and eryptosis are modified by respective channel inhibitors. Anion channels, osmolyte transport and pH regulation Activation of Cl channels during apoptosis has first been observed following stimulation of CD95 in Jurkat
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cells [35]. Subsequently, Cl channel activation has been described in TNFa or staurosporine induced apoptosis of various cell types [20,36]. In Jurkat cells the same channels serve regulatory cell volume decrease following osmotic cell swelling [37]. Activation of those Cl channels by cell swelling [37] or stimulation of CD95 [35] requires the Src-like kinase Lck56. The kinase is activated by ceramide [38], which is formed by activation of a sphingomyelinase following stimulation of CD95. In lymphocytes from patients with cystic fibrosis the Cl channels cannot be activated by protein kinase A but by cell swelling, by ceramide or by active Lck56[39]. Cl channel activation plays a pivotal role in the apoptotic machinery. Accordingly, Cl channel inhibitors abrogate CD95 induced Jurkat cell apoptosis [35], TNFa or staurosporine induced apoptosis of various cell types [20,36], apoptotic death of cortical neurons [40], GABA-induced enhancement of excitotoxic cell death of rat cerebral neurons [41], cardiomyocyte apoptosis [42], antimycin A induced death of proximal renal tubules [43] and suicidal death of erythrocytes [44]. As Lck56 does activate CFTR sensitive outwardly rectifying Cl channels in lymphocytes of cystic fibrosis patients, CD95 induced lymphocyte death is not affected in those patients [39]. Activation of Cl channels leads to exit of Cl , which tends to depolarize the cell membrane. Thus, the driving force for K+ exit is enhanced and, dependent on the activity of K+ channels, the cells release KCl. The loss of osmotically active KCl is paralleled by loss of osmotically obliged water and thus by cell shrinkage, one of the hallmarks of apoptosis [3]. Even though the underlying mechanisms are still ill-defined, it is believed that the loss of cell volume contributes to the machinery leading to apoptotic cell death [18,45]. It should be pointed out, though, that the Cl channels are activated within a few minutes following CD95 triggering of Jurkat cells, but that apoptotic cell shrinkage occurs only some 90 min later. As outlined below, the lack of early cell shrinkage is presumably a result of early K+ channel inhibition. Cl channels do not only contribute to apoptotic cell shrinkage. Several anion channels are permeable to organic osmolytes such as taurine. Activation of those anion channels leads to cellular loss of organic osmolytes [3,46,47], which is again accompanied by osmotically obliged water and thus contributes to apoptotic cell shrinkage [3]. It should be pointed out, however, that at least following CD95 induced death of Jurkat lymphocytes, the taurine release mechanism is not the outwardly rectifying Cl channel. Whereas CD95 induced activation of the outwardly rectifying Cl channel requires Lck56 [35], the taurine release is abrogated by the caspase inhibitor zVAD [46]. Moreover, inhibition of the outwardly rectifying Cl channel is an early event after CD95 triggering [35], whereas taurine release is a late event immediately preceding DNA fragmentation [3]. As organic osmolytes stabilize cellular proteins (for review see [3]), their exit could lead to protein destabilization and thus contribute to the triggering
of cell death. Along the same lines, inhibition of inositol uptake has been shown to trigger renal failure presumably due to suicidal death of renal tubular cells [48]. On the other hand, erythrocytes from mice lacking the taurine transporter are rather less sensitive to osmotically induced cell death [33]. Interestingly, the stimulation of taurine release and apoptotic DNA fragmentation following CD95 stimulation of Jurkat cells are both highly sensitive to ambient temperature [3]. Similarly, CD95 mediated stimulation of epithelial cell death by exposure to Pseudomonas is highly temperature sensitive [1]. CD95 mediated Pseudomonas induced host cell death is critically important for the host defence [49] and it is tempting to speculate that the increased body temperature of fever may help to stimulate apoptosis and thus removal of infected cells [1]. Several Cl channels allow the passage of HCO3 . Their activation leads to HCO3 exit and thus to cytosolic acidification, a typical feature of apoptotic cells [6,35,50–61]. As DNase type II has its pH optimum in the acidic range, cytosolic acidification favours DNA fragmentation (for review see [62]). Moreover, intracellular acidification may facilitate caspase activation. While the pH optimum of most caspases is pH 7.0 [63], a low cytosolic pH (6.4) has been shown to enhance cytochrome c/dATP-mediated caspase activation [64], indicating that assembly of the apoptosome might be controlled by the intracellular pH. Particularly, cellular acidification has previously been shown to foster autocatalytic maturation of procaspase-3 and to increase proteolytic cleavage by caspase-9 [65]. It should be pointed out that the acidification during apoptosis is not only due to activation of HCO3 permeable Cl channels but in addition due to inhibition of the Na+/ H+ exchanger [66], which is at least partially due to caspase dependent degradation of the carrier protein NHE1 [67]. NHE1 degradation and inhibition is not an early but a late event in the apoptotic machinery [67]. Staurosporine-induced intracellular acidification was not prevented by the caspase inhibitor zVAD-fmk but completely abrogated by Bcl-2 overexpression, pointing to a role of mitochondria in the triggering of cytosolic acidification [67]. Thus, Cl channels contribute to but do not fully account for cytosolic acidification. K+ channels In several cell types, apoptosis is stimulated by activation of K+ channels [40,68] and inhibited by K+ channel blockers [69,70] or increase of extracellular K+ concentration [70–72]. Activation of K+ channels leads to hyperpolarization of the cell membrane, which increases the electrical driving force for Cl exit into the extracellular space. Thus, as indicated above, enhanced activity of K+ channels and Cl channels leads to cellular loss of KCl with osmotically obliged water and hence to cell shrinkage. Beyond that cellular loss of K+ may favour apoptosis in a wide variety of cells [19,20,45,73–82].
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Cellular loss of K+ may not only be due to activation of K channels but may as well involve impaired activity of the Na+/K+ ATPase [83]. Inhibition of the Na+/K+ ATPase, however, does not usually shrink cells, as it leads to an increase of intracellular Na+ concentration usually outcasting the decrease of intracellular K+ concentration. In some cells, inhibition rather than activation of K+ channels may parallel apoptosis. Conversely, inhibition of K+ channels may cause apoptosis [84–89] and activation of K+ channels may inhibit [90,91] apoptosis. Along those lines, mice with mutated G-protein coupled inward rectifier K+ channels (Weaver mice) suffer from extensive neuronal cell death [92–96]. CD95 stimulation leads to early inhibition of Kv1.3 K+ channels [35,97,98], the cell volume regulatory K+ channels of Jurkat lymphocytes [99]. The inhibition of the Kv1.3 channels is paralleled by tyrosine phosphorylation of the channel protein upon CD95 stimulation [38,97]. Kv1.3 channels are sensitive to tyrosine phosphorylation [100] and inhibition of Kv1.3 channels by CD95 is abrogated by tyrosine kinase inhibitors and genetic knockout of Lck56 [38,97]. Similar to stimulation of CD95, ceramide inhibits Kv1.3 and induces apoptosis [38]. Conversely, Kv1.3 is stimulated by the serum and glucocorticoid inducible kinase SGK1 [101], which has been shown to inhibit apoptosis [102]. Upon CD95 triggering, the early inhibition of Kv1.3 channels prevents premature cell shrinkage, which would interfere with apoptosis signaling [3]. Moderate osmotic cell shrinkage prior to CD95 stimulation blunted the CD95 induced activation of reactive oxygen species and subsequent apoptosis, indicating that cell shrinkage indeed disrupts the apoptotic signaling cascade [38] without interfering with some of the upstream signaling. Thus, while excessive osmotic cell shrinkage or osmotic shock by itself induces apoptosis [3,12,18–21], at least in Jurkat lymphocytes moderate decrease of cell volume confers some resistance to receptor mediated cell death. The early inhibition of Kv1.3 is followed by late activation of Kv1.3 [103], which supports the apoptotic cell shrinkage during the execution phase of apoptosis [103]. In suicidal erythrocytes increased cytosolic Ca2+ activity stimulates Ca2+ sensitive K+ channels (Gardos channels) [104–111]. Activation of those channels leads to hyperpolarization and, due to high erythrocyte Cl permeability, to parallel exit of K+ and Cl . The exit of KCl and osmotically obliged water leads not only to cell shrinkage but enhances the scrambling of the cell membrane [70], a typical feature of suicidal erythrocyte death or eryptosis [31]. Conversely, pharmacological inhibition of the Gardos channels or increase of extracellular K+ concentration does not only abrogate eryptotic cell shrinkage but leads to a moderate blunting of the phosphatidylserine exposure following treatment of erythrocytes with the Ca2+ ionophore ionomycin [70]. Cell shrinkage leads to formation of platelet activating factor PAF, which in turn activates a sphingomyelinase leading to formation of ceramide [112]. +
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Ceramide then contributes to the triggering of cell membrane scrambling [112,113]. Presently, it is not clear, whether increased extracellular K+ concentration exerts its antieryptotic effect by interference with eryptotic cell shrinkage or by prevention of eryptotic K+ loss. Ca2+ and unselective cation channels Jurkat lymphocyte apoptosis following CD95 triggering is paralleled by inhibition of ICRAC [114,115], a channel involved in the activation and proliferation of a wide variety of cells [116–120]. Thus, in the early phase of CD95 triggering, cytosolic Ca2+ activity rather decreases in Jurkat T lymphocytes [115]. On the other hand, sustained increase of cytosolic Ca2+ activity may trigger apoptosis of a variety of nucleated cells [22,116,117,121,122] and suicidal death or eryptosis of erythrocytes [32,123–126]. In erythrocytes, the increase of cytosolic Ca2+ activity may result from activation of Ca2+ permeable cation channels, which are activated by exposure of erythrocytes to osmotic shock [127], oxidative stress [128], energy depletion [32] and infection with the malaria pathogen Plasmodium falciparum [129–131]. The eryptosis following energy depletion may partially be due to impaired replenishment of GSH and weakening of the antioxidative defence [132,133]. The cation channels are activated by prostaglandin E2 (PGE2)1, which is released upon osmotic shock [134]. The cation channels are further activated by removal of intracellular and extracellular Cl [127,128] or by incubation in low ionic strength [135–137]. Nonselective cation channels are further activated by depolarization [138–140]. Enhanced cytosolic Ca2+ concentrations lead to phospholipid scrambling [23] with breakdown of the phosphatidylserine asymmetry of the erythrocyte cell membrane [25]. Moreover, Ca2+ may activate calpain [141], which in turn leads to cell membrane blebbing, another hallmark of eryptosis [123,124]. A wide variety of further substances or conditions trigger eryptosis [31], such as paclitaxel [142], chlorpromazine [143], cyclosporine [144], mercury [145], lead [146], hemolysin [147], phosphate depletion [148], iron deficiency [149], Hemolytic Uremic Syndrome [150] and several inherited erythrocyte disorders [126]. Eryptosis is inhibited by erythropoietin [151], urea [152], catecholamines [153], by lowering of extracellular Ca2+ activity [32] and by inhibitors of cation channels [32]. Mechanisms underlying eryptosis may further contribute to erythrocyte senescence [29,31,154,155] or neocytolysis [30]. Cell shrinkage activates cation channels in a wide variety of nucleated cells including airway epithelia cells [156], colon carcinoma cells [157], cortical collecting duct cells [158], hepatocytes [159,160], mast cells [161], macrophages [162], vascular smooth muscle [157] and neuroblastoma cells [157]. Cl removal activates cation channels in salivary and 1
Abbreviation used: (PGE2), prostaglandin E2.
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lung epithelial cells [163–165] and influences the channels via a pertussis toxin sensitive G-protein [163]. Whether or not those channels participate in Ca2+ entry and apoptosis, has not been explored. Most recent experiments disclosed, however that, similar to what has been observed in erythrocytes, osmotic cell shrinkage leads to formation of PGE2 in K562 cells, which in turn activate Ca2+ permeable cation channels and leads to apoptotic cell death [166]. In those cells, silencing of the cation channel TRPC7 blunts the cell death following osmotic shock. Thus, in those cells TRPC7 contributes to the triggering of apoptosis. Conclusions Ion channels in the plasma membrane play a decisive role in the machinery eventually leading to suicidal cell death. They influence the apoptotic signalling by modifying intracellular ion concentrations and cell volume. The role of individual channels depends on the cell type, the physiological condition, the time course and the intensity of channel activation. Much has to be learned prior to a full understanding of the complex interplay between channel activity and apoptosis signalling. Acknowledgments The authors acknowledge the meticulous preparation of the manuscript by Lejla Subasic. The work of the authors was supported by the Deutsche Forschungsgemeinschaft, Nr. La 315/4-3, La 315/6-1, Le 792/3-3, DFG Schwerpunkt Intrazellula¨re Lebensformen La 315/11-1, and Bundesministerium fu¨r Bildung, Wissenschaft, Forschung und Technologie (Center for Interdisciplinary Clinical Research) 01 KS 9602. References [1] S. Fillon, K. Klingel, S. Warntges, M. Sauter, S. Gabrysch, S. Pestel, V. Tanneur, S. Waldegger, A. Zipfel, R. Viebahn, D. Haussinger, S. Broer, R. Kandolf, F. Lang, Cell Physiol. Biochem. 12 (2002) 47–54. [2] E. Gulbins, A. Jekle, K. Ferlinz, H. Grassme, F. Lang, Am. J. Physiol. Renal Physiol. 279 (2000) F605–F615. [3] F. Lang, G.L. Busch, M. Ritter, H. Volkl, S. Waldegger, E. Gulbins, D. Haussinger, Physiol. Rev. 78 (1998) 247–306. [4] F. Lang, I. Szabo, A. Lepple-Wienhues, D. Siemen, E. Gulbins, News Physiol. Sci. 14 (1999) 194–200. [5] R. Teijeiro, R. Rios, J.A. Costoya, R. Castro, J.L. Bello, J. Devesa, V.M. Arce, Cell Physiol. Biochem. 12 (2002) 31–38. [6] K.S. Lang, S. Fillon, D. Schneider, H.G. Rammensee, F. Lang, Pflugers Arch. 443 (2002) 798–803. [7] A. Alisi, I. Demori, S. Spagnuolo, E. Pierantozzi, E. Fugassa, S. Leoni, Cell Physiol. Biochem. 15 (2005) 69–76. [8] H. Long, H. Han, B. Yang, Z. Wang, Cell Physiol. Biochem. 13 (2003) 401–414. [9] A.M. Davies, EMBO J. 22 (2003) 2537–2545. [10] M.F. Walsh, V. Thamilselvan, R. Grotelueschen, L. Farhana, M. Basson, Cell Physiol. Biochem. 13 (2003) 135–146. [11] J.W. Sturm, H. Zhang, R. Magdeburg, T. Hasenberg, R. Bonninghoff, J. Oulmi, M. Keese, R. McCuskey, Cell Physiol. Biochem. 14 (2004) 249–260. [12] C. Rosette, M. Karin, Science 274 (1996) 1194–1197.
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